"gigantopterid" = an English noun describing large leaves with complex reticulate venation resembling the Cathaysian fossil seed plant genus Gigantopteris and North American genus Delnortea of the Permian Period, 260 million years ago"

You are here: Origin of Flowering Plants

ESSAY CONTENTS


[ Origin of Angiosperms ]


JOHN M. MILLER, Ph.D.

University and Jepson Herbaria
Room 1001, Valley Life Sciences Building 2465
University of California, Berkeley
Berkeley, California, USA 94720-2465



Coevolution between phytophagous insect antagonists and Carboniferous, Permian, and Triassic seed plant hosts at the level of their respective developmental tool kits with focus on selective forces that drive the logic of transcriptional regulation is proposed in the following essay to explain the origin and evolution of flowering plants and certain Holometabola.

I discuss potential coevolution of insect and seed plant helix-turn-helix proteins, specifically Engraled and Leafy enzymes that bind to cis-regulatory promoters controlling downstream expression of genes determining paedomorphic insect body patterns and plant cone and floral organ development.

The picture of the rock slab on the left is of an indeterminate pentamerous fossil rosid flower (Celastrales, Rosanae) collected by Professor David L. Dilcher from the Lower Cretaceous Dakota Formation of North America. The image was captured in 1981 while the author was visiting Indiana University.

Biologists have been encouraged to think "... both within and outside the paradigm of transcription-encoding factors ..." (page 129, Niklas 2006). The three essays on the succeeding web pages are written from this research perspective.

Were insect and shrub coevolutionary compartments of the late Paleozoic hypoxic icehouse and later hot house, venues of the first angiosperms? Possibly. This question among others is explored in this first of three essays on the origin of angiosperms.

Certain aspects of coevolution of Mesozoic arthropods and seed plants that have a bearing on the origin and diversity of angiosperms are reviewed by Takhtajan (1969), Raven (1977), Thien et al. (1985), Labandeira and Sepkoski (1993), Farrell (1998), Labandeira (1998), Danforth and Ascher (1999), Grimaldi (1999), Wilf et al. (2000), S. Hu et al. (2008), and Labandeira (2014).

Long-branch attraction (LBA) continues to cloud molecular-phylogenetic studies of seed plants, including angiosperms (Lipeng Zeng et al. 2014, Zhenxiang Xi et al. 2014). Sophisticated Bayesian analyses conducted by C. S. P. Foster et al. (2017) report low support (<80%) for the hypothesized point of divergence of monocots and Ceratophyllum from eudicots.

Do unsolved Ceratophyllales such as extant species of Ceratophyllum represent living descendents of a long branch from the Permo-carboniferous population of Sandrewia texana (Vojnovskyales)?

The diagram on the right is redrawn from Figure 4 on page 341 of D. H. Les (1988), "Hypothetical phylogenetic relationship of Ceratophyllales, Nymphaeales, and modern monocots and dicots." I colorized and changed the font of the typescript to conform to gigantopteroid web page style.

I focus on coevolving, developmentally plastic arthropod and seed plants from the perspective of progenesis as Takhtajan (1976) did in his paper on the origin of angiosperms, but with focus on interacting Paleozoic animal and plant populations. While discussing Armen Takhtajan's premise with Rudolf Schmid, Ph.D., I learned that paedomorphic heterochrony was not under consideration at the time the seminal 1969 book authored by Takhtajan was published.

Proposals considered and discussed below take Armen Takhtajan's hypothesis on a "neotenous origin of flowering plants" (page 209, 1976) one step further.

Specifically, I advance Takhtajan's ideas on angiosperm origins (1969, 1976) from 21st century research perspectives of progenesis melded with rethinking of the paleontology of detached, fossilized remains of underappreciated Paleozoic seed plant organs. Reproductive organs of some lineages of poorly understood Permo-triassic or Permo-carboniferous seed plants were possibly derived from ancestral massive, developmentally plastic, shoot apical meristems (SAMs) yet to be diagnosed from detached and shed foliar organs, seeds, and pollen.

Potential importance of certain Paleozoic seed plant fossils in deciphering the ancestry of flowering plants and paraphyletic clades of gymnosperms reflects my choice of the unusual title for this web site. The best place and time to begin a discussion of the problem is with the biogeography of basal flowering plants and magnoliids.

The Fiji Islands have long been of interest to biogeographers (Raven and Axelrod 1974, Thorne 1986, Morley 2001), to geologists as a tectonic puzzle (Rodda and Kroenke 1984), and to botanists as a "cradle of flowering plants" (title, Chapter 12, Takhtajan 1969), where some "missing links in the chain of angiosperm phylogeny" are known (page 141, Between Assam and Fiji, Takhtajan 1969). Three of the largest islands (Viti Levu, Vanua Levu, and Taveuni) support harmonic "continental" floras (A. C. Smith 1979).

There are several conifers endemic to the Fiji Archipelago including Agathis vitiensis, Acmopyle sahniana, Dacrycarpus imbricatus, Dacrydium nausoriense, Dacrydium nidulum, and Decussocarpus vitiensis. A common gnetophyte (Gnetum gnemon) and a narrowly distributed cycad (Cycas rumphii) occur in the archipelago. Tropical forests of the larger islands yield ten genera of monocotyledonous palms including the monotypic Alsmithia longipes, and the enigmatic magnoliid flowering plant family, Degeneriaceae.

The family Degeneriaceae was discovered in 1942 by I. W. Bailey and A. C. Smith. The only known species at the time, Degeneria vitiensis (pictured below), combines a number of primitive features that have ignited many debates (I. W. Bailey 1949, Cronquist 1968, Takhtajan 1969). A second species of Degeneria has been reported (A. C. Smith 1991).

All total in this rich flora of some 6,000 species, there are 812 endemic angiosperms and conifers, 12 endemic genera, and one endemic flowering plant family (A. C. Smith 1979, 1981, 1991, 1996, Table 1).



The image above is the northwestern face of the Korombasabasaga Range, Viti Levu Island, Fiji as viewed from the road between Namosi and Wainimakutu villages. Distant pinnacles and spires are weathered calc-alkaline Miocene andesites known as the Namosi Volcanics (Rodda and Kroenke 1984).

Despite several decades of effort by morphologists, paleobotanists, and plant biologists, the origin of angiosperms remains enigmatic and mysterious. Some paleontologists regard the problem of flowering plant origins, "... as intractable a mystery today as it was to Darwin 130 years ago" (page 318, Rothwell et al. 2009). Simply put, the origin of angiosperms is a conundrum.


Historical Context:

Many bibliographies on angiosperm floral diversity and the origin and evolution of flowering plants are available. Endress (1994, 2001 [a book chapter and two papers], 2004), Bateman et al. (2006), J. A. Doyle (2006), Friis et al. (2006), D. W. Taylor and Hickey (1996 [a book and one paper]), D. E. Soltis et al. (2008), Specht and Bartlett (2009), Dilcher (2010), D. W. Taylor (2010), Friis et al. (2011), and J. A. Doyle (2012) compile particularly relevant reference lists.

Flowering material of Degeneria vitiensis is shown in the right-hand image (photographed by Paddy Ryan, Ph.D.). Fragrance of this species resembles Cananga odorata according to Professor Al Smith (A. C. Smith 1981).

The International Journal of Plant Sciences devotes most of Number 7 of Volume 169 (2008) toward the ongoing search for the earliest flowers, based on an international symposium held during the summer of 2007 at the Swedish Museum of Natural History (von Balthazar et al. 2008). More than twenty articles in Volume 96, Number 1 of the American Journal of Botany explore the origin, evolution, and radiation of flowering plants to celebrate the Charles Darwin Bicentennial (Stockey et al. 2009).

Conrad Labandeira's several reviews on fossil insect-plant phytophagous associations (Labandeira 2000, 2006, 2007 [two papers], 2010, 2014) contain extensive bibliographies. While discussing the effects of ice-house/hot house planetary climatic switches on expansion of land plant invertebrate herbivores Labandeira (2006) states:

"One possibility is that these atmospheric variables have direct physiologic consequences on the selection and turnover of particular plant clades globally, which in turn elicit an associational response from selected clades of insect herbivores."

The preceding statement is quoted from page 425 of C. C. Labandeira (2006), The four phases of plant-arthropod associations in deep time, Geologica Acta 4(4): 409-438.

Some of the historical syntheses include Arber and Parkin (1907), I. W. Bailey (1949), Edgar Anderson (1934), Axelrod (1952, 1970), Leppik (1960, 1968), Raven and Kyhos (1965), Cronquist (1968), Thorne (1968), Melville (1969), Takhtajan (1969, 1976, 1991), Raven and Axelrod (1974), Stebbins (1958, 1974), C. B. Beck (1976), Hughes (1976, 1994), Meeuse (1979), Nair (1979), Krassilov (1977), Retallack and Dilcher (1981 [two papers]), Asama (1982, 1985), Melville (1983), Crane (1985), Meyen (1986, 1988), Dilcher (1986, 2000), J. A. Doyle and Donoghue (1986, 1987), Endress (1987), Friis et al. (1987), Les (1988, 1993), and Les et al. (1991), among others.

Additional compilations on the origin of angiosperms and floral morphology include Krassilov (1991), Thorne (1992), Endress (1993, 2001 [a book chapter and two papers], 2004), Friedman (1992 [two papers]), Stewart and Rothwell (1993), Nixon et al. (1994), Crane et al. (1995), H. D. Zhang (1995), Hickey and D. W. Taylor (1996), D. W. Taylor and Hickey (1992, 1996), Loconte (1996), and Krassilov (1997, 2002), among others.

Crepet (2000), Donoghue and J. A. Doyle (1991, 2000), Frohlich and Parker (2000), Friedman and Floyd (2001), G. Sun et al. (2001), Z.-Y. Wu et al. (2002), Crane et al. (2004), Davies et al. (2004), P. S. Soltis and D. E. Soltis (2004, 2015), Stuessy (2004), D. E. Soltis et al. (2005), De Bodt et al. (2005), J. A. Doyle (1978, 1994, 2005, 2006, 2008, 2012), Friis et al. (2006, 2011), Frohlich (2002, 2003, 2006), and Lipeng Zeng et al. (2014), have contributed to our knowledge of the origin and evolution of flowering plants.

Modern syntheses on the abominable mystery of the origin of angiosperms from unknown Paleozoic seed plant ancestors and modern radiations are published by Frohlich and Chase (2007), Maheshwari (2007), Sokolov and Timonin (2007), Zavada (2007), J. A. Doyle (2008), Endress (2008), D. E. Soltis et al. (2008), Berendse and Scheffer (2009), Friedman (2009), Specht and Bartlett (2009), E. L. Taylor and T. N. Taylor (2009), Xin Wang (2009), Dilcher (2010), Magallón (2010), Stephen A. Smith et al. (2010), Stuessy (2010), D. W. Taylor (2010), Xin Wang (2010), Friis et al. (2011), J. A. Doyle (2012), Amborella Genome Project (2013), Chamala et al. (2013), Seago and Fernando (2013), Crepet (2014), Drew et al. (2014), Goremykin et al. (2015), Simmons and Gatesy (2015), and Cascales-Miñana et al. (2016).

Anthophyte hypothesis. In 1986 James A. Doyle and Michael J. Donoghue proposed that flowering plants were derived from gnetophytes. The anthophyte hypothesis was developed further in later years (J. A. Doyle and Donoghue 1987, Nixon et al. 1994).

After reconsidering incongruent molecular-phylogenetic and morphological data the anthophyte hypothesis was rejected by Donoghue and J. A. Doyle (2000).

"If no living seed plants are closely related to angiosperms the only way to reconstruct the origin of angiosperms is by fitting fossils into the picture, and this can only be done by analysis of morphological characters."

The preceding quote is from page R109 of M. J. Donoghue and J. A. Doyle (2000), Seed plant phylogeny: demise of the anthophyte hypothesis?, Current Biology 10(3): R106-R109.

A reappraisal of the anthophyte hypothesis has been published (Rothwell et al. 2009).

Biome- and paleogeographically-specific hypotheses. Certain ecologists propose that physiological studies of living basal families and species of flowering plants indigenous to island tropical environments may lead to insight on the paleoecology of the angiosperm stem group (Feild et al. 2003, Feild et al. 2004, Feild and Arens 2005, Feild and Arens 2007).

Both an uplands hypothesis (Axelrod 1952) and coastal hypothesis (Retallack and Dilcher 1981) were proposed to explain topographical centers of origin and radiation of the first flowering plants.

Stebbins (1974, 1984) thought that alpine biomes of northern latitudes might have been the center of early radiation of angiosperms. A similar idea, the eastern Asian centers hypothesis, was put forth by G. Sun et al. (2001). Based on the recovery and study of fossil pollen casings (palynomorphs) recovered from deep-sea drill holes, Hochuli and Feist-Burkhardt (2004) suggested that early flowering plants might have evolved in a boreal cradle.

Daniel Axelrod suggested that angiosperms originated in Triassic or Jurassic tropical uplands of Gondwana "... Spreading out into a new adaptive zone, presumably in equable, warm upland areas ..." Axelrod (page 281, 1970) proposed that angiosperms and their insect pollinators dispersed and radiated into semiarid forest openings, and into arid lowlands from Cretaceous geologic fold belts during the early Cretaceous.

"... we hypothesize that proto-South-East Asia served both as the cradle and centre of diversification of early angiosperms" (page 332, Is the Most Recent Common Ancestor of Angiosperms Now Lost in Proto-southeast Asia Terranes That Are Underwater or Subducted?, Buerki et al. 2014).

Hypotheses suggested by Buerki et al. (2014) contradict classical ideas expressed by Axelrod (1952, 1959) and Krassilov (1997). Dispersal of early angiosperm floras from the tropics poleward was proposed by Axelrod in 1959. A statement quoted from this often overlooked paper is probably pertinent.

"... since angiosperms [Vojnovskyales?] may already have been in existence in upland areas by the Permian [Axelrod 1952], and because the record of the group is exceedingly fragmentary into the Early Cretaceous, the data obviously do not permit us to suggest any one area as the cradle of origin" (page 207, Discussion, Axelrod 1959, the words in [brackets] are mine).

Further, an important study of pollen samples recovered from isolated sedimentary layers in at least one continuous stratigraphic sequence in two deep well cores, reports monosulcate, columellate palynomorphs, and Afropollis, from the Middle Triassic (Anisian) about 240 MYA (Hochuli and Feist-Burkhardt 2013). Definitive paleontological evidence published by Peter Hochuli and Susanne Feist-Burkhardt should be read together with a review of Sanmiguelia paleobiology, also reporting three new localities from the Lower Triassic (Norian) Chinle Formation of southwestern North America (S. Ash and Hasiotis 2013).

Based on Axelrod and Krassilov's cogent arguments, and unequivocal palynological evidence published by Hochuli and Feist-Burkhardt (2004, 2013), the Buerki team (2014) should do more homework and rethink their ideas, in my opinion.

To suggest a specific geographical center of origin of angiosperms, protected place, habitat, or timing from a Gothic or other human perspective ("cradle," "dark,", "dawn," "disturbed," "shady," "stream-like," "wet and wild") might be inconsequential in view of potential >300 million year old divergences of flowering plants from their nearest gymnosperm relatives.

Chloranthoid hypothesis. This hypothesis suggests that flowering plants evolved from chloranthoid ancestors not unlike the modern angiosperm family Chloranthaceae (Leroy 1983).

Arguments presented by Stuessy (2004) in favor of Leroy's proposal include reports of data from molecular systematics that place Hedyosmum (Chloranthaceae, Piperales, Magnoliidae) in a clade basal to other extant angiosperms (Y. L. Qiu et al. 1999).

Developmental and genetic theories. Some of the hypotheses and theories on the origin of angiosperms probably have more to do with the origin of the flower. The two concepts might not be the same (J. A. Doyle 2008).

The main developmentally- and genetically-based hypotheses and theories on the origin of angiosperms and the flower are Asama's Growth Retardation Theory (Asama 1982, 1985), Meyen's gamoheterotophic hypothesis (Meyen 1986, Meyen 1988), Frohlich and Parker's Mostly Male Theory (Frohlich and Parker 2000), Becker and Theißen's out-of-male and out-of-female hypotheses (Becker and Theißen 2003), Baum and Hileman's model of cone and floral development from hermaphroditic strobili (2006), and modifications of the latter two ideas on bisexual strobilus development suggested by Theißen and Melzer (2007) and Melzer et al. (2010).

Another interpretation of the origin of angiosperms from bisexual cone axes, based upon molecular divergence in LEAFY (LFY) genes about 130 MYA, was published by Albert et al. (2002) who link the elimination of one LFY gene paralog "... to the sudden appearance of flowers in the fossil record" (abstract, Albert et al. 2002).

"Our theory may also be tested, without the vagaries of fossil discovery, in modern plants. Of the early-acting genes that control flower development, more should have close homologs (or orthologs, if gene trees are sufficiently resolved to demonstrate orthology) active in male gymnosperm reproductive structures rather than in female structures... In the coming years, topology-violating transformations that are of evolutionary importance may become recognizable using evidence from genes that control development."

The above quotation is from page 167 of M. W. Frohlich and D. S. Parker (2000), The mostly male theory of flower evolutionary origins: from genes to fossils (MMT), Systematic Botany 25(2): 155-170.

Frohlich suggests in several updates of MMT (2001, 2002, 2003) that early Mesozoic Corystospermales might be one of the possible ancestors of flowering plants. Frohlich (2003) placed an interesting idea on the table, namely that potential pollinators of gymnosperms were attracted by ectopic ovules displayed on upper (abaxial) leaf surfaces.

Several elegant studies of LFY gene expression in gymnosperm female cone primordia, using ultrasensitive radioactive probes, clearly demonstrate that transcripts of the gene are present (Shindo et al. 2001, Vásquez-Lobo et al. 2007, Carlsbecker et al. 2013), contradicting the basic premise set forth in MMT. Based on LFY gene expression studies of Gnetum and comparative expressed sequence tag (EST) analyses (Tavares et al. 2010) MMT is yet another unsupported hypothesis on the origin of angiosperms.

Further, the discovery of angiosperm and corystosperm fossils in the same Paleogene flora (McLoughlin et al. 2008) detracts from Frohlich's proposal that corystosperms were flowering plant antecedents.

Studies of wood paedomorphosis may offer new clues on a possible Mesozoic origin of angiosperms (Carlquist 2009), but studies of potentially neotenous gymnosperm secondary xylem development in deep (Paleozoic) time are lacking.

Erbar (2007) summarizes past ideas on a supposed Mesozoic origin of angiosperms from the research perspective of evolutionary-development (evo-devo).

A novel "Mosaic Theory for the Evolution of the Dimorphic Perianth" proposed by Warner et al. (2009) states that:

  • sepal and petal identities evolved "early in angiosperm history"
  • morphological features of tepals may not have been "fixed to particular organs and were primarily environmentally controlled"
  • later during the evolution of flowering plants "sepalness and petalness became fixed to whole organs in specific whorls, forming distinct sepals and petals, thus removing the need for environmental control in favour of fixed developmental control"
  • reversals observed in certain eudicots (e.g. Berberis [Berberidaceae] and Hypericum [Hypericaceae]) constitute plesiomorphies
  • Gonophyll theory. Melville develops his earlier ideas on a Gonophyll Theory (1969) in a review published in 1983 that proposes a Permian origin of angiosperms from glossopterids.

    Stewart and Rothwell (1993) recapitulated the main steps needed to form the conduplicate carpel using glossopterid-, other seed fern-, and early angiosperm fossils as examples. According to Stewart and Rothwell (1993) these main steps were:

  • "Grouping of ovules" (fossil evidence: Caytonia, Glossopteris, Petriellaea, and Ottokaria, among others)
  • "Evolution of the fertile axis" (fossil evidence: Caytonia and Petriellaea)
  • "The epiphyllous fertile branch" (fossil evidence: Glossopteris)
  • "Adnation" (fossil evidence: Jambadostrobus and Lidgettonia)
  • "Origin of the bitegmic, anatropous ovule" (fossil evidence: Denkania)
  • "Formation of the carpel" (fossil evidence: Archaeanthus, Lesqueria, among others)
  • The above bulleted quotes are from pages 461-462 of W. N. Stewart and G. W. Rothwell (1993), Paleobotany and the Evolution of Plants (second edition). Cambridge: Cambridge University Press, 521 pp., with additional comments distilled from E. L. Taylor et al. (2006).

    Retallack and Dilcher (1981) presented in-depth discussion of Melville's ideas on a glossopterid ancestry of the angiosperms including a reanalysis of glossopterid fructifications.

    Mary White (1986) proposes that glossopterid Microfructi were basal to several parallel but sometimes branching and reticulate lines of evolution leading to the Caytoniales, angiosperms, Cycas (Cycadaceae, Cycadales), Podocarpaceae (Podocarpales), Araucariaceae (Araucariales), and certain catkin-bearing angiosperms including the Casuarinaceae.

    Further, White proposed that the glossopterid Megafructi were a second basal group upon which ranalian angiosperms, monocotyledonous flowering plants including Pandanus (Pandanaceae, Pandanales, Arecidae), Williamsonia (a bennettitalean), additional cycads, and certain other angiosperms evolved (M. E. White 1986).

    Multiple origins hypotheses. Others suggest that flowering plants evolved from multiple, unrelated seed plant lineages (Edgar Anderson 1934). The polyphyletic-polychromic-polytopic hypothesis (Z.-Y. Wu et al. 2002) and Nair's Triphyletic Theory (Nair 1979) are best placed in this paragraph.

    Cyclic angiospermization is reviewed by Krassilov (1997) and Ponomarenko (1998) within the context of a polyphyletic origin of angiosperms. Principal morphologic innovations in angiosperms and gymnosperms according to Krassilov (1997) are:

  • phyllospermy (growth of ovules on upper or lower leaf surfaces)
  • advent of the micropyle (a suture or opening where pollen tubes penetrate the ovule)
  • pollen (not spore) production
  • taeniae of pollen (elongated pollen grains with parallel ribs)
  • brachyplasty (combination of male and female form)
  • destrobilization (elongation of branching within cones)
  • cupulation (curling of leaves around ovulate clusters)
  • Paleoherb hypothesis. Flowering plants evolved from herbaceous forms possessing ovule and pollen bearing organs that coalesced over time producing modern flowers according to D. W. Taylor and Hickey (1992, 1996).

    Burger published a paper in 1981 suggesting that the earliest angiosperms were monocotyledonous plants. Professor Burger proposed six hypothetical trends in the early evolution of angiosperms:

  • "Small simple plants preceded large complex plants in the early evolution of angiosperms
  • Scattered vascular bundles within the stem preceded a tubular vasculature with included cylindrical cambium
  • Simple leafy stems without aerial branching preceded complex woody growth with several orders of branching
  • Simple undifferentiated leaves preceded leaves with a clearly differentiated petiole and lamina
  • Leaves with one or a few poorly differentiated orders (ranks) of venation preceded leaves with several clearly differentiated orders of venation
  • A clasping leaf base continuous with the tissue of the stem preceded a leaf base clearly differentiated from the stem; deciduous leaves evolved later and were a major innovation"
  • The above bulleted quotation is from pages 191-194 of W. C. Burger (1981), Heresy revived: the monocot theory of angiosperm origin, Evolutionary Theory 5: 189-225.

    A differing proposal by Dahlgren and Clifford (1982) suggests:

    "The ancestors of the monocotyledons were probably shrublets or subshrubs which by environmental conditions (a pronounced alternation between wet and dry periods) evolved compact underground stems, mainly short or long rhizomes from which herbaceous aerial stems were developed ..."

    The preceding quotation is from page 344 of R. M. T. Dahlgren and H. T. Clifford (1982), The Monocotyledons: A Comparative Study. New York: Academic Press, 378 pp.

    Pseudanthial theory. Eichler (1976) proposed that unisexual gymnosperms may be the ancestors of angiosperms. A discussion of this theory and how it links to the anthophyte hypothesis is presented by T. N. Taylor et al. (pages 877-878, 2009).

    Additional discussion is available in several papers that reinvestigate conifer cone abnormalities (Flores-Rentería et al. 2011, Rudall et al. 2011, Carlsbecker et al. 2013).

    Seed fern hypotheses. The origin of flowering plants is potentially traceable to Mesozoic seed ferns such as Corystospermales (Frohlich 2002, 2003, 2006) or Paleozoic Glossopteridales (Melville 1969, Retallack and Dilcher 1981, Melville 1983). James A. Doyle suggests that Caytonia (Caytoniaceae, Caytoniales) is a sister group to the angiosperms (J. A. Doyle 1978, 1994, 2006, 2008). Asian botanists postulate that flowering plants evolved from Permo-carboniferous gigantopterids (see G. Sun et al. 2001).

    A more intriguing hypothesis was proposed by H. D. Zhang in 1995 (in Chinese). According to a translation provided by Ge Sun et al. (page 162, 2001), H. D. Zhang proposed that gigantopterids evolved into angiosperms in four phases over more than 250 million years of geologic time (note that phrases in parentheses are by Ge Sun et al. 2001, words within brackets [] are mine):

  • (1) Pregnant Stage (as seen in [phyllospermous] Permo-Triassic gigantopterids and sagenopterids
  • (2) Adaptation Stage (folding of leaves into conduplicate carpels [e.g. Sanmiguelia and Schmeissneria] in Triassic-Jurassic anthophytes)
  • (3) Expanding Stage (vicariance of Pangaean seed-plant stock and short- or long distance dispersal from tropical belts to the southern latitudes [and Antarctica]) from Middle Jurassic to Cretaceous time
  • (4) Flourishing Stage (radiation of angiosperms into modern biomes during the Cretaceous to the Neogene Periods)
  • Zhang's stages are consistent with later ideas developed by Stuessy (2004). Meeuse's Anthocorm Theory (1979) is lodged here.

    Unifying theories. Bonafide theories fall into this category despite J. A. Doyle's lukewarm enthusiasm for the Transitional-combinational Theory proposed by Stuessy (2004). Certainly the findings of the Angiosperm Phylogeny Group (APG) have nothing to do with an allopolyploid origin of flowering plants from Late Paleozoic seed plant stock.

    Stuessy proposes that carpels evolved first, followed by double fertilization, and then by flowers, slowly over many millions of years, "... perhaps more than 100 million ..." (page 6, Stuessy 2004).

    The review by J. A. Doyle (2012) is the latest installment of more than 35 years of research on the origin of angiosperms, which should be read together with a lavishly-illustrated and widely-acclaimed book by Friis et al. (2011).

    Apparently, the intent of J. A. Doyle's review of molecular and paleobotanical evidence on the origin of angiosperms was to explore "areas of congruence and conflict and ways in which conflicts might be resolved ..." (page 302, Introduction, J. A. Doyle 2012). Elaborate discussion of 1986 and 1987 milestone syntheses (coauthored with M. J. Donoghue) is incongruent with seed plant organ homologies explained by Mathews and Kramer (2012).

    Despite a 2006 discussion of YABBY transcription factors (TFs) and ovule determinants, J. A. Doyle skirts research advances on evo-devo of molecular tool kits, which is a topic of considerable significance toward a deeper understanding of seed plant organ (including cone and floral) homologies based on developmental genetics (Mathews and Kramer 2012).

    There is solid biochemical and morphological evidence that flowers are short- (spur-) shoots (Christianson and Jernstedt 2009) whose growth and development is orchestrated by intricate molecular machinery (the tool kit, also coined in the literature as "toolkit") comprised of cis-regulatory modules (CRMs), gene-regulatory networks (GRNs), auxin-based polarity networks (PINs), and cis-acting TFs in germ cells of growing SAMs.

    Another review on the origin of flowering plants has surfaced (Cascales-Miñana et al. 2016). In my opinion, this synthesis promised to deliver more than it did.

    There are many problems with the dataset used by Cascales-Miñana et al. (2016). Significant discussion of other papers published in the Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences (references listed above) and the Annual Review of Earth and Planetary Sciences (J. A. Doyle 2012, P. M. Barrett 2014), was left-out by the Cascales-Miñana team. Further, much more work is necessary to plot a solution to Darwin's so-called "mystery."

    Cascales-Miñana et al. (2016) forgot to review the evolutionary relationships of seed plants with euornithopod transverse grinders and insect mutualists. The team's unusual choice of the Hilton and Bateman 2006 seed plant phylogeny is also strange.

    Omissions by Cascales-Miñana et al. (2016) of key data-sets published by Misof et al. (2014) and Weishampel and Jianu (2000), cast doubt on outcomes shown in Figure 2.

    "What is surprising is the scale of the uncertainty surrounding our basic knowledge of angiosperms. Angiosperm relationships are only now being resolved through the application of various algorithms to the combination of molecular genetics-derived data and morphological data. Yet, the relationship of the angiosperms themselves to nonangiospermous seed plants, or understanding the origin of this major group, still remains a hotly contested mystery ... " (Abstract, Crepet 2014).

    Woody magnoliid and ranalian theories and hypotheses. Several theories and hypotheses propose that modern flowering plants evolved from gymnosperms having a bisexual (hermaphroditic) strobilus (page 878, T. N. Taylor et al. 2009).

    Arber and Parkin's Strobilus Theory of the Angiosperm Fructification (Arber and Parkin 1907), Delpino's Ranalian Theory (Endress 1993), Braun's Strobilus Theory, Takhtajan's hypothesis on a "neotenous origin of flowering plants" (page 209, 1976), and the woody magnoliid hypothesis may be grouped together for purposes of discussion because evolution of the flower from hermaphroditic gymnosperm strobili is a common thread of these proposals.

    "From this one may conclude that the angiosperm flower arose most probably from a bisexual entomophilous strobilus, especially as among the earliest gymnosperms examples of bisexuality associated with entomophily are known within the Bennettitales."

    The preceding statement is from page 35 of Armen Takhtajan (1969), Flowering Plants: Origin and Dispersal (translated by C. Jeffrey). Edinburgh: Oliver and Boyd, 310 pp.

    Woody magnoliid and ranalian theories and hypotheses tie-in with Becker and Theißen's out-of-male and out-of-female hypotheses (Becker and Theißen 2003), Baum and Hileman's model of cone and floral development from hermaphroditic strobili (2006), and modifications of the latter two ideas on bisexual strobilus development suggested by Theißen and Melzer (2007) and Melzer et al. (2010).

    Comparing theories and hypotheses. The next section compares some of the theories and hypotheses on the origin of angiosperms and the flower in view of the latest synthesis on the subject by Rothwell et al. (2009). Rothwell et al. (2009) raise several caveats in a critical reevaluation of the three categories of hypotheses and theories on the origin of flowering plants:

    One, the anthophyte hypothesis (J. A. Doyle and Donoghue 1986, 1987, Donoghue and J. A. Doyle 2000), "... proposes that the outer seed integument and carpel are derived from fertile structures that already were aggregated into a flower-like reproductive organ (i.e., a strobilus or cone) ..." (page 317, Rothwell et al. 2009).

    Two, J. A. Doyle's (1978, 2006, 2008) arguments in favor of the classical caytonialean seed fern hypothesis (Thomas 1925), specifically the glaring absence of transitional fossils and any definable heterochronic lineage linking Caytonia with basal angiosperms, and impossibly complicated evo-devo from deeply conserved cone and floral tool kit perspective, renders his proposal moot. Fossilized material of Caytonia is fragmentary and poorly preserved, leaving interpretation of developmental reproductive structures conjectural (Rothwell et al. 2009).

    A third competing set of hypotheses and theories proposes that ovules developed in positions on leaves or stems occupied by pollen-bearing organs.

    The MMT (Frohlich and Parker 2000) and Sergei Meyen’s gamoheterotopic hypotheses (1986, 1988) fall into this category according to Rothwell et al. (2009).

    I present a brief comparison of some of the hypotheses and theories on the origin of angiosperms in Table 1.

    Cells of the table contain one of three responses: "Yes" (colored in yellow), "Congruent" (beige colored), or "No" (uncolored). The second column denotes whether bisexual (hermaphroditic) cone axes consisting of spirally arranged male and female microsporophylls figure prominently in the hypothesis or theory in question. The third column titled "congenital fusion" describes an evolutionary scenario whereby a fertile axis fuses with a subtending leaf sensu Caytoniales (Xin Wang 2010) or Glossopteridales (Melville 1969).

    Gene duplications may consist of small gene duplications or WGDs (polyploidy), which are stated by the authors in question as important in the evolution of flowering plants. The term insect mediated is the same as entomophily or may refer to the importance of pollination by insects in the origin of angiosperms.

    Data in columns six and seven pertain to explicit evo-devo questions, which have more to do with the origin of the flower rather than the angiosperms as a whole. LEAFY protein gradients might potentially occur in fertile SAMs and cone axes that may affect the downstream expression of homeotic MIKC-type MADS-box genes. Column seven refers to possible interactions between MIKC-type MADS-box B and "C" genes, which are potentially important in the evo-devo of flowers.

    The word Permo-triassic in column eight refers to the Permian Period, 251 to 290 MYA, of the Paleozoic Era and/or the Triassic Period, 206 to 251 MYA, of the Mesozoic Era as being the time of origin of angiosperms. A "No" response (the box is uncolored) indicates that the paper or book chapter in question favors a younger Jurassic or Cretaceous origin of flowering plants.

    Finally the column labeled "Paraphyly or Polyphyly" denotes whether the scientific paper in question attributes the origin of flowering plants to a natural, intergeneric hybridization event or events that brought together two or more distinct lines of seed plant evolution.


    Table 1. Comparison of Some Hypotheses and Theories on the Origin of Angiosperms and the Flower

    Author/Date of Proposal

    Bisexual Cone Axes?

    Congenital Fusion?

    Gene Duplications?

    Insect-Mediated?

    LFY Protein Gradients?

    MADS-box B & C Genes?

    Permo-Triassic Origin?

    Paraphyly or Polyphyly?

    Albert et al. (2002)

    Yes

    No

    Yes

    Congruent

    Congruent

    Yes

    No

    No

    Arber and Parkin (1907)

    Yes

    No

    Congruent

    Yes

    Congruent

    Congruent

    No

    Congruent

    Baum and Hileman (2006)

    Congruent

    No

    Yes

    Congruent

    Yes

    Yes

    No

    Congruent

    Becker and Theißen (2003)

    Yes

    No

    Yes

    Congruent

    Yes

    Yes

    No

    Congruent

    Cascales-Miñana et al. (2016)

    Congruent

    Congruent

    Congruent

    Yes

    Congruent

    Congruent

    Yes

    Yes

    J. A. Doyle and Donoghue (1986, Figure 15A)

    Yes

    Yes

    Congruent

    Congruent

    Congruent

    Congruent

    Yes

    No

    J. A. Doyle (1978, 2006, 2008, 2012)

    No

    Yes

    Congruent

    Congruent

    Congruent

    Congruent

    No

    No

    Frohlich and Parker (2000)

    Congruent

    No

    Yes

    Congruent

    Congruent

    Yes

    No

    No

    Meyen (1986, 1988)

    No

    No

    Congruent

    Congruent

    Congruent

    Congruent

    Yes

    Congruent

    Stuessy (2004, 2010)

    Congruent

    No

    Congruent

    Congruent

    Congruent

    Congruent

    Yes

    Yes

    Takhtajan (1969, 1976)

    Yes

    Yes

    Congruent

    Yes

    Congruent

    Congruent

    No

    Congruent


    A few elements of ideas proposed by Cascales-Miñana et al. (2016), the anthophyte hypothesis (J. A. Doyle and Donoghue 1986, 1987) and classic research by Arber and Parkin (1907), Edgar Anderson (1934), Axelrod (1952), Ehrlich and Raven (1964), Raven and Kyhos (1965), Takhtajan (1969, 1976), and Raven (1977), dovetail with- and potentially support my coevolutionary hypothesis on the origin of flowering plants, which is developed on the following pages of the web site for purposes of classroom and seminar debate and discussion.

    Armen Takhtajan's often criticized proposal on a "neotenous" origin of flowering plants (1969, 1976, and previous papers) is my starting place.

    "... Equally puzzling is that despite intense interest in the origins of seed plants and angiosperms throughout the entire last century, few have looked at the problems from a life cycle evo-devo perspective, with perhaps one exception (Takhtajan 1976), who alluded to neoteny as one of the possible mechanisms contributing to the origin of angiosperms."

    The above quotation is from page 296 of Yin-Long Qiu (2008), Phylogeny and evolution of charophytic algae and land plants. Journal of Systematics and Evolution 46(3): 287-306.

    "Some authors seem curiously determined to prove that pre-Cretaceous fossils are crown-group angiosperms, but for understanding most aspects of the origin of angiosperms [other than their age], close stem relatives would be far more significant ..." (page 318, J. A. Doyle 2012)

    Based on four decades of study of the problem by Professor Emeritus J. A. Doyle, where on the Pangaean continent (and when) do students of angio-ovuly and the origin of flowering plants focus the search for "close stem relatives" of the group?

    First clues on the origin of angiosperms. Surprising and often ignored clues shedding light on the shadowy origin of flowering plants originate from oil and gas exploration data and the geochemistry of taxon-specific biomarkers (TSBs) and molecular traces, which are recoverable from mud logs of well boreholes, or from coal balls, compressions, and permineralizations (Moldowan and Jacobson 2002).

    Molecular tracers include naturally occurring but fossilized triterpenoids known as oleanone triterpanes (oleananes). Oleananes, together with ursenes, lupenes, and taraxerenes are important TSBs that belong to a class of Β-amirin triterpenoids (Moldowan and Jacobson 2002). Class 1c resin constituents associated with Mesozoic angiosperm amber are known from 320 million year old (Paleozoic) amber samples (Bray and K. B. Anderson 2009).

    Oleananes occur in fossilized leaf material of certain gigantopterids, bennettitaleans, and flowering plants (Moldowan and Jacobson 2002), but are absent from samples of several other fossil seed plants (D. W. Taylor et al. 2006).

    Mud-loggers are able to ascertain higher plant input into a core segment of a stratigraphic horizon pulled-up from the well-site gas chromatography and mass spectrometry, and microscopic analysis of animal and plant microfossils including pollen and vascular plant fragments in core samples.

    These TSBs are a stratigraphically-important but "inconvenient" truths which are often buried or ignored in modern syntheses on the origin and evolution of flowering plants.


    Problems with Contemporary Data Sets:

    Controversial assertions abound in the scientific literature of the 20th Century and three categories of credible hypotheses and theories exist (Rothwell et al. 2009). None of these ideas when taken as a whole are neither compelling or plausible to many scientists, including the author. Almost certainly, accomplished studies of the Amborella trichopoda genome, though useful in disentangling aspects of the evolution of GRNs and horizontal transfer (HT), will not help paleobiologists determine the origin(s) of angiosperms.

    "We have examined herein different methodological approaches (i.e. fossil-based, molecular, phylogenetic and paleobiogeographic studies) and current viewpoints about the explosive Cretaceous diversification of angiosperms. After integrating evidence as a whole with our results, the resulting scenario suggests that there is nothing particularly mysterious about the diversification of angiosperms during Cretaceous times or how it is reflected in the fossil record. The clade probably first appeared during Triassic times, possibly as a result of the re-setting of plant evolutionary history following the devastating global extinction event of the Permian–Triassic boundary ..." (4. Conclusions, Cascales-Miñana et al. 2016).

    The preceding statement is an optimistic appraisal of methodology used by Cascales-Miñana et al. (2016). Some "current viewpoints" are left out of the analysis. The fossil dataset used by the Cascales-Miñana team is grossly incomplete.

    A cartoon was drawn by Sul Ross State University geology student Mark Munday in 1981. The artwork by Mark, which is furnished David Rohr, Ph.D., and Mark's help at the delnortea beds is gratefully acknowledged.

    Caytoniales and angiosperms diverged from a common ancestor with Bennettitales in the Lower Triassic according to Cascales-Miñana et al. (page 258, Figure 1, 2016). Yet, these authors assert that "... the [angiosperm] clade probably first appeared during Triassic times," which is a stratigraphically-perplexing Gordian Knot.

    Why assume that flowering plants constitute a single clade first appearing 256 MYA without discussing Mathews (2009), Mathews et al. (2010), and C. S. P. Foster et al. (2017)? Simply put, paleontologic data are required to calibrate and validate molecular phylogenies (Peterson et al. 2007).

    "The interface of these three subject areas (Figure 1 on Page 778), molecular evolution, evolutionary developmental ('evo-devo') biology, and palaeoecology, is the theme of Molecular Palaeobiology, as it [the approach] uniquely integrates the patterns written in the two historical records, genomic and geological ... "

    The preceding statement is from Page 777 of Kevin J. Peterson, R. E. Summons, and P. C. J. Donoghue (2007), Molecular Palaeobiology, Palaeontology 50(4): 775-804.

    Further, problems associated with co-radiations of angiosperms and insects are brought to light by phylogenetics (T. Hunt et al. 2007, Ramírez et al. 2011, Misof et al. 2014), and detailed analyses of paleobiological data (Labandeira 2014).

    Presumed co-radiations of flowering plants with chrysomelid beetles are asynchronous (Gómez-Zurita et al. 2007) suggesting that evolution of certain clades of late Mesozoic phytophagous ants, bees, beetles, butterflies, flies, and moths might be independent of the explosive origin and spread of eudicot orders and families (Labandeira 2014).

    "Anthophilous insects must have played a decisive role in the transformation of a gymnosperm strobilus into the angiosperm flower."

    The preceding statement is from page 35 of Armen Takhtajan (1969), Flowering Plants: Origin and Dispersal (translated by C. Jeffrey). Edinburgh: Oliver and Boyd, 310 pp.

    Root Gorelick (2001) challenges the validity of a biotic coevolutionary hypothesis on the origin of flowering plants. Conrad Labandeira is apparently less than enthusiastic on the idea of a coevolutionary origin of the group (2014).

    Labandeira's findings (2014) might also help disprove the notion of a Hauterivian (Lower Cretaceous) origin of flowering plants (Hughes 1994, Friis et al. 2013), which is strangely incongruent with the stratigraphic distribution of Afropollis throughout the Mesozoic, because coevolution of insects and flowers is unsupported by macroecological data in a 35 million year interval in geologic time from Barremian to Turonian.

    "Angiosperms certainly contributed to the spectacular diversity of beetles, but these insects were well on their way at least 100 million years before angiosperms came on the scene ... "

    The preceding statement is quoted from page 399 of David Grimaldi and Michael S. Engel (2005), Evolution of the Insects. Cambridge: Cambridge University Press, 755 pp.

    Tetrapods might have had a surprising effect on the ecology of Mesozoic flowering plants but evidence of coevolution of dinosaurs and early angiosperms is weak (P. M. Barrett and Willis 2001, P. M. Barrett 2014). "Tight coevolution" between animal disperser and plant was probably rare (page 3, Tiffney 2004).

    Errors in molecular-phylogenetic inference may result from effects of LBA (Barrett and Willis 2001, Magallón 2010, Zhenxiang Xi et al. 2014). Paraphyly may be underappreciated (Krassilov 2002, Stuessy 2010) and effects on seed plant evolution attributable to possible HT might cloud our understanding of relationships among basal clades of the angiosperm crown group (Bergthorsson et al. 2004).

    "Darwin himself referred to the 'early origin and diversification of angiosperms' as 'an abominable mystery,' and the origin of the flower- and therefore flowering plants- is still a question ..." (page 86, Pamela S. Soltis and Douglas E. Soltis 2014)

    Molecular-phylogenetic analyses by Magallón (page 395, 2010) when calibrated with fossil data and compared with different relaxed-clock methods "... imply that the diversification that lead to living angiosperm species began sometime between the Upper Triassic and the early Permian."

    "Molecular phylogenies suggest that angiosperms are sister to all other living seed plants" (Wilson and Knoll, page 344, 2010)

    Further, ancient whole genome duplications (WGDs) are implicated in both the common ancestor of all flowering plants, and in the most recent common ancestor of all seed plants (MRCA) about 200 MYA, and 320 MYA, respectively (Jiao et al. 2011).

    Clusters of hermaphroditic pollen- and ovule bearing leaves known as bisexual strobili are the focus of most of the leading models of cone and floral organization (Melzer et al. 2010). Further, several studies of developmental abnormalities in cones of extant conifers offer a window for better understanding the origins of flowers and flower-like organs (Flores-Rentería et al. 2011, Rudall et al. 2011, Carlsbecker et al. 2013, J. M. Alvarez et al. 2015).

    If fertile spur shoots are demonstrably ancient organs known from late Paleozoic seed plant fossils then how could the flower possibly originate in the late Mesozoic? Based on my interpretation of the first sentence of Chanderbali et al. (2016), Andre S. Chanderbali, B. A. Berger, D. A. Howarth, P. S. Soltis, and D. E. Soltis resuscitate this paradox. Based on a discussion of floral evo-devo by Becker (2016), these students of the floral tool kit probably have more work to do.

    "The flower remains ill-defined and its mode (or modes) of origin remain hotly disputed; some definitions and hypotheses of evolutionary relationships preclude a role for the flower in delimiting the angiosperms."

    The preceding statement is from the abstract on page 3471 of R. A. Bateman, J. Hilton, and P. J. Rudall (2006), Morphological and molecular phylogenetic context of the angiosperms: contrasting the 'top-down' and 'bottom-up' approaches used to infer the likely characteristics of the first flowers, Journal of Experimental Botany 57(13): 3471-3503.

    In my opinion, "assembly" (page 816, J. A. Doyle 2008) of perianth parts, microsporophylls, and megasporophylls to form a flower was an improbable and unnecessarily complicated saltational event punctuating a long and gradual evolutionary history of angiosperms. In my opinion, flowering plants did not appear "suddenly," and the concept of a so-called "first flower" including proposals published by Albert et al. (2002) and Chanderbali et al. (2016), should be reconsidered.

    Simply put, massive, shortened bisexual cone axes bearing megasporophylls, laminar microsporophylls, and spirally-arranged foliar tepals, probably existed in populations of poorly understood Paleozoic seed plants described as gigantopteroids and Vojnovskyales, groups omitted by J. A. Doyle and others in their many published phylogenetic analyses. The reproductive short- (spur-) shoots of these Permo-carboniferous seed plants were equivalent to theoretical constructs of the protoflower proposed by Leppik (1960, 1968).

    Flowers and simple cones are reproductive short- [spur-] shoots according to Christianson and Jernstedt (2009). Deciphering evo-devo of short- [spur-] shoots on growing mother plants in hybridizing Permo-carboniferous seed plant populations is probably a central tenet in disentangling at least some aspects of the allopolyploid origin of the flowering plants.

    Floral morphologies are deeply-conserved in angiosperms according to Melzer et al. (2014) and Becker (2016), which are determined by expression of CRMs, GRNs, PINs, and TFs. Deciphering the ancestry of flowering plants and their paleoecologies probably requires an understanding of the paleontology of "fingerprints of developmental regulation" (quoted from page 723, Sanders et al. 2007) expressed as often disarticulated and shed, wood-, pollen-, seed-, foliar-, and cone- and floral- organs preserved in the fragmentary rock record of the Carboniferous, Permian, and Triassic periods.


    [ Developing a Coevolutionary Hypothesis ]

    Coevolution between phytophagous insect antagonists and Carboniferous, Permian, and Triassic seed plant hosts at the level of their respective developmental tool kits with focus on selective forces that drive the logic of transcriptional regulation is proposed to explain the origin of angiosperms and certain clades of holometabolous insects.

    Many colleagues suggest a coevolutionary origin and later diversification of flowering plants based on co-radiations between specific groups of animals and seed plant hosts (Ehrlich and Raven 1964, Farrell 1998, Crepet and Niklas 2009).

    While composing the three essays on the origin and evolution of flowering plants, I integrated data from many scientific disciplines, which was key to possibly solving the riddle of the origin of angiosperms and certain coevolving Holometabola from disparate research perspectives. This challenging and daunting approach was facilitated by ready access to several world class research libraries at the University of California, Berkeley.


    Discerning Fingerprints of Developmental Regulation:

    This chapter of the essay considers experimental approaches and paleobiological evidence drawn from the research perspective of evo-devo, which is necessary to identify lineages of seed plants involved in the origin and evolution of flowering plants.

    The image to the right is the passive insect trapping flowering plant, Darlingtonia californica (Sarraceniaceae, Ericales, Asteranae), photographed by the author at a seep on Eight Dollar Mountain located in the Klamath Region of western North America.

    Could paleoecologists benefit by studying experimental, 3-D printed artificial constructs of shoots and protoflowers in theoretical morphospace? Yes.

    By measuring and scaling detached and shed foliar and cone- floral-organs, and by combining these data with studies of permineralizations, "fingerprints of developmental regulation" (quoted from page 723, Sanders et al. 2007) could potentially be discerned in the fossil record.

    Studies of evolving allometries and body plans might help us understand a possible coevolutionary origin of angiosperms and certain clades of holometabolous phytophagous insect antagonists.

    Evolutionary-development of arthropod- and plant organs and molecular tool kits is "highly dynamic in evolutionary time" involving the evolution of cis-acting promoters (page 83, Baum 1998).

    The evo-devo research perspective could help us decipher more than 400 million years of insect and seed plant evolution and the enigmatic origins of flowering plants and interacting Holometabola.

    "The idea is that plants have a plastic and modular developmental system such that simple changes in regulatory genes need not lead to inviability but can generate novel, potentially favored phenotypes."

    The preceding quotation is from page 83 of D. A. Baum (1998), The evolution of plant development. Current Opinion in Plant Biology 1(1): 79-86.

    Reviews by Rothwell (1987), Arthur (2002), Meyerowitz (2002), Becker and Theißen (Figure 1, page 468, 2003), Niklas (2006), Rothwell et al. (2014), and Tomescu (2016), among others, are useful in understanding the developmental systems of animals, fungi, and plants.

    "Ontogeny in land plants can be viewed as a complex, partly hierarchical, series of developmental processes, which together with their underlying genetic controls, provide the raw material for morphological innovation. Ontogeny is thus the creative force behind botanical diversification, and small modifications at the genetic level may have a disproportionate effect on plant form as their consequences cascade and multiply through development. Plant evolution occurs as variation in genetic and epigenetic developmental processes is winnowed by ecology..."

    The preceding quotation is from page 161 of P. R. Crane and P. Kenrick (1997), Diverted development of reproductive organs: a source of morphological innovation in land plants, Plant Systematics and Evolution 206: 161-174.

    Biometry and scaling in theoretical morphospace. From the research perspectives of insect- and floral biology, and paleoentomology and floral morphology, scaling data might be applied to understanding and computing theoretical morphospace of whole invertebrate and/or plant organs (Jeune et al. 2006, McGhee 2007, Chartier et al. 2014). The interface between development and ecology may be studied from such perspectives, among others (Enquist et al. 2007).

    "In theoretical morphospaces, the axes of the reduced space are determined by a small set of parameters of morphogenetic or other biological models, derived from theoretical considerations rather than from the organisms themselves" (page 841, Chartier et al. 2014).

    Scaling studies of reproductive short- {spur-] shoots of living Ginkgo are particularly revealing to plant morphologists (Christianson and 2009).

    Sean B. Carroll (1995), Rogers et al. (1997), Gellon and McGinnis (1998), and S. B. Carroll et al. (2005) review molecular evolution of homeotic genes and homeodomain TFs needed to understand regulation of body ground plan development in phytophagous arthropod antagonists. Molecular control over arthropod growth varies among the major clades of insects (Grimaldi and Engel 2005).

    A key paper on the control of insect body size by Nijhout (2003) outlines the molecular mechanisms involving cis-acting TFs and hormones and environmental controls (nutrition and temperature) behind growth and cell division in hemimetabolous and holometabolous insects.

    Several neurosecretory hormones play an important part in mechanisms that regulate cell division and growth including insulin-like peptides (Drosophila insulin-like proteins [DILPs] and bombyxins), chitenase-derived imaginal disk factor proteins, the steroid hormone ecdysone, local autocrine and paracrine TFs, and brain neurosecretory prothoracicotropic hormone (PTTH) (Nijhout 2003).

    Cessation of growth in holometabolous insects leading to a new moulting cycle is triggered by PTTH that initiates the ecdysone growth regulatory cascade. Prothoracicotropic hormone and/or ecdysone secretion in Holometabola is negatively controlled by juvenile hormone (JH) (Truman and Riddiford 2002). Once JH circulating in the hemolymph is destroyed by juvenile hormone esterases, then PTTH secretion resumes under circadian (22-24 hour) photoperiodic control (Nijhout 2003). On the other hand, certain hemimetabolous bugs (Hemiptera) possess abdominal stretch receptors that activate secretion of PTTH (Nijhout 2003).

    Arthropod body allometry is intertwined with development of larval and imaginal disc tissues (Stern and Emlen 1999, Shingleton et al. 2008) and assembly of chitin and cuticle proteins into the exoskeleton (Charles 2010, Moussian 2010). Studies on Drosophila melanogaster eggs, specifically, artificial size-selection experimentation, affects larval patterning and body allometry (Miles et al. 2011).

    Do host seed plant brassinolides and other hormones affect insect antagonist egg size, potentially controlling larval tissue patterning?

    If the answer to the preceding question is "yes," how does this evo-devo mechanism affect arthropod antagonist body allometries and population ecology?

    The evo-devo of insect caste polyphenism is reviewed by Emlen and Nijhout (2000). A review of neotenous development in termites is available (Korb and Hartfelder 2008). Isoptera (termites) are hemimetabolous insects (Grimaldi and Engel 2005).

    Insect developmental tool kit. The insect developmental tool kit is comprised of certain homeotic selector genes (including Hox genes), zygotic (gap- maternal-, and pair-rule-) genes, field-specific selector genes, compartment selector genes, cell-type-specific selector genes, and segment polarity genes; and the TFs they encode (Rosenberg et al. 2009). In addition, the insect developmental tool kit is comprised of controlling factors behind the cessation of insect growth including bioactive PTTH, JH, juvenile hormone esterases, and ecdysone steroids (Truman and Riddiford 2002, Nijhout 2003, S. B. Carroll et al. 2005, Callier and Nijhout 2013).

    Thummel and Chory (2002) point to a possible coevolutionary connection between the 20E-ecdysone/cytochrome P450 biosynthetic machinery of insect antagonists and seed plant hosts. Structurally similar to bioactive plant brassinosteroids, 20E-ecdysone induces a cascade of TF biosynthesis important in the regulation of insect development (Truman and Riddiford 2002, De Loof 2008).

    Juvenile hormone biosynthesized in the corpora allata of the insect brain is a sesquiterpenoid epoxide methyl ester (Hartfelder 2000). Interestingly, many naturally-occurring plant sesquiterpene esters and lactones are bioactive and exhibit insecticidal properties. Juvenile hormone and its homologs are integral in vitellogenesis (Hartfelder 2000), regulation of moult cycles (Truman and Riddiford 2002), and caste development and behavior in social Hymenoptera (Guidugli et al. 2005).

    Were bioactive brassinolides and sesquiterpenes manufactured by Paleozoic seed plants used as chemical warfare agents to affect growth, development, and behaviour of herbivorous insects?

    Another important reason for students of insect-seed plant coevolution to be conversant with arthropod tool kits is that evo-devo of the anterior (head) segment is linked to feeding, pollinating, and sensory perception. Labandeira (2010) states:

    "The most obvious feature of an insect that reveals consumption of nectar or pollen, or the existence of a pollinator association, is the mouthparts and head structure ..."

    The aforementioned passage is from page 471 of C. C. Labandeira (2010), The pollination of mid-Mesozoic seed plants and the early history of long-proboscid insects, Annals of the Missouri Botanical Garden 97(4): 469-513.

    Several developmental gene families, TFs, and enzymes involved in hormone signaling cascades are known in invertebrates based in part, on experimental studies of the Drosophila model arthropod (S. B. Carroll et al. 2005, Hittinger and S. B. Carroll 2008, Rosenberg et al. 2009).

    Key elements of the Drosophila molecular tool kit include:

  • Achaete-Scute [AS-C] complex (four-gene complexes encoding TFs critical for bristle patterning and neural cell development)
  • apterous [ap] (compartment-selector gene encoding Apterous protein needed for subdivision of imaginal discs into dorsal and ventral compartments)
  • bicoid [bcd] (maternal effect gene necessary for anterior embryo development)
  • caudal and nanos (maternal effect genes needed for posterior development of the embryo)
  • decapentaplegic [dpp], short-gastrulation [sog], snail [sna], twist [twi], and zerknüllt [zen] (maternal effect genes involved in subdivision of cells in the dorsiventral axis of larvae)
  • distal-less [dll] (field-specific selector gene necessary for limb [antennae, genitalia, mouthparts, legs] development)
  • engraled [en] (compartment-selector gene encoding the homeodomain protein Engraled, which determine the posterior identity of embryos and wings).
  • even-skipped, fushi-tarazu [ftz] (encodes Ftz protein [Merebet and Hudry 2011]), hairy, and paired (pair-rule genes which act in the periodicity of double segments)
  • eyeless [ey] (encodes Ey protein, a DNA TF which regulates other field-specific genes)
  • giant, huckebein, hunchback, knirps, Krüppel, and tailless (gap genes that regulate larval segmentation)
  • hedgehog and wingless (segment polarity genes which organize the orientation and patterns of cells within the anteroposterior axis of each larval segment)
  • Hox genes (clusters of eight linked homeotic selector genes absolutely required for embryo, larval, and adult development)
  • Runx genes (clusters of homeotic selector genes that regulate development)
  • scalloped [sd] and vestigial [vg] (field-specific selector genes required for haltere and wing development)
  • tinman (field-specific selector gene that controls development of the insect heart)
  • Evolution of the Hox complex. Molecular diversification of the Hox gene complex over the course of 600 million years of metazoan evolution is analogous to the 400 million year old molecular evolution of MIKC-type MADS-box genes and related cis-acting TFs of land plants (Theißen et al. 2000, Theißen 2001, and Theißen and Becker 2004).

    Evolution of the Hox complex probably involved small gene duplications, WGDs, divergence of homeodomains, disintegration of the Hox cluster at breakpoints, and rapid changes in the nucleotide sequence of homeodomains (S. B. Carroll et al. 2005, Negre et al. 2005). Further, changes in the arthropod homeodomain and evolution of new protein motifs led to new Hox developmental tool kit functions in certain insect lineages (S. B. Carroll et al. 2005).

    The homeotic selector genes (S. B. Carroll et al. 2005, among others) of the Drosophila Hox complex are:

  • abdominal A [abd-A] (selects the developmental fate of the front-middle parts of the abdomen)
  • Abdominal B [Abd-B] (selects the developmental fate of the rear-middle part of the abdomen)
  • antennapedia [ANTb] (affects development of the middle legs and middle part of the thorax)
  • deformed [Dfd] (affects development of the upper part of the head)
  • labial [lab] (selects the developmental fate of the labium of the head)
  • proboscipedia [pb] (affects development of the lower half of the head)
  • sex combs reduced [Scr] (selects the developmental fate of the most posterior region of the head, labial segment, front legs, prothorax, and front and anterior portions of the thorax) (Rogers et al. 1997)
  • ultrabithorax [Ubx] (selects the developmental fate of the rear legs and thorax and front of the abdomen; regulator of dipteran haltere morphogenesis [Pavlopoulos and Akam 2011])
  • Ancestral arthropods possess two additional homeotic selector genes of the Hox cluster that together comprise the HOM-C, ten gene complex (see discussion in Negre et al. 2005). These additional genes are:

  • fushi-tarazu [ftz] (encodes Ftz protein [Merebet and Hudry 2011]), and
  • Hox3
  • Genomic analyses suggest that derived winged insects lost functional copies of ftz and Hox3 through disintegration of the HOM-C complex (Negre et al. 2005). Duplication of the Hox3 gene of ancestral Cyclorrhaphan flies gave rise to two maternal effect genes, bcd and zen (Stauber et al. 2002). Based upon this study it is important to include Hox3 as part of the ancestral diverging insect developmental tool kit.

    Early divergent arthropod developmental tool kit. Possible candidates for the early divergent insect developmental tool kit might include certain homeotic selector genes of the Hox complex such as homologs and paralogs of abd-A, Abd-B, Hox3, pb, Scr (Rogers et al. 1997), Ubx (Pavlopoulos and Akam 2011), and the field-specific selector gene necessary for limb development in Drosophila (Diptera) known as dll (S. B. Carroll et al. 2005).

    The importance of Ubx protein encoded by the Ubx gene in the early divergent insect developmental tool kit cannot be neglected in the present analysis since significant changes in the carboxy-terminal (C-terminal) region (Galant and Carroll 2002) and serine/threonine phosphorylation sites (Ronshaugen et al. 2002) are probably behind many insect body plan novelties seen in the paleontologic record of the past 400 million years of arthropod and crustacean evolution (Pavlopoulos and Akam 2011, Pavlopoulos and Averof 2002).

    Fushi-tarazu protein encoded by the ftz gene, intracellular tertiary enzyme structure folding environments, and the apparent flexibility of Ftz and other Hox proteins in the evolution of arthropods, are discussed in a recent review by Merebet and Hudry (2011). Another Hox protein Abd-B, when combined with the Dsx enzyme, represses expression of the wg gene in fruit flies (W. Wang et al. 2011).

    These studies, among others underway or already published by Sean Carroll and colleagues, underscore the importance of Hox proteins in evolution of the arthropod tool kit.

    I also add hexamerin moulting storage proteins which are related to hemocyanin respiratory enzymes (Burmester et al. 1998, Burmester 2001, Burmester et al. 2006, Burmester and Hankein 2007), JH esterases, vitellogenin genes and yolk proteins (Isoe and Hagedorn 2007), pheromone chemoreceptors (Robertson and Wanner 2006), and certain nuclear receptor proteins (Bonneton et al. 2003, Bonneton et al. 2008) including ultraspiracle, and ecdysone inducible TFs to the list of molecular developmental tools among early diverging arthropod lineages.

    Respiratory enzymes, specifically hemocyanins and hemoglobins, and moulting storage proteins (hexamerins) are key elements of the early divergent arthropod developmental tool kit that tie-in with the evolution of insect legs and wings from bilaterian gills. Ancient insect wings probably functioned as respiratory organs. Wings, halteres, arachnid spinnerets, and insect legs are all organs that develop from limb fields of cells where Ubx expression is prevalent (S. B. Carroll et al. 2005).

    Further, hexamerins are also implicated as silencers of JH signaling in neotenous castes of hemimetabolous termites (X. Zhou et al. 2006, X. Zhou et al. 2007) and caste polyphenism in holometabolous wasps (J. H. Hunt et al. 2007).

    Insect developmental tool kits and a Paleozoic origin of the Holometabola. Understanding the nature and timing of early molecular diversification of homeotic selector genes, developmental proteins, nuclear receptor proteins, and cis-acting TFs of both invertebrate antagonists and vascular plant hosts might be a critical first step in understanding the Paleozoic origin of holometabolous insects and their putative coevolution with the earliest angiosperms.

    The place and time to begin a molecular phylogenetic analysis is the late Frasnian-Famennian Age hypoxic icehouse that extended into the Tornaisian Age of the Carboniferous Period. Certain details of the Frasnian-famennian boundary extinction (DeCARB) are discussed in a later section.

