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Evaluating the diversity of pteridophyte embryology in the light of recent phylogenetic analyses leads to new inferences on character evolution

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Abstract

This is the first review of the developmental morphology of pteridophyte embryos since molecular phylogenies revolutionized concepts of tracheophyte evolution. In the light of these novel relationships, embryo characters are evaluated across pteridophytes to hypothesize homology and infer character transformations. Salient features of traditional categories used to classify pteridophyte embryos, for example endoscopy and exoscopy, are analyzed and related to gametophyte habit. Suspensor formation evolved in several lineages and is reinterpreted as representing a distinct developmental stage of the foot which is the only embryonic organ that is homologous across all land plants. Endoscopy in lycophytes is distinct from that of monilophytes, because lycophyte embryos undergo reorientation, lack interdigitating placental cells, and contain an interplacental space which may be related to their lack of a basal pad cell during archegonial development. Pteridophyte embryology may provide clues to tracheophytes evolution and novel developmental mechanisms.

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References

  • Albaum HG (1938) Inhibitions due to growth hormones in fern prothallia and sporophytes. Amer J Bot 25:124–133

    Article  CAS  Google Scholar 

  • Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. A Rev Ecol Syst 29:263–292

    Article  Google Scholar 

  • Bethka PC, Lonsdale JE, Fath A, Jones RL (1999) Hormonally regulated programmed cell death in barley aleurone cells. Pl Cell 11:1033–1045

    Google Scholar 

  • Bewley JD, Hempel FD, McCormick S, Zambryski P (2001) Reproductive development. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 988–1043

    Google Scholar 

  • Bierhorst DW (1953) The gametangia and embryo of Psilotum nudum. Amer J Bot 40:274–281

    Article  Google Scholar 

  • Bierhorst DW (1965) Older gametophytes and young sporophytes of Schizaea melanesica. Bul Tor Bot Club 92:475–488

    Article  Google Scholar 

  • Bierhorst DW (1968) Observations on Schizaea and Actinostachys spp., including A. oligostachys, sp. nov. Amer. J. Bot. 55:87–108

    Article  Google Scholar 

  • Bierhorst DW (1969) On Stromatopteris and its ill-defined organs. Amer J Bot 56:160–174

    Article  Google Scholar 

  • Bierhorst DW (1971) Morphology of vascular plants. Macmillan, New York

    Google Scholar 

  • Bierhorst DW (1975) Gametophytes and embryos of Actinostachys pennula, A. wagneri, and Schizaea elegans, with notes on other species. Amer J Bot 62:319–335

    Article  Google Scholar 

  • Bierhorst DW (1983) On the embryogeny of Schizaea dichotoma. Amer J Bot 70:1057–1062

    Article  Google Scholar 

  • Blockelie DJ (1994) Plant roots in core. In: Donovan SK (ed) The palaeobiology of trace fossils. Wiley, New York, pp 177–199

    Google Scholar 

  • Bower FO (1935) The ferns, vol 1. Cambridge University Press, London

    Google Scholar 

  • Brebner G (1896) On the prothallus and embryo of Danaea simplicifolia, Rudge. Ann Bot 38:109–122

    Google Scholar 

  • Bruchmann H (1898) Über die prothallien und keimpflanzen merhrer europaischer lycopodien. Gotha

  • Bruchmann H (1912) Zur embryologie der selaginellaceen. Flora 104:180–224

    Google Scholar 

  • Campbell DH (1895) The structure and development of mosses and ferns. Macmillan, New York

    Google Scholar 

  • Campbell DH (1908) The prothallium of Kaulfussia and Gleichenia. Ann Jar Bot Buit 22:69–102

    Google Scholar 

  • Campbell DH (1914) The structure and affinities of Macroglossum alidae, Copeland. Ann Bot 28:653–669

    Google Scholar 

  • Campbell DH (1922) The gametophyte and embryo of Botrychium simplex, Hitchcock. Ann Bot 36:441–455

    Google Scholar 

  • Campbell DH (1928) The embryo of Equisetum debile, Roxb. Ann Bot 42:717–728

    Google Scholar 

  • Campbell EO (1936) The embryo and stelar development of Histiopteris incisa. Trans Royal Soc New Zeal 66:1–11

    Google Scholar 

  • Carafa A, Duckett JG, Knox JP, Ligrone R (2005) Distribution of cell wall xylans in bryophytes and tracheophytes: new insights into basal interrelationships of land plants. New Phytol 168:231–240

