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Embryology of Ceratopteris richardii (Pteridaceae, tribe Ceratopterideae), with emphasis on placental development

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Abstract

This comprehensive study of early embryology in Ceratopteris richardii combines light microscopy with the first ultrastructural evaluation of any pteridophyte embryo. Emphasis is placed on ontogeny of the foot and placental transfer cells. The embryology of C. richardii shares many similarities with that of other polypodiacious ferns while exhibiting distinctive division patterns. Formative embryonic stages have been reconstructed into three-dimensional models for ease of interpretation. The zygote divides perpendicular to the gametophyte plane and anterioposterior axis. This division establishes a prone embryological habit that maximizes rapid independent establishment of a leaf-root axis in a cordate gametophyte. After the formation of a globular eight-celled stage, initials of the first leaf, and root and shoot apical meristems are defined early by discrete formative divisions. Concomitantly, the foot expands and differentiates to transport nutrients from the gametophyte for the developing embryonic organs. Transfer cell wall ingrowth deposition begins in the gametophyte placental cells before the adjacent sporophyte cells just after the eight-celled stage. These observations provide an anatomical framework for future comparative developmental genetic studies of embryogenesis in free-sporing plants.

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References

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

    Article  CAS  Google Scholar 

  • Alfayate C, Estébanez B, Ron E (2000) The sporophyte–gametophyte junction in five species of pleurocarpous mosses. Bryologist 103:467–474

    Article  Google Scholar 

  • Barrero C, Muniz L-M, Gomez E, Hueros G, Royo J (2006) Molecular dissection of the interaction between the transcriptional activator ZmMRP-1 and the promoter of BETL-1. Plant Mol Biol 62:655–668

    Article  PubMed  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. Annu Rev Ecol Syst 29:263–292

    Article  Google Scholar 

  • Bierhorst DW (1971) The morphology of vascular plants. MacMillan, New York

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bower FO (1935) Primitive land plants. Macmillan, London

    Google Scholar 

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

    Google Scholar 

  • Browning AJ, Gunning BES (1979a) Structure and function of transfer cells in the sporophyte haustorium of Funaria hygrometrica Hedw.: I. the development and ultrastructure of the haustorium. J Exp Bot 30:1233–1246

    Article  Google Scholar 

  • Browning AJ, Gunning BES (1979b) Structure and function of transfer cells in the sporophyte haustorium of Funaria hygrometrica Hedw.: III. Translocation of assimilate into the attached sporophyte and along the seta of attached and excised sporophytes. J Exp Bot 30:1265–1273

    Article  Google Scholar 

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

    Google Scholar 

  • Campbell DH (1893) On the development of Azolla filiculoides Lam. Ann Bot 7:155–187

    Google Scholar 

  • Campbell DH (1894) Observations on the development of Marattia douglasii, Baker. Ann Bot 8:1–20

    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 (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 R Soc N Z 66:1–11

    Google Scholar 

  • Chatterjee A, Roux SJ (2000) Ceratopteris richardii: a productive model for revealing secrets of signaling and development. J Plant Growth Regul 19:284–289

    Article  PubMed  CAS  Google Scholar 

  • Conard HS (1908) The structure and life-history of the hay-scented fern. Carnegie Institution, Washington DC

    Google Scholar 

  • Cordle AR, Irish EE, Cheng CL (2007) Apogamy induction in Ceratopteris richardii. Int J Plant Sci 168:361–369

    Article  Google Scholar 

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

    Article  Google Scholar 

  • DeMaggio AE (1961) Morphogenetic studies on the fern Todea barbara (L.) Moore-II. Development of the embryo. Phytomorphology 11:64–79

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dong YH, Gituru RW, Chen JM, Wang QF (2005) Effect of habitat modification on the distribution of the endangered aquatic fern Ceratopteris thalictroides (Parkeriaceae) in China. J Fresh Ecol 20:689–693

    CAS  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 92:513–521

    Article  PubMed  Google Scholar 

  • Ford S (1902) The anatomy of Ceratopteris thalictroides, (L.). Ann Bot 16:95–121

    Google Scholar 

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

  • 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. Freeman, New York

    Google Scholar 

  • Goebel K (1905) Organography of plants especially of the archegoniatae and spermophyta. Trans. Balfour IB. Clarendon, Oxford

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

    Google Scholar 

  • Gregorich M, Fisher R (2006) Auxin regulates lateral meristems activation in developing gametophytes of Ceratopteris richardii. Can J Bot 84:1520–1530

    Article  CAS  Google Scholar 

  • Gunning BES, Pate JS (1969a) Cells with wall ingrowths (transfer cells) in the placenta of ferns. Planta 87:271–274

    Article  Google Scholar 

  • Gunning BES, Pate JS (1969b) “Transfer cells” plant cells with wall ingrowths, specialized in relation to short distance transport of solutes-their occurrence, structure, and development. Protoplasma 68:107–133

    Article  Google Scholar 

  • Gutiérrez-Marcos JF, Dal-Rpa M, Giulini A, Costa LM, Gavazzi G, Cordelier S, Sellam O, Tatout C, Paul W, Perez P, Dickinson HG, Consonni G (2007) Empty pericarp4 encodes a mitochondrion-targeted pentatricopeptide repeat protein necessary for seed development and plant growth in maize. Plant Cell 19:196–201