    Molecular model systems used as tools in beetle genomic research and phylogenetic studies include proteins central to development (JH esterases), diapause proteins, heat shock proteins, ultraspiracle (an ecdysone nuclear receptor protein), cuticle proteins, hexamerins, genes encoding vitellogenin, and apolipophorins, among others (see review by Gómez-Zurita and Galián 2005).

    Several insect systematists studying beetle (Coleoptera) evolution are employing some genes and proteins of the insect development tool kit in their phylogenetic analyses (Gómez-Zurita and Galián 2005). Gómez-Zurita and Galián (2005) discuss the utility of molecular phylogenetic characters appearing in the entomological literature in a review paper, which is organized along the lines of Floyd and Bowman (2007) for land plants (see section below).

    Land plant developmental tool kit. Understanding the land plant developmental tool kit and gene regulation from a deep time research perspective ties-in with models of cone and floral organization, cell geometry and regulation of growth from SAMs, paleobiology of homeodomain TF trafficking, phyllotaxis, leaf development, and morphogenesis of fertile organs.

    Evolutionary-development of early land plants was probably intertwined with regulatory changes in polycomb repressive 2 gene complexes and other stem cell factors as evidenced from studies of the extant model bryophyte Physcomitrella (Okano et al. 2009).

    Floyd and Bowman (2007) are the first workers to estimate the developmental tool kit of early land plants including Paleozoic seed plant homeotic genes potentially important in the later evolution and diversification of angiosperms and origin of the first flowers from bisexual cone axes sensu Melzer et al. (2010).

    The work by Floyd and Bowman (2007) focuses on a molecular phylogenetic analysis of Chara (a green alga), Physcomitrella (a moss), Selaginella (a lycophyte), Arabidopsis (angiosperm malvid), Antirrhinum (angiosperm asterid), Oryza (angiosperm monocot), Populus (angiosperm fabid), Picea (gymnosperm conifer), and Pinus (among others).

    A review of plant homeobox genes and homeodomain proteins offers additional insight into critical elements of the land plant developmental tool kit (Mukherjee et al. 2009).

    Many developmental gene families and cis-acting TFs have been identified in land plants (Langdale 2008, Mukherjee et al. 2009, Specht and Bartlett 2009, Licausi 2011, Glover 2014, among others). These genes, and their TFs, together with phytohormone biosynthetic and regulatory factors, homeotic selector genes, and certain microRNAs, comprise the developmental tool kit of land plants including lignophytes. The main developmental and regulatory gene tools of focus are:

  • APETALA 2 (AP2) (see euAP2, below)
  • ARF (auxin response factor gene family)
  • ARP (KNOX regulating genes ASYMMETRIC LEAVES1, ROUGHSHEATH2, PHANTASTICA [ARP])
  • AS2 (LOB family genes that function in lateral organ formation in SAMs)
  • Class III HD-Zip (a family of SAM maintenance genes and upstream controllers of leaf development)
  • Class I KNOX (essential genes to meristem maintenance and SAM formation affected by auxins and gibberellins)
  • Class I TCP (leaf sculpting genes and cell division controllers)
  • Class II TCP (genes that determine leaf shape, floral symmetry, and flower patterns)
  • CUC (important genes in embryo, flower, and leaf development, Bilsborough et al. 2011)
  • ERF ethylene responsive factor genes encode ERF proteins that potentially reprogram metabolic pathways and morphologies affected by hypoxia (low pO2) (Licausi 2011)
  • euANT (regulating genes involved in lateral organ development)
  • euAP2 (SAM maintenance and timing of flowering including APETALA 1 [AP1]and AP2)
  • GRAS (a family of genes necessary for radial patterning of roots and shoots and axillary meristem development [HAIRY MERISTEM, LATERAL SUPRESSOR, SCARECROW], and in mediation of gibberellic acid (GA) responses during flowering and development of trichomes [DELLA genes])
  • KANADI (GARP family transcriptional regulators antagonistic to Class III HD-Zip genes important to leaf and integument development)
  • LEAFY [LFY] and FLORICAULA [FLO] (controllers of the downstream expression of several genes including MIKC-type MADS-box genes, Moyroud et al. 2010)
  • MIKC-type MADS-box genes (developmental genes that control organogenesis in seed plants) encode MIKC-type MADS-box proteins that regulate cone and floral development, among other functions
  • MYB genes encode myeloblastosis (MYB) homeodomain proteins necessary for lignin biosynthesis, secondary wall thickening, and petal morphogenesis
  • NAC genes encode NAC TFs necessary for secondary cell wall biosynthesis (Zhong et al. 2010)
  • PIN (auxin related genes needed in land plant architecture)
  • TIR (auxin related genes)
  • UFO (stem cell maintenance gene)
  • WOX Class genes including WUSCHEL [WUS] (essential genes for stem cell maintenance in organizing centers of SAMs) that encode WOX and WUS homeodomain proteins (Nardmann et al. 2009, Nardmann and Werr 2013, Costanzo et al. 2014)
  • YABBY (seed plant specific family of genes that promote differentiation of abaxial tissues and leaf growth)
  • Based on a molecular-phylogenetic analysis by Floyd and Bowman (2007) the ancestral land plant tool kit genes of our focus to deduce the timing of the origin of the first flower should be AP2, ARF, Class I and II TCP, Class III HD-Zip, GRAS, KNOX, LFY, MIKC-type MADS-box, PIN, TIR, and YABBY genes. Genes that encode the other conserved homeodomain proteins (MYB, WOX, WUS) might also be important to consider in floral tool kit studies.

    All available evidence suggests deep conservation in the xylem transcriptome of foliar organs, stems, and roots of vascular plants (X. Li et al. 2010), which is consistent with Floyd and Bowman's findings (2007).

    Ancient root apical meristems (RAMs). Definitive fossilized evidence of a growing seed plant root apical meristem (RAM), which is complete with permineralized stem cells, procambium, and Körper-Kappe, is reported from a >300 million-year-old coal ball (Hetherington et al. 2016).

    Discovery of the Radix RAM spawns more questions than answers, in my opinion. First and foremost, study of the root anatomy of Amborella trichopoda reveals a derived stem cell structure, which is eudicot-like (Seago and Fernando 2013).

    The GRAS family of homeodomain proteins and genes encoding these TFs is necessary for radial patterning of roots and shoots and axillary meristems (Floyd and Bowman 2007). Eudicot-like "fingerprints of developmental regulation" discernable in the RAM of amborellas indicate a modern GRAS homeodomain protein tool kit.

    Since the permineralized RAM of Radix carbonica is different from any known but extant gymnosperm, what can paleobotanists and plant biologists conclude from its "fingerprint of developmental regulation"?

    "... Comparison of the cellular organization of the different regions of the root apex indicates that the cellular dynamics [root cap] in R. carbonica conforms to that in extant root apical meristems [RAMS] ..." (Results and Discussion on page 1629 of Hetherington et al. [2016], words in [brackets] are mine).

    Were Radix carbonica roots once attached to a callistophytalean or vojnovskyalean seed plant rooted in a Carboniferous swamp?

    Cell geometry of shoot apical meristems (SAMs). Much progress has been made on understanding developmental biochemistry and hormonal controls behind the anatomy and cell geometry of SAMs and accessory fertile meristems of a number of diverse flowering plants and gymnosperms (Busov et al. 2008, Glover 2014). The best studied example is the diminutive mouse-ear cress (Arabidopsis thaliana [Brassicaceae, Brassicales, Rosanae]), an extant, highly derived annual species of malvid mustards (Kwiatkowska 2006).

    Floral meristem identity and integrator genes of massive SAMs of the oil palm (Elaeis guineensis [Arecaceae, Arecales, Lilianae]) have also been studied (Adam et al. 2007).

    Biomechanics is a fertile area of research in botany (Niklas 1992, Niklas 2000, Rowe and Speck 2005, Niklas et al. 2006, Read and Stokes 2006, Masselter et al. 2009). Basic to biomechanics are the biochemical pathways in plant cells (e.g. lignin biosynthesis) that result in secondary thickening of vascular tissues of the procambium and secondary cambium. Secondary cell wall biosynthesis involves R2R3 myeloblastosis (MYB) transcription factors (TFs) and NAC TFs (Zhong et al. 2010).

    Can the experiments drawn from principles of geometry and engineering answer some of the basic questions posed by Coen et al. (2004)?

    "Whatever the detailed mechanism for aligning cell axes with gradients [of morphogen flow], these considerations indicate that morphogens play two distinct roles in the generation of shape. The first is a regionalizing role, involved in elaborating differences between regions [of meristems], such as levels of gene activity, growth rate, or anisotropy. The second is a polarizing role involved in specifying directions of cell axes. Morphogens with a regionalizing role often act by influencing transcription factors, which in turn can affect parameters such as growth rate and anisotropy. Cells respond only to the overall concentration of these morphogens, not to the direction of their gradient. Morphogens with a polarizing role, influence the orientation of cell axes and can determine the principal directions of growth. Cells respond to the highest slope of the morphogen gradient or to the direction of morphogen flow. Such responses [of plant cells] are unlikely to be mediated by transcription factors, as the directional information would be lost through conversion to a gene expression level."

    The preceding quote is from E. Coen, A.-G. Rolland-Lagan, M. Mathews, A. Bangham, and P. Prusinkiewicz (2004), The genetics of geometry, Proceedings of the National Academy of Sciences 101(14): 4728-4735. The phrases in brackets [] are mine.

    Certain anatomical and enzymatic tools of the land plant hormone signaling machinery align cell axes and control morphogen flow. Some of these affect SAM development and phyllotaxis in both morphospace and time resulting in evolutionary change.

    "Evolutionary changes in developmental tissue geometry, in our terminology, are the result of heterotopy."

    The preceding sentence is quoted from M. L. Zelditch and W. L. Fink (1996), Heterochrony and heterotopy: stability and innovation in the evolution of form. Paleobiology 22(2): 241-254.

    Shoot apical meristem (SAM) organization. The SAM, stem cell geometries, and fertile SAM phyllotaxis figure prominently in several evo-devo hypotheses on the origin of cones and flowers (Theißen Saedler 2001, Becker and Theißen 2003, Baum and Hileman 2006, Theißen and Melzer 2007, Melzer et al. 2010).

    "Although the ovulate stalks of Ginkgo biloba occur on short shoots of indeterminate growth [rather than in a compound cone; Christianson and Jernstedt, 2009], they are not attached to the subtending leaf or bract, and the seeds are not inverted" (pages 934-935, Rothwell and Stockey 2016).

    Biochemical and morphological evidence suggests that cones and flowers are reproductive short shoots. If fertile spur shoots are known from late Paleozoic fossils, and the floral SAM is a deeply conserved organ (Theißen and Melzer 2007, Becker 2016, among others), then how could the flower possibly originate in the late Mesozoic? Andre S. Chanderbali et al. (2016) seemingly resuscitate this paradox in the first sentence of their review. Genomic- and tool kit phylogenies and cladograms such as APG IV, unless calibrated with definitive fossils from accurately-dated stratigraphic horizons, are probably unhelpful in deciphering the origin of canalized cone and floral morphologies, and their deeply-conserved gene regulatory program including CRMs, GRNs, and PINs.

    Reviews of SAM development in model flowering plants are available (Bäurle and Laux 2003, Aida and Tasaka 2006 [two papers], Carraro et al. 2006, Barton 2010), which tie together aspects of tool kit genes and the TFs they encode (previous sections) with phyllotaxis (next section).

    The SAM of angiosperms and certain other seed plants is layered consisting of the tunica (surface layer) and tissues within (corpus). This character has been employed in many seed plant phylogenetic analyses.

    Development of the model malvid Arabidopsis thaliana SAM operates three ways (Bäurle and Laux 2003):

  • local maintenance of stem cells
  • amplification of stem cell daughters
  • initiation of organ primordia
  • The essential gene WUS and the homeodomain TF this gene encodes operates in the organizing center of the eudicot SAM (Mayer et al. 1998, Nardmann and W. Werr 2013). At the periphery of the central zone, partitioned pre-founder cells and founder cells determine how lateral organs grow and the position of reproductive modules.

    Partitioning of cells of the central SAM in model malvids leads to discernable boundary layers: the meristem-organ primordium (M-O) boundary and a region between developing organs known as the O-O boundary (Aida and Tasaka 2006).

    Morphogenesis at the boundary cells between developing organ primordia and the SAM daughter cells is regulated by several classes of genes. Further, plasmodesmata of the boundary cells of the SAM potentially regulate flow (traffic) of small proteins and other TFs (see review by Aida and Tasaka 2006). Physiology of homeodomain TF trafficking is discussed in a later section.

    At every step of the way cells of the developing and expanding SAM exhibit discreet gene expression patterns. Further, early biochemical events in regulation of transcription, and post-transcriptional modification of mRNA, translation, and post-translational protein folding, potentially lead to canalized development of lateral organs of the seed plant shoot (Carraro et al. 2006, Johnson and Lenhard 2011, among others).

    Almost every molecular-phylogenetic study of DNA-binding seed plant TFs suggests deep conservation of the cone and floral tool kit. This fact is congruent with Bayesian molecular-clock simulations computed by Beaulieu et al. (2015) supporting Triassic age estimates for flowering plants.

    Rate Scenario 3 depicted in Figure 4 on page 874 of Beaulieu et al. (2015) is particularly intriguing from the research perspective of evo-devo. For example, there are studies in the paleobotanical and physiological literature on the evo-devo of auxin regulation (Rothwell and Lev-Yadun 2005, Rothwell et al. 2008). Further, PINs of the seed plant SAM are deeply-conserved. This premise, when applied from a paleobotanical research perspective, begs several questions.

    Based on gene expression studies of extant angiosperm species does the foliar morphology, stem anatomy, and growth habit of Sanmiguelia lewisii display the fingerprint of an "ancestral developmental tool kit" (title, Floyd and Bowman 2007) of a monocotyledonous flowering plant? According to Cornet (1986), was Sanmiguelia a flowering plant? Yes.

    What of magnoliid (and/or eudicot) reproductive spur shoot and foliar evo-devo, or co-option of the molecular tool kit to generate opposing morphologies of the vegetative leaf subtending the short shoot?

    Is the reproductive spur-shoot the very same organ as the flower? Yes, if biometric and scaling data published by Christianson and Jernstedt (2009) are taken at face value.

    Shoot apical meristem maintenance and patterning genes and TFs of the land plant developmental tool kit including WUS (Vásquez-Lobo et al. 2007, Nardmann et al. 2009) may affect downstream phyllotactic patterns (Nardmann and W. Werr 2013).

    Did early WGDs early on in the evolution of vascular plants and progymnosperms affect the expression of WUS genes and their TFs resulting in fundamental changes in the way SAMs were organized in diverging seed plant lineages?

    Phyllotaxis. Phyllotactic patterns of extant flowering plants are of ongoing interest to paleobotanists and plant systematics who seek to understand the origin of the angiosperm flower from an evo-devo research perspective (J. A. Doyle and Endress 2000, Endress and J. A. Doyle 2007). Floral phyllotaxis may be distinct from vegetative phyllotaxis.

    Extant basal angiosperms including the Magnoliales exhibit both spiral and whorled floral phyllotactic patterns (J. A. Doyle and Endress 2000, Ronse De Craene et al. 2003, Staedler et al. 2007). When floral phyllotactic characters in basal angiosperms are subjected to phylogenetic analyses, reversals from spiral to whorled and whorled to spiral become apparent (Ronse De Craene et al. 2003, Endress and J. A. Doyle 2007).

    Phyllotaxis is reviewed by Kuhlemeier (2007). An Arabidopsis model suggests that in addition to PIN proteins, the family of AUX1 LAX auxin influx carrier enzymes stabilize spiral phyllotaxis (Bainbridge et al. 2008).

    At least one model of developmental phyllotaxis and initiation of procambial strands leading to vasculature in the SAMs of extant flowering plants implicates auxins, ATPIN1, mRNA transcripts such as ATHB8-GUS, and other auxin related developmental genes (R. S. Smith et al. 2006). Development of phyllotactic geometric patterns and vasculature in SAMs of some modern flowering plant species may be traced to a common genetic and physiologic mechanism (Dengler 2006).

    Lignification of conducting cells may occur in concert with secondary growth. Biosynthesis of lignin, a class of phenylpropane polymers, involves activation of key developmental switches, a cytochrome P450 (CYP)-dependent monooxygenase, CYP hydroxylase, and R2R3 MYB TFs (Zhao et al. 2010). Syringyl subunits of lignin polymers may be angiosperm specific (Zhao et al. 2010).

    Genomic studies of conifers point to deep conservation of the xylem transcriptome (X. Li et al. 2010).

    A review of vascular cambia and secondary growth in lignophytes written from an evo-devo research perspective, is available (Rachel Spicer and A. Groover 2010).

    Were the possibly conserved mechanisms of SAM differentiation that underlie geometric patterning in sporophytes operating the same way in long extinct progymnosperm and seed plant species?

    According to Floyd and Bowman (2007) the answer to the second question is "yes." Orthologues of PIN and ARF, auxin-related genes and TFs needed in land plant architecture and phyllotaxis, were part of the ancestral land plant developmental tool kit according to Floyd and Bowman (2007).

    Floyd and Bowman (2007) identified several "PIN-like" genes from expressed sequence tag (EST) studies of moss gametophytes belonging to Physcomitrella. Five PIN genes were identified in sporophytes of extant Selaginella, and eight additional PIN genes were found in Arabidopsis (Floyd and Bowman 2007).

    "If the hypothesis that increasing complexity of auxin metabolism, transport, and perception was related to the increased sporophytic complexity accompanying land plant evolution, then we might expect these particular gene families to be less complex in the moss and lycophyte lineages than in angiosperms, as indeed appears to be the case."

    The preceding quote is from page 22 of Sandra K. Floyd and John L. Bowman (2007), The ancestral developmental tool kit of land plants, International Journal of Plant Sciences 168(1): 1-35.

    Did auxin exist in Paleozoic vascular plants? Yes, as evidenced by paleobotanical data (Rothwell and Lev-Yadun 2005, Rothwell et al. 2008).

    Macromolecular secretions (microRNAs, bioactive peptides, and other small sized molecules) when applied to the surfaces of SAMs by chewing, crawling, ovipositioning, piercing, and sucking resident, phytophagous insects, could potentially signal the host plant genome and affect phyllotaxis and other developmentally plastic traits but experimental studies are needed to support this hypothesis.

    Leaf development. Evolutionary-development of leaves is a critical body of evidence necessary to decipher paleophysiology and the origin of reproductive organs unique to flowering plants: carpels and stamens.

    Several books and review papers place leaf development of vascular plants including angiosperms in a paleontologic context including Melville (1969), J. A. Doyle (1978), Melville (1983), (J. A. Doyle and Donoghue 1986, 1987), Stewart and Rothwell (1993), Trivett and Pigg (1996), and Sinha (1999).

    Contemporary studies, which are of paramount importance toward a deep understanding of leaf development include Beerling et al. (2001), Roth-Nebelsick et al. (2001), Boyce and Knoll (2002), Boyce (2005), Feild and Arens (2005), Harrison et al. (2005), J. A. Doyle (2006), Beerling and Fleming (2007), Brodribb et al. (2007), Sanders et al. (2007), Boyce et al. (2009), Brodribb and McAdam (2011), Bolduc et al. (2012), Wengler and Bergmann (2012), Rudall et al. (2013), and Vasco et al. (2016).

    The image on the left is the distal end of the largest known specimen of the Paleozoic gigantopteroid seed plant, Delnortea abbottiae, United States National Museum (USNM) specimen number 387473, ×1. The fossil was photographed by the author in 1982, when unearthed from beds of the Lower Permian Cathedral Mountain Formation of the Del Norte Mountains of southwestern North America. It is published as Figure 18 on page 1413 of Mamay et al. (1988).

    Zimmermann's Telomb Theory has figured prominently in discussions by paleontologists and plant morphologists on the origin of megaphylls or true leaves (Stewart and Rothwell 1993, Stein and Boyer 2006, Beerling and Fleming 2007, Sanders et al. 2007, Rothwell et al. 2014). The origin and evolution of the megaphyll is reviewed in a paper by Galtier (2010).

    Research by the Vasco team challenges classical theory on the origin of enations, microphylls, and megaphylls including Zimmermann's Telomb Theory.

    "... there is a common leaf developmental mechanism conserved between ferns and seed plants ..." (abstract, Vasco et al. 2016).

    Yet, "... no single plant lineage has been found to exhibit all three crucial steps [overtopping, planation, webbing] in its fossil history" (page 5, Beerling and Fleming 2007). Remarks in brackets [] are mine.

    Delnortea abbottiae possesses leaves with four orders of veins, and certain cells of the leaf hypodermis are sclerotic (pages 1423 and 1424, Fig. 36 on page 1420, Mamay et al. 1988). According to a review by Boyce and Knoll (page 74, 2002), " ... the gigantopterids bore the most complex and morphologically distinctive leaves of any plants in the Paleozoic ... "

    Regulation of leaf development in the malvid flowering plant Arabidopsis thaliana is explained by a model (Bilsborough et al. 2011). Biochemical studies of extant malvid model organisms detect reverse flows of auxin being drained by leaf midveins. Modeling of auxin gradients in embryonic leaves posits repression of CUC2 TFs by the phytohormone as the basis of leaf-margin sculpting (Bilsborough et al. 2011).

    Leaf-margin scalloping in the Delnortea abbottiae fossil might constitute a "fingerprint of developmental regulation" of foliar organs by auxins and ancient TFs.

    Development of leaves depends on the activity of Class III HD-ZIP genes (Floyd and Bowman 2007), and a KNOX/ARP genetically based, modular switch mechanism (Beerling and Fleming 2007). At least two and probably several land plant evo-devo programs existed in deep time. Several classes of homeotic genes, homeodomain proteins, and other TFs are probably involved.

    Whether the KNOX genetic switch is on or off depends on the activity of ARP protein repressors (see review by Piazza et al. 2005), and may lead to the development of different leaf forms e.g. pinnate, palmate, or compound (Beerling and Fleming 2007).

    There are several reviews of leaf development (Braybrook and Kuhlemeier 2010, Efroni et al. 2010, Galtier 2010, among others).

    Knowledge of long extinct whole plants and paleopopulations often exists only as detached compressed or permineralized foliar organs traditionally described by paleobotanists as morphotype species. An underappreciated paleontologic problem is that detached perianth parts and vegetative leaves having different venation patterns and cell sizes, thus exhibiting heteroblasty, might have belonged to the same mother plant.

    Ongoing research on the anatomy and cell biology of leaf development from meristematic cells of SAMs, nuclei, and genetic tool kits is incrementally reviewed by Sinha (1999), Roth-Nebelsick et al. (2001), Bharathan et al. (2002), Boyce and Knoll (2002), Engström et al. (2004), Fleming (2005), Piazza et al. (2005), Aida and Tasaka (2006), Brodribb et al. (2007), Champagne et al. (2007), and Hasson et al. (2010).

    Abaxial-adaxial leaf organ development in angiosperms begins in the SAM. Adaxial faces of leaf primordia are positioned toward the SAM while the abaxial surface is orientated away from the SAM. The genetic basis of cell polarity in Arabidopsis SAMs is reviewed by Engström et al. (2004) and Carraro et al. (2006), among others.

    Three classes of TFs establish adaxial-abaxial leaf organ identity in Arabidopsis: Class III HD-Zip (PHA, PHAV, REV), KANADI, and YABBY proteins (Floyd et al. 2006, Nole-Wilson and Krizek 2006). Class III HD-Zip TFs operate on the adaxial side of organ bulges in the SAM. Kanadi and Yabby proteins are active in the abaxial domain (Carraro et al. 2006, among others).

    James A. Doyle discusses YABBY gene-expression within the context of ovular tissue layers and funicular attachment points (abaxial or adaxial) to carpels and leaves in Amborella, a basalmost angiosperm (J. A. Doyle 2006).

    Expression of the AINTEGUMENTA gene in certain extant flowering plants determines which cells of the SAM "leave the meristem to form lateral organs" (page 983, Nole-Wilson and Krizek 2006). Further, ANT and AP2 are TFs of focus in phylogenetic analyses of seed plants (Floyd and Bowman 2007) and the origin of angiosperms (S. Kim et al. 2006, among others).

    Sporophylls and their fertile regions may be viewed as kinds of reproductive modules. Based on studies of MIKC-type MADS-box genes (Zahn et al. 2005) and MIKC-type MADS-box B protein heterodimers (Hernández-Hernández et al. 2007), a WGD occurring around the time of the angiosperm-gymnosperm split roughly 300 MYA, was a critical macroevolutionary step in the origin of the first flowers from bisexual cone axes (Melzer et al. 2010).

    Chanderbali et al. (2016) probably modified Laura Zahn's ideas on the timing of the appearance of the first flower in the rock record to accommodate paleobotanical evidence published by Friis et al. (2011).

    Progenesis of reproductive modules. Modular development as it pertains to seed plant reproduction may be viewed at the cellular or organ level. Aggregations of cells (tissue fields and compartments) and whole organs are also potentially modular from an evo-devo research perspective.

    Paleontologic evidence of ovule development in bennettitalean seed plants suggests early innovation in the production of these reproductive modules (Rothwell and Stockey 2002).

    Cellular and anatomic details of sexual reproduction in extinct seed plant groups are sometimes "accessible" contrary to statements in the literature (page 145, Williams 2009) but require tedious preparation of rare permineralizations (e.g. Nishida et al. 2004, Rothwell et al. 2009).

    The image to the right is the permineralized nucellus (the megasporangium wall of a fossilized ovule) of Eoantha zerikhinii, a gnetalean "pre-flower," Baisian Assemblage, early Cretaceous Period, Transbaikal, central Asia. The fossilized ovule contains a female gametophyte with a pollen chamber filled with Ephedrites-type pollen (this picture is from an original image provided by Professor Valentin Krassilov, posted here with his permission), ×100. Plate 21-3 on page 1273 of V. A. Krassilov (2009), Diversity of Mesozoic gnetophytes and the first angiosperms, Paleontological Journal 43(10): 1272-1280, contains another image of this permineralization.

    Several key papers and reviews are devoted to the study of reproductive structures in seed plants as an approach to gain a better understanding of evolution of gymnosperms and the origin of flowering plants (Dilcher 1979, Friedman 1992 [two papers], Crepet and Nixon 1996, Crane and Kenrick 1997, Labandeira 2000, Eckardt 2002, Lord and Russell 2002, Friedman et al. 2004, Friedman and Williams 2004, Williams and Friedman 2004, Friedman et al. 2008, Friedman and Ryerson 2009, Williams 2009, among others).

    Friedman and Ryerson (2009) in a recent review of megagametogenesis in angiospermous seed plants argue that the female gametophyte of flowering plants consists of a modular quartet of cells.

    Curious molecular and developmental similarities of angiosperm reproductive modules with animal germ lines (Dickinson and Grant-Downton 2009) require further study.

    Reproductive modules are specific organs, tissue fields, or cells derived from a SAM or cone axis. Evolutionary-development and genetics of the female reproductive tract is reviewed by B. C. W. Crawford and Yanofsky (2008). The bulleted list below includes some key references:

  • archegonia (haploid tissue receptacles in certain gymnosperms that contain the egg and accessory cells)
  • carpel (an inrolled [conduplicately folded] ovule-bearing leaf) (Scutt et al. 2006, Vialette-Guiraud and Scutt 2009, among others)
  • central cell (female haploid cell of the embryo sac involved in double fertilization) (Bemer et al. 2008, Berger et al. 2008, R. J. Scott et al. 2008, among others)
  • eggs or egg nuclei (female haploid cells or nuclei, respectively) (Berger et al. 2008, R. J. Scott et al. 2008)
  • embryo (an often tiny [usually dormant] diploid daughter plant [complete with a basal cell, suspensor, and growing point] that develops from the fertilized egg, usually housed within a mature ovule or ripened seed) (Tobe et al. 2000, Forbis et al. 2002, Holloway and Friedman 2008, among others)
  • endosperm (diploid, triploid, or polyploid nutritive cells or nuclei usually housed inside of ovules and embryo sacs) (Baroux et al. 2002, Raghavan 2003, Rudall et al. 2009, Cailleau et al. 2010, among others)
  • interseminal scale (modified female organs of bennettitaleans possibly used to house toxins needed as defense against potential herbivores)
  • megasporangia (multicellular sacs that produce megaspore mother cells and megaspores)
  • megaspore mother cells (female diploid cells where meiosis occurs)
  • megaspores (female haploid products of meiosis)
  • megagametophytes (cellular or acellular haploid tissues derived from cell- and/or nuclear divisions in megaspores [termed modular quartets of cells in flowering plants]) (Yadegari and Drews 2004, Tobe et al. 2007, Blanvillain et al. 2008, Friedman et al. 2008, Madrid and Friedman 2008, Friedman and Ryerson 2009, Madrid and Freidman 2009, W.-C. Yang et al. 2010, among others)
  • microgametophytes (Russell 1991, Rudall and Bateman 2007, Blanvillain et al. 2008, Borg et al. 2009, Zobell et al. 2010, among others)
  • microsporangia (diploid multicellular sacs that produce diploid microspore mother cells, haploid microspores, and haploid pollen) (Russell 1991, Furness et al. 2002, among others)
  • microspore mother cells (male diploid meiotic cells) (Russell 1991, Furness et al. 2002, among others)
  • microspores (male haploid products of meiosis) (Russell 1991, Furness et al. 2002, Nadot et al. 2008, among others)
  • ovary (an organ of the mother plant consisting of one or more carpels; contains one to several ovules)
  • ovule (a complex organ of the mother seed plant that contains sterile diploid protective tissues termed integuments [often hardened by lignified cell walls], a vestigial megaspore wall [nucellus], megaspores; and at later stages of development: megagametophytes, other nutritive tissues in some seed plants [endosperm], archegonia [in certain seed plants], and eggs [to include accessory cells and synergids in some seed plants]) (Skinner et al. 2004, Scutt et al. 2006, Colombo et al. 2008, Kelley et al. 2009, Skinner and Gasser 2009, R. H. Brown et al. 2010, Endress 2011, Povilus et al. 2015)
  • polar nuclei (haploid nuclei of the embryo sac) (Berger et al. 2008, among others)
  • pollen grain (an endosporic microgametophyte that consists of a hardened microspore containing haploid male nuclei and/cells [Borg et al. 2009, Lora et al. 2009]; the exine layer of the pollen cell wall contains sporopollenin [Ariizumi and Toriyama 2011, among others])
  • pollen tube (a living tubular cell derived from the male [micro] gametophyte, which is lined with callose in extant flowering plants) (Russell 1991, Williams 2008, Cai and Cresti 2009, Dresselhaus and Márton 2009, Williams 2009, Michard et al. 2011, among others)
  • seed (a ripened ovule that contains an embryo, see a review by Linkies et al. 2010, among others)
  • sperm or sperm nuclei (male haploid cells [sometimes motile] or nuclei, respectively) (Russell 1991, Berger et al. 2008, Russell 2010)
  • stamen (a complex, highly modified male branch or grouping of fused male [micro] sporophylls that contains one or more microsporangia [and pollen when ripe]) (Alves-Ferreira et al. 2007, among others)
  • staminode (a sterile, often leaf-like module derived from the male [micro] sporophyll or stamen) (Walker-Larsen and Harder 2000)
  • stigma (the pollen receptive surface of a carpel)
  • style (an organ located midway between the ovary and stigma through which the pollen tube may penetrate) (J. P. Alvarez et al. 2009, among others)
  • suspensor (an often linear array of diploid cells [often containing endoreduplicated nuclei] of the embryo)
  • synergids (specialized cells of the embryo sac that interact with the pollen tube during double fertilization) (Sandaklie-Nikolova et al. 2007, among others)
  • Yet another important study of seed plant development by Professor William Friedman illuminates the highly derived reproductive anatomy of Welwitschia mirabilis (Welwitschiaceae, Gnetales, Gnetophyta), including growing prothallial tubes, endoreduplicated nuclei, and single fertilization occurring between the functional sperm nucleus of a pollen tube and one prothallium egg cell. The evolutionary history of modular reproductive development in extant Gnetales is reviewed by Friedman (2015) in two papers.

    Sporophylls. Fertile leaves (sporophylls) of heterosporous seed plants are of two kinds: 1) megasporophylls (these are leaves that bear ovules later maturing into seeds, a morphological condition termed phyllospermy) and, 2) microsporophylls (microsporangium-bearing, polleniferous leaves). Were sporophylls of some Permo-triassic seed plants laminar, pigmented foliar organs discernable to insect antagonists?

    Sporophylls in early diverging populations of Paleozoic seed plants were often clustered together on short- (spur-) shoots, which were essentially fertile simple cones, proanthostrobili, and protoflowers. Further, prevailing models of cone and floral organization of sporophylls (Theißen Saedler 2001, Becker and Theißen 2003, Baum and Hileman 2006, Theißen and Melzer 2007, Melzer et al. 2010) posit that the MRCA possessed a hermaphroditic (bisexual) strobilus (Specht and Bartlett 2009, Rudall and Bateman 2010).

    The diagram illustrates a Paleozoic megasporophyll and microsporophyll (actual size), which are artistically "detached" from a hypothetical seed plant mother shrub. Certain Paleozoic seed plants e.g. Vojnovskyales might have possessed many sporophylls that were arranged on bisexual short- (spur-) shoots.

    Generalized seed plant reproductive organs (microsporangia, pollen, ovules, and seeds) are shown not to scale. Note the retuse, petal-like tips of these detached foliar organs: a character which may help paleobotanists piece together whole protoflowers from fossilized fragments in the bedding plane. Retusely-sculptured foliar organs might suggest auxin regulation of ancient CUC2 TFs (Bilsborough et al. 2011).

    The Carboniferous and Permian Periods were times of seed plant innovations and adaptive radiation including a rich fossil history and considerable paleodiversity in detached seed plant reproductive organs and leaves. However the morphology of whole plants such as Paleozoic gigantopteroid seed plants is unknown or poorly understood (T. N. Taylor et al. 2009).

    Did angiosperm carpels evolve from megasporophylls as first suggested by Mamay (1976) in his classic paper on the Paleozoic Origin of Cycads?

    "Gymno-ovuly is the original condition from which angio-ovuly must have evolved. Thus, the search for the origin of flowering plants must have an appreciation for the biological changes that have resulted in the shift of pollination of 'naked' ovules from that of 'enclosed' ovules ... " (page 312, Introduction - The flowering plants, Tomlinson 2012).

    David W. Taylor and Kirchner state that the angiosperm carpel (page 116, 1996) is "... one of the defining characteristics of flowering plants," yet neglect to cite Mamay's defining proposal on carpel evolution published 20 years earlier.

    Reviews by D. W. Taylor and Kirchner (1996), Friedman et al. (2004), J. A. Doyle (2006), Scutt et al. (2006), Endress and J. A. Doyle (2009), Specht and Bartlett (2009), and Vialette-Guiraud and Scutt (2009) outline the great body of literature which has been devoted to evolutionary and experimental cladistic studies of carpel homologies.

    A solitary carpel of the "living fossil" magnoliid tree, Degeneria vitiensis (Degeneriaceae, Magnoliales), is depicted in the left-hand scanning electron micrograph, ×15. The right-hand image is a scanning electron micrograph of a Degeneria microsporophyll, ×5.

    The Degeneria reproductive organs were field-fixed in 1986 and 1987 from dissected flowers collected in the canopies of tagged and vouchered trees growing in stands on the slopes of Mount Naitaradamu on Viti Levu Island, and from forested flanks of Mount Delaikoro, Vanua Levu Island, Fiji.

    Scanning electron micrographs were prepared by Al Soeldner, Director, Oregon State University Electron Microscopy Laboratory. I thank the National Geographic Society for providing research funding for this study.

    David Winship Taylor and Kirchner (page 119, 1996) provide a detailed discussion of the "phyllosporous origin" and "stachyosporous origin" hypotheses of carpel homologies.

    The homology assessment of the angiosperm carpel, perianth, and flower by D. W. Taylor and Kirchner (Figure 6.3 page 124, 1996) would be confounded by the inclusion of a hypothetical Paleozoic gigantopteroid proanthostrobilus or protoflower, which is diagrammed below.

    The diagram below is a reconstructed longitudinal section of the short shoot and floral organ of a hypothetical gigantopteroid seed plant. A 25-centimeter broad bracteopetaloid perianth consisting of retuse Lonesomia mexicana-like taeniopteroid tepals is diagrammed. The hermaphroditic spur shoot attached to a small tree, pachycaulous shrub, or vine-like mother plant might have been subtended by clasping gigantopteroid leaves clothing a long shoot or vegetative branch.

    Spirally-arranged tepals might have been attached to the base of a shortened hermaphroditic cone axis illustrated above, which was not unlike the fertile spur shoot of Ginkgoales. Just inside a spiral of several tepals, a third ring might have consisted of several spirally arranged UV-absorbing and/or colored andropetals enveloping the inner ring of microsporangium-bearing leaves (microsporophylls). The leaf-like microsporophylls might have clasped an innermost ring of Phasmatocycas bridwellii-like ovule-bearing megasporophylls.

    The hypothetical gigantopteroid protoflower, which is illustrated in the preceding diagram, might have been subtended by an Evolsonia-type gigantopteroid megaphyll.

    Did some seed plant populations "start blooming" during the Permian or Carboniferous Period? Possibly.

    While speculating on the paleobiological significance of the fossilized reproductive shoot of Phasmatocycas bridwellii, Axsmith et al. (2003) introduce the term "flush," while discussing an amplified diagnosis of the species.

    My diagram of a hypothetical Paleozoic proanthostrobilus or protoflower takes this idea, which was first proposed by Brian Axsmith, Michael Krings, Serge Mamay, Rudolph Serbet, Edith Taylor, and Tom Taylor, one step further.

    Since publication of the book chapter by D. W. Taylor and Kirchner (1996), research advances on the evo-devo of the angiosperm carpel are incrementally reviewed by Friedman et al. (2004), J. A. Doyle (2006), Endress and J. A. Doyle (2009), and Vialette-Guiraud and Scutt (2009), among others.

    A detached megasporophyll of extant Cycas revoluta (Cycadaceae, Cycadales) is pictured on the left-hand side of the page. The hairy megasporophyll bears a pair of bright red ripened seeds and one brownish immature ovule on the lower edges of the dissected leaf, ×1. Ovules of cycads mature into bright red seeds (see image) that contain diploid embryos (offspring) which are protected by an indurate sarcotesta.

    Each ovule consists of a single diploid integument, pollen chamber, a multicellular megasporangium (cells at the tip of this structure disintegrate into a colloidal pollination droplet), archegonial chamber (this space receives flagellated sperm which are discharged from the pollen-grain end of the pollen tube), and a multicellular, haploid megagametophyte. The female gametophyte serves as nutritive tissue for the embryo.

    The best example of a Paleozoic megasporophyll is probably one of the foliar organs of Phasmatocycas bridwellii (Axsmith et al. 2003), but anatomical details are unknown due to poor preservation of the fossils. Paleobotanists do not know the whole plant morphology or taxonomic relationships of the gymnosperm to which Phasmatocycas leaves were attached.

    To the left is a photograph of a possible immature ectopic ovule attached to a retuse megasporophyll of Lonesomia mexicana (or the leaf was damaged before fossilization, and the object is a "tear").

    Pictured to the right is an example of a laminar microsporophyll found in the same bed, ×1. Elongate rice-shaped structures on the adaxial leaf surface may be pollen-bearing sacs. The fossil I collected is the only known microsporophyll of a gigantopteroid, and is left without a complete diagnosis of the organ and the mother plant.

    The images are 280 million year old permineralizations photographed by the author in 1982 a couple days after the fossils were excavated from the bedding plane of Unit 5 of Section IV of the uppermost Cathedral Mountain Formation, Del Norte Mountains, North America.

    One starting point for an evaluation of the origin, evolution, and homologies of the angiosperm stamen is a paper by Canright (1952). Incremental reviews are available in Cronquist (1968), Takhtajan (1969), Stebbins (1974), Crepet and Nixon (1996), Endress (1996), and Hufford (1996). Research advances on the evo-devo of stamens and staminodes are summarized by Ronse De Craene and Smets (2001).

    Ovules. Certain paleobotanists focus on the origin of bitegmic (having a two-layered integument), anatropous (reflexed) ovules from Caytoniales or other unknown gymnospermous ancestors (page 458, Stewart and Rothwell 1993, J. A. Doyle 2006).

    Ovules of flowering plants are composed of the embryo sac (megagametophyte), a nucellus (old megasporangium wall), and sterile integuments. Integuments are generally regarded as modified leaves. Many but not all angiosperms possess two integuments. It is important therefore, to understand the evo-devo genetics of integuments and details of ovule ontogeny (Skinner et al. 2004, Scutt et al. 2006, Skinner and Gasser 2009) as a prerequisite to understanding certain character homologies (Friedman et al. 2004).

    Ontogeny of ovules and seeds of water lilies are discussed by Povilus et al. (2015).

    Frohlich (2003) offers additional discussion on the origin of ovule integumentation and placement on leaf surfaces from the standpoint of YABBY signaling from SAMs. James A. Doyle discusses YABBY within the context of ovule tissue layers and attachment point (abaxial or adaxial) to carpels and leaves in Amborella, a basalmost angiosperm (J. A. Doyle 2006).

    Kelley et al. (2009) conclude that there are similarities between expression and transcriptional regulation of Class III HD-Zip, KANADI, and YABBY genes of integuments and leaves of the malvid Arabidopsis. Based on biochemical studies of ovule polarity determinants, these workers state:

    "Although these organs [integuments and leaves] have distinct evolutionary origins, a common set of polarity determinants appears to have been serially utilized in both sets of structures. The differences in the precise roles and interactions of the determinants of each structure may represent differences dating from their origin, or alternatively, differences arising from subsequent structural diversifications."

    This quote is from page 1062 of D. K. Kelley, D. J. Skinner, and C. S. Gasser (2009), Roles of polarity determinants in ovule development. The Plant Journal 57(6): 1054-1064.

    The image to the left is the distal portion of another retuse ovulate taeniopteroid "leaf" resembling foliar organs of Lonesomia mexicana (Plate 3, Figs. 1-3 on page 232 of Reinhold Weber 1997).

    The two lumps shown on the left-hand image might be ovules but evidence on the internal anatomy would be required. The fossils were collected from exposures of the lower Permian (Leonardian) Cathedral Mountain Formation, Del Norte Mountains, southwestern North America.

    Seeds. Seeds are ripened ovules that often contain nuclear and cytoplasmic products of fertilization (e.g. zygotes, embryos and nutritive cells, free-nuclei, and/or tissues including endosperm). A review on the evolution of seeds by Linkies et al. (2010) is a potential starting point for discussion.

    The treatise by Linkies and company is especially important to questions of angiosperm origins from paraphyletic lineages of the great Upper Paleozoic gymnosperm divergences since the paper discusses the evolution of seeds from evo-devo and paleoecological research perspectives.

    Megagametophytes. Despite the importance of the megagametophyte in hypotheses of the origin of angiosperms almost nothing is known of the anatomy of female haploid stages in Paleozoic gymnosperms.

    Only recently have paleobotanists begun to understand the anatomy and morphology of female gametophytes of Mesozoic seed plants (Stockey and Rothwell 2003, Rothwell et al. 2009). Preserved megagametophytes of unequivocal stem group flowering plants are unknown.

    The kodachrome on the right is a split compression of a fossilized seed assignable to the morphotype genus Cordaicarpus. Cellular details of the seed contents including the megagametophyte (or a possible embryo) were not preserved in the two-halves of this compressed and split fossil from the southwestern North American Cisuralian.

    Without permineralizations paleobotanists might never know if this fossilized Permian seed possessed a nutritive megagametophyte with archegonia, or endosperm, synergids, and an egg, or a tiny embryo.

    Additional insight has been gained from studies of megagametogenesis in evolutionarily derived extant gymnosperms including Gnetum (Gnetales) (Friedman and Carmichael 1998). Now that molecular systematists converge on the root of phylogeny of extant flowering plants, plant anatomists have turned their research focus to studies on the reproductive anatomy of basal angiosperms including magnoliids.

    Anatomical studies of megagametophytes of basal flowering plants have been conducted by Friedman and Williams (2003), Madrid and Friedman (2008), Friedman and Ryerson (2009), and Madrid and Freidman (2009). The angiosperm female gametophyte consists of a basic modular quartet of cells according to Friedman and Ryerson (2009).

    In 2006 Friedman described an unusual eight-celled and nine-nucleate female gametophyte in the basal flowering plant Amborella trichopoda (Amborellaceae, Laurales, Magnoliidae), a shrubby species indigenous to New Caledonia in the southwest Pacific. While discussing the peculiar four-celled egg apparatus (consisting of three synergids and one egg cell) of Amborella, in comparison with the common seven-celled, eight-nucleate Polygonum-type female gametophyte of angiosperms, Friedman states:

    "Ironically, it is now evident that none of the most ancient lineages of flowering plants produces a seven-celled, eight-nucleate female gametophyte, a stark reminder that much remains to be discovered or correctly circumscribed for the earliest angiosperms."

    The preceding quote is from page 339 of W. E. Friedman (2006), Embryological evidence for developmental lability during early angiosperm evolution, Nature 441: 337-340.

    Historically the seven-celled, eight-nucleate female gametophyte, also known as the Polygonum-type, was regarded as the plesiomorphic state for flowering plants. Tobe et al. (2000) reported this anatomical type in Amborella. However, in 2006 Friedman discovered a peculiar eight-celled, nine-nucleate Amborella-type female gametophyte in this same group of New Caledonian angiosperms.

    Detailed anatomical studies of Austrobaileya (Austrobaileyales) by Tobe et al. (2007), Illicium (Austrobaileyales) by Williams and Friedman (2004), Kadsura (Austrobaileyales) by Friedman et al. (2003), and Nymphaeales (including Nuphar and Hydatellaceae [Hydatella and Trithuria]) (Williams and Friedman 2002, Friedman 2008, Rudall et al. 2008), reveal a four-celled, four-nucleate, Nuphar-type or Schizandra-type female gametophyte.

    According to the review by Friedman and Ryerson (2009) the three types of female gametophyte development in basal clades of extant flowering plants are:

  • Amborella-type (known only from Amborella trichopoda (Amborellaceae)
  • Nuphar/Schizandra-type (common to all Austrobaileyales and Nymphaeales), and
  • Polygonum-type ("ancestral" to magnoliids, Ceratophyllaceae, Chloranthaceae, eudicots, monocots)
  • Further, Friedman and Ryerson propose that a four-celled egg apparatus consisting of an egg cell, two synergids, and a central cell is the most plesiomorphic character state for the angiosperm female gametophyte. Concomitantly, these authors suggest that either a one-module megagametophyte (i.e. in Austrobaileyales and Nymphaeales) or a two-module female gametophyte (i.e. among magnoliids, Ceratophyllaceae, Chloranthaceae, eudicots, monocots) could be the plesiomorphic condition in two different parsimony analyses (Friedman and Ryerson 2009).

    Pollen-containing male gametophytes. Considerable insight on the questions of the origin, evolution, and radiation of angiosperms has been gained from the recovery and study of fossil pollen (J. A. Doyle et al. 1990 [two papers], J. A. Doyle and Hotton 1991, Wing and Boucher 1998, Lupia et al. 1999, Zavada 2007, J. A. Doyle 2005, 2009, Zavialova and Gomankov 2009).

    A photomicrograph of polyplicate gnetalean pollen, which are lodged in the pollen chamber of a permineralized ovule of Eoantha zherikhinii (Gnetales, Gnetophyta), appears on the right side of the page, ×1000. The original image was supplied to the author by the late Professor Valentine Krassilov with permissions, for posting on my web site several years ago.

    Preserved pollen inside fossilized insect guts is a potential source of paleobiological data (Krassilov 1997, Labandeira 2000). Ultrastructural details of fossilized pollen and spores are known from many vascular plants (T. N. Taylor et al. 1996). Further, angiospermous pollen of the perforate-reticulate and/or columellate type is known from Permian, Triassic, and Jurassic rocks (Cornet 1989, Hochuli and Feist-Burkhardt 2004, Zavada 2007, Hochuli and Feist-Burkhardt 2013).

    Evolution and anatomical diversity of seed plant male gametophytes (also termed microgametophytes) is reviewed by Friedman (1993) and T. N. Taylor et al. (2009). A recent review of pollen exine development and genetic regulation of sporopollenin biosynthesis is available (Ariizumi and Toriyama 2011).

    Focused studies of the male gametophytes of seed plants have been underway for several years including investigations of Ginkgo (Ginkgoales) (Friedman 1987 [two papers]), Ephedra (Gnetales) (Friedman 1990), and the malvid Arabidopsis (Friedman 1999). Several MIKC* MADS-Box proteins are very important in development of the male gametophyte in the model malvid Arabidopsis (Zobell et al. 2010).

    Microgametophytes and sperm are often poorly preserved in the fossil record with the notable exception of Permian glossopterids (Nishida et al. 2003, Nishida et al. 2004). More often than not, the only evidence of male gametophytes in the fossil record consists of empty permineralized sporopollenin casings termed palynomorphs (T. N. Taylor et al. 2009).

    The biology and diversity of pollen modules and pollination syndromes as this relates to the origin of angiosperms is discussed by several authors including Hughes (1976), J. Müller (1984), Hotton (1991), Cornet and Habib (1992), T. N. Taylor et al. (1996), Krassilov (1997), Labandeira (2000), Ramanujam (2004), J. A. Doyle (2005), Zavada (2007), Friedman and S. C. H. Barrett (2008), J. A. Doyle (2009), T. N. Taylor et al. (2009), Tekleva and Krassilov (2009), Zavialova and Gomankov (2009), and J. A. Doyle (2005, 2009, 2010).

    A scanning electron micrograph is a close-up snapshot of developing pollen borne in the tapetum of a microsporophyll of Degeneria vitiensis, ×800. Microsporophylls were hand-collected from a flowering tree in the Naitaradamu stand on the island of Viti Levu, Fiji (J. M. Miller 1989). Al Soeldner of the Oregon State University Electron Microscope Laboratory prepared and imaged the sample. Field work on Degeneriaceae of the Fiji Islands was sponsored by a grant from the National Geographic Society.

    Evolutionary-development of the seed plant progamic phase. The progamic phase of seed plant reproduction is defined as, "the life history period between pollination and fertilization" (page 144, Williams 2009). The flowering plant diplophase and male and female haplophases coordinate development of pollen tubes through maternal tissues to ovules at the same time that female gametophytes develop from a megaspore mother cell. Biochemical interactions between cells of sporophytic and gametophytic reproductive modules that underlie orchestration of the progamic phase, vary widely among the angiosperms (Williams 2009).

    Solitary carpels of the "primitive" magnoliid tree, Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae), are shown on either side of the text. The left image is a scanning electron micrograph of a portion of the stigmatic secretion of a carpel. A tiny, thread-like pollen tube emanates from a single boat-shaped monosulcate pollen grain, which is just visible on the left-hand surface of the secretory plug. The pollen grain adheres to the secretory surface, ×30.

    Pollen tubes probably penetrate the flared stigmatic secretion and would eventually be guided to the egg of a modular female gametophyte inside one of several ovules within the carpel.

    The right hand image is a cutaway view revealing a row of ovules with cellular detail of the carpel, a thin placenta, and the stigmatic secretion, ×15.

    Both samples were field fixed in 1986 and later dissected from a flower collected in the canopy of a tagged and vouchered Degeneria tree, Naitaradamu Study Area, Viti Levu, Fiji. The scanning electron micrographs were prepared by Al Soeldner, Director, Oregon State University Electron Microscopy Laboratory. I thank the National Geographic Society for providing research funding for this study.

    Extant crown group flowering plants including basal angiosperms exhibit remarkable diversity in pollen tube development (Williams 2008). Yet, little is known of microgametophyte development and the progamic phase in long extinct individuals and populations of the stem group.

    Reviews of the angiosperm progamic phase, evo-devo of pollen tubes and pollen tube transmitting tissues, and the biology of pollination of the basal crown groups of flowering plants are published by Sage et al. (2009), Thien et al. (2009), Williams (2009), and Michard et al. (2011).

    A study by Michard et al. (abstract, 2011) reveals "a novel plant signaling mechanism between male gametophyte and pistil tissue similar to amino acid mediated communication commonly observed in animal nervous systems."

    Fertilization and embryology of seed plants. Scott Russell (1991), Friedman (1992, 1994), Dumas and Rogowsky (2008), and Russell (2010) outline and discuss the large body of scientific literature on the reproductive biology of seed plants including fertilization in flowering plants, development of nutritive tissue (megagametophytes discussed above), endosperm, and embryogenesis. Questions of reproductive success of flowering plants are discussed in several later reviews (Friedman 1995, 1999, 2001 [two papers], Rudall et al. 2009).

    Double fertilization is one hallmark of angiospermy (Cronquist 1968, Takhtajan 1969, Stebbins 1974). Yet, later studies reveal that certain extant gymnosperms also possess this syndrome.

    " ... this pattern of gnetalean double fertilization might well be homologous with the process of double fertilization in angiosperms (Friedman and Floyd 2001). However, a seismic shift in favored phylogenetic hypotheses for seed plants associated with the transition from morphological cladistic analyses to DNA sequence-based analyses indicated (and continues to indicate-see above) that Gnetales are not closely related to angiosperms, even if their true phylogenetic affinities remain opaque ... " (page 321, Discussion, Fertilization in Welwitschia, Ephedra, and Gnetum, Friedman 2015).

    Specific studies of double fertilization in gymnosperms belonging to the anthophyte clade sensu J. A. Doyle and Donoghue (1986, 1987) have been carried out by Carmichael and Friedman (1995, 1996) and Friedman and Carmichael (1996) on Gnetum gnemon (Gnetales).

    Many studies of double fertilization, endosperm formation, and embryology appear in the extensive literature on extant basal angiosperms (Rudall et al. 2009) including magnoliids. These include papers on endosperm development (Floyd and Friedman 2000, Rudall et al. 2009) and embryogenesis (Arias and Williams 2008).

    "Endosperm is a key feature of angiosperms, yet its homologies and evolutionary origin remain enigmatic."

    The preceding quote is from page 1592 of P. J. Rudall, T. Eldridge, J. Tratt, M. M. Ramsey, R. E. Tuckett, Selena Y. Smith, M. E. Collinson, M. V. Remizowa, and D. D. Sokoloff (2009), Seed fertilization, development, and germination in Hydatellaceae (Nymphaeales): implications for endosperm evolution in early angiosperms American Journal of Botany 96(9): 1581-1593.

    Historically the seven-celled, eight-nucleate female gametophyte, also known as the Polygonum-type, was regarded as the plesiomorphic state for flowering plants. Tobe et al. (2000) reported this anatomical type in Amborella. In 2006 Friedman discovered a peculiar eight-celled, nine-nucleate Amborella-type female gametophyte in this same group of New Caledonian angiosperms.

    An important goal toward a better understanding of coevolution with insect antagonists and the early angiosperm reproduction might be to elucidate anatomical and evo-devo interactions between insects and megasporophylls, pollen and megasporophylls, pollen and female pollen receptive surfaces, pollen tubes and ovaries (when present), pollen and carpels (including secretions), and pollen tubes and ovules.

    Reviews by Lord and Russell (2002), Bernhardt et al. (2003), Bernasconi et al. (2004), Nasrallah (2005), Friedman et al. (2008), Cai and Cresti (2009), Sage et al. (2009), Thien et al. (2009), Williams (2009), and Russell (2010), form a basis for opening new lines of research and later discussion from other perspectives.

    Did biomechanical and secretory activities of animal antagonists affect evo-devo of megasporophylls and carpels, and microsporophylls and stamens, through reciprocal selection or saltation, gradual phenotypic changes or birth of "hopeful monsters," and establishment of novel traits in paleopopulations?

    Cross-kingdom signaling and transduction. Thigmomorphogenesis involves mechanostimulation, mechanoperception, signal transduction, and cellular differentiation (Jaffe 1973). Mechanostimulation may be passive (caused by wind currents, flowing and freezing water, and scraping effects of soil particles and moving rocks) or active, triggered by touching animals, fungi, and neighboring plants (Braam 2005).

    Several reviews of thigmorphogenesis (Jaffe et al. 2002, Braam 2005, D. Lee et al. 2005, Fluch et al. 2008, Chehab et al. 2009) open a door to potentially new ways of thinking about evo-devo and ecology. Surveys of the mechanical forces that shape plant organs are also available (Mirabet et al. 2011).

    Mechanostimulation of the plant cell surfaces is perceived by the plant cytoskeleton (mechanoperception). Transduction of thigmo- (touch) stimuli by plant cells and tissues may signal certain touch-inducible (TCH) genes (Braam and Davis 1990, Lee et al. 2005), and potentially trigger developmental switches and differentiation, and change the shape and function of developmentally plastic organs (morphogenesis).

    Volatile organic compounds (VOCs) are often released by plants when mechanically stimulated by chewing, crawling, egg-laying, and sucking herbivores (Hare 2011, among many other papers).

    The diagram below illustrates how an instar of a Permo-triassic insect might convey biochemical and mechanical signals to nuclei of dividing cells of the host plant SAM. Mechanostimulation of cell walls, plasmalemmas, protoplasts, and the cytoskeleton of the plant SAM by the insect antagonist may involve a signal transduction cascade that potentially leads to de-repression of DELLA chromosomal proteins and switching on or off of meristem identity genes, differentiation, and thigmomorphogenesis.



    Strobilus formation in club mosses (Selaginella) a modern evolutionary derivative of certain Paleozoic lycopods, is a thigmo response (Jaffe et al. 2002, Braam 2005, Read and Stokes 2006).

    Based on morphological and evo-devo studies of extant club mosses, were indeterminate membrane receptors, microtubule enzymes, and TCH genes and TFs tied-in with the developmental tool kit of early land plants?

    An almost completely unexplored and potentially important phenomenon is whether insect bristles are capable of mechanically stimulating plant cell surfaces and the cytoskeleton, and inducing thigmorphogenesis in host plant organs. Arthropod bristles are innervated while hairs are not. Both types of insect organs are under developmental control and require the activity of the AS-C complex and svb/ovo gene, at least in Drosophila (S. B. Carroll et al. 2005).

    Could the potential mechanostimulatory effects of insect bristles on seed plant cell surfaces of SAMs and floral meristems affect homeodomain TF trafficking, leading to differentiation and morphogenesis?

    The engineering approach is used to study chewing in grasshoppers and locusts (acridids) and caterpillars of butterflies and moths (lepidopterans) (Clissold 2008), and to ascertain the magnitude of mechanical force potentially applied by ants (Paul and Gronenberg 1999), and other insects to artificial surfaces (Zhendong et al. 2002, Barbakadze et al. 2006). With the exception of in vivo x-ray analytical techniques there are few experimental studies in the literature to date that explore biomechanics of insect body parts and application of physical force to plant cell surfaces in a behavioral context (Clissold 2008).

    At the cellular level, mechanostimulation of plant cells and protoplasts in the laboratory affects movements of their nuclei (Qu and M.-X. Sun 2007). Mechanostimulation of Arabidopsis plants by air currents or touch may also alter gene expression by upregulating TCH genes (Braam and Davis 1990).

    Dennis Lee et al. (2005) found that 589 genes are upregulated in Arabidopsis thaliana by touch including those of the cytochrome P450 family, genes encoding calmodulin-related proteins, AP2, and WRKY TFs. The AP2 gene encodes one of the class A cis-acting TFs in the ancestral developmental tool kit of land plants (Floyd and Bowman 2007).

    Transduction of signals that originate from abiotic and biotic sources in environments external to the stationary plant body potentially involves cell walls, the plasmalemma, Hechtian strands, microtubules, calcium-binding proteins, and expression of genes of the CAM/CML and XTH gene families (Lee et al. 2005, Braam 2005). Microtubules in plant cells convey signals from the cell wall, plasmalemma, and cytoplasm to other parts of the cell, including the nuclear envelope and endoplasmic reticulum (Wasteneys 2004).

    Did extinct plants have the anatomical machinery to convey mechanostimulatory and hormonal signals from insect bodies rubbing against cell walls, to adjoining membranes, microtubules, and the nucleus? Yes.

    Intact protoplasm containing fossilized plastids and secondary plant substances has been identified in the cells of Paleogene "green-leaf" fossils of "dicotyledonous" flowering plants (Giannasi and Niklas 1981, Niklas and Brown 1981, Niklas 1982). Calcium carbonate permineralizations of pteridophyte (Tubicaulis fern) sieve elements yield fine cell wall structure (Smoot and Taylor 1984).

    Is there anatomical evidence preserved in the fossil record that cells have responded to touch? Possibly.

    When fossilized leaves containing chew marks and punctures are permineralized, the preserved plant remains exhibit thicker cells surrounding the damaged tissues (Labandeira 1998).

    Wind currents and moving parts of large herbivorous animals potentially had thigmomorphogenic effects on development of pollen dispersing reproductive modules (microsporophylls, microsporangia, synangia, stamens) and ovular points of attachment (abaxial or adaxial) on large, seed-bearing leaves, but paleontologic evidence in support of this idea is lacking.

    Exposure to wind currents results in endogenous biosynthesis of ethylene and signaling of primary and secondary meristems in some seed plant species, leading to differentiation, morphogenesis, and wood formation (Rowe and Speck 2005).

    Certain geometries of ovule-bearing shoots in extant gnetophytes (among other plant groups) affect the aerodynamics of pollen, possibly resulting in differential reproductive success (Niklas et al. 1986).

    Thigmomorphogenesis in plants is an incompletely understood, non-Lamarckian, developmental process. Some progress has been made in understanding the effects of touch stimuli on plant differentiation and the derivation of plant growth forms (Pruyn et al. 2000, Pigliucci 2002, Lee et al. 2005, Rowe and Speck 2005, Telewski 2006, Fluch et al. 2008).


    Paleoecology of Global Catastrophe:

    There is little doubt that Bayesian computational molecular-clock simulations by Beaulieu et al. (2015) predict angiosperm occurrences in Anisian times and places, which are supported by Hochuli and Feist-Burkhardt palynological data (2004, 2013), and a calibrated phylogenomic timescale (C. S. P. Foster et al. 2017).

    Were insect and shrub coevolutionary compartments of the late Paleozoic hypoxic icehouse and later hot house, venues of the first angiosperms? Possibly.

    "The 'key innovation' of metamorphosis, present in holometabolan larvae and some Paraneoptera, may have fostered the longevity of these taxa during the Pennsylvanian climatic oscillations and the Permian-Triassic extinction event" (Letter, André Nel et al. 2013).

    An imaginary apocalyptic but artistic reconstruction of an early Triassic landscape a few thousand years following the end-Permian global hiatus is shown to the right. The Hercynian Mountains are in the distance and the dark regions to the left are decayed remains of coastal gigantopteroid mangrove at the edge of the Panthalassa Sea. Lighter areas on land represent acidified ground probably unsuitable to mycorrhizal fungi and some vascular plants.