    Article  CAS  PubMed  Google Scholar 

  • Christenhusz MJM, Tuomisto H, Metzgar JS, Pryer KM (2008) Evolutionary relationships within the Neotropical, eusporangiate fern genus Danaea (Marattiaceae). Mol Phyl Evol 46:34–48

    Article  CAS  Google Scholar 

  • Cross GL (1931) Embryology of Osmunda cinnamonea. Bot Gaz 92:210–217

    Article  Google Scholar 

  • DeMaggio AE (1961) Morphogenetic studies of the fern Todea barbara (L.) Moore-II. development of the embryo. Phytomorphology:64–79

  • DeMaggio AE, Wetmore RH (1961) Morphogenetic studies of the fern Todea barbara. III. experimental embryology. Amer J Bot 48:551–565

    Article  CAS  Google Scholar 

  • Duckett JG, Ligrone R (1992) A light and electron microscope study of the fungal endophytes in the sporophyte and gametophyte of Lycopodium cernuum with observations on the gametophyte-sporophyte junction. Can J Bot 70:58–72

    Article  Google Scholar 

  • Duckett JG, Ligrone R (2003) The structure and development of haustorial placentas in leptosporangiate ferns provides a clear-cut distinction between euphyllophytes and lycophytes. Ann Bot 92:513–552

    Article  PubMed  Google Scholar 

  • Farmer JB (1892) On the embryology of Angiopteris evecta Hofm. Proc Royal Soc London 51:471–474

    Google Scholar 

  • Floyd SK, Friedman WE (2000) Evolution of endosperm patterns among basal flowering plants. Int J Pl Sci 161:S57–S81

    Article  Google Scholar 

  • Forbis TA, Floyd SK, DeQuieroz (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56: 2112–2125

  • Foster DB (1964) The gametophytes and embryogeny of five species of Botrychium. Dissertation, Cornell University, pp 216

  • Frey W, Campbell EO, Hilger HH (1994) Structure of the sporophyte-gametophyte junction in Tmesipteris elongata P.A. Dangeard (Psilotaceae, Psilotopsida) and its phylogenetic implications-an SEM analysis. Nova Hed 59:21–32

    Google Scholar 

  • Frey W, Hofmann M, Hilger HH (2001) The gametophyte-sporophyte junction: unequivocal hints for two evolutionary lines in archegoniate land plants. Flora 196:431–445

    Google Scholar 

  • Gifford EM, Foster AS (1989) Morphology and evolution of vascular plants. W.H. Freeman, New York

    Google Scholar 

  • Goebel K (1905) Organography of plants especially of the archegoniatae and spermophyta. Part II: special organography. Trans. I. B. Balfour IB. Clarendon Press, Oxford

    Google Scholar 

  • Graham LE (1993) Origin of land plants. Wiley, New York

    Google Scholar 

  • Graham LE, Wilcox LW (2000) The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport. Phil Trans Royal Soc London B Biol Sci 355:757–767

    Article  CAS  Google Scholar 

  • Guillon J-M (2007) Molecular phylogeny of horsetails (Equisetum) including chloroplast atpB sequences. J Plant Res 120:569–574

    Article  PubMed  Google Scholar 

  • Hauk WD, Parks CR, Chase MW (2003) Phylogenetic study of Ophioglossaceae: evidence from rbcL and trnL-F plastid DNA sequences and morphology. Mol Phyl Evol 28:131–151

    Article  CAS  Google Scholar 

  • Hilger HH, Weigend M, Frey W (2002) The gametophyte-sporophyte junction in Isoëtes boliviensis Weber (Isoëtales, Lycopodiophyta). Phyton 42:149–157

    Google Scholar 

  • Hofmiester W (1862) The higher cryptogamia. Ray Soc, London

    Google Scholar 

  • Holloway JE (1917) The prothallus and young plant of Tmesipteris. Trans New Zeal Inst 50:1–44

    Google Scholar 

  • Holloway JE (1920) Studies in the New Zealand species of the genus Lycopodium: part IV- the structure of the prothallus in five species. Transactions of the New Zealand Institute 52:193–239

    Google Scholar 

  • Holloway JE (1944) The gametophyte, embryo. and developing sporophyte of Cardiomanes reniforme (Forst.) Presl. Trans Royal Soc New Zeal 74:196–206

