The Sporophytes of Seed-Free Vascular Plants – Major Vegetative Developmental Features and Molecular Genetic Pathways

  • Alexandru M. F. Tomescu


Seed-free vascular plants, collectively referred to as pteridophytes, include several distinct lineages, of which some have living representatives: the lycopsids, sphenopsids, ferns, and psilotopsids. Although the last three are included in a monophyletic group (the moniliformopses) by some workers, the most comprehensive phylogenies that include both extant and extinct taxa reject the monophyly of moniliformopses. The sporophytes of the main living groups of seed-free plants exhibit significantly divergent morphologies, both among the different groups, and between those and the seed plants. In terms of vegetative features, such differences are seen in embryo structure and development, body plan, stele architecture, branching, leaf development and phyllotaxis, and rooting structures. These divergent morphologies are determined by fundamental differences in development and are thought to reflect independent origins of major developmental features that are supported by the current understanding of plant phylogeny. In this context, it becomes highly enticing to search for shared pathways (process homologies) and homoplasy in the molecular genetic mechanisms that control development. Understanding the gene pathways that control fundamental developmental features in the different lineages will greatly improve the resolution of vascular plant phylogeny. In this chapter, I present a comparative survey of major vegetative features of sporophytes, emphasizing the differences among the various living seed-free lineages and between those and seed plants, and I review the state-of-the-art knowledge of molecular genetic pathways that control the development of seed-free plant sporophytes. Results published to date point, in some cases, to highly conserved pathways, such as the one shared between the control of rhizoid development in bryophytes, and that of root hairs in flowering plants; this broad taxonomic range brackets, phylogenetically, all seed-free plant lineages which are hence hypothesized to share the same pathway. In other cases, such as leaf development, ­different lineages reveal complex mosaics of shared and divergent pathways. However, as molecular genetic studies of seed-free plants are still in their infancy compared to those of seed plants, and especially of angiosperms, most aspects of their vegetative sporophyte development have yet to be characterized from a molecular standpoint.


Apical Meristem Seed Plant Shoot Apical Meristem Leaf Primordia Stele Morphology 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aso, K., Kato, M., Banks, J. A., and Hasebe, M. 1999. Characterization of Homeodomain-Leucine Zipper genes in the fern Ceratopteris richardii and the evolution of the Homeodomain-Leucine Zipper gene family in vascular plants. Molecular Biology and Evolution 16:544–552.PubMedGoogle Scholar
  2. Axtell, M. J., and Bartel, D. P. 2005. Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673.CrossRefPubMedGoogle Scholar
  3. Axtell, M. J., and Bowman, J. L. 2008. Evolution of plant microRNAs and their targets. Trends in Plant Science 13:343–349.CrossRefPubMedGoogle Scholar
  4. Beck, C. B. 1960. The identity of the Archaeopteris and Callixylon. Brittonia 12:351–368.CrossRefGoogle Scholar
  5. Beck, C. B., Schmid, R., and Rothwell, G. W. 1982. Stelar morphology and the primary vascular system of seed plants. Botanical Review 48:691–815.CrossRefGoogle Scholar
  6. Bennett, T., and Leyser, O. 2006. Something on the side: axillary meristems and plant development. Plant Molecular Biology 60:843–854.CrossRefPubMedGoogle Scholar
  7. Bharathan, G., Goliber, T. E., Moore, C., Kessler, S., Pham, T., and Sinha, N. R. 2002. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296:1858–1860.CrossRefPubMedGoogle Scholar