    Article  PubMed  CAS  Google Scholar 

  • Gutiérrez-Marcos JF, Costa LM, Corinne B-P, Bouchaib K, O’Sullivan DM, Wormald M, Perex P, Dickinson HG (2004) maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with maternal parent-of-origin pattern of expression. Plant Cell 16:1288–1301

    Article  PubMed  Google Scholar 

  • Hickok LG, Warne TR, Fribourg RS (1995) The biology of the fern Ceratopteris and its use as a model system. Int J Plant Sci 156:3332–3345

    Article  Google Scholar 

  • Higinbotham N (1941) Development of the gametophytes and embryo of Regnellidium diphyllum. Am J Bot 28:282–300

    Article  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 Society, Hardwicke, London

    Google Scholar 

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

    Google Scholar 

  • Howe MD (1931) Origin of the leaf, and adventitious and secondary roots of Ceratopteris thalictroides. Bot Gaz 92:326–329

    Article  Google Scholar 

  • Imaichi R, Hiratsuka R (2007) Evolution of shoot apical meristems structures in vascular plants with respect to plasmodesmatal network. Am J Bot 94:1911–1921

    Article  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 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lal M, Narang M (1985) Ultrastructural and histochemical studies of transfer cells in the callus and apogamous sporophytes of Physcomitrium coorgense Broth. New Phytol 100:225–231

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Ligrone R, Duckett JG, Renzaglia KS (1993) The gametophye sporophyte junction in land plants. Adv Plant Res 19:232–317

    Google Scholar 

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

    Article  Google Scholar 

  • Nayar BK, Kaur S (1969) A reinvestigation of the morphology of the gametophyte and juvenile sporophyte of Ceratopteris thalictroides. Can J Bot 47:395–404

    Article  Google Scholar 

  • Pal N, Pal S (1962) Studies on morphology and affinity of the Parkeriaceae I. Morphological observations of Ceratopteris thalictroides. Bot Gaz 124:132–143

    Article  Google Scholar 

  • Pryer M, 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 

  • Renzaglia KS, Warne TR (1995) Ceratopteris: an ideal model system for teaching plant biology. Int J Plant Sci 156:385–392

    Article  Google Scholar 

  • Rogers LM (1926) Development of the archegone and studies in fertilization in Lygodium palmatum. Cellule 34:327–352

    Google Scholar 

  • Rutherford G, Tanurdzic M, Hasebe M, Banks JA (2004) A systematic gene silencing method suitable for high throughput reverse genetic analyses of gene function in fern gametophytes. BMC Plant Biol 4:6

    Article  PubMed  Google Scholar 

  • Sakamaki Y, Ino Y (1999) Contribution of fern gametophytes to produced sporophytes on the basis of carbon gain. Ecol Res 14:59–69

    Article  Google Scholar 

  • Salmi ML, Bushart TJ, Stout SC, Roux SJ (2005) Profile and analysis of gene expression changes during early development in germinating spores of Ceratopteris richardii. Plant Physiol 138:1734–1745

    Article  PubMed  CAS  Google Scholar 

  • Stokey AG, Atkinson LR (1957) The gametophyte of some American species of Elaphoglossum and Rhipidopteris. Phytomorphology 7:275–292

    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, Wasteneys GO, Offler CE, McCurdy DW (2007) Cellulose synthesis is required for deposition of reticulate wall ingrowths in transfer cells. Plant Cell Physiol 48:147–158

    Article  PubMed  CAS  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 

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

    Google Scholar 

  • Villarreal JC, Renzaglia KS (2006) Sporophyte structure in the neotropical hornwort Phaeomegaceros fimbriatus: implications for phylogeny, taxonomy, and character evolution. Int J Plant Sci 167:413–427

    Article  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. Am J Bot 41:428–434

    Article  Google Scholar 

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

  • Warne TR, Hickok LG (1997) C-fern manual. (see http://cfern.bio.utk.edu/manual.html, last accessed 5th February 2008)

  • Watkins JE, Mack MK, Mulkey SS (2007) Gametophyte ecology and demography of epiphytic and terrestrial tropical ferns. Am J Bot 94:701–708

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Leslie Hickok for providing the C. richardii spores, Hilarie D. Gates and Ryan McMillen for providing illustrations of the embryo models, Regina D. Kettering and Pamela Robbins for translating the German texts, the Renzaglia lab for their support and encouragement, the IMAGE faculty for their assistance with electron microscopy, and Jeffrey Duckett, Daniel L. Nickrent, and anonymous reviewers for their helpful comments. This research was supported by research grants (DEB-0322664, DEB-0423625, DEB-052177, and DEB-0228679) from the National Science Foundation as part of the Assembling the Tree of Life Programs.

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Correspondence to Gabriel P. Johnson.

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G. P. Johnson is a member of the Botanical Society of Japan.

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Johnson, G.P., Renzaglia, K.S. Embryology of Ceratopteris richardii (Pteridaceae, tribe Ceratopterideae), with emphasis on placental development. J Plant Res 121, 581–592 (2008). https://doi.org/10.1007/s10265-008-0187-3

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