    Google Scholar 

  • Holttum R (1949) The classification of ferns. Biol Rev 24:267–296

    Article  CAS  PubMed  Google Scholar 

  • Jayasekera RDE, Bell PR (1959) The effects of various experimental treatments on the development of the embryo of the fern Thelypteris paulstris. Planta 54:1–14

    Article  Google Scholar 

  • Johnson GP, Renzaglia KS (2008) Embryology of Ceratopteris richardii Brongn. (Pteridaceae, tribe Ceratopterideae) with emphasis on placental development. J Plant Res 121:581–592

    Article  PubMed  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353

    Article  CAS  PubMed  Google Scholar 

  • Kato M, Akiyama H (2005) Interpolation hypothesis for origin of the vegetative sporophyte of land plants. Taxon 54:443–450

    Google Scholar 

  • Kenrick P, Crane PR (1997) The origin and early diversification of land plants: a cladistic study. Smithsonian Institution, Washington, DC, p 441

    Google Scholar 

  • Khatoon K (1986) Occurrence of transfer cells in the sporophyte of Pteridium aquilinum L. Pak J Bot 18:9–13

    Google Scholar 

  • Korall P, Kenrick P (2004) The phylogenetic history of Selaginellaceae based on DNA sequences from the plastid and nucleus: extreme substitution rates and rate heterogeneity. Mol Phyl Evol 31:852–864

    Article  CAS  Google Scholar 

  • Korall P, Conant DS, Metzgar JS, Schneider H, Pryer KM (2007) A molecular phylogeny of the scaly tree ferns (Cyatheaceae). Amer J Bot 94:873–886

    Article  CAS  Google Scholar 

  • Kuligowski J, Ferrand M, Cheno E (1991) Stored mRNA in early embryos of a fern Marsilea vestita: a paternal and maternal origin. Mol Rep Devo 30:27–33

    Article  CAS  Google Scholar 

  • Kurotaki Y, Hatta K, Nakao K, Nabeshima Y-I, Fugimori T (2007) Blastocyst axis is specified independently of early cell lineage but aligns with the ZP shape. Science 316:719–723

    Article  CAS  PubMed  Google Scholar 

  • LaMotte C (1933) Morphology of the megagametophyte and the embryo sporophyte of Isoetes lithophila. Amer J Bot 20:217–233

    Article  Google Scholar 

  • LaMotte C (1937) Morphology and orientation of the embryo of Isoetes. Ann Bot 1:695–716

    Google Scholar 

  • Land WJG (1923) A suspensor in Angiopteris. Bot Gaz 75:421–425

    Google Scholar 

  • Lang WH (1902) On the prothalli of Ophioglossum pendulum and Helminthostachys zeylanica. Ann Bot 16:23–56

    Google Scholar 

  • Lee Y-I, Yeung EC, Lee N, Chung M-C (2006) Embryo development in the lady’s slipper orchid, Paphiopedilum delenatii with emphasis on the ultrastructure of the suspensor. Ann Bot 98:1311–1319

    Article  PubMed  Google Scholar 

  • Leitgeb H (1878) Zur embryologie der Farne. S B Akad Wiss Wie 77:222

    Google Scholar 

  • Leitgeb H (1880) Studien über entwicklung der farne. Sitz Kais Akad Wiss 80:201–226

    Google Scholar 

  • Ligrone R, Renzaglia KS (1989) The ultrastructure of the placenta in Sphagnum. New Phytol 111:197–201

    Google Scholar 

  • Ligrone R, Duckett JG, Renzaglia KS (1993) The gametophyte-sporophyte junction in land plants. Adv Bot Res 19:231–317

    Article  Google Scholar 

  • Ligrone R, Carafa A, Lumini E, Bianciotto V, Bonfante P, Duckett JG (2007) Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Amer J Bot 94:1756–1777

    Article  CAS  Google Scholar 

  • Lyon HL (1905) A new genus of Ophioglossaceae. Bot Gaz 40:455–458

    Article  Google Scholar 

  • MacMillan C (1898) The orientation of the plant egg and its ecological significance. Bot Gaz 25:301–323

    Article  Google Scholar 

  • Maddison WP, Maddison DR (2007) Mesquite: a modular system for evolutionary analysis. Version 2.01 http://mesquiteproject.org