  8. Bierhorst, D.W. 1971. Morphology of vascular plants. New York: MacmillanGoogle Scholar
  9. Bierhorst, D. W. 1977. The systematic position of Psilotum and Tmesipteris. Brittonia 29:3–13.CrossRefGoogle Scholar
  10. Bilderback, D. E. 1987. Association of mucilage with the ligule of several species of Selaginella. American Journal of Botany 74:1116–1121.CrossRefGoogle Scholar
  11. Campbell, D. H. 1911. The Eusporangiatae. The comparative morphology of the Ophioglossaceae and Marattiaceae. Washington, DC: Carnegie InstitutionGoogle Scholar
  12. Cantino, P. D., Doyle, J. A., Graham, S. W., Judd, W. S., Olmstead, R. G., Soltis, D. E., Soltis, P. S., and Donoghue, M. J. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56:822–846.CrossRefGoogle Scholar
  13. Chase, M. W., and Reveal, J. L. 2009. A phylogenetic classification of the land plants to accompany APG III. Botanical Journal of the Linnean Society 161:122–127.CrossRefGoogle Scholar
  14. Cui, H., Levesque, M. P., Vernoux, T., Jung, J. W., Paquette, A. J., Gallagher, K. L., Wang, J. Y., Blilou, I., Scheres, B., and Benfey, P. N. 2007. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425.CrossRefPubMedGoogle Scholar
  15. DeMaggio, A.E. 1982. Experimental embryology of pteridophytes. In Experimental embryology of vascular plants, ed. B.M. Johri, pp. 7–34. Berlin: SpringerGoogle Scholar
  16. Di Giacomo, E., Sestili, F., Iannelli, M. A., Testone, G., Mariotti, D., and Frugis, G. 2008. Characterization of KNOX genes in Medicago truncatula. Plant Molecular Biology 67:135–150.CrossRefPubMedGoogle Scholar
  17. Eames, A. J. 1936. Morphology of vascular plants. Lower groups. New York: McGraw-HillGoogle Scholar
  18. Esau K., 1977. Anatomy of seed plants. 2nd edn. New York: WileyGoogle Scholar
  19. Floyd, S. K., and Bowman, J. L. 2004. Ancient microRNA target sequences in plants. Nature 428:485–486.CrossRefPubMedGoogle Scholar
  20. Floyd, S. K., and Bowman, J. L. 2006. Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Current Biology 16:1911–1917.CrossRefPubMedGoogle Scholar
  21. Floyd, S. K., and Bowman, J. L. 2007. The ancestral developmental tool kit of land plants. International Journal of Plant Sciences 168:1–35.CrossRefGoogle Scholar
  22. Floyd, S. K., Zalewski, C. S., and Bowman, J. L. 2006. Evolution of class III Homeodomain-leucine zipper genes in streptophytes. Genetics 173:373–388.CrossRefPubMedGoogle Scholar
  23. Friedman, W. E., Moore, R. C., and Purugganan, M. D. 2004. The evolution of plant development. American Journal of Botany 91:1726–1741.CrossRefGoogle Scholar
  24. Gifford, E. M., and Foster, A. S. 1989. Morphology and evolution of vascular plants. 3rd edn. New York: FreemanGoogle Scholar
  25. Gola, E. M., Jernstedt, J. A., and Zagorska-Marek, B. 2007. Vascular architecture in shoots of early divergent vascular plants, Lycopodium clavatum and Lycopodium annotinum. New Phytologist 174:774–786.CrossRefPubMedGoogle Scholar
  26. Haeckel, E. 1866. Allgemeine Entwicklungsgeschichte der Organismen. Berlin: ReimerGoogle Scholar
  27. Harrison, C. J., Corley, S. B., Moylan, E. C., Alexander, D. L., Scotland, R. W., and Langdale, J. A. 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434:509–514.CrossRefPubMedGoogle Scholar
  28. Harrison, C. J., Rezvani, M., and Langdale, J. A. 2007. Growth from two transient apical initials in the meristem of Selaginella kraussiana. Development 134:881–889.CrossRefPubMedGoogle Scholar
  29. Hasebe, M., Wen, C.-K., Kato, M., and Banks, J. A. 1998. Characterization of MADS homeotic genes in the fern Ceratopteris richardii. Proceedings of the National Academy of Sciences USA 95(11):6222–6227.CrossRefPubMedGoogle Scholar
  30. Hilton, J., and Bateman, R. M. 2006. Pteridosperms are the backbone of seed-plant phylogeny. Journal of the Torrey Botanical Society 133:119–168.CrossRefGoogle Scholar
  31. Himi, S., Sano, R., Nishiyama, T., Tanahashi, T., Kato, M., Ueda, K., and Hasebe, M. 2001. Evolution of MADS-box gene induction by FLO/LFY genes. Journal of Molecular Evolution 53:387–393.CrossRefPubMedGoogle Scholar