    As the Late Palaeozoic Ice Age (LPIA) drew to a close with the demise of Central Pangaean Mountain glaciers, and aridity spread from west to east across early Pangaea, possible new habitats opened opportunities and venues for natural interspecific hybridization in sympatric seed plant populations. Colorful reproductive short- [spur-] shoots of certain species of these seed plants ("coevolutionary compartments") might have attracted pollen-eating and predatory insects with paleobiological consequences.

    "Analysis of a wider set of proxies confirms that semi-arid and then arid conditions gradually expanded from west to east across equatorial Pangaea during the latter half of the LPIA" [Late Palaeozoic Ice Age, 305 to 270 MYA] (page 111, 2. The LPIA, 2.2 Glaciation and tropical precipitation during the LPIA: geological evidence and modeling, Heavens et al. 2015).

    A Paleozoic origin of stem group flowering plants is possible from zones of sympatry in widespread seed plant populations indigenous to coastal and extrabasinal, upland habitats at the western edge of the Hercynian Mountains, which is well-separated from the site of Siberian Trap volcanism. This premise eliminates any of the late Mesozoic southwest Pacific Ocean archipelagos, island arcs, spreading centers, or now submerged continental cratons proposed by Buerki et al. (2014), as "The Cradle of the Flowering Plants" (page 137, Chapter 12, Takhtajan 1969).

    "To begin to connect ecology to the early radiation of angiosperms, we must understand the ecological starting point for angiosperm evolution."

    The preceding statement is quoted from page 385 of T. S. Feild and N. C. Arens (2005), Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossils, New Phytologist 166: 383-408.

    Mass extinctions. Among the planet's untold episodes of climatic and ecologic catastrophe (including fire, flood, glaciation, drought, global warming, and volcanism) several events stand-out as "extinction-level" global cataclysms (Wignall 2015, Van De Schootbrugge and Wignall 2016).

    When supported by fossil calibrated phylogenetic tests of possible heterochrony in floral evo-devo of the unstudied chronocline linking Vojnovskya with Sanmiguelia, would the assertion quoted below be correct?

    "... major innovations in floral evolution do not coincide with the recovery stages following mass extinctions ..."

    The passage above is quoted from page 124 of J. C. McElwain, K. J. Willis, and K. J. Niklas (2011), 5. Long-term fluctuations in atmospheric CO2 concentration influence plant speciation rates. Pp. 122-140 In: T. R. Hodkinson, M. B. Jones, S. Waldren, and J. A. N. Parnell (eds.), Climate Change, Ecology and Systematics. Cambridge: Cambridge University Press, 524 pp.

    The six most severe planetary apocalypses were the Frasnian-famennian boundary extinction extending from the Upper Devonian Period to the Tornaisian Age of the Carboniferous Period, the carbon cycle anomaly marking the end of the Guadalupian Epoch, the end-Permian extinction also known as the "Great-Dying", the Triassic-jurassic boundary carbon cycle event, the early Cretaceous end-Barremian biogeochemical perturbation, and the Cretaceous-Paleogene asteroid impact.

    "Many paleontologists persist in using the number of species (or higher taxa) present as a metric of recovery. But the response to a mass extinction is above all an ecological one, and the number of taxa is only an indirect measure of evolutionary activity. Understanding these events requires an ecological approach. What are the dynamics and interactions between species? How well were ecosystems functioning? How complex were food webs and other ecological services during the survival and recovery intervals? Perhaps most importantly, how does the structure of the ecosystem facilitate the speciation involved in biotic recovery?"

    The preceding quotation is from page 241 of D. H. Erwin (2006), Extinction: How Life on Earth Nearly Ended 250 Million Years Ago, Princeton, Princeton University Press, 306 pp.

    Paleoclimatology is the subject of active research (Berner 1999, Berner and Kothavala 2001, Beerling and Berner 2002, Huey and Ward 2005, McElwain et al. 2005, Ward et al. 2006, Lamarque et al. 2006, A. C. Scott and Glasspool 2006, Knoll et al. 2007, McElwain and Punyasena 2007, Cleveland et al. 2008, Retallack 2009, Wignall et al. 2009, Payne et al. 2010, S. V. Sobolev et al. 2011, McElwain et al. 2011, L. G. Stevens et al. 2011, Franks et al. 2014, McElwain et al. 2016).

    Refinements in the global oxygen level curve from reanalysis taking into account the effects of weathering of sulfur-containing iron pyrites on atmospheric free oxygen "... may have an important, relatively unrecognized relation to animal evolution." (page 5663, Berner 2006).

    Long-term climate forcing [increased precipitation and sedimentation] caused by optical effects of [pO2] was reported by Poulsen et al. (2015).

    The global carbon and nitrogen cycles including anthropogenic effects on atmospheric carbon dioxide (pCO2) and methane (ppCH4) are the subject of ongoing research. Paleoatmospheric carbon dioxide is another line of research that ties-in with discussion of mass extinctions and the carbon cycle (Berner 2006, Franks et al. 2014, McElwain et al. 2016, among others).

    A review of paleobotanical data by McElwain and Punyasena (2007) reveals that the Earth's last three major mass extinction episodes since the Paleozoic did little to affect survivability of vascular plant families and orders. Retallack (2009) reports that refined stomatal indices seen in fossil leaves referable to the Ginkgoales are proxies "for past CO2 spikes."

    Paleoatmospheric oxygen content has profoundly affected the incidence of wildfire with possible consequences to late Paleozoic divergences of angiosperm, conifer, cycad, ginkgophyte, and gnetophyte lineages. Papers published by Belcher et al. (2010) and Glasspool and Scott (2010) are gateways to the literature on paleowildfire.

    Based on studies of charcoal in sediments Glasspool and Scott (abstract, 2010) conclude "that variation in pO2 was not the main driver of the loss of faunal diversity during the Permo-triassic and Triassic-jurassic mass extinction events."

    Frasnian-famennian boundary extinction (DeCARB). One of the greatest mass extinctions on Earth occurred at the boundary of the Frasnian and Famennian Age during the Devonian Period, 375 MYA (McGhee 1996, Ward et al. 2006, Bishop et al. 2009). During the late Devonian Period island fragments and a chunk of Gondwana were clustered south of the equator and in the south polar region.

    A developing ice house that began 375 MYA and extended to at least the Tornaisian Age of the Lower Carboniferous 345 MYA, apparently was accompanied by low pO2 (hypoxic) conditions with oxygen levels at 13% (Berner 1999, Berner and Kothavala 2001, Huey and Ward 2005) during the time interval known as Romer's Gap (Ward et al. 2006). The warm interval preceding the DeCARB was the first phase of the expansion of invertebrate arthropod herbivores in terrestrial environments (Labandeira 2006).

    Montañez and Poulsen (2013) review the demise of the Upper Devonian and Lower Carboniferous icehouse while setting a stage for interacting arthropods and seed plants with the advent of the Permo-triassic hothouse.

    According to Ward et al. (page 16820, 2006) "no new clades" of arthropods occurred during the low oxygen interval demarcating Romer's Gap. Adaptive radiation of arthropods, land plants, and early limbed vertebrates (stegocephalians) occurred on land during the millions of years following Romer's Gap (Ward et al. 2006). As the late Paleozoic ice-house Earth slowly warmed during the Carboniferous Period, global oxygen concentration increased to levels exceeding 31% (Berner and Kothavala 2001, Ward et al. 2006), coinciding with the second phase of arthropod herbivore expansion (Labandeira 2006).

    "While mass extinction and recovery, accommodation to new habitats, and body-plan modernization have all been factors in the evolution of life, atmospheric O2 level also has been a major, if underappreciated, driver in the major features of life's history. These features include origination, diversity levels, and probably absolute size increases through time."

    The preceding quotation is from page 16821 of P. Ward, C. Labandeira, M. Laurin, and R. A. Berner (2006), Confirmation of Romer's Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization. Proceedings of the National Academy of Sciences 103(45): 16818-16822.

    While certainly not applicable to events following Romer's Gap, I suggest that evolutionary biologists should consider decreases in insect body size and cone- (or floral-) axis length as likely adaptations emerging in coevolving species pairs resulting from the selective forces of the two Paleozoic mass extinctions and later Triassic-Jurassic carbon cycle event.

    The Permian Period, despite evidence of episodic glaciation, saw a continuation of climatic warming, which was punctuated by at least two global mass extinctions (see next section). Evidence from the study of fossil soils (paleosols) supports stratigraphic division of the Permian Period into three epochs: Cisuralian (299-270 MYA), Guadalupian (270-260 MYA), and Lopingian (260-251 MYA) (Retallack 2005).

    End-Guadalupian carbon cycle event (GuCCE). Retallack et al. (2006) present evidence of a global carbon isotope anomaly coinciding with the close of the Guadalupian Epoch of the late Permian Period. Oxygen levels in Earth's atmosphere declined significantly in the final days of the Guadalupian triggered by ignition of coal seams with hot igneous intrusions and extruding lava (Lai et al. 2008), and by expulsion of carbon monoxide and carbon dioxide into the atmosphere (Retallack et al. 2006, Retallack and Jahren 2008).

    Stratigraphic evidence from Laibin and the Emeishan carbonates and volcanics of Asia coupled with magnetostratigraphic findings supporting the Illawara Reversal (Wignall et al. 2009 [two papers], Isozaki 2009), implicate a trigger for the GuCCE. Methane clathrates stored in cold undersea sedimentary layers were disrupted by volcanic activity releasing gigatons of ozone-damaging CH4 into the atmosphere (Knoll et al. 2007).

    Earth slowly became a hot house with far-reaching ecological effects on late Permian terrestrial ecosystems, as determined from study of the geochemistry of fossil soils and coals and biostratigraphy of plant and vertebrate fossils (Retallack et al. 2006). Additional details on paleoclimatic effects on late Permian floras are covered in a reviews by Looy et al. (1999), Looy et al. (2001), McElwain and Punyasena (2007) and L. G. Stevens et al. (2011).

    Prolongation of the biotic crisis is suggested by a gradual decrease in marine invertebrate biodiversity from the Wordian to end of the Changhsingian, about 253 MYA (Clapham et al. 2009).

    Pictured below is a chart that illustrates the rise and fall of oxygen levels (expressed here as percent; in the scientific literature as atmospheric partial pressure [pO2]) in Earth's atmosphere, timing of the DeCARB, and later great mass extinctions (see below).

    The graph below is based on several data sets (Berner 1999, Huey and Ward 2005, Ward et al. 2006) including GEOCARB III (Berner and Kothavala 2001) and GEOCARBSULF (Berner 2006 [two papers]). The graphic does not show the geologic interval of the Neoproterozoic snowball Earth, or periods of less severe global temperature swings (ice-house to hot house and vice-versa, except the DeCARB), and the Oligocene-Eocene cooling interval of the Paleogene Period.

    At the Permian-Triassic (PTr) boundary, global oxygen levels on the shores of the Panthalassa Sea further declined to a level of free atmospheric oxygen less than 12% (Ward et al. 2006). Carbon dioxide levels in the atmosphere were elevated with profound effects on the physiology of aquatic and terrestrial animals (Knoll et al. 2007).

    When taking into account supposed adaptations of terrestrial animals to pre-Guadalupian high oxygen levels of 31%, and effects of altitudinal compression, animals might have experienced hypoxia comparable to the higher Himalaya or the summits of Kilimanjaro and Mount McKinley (Huey and Ward 2005). Low pO2 at sea level, and in the Hercynian Mountains was probably exacerbated by carbon dioxide and sulfur dioxide outgassing linked to catastrophic volcanism that led to hotter climates within 600,000 years of the global apocalypse marking the close of the Paleozoic Era (Retallack et al. 2006).

    End-Permian extinction (EPE). Global catastrophe caused extinction of most life at the close of the Permian Period, 251.3 MYA (Erwin 2006, Knoll et al. 2007). The Great Dying at the PTr boundary coincides with a 2,000,000 million year interval of volcanic unrest causing heating of Tunguska Basin sediments (Svensen et al. 2009), and extrusion of epicontinental lava lakes known as the Siberian Traps dated precisely 250.3 MYA (Reichow et al. 2009).

    Geochemical studies of at least one subvolcanic intrusive rock formation associated with the Siberian Traps reveal high levels of sulfur contamination of the magma which potentially exacerbated the effects of SO2 outgassing on the atmosphere (C. Li et al. 2009). Mantle plume thermomechanical models proposed by S. V. Sobolev et al. (abstract, 2011) postulate that "massive degassing of CO2 and HCl, mostly from the recycled crust in the plume head, could along trigger a mass extinction."

    Several other hypotheses have been proposed that might explain the greatest of all of Earth's mass extinctions. These include collision of the Earth with a bolide, comet, or icy dwarf; episodic release of thousands of gigatons of methane gas from methane clathrate deposits in the undersea bed (de Wit et al. 2002), methane gas derived from burning coal measures ignited by volcanic activity (Retallack and Jahren 2008), disruption of the Earth's magnetosphere by galactic dust and gas clouds, or catastrophic atmospheric disturbances attributable to solar flaring (Benton and Twitchett 2003).

    No single event listed in the preceding paragraph explains the oceanic δ13 data gleaned from paleogeochemical and isotopic studies of carbonates in sediments bracketing the Permian-Triassic (PTr) boundary (Berner 2002, Payne et al. 2010, Luo et al. 2011). Lipid biomarkers suggest a prolonged period of ecological disruption in marine environments preceding and following the main global kill event (Cao et al. 2009).

    Important insight on the effects of the EPE "trigger and kill" mechanisms (page 296, Knoll et al. 2007) on early Triassic aquatic and terrestrial ecosystems, has been gained from detailed biostratigraphic, paleoclimatic, and paleophysiologic studies (Z.-Q. Wang and Zhang 1998, Looy et al. 1999, Z.-Q. Wang 2000, Rees 2002, Rees et al. 2002, Berner 2005, Gastaldo et al. 2005, Erwin 2007, Sahney and Benton 2008).

    Kozur and Weems (abstract, 2011) suggest that the EPE and associated Siberian Traps volcanism "... coincide with a rapid collapse of tropical rain forest environments (disappearance of the highly diverse Gigantopteris flora) ..." "...caused by global cooling due to a volcanic winter event ..."

    The Triassic hot house and prolonged bouts of disruption to the biosphere from volcanic gases and volatile hydrocarbons ostensibly affecting terrestrial vegetation, including reproduction in coniferous plant populations, is discussed on pages 335-337 of Van De Schootbrugge and Wignall (2. The atmosphere, 2.a. Atmospheric Pollution, page 338, 2016).

    "... increased UV radiation from decreased ozone shielding [exacerbated by volcanic outgassing and induced volatiles] may have triggered malformations in plant reproductive systems ..." (page 346, 5. Converging scenarios: similarities and differences, Van De Schootbrugge and Wignall 2016 [phrase in brackets is mine]).

    Paleogeochemical data show a rise in the proportion of rate of burial of sulphur and iron containing pyrite over organic carbon burial rate at the PTr boundary, 251.3 MYA, which was probably attributable to forest decline at that time (Fig. 4, page 3214, Berner 2005). Some estimates based on geochemical data suggest a catastrophic drop in atmospheric oxygen over a 20 million year period following the end-Permian apocalypse (Berner 2006, Bond and Wignall 2010).

    The EPE was marked by increased levels of erosion and sedimentation rate, lower pH levels in rain, and higher precipitation which was probably a result of habitat destruction on land according to studies by Algeo and Twitchett (2010) and S. G. Thomas et al. (2011). Biostratigraphic studies of Late Permian and earliest Triassic (Scythian Age) rocks in East Greenland by Looy et al. (2001) suggest spatial and temporal variability in ecosystem recovery.

    Proportional changes in the relative amounts of oxygen (pO2), carbon dioxide (pCO2), methane (pCH4), and sulfur dioxide (pSO2) at the ground surface, when accompanied by temperature swings, might have affected low-elevation terrestrial biomes with far-reaching global paleoclimatologic and paleoecologic consequences (Looy et al. 1999, Huey and Ward 2005, Retallack et al. 2006).

    Paleontologic evidence from climatic and geophysical phenomena listed above includes data gleaned from studies of fossil soils (paleosols) of Antarctica, southwestern North America, and southern Africa (Retallack 2005, Retallack et al. 2005, Pace et al. 2009), taphonomical investigations of fossorial therapsids and paleosols preserved in Permian rocks (Retallack et al. 2003), and from reports of marine foraminifers in packstone and framestone carbonate facies (Song et al. 2009).

    Conditions on land following the EPE were probably inhospitable to insects, tetrapods, and plants (Z.-Q. Wang 2000, Retallack et al. 2006), but more data are needed. Reinterpretation of channel fill deposits in the Bethulie region of the Karoo Basin of South Africa suggest that the EPE was a non-event (Gastaldo et al. 2009).

    "... new multidisciplinary data from the Karoo Basin call into question our current understanding of the terrestrial response to the end-Permian mass extinction. Paleoecological evidence does not support the reported coincidence of climate aridification, floral collapse, and tetrapod turnover ..." (Discussion and Conclusions on page 941, R. A. Gastaldo, S. L. Kamo, J. Neveling, J. W. Geissman, M. Bamford, and C. V. Looy 2015)

    Recovery of biota on land probably took a very long time relative to other global extinctions according to the review by Grauvogel-Stamm and Ash (2005). Recovery and later radiation of arthropod clades following the EPE is even more nebulous due to a general lack of meaningful paleontologic data (Béthoux et al. 2005).

    Discoveries of insect galls on Lower Triassic fossilized leaves of corystosperms "... indicate that herbivory and reproductive strategies involving galling and foliar ovipositioning were re-established relatively soon after the end-Permian mass extinction event that saw major turnovers in both the [Gondwanan] flora and insect fauna." (McLoughlin, abstract 2011). The word in [] is mine.

    An exposure of the Triassic Chinle Formation of southwestern North America is pictured to the left. Scott Williams, Petrified Forest National Park Curator and Photographer, captured colorful digital images of massive permineralized logs, which have been described as the morphospecies Araucarioxylon arizonicum, seed plant incertae cedis. Logs were weathered from Norian sedimentary beds deposited 220- to 225- million years ago (MYA).

    Palynological data from oil and gas exploratory drill holes off the northern coast of Europe suggest multiple climatic shifts at the Permo-Triassic boundary (Hochuli et al. 2010). Blooms of cyanobacteria are associated with massive volcanism in Asia at the PTr boundary (Xie et al. 2010).

    Zi-Qiang Wang and co-workers in a series of papers report that Cathaysian floras were reduced to isolated, fungal-enriched refugia dotted within arid, desolate landscapes by late Permian time. Some of the Upper Permian sedimentary red beds studied contained only charcoal fragments of vascular plants while some stratigraphic sequences up to 70 meters thick were devoid of plant fossils (Z.-Q. Wang 2000).

    The most recent review on paleoherbivory and recovery of Permian landscapes following global biotic crises is published by Labandeira and Currano (2013).

    A later paper by Peng and Shi (2009), which is based on detailed biostratigraphic data from continuous sections across the PTr boundary, suggests uneven recovery of the Cathaysian Gigantopteris flora following the EPE. These findings are complicated by results of yet another study of Wuchiapingian paleofloras extending across the PTr boundary by Xiong and Q. Wang (2011).

    When seed plant compressions of gigantopterids were found the fossilized leaves had thick cuticles suggestive of drought conditions in Cathaysia. Based on biostratigraphic and taphonomic data cycads, peltasperms, ferns, ginkgos, and certain other conifers were represented in the fossil record on both sides of Permo-Triassic boundary (Z.-Q. Wang 2000).

    In conclusion, the GuCCE, EPE, and Triassic-Jurassic boundary carbon cycle event (TrCCE) had a common thread: significant fluctuation in global carbon dioxide and oxygen levels (Berner and Kothavala 2001, Huey and Ward 2005, Berner 2006, Ward et al. 2006).

    Triassic-Jurassic boundary carbon cycle event (TrCCE). Emplacement and extrusion of magma and tectonic rifting associated with the Central Atlantic Magmatic Province (CAMP) volcanism are hallmarks of the TrCCE, which occurred about 200 MYA (Pálfy 2003). The end-Triassic mass extinction was preceded by a global increase in temperature followed by severe climatic disruption over many millions of years (Cleveland et al. 2008 [two papers]). Many studies suggest that the mass extinction was prolonged and connected with at least two intervals of higher carbon dioxide levels in the atmosphere during the Rhaetian Age preceding the TrCCE (Cleveland et al. 2008, Ruhl et al. 2009), and "extremely elevated CO2 concentrations at the Triassic/Jurassic boundary" (title, Steinthorsdottir et al. 2011).

    Hallam (2010) suggests that the Triassic-Jurassic mass extinction on land was prolonged and not sudden.

    Relatively little is known of the effects of the TrCCE on terrestrial vegetation and biodiversity (Bonis et al. 2009, Götz et al. 2009, Mander et al. 2010, Lucas et al. 2011). Studies on the classic Triassic floras of Greenland suggest that tropical forests of this boreal region began to change in composition and stratification at the onset of global warming well before the TrCCE (McElwain et al. 1999, McElwain et al. 2007).

    Data gleaned from paleoecological and taphonomic studies of the Whitmore Point Member of the Moenave Formation of southwestern North America by Lucas et al. (2011) shed light on the effects of the TrCCE on terrestrial extinction across the Triassic-Jurassic boundary.

    Beerling and Berner (2002, abstract) state that "the end-Triassic mass extinctions represent one of the five most severe biotic crises in Earth history, yet remain one of the most enigmatic." Further, Beerling and Berner (abstract, 2002) propose that global warming, "due to a buildup of volcanically derived CO2," triggered "destabilization of seafloor methane hydrates and the catastrophic release of CH4 [Pálfy et al. 2001]."

    The two papers by Beerling and Berner (2002, 2004) present data and findings that disruption of the global carbon cycle at the end of the Triassic Period resulted in the release of up to 9,000 gigatons of carbon (as carbon dioxide gas) during the Central Atlantic Magmatic Province (CAMP) basalitic eruptions (Cirilli et al. 2009), and an additional 5,000 gigatons of methane released from methane hydrates imbedded in the seafloor.

    Major perturbation of the global carbon cycle at the Triassic-jurassic boundary (Beerling and Berner 2004, Whiteside et al. 2010, Črne et al. 2011, Ruhl and Kürschner 2011, Ruhl et al. 2011, Schaller et al. 2011) is coincident with anomalies in marine sulfur cycling (Williford et al. 2009), increases in unradiogenic osmium from the CAMP mantle source (Kuroda et al. 2010), and flood basalt volcanism (Schoene et al. 2010).

    Barremian biogeochemical perturbation (BaCCE). Biogeochemical evidence exists suggesting that a global atmospheric and climatic perturbation occurred in the Late Barremian (Neocomian, early Cretaceous). The BaCCE might have accelerated the diversification of early magnoliid flowering plants and possibly monocots (Heimhofer et al. 2005).

    Paul M. Barrett and Katherine J. Willis (page 437, 2001) report that elevated levels of carbon dioxide in Earth's atmosphere during the Cretaceous Period coincide with "... emergence of the major plant groups ..." and "... increasing rates of species turnover ..." Further, the initial radiation of flowering plants may be attributable to carbon dioxide build-up in the atmosphere according to an interesting hypothesis by P. M. Barrett and Willis (2001).

    Implications of the BaCCE and other thermal maximums toward the colonization of ice free landscapes, and diversification and speciation of flowering plants and their invertebrate and vertebrate antagonists, is discussed by P. M. Barrett and Willis (2001) and Friis et al. (2006).

    Chicxulub asteroid impact. The Chicxulub asteroid impact or Cretaceous-Paleogene (K-Pg) extinction has been the subject of much discussion with respect to the demise of dinosaurs. Older literature refers to the K-Pg or Chicxulub event as the Cretaceous-Tertiary (K-T) mass extinction.

    The insect and plant paleoecological literature on the K-Pg event is vast and some important papers include Labandeira et al. (2002), Nichols and Johnson (2008), Sepúlveda et al. (2009), and Schulte et al. (2010), among others.

    Discussion of the Chicxulub event marking the close of the Cretaceous Period and beginning of the Paleogene Period of the Cenozoic Era is outside the scope of this essay.

    The next chapter explores the paleobiology of interacting organisms in the Tree of Life, mutualisms, coevolution and the arms race, and fitness landscapes in deep time, which is necessary to disentangle paleoecologies of seed plant populations having to do with the origin of angiosperms and animal antagonists including fungi, invertebrates, microbes, and vertebrates.


    Fitness Landscapes, Compartments, and Paleoenvironments:

    Paleoecologies of ancient populations of stem-group flowering plants were not "dark and disturbed," or "wet and wild," or explainable by any other nonsensical and sophomorical pairing of adjectives.

    Arid, boreal, and tropical Pangaean landscapes were probably not "devoid of angiosperms." Based on palynological data (Cornet and Habib 1992, Hochuli and Feist-Burkhardt 2004, Zavada 2007, Hochuli and Feist-Burkhardt 2013), and arguments published by Cornet (1986, 1989, 1993), the preceding phrase quoted out-of-context from page 295 of Labandeira (2014), is probably incorrect.

    Tropical maritime swamps, riparian scrub and woodlands, and dry tropical shrublands and glades and rocky outcrops in walchian coniferous forests of the Central Pangaean Mountains bordering coastal embayments such as the Hovey Channel, might offer convenient paleogeographic settings for J. A. Doyle's "hidden homeland area" where the ancestors of flowering plants including delnorteas, evolsonias, and sandrewias, "had already diversified." Daniel Axelrod proposed a similar idea in 1952.

    Early phytophagous insects and herbivorous tetrapods probably used seed plant reproductive modules including fertile leaves (megasporophylls), ovules, seeds (ripened ovules), pollen-making sacs (microsporangia), and pollen as a source of food (Tiffney 1992, Zavada and Mentis 1992, P. M. Barrett and Willis 2001, Tiffney 2004).

    The image on the left is a native Fijian iguana Brachylophus vitiensis (Iguanidae, Reptilia). The animal was photographed by my office mate, the late John R. H. Gibbons, Ph.D. while conducting research in the Fiji Archipelago of the South Pacific Ocean.

    What was the extent of pollen flow in Paleozoic seed plant shrub populations?

    Phytophagous insects developed host specificity during the Permo-triassic and this might explain the evolution of "pollinator faithfulness" (page 126, Zavada 2007). Further, host plant secondary plant biochemical pathways leading to the production of antifeedents were probably developed by the Permian Period (Zavada and Mentis 1992).

    Microsporangia, pollen, and ovules were a likely source of food for phytophagous insects including paleodictyopterans, bugs, and early beetles.

    Seeds which are the products of sexual reproduction, probably rained from early Triassic shrub- and tree-like survivors of the EPE. Small, burrowing vertebrate animals probably ate many of the ovules and seeds, adversely affecting seed plant fecundity. Trampling and digging around these shrubs and small trees by fossorial vertebrates probably affected recruitment from the seed bank.

    During the first several thousand years following the global collapse of ecosystems at the PTr boundary, acidified substrates of fragmented biomes probably limited the germination of seed recruited from the seed bank. Niklas (1997) expands and modifies Wright's fitness landscape concept in a review of the evolution of early land plants.

    How do we apply Sewall Wright's adaptive (fitness) landscape concept toward a better understanding of evolutionary ecology of biome fragments, paleoenvironments, seed plant paleoecologies, paleobiology of mycorrhizal fungi in eroding landscapes, vertebrate herbivory, and the paleobiology of phytophagous insect colonies of Pangaea?

    Vertebrate paleoecologies. I use the term habitat in the context used by wildlife biologists. This subsection describes vertebrate habitats and the likely ecological effects of tetrapods on the paleoecology of the first angiosperms. Tiffney (1992) outlines the fossil history of amphibians and reptiles to create a better understanding of the effects of these animals on the evolution and diversification of land plants. Additional references on vertebrate herbivory include Regal (1977), Wing and Tiffney (1987), Coe et al. (1987), Weishampel and Jianu (2000), P. M. Barrett and Willis (2001), Labandeira (2002), Tiffney (2004), Eriksson (2008), Butler et al. (2009 [two papers]), Butler et al. (2010), Sander et al. (2010), and Eriksson (2016).

    Interactions of vertebrates with glossopterids include increased indigestible carbon content of plant tissues, increase in the biosynthesis and secretion of natural plant defense substances, reduction in leaf size, increased production of secondary tissues (greater woodiness), and morphological adaptations to protect ovules and pollen (Zavada and Mentis 1992).

    Key evidence on the fate of dicynodonts and therapsids following the EPE, based on study of fossil bones, paleosols, and depositional environments, is presented by Retallack et al. (2003). All paleontologic, paleopedologic, and paleoclimatic data gathered to date suggests that the mechanical activities of herbivorous dinosaurs had far-reaching effects on the evolution of seed plants including angiosperms (P. M. Barrett and Willis 2001).

    Grazing and trampling of the landscape by massive archosaurian dinosaurs, creating openings in conifer forests, probably favored the spread and diversification of flowering plants into these disturbed biomes. Indurate seeds with red sarcotestae may have been adapted to withstand digestive cavities of herbivorous dinosaurs. Mesozoic angiosperms that colonized vertebrate-disturbed landscapes probably evolved antiherbivory traits including production of deleterious natural plant products, spines, leathery leaves, small-sized leaves, thorns, woody trunks (Tiffney 1992, Zavada and Mentis 1992, P. M. Barrett and Willis 2001, Tiffney 2004).

    "Although dinosaur herbivores lived through several major events in floral evolution, there is currently no evidence for plant-dinosaur coevolutionary interactions" (page 207, Abstract, Barrett 2014).

    Duckbill dinosaurs, hadrosaurians, and ceratopsians probably fed on the foliage of woody angiosperm eudicots and conifers such as Gingko (Fricke and Pearson 2008). Fossils of the giant sauropod Alamosaurus co-occur in the same beds as fallen, permineralized logs of extinct dilleniid angiosperms (Wheeler and Lehman 2000).

    Based on anatomical studies of petrified stumps in situ and fallen whole logs, Wheeler and Lehman (2000) suggest that angiosperm tree species with extensive ray parenchyma might have been better adapted to survive browsing and trampling by large dinosaur herbivores in Cretaceous times. Coprolites, which are a potential measure of vertebrate herbivory, reveal fragments of Pennistemon (Friis et al. 2006), an early Cretaceous (Neocomian) monocotyledonous flowering plant (Friis et al. 2000).



    A native Fijian iguana Brachylophus vitiensis is pictured above. The animal was photographed by my office mate, the late John R. H. Gibbons, Ph.D. while conducting research in the Fiji Archipelago of the South Pacific Ocean.

    Insect interactions in vegetated compartments. The idea that invertebrates coexisted with extinct vascular plants (including those producing seeds) and with primitive angiosperms is not a new one (Meeuse 1978, Thien et al. 1985, Labandeira 1997, Labandeira 1998, Labandeira 2000, Zherikhin 2002, Krassilov et al. 2003). Sidney Ash (1997) reports fossil evidence of interactions between arthropods and seed plants from the Upper Triassic.

    By the Jurassic Period bisexual flower-like organs were common among certain Gnetales. Friis et al. (page 254, 2006) suggest that interactions between seed plants and insects (phytophagy and pollination), "appeared earlier, and perhaps independently, in other groups."

    Labandeira (2006), in a review of insect associations, recognizes four phases of terrestrial herbivore expansion during the geologic past that may be linked with global environmental change.

    The first phase of expanding herbivores on land was associated with transformation of the Silurian hot house world into the DeCARB.

    Phase 2 led to a resurgence of herbivores on land coinciding with melting of the global icehouse during the Carboniferous and the rise of oxygen levels in the atmosphere to 31% (Labandeira 2006). As a Permian hot house Earth developed, oxygen levels declined to less than 12% culminating with the EPE (Labandeira 2006, Knoll et al. 2007).

    Herbivore Expansion 2 and developing hypoxia of the Permo-triassic "may explain major turnover of Permian plant clades," according to Labandeira (page 423, 2006). The third phased expansion began during the late Triassic and continued through the Jurassic Period ending in the middle of the Cretaceous. Finally, Herbivore Expansion 4 occurred from mid-Cretaceous times ending with the present (Labandeira 2006).

    Elegant studies of the reproductive biology of extant cycads suggest that an ancient association might have existed between beetles and pollination of ovules (Norstog et al. 1986, Norstog and Fawcett 1989); and thrips as cycad pollinators (Terry et al. 2004, Terry et al. 2007). I regard individual cycad plants as miniature fitness landscapes exploited by invertebrate antagonists.

    Beetles, weevils, and ants are often closely associated with palms (monocotyledonous flowering plants), but the nature of pollination and phytophagy in specific species is relatively unstudied (Uhl and Dransfield 1987).

    Rasnitsyn (2002) reviews the fossil history of the phytophagous insect groups. Key papers include Labandeira et al. (1994), Krassilov et al. (1997), Labandeira (2000), Labandeira (2002), Labandeira et al. (2002), Krassilov et al. (2003), Labandeira (2007), Labandeira and E. G. Allen (2007), Krassilov (2008 [two papers]), Crepet and Niklas (2009), Labandeira (2010), and Labandeira and Currano (2013).

    Another attribute of seed plants is the ability to raise ambient temperature in the immediate spaces between sexual organs, sheathing leaf bases, and wood, cavities and crevices by increasing cell metabolism. This physiologic process is termed thermogenesis. Morphological adaptations are termed thermogenic plant tissue shelters (Meeuse 1978).

    Thermogenesis has been identified in developing cones of extant cycads (Tang et al. 1987, Terry et al. 2004), in beetle-pollinated, large-flowered angiosperms (Davis et al. 2008), and extant aroid monocots (Ito-Inaba et al. 2008, Ivancic et al. 2008). Flowers of certain Nymphaeales, a basal order of angiosperms, maintain temperatures in line with optima favored by beetles (Seymour and P. G. D. Mathews 2006).

    Insect-plant mimesis. Cases of arthropods mimicking plants are encountered by ecologists rather often, especially in habitats where insects seek cover against flying carnivores such as bats, birds, and predatory insects. Fully-developed insects sometimes possess segments and appendages with bizarre modifications of the exoskeleton that are suggestive of bark, leaves, and twigs.

    Gene expression studies of the evo-devo of modified insect body parts manufactured by the animal to look like plant organs might shed light on cross-talk of homeotic TFs and hormones. Fossil evidence suggests deep conservation in the insect tool kits once used for crypsis, aposematism, and mimicry. Cis-regulatory evolution of TFs controlling expression of optix may be responsible for mimicry in certain butterflies (Reed et al. 2011).

    The fossil history of insects masquerading as plants is reviewed by Sonja Wedmann (2010). Recent studies of fossilized lacewings (Neuroptera) from the Middle Jurassic document ancient mimesis of bennettitalean and cycadalean leaf pinnation by insects (Y. Wang et al. 2010).

    Mutualisms. A brief discussion of the evolutionary history of cross-Kingdom mutualisms might be relevant to questions having to do with the great late Paleozoic seed-plant divergences and Mesozoic explosive diversification and adaptive radiation of flowering plants. Further, there are implications of mutualisms toward a better understanding of the mechanisms that underpin coevolution (see the illustrated discussion in the next section).

    While discussing an inherent "multifaceted" capacity of angiosperms for "reinvention" within the evolutionary and paleobiological context, Crepet and Niklas (2009) conclude:

    "... It is clear that plant-animal interactions were critical to the success of the earliest flowering plants in light of a reciprocal driving mechanism for angiosperm and animal diversifications."

    The preceding statement is quoted from page 378 of W. L. Crepet and K. J. Niklas (2009), Darwin's second "abominable mystery": Why are there so many angiosperm species? American Journal of Botany 96(1): 366-381.

    Mycorrhizal fungi interacting with plants. The fossil history of fungal-plant interactions is well-documented in the paleobotanical literature (Chapter 3, T. N. Taylor et al. 2009). Mycorrhizal mutualisms are of particular importance in seed plant paleoecology (page 103, T. N. Taylor et al. 2009). This milestone book is the starting point for students to review the paleobiology of fungi and their mutualisms with plants.

    Mycorrhizal fungi probably played an important ecological function in the recovery of terrestrial vegetation following the Paleozoic mass extinctions. More paleoecological studies are needed with possible focus on interacting ground dwelling fungal mycelia and gymnosperm root- and rhizome systems.

    Paleobotanical and paleopedological evidence suggests that some species of seed plants rooted in terrestrial soils of the Triassic Period possessed functional underground mycorrhizal nodules (Schwendenmann et al. 2011).

    Were vesicular-arbuscular mycorrhizal (VAM) fungi associated with these seed plants? What, if any, potential strigolactone hormonal interactions existed between possible seed plant-VAM associations of Carboniferous paleoenvironments.

    Insect-plant mutualisms. Insect-plant mutualisms involve a mobile organism (the insect) and a stationary one (the plant host). Such mutualisms evolved multiple times in many flowering plant groups. Mutualisms are often gained and then lost over time (Bernhardt 2000, Bronstein et al. 2006).

    Further, traits seen among interacting insect- and plant-mutualists are often mismatched (B. Anderson et al. 2010).

    Plant cavities and organs are used by insects for breeding, feeding, and shelter (G. N. Stone et al. 2008). For example, saproxylic beetles were prevalent in the Mesozoic and late Paleozoic eras (Kirejtshuk 2003).

    Fossil evidence of mutualistic associations between specific insect groups such as beetles, nitidulids, bees, and wasps; and early Mesozoic and Paleozoic seed plants is sparse but intriguing (Krassilov et al. 1997, Krassilov and Rasnitsyn 1997, Ponomarenko 1998, Beck and Labandeira 1998, Labandeira 1998, Zherikhin 2002, Krassilov et al. 2003, Scott et al. 2004, among others). Controversial reports of fossilized hives possibly belonging to ancestors of hymenopterans, which are commonly associated with modern flowering plant pollination and herbivory, predate the appearance of fossil flowers by more than 100 million years (Hasiotis et al. 1998).

    Sometimes hints of past insect activities on plants come from the study of ichnofossils e.g. indirect evidence of egg-laying inside leaf fossils from the Upper Permian (Vassilenko 2011).

    The most complete review of insect-seed plant mutualisms during the Albian superradiation of flowering plants is by Conrad Labandeira (2014).

  • (1) "The angiosperm radiation ... One of the major episodes in the evolution of insect herbivory is the transition from gymnosperm to angiosperm-hosts during the initial diversification of angiosperms 125 to 90 million years ago"
  • (2) "The pattern ... Thus, a major [Aptian-Albian, page 288, Figure 13.3] gap occurred during these two [angiosperm-gymnosperm host-associated insect families] diversity maxima levels present on both sides of the angiosperm radiation ... " [attributable to "major turnover and time-lag effects"]
  • (3) "Implications ... The ecology of interactions between these older insect lineages and their dominantly gymnosperm hosts needs to be explored further [see also Labandeira et al. 1994] to establish an entrée into this earlier world devoid of angiosperms"
  • Whether plant-insect mutualisms lead to coevolution of the plant host and insect antagonist is problematic (Labandeira 2014). While discussing cospeciation in fig pollination mutualisms, Bronstein et al. (page 422, 2006) suggest "... that evolution has been relatively one-sided in many of these mutualisms ..." and "... that we have not always been looking at the right insect traits."

    Coevolutionary studies of insects and their fig plant hosts employ living systems (Jousselin et al. 2003, Cook et al. 2004, Machado et al. 2005). Questions on the paleobiology of coevolution may be difficult to answer except from a molecular-phylogenetic research perspective.

    Interactions between insects and seed plants (Futuyma and Keese 1992, Labandeira et al. 1994, Krassilov et al. 1997, Labandeira 1998, Labandeira 2000, Gorelick 2001, Zherikhin 2002, Krassilov 2002, Labandeira 2002, Cornell and Hawkins 2003, Krassilov et al. 2003, A. C. Scott et al. 2004, Labandeira 2010) are well-documented in the literature.

    Animal and plant mutualisms in Upper Paleozoic time were not just confined to arthropods, myriapods, and lignophytes, but also included interacting tetrapods and plants. This subject is discussed in the next subsection.

    Tetrapod-plant interactions. There has been considerable attention paid to the paleoecology of tetrapod-seed plant mutualisms in discussions of the origin, dispersal, and adaptive radiation of angiosperms, gymnosperms, and plant-eating dinosaurians (Tiffney 1992, Zavada and Mentis 1992, Weishampel and Jianu 2000, P. M. Barrett and Willis 2001, Labandeira 2002, Tiffney 2004).

    Dinosaurians and seed plants interacted in their ancient habitats but the relationship was diffuse (Weishampel and Jianu 2000, P. M. Barrett and Willis 2001, Labandeira 2002, Tiffney 2004). The oldest evidence of vertebrate gut contents containing identifiable plant material (i.e. conifer ovules) is from fossilized food boluses of Permian tetrapods (Munk and Sues 1993).

    Positing a late Paleozoic or early Triassic origin of flowering plants (Beaulieu et al. 2016, C. S. P. Foster et al. 2017), and taking into account potentially important (if not critical) Upper Paleozoic divergences of the main clades of gymnosperms (i.e. conifers, cycads, gigantopterids, gigantopteroids, gnetophytes, ginkgophytes), might convince at least some students of paleoecology to look for evidence of diffuse coevolution in sympatric populations of Permo-triassic tetrapods and spermatophytes.

    Temnospondyls are a possible candidate group of late Paleozoic tetrapods for focused paleoecological studies (Sanchez et al. 2010). The poster-baby of evo-devo studies of tetrapod paedomorphism and neoteny is the axolotl (S. J. Gould 1977), which is the evolutionary offshoot of Permo-triassic Temnospondyli.

    Astonishingly, a species of extant salamander (Ambystoma maculatum) is mutualistic with a green alga (Kerney et al. 2011). Did green algal cells form mutualisms with late Paleozoic temnospondyls?

    If supported by paleontological evidence, did algal-vertebrate mutualisms lead to episodes of HT of plastidic DNA and tetrapod host cell mitochondria?

    In the next section I discuss potential coevolution of animals, fungi, and seed plants during the Carboniferous and Permian periods of the Paleozoic Era as a possible contributing factor in the origin and evolution of flowering plants.

    Coevolutionary compartments in deep time. This section briefly mentions studies on extant coevolutionary networks and some aspects of escape and radiation with the hope that ideas might be applied to answering questions in deep time.

    "It is clear that plant-animal interactions were critical to the success of the earliest flowering plants in light of a reciprocal driving mechanism for angiosperm and animal diversifications."

    The preceding quotation is from page 378 of Crepet and Niklas (2009), Darwin's second "abominable mystery": Why are there so many angiosperm species? American Journal of Botany 96(1): 366-381.

    What was the reciprocal mechanism sensu Crepet and Niklas (2009) that led to the diversification of the stem lineage(s) of flowering plants, certain tetrapods, and holometabolous insects?

    The picture to the right is a flower of Milla biflora (Iridaceae, Asparagales, Lilianae) and several dipteran insect visitors from the upper canyon of the Rio Quebrada de la Ventana, Sierra Madre Occidental of southwestern North America (photographed by the author in 1977).

    Students of cone- and floral- paleoecology may also wish to critique a series of little papers, which were published in the first three numbers of Botany Letters for year 2016.

    While publication of these three letters was refreshing and newsworthy to the popular-scientific readership, authors of all three papers could have done a better job of reading and discussing several articles and book chapters, which were germane.

    "... there is no reason to expect that a given pair of interacting populations should always be engaged in 'strict' coevolution, even if there is a fair amount of reciprocal adaptation going on between the species in question." (page 73, Introduction, Janz 2011).

    Despite possible irrelevance to genetic mechanisms that probably underpinned floral evolution and paleocology, the cladistic exercise published by the Angiosperm Phylogeny Group (APG IV 2016) was invoked by one of the authors. A passage quoted from Janz (2011) is relevant.

    "At least in zoogamous groups, the flower is labile and changing because it is an active co-evolutionary battlefield ..." (page 234, Flowers are no longer flagships for higher level taxa, M.-A. Selosse 2016).

    Metaphors and parables aside, there is no scientific evidence for plant- and/or floral-intelligence (Glover 2014, Becker 2016, among others). Let's not forget biochemical mechanisms underpinning floral sculpting (Nag and Jack 2010), thigmomorphogenesis (Braam 2005, Chehab et al. 2011), transcription factor (TF) movements (Xu and Jackson 2012) even within the floral shoot apical meristem (SAM), nyctinasty of the perianth, and jasmonate induction of leaf- and floral- volatiles (I. T. Baldwin 1998, Ballaré 2011). Two questions, among others, come to mind from the 2016 Botany Letters.

    Evolutionary mechanisms are at work in both sympatric and allopatric animal- and plant populations. Could a single plant organ such as the reproductive short- [spur-] shoot comprise a coevolutionary "battlefield"?

    If arguments posed by Dodinet are taken at face-value, do the two organisms pictured above, image exhibit intelligence?

    Authors of the three botanical letters might reconsider their views on floral biology and coevolution from the research perspective of population biologists while incorporating discussion of at least some basic concepts of ecology including the coevolutionary arms race (Wu and I. T. Baldwin 2010), coevolutionary compartments (J. N. Thompson 2005), and Thompson's concepts of coevolutionary "coldspots" which are dominated by non-reciprocal selection (J. N. Thompson 2005) or reciprocal selection leading to formation of coevolutionary "hotspots."

    Some of the other ecological principles left on a limb by Selosse (2016) include cospeciation (Janz 2011), escaping and oscillating (Fordyce 2010), or escaping and radiating (Ehrlich and Raven 1964, Wheat et al. 2007, Janz 2011).

    It was also strange that Selosse (2016) did not bring-up classical concepts of fitness landscapes (Niklas 1997), nested assemblies (Bascompte et al. 2003), and reciprocal radiation (Ehrlich and Raven 1964).

    A coevolutionary arms race at the molecular level between populations of coevolving flowering plant hosts and insect antagonists is supported by real-time experimental studies (Wu and I. T. Baldwin 2010). Further, evo-devo studies (Becker 2016) using biochemically altered probes, genetically-engineered TFs, and microRNAs (Nag and Jack 2010) demonstrate the lability of flowers (Paul Wilson et al. 2007) and insect bodies.

    Long terminal repeat- (LTR-) retrotransposon-mediated modification of genomic ["island"] landscapes is possible (Civáň et al. 2011).

    Are shared fly and iris LTR-retrotransposons the genetic battlefield weapons of the floral landing strips seen in the image of Milla biflora above?

    Strict coevolution of stem group flowering plants and certain lineages of holometabolous insects is probably difficult, if not impossible, to prove in paleopopulations. Diffuse "coevolution" is not (this convention was used by Labandeira 2014), when considering the paleobiology of plant-insect associations (PIAs). Labandeira (2013) reviews the paleobiological literature on PIAs of herbivory and pollination.

    There are problems associated with Cretaceous co-radiations of angiosperms and insects brought to light by phylogenetics (Gómez-Zurita et al. 2007, Wheat et al. 2007) and their paleoecologies (Chittka 1996, Labandeira 1998, among others). Tight coevolution between sympatric arthropod and flowering plant populations is unsupported by the data gleaned from Mesozoic fossils (Labandeira 2014). Presumed co-radiations are often out-of-sync (Gómez-Zurita et al. 2007), suggesting that evolution of clades of late Mesozoic phytophagous ants, bees, beetles, butterflies, flies, and moths is independent of the explosive origin and spread of eudicot orders and families.

    Professor Labandeira provides a painstaking analysis of a new data set on family-level asynchronous co-radiations of angiosperms with the families belonging to the holometabolous "Big Five" insect orders of pollinivores and pollinators (including Triassic Obrieniidae and Tipulidae) plus Triassic Pseudopolycentropodidae (Mecoptera), Trichoptera, and protohymenopteran Xyelidae, and new data on phytophagous families of hemimetabolous Paraneoptera and Polyneoptera (Table 13.1 on pages 265-271, 2014).

    "... the link between coevolution and diversification of plant and insect lineages is neither obvious theoretically nor clearly supported empirically" (Concluding Remarks and Future Directions, page 106, Suchan and N. Alvarez 2015).

    Labandeira reached this same conclusion in 2014. Ecologists should compare the paleobiological study by Labandeira (2014) with earlier work by Chittka (1996), Briscoe and Chittka (2001), and Chittka et al. (2001). Implications of these three studies toward an understanding of the deep time evolution of pollination mutualisms and color and scent perception by species of the "Big Five" holometabolous insect orders and late Paleozoic seed plants, when taking into account the paleobiology of the arthropod brain, are absolutely profound.

    "It is likely that trichromacy existed prior to the advent of angiosperm flowers" (page 138, Chittka 1996).

    Based on a decade of reading and review of the scientific literature on the origin of the flower and interacting insects, which is presented on this web site, I am skeptical of many ideas outlined in letters by Dodinet, Nadot, and Selosse.

    A review of Cretaceous records for clumped angiosperm pollen and its bearing on coevolution with insect pollinators is available (D. W. Taylor et al. 2010).

    Coevolutionary theory was developed from hypotheses tested using extant plant and animals in their native biomes, communities, and habitats (J. N. Thompson 1989, Grehan 1991, Futuyma and Keese 1992, Cornell et al. 2003, B. Anderson and S. D. Johnson 2008). Habitats are viewed by students of coevolution as nested and antagonistic networks of interacting species (Bascompte et al. 2003, Guimarães et al. 2006, Bastolla et al. 2009).

    A conceptual framework for the Geographic Mosaic Theory of Coevolution is outlined and discussed by J. N. Thompson (2005). This theory is structured by several "assumptions," "evolutionary hypotheses," and "general ecological predictions" (page 98, Table 6.1, J. N. Thompson 2005) outlined below:

  • coevolving species pairs are comprised of genetically differentiated populations
  • interacting species pairs do not always have identical geographic ranges
  • such pairs of coevolving species are phylogenetically conservative in their interactions
  • these coevolutionary relationships are held together for a long time
  • ecological outcomes in interacting species pairs differ from one plant community to another
  • coevolving species become locally adapted to local populations of other species
  • coevolution is potentially rapid
  • natural selection on interacting species pairs varies from place to place but reproductive success (fitness) of one species depends on the other
  • coevolutionary "hotspots" involve species interactions which are subject to reciprocal selection
  • "hotspots" are often imbedded among "coldspots" which are dominated by non-reciprocal selection
  • traits are remixed as a consequence of mutation, gene flow across landscapes, and drift and saltation, resulting in shifts of the geographical mosaic
  • phenotypes of coevolving species pairs are shaped by their interactions matched within plant communities
  • very few coevolved traits become fixed due to differential selection
  • Aspects of the Geographic Mosaic Theory of Coevolution might be applied to deep time animal, fungal, microbial and viral pathogen, and plant interactions, including interactomes at all levels from molecules to populations, but mathematical models are generally wanting in the literature.

    Coevolution of microbes and viruses with animals and plants. Two important reviews are available on the subject of coevolution of wasp parasites, hosts, and pathogenic viruses with implications on the manipulation of insect behavior and the coevolution of seed plant and insect tool kits (Lovisolo et al. 2003, Grimaldi and Engel, page 427, 2005).

    Students of coevolution should pay attention to clues pertaining to gene flow mechanisms involving both vertical and horizontal transfer of DNA, which are buried in the extensive literature on pathogenic baculoviruses. Baculovirus genes are incorporated into genomes of gypsy moth hosts causing large behavioral phenotypic effects. "Gypsy moths infected by a baculovirus climb to the top of trees to die, liquefy, and 'rain' virus on the foliage below to infect new hosts" (abstract, Hoover et al. 2011).

    Baculoviruses constitute one of many potential sources of cross-Kingdom mobile genome parasites, which are able to freely move from fungal and/or insect vectors to plant hosts within one of J. N. Thompson's coevolutionary compartments?

    Implications of cross-Kingdom HT of bits and pieces of tool kit DNA from accumulating LTR-retrotransposons originating in fungal and/or insect bodies to genomes of seed plant hosts, are understandably profound.

    Coevolution of arthropods and land plants. This subsection pertains to possible coevolution of arthropods and lignophytes in deep time from molecular-phylogenetic and paleophysiologic research perspectives.

    What molecular-phylogenetic aspects of arthropod antagonist/seed plant host developmental regulation should paleobiologists study?

    Studies of the helix-turn-helix (HTH) DNA-binding motif of the malvid angiosperm Arabidopsis thaliana by Hamès et al. (2008) report similarities to the active motif of Drosophila Engraled homeodomain protein. Molecular phylogenetic and biophysical studies of seed plant LFY enzyme and insect engraled protein may shed light on coevolution at the molecular level.

    It might also be important to consider the paleophysiology of homeodomain proteins and other enzymes when developing explicit hypotheses on a possible coevolutionary origin of angiosperms and certain holometabolous insects.

    The "right insect traits" (page 422, Bronstein et al. 2006) might be HTH proteins encoded by the compartment-selector gene engraled and certain homeotic selector genes of the Hox complex (e.g. homologs and paralogs of abd-A, Abd-B, Hox3, pb, Scr, and Ubx). Bronstein and company's traits of focus might also include enzymes belonging to the respiratory, moulting, and vitellogenin developmental tool kit.

    Coevolution between phytophagous insect associates of certain land plants may have been affected by the two rounds of slow decline in atmospheric oxygen levels during the Paleozoic Era. The first round coincided with the late Devonian-early Carboniferous ice-house (Berner and Kothavala 2001), and a second was initiated by the GuCCE (Retallack et al. 2006) and high carbon dioxide and methane levels in the atmosphere, culminating with "trigger and kill mechanisms" (page 296, Knoll et al. 2007) associated with the EPE.

    Based on global atmospheric and biogeochemical crises, specific invertebrate respiratory proteins of potential evolutionary interest are probably hemocyanins, hemoglobins, and hexamerins (Van Holde et al. 2001, Burmester 2004, Burmester and Hankein 2007, Hagner-Holler et al. 2004, Hagner-Holler et al. 2007).

    The diagram below illustrates how signals originating in the bodies of phytophagous insects might potentially affect the biochemical machinery of differentiating cells in SAMs of certain developmentally plastic, late Paleozoic host seed plants. Transposable elements might have moved from the insect genome to the host plant genome or vice versa within the confines of a shrub lifeboat (see next section).

    Further, host plants might have manufactured phytoecdysones including brassinolides that potentially signaled the developmental, respiratory, and storage protein biosynthetic machinery of insect antagonists inhabiting Paleozoic and early Mesozoic vegetation compartments. The paleobiology of arthropod antagonists and their habitats might never be understood.



    Clues on whether or not low pO2 is a selective force come from ecologic, physiologic, and rearing studies of extant insects (Gorr et al. 2006). The Holometabola exhibit complete metamorphosis of the fertilized egg to a wingless larval stage, a quiescent pupal stage, culminating with reproductively mature adults (page 331, Grimaldi and Engel 2005).

    Hypoxia in extant terrestrial environments is defined as an oxygen concentration below ca. 20% (Hoback and Stanley 2001). Adaptations to hypoxia in holometabolous insects are specific to developmental stages. According to the review by Hoback and Stanley (2001), several kinds of extant insects are adapted to hypoxic environments including Coleoptera (beetles and weevils), Collembola (springtails), Diptera (flies), Isoptera (termites), Lepidoptera (butterflies and moths), and Orthoptera (grasshoppers and katydids).

    Tenebrio molitor beetles exhibit 80% larval mortality, decreased instar body mass, and an increased number of moults when reared in an atmosphere of 10% oxygen in a nitrogen (Greenberg and Ar 1996). Aquatic insects are generally more susceptible to hypoxia than terrestrial insects (Hoback and Stanley 2001). Hoback and Stanley (page 540, 2001) conclude "... that the developmental plasticity of insects facilitates morphological changes in respiratory systems in chronically hypoxic situations."

    Choice of hemocyanins and hexamerins as some of the right insect traits to study ties-in with the evolution of insect legs and wings from bilaterian gills. Ancient insect wings probably functioned as respiratory organs. Wings, halteres, arachnid spinnerets, and insect legs are all organs that develop from limb fields of cells where Ubx expression is prevalent (S. B. Carroll et al. 2005).

    Escape-and-radiate or oscillate. The "escape-and-radiate" hypothesis was discussed in Chapter 7 of J. N. Thompson's book on coevolution to recapitulate Ehrlich and Raven's (1964) suggestion that reciprocal selection may produce "higher-level patterns of diversification within phylogenetically conserved interacting lineages" (page 150, J. N. Thompson 2005).

    Competing "escape-and-radiate" and "oscillate" hypotheses are reviewed by Fordyce (2010). The two hypotheses discussed by Fordyce might be applied to a couple of intractable or difficult questions in population paleoecology:

    Was there a potential for genetic release of insect induced molecular effects on the seed plant developmental machinery attributable to shifts of arthropod antagonists away from the plant host to other oxygen-enriched shrub lifeboat habitats and lignophyte hosts?

    What specific kinds of paleontologic and molecular phylogenetic data may be used to shed light on the paleobiology of insect-seed plant coevolutionary compartments?

    To my knowledge the notion of genetic release in a host plant-insect antagonist coevolutionary relationship at successively complex levels of transcriptional regulation, repetitive ("junk") DNA, genome dynamics, and neo-Goldschmidtian saltation is rarely discussed to explain observations seen by ecologists who study fitness in extant populations.

    Since Ehrlich and Raven's classic paper (1964) many colleagues have enthusiastically supported proposals on a coevolutionary origin and/or diversification of flowering plants based on co-radiations between specific groups of animals and seed plant hosts of the Cretaceous Period (Grehan 1991, Crepet and Niklas 2009, Janz 2011). A critique of this work is available (Suchan and N. Alvarez 2015).

    Aspects of coevolution of Mesozoic arthropods and seed plants which have a bearing on the origin and diversity of angiosperms were proposed by Takhtajan (1969), Raven (1977), Thien et al. (1985), Farrell (1998), Labandeira (1998), Grimaldi (1999), Wilf et al. (2000), and S. Hu et al. (2008).

    Some of these studies focus on possible coevolution of arthropods and the first angiosperms during the Jurassic or Cretaceous periods of the Mesozoic Era, not the Carboniferous or Permian periods of the Paleozoic Era.

    Coevolution and cospeciation between butterflies and host plants are probably more dynamic than appreciated (Wheat et al. 2007).

    Molecular phylogenies of chrysomelid leaf beetles suggest a younger age of the group than previously realized (Gómez-Zurita and Galián 2005, Gómez-Zurita et al. 2007). These findings contradict earlier proposals on a coevolutionary origin of angiosperms during the Cretaceous Period (Farrell 1998, Grimaldi 1999, Wilf et al. 2000).

    Could paleoecologists solve problems illuminated by Toby Hunt, Labandeira, Gomez-Zurita, and Wheat, among others, such as observed out-of-sync plant and insect co-radiations, by invoking aspects of competing "escape-and-radiate" and "oscillate" hypotheses?

    Shifting pollinators. Ecological studies and phylogenetic analyses of extant species groups with divergent floral characters point toward reciprocal selection and recurring pollinator shifts in the evolutionary history of certain parallel lineages (see review by Fenster et al. 2004).

    The recent literature contains several key articles on this subject (Paul Wilson et al. 2007, S. D. Smith et al. 2008, J. D. Thomson and Paul Wilson 2008, Muchhala and J. D. Thomson 2009, Pauw et al. 2009, Des Marais and Rausher 2010).

    Des Marais and Rausher (2010) proposed a mechanism underlying floral color polymorphisms and shifting pollinators from the research perspectives of biochemistry and genetics. Regulation of flavonoid biosynthesis by flavonol-3'-hydroxylase is affected by cis-regulatory changes in the gene encoding this enzyme.

    A study by Ramírez et al. (2007) sheds light on the time of origin of a specific orchid and its pollinator. In follow-up work Ramírez et al. (2011) explore peculiar asymmetries in bee and orchid pollination mutualisms possibly involving sensory behaviour.

    Based on a possibility that insect "sensory bias" might affect co-diversification with plant hosts (abstract, Ramírez et al. 2011), could studies of insect pollinator and flowering plant mutualisms from research perspectives of horizontal transmission of tool kit transposable elements shed light on underlying "evolutionary processes" in pollination ecology and shifts?

    Coevolution of seed plants and dinosaurian tetrapods. Weishampel and Jianu (2000), in an extensive review of dinosaurian herbivory, cast doubt on the coevolutionary-based idea that ornithischian tetrapods had an effect on the rapid radiation of flowering plants during the Cretaceous Period. Dinosaurians probably did not play a key role in the contrived Cretaceous Terrestrial Revolution (G. T. Lloyd et al. 2008).

    According to Weishampel and Jianu (page 137, 2000), three geologic intervals of diversification of euornithopod transverse grinders occurred during the Cretaceous Period "with the middle peak arguably associated with the origin of angiosperms." However, when ghost lineages are added to the cladistic analyses "the middle peak disappears" (page 137, Weishampel and Jianu 2000).

    "Whatever coevolutionary interactions may have existed between flowering plants (angiosperms) and ornithischian dinosaurs, they are not apparent at the onset of the evolutionary radiation of angiosperms, as least as far as diversity patterns are concerned."

    The preceding quotation is from page 139 of Weishampel and Jianu (2000), Chapter 5, Plant-eaters and ghost lineages: dinosaurian herbivory revisited. Pp. 123-143 In: H.-D. Sues (ed.), Evolution of Herbivory in Terrestrial Vertebrates: Perspectives from the Fossil Record, Cambridge: Cambridge University Press, 256 pp.

    Tiffney (2004), in an extensive review of vertebrate dispersal of seed plants, concludes that tight coevolution between animal dispersers and plant is rare. Biotic dispersal of seed plant propagules probably arose through "transfer of function," according to Tiffney (page 6, 2004). Further, he suggests that "the Mesozoic dynamic was dominated by reptile-gymnosperm interactions to which the angiosperms were newcomers" (page 20, Tiffney 2004).

    Coevolution of flowering plants and frugivores. A diffuse relationship between an explosive superradiation of flowering plants with frugivorous bats, multituberculates, ornithischians, passerines, primates, and rodents, is the subject of a paper published by Ove Eriksson (2016) in the Biological Reviews of the Cambridge Philosophical Society.

    Fruits of Degeneria vitiensis open in a "butterfly" fashion exposing several bright orange or red seeds that dangle from the fruit casing by funiculi (right-hand image). Frugivorous fruit doves and parrots consume and disperse seeds of degenerias. Degeneriaceae are magnoliids endemic to The Fiji Archipelago of the South Pacific Ocean (J. M. Miller 1989).

    A coevolutionary origin and radiation of angiosperms and ornithischians has been proposed by several paleontologists (see above). Paul Barrett revisits some of these ideas in his contribution to a 2014 volume of the Annual Review of Earth and Planetary Sciences.