  • Mansfield SG, Briarty LG (1991) Early embryogenesis in Arabidopsis thaliana. ii, the developing embryo. Can J Bot 69:461–476

    Article  Google Scholar 

  • Nayar BK, Kaur S (1971) Gametophytes of homosporous ferns. Bot Rev 37:295–396

    Article  Google Scholar 

  • Nickrent DL, Parkinson CL, Palmer JD, Duff RJ (2000) Multigene phylogeny of land plants with special references to bryophytes and the earliest land plants. Mol Biol Evo 17:1885–1895

    CAS  Google Scholar 

  • Peterson RL, Whittier DP (1991) Transfer cells in the sporophyte-gametophyte junction of Lycopodium appressum. Can J Bot 69:222–226

    Google Scholar 

  • Pryer KM (1999) Phylogeny of Marsileacous ferns and relationships of the fossil Hydropteris pinnata reconsidered. Int J Pl Sci 160:931–954

    Article  Google Scholar 

  • Pryer KM, Smith AR, Skog JE (1995) Phylogenetic relationships of extant ferns based on evidence from morphology and rbcL sequences. Amer Fern J 85:205–282

    Article  Google Scholar 

  • Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91:1582–1598

    Article  CAS  Google Scholar 

  • Qiu Y-L (2008) Phylogeny and evolution of charophytic algae and land plants. Plant Syst Evol 46:287–306

    Google Scholar 

  • Qiu Y-L, Li L, Wang B, Chen Z, Dombrovska O, Lee J, Kent L, Li R, Jobson R, Hendry T, Taylor DW, Testa CM, Ambros M (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168:691–708

    Article  CAS  Google Scholar 

  • Raghavan V (1989) Developmental biology of fern gametophytes. Cambridge University Press, New York

    Google Scholar 

  • Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in “lower” land plants. Phil Trans Royal Soc Lond B Biol Sci 355:815–831

    Article  CAS  Google Scholar 

  • Remy W, Gensel PG, Hagen H (1993) The gametophyte generation of some early Devonian land plants. Int J Pl Sci 154:35–58

    Article  Google Scholar 

  • Renzaglia KS, Garbary DJ (2001) Motile male gametes of land plants: diversity, development, and evolution. Crit Rev Pl Sci 20:107–213

    Article  Google Scholar 

  • Renzaglia KS, McFarland KD, Smith DK (1997) Anatomy and ultrastructure of the sporophyte of Takakia ceratophylla (Bryophyta). Amer J Bot 84:1337–1350

    Article  Google Scholar 

  • Renzaglia KS, Duff RJ, Ligrone R, Shaw AJ, Mishler BD, Duckett JG (2007) Bryophyte phylogeny: advancing the molecular and morphological frontiers. Bryologist 110:179–213

    Article  Google Scholar 

  • Rydin C, Wikström N (2002) Phylogeny of Isoëtes (Lycopsida): resolving basal relationships using rbcL sequences. Taxon 51:83–89

    Article  Google Scholar 

  • Schneider H, Pryer KM, Cranfill R, Smith AR, Wolfe PG (2002) Evolution of vascular plant body plans: a phylogenetic perspective. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor & Francis, New York, pp 330–364

    Google Scholar 

  • Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428:553–557

    Article  CAS  PubMed  Google Scholar 

  • Schuettpelz E, Pryer K (2007) Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56:1037–1050

    Article  Google Scholar 

  • Singh S, Lazzaro MD, Walles B (1999) Microtubule organization in the differentiating transfer cells of the placenta in Lilium spp. Protoplasma 207:75–83

    Article  Google Scholar 

  • Steeves TA, Sussex IM (1972) Experimental and analytical studies of embryogenesis: patterns in plant development. Prentice-Hall, Englewood Cliffs, pp 20–36

    Google Scholar 

  • Stokey AG (1930) Prothallia of the Cyatheaceae. Bot Gaz 90:1–45

    Article  Google Scholar 

  • Stone IG (1958) The gametophyte and embryo of Polyphebium venosum (R. BR.) Copeland (Hymenophyllaceae). Aust J Bot 6:183–203

    Article  Google Scholar 

  • Talbot MJ, Offler CE, McCurdy DW (2002) Transfer cell wall architecture: a contribution towards understanding localized wall deposition. Protoplasma 219:197–209