  32. Imaichi, R. 2008. Meristem organization and organ diversity. In Biology and evolution of ferns and lycophytes, eds. T. A. Ranker and C. H. Haufler, pp. 75–103. Cambridge: Cambridge University PressGoogle Scholar
  33. Jernstedt, J. A., Cutter, E. G., and Lu, P. 1994. Independence of organogenesis and cell patern in developing angle shoots of Selaginella martensii. Annals of Botany 74:343–355.CrossRefGoogle Scholar
  34. Johnson, G., and Renzaglia, K. 2009. Evaluating the diversity of pteridophyte embryology in the light of recent phylogenetic analyses leads to new inferences on character evolution. Plant Systematics and Evolution 283:149–164.CrossRefGoogle Scholar
  35. Judd, W. S., Campbell, C. S., Kellogg, E. A., Stevens, P. F., and Donoghue, M. J. 2007. Plant systematics: a phylogenetic approach. 3rd edn. Sunderland: Sinauer AssociatesGoogle Scholar
  36. Kaplan, D. R. 1977. Morphological status of the shoot systems of Psilotaceae. Brittonia 29:30–53.CrossRefGoogle Scholar
  37. Kaplan, D. R., and Groff, P. A. 1995. Developmental themes in vascular plants: functional and evolutionary significance. In Experimental and molecular approaches to plant biosystematics, eds. P. C. Hoch and A. D. Stephenson, pp. 111–145. St. Louis: Missouri Botanical GardenGoogle Scholar
  38. Karafit, S. J., Rothwell, G. W., Stockey, R. A., and Nishida, H. 2006. Evidence for sympodial vascular architecture in a filicalean fern rhizome: Dickwhitea allenbyensis gen. et sp. nov. (Athyriaceae). International Journal of Plant Science 167:721–727.CrossRefGoogle Scholar
  39. Kato, M., and Imaichi, R. 1997. Morphological diversity and evolution of vegetative organs in pteridophytes. in Evolution and diversification of land plants, eds. K. Iwatsuki and P. H. Raven, pp. 27–43. Tokyo: SpringerGoogle Scholar
  40. Kato, M., Takahashi, A., and Imaichi, R. 1988. Anatomy of the axillary bud of Helminthostachys zeylanica (Ophioglossaceae) and its systematic implications. Botanical Gazette 149:57–63.CrossRefGoogle Scholar
  41. Kenrick P., and Crane, P.R. 1997. The origin and early diversification of land plants. A cladistic study. Washington, DC: Smithsonian Institution PressGoogle Scholar
  42. Kofuji, R., and Yamaguchi, K. 1997. Phylogenetic analysis of MADS genes from the fern Ceratopteris richardii. Journal of Phytogeography and Taxonomy 45:83–91.Google Scholar
  43. Lu, P., and Jernstedt, J. A. 1996. Rhizophore and root development in Selaginella martensii: meristem transitions and identity. International Journal of Plant Sciences 157:180–194.CrossRefGoogle Scholar
  44. Menand, B., Yi, K., Jouannic, S., Hoffmann, L., Ryan, E., Linstead, P., Schaefer, D. G., and Dolan, L. 2007. An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316:1477–1480.CrossRefPubMedGoogle Scholar
  45. Munster, T., Pahnke, J., Di Rosa, A., Kim, J. T., Martin, W., Saedler, H., and Theissen, G. 1997. Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proceedings of the National Academy of Sciences USA 94:2415–2420.CrossRefPubMedGoogle Scholar
  46. Munster, T., Faigl, W., Saedler, H., and Theissen, G. 2002. Evolutionary aspects of MADS-box genes in the eusporangiate fern Ophioglossum. Plant Biology 4:474–483.CrossRefGoogle Scholar
  47. Ogura, Y. 1972. Comparative anatomy of vegetative organs of the pteridophytes. Berlin: Gebruder BorntraegerGoogle Scholar
  48. Paolillo, D. J. 1963. The developmental anatomy of Isoetes. Urbana: University of Illinois PressGoogle Scholar
  49. Petry, L. C. 1915. Branching in the Ophioglossaceae. Botanical Gazette 59:345–365.CrossRefGoogle Scholar
  50. Phillips, T. L. 1979. Reproduction of heterosporous arborescent lycopods in the Mississippian-Pennsylvanian of Euramerica. Review of Palaeobotany and Palynology 27:239–289.CrossRefGoogle Scholar