    Oxygenated shrub lifeboats as coevolutionary compartments. Pockets of air trapped by sheathing, leathery photosynthetic leaves of a monopodium and other crevices in organs of arborescent and herbaceous seed plant species might have had higher amounts of oxygen gas than the surrounding atmosphere of Devonian, Carboniferous, Permian, and Triassic time.

    I name the individual seed plant shrubs and small trees of hypoxic late Devonian-early Carboniferous, Permian, and Triassic fitness landscapes that house herbivorous insect antagonists in oxygenated air spaces and crevices, shrub lifeboats.

    A higher partial oxygen pressure within the air spaces between host plant leaves could potentially protect resident insect mutualists from atmospheric disruption and hypoxic conditions attributable the DeCARB, GuCCE, EPE, TrCCE, and BaCCE. Trapped oxygen gas of air pockets in the host shrub might have been critical for the survival and metamorphosis of instars (fertilized eggs, larvae, pupae).

    Optimal thermogenic microhabitats cast from food-bearing, sheathing leaves and woody tissues could have sustained a resident insect and tetrapod population during times of temperature extremes, hypoxia, and high ultraviolet radiation levels.

    The diagram on the left side of the page illustrates a hypothetical seed plant shrub lifeboat. The monopodium with its SAM and large, leathery sheathing leaves is shown from an overhead view. The resident insect colony of eggs and instars (or larvae, pupae, and adults) shown as red-colored objects occupies the oxygenated air spaces that surround the growing tip and hollows formed by clasping leaves of the shrub.

    Invoking coevolutionary nomenclature drawn from studies of extant biomes, a shrub lifeboat might also be viewed as a compartment housing antagonists (herbivores and predators) in a locally hot, hypercapnic, hypoxic, Permo-triassic fitness landscape.

    Did perennial seed plant shrubs furnish respiring insects with cavities and air spaces having a higher pO2 than the surrounding hypoxic oxygen desert?

    Were sheathing plant tissues including sporophylls UV screens, which were necessary to prevent damage to cells, chromosomes, membranes, and the spindle apparatus?

    Color illustrations of malformed Classopollis pollen may be found in Figure 3c, 3d on page 338 of Van De Schootbrugge and Wignall (2016). Were some of the pollen abnormalities observed in Permo-triassic fossils caused by abiotic factors?

    Were ancient baculoviruses a source of cross-Kingdom genome parasites able to move from animal bodies and/or fungal mycelia to reproductive modules and/or growing points of seed plant hosts comprising Permo-triassic shrub lifeboat coevolutionary compartments?

    What happened to complex food webs, plant communities and habitats of early Triassic time following the disruptive and extirpatory forces of the EPE?

    Some early Paleozoic forests of conifers, ferns, lycophytes, and sphenopsids were stratified and contained complex food webs involving decomposers, primary producers, mycorrhizal fungi, and populations of invertebrates and amphibians (Z.-Q. Wang 2000).

    Were elevated carbon dioxide levels and volcanic gases in the atmosphere of late Permian time when combined with low pO2, a selective force in plant and animal populations, including terrestrial arthropod invertebrates and vertebrate tetrapods?

    A recent paper by L. G. Stevens et al. (2011) provides some answers to this question, among others.

    Knoll et al. (2007) review the possible physiological effects of hypercapnia on animals and plants in connection with the end-Permian global apocalypse and biotic recovery of early Triassic aquatic and terrestrial landscapes. Geochemical studies suggest that late Permian and early Triassic air of Pangaean shorelines had oxygen levels comparable to the highest summits (>5000 meters) of most modern mountain ranges (Huey and Ward 2005).

    Based on studies of fossils, paleosols, and geochemistry it was possible that during millions of years of Paleozoic global climate changes, complex networks of generalist and antagonist animal and plant species broke down and/or were disrupted (Retallack et al. 2003, Retallack et al. 2005).

    Hypoxic ice-houses. The ice-house terrestrial paleoenvironments of the DeCARB might have been challenging to the respiratory systems of invertebrates including ancient plecopteran insects (Labandeira 2006). The DeCARB was also a time of seed plant innovation (Rothwell et al. 1996).

    Early arthropods exhibited an explosive radiation of molecular novelties of the hemocyanin class of gas-binding respiratory enzymes during the hypoxic DeCARB. At least seven clades of hemimetabolous and holometabolous insects diverged from the thawing ice-house as evidenced by molecular clock estimates of hexamerin moulting storage proteins (Hagner-Holler et al. 2007).

    Was the burst of evolution of insect hexamerin proteins from hemocyanins somehow linked to low temperature and low oxygen levels in terrestrial paleoenvironments of the DeCARB?

    Are there TFs in arthropod and land plant tool kits, respectively that act as oxygen sensors? Possibly.

    Hypoxia-inducible factors (HIFs) are unexpectedly diverse in invertebrates (Rytkönen et al. 2011). Specific HIFs are not yet known from the land plant tool kit but the ERF and AP2 family of TFs might be key players (Licausi 2011, Licausi et al. 2011).

    Hypoxic and hypercapnic hot-houses. High carbon dioxide levels in the atmosphere and water column preceding and immediately following the EPE might have had profound effects on the physiology of animals (Knoll et al. 2007). Several unanswered questions remain:

    How did terrestrial invertebrates and vertebrates cope with high carbon dioxide content and low levels of oxygen in the global atmosphere (<12%) following the GuCCE and EPE?

    Was pO2 lower at higher altitudes in, for example, the Hercynian Mountains?

    What was the effect of low pO2 and elevated carbon dioxide (hypercapnia), methane, and hydrogen sulfide levels on animals and plants indigenous to aquatic and terrestrial environments?

    Two important book chapters compiled by McElwain and coauthors explore the potential effects of hypercapnia on angiospermization, diversification, and rates of speciation in land plants (McElwain et al. 2005, McElwain et al. 2011).

    According to Andy Knoll et al. (page 302, 2007), "... hypercapnia can reduce respiratory capacity, exacerbating the physiological effects of environmental oxygen limitation."

    "It is possible, therefore, that the high CO2 [Silurian] concentrations acted as an environmental 'barrier' that prevented the origination and spread of large megaphylls. Once that environmental barrier was removed, ecological processes, especially competition between species for light, soil and water nutrients, would have driven both the co-evolution of the root and shoot and the well-documented increase in plant height (Beerling and Berner 2004)."

    The previous statement is quoted from page 10 of David J. Beerling and Andrew J. Fleming (2007), Zimmermann's telomb theory of megaphyll leaf evolution: a molecular and cellular critique, Current Opinion in Plant Biology 10: 4-12.

    Did Paleozoic seed plant shrubs and trees (or even herbs) furnish respiring insect larvae with cavities and air spaces having a higher pO2 than the surrounding hypoxic landscape?

    Could plant organs, tissues, and waxy cuticles shield insect eggs and instars from potentially deleterious UV solar radiation?

    The EPE marking the beginning of the Triassic Period of the Mesozoic Era also had devastating effects on growing substrates including extirpation of mycorrhizal fungi and certain soil bacteria. Global terrestrial and aquatic environments became acidified by 600,000 years of global volcanism and more than a million years of precipitation containing dissolved sulfur dioxide (SO2) outgassed from magma underlying the Siberian Traps, a name applied by geologists to early Triassic epicontinental lava lakes.

    The art board below shows a community of potentially coevolving animal antagonists that inhabit shrubs and trees of a biome fragment of an hypoxic late Permian fitness landscape based on descriptions by DiMichele and Hook (1992). A biome fragment near a water source in an otherwise arid landscape is depicted with overstory conifers and understory scrub, which is punctuated by dicynodont burrows. Herbivorous dicynodonts were probably the most common vertebrate animals of such late Permian landscapes (DiMichele and Hook 1992).

    Did certain Triassic seed plants possess functional underground mycorrhizal nodules? Yes, according to Schwendenmann et al. (2011).

    The vertebrate tetrapod population resided with the oxygen generating vegetation consisting of seed plant shrubs and coniferous trees, and an understory of bryophytes, ferns, horsetails, lycopsids, and seed ferns. Seeds rained on to the floor of the biome forming a seed bank sensu Harper (1977), and bisaccate pollen was transported to other shrubs and trees. Insect colonies and free-living invertebrates (antagonistic generalists and predators) are shown in dark red.

    Free living insects and certain generalists were probably only able to crawl, fly, or hop short distances from the oxygenated crevices of one shrub lifeboat to another. The surrounding hypoxic desert might have been lethal to most respiring animals. The increasingly small body size of Triassic invertebrates and larger lung cavities of certain tetrapodial vertebrates might have been adaptations of these animals to withstand oxygen deprivation.

    The preceding diagram emphasizes a possible fate of one biome fragment immediately following the EPE. In this case, the biome fragment is dominated by antagonistic networks of interacting plants and animals compartmentalized around oxygen generating vegetation including shrub lifeboats. Several questions may be posed:

    What were adaptations of land plants available for exploitation by resident insect colonies?

    Were these invertebrate colonies subject to predation by insectivorous amphibians and reptiles?

    How did the activities of dicynodonts, therapsids, and archosaurian dinosaurs (among other vertebrates) affect the evolution, diversification, and dispersal of seed plants and their angiospermization?

    Paleoecological processes in Paleozoic animals and plants were probably not homologous to living systems. Inextricably linked to paleosuccession in Permo-triassic terrestrial ecosystems following disturbance was the feeding behavior of herbivorous and insectivorous amphibians and early reptiles including archosaurians, dicynodonts, and therapsids, among other tetrapods (Tiffney 1992).

    Hypocapnic and hyperoxic fitness landscapes and the angiosperm superradiation. Impacts of hyperoxic oxygen levels in the atmosphere of Permo-carboniferous time are reviewed by Beerling and Berner (2000) and Scott and Glasspool (2006). McElwain et al. (2005) in a review chapter on the effects of atmospheric carbon dioxide on angiosperm origin, radiation, and paleodiversity conclude:

    "It is likely, therefore, that a long-term trend of CO2 decline through the Cretaceous period may have played an extremely important role in the diversification of angiosperms ..."

    The previous phrase is quoted from page 158 of J. C. McElwain, K. J. Willis, and R. Lupia, 2005, Chapter 7. Cretaceous CO2 decline and the radiation and diversification of angiosperms. Pp. 133-165 In: J. R. Ehleringer, T. E. Cerling, and M.-D. Dearing, A History of Atmospheric CO2 and its Effects on Plants, Animals, and Ecosystems. New York: Springer, 530 pp.

    Cretaceous angiosperm diversification might have been triggered by abiotic effects of carbon dioxide decline (hypocapnia) on the physiology of flowering plants as Jennifer McElwain suggests. However, a concomitant rise in atmospheric oxygen content probably also had physiologic effects on insect antagonists of early Aptian angiosperms.

    Coevolutionary arms race. The scientific literature on the coevolutionary arms race ("Darwin's race" title, Pauw et al. 2009) is vast and beyond the scope of this essay. Key references include published work by I. T. Baldwin (1998, among numerous other publications), Cornell et al. (2003), J. Wu and I. T. Baldwin (2010) and Hare (2011).

    A coevolutionary arms race at the molecular level between populations of coevolving flowering plant hosts and insect antagonists is supported by real-time experimental studies. Further, evo-devo studies using biochemically altered probes, genetically-engineered TFs, and microRNAs demonstrate the lability of flowers and insect bodies.

    Insects are unable to manufacture cholesterol ring systems required for the biosynthesis of 20E-ecdysone, an important steroid in endocrine signaling, but must obtain precursor molecules from digested products of animal and plant tissues, which are then assembled by cytochrome P450 enzymes (Truman and Riddiford 2002).

    A recent review of the evolutionary history of the cytochrome P450 protein family is available (Nelson and Werck-Reichhart 2011).

    Certain enzymes of lepidopteran insect guts are able to isomerize biosynthetic precursors of oxylipin phytohormones (Dabrowska et al. 2009). Jasmonic acid oxylipins, which are biosynthesized as a response to mechanostimulation (wounding) of tissues by herbivores (I. T. Baldwin 1998, among others), affect stamen- and pollen tool kits (Devoto and Turner 2003), and induce nectar biosynthesis (Heil 2011). Other VOCs are released by plants when attacked by herbivores (Hare 2011).

    Experimental evidence on the efficacy of arthropod digestive enzymes to alter the molecular structure of ingested phytohormone precursors may have implications toward an understanding of coevolutionary arms race dynamism.

    Plants manufacture many small polypeptides that affect reproductive development (BRICK, CLAVATA3-like/embryo-surrounding [ESR], CLE, cyclotide mini-proteins, and Dresselhaus proteins) or operate in defense and wounding responses (systemins), or in molecular mimicry. Some of these possess insulin-like (e.g. leginsulin) or neuropeptidal (e.g. plant atrial natiuretic peptides) properties that affect insect development and physiology (Germain et al. 2006).

    "Coevolution is a well characterized process that takes place at all biological levels, from ecosystems to molecules."

    The preceding quotation is from page 934 of Juan et al. (2008), High-confidence prediction of global interactomes based on genome-wide coevolutionary networks, Proceedings of the National Academy of Sciences 105(3): 934-939.


    Paleophysiology and Molecular Biology of Tool Kits:

    This chapter considers the paleophysiology of interacting plants and insects and the molecular biology of tool kits. A discussion of phytohormones and defense substances and insect developmental and respiratory proteins, hormones, and neurotransmitters is necessary to understand possible molecular coevolution of insect and seed plant developmental tool kits, animal-plant signaling, and the ongoing coevolutionary arms race (Becerra et al. 2009, Pauw et al. 2009).

    The image to the right is a 20 × 20 cm polyamid thin layer chromatogram representing successive gel filtration column fractions from a mixture of floral flavonoids (x-axis), partitioned in an aqueous solvent mixture (y-axis) by TLC. Development of the thin layer chromatogram and treatment with Natural Products Reagent A reveals a separation of flavonol mono-, di-, and triglycosides, viewed under long wave UV light and captured on ASA 25 kodachrome film. The yellow-orange spot to the right is a standard sample of quercetin-3-O-glucoside, a flavonol monoglycoside.

    Molecular coevolution of insect and seed plant developmental tool kits, CRMs, and GRNs might have underpinned diversification in Paleozoic seed plant lineages and evo-devo of short- [spur-] shoots, including protoflowers. Tool kit studies might help paleobiologists decipher cone and floral novelties and illuminate ecologies of insect mutualisms in extinct seed plant populations.

    Several Bayesian molecular-phylogenetic analyses based on cpDNA, mtDNA, and nuclear genes, and evolutionary studies of the primary structure of phytochrome enzymes and homeodomain proteins of the cone- and floral tool kit, offer clues on the origins of angiosperms and gymnosperms from a plexus of Paleozoic seed plant populations (C. S. P. Foster et al. 2017). The paleobiological and biogeographic implications of these biochemical studies are potentially profound.

    Some of the topics covered here are discussed by the contributing authors to chapters in a book edited by Hemsley and Poole (2004) and papers authored by Feild et al. (2003), Feild et al. (2004), Brodribb et al. (2007), Feild and Arens (2007), Feild et al. (2011 [two papers]), Feild and Brodribb (2013), among others.

    The time in geologic history to consider paleoecophysiology of early angiosperms should be coincident with findings suggested by molecular-phylogenetic inference (Magallón 2010, S. A. Smith et al. 2010, C. S. P. Foster et al. 2017), which is the Permian Period of the late Paleozoic Era and Triassic Period of the early Mesozoic Era.

    Hydraulic morphospace. There are studies in the paleobotanical and physiological literature on the evo-devo of seed plant conducting tissues (Zwieniecki and Boyce 2014) and auxin regulation (references are listed below). Further, auxin-based PINs are deeply conserved. Biochemical studies of extant malvid model organisms detect reverse flows of auxin being drained by leaf midveins. Modeling of auxin gradients in embryonic leaves posits repression of CUC2 TFs by the phytohormone as the basis of leaf-margin sculpting.

    Land plants possess two leaf hydraulic strategies as expressed by their anatomy and morphology (Brodribb et al. 2007). According to Brodribb et al. (pages 1894 and 1895, 2007), the first hydraulic method is to branch the system of veins to deliver water to the site of transpiration (this is the method employed by many flowering plants). The second method seen in some members of the gymnosperm clade is to modify hydraulics by lignifying certain cells of the leaf mesophyll thus channeling water to the stomates.

    Work published by Boyce and Knoll (2002) and Boyce et al. (2009) offers firm footing for the slippery slope of later optimistic conclusions on a supposed rapid rise of angiosperms and their adaptations under early Cretaceous climatic and ecological regimes (Feild and Arens 2005).

    Was the paleophysiology of gigantopterid and gigantopteroid plants as expressed by the presence of two anatomical innovations to maximize leaf hydraulics somehow linked with the success of these plants in arid Permian paleoenvironments?

    "Just as the early steps of marginal meristem evolution were constrained by the scope of developmental possibility, the ultimate range of possible leaf morphologies must have been constrained by available developmental mechanisms."

    This quote is from page 78 of C. K. Boyce and A. H. Knoll (2002), Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28(1): 70-100.

    Angiosperm leaf-vein densities [d] and their placement inside foliar organs [δ] is modeled in morphospace by Boyce, Knoll and coworkers (key references are cited below). This metric may have paleoecological significance but may be underappreciated in Lower Permian leaf compressions (Appendix 3 on page 134, Boyce 2005).

    Studying the physiologically-explicit theoretical morphospace d and δ in samples of permineralized leaves of Permian seed plants might allow useful comparison with Figure 1 of Zwieniecki and Boyce (2014). How does the relation of d to δ seen in the foliar morphospace of Delnortea abbottiae (Mamay et al. 1988) compare with theoretical morphospace of a basal angiosperm or eudicot modeled by Chartier et al. (2014)?

    When "Baileyan trends," are revealed from future analyses of innovative third and fourth order venation patterns, high DV, and complex hydraulic conduit microstructure (including protoxylem, metaxylem, and a 2° vascular cambium) documented in thin-sectioned, permineralized Gnetum-like Permian leaves, does Figure 2 on page 723 of Feild and Brodribb (2013) become more intriguing?

    Natural products, phytohormones, and signaling. This section briefly discusses the high points of a great body of literature in plant physiology, which is devoted to bioactive secondary plant products. Certain natural products are natural insecticides and phytohormones.

    According to Floyd and Bowman's phylogenetic analyses (2007) the auxin, ethylene, and gibberellin metabolic pathways are highly conserved and involve several ancient land plant enzyme systems including AP2/ARFs, DELLAs (TFs of the GRAS family), and ERFs.

    Did Paleozoic seed plants manufacture bioactive plant natural products and phytohormones and signal moulting insect instars residing in oxygenated crevices and leaf bases of massive SAMs?

    Likewise, did phytophagous insect antagonists of Permo-carboniferous and Permo-triassic seed plants signal the homeotic genetic machinery of host plants affecting SAM development and morphology?

    An important clue comes from naturally occurring but fossilized triterpenoids known as oleanone triterpanes (oleananes) and class 1c components of fossilized resins (amber).

    Oleananes, together with ursenes, lupenes, and taraxerenes are important TSBs that belong to a class of Β-amirin triterpenoids (Moldowan and Jacobson 2002). Class 1c resin constituents associated with Mesozoic angiosperm amber are known from 320 million year old (Paleozoic) amber samples (Bray and K. B. Anderson 2009).

    Do TSBs provide indirect evidence that certain Paleozoic seed plants once manufactured steroids and terpenoids?

    Were foliar organs, stems, and seeds of Vojnovskyales and gigantopteroid seed plants Delnortea, Evolsonia, and Zeilleriopteris, sources of angiosperm-like class 1c components of Carboniferous amber deposits?

    Natural products. Plants manufacture thousands of natural plant substances. The main groups of biologically active micromolecules are alkaloids (including betalains), amino acids and small polypeptides, anthocyanins and flavonoids (B. A. Bohm 1998), polyacetylenes (Lersten and Curtis 1989), steroids (Suzuki et al. 2006), terpenoids (Cheng et al. 2007, S. Lee and Chappell 2008), and lipids and waxes, which are necessary in plant protection and signaling.

    The study of anthocyanins and other flavonoids as chemotaxonomic markers in plants dominated the literature in systematic botany for almost two decades (B. A. Bohm 1998). Flavonol aglycones are biosynthesized by the flavonol synthase enzyme (Owens et al. 2008).

    A few members of the cytochrome P450 gene family are implicated in flavonoid metabolism together with R2R3 MYB TFs (Rosinski and Atchley 1998, Boudet 2007, Nelson and Werck-Reichhart 2011). The MYB-related TF MIXTA is important in epidermal cell patterning of flower petals that contain UV-absorbing flavonoids compounds visualized by insect pollinators (Baumann et al. 2007).

    Some flavonoids are antioxidants that inhibit auxin efflux carriers. Many flavonoids are implicated in hormone signaling, plant defense, and regulation of gene expression (Koes et al. 2005, Owens et al. 2008).

    Biosynthesis of chalcone synthetase is affected by the hormone gibberellic acid in some flowering plants. Chalcone synthetase manufactures many classes of flavonoids involved as antioxidants, bee-violet attractants in flowers such as Rudbeckia hirta, and as UV shields.

    Steroids are well-known natural products manufactured by plants for use in defense and signaling (Truman and Riddiford 2002).

    Phytohormones. Perception of environmental stimuli by coevolving insects and plants and transduction of signals back and forth to insect antagonist and host plant genomes were probably hallmarks of shrub lifeboat compartments in Paleozoic times. Plant and insect physiologists employing extant organisms as research subjects publish data each year that indirectly supports this hypothesis.

    Coevolution between developmental tool kits of insect herbivores and host seed plants might require that communication take place at all levels from interacting populations to molecular systems. The plant cytoskeleton, touch receptors, and phytohormones (Bari and Jones 2009); and insect secretions and sensory receptors may play key roles in communication between plant and animal and vice-versa.

    Are herbivorous insects capable of inducing morphological changes in the plants they eat or use for shelter and rearing of offspring?

    Can insect derived cues affect geometric patterns in SAMs including phyllotaxes?

    Auxins. Auxin down-regulates Class I KNOX genes in developing SAMs of extant flowering plant experimental systems permitting gibberellic acid activity in leaf primordia and promoting growth (Weiss and Ori 2007). Membrane proteins known as efflux and influx carriers control auxin movement from cell to cell in the SAM.

    Phyllotaxis is apparently regulated by the differential translocation of auxin phytohormones in SAMs in at least some extant species (R. S. Smith et al. 2006). Auxin biosynthesis catalyzed by TAA oxidase mediates cross talk with ethylene in etiolated Arabidopsis seedlings. Auxin gradients in floral meristems affect tissue patterning and the expression of YUCCA genes (Stepanova et al. 2008).

    Auxin is "a major regulator of organogenesis" (title, Bohn-Courseau 2010).

    Further, ARF genes encode cis-acting ARF proteins that bind to auxin responsive genes (Busov et al. 2008, Delker et al. 2008, R. S. Smith 2008). Auxin response factors figure prominently in the regulation of leaf morphology and belong to the ancestral developmental tool kit of land plants (Floyd and Bowman 2007).

    The MIKC-type MADS-box TF SEP3 interacts with ARF and other elements of several hormone signaling cascades in Arabidopsis (Kaufmann et al. 2009).

    Clues on the possible existence of polar auxin flow in woody stems have been uncovered in comparative anatomical studies of a 375 million-year-old fossilized progymnosperm known as Archaeopteris and modern conifers (Rothwell and Lev-Yadun 2005). The fossil record reveals that auxin regulation of secondary growth was a conserved physiologic process (Rothwell et al. 2008).

    Based on the phylogenetic analysis of Class I KNOX genes (Floyd and Bowman 2007), paleobotanical evidence of polar auxin flow in Devonian plant fossils (Rothwell and Lev-Yadun 2005), and deep conservation in terpenoid enzymology (S. Lee and Chappell 2008) needed to biosynthesize diterpenes including gibberellic acid, it is not unreasonable to add auxins and gibberellins to the regulatory tool kit of early diverging land plants.

    Brassinosteroids. Brassinolides (BRs), are structurally similar to 20E-ecdysone, a potent insect steroid moulting hormone. Brassinolides are also implicated in endogenous ethylene production (J. Li and Chory 1999, Thummel and Chory 2002, Zullo and Adam 2002).

    A recent review of brassinolide metabolism in plants is available (T.-W. Kim and Z.-Y. Wang 2010).

    Cytokinins. Zeatin and other cytokinins are modified nucleotide phytohormones that induce the expression of WUS genes in CLAV pathways in developing SAMs (Gordon et al. 2009), among other profound regulatory effects on plant growth and development.

    Ethylene. Ethylene is a gaseous hormone with profound effects on plant growth, development, and responses to biotic stress including herbivory. A family of five membrane bound receptor proteins perceives ethylene molecules from the external environment. The ethylene signaling cascade crosstalks with the biosynthetic machinery of most other phytohormones including abscisic acid (ABA), auxins, BRs, and gibberellins (Y. F. Chen et al. 2005).

    For example, ethylene adversely affects gibberellic acid by activating DELLA repressing proteins. In turn, DELLAs repress the floral integrator genes LFY and SOC1 resulting in delayed flowering in Arabidopsis (Achard et al. 2007). Ethylene and gibberellic acid (GA) biosynthesis in plants is enhanced by insect neurotransmitters such as catecholamines (Schultz 2002).

    Gibberellins. Key diterpenoid hormones of the developmental tool kit of extant plants include gibberellins (Weiss and Ori 2007). The effects of nuclear regulatory growth repressing DELLA proteins that belong to the GRAS family of transcriptional regulators are relieved by GA via the ubiquitin 26S proteasome biosynthetic pathway (Yu et al. 2004, Axtell and Bartel 2005, Lu et al. 2005, Jiang and Fu 2007, Weiss and Ori 2007, Gao et al. 2008, Hartweck 2008).

    Studies of the malvid Arabidopsis provide evidence that GA controls the development and morphology of trichomes on leaves, flowers, and shoots by de-repressing DELLAs (Gan et al. 2007). Whether the mechanism of GA action on the negative effects of nuclear regulatory growth repressing DELLA proteins on glandular hair and trichome development in other seed plants is the same as Arabidopsis is not known. Trichomes and glandular hairs play an important role in defense against herbivores.

    The DELLA TFs restrain plant growth and development under adverse environmental conditions in extant flowering plants, and repress the accumulation of reactive oxygen species (Achard et al. 2008).

    Did nuclear repressing proteins play a role in the diversification and adaptive radiation of flowering plants in fluctuating paleoclimates?

    The ubiquitin 26S proteasome pathway is employed by animals and plants to control levels of- and degrade regulatory proteins such as gibberellin-sensitive plant DELLAs and certain ethylene regulatory enzymes (Y. F. Chen et al. 2005).

    Several other plant hormones including ABA, auxin, cytokinins, and ethylene, interact with GA. Some of hormone interactions with GA are negative and reciprocal. For example, when rice is grown under hypoxic conditions, culm and internode elongation requires both ethylene and GA. Knotted 1 homeodomain proteins induce the production of cytokinins in SAMs that in turn inhibit the biosynthesis of GA (Weiss and Ori 2007).

    Oxylipins. Jasmonic acid (JA) and related esters belong to the oxylipin family of molecules (Wasternack 2007, Chico et al. 2008). Jasmonates are hormones implicated in conserved but specific biochemical- and plant-morphogenetic effects (I. T. Baldwin 1998, Biondi et al. 2001, Balbi and Devoto 2008, Katsir et al. 2008).

    Specific effects include the ability of oxylipins to reprogram expression of JA-inducible genes (Pauwels et al. 2009). Jasmonates, biosynthesized as a response to mechanostimulation (wounding) of tissues by herbivores (I. T. Baldwin 1998) orchestrate plant defense (Ballaré 2011) and affect development of stamens and pollen (Devoto and Turner 2003).

    Further, JA induces nectar formation in tissues of extant seed plants (Heil 2011).

    Salicylic acid. Salicylates (SAs) is a well known natural signaling molecule that a play key role in activating genes for defense and integrating WRKY transcription factors during plant responses to herbivory and wounding (Wasternack 2007, Balbi and Devoto 2008, Blanco et al. 2009).

    Simple gases. Nitric oxide (NO) is a gas with profound mediating effects on phytohormone cross talk, development of flowers and pollen tubes, defense, and signaling (Perazzolli et al. 2006, Besson-Bard et al. 2008 [two papers], Palavan-Unsal and Arisan 2009, Gupta et al. 2011). Nitric oxide activates protein kinase G (PKG) in mammals. Both molecules are important to survival of insects in artificial hypoxic environments (Wingrove and O'Farrell 1999, Hoback and Stanley 2001).

    Interestingly, NO also binds to hemoglobins, a class of oxygen-binding enzymes found in plants (Perazzolli et al. 2006), and vertebrates and invertebrates including certain species of the insect orders Coleoptera, Diptera, Hemiptera, Hymenoptera, and Lepidoptera (Van Holde et al. 2001, Burmester and Hankein 2007). Further, both NO and PKG enhance the survival of Drosophila larvae when deprived of oxygen in the laboratory (Wingrove and O'Farrell 1999).

    Were Paleozoic insect antagonists attracted to potential NO emissions by host plants (where NO possibly played a role in ameliorating the detrimental effects of local hypoxia on egg and larval development)?

    Carbon dioxide is also a gaseous signaling molecule, which is perceived by the olfactory receptors of blood sucking, meat eating, and herbivorous insects. At certain concentrations CO2 becomes an odor to Manduca moths (Goyret et al. 2008).

    How did hypercapnic paleoenvironments following the GuCCE, EPE, TrCCE, and BaCCE affect molecular evolution of insect olfactory receptor proteins and coevolution of stem group angiosperms and their pollinators?

    Strigolactones. Carotenoid-derived hormones are implicated in negative repression of axillary bud growth and the evo-devo of short- (spur-) shoots of seed plants. These are strigolactones (Dun et al. 2009, Rameau 2010, Koltai et al. 2012, Koltai 2013). Potential biological activity of strigolactones in insect antagonist and host plant systems should be researched.

    Evolution of strigolactone and auxin polarity networks (PINs) were important in the evo-devo of the seed plant short- (spur-) shoot, which was a critical milestone in the evolution of cones and protoflowers during Late Paleozoic Era.

    Did mycorrhizal fungi of Paleozoic terrestrial and transitional landscapes interact with seed plants and their non-seed plant congeners to supply growing stems and roots with strigolactone hormones?

    Signaling by herbivory and wounding. The mechanism of action of hormone signals in SAMs is an active area of research in plant physiology. Volatile organic compounds are often released by plants when attacked by herbivores (Hare 2011, among others).

    Through a process termed signal transduction, biochemical signals originating in the insect exoskeleton manipulate and control the genetic machinery needed for orderly, or disorderly growth and expansion of shoots and other organs of the plant (Pandey et al. 2008).

    Molecular studies on the herbivorous sphingid moth, Manduca sexta by Ian Baldwin and students, demonstrate several molecular interactions between the insect and the wild tobacco plant host Nicotiana attenuata (Solanales, Asteranae) that potentially affect the ecology and development of both organisms. The activities of the specialized insect herbivore induces "... a dramatic ethylene release, a jasmonate burst, and a suppression of nicotine accumulation ..." in simulations of herbivory on the host plant (abstract, Winz and I. T. Baldwin 2001). Further, plant mRNAs accumulate "... in response to insect-derived cues" (title, Schittko et al. 2001).

    Gall forming insects inject plant cells with modified transfer RNAs (tRNAs), which are in fact, cytokinins. Injected cytokinins biosynthesized by phloem feeding insects cause rapid differentiation and disorderly growth in plant tissues resulting in gall formation (Schultz 2002).

    Small CSE polypeptides biosynthesized in the esophageal glands of parasitic nematodes when injected through feeding stylet into plant cells, affect development of floral meristems (Germain et al. 2006). The historically elusive flowering hormone florigen is now known to be a small protein that is transported through the phloem of angiosperms (Shalit et al. 2009).

    Do hormones secreted by parasitic invertebrates or insect instars and larvae upregulate or repress homeotic genes in host seed plant SAMs?

    Possibly, at least based on a recent review by J. Wu and I. T. Baldwin (2010).

    Plant light receptors. Phytochrome, an enzymatic light receptor implicated in several physiological processes in plants, including flowering, affects regulation of MIKC-type MADS-box genes. Issue Number 12 of Volume 58 (2007) of the Journal of Experimental Botany is devoted to photomorphogenesis.

    Further discussion of photoreceptors in plants is beyond the scope of this essay although phytochrome genes figure prominently in early attempts to unravel angiosperm phylogeny (Mathews and M. J. Donoghue 1999).

    Mathews et al. (2010) present new data and valuable insight on the timing of major events in flowering plant evolution based on amino acid sequences of the phytochrome enzyme.

    Insect hexamerins and hemocyanins. Hemocyanins (Hcs) of invertebrate circulatory systems evolved during the early Paleozoic as a class of gas-binding, copper-containing enzymes needed in respiration (Burmester and Hankein 2007, Pick et al. 2009). Iron-containing hemoglobins (Hgs) of animals also evolved and diversified during this time (Burmester et al. 1998, Van Holde et al. 2001, Burmester 2004).

    Molecular evolution of copperless insect storage Hxs from Hcs of invertebrate copper containing enzymes may be linked with the late Devonian/early Carboniferous ice-house cooling of the Earth, accompanied by a drop in oxygen levels to 13% (Berner and Kothavala 2001, Ward et al. 2006). Protein storage macromolecules of the Hc family of enzymes are termed Hxs (Burmester 2001, Moreira et al. 2004).

    Thorsten Burmester and coworkers (1998) describe the molecular evolution of Hx hemolymph protein subunits from the Hc family of enzymes in two important reviews (Burmester 2001, Burmester et al. 2006). Hexamerins are moulting storage proteins composed of multimeric polypeptide chains. Each Hx enzyme subunit has a molecular weight of about 80,000.

    Hemocyanins including Hxs are critical to developing and respiring entognathous hexapods and true (ectognathous) insects, being necessary for instar development and successive moults (Hagner-Holler et al. 2004, Pick et al. 2009). Larvae digest Hx storage proteins to release certain amino acids required for development (Moreira et al. 2004).

    Hexamerins are also implicated as silencers of JH signaling in neotenous castes of hemimetabolous termites (X. Zhou et al. 2006, X. Zhou et al. 2007) and caste polyphenism in holometabolous wasps (J. H. Hunt et al. 2007).

    Moulting food storage proteins, homeotic selector genes including Hox genes, zygotic genes, field specific selector genes, compartment selector genes, cell-type-specific selector genes, segment polarity genes, and controlling factors behind the cessation of insect growth (brain neurosecretory PTTH, JH, and ecdysone steroids) comprise key elements of the developmental tool kit of insects (Truman and Riddiford 2002, S. B. Carroll et al. 2005).

    Trans-acting chromatin proteins and cis-acting TFs of eukaryotic genomes respond to oxygen levels in controlled environments. For example, lowering oxygen concentration in controlled environments affects levels of nonubiquitinated proteins and activates hypoxia-responsive genomic DNA elements (HREs) (Flück et al. 2007). Further, "hypoxia regulated gene expression very likely reflects an ancient adaptive trait that was established in primitive eukaryotes in response to alterations in levels of oxygen" (page 529, Flück et al. 2007).

    The below graphic is a crude plot of changing oxygen levels in Earth's atmosphere over geologic time based on GEOCARB III (Berner and Kothavala 2001), and other work (Beerling and Berner 2002, Huey and Ward 2005, Ward et al. 2006). I superimposed an evolutionary tree showing cladogenesis of insect Hxs from invertebrate Hcs, which is based on the most recent molecular clock estimates by Hagner-Holler et al. (2007) and morphological data. In addition, I plotted three of the four insect herbivore expansion phases outlined by Labandeira (2006) on the graph.


    The preceding plot is redrawn from Figure 6 on page 1072 of Hagner-Holler et al. (2007), Diversity of stonefly hexamerins and implication for the evolution of insect storage proteins, Insect Biochemistry and Molecular Biology 37: 1064-1074, with additional data added from GEOCARB III (Berner and Kothavala 2001), GEOCARBSULF (Berner 2006), and Labandeira (2006).

    Three bursts of molecular evolution of insect Hxs are apparent from the Hagner-Holler et al. data (2007). The first of the Hx molecular evolutionary radiations roughly corresponds with the DeCARB, 360 to 320 MYA (Hagner-Holler et al. 2007) and the initiation of Insect Herbivore Expansion Phase 2 (Labandeira 2006). During hypoxic intervals of the DeCARB seven clades of Hxs diverge from primitive Plecoptera (stoneflies) leading to many derived hemimetabolous and holometabolous insect orders (Hagner-Holler et al. 2007).

    A second burst of insect Hx evolution occurs prior to the GuCCE and a decline in atmospheric oxygen levels from 31% to 12% (Berner and Kothavala 2001, Ward et al. 2006). During this interval, Hxs diverged into clades leading to the Coleoptera (beetles and weevils), Hymenoptera (bees and wasps), and Diptera (flies), and certain Lepidoptera (butterflies and moths). This interval of Hx diversification corresponds with Insect Herbivore Expansion Phase 2 (Labandeira 2006).

    The point of divergence between the Hx class belonging to beetles and those Hxs belonging to bees and wasps roughly coincides with the second burst of Hx evolution.

    Was the second explosion of molecular evolution of insect Hx protein subunits driven by developing hypoxia following the GuCCE of the late Permian, or did diversification occur before the GuCCE as the data suggest?

    Dipteran Hxs diverged roughly about the same time as oxygen levels in Earth's atmosphere declined to 12%. The third burst of Hx evolution leading to blattarians (cockroaches) and Isoptera (termites) occurs at a point in geologic time coincident with the TrCCE (Beerling and Berner 2002).

    Rough estimates of molecular divergence times of insect Hxs published by Hagner-Holler et al. (2007) could be refined to include GEOCARB III data and calibrated with fossils.

    A more detailed synthesis of invertebrate gene duplications and later molecular evolution of Hxs and vitellogenins in populations of coevolving insect antagonists and Permo-triassic seed plants is possible. Precise molecular phylogenetic and isotope studies are needed to implicate global hypoxia as an underlying selective force in the evolution of insect Hxs. Insect Hgs remain relatively unstudied in this context. Several questions come to mind:

    At the same time that Hx molecules were probably evolving in insect populations and colonies of shrub lifeboats, trampling and secreting insect antagonists might have sent signals to the genetic machinery of SAMs of host plants. Signals, secretions, and genetic parasites originating in the bodies of phytophagous insects could have had affected developmentally plastic SAM tool kits of Permo-triassic seed plant hosts.

    Insect sensing and hormone signaling. Arthropods manufacture several classes of hormones that regulate development and together with anatomically modified appendages, they facilitate communication among individuals, within castes of social insects, or possibly with plant hosts.

    Some of the hormones produced by insects which are active in signaling and sensing include ecdysone steroids, epoxide methyl esters of sesquiterpenoids, peptides and polypeptides, and pheromones (Robertson and Wanner 2006).

    Insect olfactory and gustatory chemoreceptors (Abdel-latief 2007) and innervated bristles are of potential interest with respect to plant-to-insect, insect-to-insect, and insect-to-plant communication by biomolecules and thigmo.

    A fossilized brain from a Cambrian stem group arthropod is evidence of the early existence of an extremely conserved and sophisticated olfactory and visual sensory system in these animals ... Did evo-devo of insect eyes, mushroom bodies, neuropils, and trichromatic vision predate late Paleozoic pollen phytophagy and flying predatory behaviors of paleodictyopterans and wasps?

    The right-hand image is reproduced from Figure 1 on page 258 of X. Ma et al. (2012), "Fuxianhuia protensa from the Chengjiang Lagerstätte. Dorsal view of complete specimen, YKLP 11321. A1, antenna; Ab, abdomen; Es, eye stalk; Ey, eye; Hs, head shield; Oc, optic capsule; Th, thorax. Scale bar, 1 cm." Figure 1 is licensed and reprinted by permission from Macmillan Publishers Ltd and the journal Nature, copyright ©2012.

    Ecologists should compare this paleobiological study with earlier work by Chittka (1996), Briscoe and Chittka (2001), and Chittka et al. (2001). Implications of these three studies toward an understanding of the deep time evolution of pollination mutualisms and color and scent perception by species of the "Big Five" holometabolous insect orders and late Paleozoic seed plants, when taking into account the paleobiology of the arthropod brain, are absolutely profound.

    "It is likely that trichromacy existed prior to the advent of angiosperm flowers" (page 138, Chittka 1996).

    Nicholas Strausfeld (2009), and Xiaoya Ma et al. (2012), Edgecombe et al. (2015), and Xiaoya Ma et al. (2015), review the deeply conserved evo-devo of arthropod mushroom bodies in the biochemical and phylogenetic context. Mushroom bodies are paedomorphic neuropils of insects and firebrats that function in control of behavior, and in olfactory perception (Strausfeld et al. 1998, S. M. Farris 2005, S. M. Farris and Schulmeister 2011).

    Olfactory organs and chemoreceptors (Ray et al. 2008) allow certain insects to sense minute concentrations of pheromones, NO, carbon dioxide, and other VOCs in the air. Beetles exhibit many adaptations to smell and taste and this is reflected in considerable anatomical, biochemical, and morphological diversification in sensillae of antennae, legs, mouthparts, and wings (Abdel-latief 2007).

    The scanning electron micrograph to the left is the anterior front part of the head of Haptoncus tahktajanii (Nitidulidae, Coleoptera), the cucujiform phytophagous associate of the primitive magnoliid flowering plant Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae). Some of the gustatory, olfactory, and visual sensory organs of the nitidulid beetle are visible including antennae, sensillae, compound eyes, mandibles, maxillae, and labia.

    Nitidulids were collected by the author from flowers clipped from the canopy of Degeneria trees at the Mount Naitaradamu Study Area, Viti Levu, Fiji Islands in 1986. The National Geographic Society is acknowledged for providing research funding for this work. The photograph is by Al Soeldner of the Oregon State University Electron Microscope Laboratory, × 100.

    Certain insect hormones exhibit bioactivity in plants, and some natural plant substances are bioactive agents in insects. Many bioactive substances were probably integral components of the early-diverging arthropod developmental tool kit.

    To the right is a scanning electron micrograph (SEM) of the epidermis of a leaf-like staminode of Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae). Epidermal cells and two guard cells surrounding a stomate are visible. The anatomy and development of the stomatal pore of Degeneria vitiensis is probably unstudied.

    Staminodes of Degeneria vitiensis are covered with bright-yellow, oily exudate and emit VOCs including fragrant terpenes and acetate esters. Fragrance analyses and the ecological studies of pollination in both species of Degeneria are needed.

    The scanning electron micrograph is from a dissected and fixed floral organ collected in a Degeneria tree canopy at Mount Naitaradamu, Fiji (J. M. Miller 1989).

    What can the paleophysiology of seed plant conducting tissues and the fragrance-emitting stomatal pore (right-hand SEM) tell us about the evolution of magnoliids and coevolution with insect antagonists?

    Genomic analyses and indirect proteome computational modeling reveal numerous insect specific olfactory proteins implying a rich and conserved evolutionary history (G. Zhang et al. 2007).

    Several neurosecretory hormones play an important part in mechanisms that regulate cell division and growth including insulin-like peptides (Drosophila insulin-like DILPs and bombyxins), chitenase-derived imaginal disk factor proteins, the steroid hormone ecdysone, local autocrine and paracrine TFs, and PTTH (Nijhout 2003).

    Juvenile hormone biosynthesized in the corpora allata of the insect brain is a sesquiterpenoid epoxide methyl ester (Hartfelder 2000). Interestingly, many naturally-occurring plant sesquiterpene esters and lactones are bioactive and exhibit insecticidal properties. Juvenile hormone and its homologs are intertwined with vitellogenesis (Hartfelder 2000), regulation of moult cycles (Truman and Riddiford 2002), and caste development and behavior in social Hymenoptera (Guidugli et al. 2005).

    Vitellogenins play a central role in insect female reproductive development. High levels of vitellogenin inhibit the production of JH. It is widely believed that such interactions are highly conserved ancient features of female insect physiology (Guidugli et al. 2005).

    Ecdysone steroids play a central role in regulation of growth and development of moulting insects comprising the Holometabola (Grimaldi and Engel 2005). In Manduca sexta (Lepidoptera), PTTH is released by the insect brain to initiate a moult. In turn, PTTH triggers the ecdysone cascade and the larva develops into the pupa, and so forth (Truman and Riddiford 2002).

    Are natural plant substances including BRs and sesquiterpene lactones capable of regulating the expression of insect Hox genes including Ubx and pb?

    Based on Drosophila melanogaster work 20E-ecdysone signals are received by cis-acting EcR isoforms. The functional EcR is a heterodimer made-up of usp and EcR. Further, the ligand binding domains (LBDs) of EcR isoforms is unusually divergent in holometabolous clades of insects (Truman and Riddiford 2002, Watanabe et al. 2010).

    Interestingly, the "sudden divergence" of dipteran and lepidopteran LBDs of the EcR (page 847, Truman and Riddiford 2002) coincides with the supposed angiosperm-gymnosperm split, roughly 300 MYA, seen in evolution of MIKC-type MADS-box TFs and LFY protein CRMs.

    Is timing of divergence of EcR isoforms, MIKC-type MADS-box TFs, Engraled protein, and LFY enzyme coincidental, or is this an example of possible molecular coevolution of certain elements of insect and seed plant developmental tool kits leading to the origin of flowers and holometabolous insect body plan novelties of butterflies, moths, and flies?

    Can we pin-point divergences of insect- and angiosperm tool kit components using fossil calibrated molecular phylogenies? Yes.

    Helix-turn-helix (HTH) proteins. There are four major groups of deeply-conserved regulatory proteins present in most forms of life that share a similar conserved amino acid sequence in the DNA-binding domain: helix-loop-helix, HTH, leucine zipper, and zinc finger (Rosinsky and Atchley 1999, S. B. Carroll et al. 2005, Feller et al. 2011, among others).

    Helix-turn-helix proteins mediate interactions between substrates and the enzymes that bind to DNA, affect cell division, control circadian rhythms, transport and organize DNA, and regulate transcription in bacteria, algae, animals, fungi, and plants. There are several main classes of HTH proteins and many hundreds of structural forms found in most forms of life (Aravind et al. 2005).

    Enzymes with a helix-loop-helix and/or HTH DNA-binding motif consisting of a trihelical bundle are termed homeodomain proteins (Aravind et al. 2005). The HTH DNA-binding motif is an important component of developmental CRMs which are critical in insect and plant body patterning (S. B. Carroll et al. 2005, Glover 2014).

    Homeodomain proteins are important in animal, fungal, and plant development (Bharathan et al. 1997, Rosinsky and Atchley 1999, Aravind et al. 2005, Baumann et al. 2007). Certain MYB proteins also possess an HTH structure in the DNA-binding homeodomain (Dubos et al. 2010, Feller et al. 2011, among others).

    Phylogenetic analyses suggest a possible close evolutionary relationship in deep time between several classes of animal, fungal, and plant homeodomain proteins (Bharathan et al. 1997). Two groups of KNOX homeodomain proteins exist in angiosperms based on phylogenetic studies (Bharathan et al. 1999). These are the BEL1-like and KNOX homeodomain proteins that belong to the TALE family of TFs (Hamant and Pautot 2010).

    It may be important to consider the molecular paleobiology and paleophysiology of homeodomain proteins in developing explicit hypotheses on a possible coevolutionary origin of angiosperms and certain holometabolous insects.

    Rosinsky and Atchley suggested on page 306 of a 1999 review paper that "the evolution of the HTH family of proteins has been marked by strong evolutionary forces maintaining a specific secondary structure (the HTH structure) and a single function (sequence specific DNA binding)." The specific primary and secondary structures being discussed by these authors were the two alpha helices of the HTH DNA-binding motif, and primary structural amino acid residue 390 (R390), which is lysine.

    Fascinating insight from biochemical research of WUSCHEL homeodomain protein TFs and the foliar tool kit, including knockout studies of the WOX homeobox, continue to surface in the literature (Nardmann and Werr 2013, J. M. Alvarez et al. 2015).

    "The similarities in expression patterns in needle primordia between PaWOX3 and its orthologues in the gymnosperms Ginkgo biloba, Gnetum gnemon and Pinus sylvestris (Nardmann and Werr, 2013), suggest that the expression pattern and functions of PaWOX3-related genes might be shared between all gymnosperms."

    Published research findings by J. M. Alvarez et al. (2015) illuminate details of a "largely conserved" process homology among foliar tool kits of cycads, ginkgos, gnetophytes, malvids, and pinids.

    "Thus, the phenotypic consequences of PaWOX3 knockdown in Norway spruce resemble those observed in mutants for the orthologous genes in angiosperms. Both in Norway spruce and angiosperm models, needles/leaves and cotyledons are narrower and curled or folded, and lateral margin development is impaired, indicating that WOX3 is instrumental for lateral margin cell growth and development."

    The two preceding quotations are from J. M. Alvarez, J. Sohlberg, P. Engström, Tianqing Zhu, M. Englund, P. N. Moschou, and S. von Arnold (2015), The WUSCHEL-RELATED HOMEOBOX 3 gene PaWOX3 regulates lateral organ formation in Norway spruce. New Phytologist 208(4): 1078–1088.

    Clues may be found in biochemical studies by Bilsborough et al. (2011) of the extant malvid model species, Arabidopsis thaliana. Reverse flows of auxin being drained by leaf midveins have been detected in living foliar organs, and bidirectional hormone flow affects the shape of developing leaves (see Figure 5 on page 3427, Bilsborough et al. 2011). Modeling of auxin gradients in embryonic leaves posits repression of CUC2 TFs by the phytohormone auxin as the basis of leaf-margin sculpting (Bilsborough et al. 2011).

    Were these deeply-conserved tool kit interactions between auxin, homeodomain protein TFs (CUC2, Class III HD-Zips, Knotted 1, MYB, WUSCHEL), and PIN proteins, present in foliar organs and shoots of Paleozoic seed plants? Possibly, but more work is needed to answer these and other related questions.

    Despite compatibility with the Fading Borders Model of floral regulation reviewed by Chanderbali et al. (2016), the hypothesis proposed by Warner et al. (page 3571, 2009) neglects to account for a possible role of MYB TFs in environmental control of perianth pigmentation and evolution.

    Hamès et al. (2008) deduced the primary and secondary structure of two alpha helices of the HTH DNA-binding motif of LFY protein.

    "The acquisition R390 [of LEAFY protein] might therefore have been important for flower evolution."

    The previous statement is quoted from page 2635 of C. Hamès, D. Ptchelkine, C. Grimm, E. Thevenon, E. Moyroud, F. Gérard, J.-L. Martiel, R. Benlloch, F. Parcy, and C. W. Müller (2008), Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. The EMBO Journal 27: 2628-2637. The phrase in brackets [] is mine.

    Are there structural and functional relationships between the homeodomain proteins of insect antagonists (e.g. Engraled [en]) and homeodomain proteins (Class III HD-Zip, KNOX, R2R3 MYB, WUSCHEL) of seed plant hosts, which might have a bearing on a coevolutionary origin of hexapods and angiosperms?

    Plant biology of cone development and flowering. Since the pioneering work of Coen and Meyerowitz (1991) tremendous advances have been made in understanding the physiology and molecular biology of flowering within an evo-devo context (Endress 2006, Irish 2006, D. E. Soltis et al., eds. 2006, Whitney and Glover 2007, Hileman and Irish 2009, P. S. Soltis et al. 2009, Specht and Bartlett 2009, Glover 2014).

    Regulation of flowering is reviewed by Specht and Bartlett (2009), Chanderbali et al. (2010), Melzer et al. (2010), Rudall and Bateman (2010), D. W. Taylor (2010), Dornelas et al. (2011), Rudall et al. (2011), Glover (2014), Glover et al. (2015), Specht and Howarth (2015), and Becker (2016).

    A compilation of reviews on the biochemistry and genetics of cones and flowers appears in Issue 1 of Volume 21 of Seminars in Cell and Developmental Biology (2010).

    Induction of flowering from vegetative SAMs and changes in accessory meristem identity occurs four different ways (Glover 2014):

  • induction of flowering by perception of photoperiodism
  • meristem determination and flower formation by DELLA de-repression, the ubiquitin 26S proteasome pathway, and GA
  • autonomous flowering
  • vernalization
  • Floricaula and LFY genes and the DNA-binding HTH proteins they encode i.e. Floricaula and Leafy enzymes, are main integrators of the biosynthetic and developmental pathway that leads to organ identity and formation of reproductive modules in the fertile SAMs of seed plants (Becker et al. 2000, Irish 2006, Jack 2004, Theißen and Kaufmann 2006, Theißen and Melzer 2007, Specht and Bartlett 2009, Gramzow et al. 2010, Zobell et al. 2010), but FLC, PAN (a bZIP protein), SEP3 (a MIKC-type MADS-box protein), UFO, and Wuschel [WUS] (a homeodomain protein} are also possibly involved as cofactors and regulators (Vásquez-Lobo et al. 2007, Nardmann et al. 2009, Liu and Mara 2010, Deng et al. 2011, Nardmann and T. Werr 2013).

  • Response of the SAM to environmental (light, temperature, touch) and endogenous/exogenous biochemical signals (hormones produced by the insect and the plant, polypeptides, and microRNAs) that switches the meristem from vegetative to reproductive
  • Integration of signals leading to activation of SAM identity genes
  • Meristem identity genes activate reproductive organ identity genes in specific regions of the expanding SAM
  • Reproductive identity genes activate organ building genes of the growing SAM
  • Development of fertile organs (bract and cone scale complexes, carpels, perianth parts, sporophylls) following the integration and induction of MIKC-type MADS-box genes in bisexual strobili may be divided into four sequential steps:

    "Our morphological and gene expression analyses give support to the hypothesis that the modern cone is a complex structure, and the ovuliferous scale the result of reductions and compactions of an ovule-bearing axillary short shoot in cones of Paleozoic conifers" (page 261, Carlsbecker et al. 2013).

    A commentary (Ruelens and Geuten 2013) on this study by Peter Engström and coworkers, discusses spur shoot-like ovuliferous organ development in Picea abies var. acrocona mutants within the context of Permian Pseudovoltzia liebeana and Thuringiostrobus florinii cone anatomy and expression patterns of angiosperm LFY and the SEP (MIKC-type MADS-box E) gene family.

    "... the phylogeny of gymnosperms and their relationship to flowering plants remains debated as morphological and molecular analyses contradict each other on key relationships" (page 10, Ruelens and Geuten 2013).

    Ferns and fern allies, might carry out development of fertile structures differently (Hasebe et al. 1998, Himi et al. 2001). Floricaula and LFY genes of the fern model organism Ceratopteris "do not directly induce MADS-box genes" (page 1205, Shindo et al. 2001).

    Induction of seed plant reproductive structures in the four whorls of monopodial SAMs is under genetic control (Irish 2006, Specht and Bartlett 2009). While the biochemistry and development of expanding cells of SAMs and accessory fertile meristems is just barely understood (and only in a few extant seed plant species), at least two working models on the molecular mechanism of floral control and evolution, either the ABCDE model (Ditta et al. 2004) or floral quartet model (Theißen 2001) have been proposed.

    Evidence of the involvement of floral quartets in floral development is supported by in vitro experiments using MIKC-type MADS-box B and E proteins (Melzer and Theißen 2009, Melzer et al. 2009, Melzer et al. 2014).

    "Our data suggest that the interactions governing flower development in core eudicots were already established at the base of extant angiosperms and remained highly conserved since then. Specifically, our results indicate that the heterodimerization between DEF-like and GLO-like proteins was already present in the [most common recent ancestor] MRCA of extant angiosperms and was virtually never rewired" (page 1438, Discussion, Conservation of the MADS-domain protein interaction pattern during angiosperm evolution, Melzer et al. 2014).

    Leafy and the biochemical logic behind FLO, LFY, and NLY DNA-binding HTH proteins figure prominently in papers that explore the use of evo-devo approaches in understanding gymnosperm phylogeny, the origin of angiosperms, and floral origins (Frohlich and Parker 2000, Shindo et al. 2001, Albert et al. 2002, Frohlich 2003, Baum and Hileman 2006, Frohlich 2006, Theißen and Melzer 2007, Vásquez-Lobo et al. 2007, Rudall et al. 2009).

    Vásquez-Lobo et al. (2007), in an elegant study of FLO/LFY orthologs in Picea (Coniferales), Podocarpus (Podocarpales), and Taxus (Taxales), while employing ultrasensitive radioactive probes and histochemical methods, clearly demonstrate in situ expression of FLO/LFY gene transcripts in all the organs of female fertile SAMs. These findings, when taken together with similar studies by Shindo et al. (2001) on Gnetum parvifolium (Gnetales), disprove MMT.

    The ancestral function of LFY, paralogous NLY and various orthologs, and the putative arthropod and seed plant biological activity of the DNA-binding HTH proteins they encode remain as enigmatic as ever (see the later subsection on the LFY switch and insect Engraled protein).

    DELLA de-repression and GA. What are DELLA nuclear regulatory proteins? The DELLA subfamily of nuclear repressing proteins belongs to the larger family of plant specific GRAS proteins (Bolle 2004). Further, the DELLA subfamily of proteins is gibberellin sensitive and functions in holding-back plant growth and development in cells of floral meristems in extant angiosperms (Jiang and Fu 2007).

    Hao Yu et al. (2004) suggest a close relationship between GAs and other indeterminate morphogens and expression of homeotic selector genes. Yu et al. state:

    "Taken together, the work presented here suggests that GA promotes normal development of floral organs partly by up-regulating the expression of floral homeotic genes AP3, PI, and AG. Gibberellic acid achieves this effect by suppressing the function of two DELLA proteins, RGA and RGL2."

    The preceding phrase is quoted from page 7832 of H. Yu, T. Ito, Y. Zhao, J. Peng, P. Kumar, and E. M. Meyerowitz (2004), Floral homeotic genes are targets of gibberellin signaling in flower development, Proceedings of the National Academy of Sciences 101(20): 7827-7832.

    Further, studies of Arabidopsis suggest that DELLA proteins mediate the GA-dependent development of floral organs however, the detailed interactions between DELLAs and the floral meristem organ identity and integrator genes they repress remain incompletely understood (Hou et al. 2008).

    It might be important to understand the details of DELLA repression of floral homeotic genes (and relief of repression by GA) in other experimental seed plant systems (and in a molecular-phylogenetic context), as floral regulators are probably a key part of the puzzle behind the origin of the angiosperm flower (Theißen and Melzer 2007, Melzer et al. 2010).

    A possible relationship exists between the plant gibberellin nuclear receptor GIBBERELLIN INSENSITIVE DWARF (GID1), DELLAs, and hormone specific lipases (HSLs) (Itoh et al. 2008, Murase et al. 2008).

    Do certain insect nuclear receptor proteins and HSLs bind to plant GA?

    Are gibberellins manufactured by host plants bioactive in developing instars and larvae of insect antagonists?

    The LEAFY (LFY) switch and insect Engraled protein. The LFY gene encodes a diffusible 47 kilodalton-sized TF which is unique to plants (Sessions et al. 2000, X. Wu et al. 2003). Leafy protein regulates patterning of cells in developing SAMs of the model flowering plant, Arabidopsis thaliana (Maizel et al. 2005, Moyroud et al. 2009, Moyroud et al. 2010).

    The left-hand image is reproduced from Figure 6 on page 2634 of Hamès et al. (2008), "Comparison of LFY-C with paired and homeodomain DNA binding. (A) Two orthogonal views of LFY-C helices α1 - α3 bound to their DNA target site [red] superimposed with the three helical bundle core of the N-terminal subdomain of the paired domain of Drosophila Prd [blue, PDB-id: 1pdn]. (B) Superposition with the homeodomain of Drosophila engrailed bound to DNA [yellow, PBD-id: 1hdd], where the centre of recognition helix α3 inserts into the major groove."

    Reprinted by permission from Macmillan Publishers Ltd: The European Molecular Biology Organization (EMBO) Journal, Hamès, C., D. Ptchelkine, C. Grimm, E. Thevenon, E. Moyroud, F. Gérard, J.-L. Martiel, R. Benlloch, F. Parcy, and C. W. Müller. 2008. Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins, The EMBO Journal 27: 2628-2637, copyright ©2008.

    Leafy protein regulates GA mediated transition to flowering and downstream expression of MIKC-type MADS-box genes that determine floral organ identity (H. Yu et al. 2004, Theißen and Melzer 2007, Hou et al. 2008, Sayou et al. 2014).

    Engraled (en), also spelled "engrailed" in the literature, is an insect compartment selector gene that encodes the Engraled homeodomain TF that determines the posterior identity of embryos and wings of the Drosophila model arthropod. The Apterous (ap) compartment selector gene encodes Apterous protein, which is another TF involved in subdivision of imaginal discs into dorsal and ventral compartments of developing fruit flies (S. B. Carroll et al. 2005).

    The structure of the LFY-C protein of Arabidopsis thaliana shown in the image above, consists of a HTH DNA-binding motif with uncanny similarities to the active motif of Drosophila Engraled homeodomain protein, Tc3A transposase, and Hin recombinase enzymes (Hamès et al. 2008).

    "A highly conserved and essential TF [LFY homeodomain protein] evolved radical shifts in DNA binding specificity by a mechanism that does not require gene duplication." (page 648, Sayou et al. 2014).

    Now that Hamès et al. (2008) deduced the 3-dimensional crystal structure of LFY-C protein from Arabidopsis, it is possible to formulate explicit hypotheses on the origin of angiosperms and the origin of the first flower involving molecular coevolution of seed plant LFY protein and insect homeodomain proteins including Engraled (Hittinger and S. B. Carroll 2008).

    "Our study reveals that the LFY master regulator, which determines flower meristem fate and controls the expression of floral organ identity genes, shares structural similarity with other HTH proteins, indicating that this universal DNA-binding motif has also been adopted in plants to trigger major developmental switches."

    The preceding paragraph is quoted from page 2635 of C. Hamès, D. Ptchelkine, C. Grimm, E. Thévenon, E. Moyroud, F. Gérard, J.-L. Martiel, R. Benlloch, F. Parcy, and C. W. Müller (2008), Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. The EMBO Journal 27: 2628-2637.

    A focus of the exercise should now be further development of hypotheses on the origin of the angiosperms, the origin of the flower, and MIKC-type MADS-box protein evolution proposed by Theißen and Saedler (2001), Albert et al. (2002), Kaufmann et al. (2005), Maizel et al. (2005), Baum and Hileman (2006), and Theißen and Melzer (2007).

    Clusters of hermaphroditic pollen- and ovule bearing leaves known as bisexual strobili are the focus of most of the leading models of cone and floral organization (Melzer et al. 2010). Further, studies of developmental abnormalities in cones of extant conifers offer a window for better understanding the origins of flowers and flower-like organs (Flores-Rentería et al. 2011, Rudall et al. 2011).