    Article  PubMed  Google Scholar 

  • Talbot MJ, Wasteneys G, McCurdy DW, Offler CE (2007a) Deposition patterns of cellulose microfibrils in flange wall ingrowths of transfer cells indicate clear parallels with those of secondary cell wall thickenings. Func Pl Biol 34:307–313

    Article  CAS  Google Scholar 

  • Talbot MJ, Wasteneys G, Offler CE, McCurdy DW (2007b) Cellulose synthesis is required for deposition of reticulate wall ingrowths in transfer cells. Pl Cell Physiol 48:147–158

    Article  CAS  Google Scholar 

  • Taylor TMC (1939) Some features of the organization of the sporophyte of Equisetum arvense L. New Phytol 38:159–166

    Article  Google Scholar 

  • Testa C, Ambros M (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Pl Sci 168:691–708

    Article  Google Scholar 

  • Treub M (1890) Le embryon et al. plantule du Lycopodium cernuum L. Ann Jar Bot Buit 8:1–15

    Google Scholar 

  • Vaughn KC, Talbot MJ, Offler CE, McCurdy DW (2007) Wall ingrowths in epidermal transfer cells of Vicia faba cotyledons are modified primary walls marked by localized accumulations of arabinogalactan proteins. Pl Cell Physiol 48:159–168

    Article  CAS  Google Scholar 

  • Vladesco MA (1935) Researches morphologiques et expérimentales sur l’embryogénie et l’organogénie des fougères leptosporangiées. Rev Gen Bot 47:741–763

    Google Scholar 

  • Ward M (1954) The development of the embryo of Phlebodium aureum J. SM. Phytomorphology 4:18–26

    Google Scholar 

  • Ward M, Wetmore RH (1954) Experimental control of development in the embryo of the fern, Phlebodium aureum. Amer J Bot 41:428–434

    Article  Google Scholar 

  • Wardini T, Talbot MJ, Offler CE, Patrick JW (2006) Role of sugars in regulating transfer cell development in cotyledons of developing Vicia faba seeds. Protoplasma 230:75–88

    Article  PubMed  CAS  Google Scholar 

  • Wardlaw CW (1955) Embryogenesis in leptosporangiate ferns: embryogenesis in plants. Wiley, New York, pp 142–170

  • Weber H, Borisjuk L, Wobus U (1997) Sugar import and metabolism during seed development. Trends Pl Sci 2:169–174

    Article  Google Scholar 

  • Whittier DP, Carter R (2007) The gametophyte of Lycopodiella prostrata. Amer Fern J 97:230–233

    Article  Google Scholar 

  • Whittier DP, Pintaud JC, Braggins JE (2005) The gametophyte of Lycopodium deuterodensum- type I or II. Amer Fern J 95:22–29

    Article  Google Scholar 

  • Wikström N, Kenrick P (2001) Evolution of lycopodiaceae (Lycopsida): estimating divergence times from rbcL gene sequences by use of nonparametric rate smoothing. Mol Phylo Evol 19:177–186

    Article  CAS  Google Scholar 

  • Winther JL, Friedman WE (2007a) Arbuscular mycorrhizal associations in Lycopodiaceae. New Phytol 177:790–801

    Article  PubMed  CAS  Google Scholar 

  • Wnuk C (1996) The development of floristic provinciality during the Middle and late Paleozoic. Rev Palaeobot Palynol 90:4–40

    Google Scholar 

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Acknowledgments

The authors would like to thank Regina D. Kettering and Pamela Robbins for translating the German texts, Dr Jeffrey Duckett for his helpful comments, and the Renzaglia laboratory for their support. Funding for this work was provided by grants (DEB-0322664, DEB-0423625, DEB-052177, and DEB-0228679) through the National Science Foundation as part of the Assembling the Tree of Life Project.

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  1. Department of Botany, Smithsonian Institution, MSC A1014 , 4210 Silver Hill Road, Suitland, MD, 20746, USA

    Gabriel P. Johnson

  2. Green Plant Morphology Group, Department of Plant Biology, Southern Illinois University, 1125 Lincoln Drive, Carbondale, IL, 62901, USA

    Karen S. Renzaglia

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Correspondence to Gabriel P. Johnson.

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Johnson, G.P., Renzaglia, K.S. Evaluating the diversity of pteridophyte embryology in the light of recent phylogenetic analyses leads to new inferences on character evolution. Plant Syst Evol 283, 149–164 (2009). https://doi.org/10.1007/s00606-009-0222-4

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