    Further, phylogenetic analysis suggests that a critical MIKC-type MADS-box gene duplication or WGD occurred in the common seed plant ancestor of angiosperms and gymnosperms at least 300 MYA (Becker et al. 2000, Zahn et al. 2005).

    Based upon a brief paleontologic survey of Paleozoic seed plants having bisexual strobili, the prime candidate populations for the 300 million year old gene duplication event were among the species and genera of Vojnovskyales, Permo-carboniferous gymnosperms with bisexual cone axes, and Permian gigantopteroids (diagrammed below), and their potential intergeneric hybrids.

    Based on modern biochemical- and evolutionary-developmental models of vegetative- and/or reproductive-shoot apical meristematic growth (Baum and Hileman 2006, Theißen and Melzer 2007, J. M. Alvarez et al. 2015, among others) does the Clear Fork Gigantopteroid, which is diagrammed above, display the morphological fingerprint of a deeply-conserved leaf- and shoot- molecular tool kit?

    Evolution in MADS-box proteins is reviewed by Kaufmann et al. (2005), Rijpkema et al. (2007), Veron et al. (2007), Leseberg et al. (2008), Gramzow et al. (2010), Y.-Q Wang et al. (2010), and Dornelas et al. (2011).

    Physiology of homeodomain protein trafficking. Traditional concepts of SAM organization in eudicots are being reevaluated using scanning electron microscopy and fluorescence light microscopic techniques involving fusion of probes with homeodomain proteins. Shoot apical meristems of flowering plants contain two fields of meristematic cells: the central zone and a peripheral zone (Ori et al. 2000, among others).

    Further, SAMs produce specialized boundary cells at the interface between meristematic cells of the central zone and organ cells in the peripheral zone where TFs necessary for the regulation of development move from cell-to-cell (Aida and Tasaka 2006).

    Certain KNOX homeodomain proteins, FLO/LFY proteins, and other small-sized (<60 kilodalton) TFs and their mRNAs move from cell to cell via plasmodesmata in the SAMs of some of the model eudicot angiosperms studied (Jackson 2002, J.-Y. Kim et al. 2003, Jackson 2005, X. M. Xu et al. 2011, X. M. Xu and Jackson 2012).

    Chaperonins are necessary for homeodomain TF trafficking in SAMs (Xu et al. 2011).

    Studies of SAMs in the model malvid species Arabidopsis thaliana using fused green fluorescent protein (GFP) and the 47 kilodalton-sized LFY enzyme, suggest that movement within the SAM through secondary plasmodesmata is by simple diffusion (X. Wu et al. 2003). In contrast MIKC-type MADS-box proteins AP3 and PI do not move from cell to cell between tissues layers.

    Does thigmo affect homeodomain TF movements in SAMs of extant model eudicots?

    Trafficking of certain homeodomain TFs in SAMs of extant model eudicots is conserved, often unidirectional, developmentally important, and ontogenetically controlled (J.-Y. Kim et al. 2003). The physiology of SAM macromolecular trafficking, when extrapolated to seed plants in deep time is an important component of the prevailing models of cone organization and floral origins (Baum and Hileman 2006, Theißen and Melzer 2007, Melzer et al. 2010).

    Baum and Hileman (page 16, 2006) propose that since the GA signaling pathway positively regulates LFY gene expression (and LFY integrates fertile meristem ontogenetic change from vegetative to reproductive), the bisexual cone axis in "... the common ancestor of angiosperms and gymnosperms would have gradually accumulated higher and higher levels of LFY protein during development."

    When considering the evo-devo of modular SAM developmental programs in deep time, conceptual models that incorporate chaperonins, movable cis-acting homeodomain proteins, promoters, and enhancers have potentially profound implications toward evolution of progymnosperm and seed plant reproductive axes. My concept of "developmental programs" is probably similar to biological process-based, evo-devo homology concepts suggested by Laubichler (2000) and Brigandt (2003), among others.

    Boyce and Knoll (page 70, 2002) reaffirm a common theme that, "Cell walls also prohibit cell migration, constraining the types of development that are possible in plants ...." but neglect to discuss potential cell to cell movements of homeodomain proteins (Jackson 2002), and the implication of this phenomenon toward regulation of transcription and meristematic evo-devo of novel leaf morphologies.

    Based on the possibility that several traffic patterns of homeodomain protein movement emerged in meristems of aerial shoots of extinct progymnosperms and seed plants, at least some traditionally important doctrine and supposed homologies of certain lignophyte organs, are called into question.


    Genome Landscapes and Gene Regulatory Networks:

    In this chapter I discuss molecular evolution of gene-regulatory networks (GRNs), including CRMs, auxin-mediated polarity networks (PINs), and cis-acting TFs. Brief discussion of the genome landscape is included with an outline of genetic mechanisms such as co-option and exaptation, developmental recombination and reprogramming, genetic accommodation, homeotic selector genes, horizontal transfer of genes, chloroplast capture, mobile chromosome parasites, gene duplications, chromosome doubling as a consequence of interspecific hybridization, and paleopolyploidy.

    Studies of the genome landscape of Amborella trichopoda figure prominently in any debate on the evolutionary history of flowering plants (Zuccolo et al. 2011, Amborella Genome Project 2013, Chamala et al. 2013, Jiao and Guo 2014).

    The genome-scale molecular-phylogenetic analyses by Zhenxiang Xi et al. (2014) are the first to resolve an Amborella + Nuphar phylogenetic couplet as sister to all other extant angiosperms when coalescent techniques are employed in computation, simulations, and tree-thinking.

    "... Our results lend further empirical support for analyzing genome-scale data to resolve deep phylogenetic relationships using coalescent methods, and provide the most convincing evidence to date that Amborella plus Nymphaeales together represent the earliest diverging lineage of extant angiosperms" (page 929, Results and Discussion, Accommodating Elevated Rates of Substitution in Coalescent versus Concatenation Analyses, Xi et al. 2014).

    The image on the right is a stained preparation of the chromosomes of Joinvillea plicata (Joinvilleaceae, Poales, Lilianae), a species of grass-like monocots with a fully developed perianth.

    Chromosomes in this image were fixed at the moment of metaphase I of meiosis in a microspore mother cell, × 2000. In the living Joinvillea plant, meiotic chromosomes would be identifiable in two places: inside the immature megasporangium of the ovule and within young microsporangia of very young stamens.

    In addition, I summarize key research advances in our understanding of the possible effects of signals on whole genomes, homeotic selector genes, gene transcripts such as microRNAs (miRNAs and siRNAs), and cis-regulatory sequences that bind TFs.

    "A central concept that is emerging from comparative studies of developmental genes and their interactions is the co-option of these for different functional roles as evolution proceeds."

    This quotation is from page 761 of W. Arthur (2002), The emerging conceptual framework of evolutionary developmental biology. Nature 415: 757-764.

    Could the application of mechanical force, simple thigmo, and/or secretion of phytohormone signals by chewing, crawling, feeding, ovipositing, and sucking insect mutualists on elongated (or shortened) cone axis SAMs affect movement of homeodomain proteins and trigger developmental switches that determine downstream reproductive organ identity and formation?

    "I argue that the origin of species differences can be explained, and the synthesis of Darwinism with genetics can be improved, by invoking two concepts: developmental recombination and genetic accommodation. Developmental recombination, or developmental reorganization of the ancestral phenotype, explains where new variants come from: they come from the preexisting phenotype, which is developmentally plastic and therefore subject to reorganization to produce novel variants when stimulated to do so by new inputs from the genome or the environment. Genetic accommodation, or genetic change in the regulation or form of a novel trait, is the process by which new developmental variants become established within populations and species because of genetic evolution by selection on phenotypic variation when it has a genetic component."

    The preceding passage is quoted from page 6544 of M. J. West-Eberhard (2005), Developmental plasticity and the origin of species differences, Proceedings of the National Academy of Sciences 102(Supplement 1): 6543-6549.

    Students of neo-Darwinian thought and Goldschmidtian saltation should read the review by Moczek et al. (2011).

    "... developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes."

    This phrase is quoted from the abstract of A. P. Moczek, S. Sultan, S. Foster, C. Ledón-Rettig, I. Dworkin, H. F. Nijhout, E. Abouheif, and D. W. Pfennig (2011), The role of developmental plasticity in evolutionary innovation. Proceedings of the Royal Society of London, Series B, Biological Sciences 278(1719): 2705-2713.

    Homeotic selector genes. Homeotic selector genes are known from metazoans, fungi, and plants. These genes are key regulators in insect and land plant developmental tool kits being important in plant organ or body segment identity (S. B. Carroll et al. 2005, Floyd and Bowman 2007). Homeotic selector genes of insects include Hox genes, zygotic (gap- maternal-, and pair-rule-) genes, field-specific selector genes, compartment selector genes, cell-type-specific selector genes, and segment polarity genes (S. B. Carroll et al. 2005).

    Homeotic selector genes of plants include SAM maintenance genes and floral meristem organ identity and integrator genes that encode MIKC-type MADS-box TFs.

    Developmental proteins encoded by homeotic selector genes of plants have been the subject of active research by biochemists, plant cell biologists, and molecular systematists for a long time (Coen and Meyerowitz 1991, Theißen et al. 1996, Kramer et al. 1998, Becker et al. 2000, Cubas et al. 2001, Stuurman et al. 2002, Becker and Theißen 2003, Irish 2003, S. Tucker 2003, Yamada et al. 2003, Kaufmann et al. 2009, Melzer et al. 2009, among others).

    Studies having to do with the origin of the flower, perianth parts, bisexual cone axes, ovules and carpels include Buzgo et al. (2004), Jack (2004), S. Kim et al. (2004), P. Zhang et al. (2004), Adam et al. (2005), Buzgo et al. (2005), Irish and Litt (2005), Kaufmann et al. (2005), S. Kim et al. (2005 [two papers]), Zahn et al. (2005 [two papers]), Baum and Hileman (2006), Cronk (2006), De Bodt et al. (2006), Doerner (2006), Endress (2006), Feng et al. (2006), Irish (2006), S. Kim et al. (2006), Scutt et al. (2006), P. S. Soltis et al. (2006), Kramer et al. (2007), Theißen and Melzer (2007), and Melzer et al. (2010), among others.

    Developmental cis-regulatory modules (CRMs). Non enzyme-coding DNA sequences involved in the control of gene expression are termed CRMs (Zinzen et al. 2009, Borok et al. 2010).

    Clusters of regulatory DNA spaced at irregular intervals on the chromosomes of diverse eukaryotes sometimes contain enhancer and promoter cis-regulatory sequences that bind TFs (Borok et al. 2010). Promoters are cis-regulatory sequences that affect transcription. Some promoters work together with additional factors termed modular enhancers, which are cis-regulatory elements (CREs) (Rebeiz et al. 2009, Borok et al. 2010).

    Modular enhancer CREs of certain insects are subject to mutation. Further mutations in CREs within Drosophila populations potentially lead to adaptive morphological changes with "large phenotypic effect" (abstract, Rebeiz et al. 2009).

    "Plant evolution may often entail changes to the promoter/enhancer elements that cause changes in the expression patterns of regulatory genes."

    The preceding quotation is from page 59 of D. A. Baum and M. J. Donoghue (2002), Transformation of function, heterotopy, and the evolution of plant development. Pp. 52-69 In: Q. C. B. Cronk, R. Bateman, and J. Hawkins (eds.), Developmental Genetics and Plant Evolution, The Systematics Association Special Volume Series 65. London: Taylor and Francis, 543 pp.

    Transcription factors (TFs) are cis-acting proteins that bind to cis-regulatory sequences (Wray et al. 2003).

    It is increasingly clear that MADS-box domain TFs interact even with their own promoters. Further, "MADS-box proteins seem to function mostly as subunits of larger protein complexes" (page 34, Rijpkema et al. 2007).

    Evolution of CRMs in relation to animal and plant body plan patterning, development of organs of insects and seed plants, and natural selection is reviewed by Rodríques-Trelles et al. (2003), Wray (2003), Wray et al. (2003), Theißen and Becker (2004), S. B. Carroll (2005), De Bodt et al. (2006), Wittkopp (2006), Hoekstra and Coyne (2007), Wray (2007), and S. B. Carroll (2008).

    The diagram below, which is redrawn from Carroll (2005), shows how the cis-regulatory molecular evolution and duplication of genes in insects or plants may potentially increase gene function while minimizing pleiotropy. The blue lines are segments of coding and non-coding DNA. Intron pairs are gray-colored rectangles. Orange circles are cis-regulatory promoters. Finally, asterisks denote mutations.



    The first line of "A" illustrates a progenitor gene with its introns and promoter. The second two lines of "A" shows a gene duplication. Potential mutations of the cis-regulatory promoter and gene intron are denoted by asterisks. "B" illustrates expansion of cis-regulatory elements. "C" depicts the genesis of a novel intron and potential splicing sites that may lead to biosynthesis of alternative protein forms without the deleterious effects of mutations.

    The above graphic is redrawn from Figure 1 of Sean B. Carroll, 2005, Evolution at two levels: on genes and form, PLoS Biology 3(7): 1159-1166.

    A typical promoter consists of fewer than 50 binding sites for less than 15 different TFs. Transcription factor binding sites are about a dozen nucleotide base pairs wide, spaced irregularly along a segment of chromatin. Some promoters may be conserved while others are not.

    Shoot apical meristem (SAM) maintenance genes. Function and patterning in the SAM requires several gene families and their cis-acting TFs. The main SAM identity genes are Class III HD-Zip, KANADI, Class 1 KNOX (KNOTTED1-like), and ARP genes (Ori et al. 2000, Reiser et al. 2000, Hake et al. 2004, Di Giacomo et al. 2008, among others).

    Class III homeodomain-leucine zipper proteins, which are encoded by Class III HD-Zip genes, include AtHB8, CNA, PHB, PHV, and REV (see reviews by Floyd et al. 2006, Prigge and S. E. Clark 2006, and Langdale 2008). Class III HD-Zip genes and the enzymes they encode have been isolated from extant flowering plants, gymnosperms, ferns, lycophytes, bryophytes, and charophytes including most of the model photosynthetic organisms used in evo-devo research. All were probably key players in the land plant developmental tool kit of cis-acting genes, TFs, and homeodomain proteins (Floyd and Bowman 2007).

    Tantalizing clues are gained by experimentally manipulating malvid SAMs with synthetic promoters causing misexpression of KNOX genes leading to bizarre pteridosperm-like ectopic shoots on abaxial leaf surfaces (see Reiser et al. 2000).

    Knotted1-like homeobox genes are expressed in the actively dividing cell fields in the SAMs of extant seed plants (Ori et al. 2000, among others). Downregulation of KNOX genes occurs in organ primordia founder cells of the malvid SAM and other angiosperms and gymnosperms studied to date (Bharathan et al. 2002). When these genes are not expressed properly in monocots, ectopic shoots grow from new fields of meristematic cells on the abaxial surfaces of leaves or other deformities occur, invoked by experimentally manipulating KNOX cis-regulatory function (Reiser et al. 2000).

    Class 1 KNOX genes are necessary components of SAM development in conifers (Guillet-Claude et al. 2004). In seedlings of the gnetophyte Welwitschia mirabilis, Class I KNOX genes are expressed in the SAM but not in primordia of the only two leaves (Pham and Sinha 2003). Movable, small-sized Class I KNOX homeodomain proteins are assembled upon translation of KNOX gene mRNA transcripts in cells of organizing centers of the SAM (Jackson 2002).

    Pham and Sinha (2003) do not address potential significance of KNOX homeodomain protein movements from the SAM to leaf primordia, thence to regions of indeterminate growth, when discussing ontogeny of accessory scaly bodies and reproductive organs of Welwitschia.

    These genes are organized into KNOX/ARP modules in the vascular plants studied to date. The SAMs of extant flowering plants typically express KNOX but not ARP (ASYMMETRIC LEAVES1, ROUGHSHEATH2, PHANTASTICA) genes. Conversely expression of ARP genes in leaf primordium cells of the SAM leads to suppression of KNOX function. Whether the KNOX genetic switch is on or off depends on the activity of ARP repressors, and may lead to the development of different leaf forms e.g. pinnate, palmate, or compound (Beerling and Fleming 2007).

    Class I KNOX genes are important when considering the genetic basis of land plants and the origin of angiosperms as they figure prominently in discussions of classic theories on telomb transformational series within the evo-devo context (Beerling and Fleming 2007, Sanders et al. 2007). Understanding KNOX genes and their expression may offer clues toward unraveling complex mechanisms behind morphogenetic patterns in flowering plants (Bharathan et al. 1999), among other seed plants.

    Cytokinins and gibberellins act downstream of Class I KNOX genes in the rice and mouse-eared cress subjects studied (Di Giacomo et al. 2008). Among the many other TFs found in plant meristems, Class II TCP genes encoding TCP proteins are involved in the shaping of leaves and flowers (Cubas 2004, Damerval et al. 2007).

    Deep conservation in tool kit gene families in land plants (Floyd and Bowman 2007) such as SAM maintenance genes e.g. Class III HD-Zip and KNOX/ARP CREs and the conserved HTH DNA-binding motifs of homeodomain proteins, illuminates the critical importance of CRMs in the evolution of sporophyte SAMs, axillary SAMs, and cone- and floral SAMs of ancient seed plants, including flowering plants (Becker 2016).

    Cone and floral meristem organ identity and integrator genes and transcription factors (TFs). The development of perianth parts of the flower involves homeotic cis-acting TFs that act downstream of SAM maintenance genes (Glover 2014, among others).

    Pamela S. Soltis et al. (2009), Specht and Bartlett (2009), Chanderbali et al. (2010), Melzer et al. (2010), Rudall and Bateman (2010), and D. W. Taylor (2010), among others, review the developmental genetics and evolution of cones and flowers.

    Leafy protein encoded by the LFY gene is a key developmental switch in floral meristems of many angiosperms including Arabidopsis (Hamès et al. 2008, Moyroud et al. 2009, Chahtane et al. 2013, Yamaguchi et al. 2013, Glover 2014), and Liriodendron (Magnoliaceae, Magnoliales, Magnolianae) (Liang et al. 2011). Floricaula/Leafy proteins are key controllers of cone and bract-scale development in several diverse genera of gymnosperms including Cryptomeria (Cupressaceae, Coniferales) (Shiokawa et al. 2008), Gnetum (Gnetaceae, Gnetales) (Shindo et al. 2001), and Taxus (Taxaceae, Taxales), among others (Vázquez-Lobo et al. 2007, Moyroud et al. 2009).

    The main floral meristem organ identity and integrator genes in Arabidopsis include LFY, AG, AP1, AP2, CAL, FLO, SOC1, TFL1, and UFO.

    A gymnosperm paralog of LFY termed NLY has been isolated from Pinus [Pinaceae, Coniferales] (Mouradov et al. 1998). Shiokawa et al. (2008) demonstrated that transgenic Nicotiana tabacum (Solanaceae, Solanales, Asteranae) that expressed a CjNdly gene isolated from Cryptomeria japonica possessed stamens expressed as petals. These workers conclude that the gymnosperm CjNdly gene is a homolog of angiosperm FLO/LFY.

    The FLO/LFY family of TFs controls the downstream expression of several genes in extant anthophyte seed plants including MIKC-type MADS-box genes (Theißen and Melzer 2007, Melzer et al. 2010, among many other papers).

    High points of the extensive work on LFY in seed plants with implications toward MMT, the timing of the angiosperm-gymnosperm split, and the origin of flowering plants, are discussed by Shindo et al. (2001), Baum and Hileman (2006), and Vázquez-Lobo et al. (2007).

    Several TFs are implicated in changing the shape and size of flowers (Glover 2014). These include ANT, ARGOS, BB, CYCLOIDEA (CYC), DICH, and DIVARICATA (Glover 2014, among others). AINTEGUMENTA is a principal controller of both flower- and leaf size. Further, ANT negatively regulates the expression of the Class C MIKC-type MADS-box gene AG (Krizek 2009). The AINTEGUMENTA TF is a component of the auxin regulated signaling cascade (Busov et al. 2008, Krizek 2009, among others).

    Floricaula, which is encoded by FLC represses both FT and SOC1 in the malvid model plant Arabidopsis (Deng et al. 2011).

    The APETALA- (AP-) 2 gene subfamily is comprised of AINTEGUMENTA and AP2 (and a number of other genes and TFs known from Arabidopsis), which is part the larger AP2/ERF (ethylene responsive factor) family of TFs (S. Kim et al. 2006).

    All of these genes including their paralogs, orthologues, and cis-acting TFs, figure prominently in discussions of the ancestral developmental tool kit of land plants (Floyd and Bowman 2007, among others), and in numerous studies of the origin of the angiosperm flower and floral diversification (S. Kim et al. 2006, P. S. Soltis et al. 2009, among others).

    In 2006 Baum and Hileman proposed a modification of Theißen and Saedler's (2001) protein quartet model involving genetic interactions of B and C homeotic selector genes, SEP genes, and small-sized growth promoting molecules (phytohormones and other factors) aligned along gradients within a developing seed plant cone axis.

    The protein quartet model of floral molecular evolution is now widely accepted among plant biologists (Leseberg et al. 2008). Plant systematists view the expanded ABC model as "the default program" behind the identity of organs of the flower (page 18, D. E. Soltis et al. 2008; page 117, Figure 2, P. S. Soltis et al. 2009). MIKC-type MADS-box E proteins such as SEP3 bind to DNA in the test tube as quartet-like complexes (Melzer et al. 2009).

    "Out-of-male" and "out-of-female" hypotheses on the origin of the angiosperm flower (Theißen Saedler 2001, Becker and Theißen 2003) are potential examples of how cis-acting protein modules "might exert their function as transcription factors by binding to the promoters of target genes" (page 132, Theißen and Becker 2004).

    While discussing evidence that seed plant class B homeotic selector genes diverged into the two lineages leading to extant gymnosperms and angiosperms 300 million years ago during the late Carboniferous Period following a gene duplication or WGD, Theißen and Becker (2004) state:

    "Changes in cis-regulatory elements, typically located in the promoter region of a respective gene, in enhancers or silencers up- or downstream of the coding region, or even in introns, might have rendered B gene expression more susceptible to a hypothetical apical-basal gradient already present within the cone. Such a gradient could be based on a low molecular weight compound such as a phytohormone or on a protein (presumable another TF). The underlying molecular changes within the B gene could range from a simple single nucleotide change to major rearrangements at the B gene locus."

    The preceding statement is quoted from page 142 of Günter Theißen and Annette Becker (2004), Gymnosperm orthologues of class B floral homeotic genes and their impact on understanding flower origin, Critical Reviews in Plant Sciences 23(2): 129-148.

    Is Theißen and Becker's hypothetical cone concept (2004) applicable to bisexual axes of Carboniferous Vojnovskyales?

    MIKC-type MADS-box genes and transcription factors (TFs). Certain MADS-box floral meristem organ identity and integrator genes encode MIKC-type MADS-box TFs that determine development of cones and flowers (Ma and dePamphilis 2000, Theißen et al. 2000, Theißen 2001, Becker and Theißen 2003, Theißen and Melzer 2007, Melzer et al. 2010, Becker 2016, among others).

    "While the amazing conservation of the major floral identity [ABCDE] program is being unravelled by analysing floral homeotic gene function and expression, we are only just beginning to understand the evolution of the gene network governing the organ identity genes ... " (Abstract Scope and Conclusions, page 145, Becker 2016, item in [brackets] is mine).

    The acronym "MADS" was coined from names of homeotic genes isolated from yeast (MCM1), snapdragon (AG and DEF), and humans (SRF) (Ma and dePamphilis 2000). Protein subunits encoded by the MIKC-type MADS-box genes possess a modular organization that includes a MADS (M) intervening (I), keratin-like (K), and a C-terminal (C) domain (Theißen et al. 2000).

    The extreme age of MIKC-type MADS-box genes as controllers of development is supported by numerous biochemical and phylogenetic analyses (Nam et al. 2003, Gramzow et al. 2010, among others). Gymnosperms possess orthologs of certain MADS-box genes. It is not unreasonable to accept the proposal that at least some MADS-box genes operated in more general developmental patterning in Carboniferous seed plants supposedly before the angiosperm-gymnosperm split roughly 300 MYA (Nam et al. 2003).

    Further, based on studies of extant Ceratopteris [a monilophyte fern] (Hasebe et al. 1998), Chara (an algal charophyte), Physcomitrella (a moss), and Selaginella (a lycophyte), early land plants probably had two MIKC-type MADS-box genes and that the MADS-box gene family diverged widely after the seed plant/fern split (Floyd and Bowman 2007).

    Douglas E. Soltis et al. (2006), Kramer (2007), P. S. Soltis et al. (2009), Specht and Bartlett (2009), Rudall and Bateman (2010), Melzer et al. (2010), D. W. Taylor (2010), Yamaguchi et al. (2013), and Glover (2014), among others, incrementally review advances in our understanding of the genetics and regulation of flowering.

    A compilation of published research on regulation of cone and floral development appears in Volume 21, Number 1 (2010) of the serial Seminars in Cell and Developmental Biology. This issue contains papers by Alvarez-Buylla et al. (2010), Causier et al. (2010), Immink et al. (2010), Litt and Kramer (2010), Liu and Mara (2010), Melzer et al. (2010), Rijpkema et al. (2010), and Sablowski (2010).

    There are three fundamental classes of floral organ identity genes, "A," "B," and "C" that comprise the first unifying principle of fertile meristem development (Jack 2004, Causier et al. 2010 [two papers], among others). In extant flowering plants A function is responsible for sepal identity (M.-K. Chen et al. 2008, among others), A + B expression determines the identity of petals (Su et al. 2008, among others), B + C expression affects stamen morphology (Kramer et al. 1998, Piwarzyk et al. 2007, among others), and C gene expression controls the identity of carpels and stamens (Causier et al. 2009, Yellina et al. 2010, among others).

    Variations in B-gene expression determine the identity, shape, and form of unusual perianth parts in columbines (Kramer et al. 2007, Bharti Sharma et al. 2011), grasses (Whipple et al. 2007), papaya (Ackerman et al. 2008), and potatoes (Geuten et al. 2011).

    Gymnosperm orthologues of the B and C genes including AGAMOUS (AG) are known: their conserved evolution is demonstrable (P. Zhang et al. 2004). Apparently gymnosperm "B" genes are only expressed in male cones (Theißen and Becker 2004). The evolution of "B" and "C" genes is recently reviewed by Causier et al. (2010, among others).

    Additional classes "D," "E," and "F" been identified in certain extant seed plants. D-class genes apparently operate to determine organ identity in the flowering plant genus Petunia (Solanaceae, Solanales, Asteranae) (Ferrario et al. 2006).

    "... the most parsimonious explanation [i.e. differential expression of class B, C, and D genes as the 'primary sex-determination mechanism in all seed plants'] would be that the mechanism of female/male reproductive organ specification/distinction in angiosperms was recruited from a similar system that was already established in the lineage leading to all extant seed plants about 300 MYA (Theißen et al. 2000). At the molecular level, therefore, flower origin seems less mysterious than the morphological difference between flowers and gymnosperm cones or strobili might suggest."

    The preceding statement is from page 138 of Günther Theißen and Annette Becker (2004), Gymnosperm orthologues of class B floral homeotic genes and their impact on understanding flower origin, Critical Reviews in Plant Sciences 23(2): 129-148. The phrase and within-context but out of place quote from the original article denoted by brackets [] is mine.

    There are apparently two of A-class floral meristem identity genes, AP1 and AP2, in Arabidopsis thaliana. The B-class genes of Arabidopsis, including APETALA 3 (AP3) and PISTILLATA (PI) are specifiers of petaloid organs in whorl two, and staminate organs in whorl three of the SAM (Hileman and Irish 2009). The C-class gene AGAMOUS (AG) integrates the activity of whorl three stamens and carpels of the fourth whorl. C-class genes evidently repress the activity of A-class genes that operate in whorls three and four (Jack 2004).

    A fourth class of MIKC-type MADS-box genes known as SEPALLATA (SEP) is implicated in determination of floral identity (Becker and Theißen 2003, Kaufmann et al. 2009, Melzer et al. 2009, among others). Zahn et al. (2005) report SEP homologues in basal angiosperms including Amborella trichopoda.

    "The coincidence between the origin and diversification of the SEP subfamily and the emergence of angiosperms suggests that the origin of the SEP subfamily may be part of a hypothesized 'molecular innovation' that made possible the morphological invention of the flower."

    The previous quotation is from page 2219 of L. M. Zahn, H. Kong, J. H. Leebens-Mack, S. Kim, P. S. Soltis, L. L. Landherr, D. E. Soltis, C. W. dePamphilis, and H. Ma (2005), The evolution of the SEPALLATA subfamily of MIKC type MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history, Genetics 169: 2209-2223.

    Zahn et al. (2005) suggest that since the SEP and SQUA subfamilies of MIKC-type MADS-box genes are not known from gymnosperms the first SEP gene duplication might have occurred after flowering plants diverged from their naked seed plant ancestors some 300 MYA.

    SEPALLATA genes are known as MIKC-type MADS-box E genes. The revised Coen and Meyerowitz ABC model, at least for the extant flowering plant species studied to date, states that sepals are specified by A gene activity alone, petals by A + B + E genes, stamens by B + C + E MADS-box factors, and carpels by C + E genes. Higher order MIKC-type MADS-box gene combinations are also now suspect to operate in certain seed plant species but much work remains to be done (Jack 2004), and is underway in many laboratories all over the world.

    Study of floral meristem organ identity genes in Persea (Lauraceae, Laurales, Magnolianae) identified "... spatial and temporal shifts in gene expression that coincide with an evolutionary change in perianth morphology." (page 1081, Chanderbali et al. 2006).

    Molecular systematists have identified and studied MIKC-type MADS-box genes in basal angiosperms (Aoki et al. 2004, S. Kim et al. 2005, P. S. Soltis et al. 2009, among others). Sangtae Kim and coworkers report several homologs of MADS-box genes including AP3 and P1. These two genes are expressed in all the floral organs of Amborella. APETALA3 and PI were either not expressed at all, or only weakly expressed in several other basal angiosperms.

    Broader expression of AP3 and P1 homologs in basal flowering plants suggested that this was the ancestral condition. Other deviations from the Coen and Meyerowitz ABC model were noted by S. Kim et al. (2005) as a basis for a Fading Borders Model (D. E. Soltis et al. 2007, P. S. Soltis et al. 2009, Chanderbali et al. 2016).

    "Despite numerous genetic-based models for the origin of the flower (e.g. Frohlich and Parker 2000; Albert et al., 2002; Theissen et al., 2002), how that ancestral reproductive program was modified to yield a flower largely remains an abominable mystery itself."

    The preceding statement is from page 118 of P. S Soltis, S. F. Brockington, M.-J. Yoo, A. Piedrahita, M. Latvis, M. J. Moore, A. S. Chanderbali, and D. E. Soltis (2009), Floral variation and floral genetics in basal angiosperms. American Journal of Botany 96(1): 110-128.

    Gene and whole genome duplications (WGDs). Consideration of both small gene duplications and WGDs is important in understanding the timing of the origin of angiosperms, radiation of basal flowering plants and eudicots (D. E. Soltis et al. 2007, D. E. Soltis et al. 2009, Jiao et al. 2011, P. S. Soltis and D. E. Soltis 2016), and in the evolution of seed plants (Guillet-Claude et al. 2004, Jiao et al. 2011, McGrath and M. Lynch 2012).

    By knowing the interval in geologic deep time when molecular systematists predict divergence of molecular tool kits, paleobotanists might be able to better focus on candidate seed plant groups for detailed anatomical study of permineralized fossils (Crepet 2008).

    Van de Peer et al. (2009) and Jiao et al. (2011) discuss the high points of research on WGDs in eukaryotes and the evolutionary consequences of polyploidy. Pamela S. Soltis et al. (2009) and P. S. Soltis and D. E. Soltis (2016) review and summarize the role of gene duplications in angiosperm floral diversification.

    Phylogenetic analyses suggest that duplications in floral meristem identity genes took place prior to the origin of angiosperms more than 260 MYA (Bowe et al. 2000, Bowers et al. 2003, S. Kim et al. 2004). Mathematical modeling studies of Arabidopsis reveal that diversification of genes involved in signal transduction, SAM development, and the regulation of transcription are attributable to three WGDs during the last 350 million years (Maere et al. 2005).

    A phylogenetic analysis of KNOX1 genes by Guillet-Claude et al. (page 2242, 2004) "suggests that three duplication events (D1, D2, and D3) occurred between the split of the lineage leading to conifers from that leading to angiosperms, around 300 m.y.a. [MYA] ..." and the Cretaceous divergence of pines and spruces (the acronym [in brackets] is mine).

    Jiao et al. (2011) narrow this estimate by employing phylogenetic models to all available seed plant genomic data to "... two groups of duplications, one in the common ancestor of all angiosperms and the other in the common ancestor of all seed plants."

    Studies of the "angiosperm history" and the genome landscape of the poster-boy [-girl] basal angiosperm Amborella trichopoda (Amborellaceae, Amborellales, Amborellanae) are probably unhelpful in deciphering the paleobiology of Permo-carboniferous seed plant groups modeled by Jiao et al. (2011).

    Most of the explosive radiation of floral diversity in basal lineages of flowering plants is explained by duplication and diversification of the MIKC-type MADS-box family of genes (P. S. Soltis et al. 2009, P. S. Soltis and D. E. Soltis 2016).

    Evolution of the Hox gene cluster and MADS-box genes. Gene duplications were an important part of the assembly of the early bilaterian animal tool kit that led to tetraploidization and the creation of several gene families including the HOM-Hox and Parahox clusters of homeobox genes (Carroll et al. 2005). Homeobox genes are not the same as homeotic MADS-box genes (Meyerowitz 2002).

    An ancestral MADS-box gene duplication took place before the divergence of animals, fungi, and plants hundreds of millions of years ago (Alvarez-Buylla et al. 2000), probably before or during the Neoproterozoic snowball Earth or later warming leading to the Cambrian explosion of life. This earliest gene duplication gave rise to the Type 1 and Type II lineages of MADS-box genes (see Figure 1, page 468, Becker and Theißen 2003).

    Animal homeotic genes such as MEF2 encode certain enzymes involved in muscle differentiation of both invertebrates and vertebrates and wing vein and tracheal development in certain insects. Duplicated MADS-box genes in plants have completely different functions (Meyerowitz 2002).

    Some of the better understood duplicated MADS-box floral meristem organ identity and integrator genes encode MIKC-type MADS-box TFs that determine development of cones and flowers (Ma and dePamphilis 2000, Theißen et al. 2000, Theißen 2001, Becker and Theißen 2003, Theißen and Melzer 2007).

    An evolutionary history of MIKC-type MADS-box A genes, including gene duplications and functional divergence is reviewed by S. Kim et al. (2006) and Shan et al. (2007). Recent functional analyses of A-class genes in monocots is published by M.-K. Chen et al. (2008).

    Irish and Litt (2005) and Irish (2006) review the evolutionary history of B-, C-, and E-class MADS-box gene duplications in plants. The molecular evolution of B-class MADS-box genes has been extensively researched by Kramer et al. (1998), Kramer et al. (2003), Aoki et al. (2004), S. Kim et al. (2004), Zahn et al. (2005), and Hernández-Hernández et al. (2007).

    Molecular evolution of MIKC-type MADS-box C genes over the course of 300 million years of seed plant evolution is reviewed by Kramer et al. (2004), P. Zhang et al. (2004), and Irish and Litt (2005).

    Finally, the importance of MADS-box gene duplications and the interactions among the proteins they encode toward the evolution and radiation of flowering plants is reviewed by Rijpkema et al. (2007) and Veron et al. (2007).

    Paleopolyploidy. A great body of data has been assembled on paleopolyploidy in plants (Bennett and Leitch 2005, J. J. Doyle et al. 2008, Jiao et al. 2011). Evidence from an exhaustive genomic study of the cultivated grape overwhelmingly supports the existence of paleohexaploidy (Jaillon et al. 2007), which is equivalent to the "γ triplication" (Jiao et al. 2011).

    Volume 66, Number 1 (2011) of The Plant Journal is devoted to evolution of the plant genome.

    "... Here I aim to highlight one key realization of this 'genomics era' in which we find ourselves, namely, that all modern flowering plant genomes derive from processes set in motion by a history of repeated, episodic whole-genome doubling or polyploidy" (page 1753, Wendel 2015).

    Evidently, WGDs in ancient seed plants were necessary as a building scaffold for developmental recombination and evolution of innovative morphologies (S. Kim et al. 2004, Zahn et al. 2005, Jiao et al. 2011) such as developmentally labile bisexual cone axes and flowers (Baum and Hileman 2006, Theißen and Melzer 2007, Melzer et al. 2010, Lomax et al. 2014).

    "Both palaeopolyploidy events [350 MYA and 200 MYA, Jiao et al. 2011] appear to coincide with relatively high, yet declining, atmospheric carbon dioxide concentration (Fig. 2c, d). However, using the fossil record rather than molecular dating techniques, the earlier event actually corresponds with the initial radiation of seed plants in the Late Devonian and Mississippian, while the latter is contemporaneous with the Triassic–Jurassic boundary and hence significantly pre-dates the earliest morphologically recognisable angiosperms (see Bateman and Hilton 2006) ..." (Page 639 and 640, Lomax et al. 2014).

    Douglas E. Soltis et al. (2007) suggest that WGDs were important in the early evolution of the angiosperm stem group. This line of inquiry continues to dominate the literature on WGDs in flowering plants (P. S. Soltis and D. E. Soltis 2016).

    "It is noteworthy that polyploidy is absent in some ancient plant lineages, such as the cycads, which argues against the proposition that the frequency of polyploidy in a lineage is merely of symptom of lineage age (Fig. 9)."

    The preceding quotation is from page 376 of W. L. Crepet and K. J. Niklas, (2009), Darwin's second "abominable mystery": Why are there so many angiosperm species? American Journal of Botany 96(1): 366-381.

    Ancient WGDs are implicated in both the γ triplication at the heart of the eudicots (Jiao et al. 2012), and in the MRCA (Jiao et al. 2011).

    Let's not forget that Volume 342, Number 6165 of Science publishes three significant papers on paleopolyploidy and the genome ecology of Amborella trichopoda, which is a specialized, root-sprouting understory endemic shrub of the high island of New Caledonia (Carlquist 1974, Morat et al. 2012).

    Nancy Eckardt (2004) in one of many journal article summaries for The Plant Cell reports on a paper by Blanc and Wolfe (2004). Blanc and Wolfe (2004 [two papers]) deduce the timing of gene duplications in several monocots, eudicots, and rosids over the course of the last few million years using mathematical models, which were refined in later studies by Cui et al. (2006), Jiao et al. (2011), and Jiao et al. ( 2012).

    The genome of the malvid Arabidopsis thaliana has undergone at least three WGDs in its evolutionary history (Proost et al. 2011).

    Phylogenetic analyses permit accurate estimates of the divergence times of major eudicot clades (D. E. Soltis et al. 2008), with precision enhanced by including fossil minimum age data mapped on to branch points (Crepet et al. 2004).

    Based upon studies of gene and genome duplications in rice (Oryza sativa, Poaceae, Poales, Commelinidae) and mouse-eared cress, Chapman et al. (2006) provide insight on the functional divergence and buffering models for genome duplication. Chapman et al. (page 2734, 2006) suggest that as ancient duplicated genes diverge "... reciprocal buffering presumably erodes with time ..." leading to cyclic genome duplication.

    "... the WGD [α-swarm or ε?] that preceded the origin of the angiosperms clearly provided genetic fodder that appears to have resulted in the key innovation we know as the flower [protoflower?]" (Key innovations on page 160, P. S. Soltis and D. E. Soltis [2016], symbols [in brackets] are mine)

    What are examples of "fodder" of the genome landscape, which is described by P. S. Soltis and D. E. Soltis (2016)?

    Genes retained in duplicate from WGDs in Arabidopsis over the course of million of years are involved in developmental gene regulation and often do not retain redundant functions (Blanc and Wolfe 2004). Gene duplications result in either neofunctionalization, loss of function thus forming pseudogenes, or provide raw material for divergence in animals (Carroll et al. 2005) and plants (Irish and Litt 2005).

    "Given that such genes [developmental, regulatory, and signaling genes] are considered important for introducing phenotypic variation and increase in biological complexity, linking ancient polyploidy events with decisive moments in evolution becomes less speculative and the origin and evolution of angiosperms perhaps less of a mystery."

    The above quotation is from page 596 of S. De Bodt, S. Marie, and Y. Van der Peer (2005), Genome duplication and the origin of angiosperms. Trends in Ecology and Evolution 20(11): 591-597. The phrase in brackets [] is mine.

    Interspecific hybridization. Paleopolyploidy as a consequence of interspecific hybridization and polyploidization of unrelated gymnosperms having two different chromosome base numbers was proposed by Edgar Anderson in 1934. Certain aspects of this early work were developed later (Stebbins 1958, Raven and Kyhos 1965).

    While G. Ledyard Stebbins (1958) probably disagreed with specifics stated in Edgar Anderson's hypothesis, he once proposed that Cretaceous angiosperms were products of interspecific hybridization between flowering plant prototypes. Stebbins (1958) stated:

    "Because of this fact [see above], and also because of the possibility that in its early stages the phylogeny of the angiosperms may have been highly reticulate, I believe that no phylogenetic tree which can be constructed on the basis of present day knowledge can express the genetic interrelationships between orders and families of angiosperms with any degree of accuracy ..."

    The above quotation is from page 269 of Stebbins (1958), On the hybrid origin of the angiosperms, Evolution (Lancaster) 12: 267-270.

    Polyploidy in seed plants may result from meiotic irregularities including formation of unreduced gametes in hybrids, pollen aberrations, or offspring subjected to environmental stress (Stebbins 1958, among others).

    Detailed paleobiological studies by Wolfram Kürschner et al. (2013) constitute the first report of unreduced gamete formation (inferred from light microscopic study of dispersed pollen) in a vascular plant, which dovetails with molecular-phylogenetic modeling by Jiao et al. (2011) documenting a swarm of WGDs in seed plants, about 192 MYA:

    Color illustrations of malformed Classopollis pollen may be found in Figure 3c, 3d on page 338 of Van De Schootbrugge and Wignall (2016).

    Consideration of allopolyploidy in deep-time (Jiao et al. 2011) as starting points of flowering plant lineage diversification could be pivotal. If the first angiosperms evolved from allopolyploid populations spread across thousands of kilometers then how can flowering plants be monophyletic?

    MicroRNAs. MicroRNAs (miRNAs) are tiny ribonucleic acid fragments comprised of about a dozen nucleotides found in animal and plant cells. Their precursors possess a characteristic hairpin loop structure (reviewed by Carraro et al. 2006, Axtell et al. 2007).

    A phylogenetic analysis of miRNA164 presents new data needed to disentangle the phylogenetic relationships of major clades of seed plants (Jasinski et al. 2010).

    While many microRNA's are deeply conserved in land plants as determined from molecular-phylogenetic analyses (S. Kim et al. 2006, Barakat et al. 2007), the birth and death of certain miRNAs may occur within a short evolutionary time span (Axtell et al. 2007).

    Are plant microRNAs involved in repressing homeotic genes in growing cells and tissues?

    Yes, according to Axtell and Bartel (2005) and Axtell et al. (2007). Most microRNAs are involved in negative regulation of gene expression, specifically in control of transcriptional regulators that affect plant development and morphology (Axtell et al. 2007). They are powerful but negative repressors of key transcriptional regulators in the land plant developmental tool kit (B. Zhang et al. 2006, Floyd and Bowman 2007, Axtell and Bowman 2008).

    Some key examples of miRNA regulation of TFs include repression of Class III HD-Zip genes necessary for SAM and leaf development by miR165 and miR166 (Floyd et al. 2006), targeting of AP2 floral development Class A genes by miR172 (S. Kim et al. 2006), repression of scarecrow-like GRAS family genes by miR172, cleavage of GAMYB proteins (positive regulators of LFY gene expression) by miR159, loss-of-function of CUC genes (important in embryo and flower development) caused by miR164, and negative effects on ARF genes by miR160 and miR167 (B. Zhang et al. 2006).

    Regulatory effects of miRNAs are modeled by Djuranovic et al. (2011).

    MicroRNAs specifically small-interfering RNAs (siRNAs) are implicated in the regulation of plant defense responses to insect herbivore attack. These small RNAs may move through living cells and tissues via plasmadesmata from plant to plant, or from plant to insect and vice-versa (Pandey et al. 2008).

    Chloroplast capture and horizontal transfer (HT) of genes. Phylogenetic systematists who study the origin and evolution of angiosperms have identified genes that originated outside of the host plant (Bergthorsson et al. 2004). Foreign chloroplasts and mitochondria (including their genetic material) may be incorporated into new symbionts (seed plants) (Tsitrone et al. 2003, Cho et al. 2004).

    Horizontal transfer of genes occurs in both prokaryotes and eukaryotes including animals, fungi, plants, and protists. According to a recent survey by Richardson and J. D. Palmer (2007), HT involves housekeeping respiratory- or ribosomal protein encoding- mitochondrial genes.

    Robert Jansen et al. (2011) report numerous transfers of rpl22, a plastidic sequence, to the nuclear genomes of several rosids.

    Transfer of genes from donor epiphytic or saprophytic (or other) species to certain organelles of seed plant hosts is demonstrable. At least 26 mitochondrial genes in the basal angiosperm Amborella trichopoda originated from other plants (Bergthorsson et al. 2004) including nine genes from probably epiphytic mosses, and another 19 from sympatric eudicots (Richardson and J. D. Palmer 2007). This is in contrast to the chloroplast genome of Amborella where no horizontally transferred genes are apparent (Goremykin et al. 2003).

    "The horizontal gene transfer concept is potentially of great importance for leading evolutionary thinking beyond the ossified tenets of 'synthetic' theory, first of all, by introducing a long sought - and vigorously denied by traditionalists - mechanism by which macromutations can spread ..."

    The passage above is quoted from page 381 of Krassilov (2002), Chapter 29, Character parallelism and reticulation in the origin of angiosperms, Pp. 373-382 In: M. Syvanen and C. I. Kado (eds.), Horizontal Gene Transfer (second edition), San Diego: Academic Press, 445 pp.

    Potential plastid genome conflict resulting from HT of mitochondrial DNA (mtDNA) from parasitic santalalean flowering plants to Amborella trichopoda (Rice et al. 2013) should be explored.

    Plant pathologists provide important clues on the nature of bioactive substances manufactured by insects and signaling between plant hosts and herbivores. Professor Jack Schultz states:

    "We should not be surprised to find that plants and animals employ microbes to manipulate each other's signaling systems. It appears that both symbionts and lateral gene transfer offer such possibilities, and that the origin of some (many?) plant-herbivore interaction traits is neither insect nor plant."

    The preceding quotation is from page 460 of Schultz (2002), Shared signals and the potential for phylogenetic espionage between plants and animals, Integrative and Comparative Biology: 42: 454-462.

    A well-studied basis of "phylogenetic espionage" is buried in the extensive literature on pathogenic baculoviruses. Insect bodies are often infected by baculoviruses. In certain cases baculovirus genes are incorporated into genomes of lepidopteran hosts causing large behavioral phenotypic effects (Hoover et al. 2011).

    Further, it might have been possible for genome parasites such as transposable elements (Venner et al. 2009) to move from fungal-, insect-, or tetrapod genomes to the host plant genome or vice-versa by baculovirus vectors in their eukaryotic hosts residing coevolutionary compartments.

    Were ancient baculoviruses a source of cross-Kingdom genome parasites able to move from bacterial, animal, and/or fungal hosts and vectors to shrub lifeboats (or vice-versa) of Permo-triassic coevolutionary compartments?

    Transposable elements (TEs). One key ingredient often left out of the steaming cauldron of past ideas on the origin of flowering plants is a class of mobile chromosome parasites known as transposable elements (TEs). Transposable elements are "pieces of DNA characterized by their ability to move from one locus to another in the genome" (page 537, Schaack et al. 2010).

    Good places to gain a basic understanding of transposons within an evolutionary context are reviews by Lovisolo et al. (page 350, 2003), Schaack et al. (2010), Blumenstiel (2011), Parisod and Senerchia (2012), and Schulman and Wicker (2013).

    Transposable elements are known from prokaryotes and eukaryotes including animals, fungi, plants, and protozooans (Lovisolo et al. 2003, Tu 2005, de la Chaux et al. 2011). Long terminal repeat (LTR) retrotransposons are eukaryotic DNA sequences "... with homology to retroviruses ..." (page 350, Lovisolo et al. 2003).

    Sarah Schaack et al. (page 537, 2010) define several types of TEs:

  • Autonomous TEs "... encode the proteins necessary to perform a complete transposition reaction on their own i.e. to move from one genomic locus to another"
  • Class 2 DNA transposons are TEs "... that transpose via a DNA intermediate ..."
  • Cut-and-paste TEs are Class 2 DNA TEs that "... excise and integrate elsewhere ..." on the chromosome
  • Retro-TEs are class 2 DNA TEs that "... do not excise ..."
  • LTR retrotransposons constitute one class of retro-TEs "... comprised of several superfamilies (e.g. Ty1/Copia), some of which produce virus-like particles; characterized by long terminal repeats (LTRs) which are generated upon chromosomal integration"
  • Non-autonomous TEs are TEs "... that do not encode the transposition machinery and are therefore not able to transpose on their own... "
  • Non-LTR retrotransposons are a second class of retro-TEs "... also comprised of numerous superfamilies (e.g. L1, RTE, and Alu) ..." "... characterized by the lack of terminal repeats ..."
  • Class 1 retrotransposons are TEs "that replicate based on the reverse transcription of an RNA intermediate ..."
  • Some retrotransposons of plants are localized in the centromere of chromosomes (Neumann et al. 2011).

    Why should students of the evo-devo of arthropod- and floral tool kits, coevolution, heterochrony, molecular systematics, and paleobotany, and the population ecology of pollination, be concerned with these bizarre mobile genetic parasites?

    A promising clue that indirectly suggests transposon activity in putatively coevolving arthropod and seed plant genomes is contained in an important paper by Hamès et al. (2008) published in The European Molecular Biology Organization (EMBO) Journal.

    Further, TEs are an unstudied yet ostensibly critical ingredient in genome dynamics with potentially profound effects on transcription, translation, enzyme folding, and coevolution of manufactured homeodomain proteins. Amino acids including lysine residue 390 of the LFY-C primary polypeptide chain, and secondary HTH coiling of homeodomain proteins e.g. Tc3 transposase, Hin recombinase, insect Engraled, and LFY, are noteworthy clues (Hamès et al. 2008) and possible signatures suggesting cross-Kingdom TE activity.

    "Transposable elements in Amborella are ancient and highly divergent, with no recent transposon radiations" (Abstract, Amborella Genome Project 2013).

    Equally important toward a greater appreciation of the role of TEs in the coevolution of angiosperms and holometabolous insects is the landscape evolutionary ecology of dynamic animal, fungal, and plant genomes. Repetitive DNA elements such as LTR-retrotransposons together with "non-protein-encoding sequence types" (i.e. CREs including enhancers and promoters) are responsible for interspecific variation in DNA content of plants (Grover and Wendel 2010).

    Did surviving insects of the EPE and TrCCE feed, reproduce, and secrete biologically active molecules on, or infect growing points and reproductive modules with transposons, while chewing, piercing, ovipositioning, scraping, sponging, stinging, and trampling the surfaces of SAMs and accessory bisexual cone axes?

    Deciphering evolutionary complexities behind vertical transmission of viruses in insects, cross-Kingdom horizontal movement of TEs, and HT, might help us to better model coevolution of insect antagonist- and seed plant host tool kits.


    Conclusions on the Origin of Angiosperms:

    I propose that insect- and fungal-seed plant interactions at the molecular level led to diversification in seed plant lineages, evo-devo of the short- (spur-) shoot, and evolution of protoflowers from bisexual cone axes. Therefore, it is not surprising that similarities exist among the HTH DNA-binding motifs of some homeodomain regulatory proteins and the seven-helix fold of the Leafy switch (Hamès et al. 2008).

    Was Triassic Pangaea a "world devoid of angiosperms" (page 295, Conclusions, Labandeira 2014). No, according to Cornet (1986, 1989, 1993), Zavada (2007), and Hochuli and Feist-Burkhardt (2004, 2013).

    Does APG IV have any bearing on the origin and early dispersal of flowering plants, including ANA grade angiosperms, as suggested by J. A. Doyle (2012) and Buerki et al. (2014)? No.

    "... The congruence of the stratigraphic sequence of pollen types and their presumed evolutionary sequence would make no sense if angiosperms had already diversified in a hidden homeland area; there is no reason to expect that groups would migrate into better-known areas in the order in which they evolved much earlier ... " (page 303, Status of the Problem Prior to Molecular Systematics, J. A. Doyle 2012).

    Theißen and Saedler's (2001), Baum and Hileman's (2006), and Theißen and Melzer's (2007) molecular evolutionary models of cis-acting enzyme quartets is now the most widely accepted explanation for the evolution of floral regulators (Melzer et al. 2010).

    Despite an apparent lack of enthusiasm by Labandeira (2014), the paleobiology of coevolution of insect antagonist and seed plant host was potentially reciprocal, simultaneous, and specialized.

    Surprisingly, Labandeira's findings (2014) might also help disprove the notion of a Hauterivian (Lower Cretaceous) origin of flowering plants (Hughes 1994, Friis et al. 2013), which is strangely incongruent with the stratigraphic distribution of Afropollis throughout the Mesozoic, because coevolution of insects and flowers is unsupported by macroecological data in a 35 million year interval in geologic time from Barremian to Turonian.

    "Angiosperms certainly contributed to the spectacular diversity of beetles, but these insects were well on their way at least 100 million years before angiosperms came on the scene ... "

    The preceding statement is quoted from page 399 of David Grimaldi and Michael S. Engel (2005), Evolution of the Insects. Cambridge: Cambridge University Press, 755 pp.

    A milestone research report on the molecular systematics of insect nuclear genes by Misof et al. (2014) suggest Early Cretaceous "spectacular diversifications" of ants, bees, butterflies, moths, flies, and wasps with "the radiation of flowering plants."

    Yet, the elaborate and "statistically-robust" phylogenomic study by Misof et al. (2014) is questioned in a later reanalysis of the data by K. Jun Tong et al. (2015), which employed Bayesian priors and added calibrations and discussion of paleoentomological evidence published in vast literature on insect fossils.

    "... we estimate the ages of the megadiverse orders Diptera [flies] and Lepidoptera [butterflies and moths] at ≈266 and ≈263 Ma [million years ago], respectively. These are ≈100 My [million years] earlier than those of Misof et al. [2014]. Our estimates are consistent with the fossil record ... and challenge the hypothesis that these two orders diversified contemporaneously with angiosperms" (quoted from K. Jun Tong et al. 2015, words in brackets [] are mine).

    Based on cladistic studies of ornithischian tetrapod ghost lineages (Weishampel and Jianu 2000) and paleoecological data it was unlikely that dinosaurians invented flowers (Barrett and Willis 2001).

    There is little doubt that Bayesian computational molecular-clock simulations by Beaulieu et al. (2015) predict angiosperm occurrences in Anisian times and places, which are supported by Hochuli and Feist-Burkhardt palynological data (2004, 2013), and a calibrated phylogenomic timescale (C. S. P. Foster et al. 2017).

    By reviewing the vast literature on tool kit evo-devo and by incorporating results of molecular-phylogenetic studies, and when modeling of the alpha (α)- swarm of WGDs by Jiao and colleagues is considered, I have reached a surprising conclusion that intergeneric hybrids between Permo-carboniferous gigantopteroids including Delnortea abbottiae, Evolsonia texana, Zeilleriopteris wattii, and species of Vojnovskyales constitute the ancestors of the first angiosperm allopolyploids.

    Choice of Hcs and Hxs as evolutionarily-significant oxygen-binding proteins of the early divergent arthropod developmental tool kit tie-in with the evolution of insect legs and wings from bilaterian gills. Ancient insect wings probably functioned as respiratory organs. Wings, halteres, arachnid spinnerets, and insect legs are all organs that develop from limb fields of cells where Ubx expression is prevalent (S. B. Carroll et al. 2005).

    Ancient WGDs are implicated at the heart of the eudicots (Jiao et al. 2012). Further, an exhaustive genomic study of the cultivated grape overwhelmingly supports the existence of paleohexaploidy (Jaillon et al. 2007), which is equivalent to the "γ triplication" cited by Jiao et al. (2011).

    A divergence of angiosperms from the MRCA is probably much older than suggested by paleontologic data, which casts considerable doubt on many of J. A. Doyle's so-called combined molecular- and morphological- seed plant phylogenies. If the flowering plant crown node is centered in the Middle Triassic (C. S. P. Foster et al. 2017), then most of the seed plant groups discussed by J. A. Doyle (1978, 1994, 1996, 1998, 2001, 2006, 2008) could not possibly have anything to do with the origin of angiosperms.

    Further, it is may be prudent for Chanderbali et al. (2016) to define the seed plant cone and flower with greater morphological precision, to incorporate opposing points of view published by another plant biologist (Becker 2016), and to rethink their ideas on evolution of Amborellanae and the timing of the appearance in the fossil record of the so-called first flower.

    Certainly a Triassic or even older Permian origin of flowering plants is likely (Stephen A. Smith et al. 2010, Magallón 2010, 2014; Magallón et al. 2015, C. S. P. Foster et al. 2017).

    By incorporating advances in evo-devo and the paleobiology of auxin regulation of tool kits, by identifying morphological fingerprints discerned from permineralized seed plant organs, and by study of insect antagonists, the paleoecology of populations of delnorteas, evolsonias, and sandrewias might be better understood. Paleobiological proof of some of these ideas and disentangling a putative hybrid origin of flowering plants is an elusive and challenging exercise.

    Making progress on understanding at least some aspects of the enigmatic origin of angiosperms is possible by applying mathematical scaling to explicit models of whole- organ and short- (spur-) shoot morphospace compiled from biometry of detached and shed fossilized seed plant organs, by calibrating tool kit phylogenies, and by applying proxies to infer at least some paleoecologies of whole mother seed plants as insect habitat.

    Studies of the Amborella trichopoda genome landscape are probably unhelpful in solving the likely allopolyploid origins of angiosperms. The evolution of flowering plants from a nexus of Permo-carboniferous seed plant ancestors, and deciphering morphological-development of angio-ovuliferous cones and protoflowers might never be fully understood. The origin of angiosperms is a conundrum.


    Literature Cited on the Origin of Angiosperms:

    Abdel-latief, M. 2007. A family of chemoreceptors in Tribolium castaneum (Tenebrionidae: Coleoptera). PLoS ONE 2(12): e1319.

    Achard, P., M. Baghour, A. Chapple, P. Hedden, D. van der Straeten, P. Genschik, T. Moritz, and N. P. Harberd. 2007. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proceedings of the National Academy of Sciences 104(15): 6484-6489.

    Achard, P., J.-P. Renou, R. Berthomé, N. P. Harberd, and P. Genschik. 2008. Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biology 18: 656-660.

    Ackerman, C. M., Q. Yu, S. Kim, R. E. Paull, P. H. Moore, and R. Ming. 2008. B-class MADS-box genes in trioecious papaya: two paleoAP3 paralogs, CpTM6-1 and CpTM6-2, and a PI ortholog CpPI. Planta 227(4): 741-753.

    Adam, H., S. Jouannic, J. Escoute, Y. Duval, J-L. Verdeil, and J. W. Tregear. 2005. Reproductive developmental complexity in the African oil palm (Elaeis guineensis, Arecaceae). American Journal of Botany 92(11): 1836-1852.

    Adam, H., S. Jouannic, F. Morcillo, J-L. Verdeil, Y. Duval, and J. W. Tregear. 2007. Determination of flower structure in Elaeis guineensis: do palms use the same homeotic genes as other species? Annals of Botany 99(6): 1-12.

    Aida, M. and M. Tasaka. 2006. Genetic control of shoot organ boundaries. Current Opinion in Plant Biology 9(1): 72-77.

    Aida, M. and M. Tasaka. 2006. Morphogenesis and patterning at the organ boundaries in the higher plant shoot apex. Plant Molecular Biology 60: 915-928.

    Albert, V. A., D. G. Oppenheimer, and C. Lindqvist. 2002. Pleiotropy, redundancy and the evolution of flowers. Trends in Plant Science 7(7): 297-301.

    Algeo, T. J. and R. J. Twitchett. 2010. Anomalous early Triassic sediment fluxes due to elevated weathering rates and their biological consequences. Geology 38(11): 1023-1026.

    Alvarez, J. P., A. Goldshmidt, I. Efroni, J. L. Bowman, and Y. Eshed. 2009. The NGATHA distal organ developmental genes are essential for style specification in Arabidopsis. The Plant Cell 21: 1373-1393.

    Alvarez, J. M., J. Sohlberg, P. Engström, Tianqing Zhu, M. Englund, P. N. Moschou, and S. von Arnold. 2015. The WUSCHEL-RELATED HOMEOBOX 3 gene PaWOX3 regulates lateral organ formation in Norway spruce. New Phytologist 208(4): 1078–1088.

    Alvarez-Buylla, E. R., E. Azpeitia, R. Barrio, M. Benítez, and P. Padilla-Longoria. 2010. From ABC genes to regulatory networks, epigenetic landscapes and flower morphogenesis: making biological sense of theoretical approaches. Seminars in Cell & Developmental Biology 21(1): 108-117.

    Alvarez-Buylla, E. R., S. Pelaz, S. J. Liljegren, S. E. Gold, C. Burgeff, G. S. Ditta, L. R. de Pouplana, L. Martinez-Castilla, and M. F. Yanofsky. 2000. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proceedings of the National Academy of Sciences 97(10): 5328-5333.

    Alves-Ferreira, M., F. Wellmer, A. Banhara, V. Kumar, J. L. Riechmann, and E. M. Meyerowitz. 2007. Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiology 145: 747-762.

    Amborella Genome Project. 2013. The Amborella genome and the evolution of flowering plants. Science 342(6165): 1467.

    Anderson, B. and S. D. Johnson. 2008. The geographical mosaic of coevolution in a plant-pollinator mutualism. Evolution 62(1): 220-225.

    Anderson, B., J. S. Terblanche, and A. G. Ellis. 2010. Predictable patterns of trait mismatches between interacting plants and insects. BMC Evolutionary Biology 10: 204.

    Anderson, Edgar. 1934. Origin of the angiosperms. Nature 133: 462.

    Aoki, S., K. Uehara, M. Imafuku, M. Hasebe, and M. Ito. 2004. Phylogeny and divergence of basal angiosperms inferred from APETALA3- and PISTILLATA-like MADS-box genes. Journal of Plant Research 117(3): 229-244.

    APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20.

    Aravind, L., V. Anantharaman, S. Balaji, M. M. Babu, and L. M. Iyer. 2005. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiology Reviews 29: 231-262.

    Arber, E. A. N. and J. Parkin. 1907. On the origin of angiosperms. Botanical Journal of the Linnaean Society 38: 28-80.

    Arias, T. and J. H. Williams. 2008. Embryology of Manekia naranjoana (Piperaceae) and the origin of tetrasporic 16-nucleate female gametophytes in Piperales. American Journal of Botany 95(3): 272-285.

    Ariizumi, T. and K. Toriyama. 2011. Genetic regulation of sporopollenin synthesis and pollen exine development. Annual Review of Plant Biology 62: 437-460.

    Arthur, W. 2002. The emerging conceptual framework of evolutionary developmental biology. Nature 415: 757-764.

    Asama, K. 1982. Evolution and phylogeny of vascular plants based on the principles of growth retardation: Part 5. Origin of angiosperms inferred from the evolution of leaf forms. Bulletin of the National Science Museum, Tokyo, Series C (Geology) 8: 43-58.

    Asama, K. 1985. Permian to Triassic floral changes and some problems of the paleobiogeography, parallelism, mixed floras, and the origin of angiosperms. Pp. 199-218 In: K. Nakazawa and J. M. Dickens (eds.), The Tethys. Tokyo: Tokyo University Press.

    Ash S. 1997. Evidence of arthropod-plant interactions in the Upper Triassic of the Southwestern United States. Lethaia 29: 237-248.

    Ash, S. R. and S. T. Hasiotis. 2013. New occurrences of the controversial late Triassic plant fossil Sanmiguelia Brown and associated ichnofossils in the Chinle Formation of Arizona and Utah, USA. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 268(1): 65-82.

    Axelrod, D. I. 1952. A theory of angiosperm evolution. Evolution 6(1): 29-60.

    Axelrod, D. I. 1959. Poleward migration of early angiosperm flora - angiosperms only displaced the relict Jurassic-type flora at high latitudes in late Cretaceous time. Science 130(3369): 203-207.

    Axelrod, D. I. 1970. Mesozoic paleogeography and early angiosperm history. Botanical Review 36(3): 277-319.

    Axsmith, B. J., R. Serbet, M. Krings, T. N. Taylor, E. L. Taylor, and S. H. Mamay. 2003. The enigmatic Paleozoic plants Spermopteris and Phasmatocycas reconsidered. American Journal of Botany 90(11): 1585-1595.

    Axtell, M. J. and D. P. Bartel. 2005. Antiquity of microRNAs and their targets in land plants. The Plant Cell 17: 1658-1673.

    Axtell, M. J. and J. L. Bowman. 2008. Evolution of plant microRNAs and their targets. Trends in Plant Science 13(7): 343-349.

    Axtell, M. J., J. A. Snyder, and D. P. Bartel. 2007. Common functions for diverse small RNAs of land plants. The Plant Cell 19: 1750-1769.

    Bailey, I. W. 1949. Origin of the angiosperms: need for a broadened outlook. Journal of the Arnold Arboretum 30: 64-70.

    Bailey, I. W. and A. C. Smith. 1942. Degeneriaceae, a new family of flowering plants from Fiji. Journal of the Arnold Arboretum 23: 356-365.

    Bainbridge, K., S. Guyomarc'h, E. Bayer, R. Swarup, M. Bennett, T. Mandel, and C. Kuhlemeier. 2008. Auxin influx carriers stabilize phyllotactic patterning. Genes and Development 22: 810-823.

    Balbi, V. and A. Devoto. 2008. Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytologist 177: 301-318.

    Baldwin, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences 95: 8113-8118.

    Ballaré, C. L. 2011. Jasmonate-induced defenses: a tale of intelligence, collaborators, and rascals. Trends in Plant Science 16(5): 249-257.

    von Balthazar, M., J. Schönenberger, and T. Denk. 2008. In search of the earliest flowers: introduction. International Journal of Plant Sciences 169(7): 815.

    Barakat, A., K. Wall, J. Leebens-Mack, Y. J. Wang, J. E. Carlson, and C. W. dePamphilis. 2007. Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. The Plant Journal 51(6): 991-1003.

    Barbakadze, N., S. Enders, S. Gorb, and E. Arzt. 2006. Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabacidae). Journal of Experimental Biology 209(4): 722-730.

    Bari, R. and J. D. G. Jones. 2009. Role of plant hormones in plant defence responses. Plant Molecular Biology 69(4): 473-488.

    Baroux, C., C. Spillane, and U. Grossniklaus. 2002. Evolutionary origins of the endosperm in flowering plants. Genome Biology 3(9).

    Barrett, P. M. 2014. Paleobiology of herbivorous dinosaurs. Annual Review of Earth and Planetary Sciences 42: 207-230.

    Barrett, P. M. and K. J. Willis. 2001. Did dinosaurs invent flowers? Dinosaur-angiosperm coevolution revisited. Biological Reviews of the Cambridge Philosophical Society 76: 411-447.

    Barton, M. K. 2010. Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Developmental Biology 341: 95-113.

    Bascompte, J., P. Jordano, C. J. Melián, and J. M. Olesen. 2003. The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences 100(16): 9383-9387.

    Bastolla, U., M. A. Fortuna, A. Pascual-García, A. Ferrera, B. Luque, and J. Bascompte. 2009. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458: 1018-1020.

    Bateman, R. A., J. Hilton, and P. J. Rudall. 2006. Morphological and molecular phylogenetic context of angiosperms: contrasting the "top-down" and "bottom-up" approaches used to infer the likely characteristics of the first flowers. Journal of Experimental Botany 57(13): 3471-3503.

    Baum, D. A. 1998. The evolution of plant development. Current Opinion in Plant Biology 1(1): 79-86.

    Baum, D. A. and M. J. Donoghue. 2002. Transformation of function, heterotopy, and the evolution of plant development. Pp. 52-69 In: Q. C. B. Cronk, R. Bateman, and J. Hawkins (eds.), Developmental Genetics and Plant Evolution, The Systematics Association Special Volume Series 65. London: Taylor and Francis, 543 pp.

    Baum, D. A. and L. C. Hileman. 2006. A developmental genetic model for the origin of the flower. Pp. 3-27 In: C. Ainsworth (ed.), Volume 20, Annual Plant Reviews, Flowering and Its Manipulation. Sheffield: Blackwell, 304 pp.

    Baumann, K., M. Perez-Rodriguez, D. Bradley, J. Venail, P. Bailey, H. Jin, R. Koes, K. Roberts, and C. Martin. 2007. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134: 1691-1701.

    Beaulieu, J. M., B. C. O'Meara, P. R. Crane, and M. J. Donoghue. 2015. Heterogeneous rates of molecular evolution and diversification could explain the Triassic age estimate for angiosperms. Systematic Biology 64(5): 869-878.

    Bäurle, I. and T. Laux. 2003. Apical meristems: the plant's fountain of youth. BioEssays 25(10): 961-970.

    Becerra, J. X., K. Noge, and D. L. Venable. 2009. Macroevolutionary chemical escalation in an ancient plant-herbivore arms race. Proceedings of the National Academy of Sciences 106(43): 18062-18066.

    Beck, A. L. and C. C. Labandeira. 1998. Early Permian folivory on a gigantopterid-dominated riparian flora from North central Texas. Palaeogeography, Palaeoclimatology, Palaeoecology 142: 139-173.

    Beck, C. B. (ed.) 1976. Origin and Early Evolution of Angiosperms. New York: Columbia University Press.

    Becker, A. 2016. Tinkering with transcription factor networks for developmental robustness in Ranunculales flowers. Annals of Botany 117: 845-858.

    Becker, A. and G. Theißen. 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics and Evolution 29: 464-489.

    Becker, A., K.-U. Winter, B. Meyer, H. Saedler, and G. Theißen. 2000. MADS-Box gene diversity in seed plants 300 million years ago. Molecular Biology and Evolution 17(10): 1425-1434.

    Beerling, D. J. and R. A. Berner. 2000. Impact of a Permo-Carboniferous high O2 event on the terrestrial carbon cycle. Proceedings of the National Academy of Sciences 97(23): 12428-12432.

    Beerling, D. J. and R. A. Berner. 2002. Biogeochemical constraints on the Triassic-Jurassic boundary carbon cycle event. Global Biogeochemical Cycles 16(3): 1036.

    Beerling, D. J. and R. A. Berner. 2004. Feedbacks and the coevolution of plants and atmospheric CO2. Proceedings of the National Academy of Sciences 102: 1302-1305.

    Beerling, D. J. and A. J. Fleming. 2007. Zimmermann's telomb theory of megaphyll leaf evolution: a molecular and cellular critique. Current Opinion in Plant Biology 10: 4-12.

    Beerling, D. J., C. P. Osborne, and W. G. Chaloner. 2001. Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the late Paleozoic era. Nature 410: 352-354.

    Belcher, C. M., J. M. Yearsley, R. M. Hadden, J. C. McElwain, and G. Rein. 2010. Baseline intrinsic flammability of Earth's ecosystems estimated from paleoatmospheric oxygen over the past 350 million years. Proceedings of the National Academy of Sciences 107(52): 22448-22453.

    Bellaïche, Y. and E. Munro. 2009. Pushing the frontiers of development. Development 136(2): 173-177.

    Bemer, M., M. Wolters-Arts, U. Grossniklaus, and G. C. Angenent. 2008. The MADS domain protein DIANA acts together with AGAMOUS-like80 to specify the central cell in Arabidopsis ovules. The Plant Cell 20: 2088-2101.

    Bennett, M. D. and I. J. Leitch. 2005. 2. Genome size evolution in plants. Pp. 89-162 In: T. R. Gregory (ed.), The Evolution of the Genome. Burlington: Elsevier Academic Press, 740 pp.

    Benton, M. J. and R. J. Twitchett. 2003. How to kill (almost) all life: the end-Permian extinction event. Trends in Ecology and Evolution 18(7): 358-365.

    Berendse, F. and M. Scheffer. 2009. The angiosperm radiation revisited, an ecological explanation for Darwin's 'abominable mystery.' Ecology Letters 12(9): 865-872.

    Berger, F., Y. Hamamura, M. Ingouff, and T. Higashiyama. 2008. Double fertilization - caught in the act. Trends in Plant Science 13(8): 437-443.

    Bergthorsson, A., O. Richardson, G. J. Young, L. R. Goertzen, and J. D. Palmer. 2004. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proceedings of the National Academy of Sciences 101(51): 17747-17752.

    Bernasconi, G., T.-L. Ashman, T. R. Birkhead, J. D. D. Bishop, U. Grossniklaus, E. Kubli, D. L. Marshall, B. Schmid, I. Skogsmyr, R. R. Snook, D. Taylor, I. Till-Bottraud, P. I. Ward, D. W. Zeh, and B. Hellriegel. 2004. Evolutionary ecology of the prezygotic stage. Science 303: 971-975.

    Berner, R. A. 1999. Atmospheric oxygen over Phanerozoic time. Proceedings of the National Academy of Sciences 96(20): 10955-10957.

    Berner, R. A. 2002. Examination of hypotheses for the Permo-Triassic boundary extinction by carbon cycle modeling. Proceedings of the National Academy of Sciences 99(7): 4172-4177.

    Berner, R. A. 2005. The carbon and sulfur cycles and atmospheric oxygen from middle Permian to middle Triassic. Geochimica et Cosmochimica Acta 69(13): 3211-3217.

    Berner, R. A. 2006. GEOCARBSULF: A combined model for Phanerozoic atmospheric O2 and CO2. Geochimica et Cosmochimica Acta 70(23): 5653-5664.

    Berner, R. A. 2006. Carbon, sulfur, and O2 across the Permian-Triassic boundary. Journal of Geochemical Exploration 88: 416-418.

    Berner, R. A. and Z. Kothavala. 2001. GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. American Journal of Science 301: 182-204.

    Bernhardt, P. 2000. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Plant Systematics and Evolution 222(1-4): 293-320.

    Bernhardt, P., T. Sage, P. Weston, H. Azuma, M. Lam, L. B. Thien, and J. Bruhl. 2003. The pollination of Trimenia moorei (Trimeniaceae): floral volatiles, insect/wind pollen vectors and stigmatic self-incompatibility in a basal angiosperm. Annals of Botany 92: 445-458.

    Besson-Bard, A., C. Courtois, A. Gauthier, J. Dahan, G. Dobrowolska, S. Jeandroz, A. Pugin, and D. Wendehenne. 2008. Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Molecular Plant 1(2): 218-228.

    Besson-Bard, A., A. Pugin, and D. Wendehenne. 2008. New insights into nitric oxide signaling in plants. Annual Review of Plant Biology 59: 21-39.

    Béthoux, O., F. Papier, and A. Nel. 2005. The Triassic radiation of the entomofauna. Comptes Rendus Palevol 4: 609-621.

    Bharathan, G., T. E. Goliber, C. Moore, S. Kessler, T. Pham, and N. R. Sinha. 2002. Homologies in leaf form inferred from KNOX1 gene expression during development. Science 296: 1858-1860.

    Bharathan, G., B.-J. Janssen, E. A. Kellogg, and N. R. Sinha. 1997. Did homeodomain proteins duplicate before the origin of angiosperms, fungi, and metazoa? Proceedings of the National Academy of Sciences 94(25): 13749-13753.

    Bharathan, G., B.-J. Janssen, E. A. Kellogg, and N. R. Sinha. 1999. Phylogenetic relationships and evolution of the KNOTTED class of plant homeodomain proteins. Molecular Biology and Evolution 16(4): 553-563.

    Bilsborough, G. D., A. Runions, M. Barkoulas, H. W. Jenkins, A. Hasson, C. Galinha, P. Laufs, A. Hay, P. Prusinkiewicz, and M. Tsiantis. 2011. Model for the regulation of Arabidopsis thaliana leaf development. Proceedings of the National Academy of Sciences 108(8): 3424-3429.

    Biondi, S., S. Scaramagli, F. Capitani, M. M. Altamura, and P. Torrigiani. 2001. Methyl jasmonate upregulates biosynthetic gene expression, oxidation and conjugation of polyamines, and inhibits shoot formation in tobacco thin layers. Journal of Experimental Botany 52(355): 231-245.

    Bishop, J. W., I. P. Montañez, E. L. Gulbranson, and P. L. Brenckle. 2009. The onset of mid-Carboniferous glacioeustasy: sedimentologic and diagenetic constraints, Arrow Canyon, Nevada. Palaeogeography, Palaeoclimatology, and Palaeoecology 276(1-4): 217-243.

    Blanvillain, R., L. C. Boavida, S. McCormick, and D. W. Ow. 2008. EXPORTIN1 genes are essential for development and function of the gametophytes in Arabidopsis thaliana. Genetics 180: 1493-1500.

    Blanc, G. and K. H. Wolfe. 2004. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. The Plant Cell 16: 1667-1678.

    Blanc, G. and K. H. Wolfe. 2004. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. The Plant Cell 16: 1679-1691.

    Blanco, F., P. Salinas, N. M. Cecchini, M. E. Alvarez, and L. Holuigue. 2009. Early genomic responses to salicylic acid in Arabidopsis. Plant Molecular Biology 70(1-2): 79-102.

    Blumenstiel, J. P. 2011. Evolutionary dynamics of transposable elements in a small RNA world. Trends in Genetics 27(1): 23-31.

    Bohm, B. A. 1998. Introduction to Flavonoids, Chemistry and Biochemistry of Organic Products, Volume 2. Amsterdam: Harwood Academic Publishers, Overseas Publishers Association, 503 pp.

    Bohn-Courseau, I. 2010. Auxin: a major regulator of organogenesis. Comptes Rendus Biologies 333(4): 290-296.

    Bolduc, N., D. O'Connor, J. Moon, M. Lewis, and S. Hake. 2012. How to pattern a leaf. Cold Spring Harbor Symposia on Quantitative Biology 77: 47-51.

    Bolle, C. 2004. The role of GRAS proteins in plant signal transduction and development. Planta 218(5): 683-692.

    Bond, D. P. G. and P. B. Wignall. 2010. Pyrite framboid study of marine Permian-triassic boundary sections: a complex anoxic event and its relationship to contemporaneous mass extinction. GSA Bulletin 122(7-8): 1265-1279.

    Bonis, N. R., W. M. Kürschner, and L. Krystyn. 2009. A detailed palynological study of the Triassic-Jurassic transition in key sections of the Eiberg Basin (northern calcareous Alps, Austria). Review of Palaeobotany and Palynology 156(3-4): 376-400.

    Bonneton, F., A. Chaumot, and V. Laudet. 2008. Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Insect Biochemistry and Molecular Biology 38: 416-429.

    Bonneton, F., D. Zelus, T. Iwema, M. Robinson-Rechavi, and V. Laudet. 2003. Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between ECR and USP-RXR. Molecular Biology and Evolution 20(4): 541-553.

    Borg, M., L. Brownfield, and D. Twell. 2009. Male gametophyte development: a molecular perspective. Journal of Experimental Botany 60(5): 1465-1478.

    Borok, M. J., D. A. Tran, M. C. W. Ho, and R. A. Drewell. 2010. Dissecting the regulatory switches of development: lessons from enhancer evolution in Drosophila. Development 137(1): 5-13.

    Boudet, A.-M. 2007. Evolution and current status of research in phenolic compounds. Phytochemistry 68(22-24): 2722-2735.

    Bowe, L. M., G. Coat, and C. W. dePamphilis. 2000. Phylogeny of seed plants based on all three genomic compartments: Extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proceedings of the National Academy of Sciences 97(8): 4092-4097.

    Bowers, J. E., B. A. Chapman, J. Rong, and A. H. Paterson. 2003. Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.

    Boyce, C. K. 2005. Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31(1): 117-140.

    Boyce, C. K., T. J. Brodribb, T. S. Field, and M. A. Zwieniecki. 2009. Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society of London, Series B, Biological Sciences 276(1663): 1771-1776.

    Boyce, C. K. and A. H. Knoll. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28(1): 70-100.

    Braam, J. 2005. In touch: plant responses to mechanical stimuli. New Phytologist 165: 373-389.

    Braam, J. and R. W. Davis. 1990. Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60: 357-364.

    Bray, P. S. and K. B. Anderson. 2009. Identification of Carboniferous (320 million years old) class 1c amber. Science 326(5949): 132-134.

    Braybrook, S. A. and C. Kuhlemeier. 2010. How a plant builds leaves. The Plant Cell 22(4): 1006-1018.

    Brigandt, I. 2003. Homology in comparative, molecular, and evolutionary developmental biology: the radiation of a concept. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 299B(1): 9-17.

    Briscoe, A. D. and L. Chittka. 2001. The evolution of color vision in insects. Annual Review of Entomology 46: 471–510.

    Brodribb, T. J. and S. A. M. McAdam. 2011. Passive origins of stomatal control in vascular plants. Science 331(6017): 582-585.

    Brodribb, T. J., T. S. Feild, and G. J. Jordan. 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144: 1890-1898.

    Bronstein, J. L., R. Alarcón, and M. Geber. 2006. The evolution of plant-insect mutualisms. New Phytologist 172: 412-428.

    Brown, R. H., D. L. Nickrent, and C. S. Gasser. 2010. Expression of ovule and integument-associated genes in reduced ovules of Santalales. Evolution and Development 12: 231-240.

    Buerki, S., F. Forest, and N. Alvarez. 2014. Proto-southeast Asia as a trigger of early angiosperm diversification. Botanical Journal of the Linnean Society 174(3): 326–333.

    Burger, W. C. 1981. Heresy revived: the Monocot Theory of angiosperm origin. Evolutionary Theory 5: 189-225.

    Burmester, T. 2001. Molecular evolution of the arthropod hemocyanin superfamily. Molecular Biology and Evolution 18: 184-195.

    Burmester, T. 2004. Evolutionary history and diversity of arthropod hemocyanins. Micron 35(1-2): 121-122.

    Burmester, T. and T. Hankein. 2007. The respiratory proteins of insects. Journal of Insect Physiology 53(4): 285-294.

    Burmester, T., H. C. Massey, Jr., S. O. Zakharkin, and H. Benes. 1998. The evolution of hexamerins and the phylogeny of insects. Journal of Molecular Evolution 47(1): 93-108.

    Burmester, T., J. Storf, A. Hasenjäger, S. Klawitter, and T. Hankein. 2006. The hemoglobin genes of Drosophila. FEBS Journal 273(3): 468-480.

    Busov, V. B., A. M. Brunner, and S. H. Strauss. 2008. Genes for control of plant stature and form. New Phytologist 177: 589-607.

    Butler, R. J., P. M. Barrett, P. Kenrick, and M. G. Penn. 2009. Diversity patterns amongst herbivorous dinosaurs and plants during the Cretaceous: implications for hypotheses of dinosaur/angiosperm coevolution. Journal of Evolutionary Biology 22(3): 446-459.

    Butler, R. J., P. M. Barrett, P. Kenrick, and M. G. Penn. 2009. Testing coevolutionary hypotheses over geological timescales: interactions between Mesozoic non-avian dinosaurs and cycads. Biological Reviews 84(1): 73-89.

    Butler, R. J., P. M. Barrett, M. G. Penn, and P. Kenrick. 2010. Testing coevolutionary hypotheses over geological timescales: interactions between Cretaceous dinosaurs and plants. Biological Journal of the Linnean Society 100(1): 1-15.

    Buzgo, M., P. S. Soltis, S. Kim, and D. E. Soltis. 2005. The making of the flower. Biologist 52(3): 149-154.

    Buzgo, M., P. S. Soltis, and D. E. Soltis. 2004. Floral developmental morphology of Amborella trichopoda (Amborellaceae). International Journal of Plant Sciences 165(6): 925-947.

    Cai, G. and M. Cresti. 2009. Organelle motility in the pollen tube: a tale of 20 years. Journal of Experimental Botany 60(2): 495-508.

    Cailleau, A., P.-C. Cheptou, and T. Lenormand. 2010. Ploidy and the evolution of endosperm of flowering plants. Genetics 184: 439-453.

    Callier, V. and H. F. Nijhout. 2013. Body size determination in insects: a review and synthesis of size- and brain-dependent and independent mechanisms. Biological Reviews 88(4): 944-954.

    Canright, J. E. 1952. The comparative morphology and relationships of the Magnoliaceae. I. Trends of specialization in the stamens. American Journal of Botany 39: 484-497.

    Cao, C., G. D. Love, L. E. Hays, W. Wang, S. Shen, and R. E. Summons. 2009. Biogeochemical evidence for euxinic oceans and ecological disturbance presaging the end-Permian mass extinction event. Earth and Planetary Science Letters 281(3-4): 188-201.

    Carlquist, S. 2009. Xylem heterochrony: an unappreciated key to angiosperm origin and diversifications. Botanical Journal of the Linnaean Society 161(1): 26-65.

    Carlsbecker, A., J. F. Sundström, M. Englund, D. Uddenberg, L. Izquierdo, A. Kvarnheden, F. Vergara-Silva, and P. Engström. 2013. Molecular control of normal and acrocona mutant seed cone development in Norway spruce (Picea abies) and the evolution of conifer ovule-bearing organs. New Phytologist 200(1): 261-275.

    Carmichael, J. S. and W. E. Friedman. 1995. Double fertilization in Gnetum gnemon: the relationship between the cell cycle and sexual reproduction. The Plant Cell 7: 1975-1988.

    Carmichael, J. S. and W. E. Friedman. 1996. Double fertilization in Gnetum gnemon (Gnetaceae): its bearing on the evolution of sexual reproduction within the Gnetales and the anthophyte clade. American Journal of Botany 83: 767-780.

    Carraro, N., A. Peaucelle, P. Laufs, and J. Traas. 2006. Cell differentiation and organ initiation at the shoot apical meristem. Plant Molecular Biology 60: 811-826.

    Carroll, S. B. 1995. Homeotic genes and the evolution of arthropods and chordates. Nature 376: 479-485.

    Carroll, S. B. 2005. Evolution at two levels: on genes and form. PLoS Biology 3(7): 1159-1166.

    Carroll, S. B. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134(1): 25-36.

    Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2005. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. Malden: Blackwell Publishing, 258 pp.

    Cascales-Miñana, B., C. J. Cleal, P. Gerrienne. 2016. Is Darwin's 'Abominable Mystery' still a mystery today? Cretaceous Research 61: 256–262.

    Causier, B., D. Bradley, H. Cook, and B. Davies. 2009. Conserved intragenic elements were critical for the evolution of floral C-function. The Plant Journal 58(1): 41-52.

    Causier, B., R. Castillo, Y. Xue, Z. Schwarz-Sommer, and B. Davies. 2010. Tracing the evolution of the floral homeotic B- and C-function genes through genome synteny. Molecular Biology and Evolution 27(11): 2651-2664.

    Causier, B., Z. Schwarz-Sommer, and B. Davies. 2010. Floral organ identity: the 20 years of ABCs. Seminars in Cell & Developmental Biology 21(1): 73-79.

    Chahtane, H., G. Vachon, M. Le Masson, E. Thévenon, S. Périgon, N. Mihajlovic, A. Kalinina, R. Michard, E. Moyroud, M. Monniaux, C. Sayou, V. Grbic, F. Parcy, and G. Tichtinsky. 2013. A variant of LEAFY reveals its capacity to stimulate meristem development by inducing RAX1. The Plant Journal 74(4): 678-689.

    Chamala, S., A. S. Chanderbali, J. P. Der, T. Lan, B. Walts, V. A. Albert, C. W. dePamphilis, J. Leebens-Mack, S. Rounsley, S. C. Schuster, R. A. Wing, N. Xiao, R. Moore, P. S. Soltis, D. E. Soltis, and W. B. Barbazuk. 2013. Assembly and validation of the genome of the nonmodel basal angiosperm Amborella. Science 342(6165): 1516-1517.

    Champagne, C. E. M., T. E. Goliber, M. F. Wojciechowski, R. W. Mei, B. T. Townsley, K. Wang, M. M. Paz, R. Geeta, and N. R. Sinha. 2007. Compound leaf development and evolution in the legumes. The Plant Cell 19: 3369-3378.

    Chanderbali, A. S., B. A. Berger, D. A. Howarth, P. S. Soltis, and D. E. Soltis. 2016. Evolving ideas on the origin and evolution of flowers: new perspectives in the genomic era. Genetics 202: 1255-1265.

    Chanderbali, A. S., S. Kim, M. Buzgo, Z. Zheng, D. G. Oppenheimer, D. E. Soltis, and P. S. Soltis. 2006. Genetic footprints of stamen ancestors guide perianth evolution in Persea (Lauraceae). International Journal of Plant Sciences 167(6): 1075-1089.

    Chanderbali, A. S., M-J. Yoo, L. M. Zahn, S. F. Brockington, P. K. Wall, M. A. Gitzendanner, V. A. Albert, J. Leebens-Mack, N. S. Altman, H. Ma, C. W. dePamphilis, D. E. Soltis, and P. S. Soltis. 2010. Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower. Proceedings of the National Academy of Sciences 107(52): 22570-22575.

    Chapman, B. A., J. E. Bowers, F. A. Feltus, and A. H. Paterson. 2006. Buffering of crucial functions by paleologous duplicated genes may contribute cyclicity to angiosperm genome duplication. Proceedings of the National Academy of Sciences 103(8): 2730-2735.

    Charles, J. P. 2010. The regulation of expression of insect cuticle protein genes. Insect Biochemistry and Molecular Biology 40(3): 205-213.

    Chartier, M., F. Jabbour, S. Gerber, P. Mitteroecker, H. Sauquet, M. von Balthazar, Y. Staedler, P. R. Crane, and J. Schönenberger. 2014. The floral morphospace - a modern comparative approach to study angiosperm evolution. New Phytologist 204: 841-853.

    de la Chaux, N. and A. Wagner. 2011. BEL/Pao retrotransposons in metazooan genomes. BMC Evolutionary Biology 11: 154.

    Chehab, E. W., E. Eich, and J. Braam. 2009. Thigmomorphogenesis: a complex plant response to mechano-stimulation. Journal of Experimental Botany 60(1): 43-56.

    Chen, M.-K., I.-C. Lin, and C.-H. Yang. 2008. Functional analysis of three lily (Lilium longiflorum) APETALA1-like MADS-box genes in regulating floral transition and formation. Plant and Cell Physiology 49(5): 704-717.

    Chen, Y.-F., N. Etheridge, G. E. Schaller. 2005. Ethylene signal transduction. Annals of Botany 95: 901-915.

    Cheng, A.-X., Y.-G. Lou, Y.-B. Mao, S. Lu, L.-J. Wang, and X.-Y. Chen. 2007. Plant terpenoids: biosynthesis and ecological functions. Journal of Integrative Plant Biology 49(2): 179-186.

    Chico, J. M., A. Chini, S. Fonseca, and R. Solano. 2008. JAZ repressors set the rhythm in jasmonate signaling. Current Opinion in Plant Biology 11(5): 486-494.

    Chittka, L. 1996. Does bee color vision predate the evolution of flower color? Naturwissenschaften 83: 136-138.

    Chittka, L., A. Schmidt, N. Troje, and R. Menzel. 1994. Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vision Research 34: 1489-1508.

    Chittka, L., J. Spaethe, A. Schmidt, and A. Hickelsberger. 2001. 6. Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. Pp. 106-126 In: L. Chittka and J. D. Thomson (eds.), Cognitive Ecology of Pollination, Animal Behaviour and Floral Evolution. Cambridge: Cambridge University Press, 344 pp.

    Cho, Y., J. P. Mower, Y.-L. Qiu, and J. D. Palmer. 2004. Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proceedings of the National Academy of Sciences 101(51): 17741-17746.

    Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

    Cirilli, S., A. Marzoli, L. Tanner, H. Bertrand, N. Buratti, F. Jourdan, G. Bellieni, D. Kontak, and P. R. Renne. 2009. Latest Triassic onset of the Central Atlantic Magmatic Province (CAMP) volcanism in the Fundy Basin (Nova Scotia): new stratigraphic constraints. Earth and Planetary Science Letters 286(3-4): 514-525.

    Clapham, M. E., S. Shen, and D. J. Bottjer. 2009. The double mass extinction revisited: reassessing the severity, selectivity, and causes of the end-Guadalupian biotic crisis (late Permian). Paleobiology 35(1): 32-50.

    Cleveland, D. M., L. C. Nordt, S. I. Dworkin, and S. C. Atchley. 2008. Pedogenic carbonate isotopes as evidence for extreme climatic events preceding the Triassic-Jurassic boundary: implications for a biotic crisis? GSA Bulletin 120(11-12): 1408-1415.

    Cleveland, D. M., L. C. Nordt, and S. C. Atchley. 2008. Paleosols, trace fossils, and precipitation estimates of the uppermost Triassic strata in northern New Mexico. Palaeogeography, Palaeoclimatology, Palaeoecology 257(4): 421-444.

    Clissold, F. J. 2008. The biomechanics of chewing and plant fracture: mechanisms and implications. Pp. 317-372 In: J. Casas and S. J. Simpson (eds.), Advances in Insect Physiology, Insect Mechanics and Control, Volume 34. Burlington: Academic Press, Elsevier, 379 pp.

    Coe, M. J., D. L. Dilcher, J. O. Farlow, D. M. Jarzen, and D. A. Russell. 1987. Dinosaurs and land plants. Pp. 225-258 In: E. M. Friis, W. G. Chaloner, and P. R. Crane (eds.), The Origins of Angiosperms and Their Biological Consequences, Cambridge: Cambridge University Press, 358 pp.

    Coen, E. S. and E. M. Meyerowitz. 1991. The war of the whorls: genetic interactions controlling floral development. Nature 353: 31-37.

    Coen, E., A.-G. Rolland-Lagan, M. Matthews, A. Bangham, P. Prusinkiewicz. 2004. The genetics of geometry. Proceedings of the National Academy of Sciences 101(14): 4728-4735.

    Colombo, L., R. Battaglia, and M. M. Katar. 2008. Arabidopsis ovule development and its evolutionary conservation. Trends in Plant Science 13(8): 444-450.

    Costanzo, E., C. Trehin, and M. Vandenbussche. 2014. The role of WOX genes in flower development. Annals of Botany (Oxford) 114 (7): 1545-1553.

    Cook, J. M., D. Bean, S. A. Power, and D. J. Dixon. 2004. Evolution of a complex coevolved trait: active pollination in a genus of fig wasps. Journal of Evolutionary Biology 17: 238-246.

    Cornell, H. V. and B. A. Hawkins. 2003. Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. The American Naturalist 161: 507-522.

    Cornet, B. 1986. The leaf venation and reproductive structures of a late Triassic angiosperm, Sanmiguelia lewisii. Evolutionary Theory 7: 231-309.

    Cornet, B. 1989. The reproductive morphology and biology of Sanmiguelia lewisii, and its bearing on angiosperm evolution in the late Triassic. Evolutionary Trends in Plants 3(1): 25-51.

    Cornet, B. 1993. Dicot-like leaf and flowers from the Late Triassic tropical Newark Supergroup Rift Zone, U.S.A. Modern Geology 19: 81-99.

    Cornet, B. and D. Habib. 1992. Angiosperm-like pollen from the ammonite-dated Oxfordian (Upper Jurassic) of France. Review of Palaeobotany and Palynology 71: 269-294.

    Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanic Garden 72: 716-793.

    Crane, P. R., E. M. Friis, and K. R. Pedersen. 1995. The origin and early diversification of angiosperms. Nature 374: 27-33.

    Crane, P. R., P. Herendeen, and E. M. Friis. 2004. Fossils and plant phylogeny. American Journal of Botany 91(10): 1683-1699.

    Crane, P. R. and P. Kenrick. 1997. Diverted development of reproductive organs: a source of morphological innovation in land plants. Plant Systematics and Evolution 206: 161-174.

    Crawford, B. C. W. and M. F. Yanofsky. 2008. The formation and function of the female reproductive tract in flowering plants. Current Biology 18(20): R972-R978.

    Crepet, W. L. 2000. Progress in understanding angiosperm history, success, and relationships: Darwin´s abominably "perplexing phenomenon." Proceedings of the National Academy of Sciences 97(24): 12939-12941.

    Crepet, W. L. 2008. The fossil record of angiosperms: requiem or renaissance? Annals of the Missouri Botanical Garden 95(1): 3-33.

    Crepet, W. L. 2014. Advances in Flowering Plant Evolution. eLS (Citable Reviews in the Life Sciences [Fossils and Evolution]). Chichester: John Wiley & Sons, Ltd., 11 pp.

    Crepet, W. L. and K. J. Niklas. 2009. Darwin´s second "abominable mystery": Why are there so many angiosperm species? American Journal of Botany 96(1): 366-381.

    Crepet, W. L. and K. C. Nixon. 1996. 2. The fossil history of stamens. Pp. 25-57 In: W. G. D'Arcy and R. C. Keating (eds.), The Anther: Form, Function, and Phylogeny. New York: Cambridge University Press, 351 pp.

    Crepet, W. L., K. C. Nixon, and M. A. Gandolfo. 2004. Fossil evidence and phylogeny: the age of major angiosperm clades based on mesofossil and macrofossil evidence from Cretaceous deposits. American Journal of Botany 91(10): 1666-1682.

    Črne, A. E., H. Weissert, Š. Goričan, and S. M. Bernasconi. 2011. A biocalcification crisis at the Triassic-Jurassic boundary recorded in the Budva Basin (Dinarides, Montenegro). GSA Bulletin 123(1-2): 40-50.

    Cronk, Q. C. B. 2006. Legume flowers bear fruit. Proceedings of the National Academy of Sciences 103(13): 4801-4802.

    Cronquist, A. 1968. The Evolution and Classification of Flowering Plants. Boston: Houghton Mifflin; London: Nelson, 396 pp.

    Cubas, P. 2004. Floral zygomorphy, the recurring evolution of a successful trait. BioEssays 26: 1175-1184.

    Cubas, P., E. Coen, and J. M. M. Zapater. 2001. Ancient asymmetries in the evolution of flowers. Current Biology 11: 1050-1052.

    Cui, L., P. K. Wall, J. H. Leebens-Mack, B. G. Lindsay, D. E. Soltis, J. J. Doyle, P. S. Soltis, J. E. Carlson, K. Arumuganathan, A. Barakat, V. A. Albert, H. Ma, and C. W. dePamphilis. 2006. Widespread genome duplications throughout the history of flowering plants. Genome Research 16: 738-749.

    Dabrowska, P., D. Freitak, H. Vogel, D. G. Heckel, and W. Boland. 2009. The phytohormone precursor OPDA is isomerized in the insect gut by a single, specific glutathione transferase. Proceedings of the National Academy of Sciences 106(38): 16304-16309.

    Dahlgren, R. M. T. and H. T. Clifford. 1982. The Monocotyledons: A Comparative Study. New York: Academic Press, 378 pp.

    Damerval, C., M. L. Guilloux, M. Jager, and C. Charon. 2007. Diversity and evolution of CYCLOIDEA-like TCP genes in relation to flower development in Papaveraceae. Plant Physiology 143: 759-772.

    Danforth, B. N. and J. Ascher. 1999. Flowers and insect evolution. Science 283(5399): 143.

    Davies, T. J., T. G. Barraclough, M. W. Chase, P. S. Soltis, D. E. Soltis, and V. Savolainen. 2004. Darwin's abominable mystery: insights from a supertree of the angiosperms. Proceedings of the National Academy of Sciences 101(7): 1904-1909.

    Davis, C. C., P. K. Endress, and D. A. Baum. 2008. The evolution of floral gigantism. Current Opinion in Plant Biology 11: 49-57.

    Delker, C., A. Raschke, and M. Quint. 2008. Auxin dynamics: the dazzling complexity of a small molecule's message. Planta 227: 929-941.

    De Bodt, S., S. Marie, and Y. Van der Peer. 2005. Genome duplication and the origin of angiosperms. Trends in Ecology and Evolution 20(11): 591-597.

    De Bodt, S., G. Theissen, and Y. Van de Peer. 2006. Promoter analysis of MADS-box genes in eudicots through phylogenetic footprinting. Molecular Biology and Evolution 23(6): 1293-1303.

    De Loof, A. 2008. Ecdysteroids, juvenile hormone and insect neuropeptides: recent successes and remaining major challenges. General and Comparative Endocrinology 155(1): 3-13.

    Deng, W., H. Ying, C. A. Helliwell, J. M. Taylor, W. J. Peacock, and E. S. Dennis. 2011. FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proceedings of the National Academy of Sciences 108(16): 6680-6685.

    Dengler, N. G. 2006. The shoot apical meristem and development of vascular architecture. Canadian Journal of Botany 84: 1660-1671.

    Des Marais, D. L. and M. D. Rausher. 2010. Parallel evolution at multiple levels in the origin of hummingbird pollinated flowers in Ipomoea. Evolution 64(7): 2044-2054.

    Devoto, A. and J. G. Turner. 2003. Regulation of jasmonate-mediated plant responses in Arabidopsis. Annals of Botany 92: 329-337.

    Dickinson, H. G. and R. Grant-Downton. 2009. Bridging the generation gap: flowering plant gametophytes and animal germlines reveal unexpected similarities. Biological Reviews 84(4): 589-615.

    Di Giacomo, E. F. Sestili, M. A. Ianelli, G. Testone, D. Mariotti, and G. Frugis. 2008. Characterization of KNOX genes in Medicago truncatula. Plant Molecular Biology 67: 135-150.

    Dilcher, D. L. 1979. Early angiosperm reproduction: an introductory report. Review of Palaeobotany and Palynology 27: 291-328.

    Dilcher, D. L. 1986. Origin of Flowering Plants. McGraw-Hill Yearbook of Science and Technology 339-343.

    Dilcher, D. L. 2000. Toward a new synthesis: Major evolutionary trends in the angiosperm fossil record. Proceedings of the National Academy of Sciences 97(13): 7030-7036.

    Dilcher, D. L. 2010. Major innovations in angiosperm evolution. Pp. 97-116 In: C. T. Gee (ed.), Plants in Mesozoic Time, Morphological Innovations, Phylogeny, Ecosystems. Bloomington: Indiana University Press, 373 pp.

    DiMichele, W. A. and R. W. Hook. 1992. 5. Paleozoic terrestrial ecosystems. Pp. 205-325 In: A. K. Behrensmeyer, J. D. Damuth, W. A. DiMichele, R. Potts, H.-D. Sues, and S. L. Wing (eds.), Terrestrial Ecosystems Through Time, Evolutionary Paleoecology of Terrestrial Plants and Animals. Chicago: The University of Chicago Press, 568 pp.

    Ditta, G., A. Pinyopich, P. Robles, S. Pelaz, and M. F. Yanofsky. 2004. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Current Biology 14: 1935-1940.

    Djuranovic, S., A. Nahvi, and R. Green. 2011. A parsimonious model for gene regulation by miRNAs. Science 331(6017): 550-553.

    Doerner, P. 2006. Plant meristems: what you see is what you get? Current Biology 16(2): R56-R58.

    Dodinet, E. 2016. Letters to the twenty-first century botanist: "What is a flower?" The social science perspective. Botany Letters 163(2): 155–158.

    Donoghue, M. J. and J. A. Doyle. 1991. Angiosperm monophyly. Trends in Ecology and Evolution 6(12): 407.

    Donoghue, M. J. and J. A. Doyle. 2000. Seed plant phylogeny: demise of the anthophyte hypothesis? Current Biology 10(3): R106-109.

    Dornelas, M. C., C. M. Patreze, G. C. Angenent, and R. G. H. Immink. 2011. MADS: the missing link between identity and growth? Trends in Plant Science 16(2): 89-97.

    Doyle, J. A. 1978. Origin of Angiosperms. Annual Review of Ecology and Systematics 9: 365-392.

    Doyle, J. A. 1994. Origin of the angiosperm flower: a phylogenetic perspective. Plants Systematics and Evolution (Supplement) 8: 7-29.

    Doyle, J. A. 1996. Seed plant phylogeny and the relationships of Gnetales. International Journal of Plant Sciences 157(6 Supplement): S3-S39.

    Doyle, J. A. 1998. Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Molecular Phylogenetics and Evolution 9: 448-462.

    Doyle, J. A. 2001. Significance of molecular phylogenetic analyses for paleobotanical investigations on the origin of angiosperms. The Palaeobotanist 50: 167-188.

    Doyle, J. A. 2005. Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana 44(4): 227-251.

    Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. The Journal of the Torrey Botanical Society 133(1): 169-209.

    Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169(7): 816-843.

    Doyle, J. A. 2009. Evolutionary significance of granular exine structure in the light of phylogenetic analyses. Review of Palaeobotany and Palynology 156(1-2): 198-210.

    Doyle, J. A. 2010. Function and evolution of saccate pollen. New Phytologist 188: 6-9.

    Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.

    Doyle, J. A. and M. J. Donoghue. 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Botanical Review (Lancaster) 52(4): 321-431.

    Doyle, J. A. and M. J. Donoghue. 1987. The origin of angiosperms: a cladistic approach.  Pp. 17-49 in: E. M. Friis, W. G. Chaloner, and P. R. Crane, The Origin of Angiosperms and Their Biological Consequences.  Cambridge: Cambridge University Press, 358 pp.

    Doyle, J. A. and P. K. Endress. 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. International Journal of Plant Sciences 161(Supplement 6): S121-S153.

    Doyle, J. A. and C. L. Hotton. 1991. Diversification of early angiosperm pollen in a cladistic context. Pp. 169-195 In: S. Blackmore and S. H. Barnes (eds.), Pollen and Spores: Patterns of Diversification, The Systematics Association Special Volume no. 44. Oxford: Oxford University Press, 391 pp.

    Doyle, J. A., C. L. Hotton, and J. V. Ward. 1990. Early Cretaceous tetrads, zonasulculate pollen, and Winteraceae. I. Taxonomy, morphology, and ultrastructure. American Journal of Botany 77(12): 1544-1557.

    Doyle, J. A., C. L. Hotton, and J. V. Ward. 1990. Early Cretaceous tetrads, zonasulculate pollen, and Winteraceae. II. Cladistic analysis and implications. American Journal of Botany 77(12): 1558-1568.

    Doyle, J. J., L. E. Flagel, A. H. Paterson, R. A. Rapp, D. E. Soltis, P. S. Soltis, and J. F. Wendel. 2008. Evolutionary genetics of genome merger and doubling in plants. Annual Review of Genetics 42: 443-461.

    Dresselhaus, T. and M. L. Márton. 2009. Micropylar pollen tube guidance and burst: adapted from defense mechanisms? Current Opinion in Plant Biology 12(6): 773-780.

    Drew, B. T., B. R. Ruhfel, Stephen A. Smith, M. J. Moore, B. G. Briggs, M. A. Gitzendanner, P. S. Soltis, and D. E. Soltis. 2014. Another look at the root of the angiosperms reveals a familiar tale. Systematic Biology 63(3): 368-382.

    Dubos, C., R. Stracke, E. Grotewold, B. Weisshaar, C. Martin, and L. Lepiniec. 2010. MYB transcription factors in Arabidopsis. Trends in Plant Science 15(10): 573-581.

    Dumas, C. and P. Rogowsky. 2008. Fertilization and early seed formation. Comptes Rendus Biologies 331(10): 715-725.

    Dun, E. A, P. B. Brewer, and C. A. Beveridge. 2009. Strigolactones: discovery of the elusive shoot branching hormone. Trends in Plant Science 14(7): 364-372.

    Eckardt, N. A. 2002. Plant reproduction: insights into the "abominable mystery." The Plant Cell 14: 1669.

    Eckardt, N. A. 2004. Two genomes are better than one: widespread paleopolyploidy in plants and evolutionary effects. The Plant Cell 16: 1647-1649.

    Edgecombe, G. D., Xiaoya Ma, and N. J. Strausfeld. 2015. Unlocking the early fossil record of the arthropod central nervous system. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 370(1684): DOI 10.1098/rstb.2015.0038.

    Efroni, I., Y. Eshed, and E. Lifschitz. 2010. Morphogenesis of simple and compound leaves: a critical review. The Plant Cell 22: 1019- 1032.

    Ehrlich, P. R. and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18: 586-608.

    Eichler, A. W. 1876. Syllabus der Vorlesungen &$252;ber Spezielle und Medizinisch-pharmazeutische Botanik, first edition. Berlin: Borntraeger.

    Emlen, D. J. and H. F. Nijhout. 2000. The development and evolution of exaggerated morphologies in insects. Annual Review of Entomology 45: 661-708.

    Endress, P. K. 1987. The early evolution of the angiosperm flower. Trends in Ecology and Evolution 2(10): 300-304.

    Endress, P. K. 1993. Federico Delpino and early views on angiosperm origin and macroevolution. Dissertationes Botanicae 196: 77-83.

    Endress, P. K. 1994. Diversity and Evolutionary Biology of Tropical Flowers. Cambridge University Press: Cambridge, 511 pp.

    Endress, P. K. 1996. 4. Diversity and evolutionary trends in angiosperm anthers. Pp. 92-110 In: W. G. D'Arcy and R. C. Keating (eds.), The Anther: Form, Function, and Phylogeny. New York: Cambridge University Press, 351 pp.

    Endress, P. K. 2001. Origins of flower morphology. Chapter 21, Pp. 493-510 In: G. P. Wagner (ed.), The Character Concept in Evolutionary Biology, San Diego: Academic Press, 622 pp.

    Endress, P. K. 2001. The flowers in extant basal angiosperms and inferences on ancestral flowers. International Journal of Plant Sciences 162(5): 1111-1140.

    Endress, P. A. 2001. Origins of floral morphology. Journal of Experimental Zoology 291: 105-115.

    Endress, P. K. 2004. Structure and relationships of basal relictual angiosperms. Australian Systematic Botany 17(4): 343-366.

    Endress, P. K. 2006. Angiosperm floral evolution: morphological developmental framework. Pp. 1-61 In: D. E. Soltis, J. H. Leebens-Mack, P. S. Soltis (eds.), Vol. 44, Advances in Botanical Research, Developmental Genetics of the Angiosperm Flower. Amsterdam: Elsevier.

    Endress, P. K. 2008. Perianth biology in the basal grade of extant angiosperms. International Journal of Plant Sciences 169(7): 844-862.

    Endress, P. K. 2011. Angiosperm ovules: diversity, development, evolution. Annals of Botany 107(9): 1465-1489.

    Endress, P. K. and J. A. Doyle. 2007. Floral phyllotaxis in basal angiosperms: development and evolution. Current Opinion in Plant Biology 10: 52-57.

    Endress, P. K. and J. A. Doyle. 2009. Reconstructing the ancestral angiosperm flower and its initial specializations. American Journal of Botany 96(1): 22-66.

    Engström, E. M., A. Izhaki, and J. L. Bowman. 2004. Promoter bashing, microRNAs, and KNOX genes. New insights, regulators, and targets-of-regulation in the establishment of lateral organ polarity in Arabidopsis. Plant Physiology 135(2): 685-694.

    Enquist, B. J., B. H. Tiffney, and K. J. Niklas. 2007. Metabolic scaling and the evolutionary dynamics of plant size, from, and diversity: toward a synthesis of ecology, evolution, and paleontology. International Journal of Plant Sciences 168(5): 729-749.

    Erbar, C. 2007. Current opinions in flower development and the evo-devo approach in plant phylogeny. Plant Systematics and Evolution 269(1-2): 107-132.

    Eriksson, O. 2008. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence. International Journal of Plant Sciences 169(7): 863-870.

    Eriksson, O. 2016. Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores. Biological Reviews 91(1): 168–186.

    Erwin, D. H. 2006. Extinction: How Life on Earth Nearly Ended 250 Million Years Ago. Princeton: Princeton University Press, 306 pp.

    Erwin, D. H. 2007. Increasing returns, ecological feedback and the early Triassic recovery. Palaeoworld 16(1-3): 9-15.

    Farrell, B. D. 1998. "Inordinate fondness" explained: why are so many beetles? Science 281(5376): 555-559.

    Farris, S. M. 2005. Evolution of insect mushroom bodies: old clues, new insights. Arthropod Structure and Development 34:211-234.

    Farris, S. M. and S. Schulmeister. 2011. Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proceedings of the Royal Society of London, Series B, Biological Sciences 278(1707): 940-951.

    Feild, T. S. and N. C. Arens. 2005. Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossils. New Phytologist 166: 383-408.

    Feild, T. S. and N. C. Arens. 2007. The ecophysiology of early angiosperms. Plant, Cell and Environment 30(3): 291-309.

    Feild, T. S., N. C. Arens, and T. E. Dawson. 2003. The ancestral ecology of angiosperms: emerging perspectives from extant basal lineages. International Journal of Plant Sciences 164(Supplement 3): S129-S142.

    Feild T. S., N. C. Arens, J. A. Doyle, T. E. Dawson, and M. J. Donoghue. 2004. Dark and disturbed: a new image of early angiosperm ecology.  Paleobiology 30(1): 82-107.

    Feild, T. S. and T. J. Brodribb. 2013. Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks. New Phytologist 199(3): 720-726.

    Feild, T. S., T. J. Brodribb, A. Iglesias, D. S. Chatelet, A. Baresch, G. R. Upchurch, Jr., B. Gomez, B. A. R. Mohr, C. Coiffard, J. Kvaček, and C. Jaramillo. 2011. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences 108(20): 8363-8366.

    Feild, T. S., G. R. Upchurch, Jr., D. S. Chatelet, T. J. Brodribb, K. C. Grubbs, M-S. Samain, and S. Wanke. 2011. Fossil evidence for low gas exchange capacities for early Cretaceous angiosperm leaves. Paleobiology 37(2): 195-213.

    Feller, A., K. Machemer, E. L. Braun, and E. Grotewold. 2011. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. The Plant Journal 66(1): 94-116.

    Feng, X., Z. Zhao, Z. Tian, S. Xu, Y. Luo, Z. Cai, Y. Wang, J. Yang, Z. Wang, L. Weng, J. Chen, L. Zheng, X. Guo, J. Luo, S. Sato, S. Tabata, W. Ma, X. Cao, X. Hu, C. Sun, and D. Luo. 2006. Control of petal shape and floral zygomorphy in Lotus japonicus. Proceedings of the National Academy of Sciences 103(13): 4970-4975.

    Fenster, C. B., W. S. Armbruster, P. Wilson, M. R. Dudash, and J. D. Thomson. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35: 375-403.

    Ferrario, S., A. V. Shchennikova, J. Franken, R. G. H. Immink, and G. C. Angenent. 2006. Control of floral meristem determinacy in Petunia by MADS-box transcription factors. Plant Physiology 140: 890-898.

    Fleming, A. J. 2005. The control of leaf development. New Phytologist 166(1): 9-20.

    Flores-Rentería, L., A. Vásquez-Lobo, A. V. Whipple, D. Piñero, J. Márquez-Guzmán, and C. A. Domínguez. 2011. Functional bisporangiate cones in Pinus johannis (Pinaceae): implications for the evolution of bisexuality in seed plants. American Journal of Botany 98(1): 130-139.

    Floyd, S. K. and J. L. Bowman. 2007. The ancestral developmental tool kit of land plants. International Journal of Plant Sciences 168(1): 1-35.

    Floyd, S. K. and W. E. Friedman. 2000. Evolution of endosperm developmental patterns among basal flowering plants. International Journal of Plant Sciences 161(Supplement 6):S51-S81.

    Floyd, S. K., C. S. Zalewski, and J. L. Bowman. 2006. Evolution of class III homeodomain-leucine zipper genes in Streptophytes. Genetics 173: 373-388.

    Fluch, S., C. C. Olmo, S. Tauber, M. Stierschneider, D. Kopecky, T. G. Reichenauer, and I. Matusikova. 2008. Transcriptomic changes in wind-exposed poplar leaves are dependent on developmental stage. Planta 228(5): 757-764.

    Flück, M., K. A. Webster, J. Graham, F. Giomi, F. Gerlach, and A. Schmitz. 2007. Coping with cyclic oxygen availability: evolutionary aspects. Integrative and Comparative Biology 47(4): 524-531.

    Forbis, T. A., S. K. Floyd, and A. De Queiroz. 2002. The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56(1): 2112-2125.

    Fordyce, J. A. 2010. Host shifts and evolutionary radiations of butterflies. Proceedings of the Royal Society of London, Series B, Biological Sciences 277(1701): 3735-3743.

    Foster, C. S. P., H. Sauquet, M. van der Merwe, H. McPherson, M. Rossetto, and S. Y. W. Ho. 2017. Phylogenomic timescale for angiosperm evolution: evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Systematic Biology XX: XXX-XXX.

    Franks, P. J., D. L. Royer, D. J. Beerling, P. K. Vandewater, D. J. Cantrill, M. M. Barbour, and J. A. Barry. 2014. New constraints on atmospheric CO2 concentration for the Phanerozoic. Geophysical Research Letters 41: 4685-4694.

    Fricke, H. C. and D. A. Pearson. 2008. Stable isotope evidence for changes in dietary niche partitioning among hadrosaurian and ceratopsian dinosaurs of the Hell Creek Formation, North Dakota. Paleobiology 34(4): 534-552.

    Friedman, W. E. 1987. Growth and development of the male gametophyte of Ginkgo biloba within the ovule (in vivo). American Journal of Botany 74(12): 1797-1815.

    Friedman, W. E. 1987. Morphogenesis and experimental aspects of growth and development of the male gametophyte of Ginkgo biloba in vitro. American Journal of Botany 74(12): 1816-1830.

    Friedman, W. E. 1990. Sexual reproduction in Ephedra nevadensis (Ephedraceae): further evidence of double fertilization in a non-flowering seed plant. American Journal of Botany 77: 1582-1598.

    Friedman, W. E. 1992. Evidence of a pre-angiosperm origin of endosperm: implications for the evolution of flowering plants. Science 255: 336-339.

    Friedman, W. E. 1992. Double fertilization in nonflowering seed plants and its relevance to the origin of flowering plants. Pp. 319-356 In: S. D. Russell and C. Dumas (eds.), Sexual Reproduction in Flowering Plants. San Diego: Academic Press, 615 pp.

    Friedman, W. E. 1993. The evolutionary history of the seed plant male gametophyte. Trends in Ecology and Evolution 8(1): 15-21.

    Friedman, W. E. 1994. The evolution of embryogeny in seed plants and the developmental origin and early history of endosperm. American Journal of Botany 81: 1468-1486.

    Friedman, W. E. 1995. Organismal duplication, inclusive fitness theory, and altruism: understanding the evolution of endosperm and the angiosperm reproductive syndrome. Proceedings of the National Academy of Sciences 92: 3913-3917.

    Friedman, W. E. 1999. Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development 126: 1065-1075.

    Friedman, W. E. 2001. Developmental and evolutionary hypotheses for the origin of double fertilization and endosperm. Comptes Rendus de l'Académie des Sciences, Series III Sciences de la Vie 324: 559-567.

    Friedman, W. E. 2001. Comparative embryology of basal angiosperms. Current Opinion in Plant Biology 4: 14-20.

    Friedman. W. E. 2006. Embryological evidence for developmental lability during early angiosperm evolution. Nature 441:337-340.

    Friedman. W. E. 2008. Hydatellaceae are water lilies with gymnospermous tendencies. Nature 453: 94-97.

    Friedman, W. E. 2009. The meaning of Darwin's "abominable mystery." American Journal of Botany 96(1): 5-21.

    Friedman, W. E. 2015. Evolving words and the egg-bearing tubes of Welwitschia (Welwitschiaceae). American Journal of Botany 102(2): 176-179.

    Friedman, W. E. 2015. Development and evolution of the female gametophyte and fertilization process in Welwitschia mirabilis (Welwitschiaceae). American Journal of Botany 102(2): 312-324.

    Friedman, J. and S. C. H. Barrett. 2008. A phylogenetic analysis of the evolution of wind pollination in the angiosperms. International Journal of Plant Sciences 169(1): 49-58.

    Friedman, W. E. and J. S. Carmichael. 1996. Double fertilization in Gnetales: implications for understanding reproductive diversification among seed plants. International Journal of Plant Sciences 157(6 Supplement): S77-S94.

    Friedman, W. E. and J. S. Carmichael. 1998. Heterochrony and developmental innovation: evolution of female gametophyte ontogeny in Gnetum, a highly apomorphic seed plant. Evolution 52: 1016-1030.

    Friedman, W. E. and S. K. Floyd. 2001. The origin of flowering plants and their respective biology: a tale of two phylogenies. Evolution 55: 217-231.

    Friedman, W. E., W. N. Gallup, and J. H. Williams. 2003. Female gametophyte development in Kadsura: implications for Schizandraceae, Illiciales, and the early evolution of flowering plants. International Journal of Plant Sciences 164 (Supplement 5): S293-S305.

    Friedman, W. E., E. N. Madrid, and J. H. Williams. 2008. Origin of the fittest and survival of the fittest: relating female gametophyte development to endosperm genetics. International Journal of Plant Sciences 169(1): 79-92.

    Friedman, W. E., R. C. Moore, and M. D. Purugganan. 2004. The evolution of plant development. American Journal of Botany 91(10): 1726-1741.

    Friedman, W. E. and K. C. Ryerson. 2009. Reconstructing the ancestral female gametophyte of angiosperms: insights from Amborella and other ancient lineages of flowering plants. American Journal of Botany 96(1): 129-143.

    Friedman, W. E. and J. H. Williams. 2003. Modularity of the angiosperm female gametophyte and its bearing on the early evolution of endosperm in flowering plants. Evolution 57: 216-230.

    Friedman, W. E. and J. H. Williams. 2004. Developmental evolution of the sexual process in ancient flowering plant lineages. The Plant Cell (Supplement) 16: S119-S132.

    Friis, E. M., W. G. Chaloner, and P. R. Crane. 1987. Introduction to angiosperms. Pp. 1-15 In: E. M. Friis, W. G. Chaloner, and P. R. Crane (eds.), The Origins of Angiosperms and Their Biological Consequences, Cambridge: Cambridge University Press, 358 pp.

    Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.

    Friis, E. M., K. R. Pedersen, and P. R. Crane. 2000. Fossil floral structures of a basal angiosperm with monocolpate, reticulate-acolumellate from the Early Cretaceous of Portugal. Grana 39: 226-245.

    Friis, E. M., K. R. Pedersen, and P. R. Crane. 2006. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, and Palaeoecology 232: 251-293.

    Frohlich, M. W. 2001. 3. A detailed scenario and possible tests of the mostly male theory of flower evolutionary origins. Pp. 59-104 In: M. L. Zelditch (ed.), Beyond Heterochrony: the Evolution of Development. New York: Wiley, 371 pp.

    Frohlich, M. W. 2002. The mostly male theory of flower origins: summary and update regarding the Jurassic pteridosperm Pteroma. Pp. 85-108 In: Q. C. B. Cronk, R. M. Bateman, and J. A. Hawkins (eds.), Developmental Genetics and Plant Evolution. London: Taylor and Francis, 543 pp.

    Frohlich, M. W. 2003. An evolutionary scenario for the origin of flowers. Nature Reviews Genetics 4: 559-566.

    Frohlich, M. W. 2006. Recent developments regarding the evolutionary origin of flowers. Pp. 63-127 In: D. E. Soltis, J. H. Leebens-Mack, P. S. Soltis (eds.), Vol. 44, Advances in Botanical Research, Developmental Genetics of the Angiosperm Flower. Amsterdam: Elsevier.

    Frohlich, M. W. and M. W. Chase. 2007. After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450: 1184-1189.

    Frohlich, M. W. and D. S. Parker. 2000. The mostly male theory of flower evolutionary origins: from genes to fossils. Systematic Botany 25: 155-170.

    Furness, C. A., P. J. Rudall, and F. B. Sampson. 2002. Evolution of microsporogenesis in angiosperms. International Journal of Plant Sciences 163(2): 235-260.

    Futuyma, D. J. and M. C. Keese. 1992. Evolution and coevolution of plants and phytophagous arthropods. Pp. 439-475, In: G. A. Rosenthal and M. R. Berenbaum (eds.), Herbivores: Their Interactions with Secondary Plant Metabolites (2nd ed.). New York: Academic Press.

    Galant, R. and S. B. Carroll. 2002. Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415(6874): 910-913.

    Galtier, J. 2010. The origins and early evolution of the megaphyllous leaf. International Journal of Plant Sciences 171(6): 641-661.

    Gan, Y., H. Yu, J. Peng, and P. Broun. 2007. Genetic and molecular regulation by DELLA proteins of trichome development in Arabidopsis. Plant Physiology 145: 1031-1042.

    Gao, X.-H., X.-Z. Huang, S.L. Xiao, and X. D. Fu. 2008. Evolutionarily conserved DELLA-mediated gibberellin signaling in plants. Journal of Integrative Plant Biology 50(7): 825-834.

    Gastaldo, R. A., R. Adendorff, M. Bamford, C. C. Labandeira, J. Neveling, and H. Sims. 2005. Taphonomic trends of macrofloral assemblages across the Permian-Triassic boundary, Karoo Basin, South Africa. Palaios 20(5): 479-497.

    Gastaldo, R. A., S. L. Kamo, J. Neveling, J. W. Geissman, M. Bamford, and C. V. Looy. 2015. Is the vertebrate-defined Permian-Triassic boundary in the Karoo Basin, South Africa, the terrestrial expression of the end-Permian marine event? Geology 43(10): 939-942.

    Gastaldo, R. A., J. Neveling, C. K. Clark, and S. S. Newbury. 2009. The terrestrial Permian-Triassic boundary event bed is a non-event. Geology 37(3): 199-202.

    Gellon, G. and W. McGinnis. 1998. Shaping body plans in development and evolution by modulation of Hox expression patterns. BioEssays 20(2): 116-125.

    Germain, H., E. Chevalier, and D. P. Matton. 2006. Plant bioactive peptides: an expanding class of signaling molecules. Canadian Journal of Botany 84: 1-19.

    Geuten, K., T. Viaene, and V. F. Irish. 2011. Robustness and evolvability in the B-system of flower development. Annals of Botany 107(9): 1545-1556.

    Giannasi, D. E. and K. J. Niklas. 1981. Comparative paleobiochemistry of some fossil and extant Fagaceae. American Journal of Botany 68(6): 762-770.

    Glasspool, I. J. and A. C. Scott. 2010. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nature Geoscience 3: 627-630.

    Glover, B. 2014. Understanding Flowers and Flowering, Second Edition. Oxford: Oxford University Press, 320 pp.

    Glover, B. J., C. A. Airoldi, S. F. Brockington, M. Fernández-Mazuecos, C. Martínez-Pérez, G. Mellers, E. Moyroud, and L. Taylor. 2015. How have advances in comparative floral development influenced our understanding of floral evolution? International Journal of Plant Sciences 176(4): 307-323.

    Gómez-Zurita, J. and J. Galián. 2005. Current knowledge on genes and genomes of phytophagous beetles (Coleoptera: Chrysomeloidea, Curculionoidea): a review. European Journal of Entomology 102: 577-597.

    Gómez-Zurita, J., T. Hunt, F. Kopliku, and A. P. Vogler. 2007. Recalibrated tree of leaf beetles (Chrysomelidae) indicates independent diversification of angiosperms and their insect herbivores. PLoS ONE 2(4): e360.

    Gordon, S. P., V. S. Chickarmane, C. Ohno, and E. M. Meyerowitz. 2009. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proceedings of the National Academy of Sciences 106(38): 16529-16534.

    Gorelick, R. 2001. Did insect pollination cause increased seed plant diversity? Biological Journal of the Linnaean Society 74: 407-427.

    Goremykin, V. V., K. I. Hirsch-Ernst, S. Wölfl, and F. H. Hellwig. 2003. Analysis of the Amborella trichopoda chloroplast genome sequence suggests that Amborella is not a basal angiosperm. Molecular Biology and Evolution 20(9): 1499-1505.

    Goremykin, V. V., S. V. Nikiforova, D. Cavalieri, M. Pindo, and P. Lockhart. 2015. The root of flowering plants and total evidence. Systematic Biology 64(5): 875-891.

    Gorr, T. A., M. Gassmann, and P. Wappner. 2006. Sensing and responding to hypoxia via HIF in model invertebrates. Journal of Insect Physiology 52(4): 349-364.

    Götz, A. E., K. Ruckwied, J. Pálfy, and J. Haas. 2009. Palynological evidence of synchronous changes within the terrestrial and marine realm at the Triassic/Jurassic boundary (Csóvár section, Hungary). Review of Palaeobotany and Palynology 156(3-4): 401-409.

    Gould, R. E. and T. Delevoryas. 1977. The biology of Glossopteris: evidence from petrified seed-bearing and pollen-bearing organs. Alcheringa 1: 387-399.

    Gould, S. J. 1977. Part two, heterochrony and paedomorphosis. Pp. 203-404 In: S. J. Gould, Ontogeny and Phylogeny. Cambridge: The Belknap Press of Harvard University Press, 501 pp.

    Goyret, J., P. M. Markwell, and R. A. Raguso. 2008. Context- and scale-dependent effects of floral CO2 on nectar foraging by Manduca sexta. Proceedings of the National Academy of Sciences 105(12): 4565-4570.

    Gramzow, L., M. S. Ritz, and G. Theißen. 2010. On the origin of MADS-domain transcription factors. Trends in Genetics 26(4): 149-153.

    Grauvogel-Stamm, L. and S. R. Ash. 2005. Recovery of the Triassic land flora from the end-Permian life crisis. Comptes Rendus Palevol 4(6-7): 593-608.

    Greenberg, S. and A. Ar. 1996. Effects of chronic hypoxia, normoxia, and hyperoxia on larval development in the beetle Tenebrio molitor. Journal of Insect Physiology 42(11-12): 991-996.

    Grehan, J. R. 1991. A panbiogeographic perspective for pre-Cretaceous angiosperm-Lepidoptera coevolution. Australian Systematic Botany 4(1): 91-110.

    Grimaldi, D. 1999. The co-radiations of pollinating insects and angiosperms in the Cretaceous. Annals of the Missouri Botanical Garden 86(2): 373-406.

    Grimaldi, D. and M. S. Engel. 2005. Evolution of the Insects. Cambridge: Cambridge University Press, 755 pp.

    Grover, C. E. and J. F. Wendel. 2010. Recent insight into mechanisms of genome size change in plants. Journal of Botany 2010(382732): 10.

    Guidugli, K. R., A. M. Nascimento, G. V. Amdam, A. R. Barchuk, S. Omholt, Z. L. P. Simões, and K. M. Hartfelder. 2005. Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Letters 579: 4961-4965.

    Guillet-Claude, C., N. Isabel, B. Pelgas, and J. Bousquet. 2004. The evolutionary implications of KNOX-1 gene duplications in conifers: correlated evidence from phylogeny, gene mapping, and analysis of functional divergence. Molecular Biology and Evolution 21(12): 2232-2245.

    Guimarães, Jr., P. R., V. Rico-Gray, S. Furtado dos Reis, and J. N. Thompson. 2006. Asymmetries in specialization in ant-plant mutualistic networks. Proceedings of the Royal Society of London, Series B, Biological Sciences 273: 2041-2047.

    Gupta, K. J., A. R. Fernie, W. M. Kaiser, and J. T. van Dongen. 2011. On the origins of nitric oxide. Trends in Plant Science 16(3): 160-168.

    Hagner-Holler, S., C. Pick, S. Girgenrath, J. H. Marden, and T. Burmester. 2007. Diversity of stonefly hexamerins and implication for the evolution of insect storage proteins. Insect Biochemistry and Molecular Biology 37(10): 1064-1074.

    Hagner-Holler, S., A. Schoen, W. Erker, J. H. Marden, R. Ruprecht, H. Decker, and T. Burmester. 2004. A respiratory protein from an insect. Proceedings of the National Academy of Sciences 101(3): 871-874.

    Hake, S., H. M. S. Smith, H. Holtan, E. Magnani, G. Mele, and J. Ramirez. 2004. The role of KNOX genes in plant development. Annual Review of Cell and Developmental Biology 20: 125-151.

    Hallam, A. 2010. How catastrophic was the end-Triassic mass extinction. Lethaia 35(2): 147-157.

    Hamant, O. and V. Pautot. 2010. Plant development: a TALE story. Comptes Rendus Biologies 333(4): 371-381.

    Hamès, C., D. Ptchelkine, C. Grimm, E. Thévenon, E. Moyroud, F. Gérard, J.-L. Martiel, R. Benlloch, F. Parcy, and C. W. Müller. 2008. Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. The EMBO Journal 27: 2628-2637.

    Hare, J. D. 2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Review of Entomology 56: 161-180.

    Harper, J. L. 1977. Population Biology of Plants. London: Academic Press, 892 pp.

    Harrison, C. J., S. B. Corley, E. C. Moylan, D. L. Alexander, R. Scotland, and J. A. Langdale. 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434: 509-514.

    Hartfelder, K. 2000. Insect juvenile hormone: from "status quo" to high society. Brazilian Journal of Medical and Biological Research 33(2): 157-177.

    Hartweck, L. M. 2008. Gibberellin signaling. Planta 229: 1-13.

    Hasebe, M., C. K. Wen, M. Kato, and J. A. Banks. 1998. Characterization of MADS homeotic genes in the fern Ceratopteris richardii. Proceedings of the National Academy of Sciences 95(11): 6222-6227.

    Hasiotis, S. T., R. F. Dubiel, P. T. Kay, T. M. Demko, K. Kowalska, and D. McDaniel. 1998. Research update on hymenopteran nests and cocoons, Upper Triassic Chinle Formation, Petrified Forest National Park, Arizona. National Park Service Paleontological Research 3: 116-121.

    Hasson, A., T. Blein, and P. Laufs. 2010. Leaving the meristem behind: the genetic and molecular control of leaf patterning and morphogenesis. Comptes Rendus Biologies 333(4): 350-360.

    Heavens, N. G., N. M. Mahowald, G. S. Soreghan, M. J. Soreghan, and C. A. Shields. 2015. A model-based evaluation of tropical climate in Pangaea during the late Palaeozoic icehouse. Palaeogeography, Palaeoclimatology, Palaeoecology 425: 109–127.

    Heil, M. 2011. Nectar: generation, regulation, and ecological functions. Trends in Plant Science 16(4): 191-200.

    Heimhofer, U., P. A. Hochuli, S. Burfa, J. M. L. Dinis, and H. Weissert. 2005. Timing of Early Cretaceous angiosperm diversification and possible links to major paleoenvironmental change. Geology 33(2): 141-144.

    Hemsley, A. R. and I. Poole (eds.). 2004. The Evolution of Plant Physiology, From Whole Plants to Ecosystems, Linnean Society Symposium Series Number 21. London: Elsevier Academic Press, 492 pp.

    Hernández-Hernández, T., L. P. Martínez-Castilla, and E. R. Alvarez-Buylla. 2007. Functional diversification of B MADS-Box homeotic regulators of flower development: adaptive evolution of protein-protein interaction domains after major gene duplication events. Molecular Biology and Evolution 24(2): 465-481.

    Hetherington, A. J., J. G. Dubrovsky, and L. Dolan. 2016. Unique cellular organization in the oldest root apical meristem. Current Biology 26: 1629-1633.

    Hickey, L. J. and D. W. Taylor. 1996. Chapter 8. Origin of the angiosperm flower. Pp. 176-231 In: D. W. Taylor and L. J. Hickey (eds.), Flowering Plant Origin, Evolution, and Phylogeny. London: Chapman and Hall, 403 pp.

    Hileman, L. C. and V. F. Irish. 2009. More is better: the uses of developmental genetic data to reconstruct perianth evolution. American Journal of Botany 96(1): 83-95.

    Himi, S., R. Sano, T. Nishiyama, T. Tanahashi, M. Kato, K. Ueda, and M. Hasebe. 2001. Evolution of MADS-box gene induction by FLO/LFY genes. Journal of Molecular Evolution 53(4-5): 387-393.

    Hittinger, C. T. and S. B. Carroll. 2008. Evolution of an insect-specific GROUCHO-interaction motif in the ENGRAILED selector protein. Evolution and Development 10(5): 537-545.

    Hoback, W. W. and D. W. Stanley. 2001. Insects in hypoxia. Journal of Insect Physiology 47(6): 533-542.

    Hochuli, P. A. and S. Feist-Burkhardt. 2004. A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). Journal of Micropalaeontology 23: 97-104.

    Hochuli, P. A. and S. Feist-Burkhardt. 2013. Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Frontiers in Plant Science, Plant Evolution and Development 4: Article 344.

    Hochuli, P. A., J. Os Vigran, E. Hermann, and H. Bucher. 2010. Multiple climatic changes around the Permian-Triassic boundary revealed by an expanded palynological record from mid-Norway. GSA Bulletin 122(5-6): 884-896.

    Hoekstra, H. E. and J. A. Coyne. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61(5): 995-1016.

    Holloway, S. J. and W. E. Friedman. 2008. Embryological features of Tofieldia glutinosa and their bearing on the early diversification of monocotyledonous plants. Annals of Botany 102(2): 167-182.

    Hoover, K., M. Grove, M. Gardner, D. P. Hughes, J. McNeil, and J. Slavicek. 2011. A gene for an extended phenotype. Science 333(6048): 1401.

    Hotton, C. L. 1991. Diversification of early angiosperm pollen in a cladistic context. Pp. 169-195 In: S. Blackmore and S. H. Barnes (eds.), Pollen and Spores: Patterns of Diversification. Oxford: Clarendon.

    Hou, X., W.-W. Hu, L. Shen, L. Y. C. Lee, Z. Tao, J.-H. Han, and H. Yu. 2008. Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiology 147: 1126-1142.

    Hu, S., D. L. Dilcher, D. M. Jarzen, and D. W. Taylor. 2008. Early steps of angiosperm-pollinator coevolution. Proceedings of the National Academy of Sciences 105(1): 240-245.

    Huey, R. B. and P. D. Ward. 2005. Hypoxia, global warming, and terrestrial Late Permian extinctions. Science 308(5720): 398-401.

    Hufford, L. 1996. 3. The fossil history of stamens. Pp. 58-91 In: W. G. D'Arcy and R. C. Keating (eds.), The Anther: Form, Function, and Phylogeny. New York: Cambridge University Press, 351 pp.

    Hughes, N. F. 1976. Palaeobiology of Angiosperm Origins.  Cambridge: Cambridge University Press, 242 pp.

    Hughes, N. F. 1994. The Enigma of Angiosperm Origins. Cambridge: Cambridge University Press, 303 pp.

    Hunt, J. H., B. J. Kensinger, J. A. Kossuth, M. T. Henshaw, K. Norberg, F. Wolschin, and G. V. Amdam. 2007. A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies. Proceedings of the National Academy of Sciences 104(35): 14020-14025.

    Hunt, T., J. Bergsten, Z. Levkanicova, A. Papadopoulou, O. St. John, R. Wild, P. M. Hammond, D. Ahrens, M. Balke, M. S. Caterino, J. Gomez-Zurita, I. Ribera, T. S. Barraclough, M. Bocakova, L. Bocak, and A. P. Vogler. 2007. A comprehensive phylogeny of beetles reveals the evolutionary origins of superradiation. Science 318(5858): 1913-1916.

    Immink, R. G. H., K. Kaufmann, and G. C. Angenent. 2010. The 'ABC' of MADS domain protein behaviour and interactions. Seminars in Cell & Developmental Biology 21(1): 87-93.

    Irish, V. F. 2003. The evolution of floral homeotic gene function. BioEssays 25: 637-646.

    Irish, V. F. 2006. Duplication, diversification, and comparative genetics of angiosperm MADS-Box genes. Pp. 129-161 In: D. E. Soltis, J. H. Leebens-Mack, P. S. Soltis (eds.), Vol. 44, Advances in Botanical Research, Developmental Genetics of the Angiosperm Flower. Amsterdam: Elsevier.

    Irish, V. F. and A. Litt. 2005. Flower development and evolution: gene duplication, diversification and redeployment. Current Opinion in Genetics and Development 15(4): 454-460.

    Isoe, J. and H. H. Hagedorn. 2007. Mosquito vitellogenin genes: comparative sequence analysis, gene duplication, and the role of rare synonymous codon usage in regulating expression. Journal of Insect Science 7: 1-49.

    Isozaki, Y. 2009. Illawara Reversal: the fingerprint of a superplume that triggered Pangaean breakup and the end-Guadalupian (Permian) mass extinction. Gondwana Research 15(3-4): 421-432.

    Itoh, H., M. Ueguchi-Tanaka, and M. Matsuoka. 2008. Molecular biology of gibberellins signaling in higher plants. Pp. 191-220 In: K. W. Jeon (ed.), International Review of Cell and Molecular Biology, Volume 268. Boston: Academic Press, Elsevier, 316 pp.

    Ito-Inaba, Y., Y. Hida, H. Mori, and T. Inaba. 2008. Molecular identity of uncoupling proteins in thermogenic skunk cabbage. Plant and Cell Physiology 49(12): 1911-1916.

    Ivancic, A., O. Roupsard, J. Q. Garcia, M. Melteras, T. Molisale, S. Tara, and V. Lebot. 2008. Thermogenesis and flowering biology of Colocasia gigantea, Araceae. Journal of Plant Research 121: 73-82.

    Jack, T. 2004. Molecular and genetic mechanisms of floral control. The Plant Cell 16: S1-S17.

    Jackson, D. 2002. Double labeling of KNOTTED1 mRNA and protein reveals multiple potential sites of protein trafficking in the shoot apex. Plant Physiology 129: 1423-1429.

    Jackson, D. 2005. 6. Transcription factor movement through plasmodesmata. Pp. 113-134 In: K. J. Oparka (ed.), Plasmodesmata, Annual Plant Reviews, Volume 18. Oxford: Blackwell Publishing, Inc., 311 pp.

    Jaffe, M. J. 1973. Thigmomorphogenesis: the response of plant growth and development to mechanical stimulation. Planta 114: 143-157.

    Jaffe, M. J., A. C. Leopold, and R. C. Staples. 2002. Thigmo responses in plants and fungi. American Journal of Botany 89(3): 375-382.

    Jaillon, C. O., J.-M. Aury, B. Noel, A. Policriti, C. Clepet, A. Casagrande, N. Choisne, S. Aubourg, N. Vitulo, C. Jubin, A. Vezzi, F. Legeai, P. Hugueney, C. Dasilva, D. Horner, E. Mica, D. Jublot, J. Poulain, C. Bruyère, A. Billault, B. Segurens, M. Gouyvenoux, E. Ugarte, F. Cattonaro, V. Anthouard, V. Vico, C. Del Fabbro, M. Alaux, G. Di Gaspero, V. Dumas, N. Felice, S. Paillard, I. Juman, M. Moroldo, S. Scalabrin, A. Canaguier, I. Le Clainche, G. Malacrida, E. Durand, G. Pesole, V. Laucou, P. Chatelet, D. Merdinoglu, M. Delledonne, M. Pezzotti, A. Lecharny, C. Scarpelli, F. Artiguenave, M. E. Pè, G. Valle, M. Morgante, M. Caboche, A.-F. Adam-Blondon, J. Weissenbach, F. Quétier, and P. Wincker. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.

    Jansen, R. K., C. Saski, S.-B. Lee, A. K. Hansen, and H. Daniell. 2011. Complete plastid genome sequences of three rosids (Castanea, Prunus, Theobroma): evidence for at least two independent transfers of rpl22 to the nucleus. Molecular Biology and Evolution 28(1): 835-847.

    Janz, N. 2011. Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annual Review of Ecology, Evolution, and Systematics 42: 71-89.

    Jasinski, S., A. C. M. Vialette-Guiraud, and C. P. Scutt. 2010. The evolutionary-developmental analysis of plant microRNAs. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 469-476.

    Jeune, B., D. Barabé, and C. Lacroix. 2006. Classical and dynamic morphology: toward a synthesis through the space of forms. Acta Biotheoretica 54: 277-293.

    Jiang, C. and X. Fu. 2007. GA action: turning on de-DELLA repressing signaling. Current Opinion in Plant Biology 10(5): 461-465.

    Jiao, Y. and H. Guo. 2014. Chapter Nine. Prehistory of the angiosperms: characterization of the ancient genomes. Pp. 223-246 In: A. H. Paterson (ed.), Advances in Botanical Research, Volume 69. London: Elsevier-Academic Press, 432 pp.

    Jiao, Y., J. Leebens-Mack, S. Ayyampalayam, J. E. Bowers, M. R. McKain, J. McNeal, M. Rolf, D. R. Ruzicka, E. Wafula, N. L. Wickett, X. Wu, Yong Zhang, J. Wang, Yeting Zhang, E. J. Carpenter, M. K. Deyholos, T. M. Kutchan, A. S. Chanderbali, P. S. Soltis, D. Wm. Stevenson, R. McCombie, J. C. Pires, G. K.-S. Wong, D. E. Soltis, and C. W. dePamphilis. 2012. A genome triplication associated with early diversification of eudicots. Genome Biology 13: R3.

    Jiao, Y., N. L. Wickett, S. Ayyampalayam, A. S. Chanderbali, L. Landherr, P. E. Ralph, L. P. Tomsho, Y. Hu, H. Liang, P. S. Soltis, D. E. Soltis, S. W. Clifton, S. E. Schlarbaum, S. C. Schuster, H. Ma, J. Leebens-Mack, and C. W. dePamphilis. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345): 97-100.

    Johnson, K. and M. Lenhard. 2011. Genetic control of plant organ growth. New Phytologist 191(2): 319-333.

    Jousselin, E., Jean-Yves Rasplus, and F. Kjellberg. 2003. Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Ficus. Evolution 57(6): 1255-1269.

    Juan, D., F. Pazos, and A. Valencia. 2008. High-confidence prediction of global interactomes based on genome-wide coevolutionary networks. Proceedings of the National Academy of Sciences 105(3): 934-939.

    Katsir, L., H. S. Chung, A. J. K. Koo, and G. A. Howe. 2008. Jasmonate signaling: a conserved mechanism of hormone sensing. Current Opinion in Plant Biology 11(4): 428-435.

    Kaufmann, K., R. Melzer, and G. Theißen. 2005. MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347(2): 183-198.

    Kaufmann, K., J. M. Muiño, R. Jauregui, C. A. Airoldi, C. Smaczniak, P. Krajewski, and G. C. Angenent. 2009. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biology 7(4): e1000090.

    Kelley, D. R., D. J. Skinner, and C. S. Gasser. 2009. Roles of polarity determinants in ovule development. The Plant Journal 57(6): 1054-1064.

    Kerney, R., E. Kim, R. P. Hangarter, A. E. Heiss, C. D. Bishop, and B. K. Hall. 2011. Intracellular invasion of green algae in a salamander host. Proceedings of the National Academy of Sciences 108(16): 6497-6502.

    Kim, J.-Y., Z. Yuan, and D. Jackson. 2003. Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130: 4351-4362.

    Kim, S., M.-J. Yoo, V. A. Albert, J. S. Farris, P. S. Soltis, and D. E. Soltis. 2004. Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication. American Journal of Botany 91(12): 2102-2118.

    Kim, S., J. Koh, M. Jeong, H. Kong, Y. Hu, H. Ma, P. S. Soltis, and D. E. Soltis. 2005. Expression of MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. The Plant Journal 43: 724-744.

    Kim, S., J. Koh, H. Ma, Y. Hu, P. K. Endress, M. Buzgo, B. A. Hauser, P. S. Soltis, and D. E. Soltis. 2005. Sequence and expression studies of A-, B-, and E-class MADS-box genes in Eupomatia (Eupomatiaceae): support for the bracteate origin of the calyptra. International Journal of Plant Science 166: 185-198.

    Kim, S., P. S. Soltis, K. Wall, and D. E. Soltis. 2006. Phylogeny and domain evolution in the APETALA2-like gene family. Molecular Biology and Evolution 23(1): 107-120.

    Kim, T.-W. and Z.-Y. Wang. 2010. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annual Review of Plant Biology 61: 681-704.

    Kirejtshuk, A. G. 2003. Subcortical space as an environment for palaeoendemic and young groups of beetles, using mostly examples from sap-beetles (Nitidulidae, Coleoptera). Proceedings of the Second Pan-European Conference on Saproxylic Beetles. People's Trust for Endangered Species, London, 7 pp.

    Knoll, A. H., R. K. Bambach, J. L. Payne, S. Pruss, and W. W. Fischer. 2007. Paleophysiology and end-Permian extinction. Earth and Planetary Science Letters 256(3-4): 295-313.

    Koes, R., W. Verweij, and F. Quattrocchio. 2005. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends in Plant Science 10(5): 236-242.

    Koltai, H. L. 2013. Strigolactones activate different hormonal pathways for regulation of root development in response to phosphate growth conditions. Annals of Botany 112(2): 409-415.

    Koltai, H., R. Matusova, and Y. Kapulnik. 2012. Strigolactones in root exudates as a signal in symbiotic and parasitic interactions. Pp. 49-73 In: J. M. Vivanco and F. Baluška (eds.), Secretions and Exudates in Biological Systems, Signaling and Communication in Plants, 12. New York: Springer, 283 pp.

    Korb, J. and K. Hartfelder. 2008. Life history and development - a framework for understanding developmental plasticity in lower termites. Biological Reviews 83: 295-313.

    Kozur, H. W. and R. E. Weems. 2011. Detailed correlation and age of continental Changhsingian and earliest Triassic beds: implications for the role of the Siberian Trap in the Permian-Triassic biotic crisis. Palaeogeography, Palaeoclimatology, Palaeoecology 308(1-2): 22-40.

    Kramer, E. M. 2007. Understanding the genetic basis of floral diversity. BioScience 57(6): 479-487.

    Kramer, E. M., R. L. Dorit, and V. F. Irish. 1998. Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149: 765-777.

    Kramer, E. M., V. S. Di Stilio, and P. M. Schlüter. 2003. Complex patterns of gene duplications in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. International Journal of Plant Sciences 164: 1-11.

    Kramer, E. M., M. A. Jaramillo, and V. S. Di Stilio. 2004. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166: 1011-1023.

    Kramer, E. M., L. Holappa, B. Gould, M. A. Jaramillo, D. Setnikov, and P. M. Santiago. 2007. Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. The Plant Cell 19: 750-766.

    Krassilov, V. A. 1977. The origin of angiosperms. Botanical Review 43(1): 143-176.

    Krassilov, V. A. 1991. The origin of angiosperms: new and old problems. Trends in Ecology and Evolution 6(7): 215-220.

    Krassilov, V. A. 1997. Angiosperm Origins: Morphological and Ecological Aspects. Sofia: Pensoft, 270 pp.

    Krassilov, V. A. 2002. Character parallelism and reticulation in the origin of angiosperms. Chapter 29, Pp. 373-382 In: M. Syvanen and C. I. Kado (eds.), Horizontal Gene Transfer, San Diego: Academic Press, 445 pp.

    Krassilov, V. A. 2008. Mine and gall predation as top down regulation in the plant-insect systems from the Cretaceous of Negev, Israel. Palaeogeography, Palaeoclimatology, Palaeoecology 261(3-4): 261-269.

    Krassilov, V. A. 2008. Evidence of temporary mining in the Cretaceous fossil mine assemblage of Negev, Israel. Insect Science 15(3): 285-290.

    Krassilov, V. A. and L. B. Golovneva. 2004. A minute mid-Cretaceous flower from Siberia and implications for the problem of basal angiosperms. Geodiversitas 26(1): 5-15.

    Krassilov, V. A. and A. P. Rasnitsyn. 1997. Pollen in the guts of Permian insects: first evidence of pollenivory and its evolutionary significance. Lethaia 29: 369-372.

    Krassilov, V., M. Tekleva, N. Meyer-Melikyan, and A. Rasnitsyn. 2003. New pollen morphotype from gut compression of a Cretaceous insect, and its bearing on palynomorphological evolution and palaeoecology. Cretaceous Research 24: 149-156.

    Krassilov, V. A., V. V. Zherikhin, and A. P. Rasnitsyn. 1997. Classopollis in the guts of Jurassic insects. Palaeontology 40(4): 1095-1101.

    Krizek, B. A. 2009. AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiology 150: 1916-1929.

    Kuhlemeier, C. 2007. Phyllotaxis. Trends in Plant Science 12(4): 143-150.

    Kuroda, J., R. S. Hori, K. Suzuki, D. R. Gröcke, and N. Ohkouchi. 2010. Marine osmium isotope record across the Triassic-Jurassic boundary from a Pacific pelagic site. Geology 38(12): 1095-1098.

    Kürschner, W. M., S. J. Batenburg, and L. Mander. 2013. Aberrant Classopollis pollen reveals evidence for unreduced (2n) pollen in the conifer family Cheirolepidiaceae during the Triassic-Jurassic transition. Proceedings of the Royal Society of London, Series B, Biological Sciences 280(1768): 20131708.

    Kwiatkowska, D. 2006. Flower primordium formation at the Arabidopsis shoot apex: quantitative analysis of surface geometry and growth. Journal of Experimental Botany 57(3): 571-580.

    Labandeira, C. C. 1997. Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics 28: 153-193.

    Labandeira, C. C. 1998. Early history of arthropod and vascular plant associations. Annual Review of Ecology and Planetary Sciences 26: 329-377.

    Labandeira, C. C. 1998. How old is the flower and the fly? Science 280: 57-59.

    Labandeira, C. C. 2000. The paleobiology of pollination and its precursors. Pp. 233-269 In: R. A. Gastaldo and W. A. DiMichele (eds.), Phanerozoic Terrestrial Ecosystems. Paleontological Society Papers 6: 233-269.

    Labandeira, C. C. 2002. Chapter 2. The history of associations between plants and insects. Pp. 26-74 In: C. M. Herrera and O. Pellmyr (eds.), Plant Animal Interactions: An Evolutionary Approach. Oxford: Blackwell, 328 pp.

    Labandeira, C. C. 2006. The four phases of plant-arthropod associations in deep time. Geologica Acta 4(4): 409-438.

    Labandeira, C. C. 2007. Pollination drops, pollen, and insect pollination of Mesozoic gymnosperms. Taxon 56(3): 663-695.

    Labandeira, C. C. 2007. The origin of herbivory on land: initial patterns of plant tissue consumption by arthropods. Insect Science 14(4): 259-275.

    Labandeira, C. C. 2010. The pollination of mid-Mesozoic seed plants and the early history of long-proboscid insects. Annals of the Missouri Botanical Garden 97(4): 469-513.

    Labandeira, C. C. 2013. A paleobiologic perspective on plant-insect interactions. Current Opinion in Plant Biology 16: 414-421.

    Labandeira, C. C. 2014. Chapter 13. Why did terrestrial insect diversity not increase during the angiosperm radiation? Mid-Mesozoic, plant-associated insect lineages harbor clues. Pp. 261-299 In: P. Pontarotti (ed.), Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life. New York: Springer, 398 pp.

    Labandeira, C. C. and E. G. Allen. 2007. Minimal insect herbivory for the Lower Permian coprolite bone bed site of north-central Texas, USA, and comparison to other late Paleozoic floras. Palaeogeography, Palaeoclimatology, and Palaeoecology 247(3-4): 197-219.

    Labandeira, C. C. and E. D. Currano. 2013. The fossil record of plant-insect dynamics. Annual Review of Earth and Planetary Sciences 41: 287-311.

    Labandeira, C. C., D. L. Dilcher, D. R. Davis, and D. L. Wagner. 1994. Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proceedings of the National Academy of Sciences 91(25): 12278-12282.

    Labandeira, C. C., K. R. Johnson, and P. Wilf. 2002. Impact of the terminal Cretaceous event on plant-insect associations. Proceedings of the National Academy of Sciences 99(4): 2061-2066.

    Labandeira, C. C. and J. J. Sepkoski, Jr. 1993. Insect diversity in the fossil record. Science 261: 310-315.

    Lai, X., W. Wang, P. B. Wignall, D. P. G. Bond, H. Jiang, J. R. Ali, E. H. John, and Y. Sun. 2008. Palaeoenvironmental change during the end-Guadalupian (Permian) mass extinction in Sichuan, China. Palaeogeography, Palaeoclimatology, Palaeoecology 269(1-2): 78-93.

    Lamarque, J.-F., J. T. Kiehl, C. A. Shields, B. A. Boville, and D. E. Kinnison. 2006. Modeling the response to changes in tropospheric methane concentration: application to the Permian-Triassic boundary. Paleoceanography 21.

    Langdale, J. A. 2008. Evolution of developmental mechanisms in plants. Current Opinion in Genetics and Development 18(4): 368-373.

    Laubichler, M. D. 2000. Homology and the development of the homology concept. American Zoologist 40: 777-788.

    Lee, D., D. H. Polisensky, and J. Braam. 2005. Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. New Phytologist 165: 429-444.

    Lee, S. and J. Chappell. 2008. Biochemical and genomic characterization of terpene synthases in Magnolia grandiflora. Plant Physiology 147: 1017-1033.

    Leppik, E. E. 1960. Early evolution of flower types. Lloydia 23(3): 72-92.

    Leppik, E. E. 1968. Directional trend of floral evolution. Acta Biotheoretica 18A(1-4): 87-102.

    Leroy, J.-F. 1983. The origin of angiosperms: an unrecognized ancestral dicotyledon, Hedyosmum (Chloranthales), with a strobiloid flower is living today. Taxon 32: 169-175.

    Lersten, N. R. and J. D. Curtis. 1989. Polyacetylene reservoir (duct) development in Ambrosia trifida (Asteraceae) staminate flowers. American Journal of Botany 76(7): 1000-1005.

    Les, D. H. 1988. The origin and affinities of the Ceratophyllaceae. Taxon 37(2): 326-345.

    Les, D. H. 1993. Ceratophyllaceae. Pp. 246-250 In: K. Kubitzki, J. G. Rohwer, and V. Bittrich (eds.), The Families and Genera of Vascular Plants, Volume II, Flowering Plants - Dicotyledons, Magnoliids, Hamamelids, and Caryophyllids. Berlin, Springer.

    Les, D. H., D. K. Garvin, and C. M. Wimpee. 1991. Molecular evolutionary history of ancient aquatic angiosperms. Proceedings of the National Academy of Sciences 88: 10119-10123.

    Leseberg, C. H., C. L. Eissler, X. Wang, M. A. Johns, M. R. Duvall, and L. Mao. 2008. Interaction study of MADS-domain proteins in tomato. Journal of Experimental Botany 59(8): 2253-2265.

    Li, C., E. M. Ripley, A. J. Naldrett, A. K. Schmitt, and C. H. Moore. 2009. Magmatic anhydrite-sulfide assemblages in the plumbing system of the Siberian Traps. Geology 37(3): 259-262.

    Li, J. and J. Chory. 1999. Brassinosteroid actions in plants. Journal of Experimental Botany 50(332): 275-282.

    Li, X., H. X. Wu, and S. G. Southerton. 2010. Comparative genomics reveals conservative evolution of the xylem transcriptome in vascular plants. BMC Plant Biology 10: 190.

    Liang, H., A. Barakat, S. E. Schlarbaum, and J. E. Carlson. 2011. Organization of the chromosome region harboring a FLORICAULA/LEAFY gene in Liriodendron. Tree Genetics and Genomes 7(2): 373-384.

    Licausi, F. 2011. Regulation of the molecular response to oxygen limitations in plants. New Phytologist 190(3): 550-555.

    Licausi, F., D. A. Weits, B. D. Pant, W-R. Scheible, P. Geigenberger, and J. T. van Dongen. 2011. Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytologist 190(2): 442-456.

    Linkies, A., K. Graeber, C. Knight, and G. Leubner-Metzger. 2010. The evolution of seeds. New Phytologist 186(4): 817-831.

    Litt, A. and E. M. Kramer. 2010. The ABC model and the diversification of floral organ identity. Seminars in Cell & Developmental Biology 21(1): 129-137.

    Liu, C., J. Zhang, N. Zhang, H. Shan, K. Su, J. Zhang, Z. Meng, H. Kong, and Z. Chen. 2010. Interactions among proteins of floral MADS-Box genes in basal eudicots: implications for evolution of the regulatory network for flower development. Molecular Biology and Evolution 27(7): 1598-1611.

    Liu, Z. and C. Mara. 2010. Regulatory mechanisms for floral homeotic gene expression. Seminars in Cell & Developmental Biology 21(1): 80-86.

    Lloyd, G. T., K. E. Davis, D. Pisani, J. E. Tarver, M. Ruta, M. Sakamoto, D. W. E. Hone, R. Jennings, and M. J. Benton. 2008. Dinosaurs and the Cretaceous terrestrial revolution. Proceedings of the Royal Society of London, Series B, Biological Sciences 275(1650): 2483-2490.

    Loconte, H. 1996. Chapter 10. Comparison of alternative hypotheses for the origin of angiosperms. Pp. 267-284 In: D. W. Taylor and L. J. Hickey (eds.) Flowering Plant Origin, Evolution, and Phylogeny, New York: Chapman and Hall, 403 pp.

    Lomax, B. H., J. Hilton, R. M. Bateman, G. R. Upchurch, J. A. Lake, I. J. Leitch, A. Cromwell, and C. A. Knight. 2014. Reconstructing relative genome size of vascular plants through geological time. New Phytologist 201(2): 636–644.

    Looy, C. V., W. A. Brugman, D. L. Dilcher, and H. Visscher. 1999. The delayed resurgence of equatorial forests after the Permian-Triassic ecological crisis. Proceedings of the National Academy of Sciences 96(24): 13857-13862.

    Looy, C. V., R. J. Twitchett, D. L. Dilcher, J. H. A. Van Konijnenburg-Van Cittert, and H. Visscher. 2001. Life in the end-Permian dead zone. Proceedings of the National Academy of Sciences 98(14): 7879-7883.

    Lora, J., M. Herrero, and J. I. Hormaza. 2009. The coexistence of bicellular and tricellular pollen in Annona cherimola (Annonaceae): implications for pollen evolution. American Journal of Botany 96(4): 802-808.

    Lord, E. M. and S. D. Russell. 2002. The mechanism of pollination and fertilization in plants. Annual Review of Cell and Developmental Biology 18: 81-105.

    Lovisolo, O., R. Hull, and O. Rösler. 2003. Coevolution of viruses with hosts and vectors and possible paleontology. Pp. 325-379 In: K. Maramorosch, F. A. Murphy, and A. J. Shatkin (eds.), Advances in Virus Research, Volume 62. Boston: Elsevier-Academic Press.

    Lu, S., Y.-H. Sun, R. Shi, C. Clark, L. Li, and V. L. Chiang. 2005. Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. The Plant Cell 17: 2186-2203.

    Lucas, S. G., L. H. Tanner, L. L. Donohoo-Hurley, J. W. Geissman, H. W. Kozur, A. B. Heckert, and R. E. Weems. 2011. Position of the Triassic-Jurassic boundary and timing of the end-Triassic extinctions on land: data from the Moenave Formation on the southern Colorado Plateau, USA. Palaeogeography, Palaeoclimatology, and Palaeoecology 302(3-4): 194-205.

    Luo, G., Y. Wang, H. Yang, T. J. Algeo, L. R. Kump, J. Huang, and S. Xie. 2011. Stepwise and large-magnitude shift in δ13Ccarb preceded the main marine mass extinction of the Permian-Triassic crisis interval. Palaeogeography, Palaeoclimatology, and Palaeoecology 299(1-2): 70-82.

    Lupia, R., S. Lidgard, and P. R. Crane. 1999. Comparing palynological abundance and diversity: implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology 25: 305-340.

    Ma, H. and C. dePamphilis. 2000. The ABCs of floral evolution. Cell 101(1): 5-8.

    Ma, Xiaoya, G. D. Edgecombe, Xianguang Hou, T. Goral, and N. J. Strausfeld. 2015. Preservational pathways of corresponding brains of a Cambrian euarthropod. Current Biology 25(22): 2969-2975.

    Ma, Xiaoya, X. Hou, G. D. Edgecombe, and N. J. Strausfeld. 2012. Complex brain and optic lobes in an early Cambrian arthropod. Nature 490(7419): 258-262.

    Machado, C. A., N. Robbins, M. T. P. Gilbert, and E. A. Herre. 2005. Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proceedings of the National Academy of Sciences 102(Supplement 1): 6558-6565.

    Madrid, E. N. and W. E. Friedman. 2008. Female gametophyte development in Aristolochia labiata Willd. (Aristolochiaceae). Botanical Journal of the Linnaean Society 158(1): 19-29.

    Madrid, E. N. and W. E. Friedman. 2009. The developmental basis of an evolutionary diversification of female gametophyte structure in Piper and Piperaceae. Annals of Botany 103(6): 869-884.

    Maere, S., S. De Bodt, J. Raes, T. Casneuf, M. Van Montagu, M. Kuiper, and Y. Van de Peer. 2005. Modeling gene and genome duplications in eukaryotes. Proceedings of the National Academy of Sciences 102(15): 5454-5459.

    Magallón, S. 2010. Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Systematic Biology 59(4): 384-399.

    Magallón, S. 2014. A review of the effect of relaxed clock method, long branches, genes, and calibrations in the estimation of angiosperm age. Botanical Sciences (Boletín de la Sociedad Botánica de México) 92[1]: 1-22.

    Magallón, S., S. Gómez-Acevedo, L. L. Sánchez-Reyes, and T. Hernández-Hernández. 2015. A meta-calibrated time tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist 207: 437-453.

    Maheshwari, H. K. 2007. Deciphering angiosperm origins. Current Science 92(5): 606-611.

    Maizel, A., M. A. Busch, T. Tanahashi, J. Perkovic, M. Kato, M. Hasebe, and D. Weigel. 2005. The floral regulator LEAFY evolves by substitutions in the DNA-binding domain. Science 308(5719): 260-263.

    Mamay, S. H. 1976. Paleozoic Origin of the Cycads. U. S. Geological Survey Professional Paper 934, 48 pp.

    Mamay, S. H., J. M. Miller, D. M. Rohr, and W. E. Stein, Jr. 1988. Foliar morphology and anatomy of the gigantopterid plant Delnortea abbottiae from the Lower Permian of West Texas. American Journal of Botany 75(9): 1409-1433.

    Mander, L., W. M. Kürschner, and J. C. McElwain. 2010. An explanation for conflicting records of Triassic-Jurassic plant diversity. Proceedings of the National Academy of Sciences 107(35): 15351-15356.

    Masselter, T., N. Rowe, J. Galtier, and T. Speck. 2009. Secondary growth and deformation of stem tissues in the Lower Carboniferous seed fern Calamopitys. International Journal of Plant Sciences 170(9): 1228-1239.

    Mathews, S. 2009. Phylogenetic relationships among seed plants: persistent questions? American Journal of Botany 96(1): 228-236.

    Mathews, S., M. D. Clements, and M. A. Beilstein. 2010. A duplicate gene rooting of seed plants and the phylogenetic position of flowering plants. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 383-395.

    Mathews, S. and M. J. Donoghue. 1999. The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286: 947-950.

    Mathews, S. and E. M. Kramer. 2012. The evolution of reproductive structures in seed plants: a re-examination based on insights from developmental genetics. New Phytologist 194(4): 910-923.

    Mayer, K. F. X., H. Schoof, A. Haecker, M. Lenhard, G. Jürgens, and T. Laux. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95(6): 805-815.

    McElwain, J. C., D. J. Beerling, and F. I. Woodward. 1999. Fossil plants and global warming at the Triassic-Jurassic boundary. Science 285: 1386-1390.

    McElwain, J. C., I. Montañez, J. D. White, J. P. Wilson, and Y. Yiotis. 2016. Was atmospheric CO2 capped at 1000 ppm over the past 300 million years? Palaeogeography, Palaeoclimatology, and Palaeoecology 441(3-4): 653-658.

    McElwain, J. C., M. E. Popa, S. P. Hesselbo, M. Haworth, and F. Surlyk. 2007. Macroecological responses of terrestrial vegetation to climatic and atmospheric change across the Triassic/Jurassic boundary in east Greenland. Paleobiology 33(4): 547-573.

    McElwain, J. C. and S. W. Punyasena. 2007. Mass extinction events and the plant fossil record. Trends in Ecology and Evolution 22(10): 548-557.

    McElwain, J. C., K. J. Willis, and R. Lupia. 2005. Chapter 7. Cretaceous CO2 decline and the radiation and diversification of angiosperms. Pp. 133-165 In: J. R. Ehleringer, T. E. Cerling, and M.-D. Dearing, A History of Atmospheric CO2 and its Effects on Plants, Animals, and Ecosystems. New York: Springer, 530 pp.

    McElwain, J. C., K. J. Willis, and K. J. Niklas. 2011. 5. Long-term fluctuations in atmospheric CO2 concentration influence plant speciation rates. Pp. 122-140 In: T. R. Hodkinson, M. B. Jones, S. Waldren, and J. A. N. Parnell (eds.), Climate Change, Ecology and Systematics. Cambridge: Cambridge University Press, 524 pp.

    McGhee, G. R., Jr. 1996. The Late Devonian Mass Extinction: The Frasnian/Famennian Crisis. New York: Columbia, 303 pp.

    McGhee, G. R., Jr. 2007. The Geometry of Evolution: Adaptive Landscapes and Theoretical Morphospaces. Cambridge: Cambridge University Press, 212 pp.

    McGrath, C. L. and M. Lynch. 2012. Chapter 1. Evolutionary significance of whole-genome duplication. Pp. 1-20 In: P. S. Soltis and D. E. Soltis (eds.), Polyploidy and Genome Evolution. New York: Springer, 415 pp.

    McLoughlin, S. 2011. New records of leaf galls and arthropod oviposition scars in Permian-triassic Gondwanan gymnosperms. Australian Journal of Botany 59(2): 156-169.

    McLoughlin, S., R. J. Carpenter, G. J. Jordan, and R. S. Hill. 2008. Seed ferns survived the end-Cretaceous mass extinction in Tasmania. American Journal of Botany 95(4): 465-471.

    Meeuse, B. J. D. 1978. The Physiology of some sapromyophilous flowers. Pp. 97-104 In: A. J. Richards, ed., The Pollination of Flowers by Insects. Academic Press: Linnean Society of London, 213 pp.

    Meeuse, B. J. D. 1979. Anthocorm Theory. Amsterdam: University of Amsterdam.

    Melzer, R., A. Härter, F. Rümpler, S. Kim, P. S. Soltis, D. E. Soltis, and G. Theißen. 2014. DEF- and GLO-like proteins may have lost most of their interaction partners during angiosperm evolution. Annals of Botany (Oxford) 114 (7): 1431-1443.

    Melzer, R. and G. Theißen. 2009. Reconstitution of "floral quartets" in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Research 37(8): 2723-2736.

    Melzer, R., W. Verelst, and G. Theißen. 2009. The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in "floral quartet"-like complexes in vitro. Nucleic Acids Research 37(1): 144-157.

    Melzer, R., Y.-Q. Wang, and G. Theißen. 2010. The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Seminars in Cell & Developmental Biology 21(1): 118-128.

    Melville, R. 1969. Leaf venation patterns and the origin of angiosperms. Nature 224: 121-125.

    Melville, R. 1983. Glossopteridae, Angiospermidae and the evidence for angiosperm origin. Botanical Journal of the Linnaean Society 86: 279-323.

    Merebet, S. and B. Hudry. 2011. On the border of the homeotic function: re-evaluating the controversial role of cofactor-recruiting motifs. BioEssays 33(7): 499-507.

    Meyen, S. V. 1986. Hypothesis of the origin of angiosperms from Bennettitales by gamoheterotophy: transition of characters from one sex to another. Zhurnal Obshchei Biologii 47: 291-309.

    Meyen, S. V. 1988. Origin of the angiosperm gynoecium by gamoheterotophy. Botanical Journal of the Linnaean Society 97: 171-178.

    Meyerowitz, E. M. 2002. Plants compared to animals: the broadest comparative study of development. Science 295: 1482-1485.

    Michard, E., P. T. Lima, F. Borges, A. C. Silva, M. T. Portes, J. E. Carvalho, M. Gilliham, L-H. Liu, G. Obermeyer, and J. A. Feijó. 2011. Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332(6028): 434-437.

    Miles, C. M., S. E. Lott, C. L. Luengo-Hendriks, M. Z. Ludwig, Manu, C. L. Williams, and M. Kreitman. 2011. Artificial selection on egg size perturbs early pattern formation in Drosophila melanogaster. Evolution 65(1): 33-42.

    Miller, J. M. 1989. The archaic flowering plant family Degeneriaceae: its bearing on an old enigma. National Geographic Research 5(2): 218-231.

    Mirabet, V., P. Das, A. Boudaoud, and O. Hamant. 2011. The role of mechanical forces in plant morphogenesis. Annual Review of Plant Biology 62: 365-385.

    Misof, B., Shanlin Liu, K. Meusemann, R. S. Peters, A. Donath, C. Mayer, P. B. Frandsen, J. Ware, T. Flouri, R. G. Beutel, O. Niehuis, M. Petersen, F. Izquierdo-Carrasco, T. Wappler, J. Rust, A. J. Aberer, U. Aspöck, H. Aspöck, D. Bartel, A. Blanke, S. Berger, A. Böhm, T. R. Buckley, B. Calcott, Junqing Chen, F. Friedrich, M. Fukui, M. Fujita, C. Greve, P. Grobe, Shengchang Gu, Ying Huang, L. S. Jermiin, A. Y. Kawahara, L. Krogmann, M. Kubiak, R. Lanfear, H. Letsch, Yiyuan Li, Zhenyu Li, Jiguang Li, Haorong Lu, R. Machida, Y. Mashimo, P. Kapli, D. D. McKenna, Guanliang Meng, Y. Nakagaki, J. L. Navarrete-Heredia, M. Ott, Yanxiang Ou, G. Pass, L. Podsiadlowski, H. Pohl, B. M. von Reumont, K. Schütte, K. Sekiya, S. Shimizu, A. Slipinski, A. Stamatakis, Wenhui Song, Xu Su, N. U. Szucsich, Meihua Tan, Xuemei Tan, Min Tang, Jingbo Tang, G. Timelthaler, S. Tomizuka, M. Trautwein, Xiaoli Tong, T. Uchifune, M. G. Walz, B. M. Wiegmann, J. Wilbrandt, B. Wipfler, T. K. F. Wong, Qiong Wu, Gengxiong Wu, Yinlong Xie, Shenzh Yang, D. K. Yeates, K. Yoshizawa, Qing Zhang, Rui Zhang, Wenwei Zhang, Yunhui Zhang, Jing Zhao, Chengran Zhou, Lili Zhou, T. Ziesmann, Shijie Zou, Yingrui Li, Xun Xu, Yong Zhang, Huanming Yang, Jian Wang, Jun Wang, K. M. Kjer, and Xin Zhou. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346(6210): 763-767.

    Moczek, A. P., S. Sultan, S. Foster, C. Ledón-Rettig, I. Dworkin, H. F. Nijhout, E. Abouheif, and D. W. Pfennig. 2011. The role of developmental plasticity in evolutionary innovation. Proceedings of the Royal Society of London, Series B, Biological Sciences 278(1719): 2705-2713.

    Moldowan, J. M. and S. R. Jacobson. 2002. Chemical signals for early evolution of major taxa: biosignatures and taxon-specific biomarkers. Pp. 19-26 In: W. G. Ernst (ed.), Frontiers in Geochemistry, Organic, Solution, and Ore Deposit Geochemistry, Konrad Krauskopf Volume 2, International Book Series, Volume 6. Columbia: Bellwether Publishing Ltd., 265 pp.

    Montañez, I. P. and C. J. Poulsen. 2013. The late Paleozoic ice age: an evolving paradigm. Annual Review of Earth and Planetary Sciences 41: 629-656.

    Moreira, C. K., M. de L. Capurro, M. Walter, E. Pavlova, H. Biessmann, A. A. James, A. G. deBianchi, and O. Marinotti. 2004. Primary characterization and basal promoter activity of two hexamerin genes of Musca domestica. Journal of Insect Science 4: 1-10.

    Morley, R. J. 2001. Why are there so many primitive angiosperms in the rain forests of Asia-Australasia. Pp. 185-200 In: I. Metcalfe, J. M. B. Smith, M. Morwood, and I. Davidson (eds.), Faunal and Floral Migrations and Evolution in SE Asia-Australasia. Lisse: Swets and Zeitlinger, 419 pp.

    Mouradov, A., T. Glassick, B. Hamdorf, L. Murphy, B. Fowler, S. Marla, and R. D. Teasdale. 1998. NEEDLY, a Pinus radiata ortholog of FLORICAULA/LEAFY genes, expressed in both reproductive and vegetative meristems. Proceedings of the National Academy of Sciences 95: 6537-6542.

    Moussian, B. 2010. Recent advances in understanding mechanisms of insect cuticle differentiation. Insect Biochemistry and Molecular Biology 40(5): 363-375.

    Moyroud, E., E. Kusters, M. Monniaux, R. Koes, and F. Parcy. 2010. LEAFY blossoms. Trends in Plant Science 15: 346-352.

    Moyroud, E., G. Tichtinsky, and F. Parcy. 2009. The LEAFY floral regulators in angiosperms: conserved proteins with diverse roles. Journal of Plant Biology 52(3): 177-185.

    Muchhala, N. and J. D. Thomson. 2009. Going to great lengths: selection for long corolla tubes in an extremely specialized bat-flower mutualism. Proceedings of the Royal Society of London, Series B, Biological Sciences 276(1665): 2147-2152.

    Mukherjee, K., L. Brocchieri, and T. R. Bürglin. 2009. A comprehensive classification and evolutionary analysis of plant homeobox genes. Molecular Biology and Evolution 26(12): 2775-2794.

    Müller, J. 1984. Significance of fossil pollen for angiosperm history. Annals of the Missouri Botanical Garden 71(2): 419-443.

    Munk, W. and H.-D. Sues. 1993. Gut contents of Parasaurus (Pareiasauria) and Protorosaurus (Archosauromorpha) from the Kupfierschiefer (Upper Permian) of Hessen, Germany. Palaontologische Zeitschrift 67: 169-176.

    Murase, K., Y. Hirano, T.-P. Sun, and T. Hakoshima. 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456(7221): 459-463.

    Nadot, S. and E. Dodinet. 2016. Letters to the twenty-first century botanist: "What is a flower?" Botany Letters 163(1): 9–10.

    Nadot, S., C. A. Furness, J. Sannier, L. Penet, S. Triki-Teurtroy, B. Albert, and A. Ressayre. 2008. Phylogenetic comparative analysis of microsporogenesis in angiosperms with a focus on monocots. American Journal of Botany 95(11): 1426-1436.

    Nair, P. K. K. 1979. The palynological basis for the triphyletic theory of angiosperms. Grana 18: 141-144.

    Nam, J., C. W. de Pamphilis, H. Ma, and M. Nei. 2003. Antiquity and evolution of the MADS-box gene family controlling flower development in plants. Molecular Biology and Evolution 20: 1435-1447.

    Nardmann, J., P. Reisewitz, and W. Werr. 2009. Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Molecular Biology and Evolution 26(8): 1745-1755.

    Nardmann, J. and W. Werr. 2013. Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. New Phytologist 199(4): 1081-1092.

    Nasrallah, J. B. 2005. Recognition and rejection of self in plant self-incompatibility: comparisons to animal histocompatibility. Trends in Immunology 26(8): 412-418.

    Negre, B., S. Casilla, M. Suzanne, E. Sánchez-Herrero, M. Akam, M. Nefedov, A. Barbadilla, P. de Jong, and A. Ruiz. 2005. Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox gene complex. Genome Research 15: 692-700.

    Nel, A., P. Roques, P. Nel, A. A. Prokin, T. Bourgoin, J. Prokop, J. Szwedo, D. Azar, L. Desutter-Grandcolas, T. Wappler, R. Garrouste, D. Coty, D. Huang, M. S. Engel, and A. G. Kirejtshuk. 2013. The earliest known holometabolous insects. Nature 503(7475): 257-261.

    Nelson, D. and D. Werck-Reichhart. 2011. A P450-centric view of plant evolution. The Plant Journal 66(1): 194-211.

    Neumann, P., A. Navrátilová, A. Koblízková, E. Kejnovsky, E. Hribová, R. Hobza, A. Widmer, J. Dolezel, and J. Macas. 2011. Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mobile DNA 2: 4.

    Nichols, D. J. and K. R. Johnson. 2008. Plants and the K-T Boundary. Cambridge: Cambridge University Press, 292 pp.

    Nijhout, H. F. 2003. The control of body size in insects. Developmental Biology 261(1): 1-9.

    Niklas, K. J. 1982. Differential preservation of protoplasm in fossil angiosperm leaf tissues. American Journal of Botany 69(3): 325-334.

    Niklas, K. J. 1992. Plant Biomechanics: An Engineering Approach to Plant Form and Function. Chicago: University of Chicago Press.

    Niklas, K. J. 1997. Adaptive walks through fitness landscapes for early vascular plants. American Journal of Botany 84(1): 16-25.

    Niklas, K. J. 2000. The evolution of plant body plans- a biomechanical perspective. Annals of Botany 85: 411-438.

    Niklas, K. J. 2006. Thinking outside the HOX. Biological Theory 1(2): 128-129.

    Niklas, K. J. and R. M. Brown, Jr. 1981. Ultrastructural and paleobiochemical correlations among fossil leaf tissues from the St. Maries River (Clarkia) area, northern Idaho, USA. American Journal of Botany 68(3): 332-341.

    Niklas, K. J., H. Spatz, and J. Vincent. 2006. Plant biomechanics: an overview and prospectus. American Journal of Botany 93(10): 1369-1378.

    Nishida, H., K. B. Pigg, K. Kudo, and J. F. Rigby. 2004. Zooidogamy in the late Permian genus Glossopteris. Journal of Plant Research 117: 323-328.

    Nishida, H., K. B. Pigg, and J. F. Rigby. 2003. Swimming sperm in an extinct Gondwanan plant. Nature 422: 396-397.

    Nixon, K. C., W. L. Crepet, D. M. Stevenson, and E. M. Friis. 1994. A reevaluation of seed plant phylogeny. Annals Missouri Botanical Garden 81: 484-533.

    Nole-Wilson, S. and B. A. Krisek. 2006. AINTEGUMENTA contributes to organ polarity and regulates growth of lateral organs in combination with YABBY genes. Plant Physiology 141: 977-987.

    Norstog, K. J., D. M. Stevenson, and K. J. Niklas. 1986. The role of beetles in the pollination of Zamia furfuracea L. (Zamiaceae). Biotropica 18(4): 300-306.

    Norstog, K. J. and P. K. S. Fawcett. 1989. Insect-cycad symbiosis and its relation to the pollination of Zamia furfuracea (Zamiaceae) by Rhopalotria mollis (Curculionidae). American Journal of Botany 76(9): 1380-1394.

    Okano, Y., N. Aono, Y. Hiwatashi, T. Murata, T. Nishiyama, T. Ishikawa, M. Kubo, and M. Hasebe. 2009. A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proceedings of the National Academy of Sciences 106(38): 16321-16326.

    Ori, N., Y. Eshed, G. Chuck, J. L. Bowman, and S. Hake. 2000. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127: 5523-5532.

    Owens, D. K., A. B. Alerding, K. C. Crosby, A. B. Bandara, J. H. Westwood, and B. S. J. Winkel. 2008. Functional analysis of a predicted flavonol synthase gene family in Arabidopsis. Plant Physiology 147: 1046-1061.

    Pace, D. W., R. A. Gastaldo, and J. Neveling. 2009. Aggradational and degradational landscapes in the early Triassic of the Karoo Basin and evidence for climatic oscillation following the P/Tr event. Journal of Sedimentary Research 79: 276-291.

    Palavan-Unsal, N. and D. Arisan. 2009. Nitric oxide signalling in plants. The Botanical Review 75(2): 203-229.

    Pálfy, J. 2003. Volcanism of the Central Atlantic Magmatic Province as a potential driving force in the end-Triassic mass extinction. Pp. 255-267 In: W. Hames, J. G. Mcgone, P. Renne, and C. Ruppel (eds.), The Central Atlantic Magmatic Province: Insights from Fragments of Pangea. Washington, D. C.: American Geophysics Union.

    Pálfy, J., A. Demény, J. Haas, M. Hetényi, M. J. Orchard, and I. Vetõ. 2001. Carbon isotope anomaly and other geochemical changes at the Triassic-Jurassic boundary. Geology 29: 1047-1050.

    Pandey, S. P., P. Shahi, K. Gase, and I. T. Baldwin. 2008. Herbivory-induced changes in small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proceedings of the National Academy of Sciences 105(12): 4559-4564.

    Parisod, C. and N. Senerchia. 2012. Chapter 9. Responses of transposable elements to polyploidy. Pp. 147-168 In: M-A. Grandbastien and J. M. Casacuberta (eds.), Plant Transposable Elements, Impact on Genome Structure and Function, Volume 24, Topics in Current Genetics. Berlin: Springer, 330 pp.

    Pauw, A., J. Stofberg, and W. J. Waterman. 2009. Flies and flowers in Darwin's race. Evolution 63(1): 268-279.

    Pauwels, L. D. Inzí, and A. Goossens. 2009. Jasmonate-inducible gene: what does it mean? Trends in Plant Science 14(2): 87-91.

    Pavlopoulos, A. and M. Akam. 2011. Hox gene Ultrabithorax regulates distinct sets of target genes at successive stages of Drosophila haltere morphogenesis. Proceedings of the National Academy of Sciences 108(7): 2855-2860.

    Pavlopoulos, A. and M. Averof. 2002. Developmental evolution: Hox proteins ring the changes. Current Biology 12: R291-R293.

    Payne, J. L., A. V. Turchyn, A. Paytan, D. J. DePaolo, D. J. Lehrmann, M. Yu, and J. Wei. 2010. Calcium isotope constraints on the end-Permian mass extinction. Proceedings of the National Academy of Sciences 107(19): 8543-8548.

    Pellmyr, O. and J. Leebens-Mack. 1999. Forty million years of mutualism: evidence for Eocene origin of the yucca-yucca moth association. Proceedings of the National Academy of Sciences 96(16): 9178-9183.

    Peng, Y. and G. R. Shi. 2009. Life crises on land across the Permian-Triassic boundary in south China. Global and Planetary Change 65(3-4): 155-165.

    Perazzolli, M., M. C. Romero-Puertas, and M. Delledonne. 2006. Modulation of nitric oxide bioactivity by plant haemoglobins. Journal of Experimental Botany 57(3): 479-488.

    Pham, T. and N. Sinha. 2003. Role of KNOX genes in shoot development of Welwitschia mirabilis. International Journal of Plant Sciences 164(3): 333-343.

    Piazza, P., S. Jasinski, and M. Tsiantis. 2005. Evolution of leaf developmental mechanisms. New Phytologist 167: 693-710.

    Pick, C., M. Schneuer, and T. Burmester. 2009. The occurrence of hemocyanin in Hexapoda. The FEBS Journal 276(7): 1930-1941.

    Pigliucci, M. 2002. Touchy and bushy: phenotypic plasticity and integration in response to wind stimulation in Arabidopsis thaliana. International Journal of Plant Sciences 163:399-408.

    Piwarzyk, E., Y. Yang, and T. Jack. 2007. Conserved C-terminal motifs of the Arabidopsis proteins APETALA3 and PISTILLATA are dispensable for floral organ identity function. Plant Physiology 145: 1495-1505.

    Ponomarenko, A. G. 1998. Paleobiology of angiospermization. Paleontologicheskii Zhurnal 32(4): 325-331.

    Porter, B. W., Y. J. Zhu, D. T. Webb, and D. A. Christopher. 2009. Novel thigmomorphogenetic responses in Carica papaya: touch decreases anthocyanin levels and stimulates petiole cork outgrowths. Annals of Botany 103(6): 847-858.

    Poulsen, C. J., C. Tabor, and J. D. White. 2015. Long-term climate forcing by atmospheric oxygen concentrations, Science 348 (6240): 1238-1241.

    Povilus, R. A., J. M. Losada, and W. E. Friedman. 2015. Floral biology and ovule and seed ontogeny of Nymphaea thermarum, a water lily at the brink of extinction with potential as a model system for basal angiosperms. Annals of Botany (Oxford) 115(2): 211-226.

    Prigge, M. J. and S. E. Clark. 2006. Evolution of the class III HD-Zip family in land plants. Evolution and Development 8(4): 350-361.

    Proost, S., P. Pattyn, T. Gerats, and Y. Van de Peer. 2011. Journey through the past 150 million years of plant genome evolution. The Plant Journal 66(1): 58-65.

    Pruyn, M. L., F. W. Ewers, and F. Telewski. 2000. Thigmomorphogenesis: changes in the morphology and mechanical properties of two Populus hybrids in response to mechanical perturbation. Tree Physiology 20: 535-540.

    Qiu, Y.-L. 2008. Phylogeny and evolution of charophytic algae and land plants. Journal of Systematics and Evolution 46(3): 287-306.

    Qiu, Y.-L., L. Jungho, F. Bernasconi-Quadroni, D. E. Soltis, P. Soltis, M. Zanis, E. Zimmer, C. Ziduan, V. Savolainen, and M. W. Chase. 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402(6760): 404-407.

    Qu, L.-H. and M.-X. Sun. 2007. The plant cell nucleus is constantly alert and highly sensitive to repetitive local mechanical stimulations. Plant Cell Reports 26(8): 1187-1193.

    Raghavan, V. 2003. Some reflections on double fertilization, from its discovery to the present. New Phytologist 159: 565-583.

    Ramanujam, C. G. K. 2004. Palms through ages in southern India: a reconnaissance. Palaeobotanist 53: 1-4.

    Rameau, C. 2010. Strigolactones, a novel class of plant hormone controlling shoot branching. Comptes Rendus Biologies 333(4): 344-349.

    Ramírez, S. R., T. Eltz, M. K. Fujiwara, G. Gerlach, B. Goldman-Huertas, N. D. Tsutsui, and N. E. Pierce. 2011. Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333(6050): 1742-1746.

    Ramírez, S. R., B. Gravendeel, R. B. Singer, C. R. Marshall, and N. E. Pierce. 2007. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448(7157): 1042-1045.

    Rasnitsyn, A. P. 2002. History of Insect Orders, Pp. 65-324 In.: A. P. Rasnitsyn and D. I. J. Quicke, eds. History of Insects. London: Kluwer Academic Publishers, 517 pp.

    Raven, P. H. 1977. A suggestion concerning the Cretaceous rise to dominance of the angiosperms. Evolution 31: 451-452.

    Raven, P. H. and D. I. Axelrod. 1974 (1981 republication). Angiosperm Biogeography and Past Continental Movements. Annals Missouri Botanical Garden 61: 539-673.

    Raven, P. H. and D. W. Kyhos. 1965. New evidence concerning the original base chromosome number of angiosperms. Evolution 19(2): 244-248.

    Ray, A., W. vd-G. van Naters, and J. R. Carlson. 2008. A regulatory code for neuron-specific odor receptor expression. PLoS Biology 6(5): e125.

    Read, J. and A. Stokes. 2006. Plant biomechanics in an ecological context. American Journal of Botany 93(10): 1546-1565.

    Rebeiz, M., J. E. Pool, V. A. Kassner, C. F. Aquadro, and S. B. Carroll. 2009. Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326(5960): 1663-1667.

    Reed, R. D., R. Papa, A. Martin, H. M. Hines, B. A. Counterman, C. Pardo-Diaz, C. D. Jiggins, N. L. Chamberlain, M. R. Kronforst, R. Chen, G. Halder, H. F. Nijhout, and W. O. McMillan. 2011. Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333(6046): 1137-1141.

    Rees, P. M. 2002. Land-plant diversity and the end-Permian mass extinction. Geology 30(9): 827-830.

    Rees, P. M., A. M. Ziegler, M. T. Gibbs, J. E. Kutzbach, P. J. Behling, and D. B. Rowley. 2002. Permian phytogeographic patterns and climate data/model comparisons. The Journal of Geology 110(1): 1-31.

    Regal, P. J. 1977. Ecology and evolution of flowering plant dominance. Science 196(4290): 622-629.

    Reichow, M. K., M. S. Pringle, A. J. Al'Mukhamedov, M. B. Allen, V. L. Andreichev, M. M. Buslov, C. E. Davies, G. S. Fedoseev, J. G. Fitton, S. Inger, A. Y. Medvedev, C. Mitchell, V. N. Puchkov, I. Y. Safonova, R. A. Scott, and A. D. Saunders. 2009. The timing and extent of the eruption of the Siberian Traps igneous province: implications for the end-Permian environmental crisis. Earth and Planetary Science Letters 277(1-2): 9-20.

    Reiser, L., P. Sánchez-Baracaldo, and S. Hake. 2000. Knots in the family tree: evolutionary relationships and functions of KNOX homeobox genes. Plant Molecular Biology 42(1): 151-166.

    Retallack, G. J. 2005. Permian Greenhouse Crises. Pp. 256-269 In: S. G. Lucas and K. E. Zeigler (eds.), The Nonmarine Permian, New Mexico Museum of Natural History and Science Bulletin No. 30. Albuquerque: University of New Mexico.

    Retallack, G. J. 2009. Greenhouse crises of the past 300 million years. GSA Bulletin 121(9-10): 1441-1455.

    Retallack, G. J. and D. L. Dilcher. 1981. A coastal hypothesis for the dispersal and rise to dominance of flowering plants. Pp. 27-77 In: K. J. Niklas (ed.) Paleobotany, Paleoecology, and Evolution. New York: Praeger.

    Retallack, G. J. and D. L. Dilcher. 1981. Arguments for a glossopterid ancestry of angiosperms. Paleobiology 7: 54-67.

    Retallack, G. J. and A. H. Jahren. 2008. Methane release from igneous intrusion of coal during late Permian extinction events. The Journal of Geology 116(1): 1-20.

    Retallack, G. J., A. H. Jahren, N. D. Sheldon, R. Chakrabarti, C. A. Metzger, and R. M. H. Smith. 2005. The Permian-Triassic boundary in Antarctica. Antarctic Science 17(2) 241-258.

    Retallack, G. J., C. A. Metzger, T. Greaver, A. H. Jahren, R. M. H. Smith, and N. D. Sheldon. 2006. Middle-Late Permian extinction on land. GSA Bulletin 118(11-12): 1398-1411.

    Retallack, G. J., R. M. H. Smith, and P. D. Ward. 2003. Vertebrate extinction across Permian-Triassic boundary in Karoo Basin, South Africa. GSA Bulletin 115(9): 1133-1152.

    Rice, D. W., A. J. Alverson, A. O. Richardson, G. J. Young, M. V. Sanchez-Puerta, J. Munzinger, K. Berry, J. L. Boore, Y. Zhang, C. W. dePamphilis, E. B. Knox, and J. D. Palmer. 2013. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342(6165): 1468-1473.

    Richardson, A. O. and J. D. Palmer. 2007. Horizontal gene transfer in plants. Journal of Experimental Botany 58(1): 1-9.

    Rijpkema, A. S., T. Gerats, and M. Vandenbussche. 2007. Evolutionary complexity of MADS complexes. Current Opinion in Plant Biology 10: 32-38.

    Rijpkema, A. S., M. Vandenbussche., R. Koes, K. Heijmans, and T. Gerats. 2010. Variations on a theme: changes in the floral ABCs in angiosperms. Seminars in Cell & Developmental Biology 21(1): 100-107.

    Rodda, P. and L. W. Kroenke. 1984. Fiji: A Fragment Arc. Pp. 87-107 In: Cenozoic Tectonic Development of the Southwest Pacific. United Nations ESCAP, CCOP/SOPAC Technical Bulletin No. 6, 126 pp.

    Rodríques-Trelles, F., R. Tarrío, and F. J. Ayala. 2003. Evolution of cis-regulatory regions versus codifying regions. International Journal of Developmental Biology 47: 665-673.

    Robertson, H. M. and K. W. Wanner. 2006. The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Research 16(11): 1395-1403.

    Rogers, B. T., M. D. Peterson, and T. C. Kaufman. 1997. Evolution of the insect body plan as revealed by the Sex combs reduced expression pattern. Development 124: 149-157.

    Ronshaugen, M., N. McGinnis, and W. McGinnis. 2002. Hox protein mutation and macroevolution of the insect body plan. Nature 415(6874): 914-917.

    Ronse De Craene, L. P. and E. F. Smets. 2001. Staminodes: their morphological and evolutionary significance. The Botanical Review 67(3): 351-402.

    Ronse De Craene, L. P., P. S. Soltis, and D. E. Soltis. 2003. Evolution of floral structures in basal angiosperms. International Journal of Plant Sciences 164(Supplement 5): S329-S363.

    Rosenberg, M. I., J. A. Lynch, and C. Desplan. 2009. Heads and tails: evolution of antero-posterior patterning in insects. Biochimica et Biophysica Acta (BBA), Gene Regulatory Mechanisms 1789(4): 333-342.

    Rosinski, J. A. and W. R. Atchley. 1998. Molecular evolution of the MYB family of transcription factors. Journal of Molecular Evolution 46: 74-83.

    Rosinski, J. A. and W. R. Atchley. 1999. Molecular evolution of helix-turn-helix proteins. Journal of Molecular Evolution 49: 301-309.

    Roth-Nebelsick, A., Dieter Uhl, V. Mosbrugger, and H. Kerp. 2001. Evolution and function of leaf venation architecture: a review. Annals of Botany 87: 553-566.

    Rothwell, G. W. 1987. The role of development in plant phylogeny: a paleobotanical perspective. Review of Palaeobotany and Palynology 50: 97-114.

    Rothwell, G. W., W. L. Crepet, and R. A. Stockey. 2009. Is the anthophyte hypothesis alive and well? New evidence from the reproductive structures of Bennettitales. American Journal of Botany 96(1): 296-322.

    Rothwell, G. W. and S. Lev-Yadun. 2005. Evidence of polar auxin flow in 375 million-year-old fossil wood. American Journal of Botany 92: 903-906.

    Rothwell, G. W., G. Mapes, and R. H. Mapes. 1996. Anatomically preserved Vojnovskyalean seed plants in Upper Pennsylvanian (Stephanian) marine shales of North America. Journal of Paleontology 70(6): 1067-1079.

    Rothwell, G. W., H. Sanders, S. E. Wyatt, and S. Lev-Yadun. 2008. A fossil record for growth regulation: the role of auxin in wood evolution. Annals of the Missouri Botanical Garden 95(1): 121-134.

    Rothwell, G. W. and R. A. Stockey. 2002. Anatomically preserved Cycadeoidea (Cycadeiodaceae), with a reevaluation of systematic characters for the seed cones of Bennettitales. American Journal of Botany 89: 1447-1458.

    Rothwell, G. W., S. E. Wyatt, and A. M. F. Tomescu. 2014. Plant evolution at the interface of paleontology and developmental biology: an organism-centered paradigm. American Journal of Botany 101(6): 899-913.

    Rowe, N. P. and T. Speck. 2005. Plant growth forms: an ecological and evolutionary perspective. New Phytologist 166: 61-72.

    Rudall, P. J. and R. M. Bateman. 2007. Developmental bases for key innovations in the seed-plant microgametophyte. Trends in Plant Science 12(7): 317-326.

    Rudall, P. J. and R. M. Bateman. 2010. Defining the limits of flowers: the challenge of distinguishing between the evolutionary products of simple versus compound strobili. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 397-409.

    Rudall, P. J., T. Eldridge, J. Tratt, M. M. Ramsey, R. E. Tuckett, Selena Y. Smith, M. E. Collinson, M. V. Remizowa, and D. D. Sokoloff. 2009. Seed fertilization, development, and germination in Hydatellaceae (Nymphaeales): implications for endosperm evolution in early angiosperms. American Journal of Botany 96(9): 1581-1593.

    Rudall, P. J., J. Hilton, and R. M. Bateman. 2013. Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants. New Phytologist 200(3): 598-614.

    Rudall, P. J., J. Hilton, F. Vergara-Silva, and R. M. Bateman. 2011. Recurrent abnormalities in conifer cones and the evolutionary origins of flower-like structures. Trends in Plant Science 16(3): 151-159.

    Rudall, P. J., M. V. Remizowa, A. S. Beer, E. Bradshaw, D. Wm. Stevenson, T. D. Macfarlane, R. E. Tuckett, S. R. Yadav, and D. D. Sokoloff. 2008. Comparative ovule and megagametophyte development in Hydatellaceae and water lilies reveal a mosaic of features among the earliest angiosperms. Annals of Botany 101(7): 941-956.

    Ruelens, P. and K. Geuten. 2013. When paleontology and molecular genetics meet: a genetic context for the evolution of conifer ovuliferous scales. New Phytologist 200(1): 10-12.

    Ruhl, M., N. R. Bonis, G.-J. Reichert, J. S. S. Damsté, and W. M. Kürschner. 2011. Atmospheric carbon injection linked to end-Triassic mass extinction. Science 333(6041): 430-434.

    Ruhl, M. and W. M. Kürschner. 2011. Multiple phases of carbon cycle disturbance from large igneous province formation at the Triassic-Jurassic transition. Geology 39(5): 431-434.

    Ruhl, M., W. M. Kürschner, and L. Krystyn. 2009. Triassic-Jurassic organic carbon isotope stratigraphy of key sections in the western Tethys realm (Austria). Earth and Planetary Science Letters 281(3-4): 169-187.

    Russell, S. D. 1991. Isolation and characterization of sperm cells in flowering plants. Annual Review of Plant Physiology and Plant Molecular Biology 42: 189-204.

    Russell, S. D. 2010. Chapter 14. Fertilization in angiosperms. Pp. 283-300 In: E. C. Pua and M. R. Davey (eds.), Gene Regulatory Models for Plant Development and Evolution, Biotechnological Perspectives Volume 1. Berlin: Springer, 497 pp.

    Rytkönen, K. T., T. A. Williams, G. M. Renshaw, C. R. Primmer, and M. Nikinmaa. 2011. Molecular evolution of the metazooan PHD-HIF oxygen-sensing system. Molecular Biology and Evolution 28(6): 1913-1926.

    Sablowski, R. 2010. Genes and functions controlled by floral organ identity genes. Seminars in Cell & Developmental Biology 21(1): 94-99.

    Sage, T. L., K. Hristova-Sarkovski, V. Koehl, J. Lyew, V. Pontieri, P. Bernhardt, P. Weston, S. Bagha, and G. Chiu. 2009. Transmitting tissue architecture in basal-relictual angiosperms: implications for transmitting tissue origins. American Journal of Botany 96(1): 183-206.

    Sahney, S. and M. J. Benton. 2008. Recovery from the most profound mass extinction of all time. Proceedings of the Royal Society of London, Series B, Biological Sciences 275(1636): 759-765.

    Sanchez, S., D. Germain, A. De Ricqlès, A. Abourachid, F. Goussard, and P. Tafforeau. 2010. Limb-bone histology of temnospondyls: implications for understanding the diversification of paleoecologies and patterns of locomotion of Permo-triassic tetrapods. Journal of Evolutionary Biology 23(10): 2076-2090.

    Sandaklie-Nikolova, L., R. Palanivelu, E. J. King, G. P. Copenhaver, and G. N. Drews. 2007. Synergid cell death in Arabidopsis is triggered following direct interaction with the pollen tube. Plant Physiology 144: 1753-1762.

    Sander, P. M., C. T. Gee, J. Hummel, and M. Clauss. 2010. Mesozoic plants and dinosaur herbivory. Pp. 331-359 In: C. T. Gee (ed.), Plants in Mesozoic Time, Morphological Innovations, Phylogeny, Ecosystems. Bloomington: Indiana University Press, 373 pp.

    Sanders, H., G. W. Rothwell, and S. Wyatt. 2007. Paleontological context for the developmental mechanisms of evolution. International Journal of Plant Sciences 168(5): 719-728.

    Sayou, C., M. Monniaux, M. H. Nanao, E. Moyroud, S. F. Brockington, E. Thévenon, H. Chahtane, N. Warthmann, M. Melkonian, Y. Zhang, G. K.-S. Wong, D. Weigel, F. Parcy, and R. Dumas. 2014. A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 343(6171): 645-648.

    Schaack, S., C. Gilbert, and C. Feschotte. 2010. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends in Ecology and Evolution 25(9): 537-546.

    Schaller, M. F., J. D. Wright, and D. V. Kent. 2011. Atmospheric CO2 perturbations associated with the Central Atlantic Magmatic Province. Science 331(6023): 1404-1409.

    Schittko, D. Hermsmeier, and I. T. Baldwin. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of plant mRNAs in response to insect-derived cues. Plant Physiology 125: 701-710.

    Schoene, B., J. Guex, A. Bartolini, U. Schaltegger, and T. J. Blackburn. 2010. Correlating the end-Triassic mass extinction and flood basalt volcanism at the 100 ka level. Geology 38(5): 387-390.

    Schulman, A. H. and T. Wicker. 2013. Chapter 2. A field guide to transposable elements. Pp. 15-40 In: N. V. Fedoroff (ed.), Plant Transposons and Genome Dynamics in Evolution. Oxford: Wiley-Blackwell, 232 pp.

    Schulte, P., L. Alegret, I. Arenillas, J. A. Arz, P. J. Barton, P. R. Bown, T. J. Bralower, G. L. Christeson, P. Claeys, C. S. Cockell, G. S. Collins, A. Deutsch, T. J. Goldin, K. Goto, J. M. Grajales-Nishimura, R. A. F. Grieve, S. P. S. Gulick, K. R. Johnson, W. Kiessling, C. Koeberl, D. A. Kring, K. G. MacLeod, T. Matsui, J. Melosh, A. Montanari, J. V. Morgan, C. R. Neal, D. J. Nichols, R. D. Norris, E. Pierazzo, G. Ravizza, M. Rebolledo-Vieyra, W. U. Reimold, E. Robin, T. Salge, R. P. Speijer, A. R. Sweet, J. Urrutia-Fucugauchi, V. Vajda, M. T. Whalen, and P. S. Willumsen. 2010. The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary. Science 327(5970): 1214-1218.

    Schultz, J. C. 2002. Shared signals and the potential for phylogenetic espionage between plants and animals. Integrative and Comparative Biology: 42: 454-462.

    Schwendenmann, A. B., A.-L. Decombeix, T. N. Taylor, E. L. Taylor, and M. Krings. 2011. Morphological and functional stasis in mycorrhizal root nodules as exhibited by a Triassic conifer. Proceedings of the National Academy of Sciences 108(33): 13630-13634.

    Scott, A. C., J. M. Anderson, and H. M. Anderson. 2004. Evidence of plant-insect interactions in the Upper Triassic Molteno Formation of South Africa. Journal of the Geological Society 161: 401-410.

    Scott, A. C. and I. J. Glasspool. 2006. The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration. Proceedings of the National Academy of Sciences 103(29): 10861-10865.

    Scott, R. J., S. J. Armstrong, J. Doughty, and M. Spielman. 2008. Double fertilization in Arabidopsis thaliana involves a polyspermy block on the egg but not the central cell. Molecular Plant 1(4): 611-619.

    Scutt, C. P., M. Vinauger-Douard, C. Fourquin, C. Finet, and C. Dumas. 2006. An evolutionary perspective on the regulation of carpel development. Journal of Experimental Botany 57(10): 2143-2152.

    Seago, J. L., Jr. and D. D. Fernando. 2013. Anatomical aspects of angiosperm root evolution. Annals of Botany 112(2): 223-238.

    Selosse, M.-A. 2016. Letters to the twenty-first century botanist: "What is a flower?" (3) The flower as an evolutionary arms race: was Linnaeus's choice misleading. Botany Letters 163(3): 231–235.

    Sepúlveda, J., J. E. Wendler, R. E. Summons, and K.-U. Hinrichs. 2009. Rapid resurgence of marine productivity after the Cretaceous-Paleogene mass extinction. Science 326(5949): 129-132.

    Sessions, A., M. F. Yanofsky, and D. Weigel. 2000. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289(5480): 779-781.

    Seymour, R. S. and P. G. D. Mathews. 2006. The role of thermogenesis in the pollination biology of the Amazon waterlily, Victoria amazonica. Annals of Botany 98: 1129-1135.

    Shalit, A., A. Rozman, A. Goldshmidt, J. P. Alvarez, J. L. Bowman, Y. Eshed, and E. Lifschitz. 2009. The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proceedings of the National Academy of Sciences 106(20): 8392-8397.

    Sharma, B., C. Guo, H. Kong, and E. M. Kramer. 2011. Petal-specific subfunctionalization of an APETALA3 paralog in the Ranunculales and its implications for petal evolution. New Phytologist 191(3): 870-883.

    Shan, H., N. Zhang, C. Liu, G. Xu, J. Zhang, Z. Chen, and H. Kong. 2007. Patterns of gene duplication and functional diversification during the evolution of the AP1/SQUA subfamily of plant MADS-box genes. Molecular Phylogenetics and Evolution 44(1): 26-41.

    Shindo, S., K. Sakakibara, R. Sano, K. Ueda, and M. Hasebe. 2001. Characterization of FLORICAULA/LEAFY homologue of Gnetum parvifolium and its implications for the evolution of reproductive organs in seed plants. International Journal of Plant Sciences 162(6): 1199-1209.

    Shingleton, A. W., C. K. Mirth, and P. W. Bates. 2008. Developmental model of static allometry in holometabolous insects. Proceedings of the Royal Society of London, Series B, Biological Sciences 275(1645): 1875-1885.

    Shiokawa, T., S. Yamada, N. Futamura, K. Osanai, D. Murasugi, K. Shinohara, S. Kawai, N. Morohoshi, Y. Katayama, and S. Kajita. 2008. Isolation and functional analysis of the CjNdly gene, a homolog in Cryptomeria japonica of FLORICAULA/LEAFY genes. Tree Physiology 28: 21-28.

    Simmons, M. P. and J. Gatesy. 2015. Coalescence vs. concatenation: sophisticated analyses vs. first principles applied to rooting of the angiosperms. Molecular Phylogenetics and Evolution 91: 98-122.

    Sinha, N. 1999. Leaf development in angiosperms. Annual Review of Plant Physiology and Plant Molecular Biology 50: 419-446.

    Skinner, D. J. and C. S. Gasser. 2009. Expression-based discovery of candidate ovule development regulators through transcriptional profiling of ovule mutants. BMC Plant Biology 9: 29.

    Skinner, D. J., T. A. Hill, and C. S. Gasser. 2004. Regulation of ovule development. The Plant Cell (Supplement) 16: S32-S-45.

    Smith, A. C. 1979. Introduction Pp. 1-88 In: A. C. Smith, Flora Vitiensis Nova, Volume 1. Lawai: Pacific Tropical Botanical Garden, 495 pp.

    Smith, A. C. 1981. Degeneriaceae Pp. 7-13 In: A. C. Smith, Flora Vitiensis Nova, Volume 2. Lawai: Pacific Tropical Botanical Garden, 810 pp.

    Smith, A. C. 1991. Degeneriaceae Pp. 587-588 In: A. C. Smith, Flora Vitiensis Nova, Volume 5. Lawai: National Tropical Botanical Garden, 626 pp.

    Smith, A. C. 1996. Comprehensive Indices, Flora Vitiensis Nova, Volume 6. Lawai: National Tropical Botanical Garden.

    Smith, R. S. 2008. The role of auxin transport in plant patterning mechanisms. PLoS Biology 6(12): 2631-2633.

    Smith, R. S., S. Guyomarc'h, T. Mandel, D. Reinhardt, C. Kuhlemeier, and P. Prusinkiewicz. 2006. A plausible model of phyllotaxis. Proceedings of the National Academy of Sciences 103(5): 1301-1306.

    Smith, Stephen A., J. M. Beaulieu, and M. J. Donoghue. 2010. An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proceedings of the National Academy of Sciences 107(13): 5897-5902.

    Smith, S. D., C. Ané, and D. A. Baum. 2008. The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae). Evolution 62(4): 793-806.

    Smoot, E. L. and T. N. Taylor. 1984. The fine structure of fossil plant cell walls. Science 225: 621-623.

    Sobolev, S. V., A. V. Sobolev, D. V. Kuzmin, N. A. Krivolutskaya, A. G. Petrunin, N. T. Arndt, V. A. Radko, and Y. R. Vasiliev. 2011. Linking mantle plumes, large igneous provinces and environmental catastrophes. Nature 477(7364): 312-316.

    Sokolov, D. D. and A. K. Timonin. 2007. Morphological and molecular data on the origin of angiosperms: on a way to a synthesis. Zhurnal Obschei Biologii 68(2): 83-97.

    Soltis, D. E., V. A. Albert, J. Leebens-Mack, C. D. Bell, A. H. Paterson, C. Zheng, D. Sankoff, C. W. dePamphilis, P. K. Wall, and P. S. Soltis. 2009. Polyploidy and angiosperm diversification. American Journal of Botany 96(1): 336-348.

    Soltis, D. E., C. D. Bell, S. Kim, and P. S. Soltis. 2008. Origin and early evolution of angiosperms. Pp. 3-25 In: C. D. Schlichting and T. A. Mousseau (eds.), Annals of the New York Academy of Sciences, Volume 1133 Issue, The Year in Evolutionary Biology 2008. New York: The New York Academy of Sciences, 203 pp.

    Soltis, D. E., M. A. Gitzendanner, and P. S. Soltis. 2007. A 567 - taxon data set for angiosperms: the challenges posed by Bayesian analyses of large data sets. International Journal of Plant Sciences 168(2): 137-157.

    Soltis, D. E., J. H. Leebens-Mack, and P. S. Soltis (eds.). 2006. Advances in Botanical Research, Volume 44, Developmental Genetics of the Angiosperm Flower. Amsterdam: Elsevier.

    Soltis, D. E., H. Ma, M. W. Frohlich, P. S. Soltis, V. A. Albert, D. G. Oppenheimer, N. S. Altman, C. dePamphilis, and J. Leebens-Mack. 2007. The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression. Trends in Plant Science 12(8): 358-367.

    Soltis, D. E., P. S. Soltis, P. K. Endress, and M. W. Chase. 2005. Phylogeny and Evolution of Angiosperms. Sunderland: Sinauer, 370 pp.

    Soltis, P. S., S. F. Brockington, M.-J. Yoo, A. Piedrahita, M. Latvis, M. J. Moore, A. S. Chanderbali, and D. E. Soltis. 2009. Floral variation and floral genetics in basal angiosperms. American Journal of Botany 96(1): 110-128.

    Soltis, P. S. and D. E. Soltis. 2004. The origin and diversification of angiosperms. American Journal of Botany 91(10): 1614-1626.

    Soltis, P. S. and D. E. Soltis. 2014. Chapter 4. Flower diversity and angiosperm diversification. Pp. 85-102 In: J. L. Riechmann and F. Wellmer [eds.], Flower Development: Methods and Protocols, Volume 1110. New York: Springer, 475 pp).

    Soltis, P. S. and D. E. Soltis. 2016. Ancient WGD events as drivers of key innovations in angiosperms. Current Opinion in Plant Biology 30: 159-165.

    Soltis, P. S., D. E. Soltis, S. Kim, A. Chanderball, and M. Buzgo. 2006. Expression of floral regulators in basal angiosperms and the origin and evolution of ABC-function. Pp. 483-506 In: D. E. Soltis, J. H. Leebens-Mack, P. S. Soltis (eds.), Vol. 44, Advances in Botanical Research, Developmental Genetics of the Angiosperm Flower. Amsterdam: Elsevier.

    Song, H., J. Tong, Z. Q. Chen, H. Yang, and Y. Wang. 2009. End-Permian mass extinction of foraminifers in the Nanpanjiang Basin, South China. Journal of Paleontology 83(5): 718-738.

    Specht, C. D. and M. E. Bartlett. 2009. Flower evolution: the origin and subsequent diversification of the angiosperm flower. Annual Review of Ecology, Evolution, and Systematics 40: 217-243.

    Specht, C. D. and D. G. Howarth. 2015. Adaptation in flower form: a comparative evodevo approach. New Phytologist 206: 74-80.

    Spicer, Rachel and A. Groover. 2010. Evolution of development of vascular cambia and secondary growth. New Phytologist 186(3): 577-592.

    Staedler, Y. M., P. H. Weston, and P. K. Endress. 2007. Floral phyllotaxis and floral architecture in Calycanthaceae (Laurales). International Journal of Plant Sciences 168(3): 285-306.

    Stauber, M., A. Prell, and U. Schmidt-Ott. 2002. A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proceedings of the National Academy of Sciences 99(1): 274-279.

    Stebbins, G. L. 1958. On the hybrid origin of angiosperms. Evolution (Lancaster) 12(2): 267-270.

    Stebbins, G. L. 1974. Flowering Plants: Evolution above the Species Level. Cambridge: Belknap Press of Harvard University Press, 399 pp.

    Stebbins, G. L. 1984. Polyploidy and distribution of the arctic-alpine flora: new evidence and a new approach. Botanica Helvetica 94: 1-13.

    Stein, W. E. and J. S. Boyer. 2006. Evolution of land plant architecture: beyond the telomb theory. Paleobiology 32(3): 450-482.

    Steinthorsdottir, M., A. J. Jeram, and J. C. McElwain. 2011. Extremely elevated CO2 concentrations at the Triassic/Jurassic boundary. Palaeogeography, Palaeoclimatology, Palaeoecology 308(3-4): 418-432.

    Stepanova, A. N., J. Robertson-Hoyt, J. Yun, L. M. Benavente, D.-Y. Xie, K. Dolezal, A. Schereth, G. Jürgens, and J. M. Alonso. 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177-191.

    Stern, D. L. and D. J. Emlen. 1999. The developmental basis for allometry in insects. Development 126(6): 1091-1101.

    Stevens, L. G., J. Hilton, D. P. G. Bond, I. J. Glasspool, and P. E. Jardine. 2011. Radiation and extinction patterns in Permian floras from North China as indicators for environmental and climate change. Journal of the Geological Society 168(2): 607-619.

    Stewart, W. N. and G. W. Rothwell. 1993. Paleobotany and the Evolution of Plants (second edition). Cambridge: Cambridge University Press, 521 pp.

    Stockey, R. A. and G. W. Rothwell. 2003. Anatomically preserved Williamsonia (Williamsoniaceae): evidence for Bennettitalean reproduction in the Late Cretaceous of western North America. International Journal of Plant Sciences 164(2): 251-262.

    Stockey, R. A., Sean W. Graham, and P. R. Crane. 2009. Introduction to the Darwin Special Issue. American Journal of Botany 96(1): 3-4.

    Stone, G. N., R. W. J. M. van der Ham, and J. G. Brewer. 2008. Fossil oak galls preserve ancient multitrophic interactions. Proceedings of the Royal Society of London, Series B, Biological Sciences 275(1648): 2213-2219.

    Strausfeld, N. J. 2009. Brain organization and the origin of insects: an assessment. Proceedings of the Royal Society of London, Series B, Biological Sciences 276(1664): 1929-1937.

    Strausfeld, N. J., L. Hansen, Y. Li, R. S. Gomez, and K. Ito. 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learning and Memory 5(1): 11-37.

    Stuessy, T. F. 2004. A transitional-combinational theory for the origin of angiosperms. Taxon 53(1): 3-16.

    Stuessy, T. F. 2010. Paraphyly and the origin and classification of angiosperms. Taxon 59(3): 689-693.

    Stuurman, J., F. Jaggi, and C. Kuhlemeier. 2002. Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes and Development 16: 2213-2218.

    Su, K., S. Zhao, H. Shan, H. Kong, W. Lu, G. Theißen, Z. Chen, and Z. Meng. 2008. The MIK region rather than the C-terminal domain of AP3-like class B floral homeotic proteins determines functional specificity in the development and evolution of petals. New Phytologist 178(3): 544-558.

    Suchan, T and N. Alvarez. 2015. Fifty years after Ehrlich and Raven, is their support for plant-insect coevolution as a major driver of species diversification? Entomologica et Experimentalis Applicata 157: 98-112.

    Sun, G., S. Zheng, D. L. Dilcher, Y. Wang, and S. Mei. 2001. Early Angiosperms and Their Associated Plants from Western Liaoning, China. Shanghai: Scientific and Technological Education Publishing House, 227 pp.

    Suzuki, M., T. Xiang, K. Ohyama, H. Seki, K. Saito, T. Muranaka, H. Hayashi, Y. Katsube, T. Kushiro, M. Shibuya, and Y. Ebizuka. 2006. Lanosterol synthase in dicotyledonous plants. Plant and Cell Physiology 47(5): 565-571.

    Svensen, H., S. Planke, A. G. Polozov, N. Schmidbauer, F. Corfu, Y. Y. Podladchikov, and B. Jamveit. 2009. Siberian gas venting and the end-Permian environmental crisis. Earth and Planetary Science Letters 277(3-4): 490-500.

    Takhtajan, A. 1969. Flowering Plants: Origin and Dispersal (translated by C. Jeffrey). Edinburgh: Oliver and Boyd, 310 pp.

    Takhtajan, A. 1976. Neoteny and the origin of flowering plants. Pp. 207-219 In: C. B. Beck (ed.), Origin and Early Evolution of Angiosperms. New York: Columbia University Press, 341 pp.

    Takhtajan, A. 1991. Evolutionary Trends in Flowering Plants. New York: Columbia University Press. 240 pp.

    Tang, W., L. Sternberg, and D. Price. 1987. Metabolic aspects of thermogenesis in male cones of five cycad species. American Journal of Botany 74(10): 1555-1559.

    Tavares, R., M. Cagnon, I. Negrutiu, and D. Mouchiroud. 2010. Testing the recent theories for the origin of the hermaphrodite flower by comparison of the transcriptomes of gymnosperms and angiosperms. BMC Evolutionary Biology 10: 240.

    Taylor, D. W. 2010. Implications of fossil floral data on understanding the early evolution of molecular developmental controls of flowers. Pp. 119-169 In: C. T. Gee (ed.), Plants in Mesozoic Time, Morphological Innovations, Phylogeny, Ecosystems. Bloomington: Indiana University Press, 373 pp.

    Taylor, D. W., D. L. Dilcher, and S. Hu. 2010. Coevolution of early angiosperms and their pollinators: evidence from pollen. Palaeontographica Abt. B 283: 103-135.

    Taylor, D. W. and L. J. Hickey. 1992. Phylogenetic evidence for the herbaceous origin of angiosperms. Plant Systematics and Evolution 180: 137-156.

    Taylor, D. W. and L. J. Hickey (eds). 1996. Flowering Plant Origin, Evolution, and Phylogeny. London: Chapman and Hall, 403 pp.

    Taylor, D. W. and L. J. Hickey. 1996. Chapter 9. Evidence for and implications of an herbaceous origin for angiosperms. Pp. 232-266 In: D. W. Taylor and L. J. Hickey (eds.), Flowering Plant Origin, Evolution, and Phylogeny. London: Chapman and Hall, 403 pp.

    Taylor, D. W. and G. Kirchner. 1996. Chapter 6. The origin and evolution of the angiosperm carpel. Pp. 116-140 In: D. W. Taylor and L. J. Hickey (eds.), Flowering Plant Origin, Evolution, and Phylogeny. London: Chapman and Hall, 403 pp.

    Taylor, D. W., H. Li, J. Dahl, F. J. Fago, D. Zinniker, and J. M. Moldowan. 2006. Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils. Paleobiology 32(2): 179-190.

    Taylor, E. L. and T. N. Taylor. 2009. Seed ferns from the late Paleozoic and Mesozoic: any angiosperm ancestors lurking there? American Journal of Botany 96(1): in press.

    Taylor, E. L., T. N. Taylor, H. Kerp, and E. J. Hermsen. 2006. Mesozoic seed ferns: old paradigms, new discoveries. Journal of the Torrey Botanical Society 133(1): 62-82.

    Taylor, T. N., J. M. Osborn, and E. L. Taylor. 1996. In situ pollen and spores in plant evolution 14C - The importance of in situ pollen and spores in understanding the biology and evolution of fossil plants. Pp. 427-441 In: J. Jansonius and D. C. McGregor (eds.), Volume 1, Palynology: Principles and Applications, American Association of Stratigraphic Palynologists Foundation.

    Taylor, T. N., E. L. Taylor, and M. Krings. 2009. Paleobotany: The Biology and Evolution of Fossil Plants, Second Edition. Burlington: Elsevier Academic Press, 1230 pp.

    Tekleva, M. V. and V. A. Krassilov. 2009. Comparative pollen morphology and ultrastructure of modern and fossil gnetophytes. Review of Palaeobotany and Palynology 156(1-2): 130-138.

    Telewski, F. W. 2006. A unified hypothesis of mechanoperception in plants. American Journal of Botany 93(10): 1466-1476.

    Terry, I., C. J. Moore, G. H. Walter, P. I. Forster, R. B. Roemer, J. D. Donaldson, and P. J. Machin. 2004. Association of cone thermogenesis and volatiles with pollinator specificity in Macrozamia cycads. Plant Systematics and Evolution 243(3-4): 233-247.

    Terry, I., G. H. Walter, C. Moore, R. Roemer, and C. Hull. 2007. Odor-mediated push-pull pollination in cycads. Science 318(5847): 70.

    Theißen, G. 2001. Development of floral organ identity: stories from the MADS house. Current Opinion in Plant Biology 4: 75-85.

    Theißen, G. and A. Becker. 2004. Gymnosperm orthologues of class B floral homeotic genes and their impact on understanding flower origin. Critical Reviews in Plant Sciences 23(2): 129-148.

    Theißen, G., A. Becker, A. Di Rosa, A. Kanno, J. T. Kim, T. Münster, K.-U. Winter, and H. Saedler. 2000. A short history of MADS-box genes in plants. Plant Molecular Biology 42: 115-149.

    Theißen, G. and K. Kaufmann. 2006. 6. Molecular developmental genetics and the evolution of flowers. Pp. 124-149 In: B. R. Jordan (ed.), The Molecular Biology and Biotechnology of Flowering, Second Edition. Wallingford: CABI Publishing, 404 pp.

    Theißen, G., J. T. Kim, and H. Saedler. 1996. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. Journal of Molecular Evolution 43: 484-516.

    Theißen, G. and R. Melzer. 2007. Molecular mechanisms underlying origin and diversification of the angiosperm flower. Annals of Botany 100(3): 1-17.

    Theißen, G. and H. Saedler 2001. Floral quartets. Nature 409: 469-471.

    Thien, L. B., P. Bernhardt, M. S. Devall, Z. Chen, Y. Luo, J.-H. Fan, L.-C. Yuan, and J. H. Williams. 2009. Pollination biology of basal angiosperms (ANITA grade). American Journal of Botany 96(1): 166-182.

    Thien, L. H., P. Bernhardt, G. W. Gibbs, O. Pellmyr, G. Bergstrom, I. Groth, and G. McPherson. 1985. The pollination of Zygogynum (Winteraceae) by a moth, Sabatinca (Micropterigidae): an ancient association? Science 227: 540-543.

    Thomas, H. H. 1925. The Caytoniales, a new group of angiospermous plants from the Jurassic rocks of Yorkshire. Philosophical Transactions 213: 299-363.

    Thomas, S. G., N. J. Tabor, W. Yang, T. S. Myers, Y. Yang, and D. Wang. 2011. Palaeosol stratigraphy across the Permian-Triassic boundary, Bogda Mountains, NW China: implications for palaeoenvironmental transition through Earth's largest mass extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 308(1-2): 41-64.

    Thomson, J. D. and P. Wilson. 2008. Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. International Journal of Plant Sciences 169(1): 23-38.

    Thompson, J. N. 1989. Concepts of coevolution. Trends in Ecology and Evolution 4: 179-193.

    Thompson, J. N. 2005. The Geographic Mosaic of Coevolution. Chicago: University of Chicago Press, 443 pp.

    Thorne, R. F. 1968. Synopsis of a putatively phylogenetic classification of the flowering plants. Aliso 6:57-66.

    Thorne, R. F. 1986. Antarctic elements in Australasian rainforests. Telopea 2(6): 611-617.

    Thorne, R. F. 1992. Classification and geography of the flowering plants. The Botanical Review 58(3): 225-348.

    Thummel, C. S. and J. Chory. 2002. Steroid signaling in plants and insects - common themes, different pathways. Genes and Development 16(24): 3113-3129.

    Tiffney, B. H. 1992. The role of vertebrate herbivory in the evolution of land plants. The Palaeobotanist 41: 87-97.

    Tiffney, B. H. 2004. Vertebrate dispersal of seed plants through time. Annual Review of Ecology, Evolution, and Systematics 35: 1-29.

    Tobe, H., T. Jaffré, and P. H. Raven. 2000. Embryology of Amborella (Amborellaceae): descriptions and polarity of character states. Journal of Plant Research 113(3): 271-280.

    Tobe, H., Y. Kimoto, and N. Prakash. 2007. Development and structure of the female gametophyte in Austrobaileya scandens (Austrobaileyaceae). Journal of Plant Research 120(3): 431-436.

    Tomescu, A. M. F. 2016. Development: paleobotany at the high-table of evo-devo. Current Biology 26: R505-R508.

    Tomlinson, P. B. 2012. Rescuing Robert Brown - the origins of angio-ovuly in the seed cones of conifers. The Botanical Review 78: 310-334.

    Tong, K. Jun, S. Duchêne, S. Y. W. Ho, and N. Lo. 2015. Comment on "Phylogenomics resolves the timing and pattern of insect evolution." Science 349(6247): Research Technical Comment Number 487, Insect Phylogenomics.

    Trivett, M. L. and K. B. Pigg. 1996. A survey of reticulate venation among fossil and living plants. Pp. 8-31 In: D. W. Taylor and L. J. Hickey (eds.), Flowering Plant Origin, Evolution, and Phylogeny. New York: Chapman and Hall, 403 pp.

    Truman, J. W. and L. M. Riddiford. 2002. 34. Insect Developmental Hormones and Their Mechanism of Action. Pp. 841-873 In: D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, and R. T. Rubin (eds.), Hormones, Brain, and Behavior, Volume 2. Boston: Academic Press, 873 pp.

    Tsitrone, A., M. Kirkpatrick, and D. A. Levin. 2003. A model for chloroplast capture. Evolution 57(8): 1776-1782.

    Tu, Z. 2005. 4.12. Insect transposable elements. Pp. 395-436 In: L. I. Gilbert, K. Iatrou, and S. S. Gill (eds.), Comprehensive Molecular Insect Science, Volume 4, Biochemistry and Molecular Biology. Amsterdam: Elsevier, 3200 pp.

    Tucker, S. 2003. Floral development in legumes. Plant Physiology 131: 911-926.

    Uhl, N. W. and J. Dransfield. 1987. The Ecology of Palms. Pp. 45-56 in: Genera Palmarum, A Classification of Palms Based upon the Work of Harold E. Moore, Jr. Lawrence: Allen Press, 610 pp.

    Van de Peer, Y., S. Maere, and A. Meyer. 2009. The evolutionary significance of ancient genome duplications. Nature Reviews Genetics 10: 725-732.

    Van De Schootbrugge, B. and P. B. Wignall. 2016. A tale of two extinctions: converging end-Permian and end-Triassic scenarios. Geological Magazine 153(2): 332-354.

    Van Holde, K. E., K. I. Miller, and H. Decker. 2001. Hemocyanins and invertebrate evolution. Journal of Biological Chemistry 276: 15563-15566.

    Vasco, A., T. L. Smalls, Sean W. Graham, E. D. Cooper, G. K-S. Wong, D. Wm. Stevenson, R. C. Moran, and B. A. Ambrose. 2016. Challenging the paradigms of leaf evolution: Class III HD-Zips in ferns and lycophytes. New Phytologist DOI: 10-1111/nph 14075.

    Vassilenko, D. V. 2011. The first record of endophytic insect oviposition from the Tartarian of European Russia. Paleontologicheskii Zhurnal 45(3): 333-334.

    Vásquez-Lobo, A., A. Carlsbecker, F. Vergara-Silva, E. R. Alvarez-Buylla, D. Piñero, and P. Engström. 2007. Characterization of the expression patterns of LEAFY/FLORICAULA and NEEDLY orthologs in female and male cones of the conifer genera Picea, Podocarpus, and Taxus: implications for current evo-devo hypotheses for gymnosperms. Evolution and Development 9(5): 446-459.

    Venner, S., C. Feshotte, and C. Biémont. 2009. Dynamics of transposable elements: towards a community ecology of the genome. Trends in Genetics 25(7): 317-323.

    Veron, A. S., K. Kaufmann, and E. Bornberg-Bauer. 2007. Evidence of interaction network evolution by whole-genome duplications: a case study in MADS-Box proteins. Molecular Biology and Evolution 24(3): 670-678.

    Vialette-Guiraud, A. C. M. and C. P. Scutt. 2009. Chapter 1. Carpel evolution. Pp. 1-34 In: L. Østergaard (ed.), Fruit Development and Seed Dispersal, Annual Plant Reviews Volume 38. Oxford: Wiley-Blackwell, 368 pp.

    Walker-Larsen, J. and L. D. Harder. 2000. The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention. American Journal of Botany 87(10): 1367-1384.

    Wang, W., B. J. Kidd, S. B. Carroll, and J. H. Yoder. 2011. Sexually dimorphic regulation of the Wingless morphogen controls sex-specific segment number in Drosophila. Proceedings of the National Academy of Sciences 108(27): 11139-11144.

    Wang, X. 2009. New fossils and new hope for the origin of angiosperms. Pp. 51-70 In: P. Pontarotti (ed.), Evolutionary biology: Concept, Modeling, and Application. London: Springer Verlag, 398 pp.

    Wang, X. 2010. Axial nature of the cupule-bearing organ in Caytoniales. Journal of Systematics and Evolution 48(3): 207-214.

    Wang, Y., Z. Liu, X. Wang, C. Shih, Y. Zhao, M. S. Engel, and D. Ren. 2010. Ancient pinnate leaf mimesis among lacewings. Proceedings of the National Academy of Sciences 107(37): 16212-16215.

    Wang, Y.-Q., R. Melzer and G. Theißen. 2010. Molecular interactions of orthologues of floral homeotic proteins from the gymnosperm Gnetum gnemon provide a clue to the evolutionary origin of 'floral quartets.' The Plant Journal 64(2): 177-190.

    Wang, Z.-Q. 2000. Vegetation declination on the eve of the P-T event in north China and plant survival strategies: an example of Upper Permian refugium in northwestern Shanxi, China. Acta Palaeontologica Sinica 39(Supplement): 127-153.

    Wang, Z.-Q. and Z. Zhang. 1998. Gymnosperms on the eve of the terminal Permian mass extinction in north China and their survival strategies. Chinese Science Bulletin 43(11): 889-897.

    Ward, P., C. C. Labandeira, M. Laurin, and R. A. Berner. 2006. Confirmation of Romer's Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization. Proceedings of the National Academy of Sciences 103(45): 16818-16822.

    Warner, K. A., P. J. Rudall, and M. W. Frohlich. 2009. Environmental control of sepalness and petalness in perianth organs of waterlilies: a new Mosaic Theory for the evolutionary origin of a differentiated perianth. Journal of Experimental Botany 60(12): 3559-3574.

    Wasteneys, G. O. 2004. Progress in understanding the role of microtubules in plant cells. Current Opinion in Plant Biology 7(6): 651-660.

    Wasternack, C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100: 681-697.

    Watanabe, T., H. Takeuchi, and T. Tubo. 2010. Structural diversity and evolution of the N-terminal isoform-specific region of ecdysone receptor-A and -B1 isoforms in insects. BMC Evolutionary Biology 10: 40.

    Wedmann, S. 2010. A brief review of the fossil history of plant masquerade by insects. Palaeontographica Abt. B 283(4-6): 175-182.

    Weishampel, D. B. and C.-M. Jianu. 2000. Chapter 5, Plant-eaters and ghost lineages: dinosaurian herbivory revisited. Pp. 123-143 In: H.-D. Sues (ed.), Evolution of Herbivory in Terrestrial Vertebrates: Perspectives from the Fossil Record. Cambridge: Cambridge University Press, 256 pp.

    Weiss, D. and N. Ori. 2007. Mechanisms of cross talk between gibberellin and other hormones. Plant Physiology 144: 1240-1246.

    Wendel, J. F. 2015. The wondrous cycles of polyploidy in plants. American Journal of Botany 102(11): 1753-1756.

    Wengler, D. L. and D. C. Bergmann. 2012. On fate and flexibility in stomatal development. Cold Spring Harbor Symposia on Quantitative Biology 77: 53-62.

    West-Eberhard, M. J. 2005. Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences 102(Supplement 1): 6543-6549.

    Wheat, C. W., H. Vogel, U. Wittstock, M. F. Braby, D. Underwood, and T. Mitchell-Olds. 2007. The genetic basis of a plant-insect coevolutionary key innovation. Proceedings of the National Academy of Sciences 104(51): 20427-20431.

    Wheeler, E. H. and T. M. Lehman. 2000. Late Cretaceous woody dicots from the Aguja and Javelina formations, Big Bend National Park, Texas, USA. IAWA Journal 21(1): 83-120.

    Whipple, C. J., M. J. Zanis, E. A. Kellogg, and R. J. Schmidt. 2007. Conservation of B class gene expression in the second whorl of a basal grass and outgroups links the origin of lodicules and petals. Proceedings of the National Academy of Sciences 104(3): 1081-1086.

    White, M. E. 1986. The Greening of Gondwana: the 400 Million Year Story of Australia's Plants. Frenchs Forest: Reed Books Party Limited, 256 pp.

    Whiteside, J. H., P. E. Olsen, T. Eglinton, M. E. Brookfield, and R. N. Sambrotto. 2010. Compound-specific carbon isotopes from Earth's largest flood basalt eruptions directly linked to the end-Triassic mass extinction. Proceedings of the National Academy of Sciences 107(15): 6721-6725.

    Whitney, H. M. and B. J. Glover. 2007. Morphology and development of floral features recognized by pollinators. Arthropod-Plant Interactions 1: 147-158.

    Wignall, P. B. 2015. The Worst of Times: How Life on Earth Survived 80 Million Years of Extinctions. Princeton: Princeton University Press, 199 pp.

    Wignall, P. B., Y. Sun, D. P. G. Bond, G. Izon, R. J. Newton, S. Védrine, M. Widdowson, J. R. Ali, X. Lai, H. Jiang, H. Cope, and S. H. Bottrell. 2009. Volcanism, mass extinction, and carbon isotope fluctuations in the Middle Permian of China. Science 324(5931): 1179-1182.

    Wignall, P. B., S. Védrine, D. P. G. Bond, W. Wang, X.-L. Lai, J. R. Ali, and H.-S. Jiang. 2009. Facies analysis and sea-level change at the Guadalupian-Lopingian global stratotype (Laibin, South China), and its bearing on the end-Guadalupian mass extinction. Journal of the Geological Society 166(4): 655-666.

    Wilf, P., C. C. Labandeira, W. J. Kress, C. L. Staines, D. M. Windsor, A. L. Allen, and K. R. Johnson. 2000. Timing the radiations of leaf beetles: hispines on gingers from latest Cretaceous to Recent. Science 289: 291-294.

    Williams, J. H. 2008. Novelties of the flowering plant pollen tube underlie diversification of a key life history stage. Proceedings of the National Academy of Sciences 105(32): 11259-11263.

    Williams, J. H. 2009. Amborella trichopoda (Amborellaceae) and the evolutionary developmental origins of the angiosperm progamic phase. American Journal of Botany 96(1): 166-182.

    Williams, J. H. and W. E. Friedman. 2002. Identification of diploid endosperm in an early angiosperm lineage. Nature 415: 522-526.

    Williams, J. H. and W. E. Friedman. 2004. The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): Implications for understanding the origin and early evolution of monocots, eumagnoliids, and eudicots. American Journal of Botany 91(3): 332-351.

    Williford, K. H., J. Foriel, P. D. Ward, and E. J. Steig. 2009. Major perturbation in sulfur cycling at the Triassic-Jurassic boundary. Geology 37(9): 835-838.

    Wilson, Paul, A. D. Wolfe, W. S. Armbruster, and J. D. Thomson. 2007. Constrained lability in floral evolution: counting convergent origins of hummingbird pollination in Penstemon and Keckiella. New Phytologist 176: 883-890.

    Wing, S. L. and B. H. Tiffney. 1987. Interactions of angiosperms and herbivorous tetrapods through time. Pp. 203-224 In: E. M. Friis, W. G. Chaloner, and P. R. Crane (eds.), The Origins of Angiosperms and Their Biological Consequences, Cambridge: Cambridge University Press, 358 pp.

    Wingrove, J. A. and P. H. O'Farrell. 1999. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98: 105-114.

    Winz, R. A. and I. T. Baldwin. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiology 125: 2189-2202.

    de Wit, M. J., J. G. Ghosh, S. de Villiers, N. Rakotosolofu, J. Alexander, A. Tripathi, and C. V. Looy. 2002. Multiple organic carbon isotope reversals across the Permo-Triassic boundary of terrestrial Gondwana sequences: clues to extinction patterns and delayed ecosystem recovery. The Journal of Geology 110: 227-240.

    Wittkopp, P. J. 2006. Evolution of cis-regulatory sequence and function in Diptera. Heredity 97: 139-147.

    Wray, G. A. 2003. Transcriptional regulation and the evolution of development. International Journal of Developmental Biology 47: 675-684.

    Wray, G. A. 2007. The evolutionary significance of cis-regulatory mutations. Nature Reviews Genetics 8: 206-216.

    Wray, G. A., M. W. Hahn, E. Abouheif, J. P. Balhoff, M. Pizer, M. V. Rockman, and L. A. Romano. 2003. The evolution of transcriptional regulation in eukaryotes. Molecular Biology and Evolution 20(9): 1377-1419.

    Wu, J. and I. T. Baldwin. 2010. New insights into plant responses to attack from insect herbivores. Annual Review of Genetics 44: 1-24.

    Wu, X., J. R. Dinneny, K. M. Crawford, Y. Rhee, V. Citovsky, P. C. Zambryski, and D. Weigel. 2003. Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130: 3735-3745.

    Wu, Z.-Y., A.-M. Lu, Y.-C. Tang, Z.-D. Chen, and W.-H. Li. 2002. Synopsis of a new "polyphyletic-polychromic-polytopic" system of the angiosperms. Acta Phytotaxonomica Sinica 40: 289-322.

    Xi, Zhenxiang, L. Liang, J. S. Rest, and C. C. Davis. 2014. Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies. Systematic Biology 63(6): 919-932.

    Xie, S., R. D. Pancost, Y. Wang, H. Yang, P. B. Wignall, G. Luo, C. Jia, and L. Chen. 2010. Cyanobacterial blooms tied to volcanism during the 5 m.y. Permo-triassic biotic crisis. Geology 38(5): 447-450.

    Xiong, C. and Q. Wang. 2011. Permian-Triassic land-plant diversity in south China: was there a mass extinction at the Permian/Triassic boundary? Paleobiology 37(1): 157-167.

    Xu, X. M. and D. Jackson. 2012. Chapter 4. Cell-to-cell movement of homeodomain transcription factors: yesterday, today, and tomorrow. Pp. 87-98 In: F. Kragler and M. Hülskamp (eds.), Short and Long Distance Signaling, Advances in Plant Biology 3. New York: Springer, 185 pp.

    Xu, X. M., J. Wang, Z. Xuan, A. Goldshmidt, P. G. M. Borrill, N. Harlharan, J. Y. Kim, and D. Jackson. 2011. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 333(6046): 1141-1144.

    Yadegari, R. and G. Drews. 2004. Female gametophyte development. The Plant Cell 16: S133-S141.

    Yamada, T., M. Ito, and M. Kato. 2003. Expression pattern of INNER NO OUTER homologue in Nymphaea (water lily family, Nymphaeaceae). Developmental Genes and Evolution 213: 510-513.

    Yamaguchi, N., M.-F. Wu, C. M. Winter, M. C. Berns, S. Nole-Wilson, A. Yamaguchi, G. Coupland, B. A. Krizek, and D. Wagner. 2013. A molecular framework for auxin-mediated initiation of flower primordia. Developmental Cell 24(3): 271-282.

    Yang, W.-C., D.-Q. Shi, and Y.-H. Chen. 2010. Female gametophyte development in flowering plants. Annual Review of Plant Biology 61: 89-108.

    Yellina, A. L., S. Orashakova, S. Lange, R. Erdmann, J. Leebens-Mack, and A. Becker. 2010. Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica). EvoDevo 1(1): 13.

    Yu, H., T. Ito, Y. Zhao, J. Peng, P. Kumar, and E. M. Meyerowitz. 2004. Floral homeotic genes are targets of gibberellin signaling in flower development. Proceedings of the National Academy of Sciences 101(20): 7827-7832.

    Zahn, L. M., H. Kong, J. H. Leebens-Mack, S. Kim, P. S. Soltis, L. L. Landherr, D. E. Soltis, C. W. dePamphilis, and H. Ma. 2005. The evolution of the SEPALLATA subfamily of MADS-Box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169: 2209-2223.

    Zahn, L. M., J. H. Leebens-Mack, C. W. dePamphilis, H. Ma. and G. Theißen. 2005. To B or not to B a flower: the role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. Journal of Heredity 96(3): 225-240.

    Zavada, M. S. 2007. The identification of fossil angiosperm pollen and its bearing on the time and place of the origin of angiosperms. Plant Systematics and Evolution 263: 117-134.

    Zavada, M. S. and M. T. Mentis. 1992. Plant-animal interaction: the effect of Permian megaherbivores on the glossopterid flora. The American Midland Naturalist 127(1): 1-12.

    Zavialova, N. E. and A. V. Gomankov. 2009. Occurrence of angiosperm-like ultrastructural features in gymnosperm pollen from the Permian of Russia. Review of Palaeobotany and Palynology 156(1-2): 79-89.

    Zelditch, M. L. and W. L. Fink. 1996. Heterochrony and heterotopy: stability and innovation in the evolution of form. Paleobiology 22(2): 241-254.

    Zeng, Lipeng, Qiang Zhang, Renran Sun, Hongzhi Kong, Ning Zhang, and Hong Ma. 2014. Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nature Communications 5: 4956.

    Zhang, B., X. Pan, G. P. Cobb, and T. A. Anderson. 2006. Plant microRNA: a small regulatory molecule with big impact. Developmental Biology 289: 3-16.

    Zhang, G., H. Wang, J. Shi, X. Wang, H. Zheng, G. K.-S. Wong, T. Clark, W. Wang, J. Wang, and L. Kang. 2007. Identification and characterization of insect-specific proteins by genome data analysis. BMC Genomics 8: 93.

    Zhang, H. D. 1995. Florology. Guangzhou: Zhongshan University Press, 234 pp. (in Chinese).

    Zhang, P., H. T. W. Tan, K.-H. Pwee, and P. P. Kumar. 2004. Conservation of class C function of floral organ development during 300 million years of evolution from gymnosperms to angiosperms. The Plant Journal 37: 566-577.

    Zhao, Q., H. Wang, Y. Yin, Y. Xu., F. Chen, and R. A. Dixon. 2010. Syringyl lignin biosynthesis is directly regulated by a secondary cell wall master switch. Proceedings of the National Academy of Sciences 107(32): 14496-14501.

    Zhendong, D., S. N. Gorb, and U. Schwarz. 2002. Roughness-dependent friction force of the tarsal claw system in the beetle Pachnoda marginata (Coleoptera, Scarabacidae). Journal of Experimental Biology 205(16): 2479-2488.

    Zherikhin, V. V. 2002. Ecological History of Terrestrial Insects. Pp. 331-388 In.: A. P. Rasnitsyn & D. I. J. Quicke, eds. History of Insects. London: Kluwer Academic Publishers, 517 pp.

    Zhong, R., C. Lee, and Z.-H. Ye. 2010. Evolutionary conservation of the transcriptional network regulating secondary wall biosynthesis. Trends in Plant Science 15(11): 625-632.

    Zhou, X., F. M. Oi, and M. E. Scharf. 2006. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proceedings of the National Academy of Sciences 103(12): 4499-4504.

    Zhou, X., M. R. Tarver, and M. E. Scharf. 2007. Hexamerin-based regulation of juvenile hormone-dependent gene expression underlies phenotypic plasticity in a social insect. Development 134: 601-610.

    Zinzen, R. P., C. Giradot, J. Gagneur, M. Braun, and E. E. M. Furlong. 2009. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 462: 65-70.

    Zobell, O., W. Faigl, H. Saedler, and T. Münster. 2010. MIKC* MADS-Box proteins: conserved regulators of the gametophytic generation of land plants. Molecular Biology and Evolution 27(5): 1201-1211.

    Zuccolo, A., J. E. Bowers, J. C. Estill, Z. Xiong, M. Luo, A. Sebastian, J. L. Goicoechea, K. Collura, Y. Yu, A. Chanderbali, D. E. Soltis, S. Chamala, B. Barbazuk, P. S. Soltis, V. A. Albert, H. Ma, D. Mandoli, J. Banks, J. E. Carlson, J. Tompkins, C. W. dePamphilis, R. A. Wing, and J. Leebens-Mack. 2011. A physical map for the Amborella trichopoda genome sheds light on the evolution of angiosperm genome structure. Genome Biology 12: R48.

    Zullo, M. A. T. and G. Adam. 2002. Brassinosteroid phytohormones - structure, bioactivity and applications. Brazilian Journal of Plant Physiology 14(3): 143-181.

    Zwieniecki, M. A. and C. K. Boyce. 2014. Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology. Proceedings of the Royal Society of London, Series B, Biological Sciences 281: 20132829.

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    ESSAY CONTENTS

  • Biometry and Scaling in Theoretical Morphospace
  • Chloroplast Capture and Horizontal Transfer (HT) of Genes
  • Coevolutionary Arms Race
  • Coevolutionary Compartments in Deep Time
  • Comparing Theories and Hypotheses
  • Conclusions on the Origin of Angiosperms
  • Cross-kingdom Signaling and Transduction
  • Developing a Coevolutionary Hypothesis
  • Discerning Fingerprints of Developmental Regulation
  • First Clues on the Origin of Angiosperms
  • Fitness Landscapes, Compartments, and Paleoenvironments
  • Gene and Whole Genome Duplications (WGDs)
  • Genome Landscapes and Gene Regulatory Networks
  • Helix-turn-helix (HTH) Proteins
  • Historical Context
  • Homeotic Selector Genes
  • Hydraulic Morphospace
  • Insect Developmental Tool Kit
  • Insect Hexamerins and Hemocyanins
  • Insect Sensing and Hormone Signaling
  • Interspecific Hybridization
  • Land Plant Developmental Tool Kit
  • Literature Cited on the Origin of Angiosperms
  • Mass Extinctions
  • MicroRNAs (MiRNAs)
  • Mutualisms
  • Natural Products, Phytohormones, and Signaling
  • Paleoecology of Global Catastrophe
  • Paleophysiology and Molecular Biology of Tool Kits
  • Physiology of Homeodomain Protein Trafficking
  • Plant Biology of Cone Development and Flowering
  • Problems with Contemporary Data Sets
  • Progenesis of Reproductive Modules
  • Transposable Elements (TEs)

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    APRIL 3, 2017


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