  51. Prigge, M. J., and Clark, S. E. 2006. Evolution of the class III HD-Zip gene family in land plants. Evolution and Development 8:350–361.CrossRefGoogle Scholar
  52. Pryer, K. M., Schneider, H., Smith, A. R., Cranfill, R., Wolf, P. G., Hunt, J. S., and Sipes, S. D. 2001. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–622.CrossRefPubMedGoogle Scholar
  53. Rothwell, G. W. 1999. Fossils and ferns in the resolution of land plant phylogeny. Botanical Review 65:188–218.CrossRefGoogle Scholar
  54. Rothwell, G. W., and Erwin, D. M. 1985. The rhizomorph apex of Paurodendron: implications for homologies among the rooting organs of Lycopsida. American Journal of Botany 72:86–98.CrossRefGoogle Scholar
  55. Rothwell, G. W., and Karrfalt, E. E. 2008. Growth, development, and systematics of ferns: does Botrychium s.l. (Ophioglossales) really produce secondary xylem? American Journal of Botany 95:414–423.CrossRefGoogle Scholar
  56. Rothwell, G. W., and Nixon, K. C. 2006. How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes? International Journal of Plant Sciences 167:737–749.CrossRefGoogle Scholar
  57. Rothwell, G. W., and Stockey, R. A. 1989. Fossil Ophioglossales in the Paleocene of western North America. American Journal of Botany 76:637–644.CrossRefGoogle Scholar
  58. Rothwell, G. W., Scheckler, S. E., and Gillespie, W. H. 1989. Elkinsia gen. nov., a late Devonian gymnosperm with cupulate ovules. Botanical Gazette 158:170–189.CrossRefGoogle Scholar
  59. Rothwell, G. W., Sanders, H., Wyatt, S. E., and Lev-Yadun, S. 2008. A fossil record for growth regulation: the role of auxin in wood evolution. Annals of the Missouri Botanical Garden 95:121–134.CrossRefGoogle Scholar
  60. Rychel, A. L., Peterson, K. M., and Torii, K. U. 2010. Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. Journal of Plant Research 123:275–280.CrossRefPubMedGoogle Scholar
  61. Sanders, H., Rothwell, G. W., and Wyatt, S. E. 2009. Key morphological alterations in the evolution of leaves. International Journal of Plant Sciences 170:860–868.CrossRefGoogle Scholar
  62. Sano, R., Juarez, C. M., Hass, B., Sakakibara, K., Ito, M., Banks, J. A., and Hasebe, M. 2005. KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not in haploid meristems. Evolution and Development 7:69–78.CrossRefGoogle Scholar
  63. Schneider, H., Smith, A. R., and Pryer, K. M. 2009. Is morphology really at odds with molecules in estimating fern phylogeny? Systematic Botany 34:455–475.CrossRefGoogle Scholar
  64. Stanich, N. A., Rothwell, G. W., and Stockey, R. A. 2009. Phylogenetic diversification of Equisetum (Equisetales) as inferred from Lower Cretaceous species of British Columbia, Canada. American Journal of Botany 96:1–12.CrossRefGoogle Scholar
  65. Steeves, T. A., and Sussex, I. M. 1989. Patterns in plant development. 2nd edn. Cambridge: Cambridge University PressCrossRefGoogle Scholar
  66. Stewart, B. L., and Tomescu, A. M. F. 2009. Phylogenetic patterns of endodermis development across vascular plant lineages. Botanical Society of America annual meeting abstracts. Scholar
  67. Stewart, W. N., and Rothwell, G.W. 1993. Paleobotany and the evolution of plants. 2nd edn. Cambridge: Cambridge University PressGoogle Scholar
  68. Stubblefield, S. P., and Rothwell G. W. 1981. Embryogeny and reproductive biology of Bothrodendrostrobus mundus (Lycopsida). American Journal of Botany 68:625–634.CrossRefGoogle Scholar
  69. Stutzel, T., and Jaedicke, A. 2000. Verzweigung bei Schachtelhalmen. Feddes Repertorium 111:15–22.CrossRefGoogle Scholar
  70. Svensson, M. E., and Engstrom, P. 2002. Closely related MADS-box genes in club moss (Lycopodium) show broad expression patterns and are structurally similar to, but phylogenetically distinct from, typical seed plant MADS-box genes. New Phytologist 154:439–450.CrossRefGoogle Scholar
  71. Svensson, M. E., Johannesson, H., and Engstrom, P. 2000. The LAMB1 gene from the clubmoss, Lycopodium annotinum, is a divergent MADS-box gene, expressed specifically in sporogenic structures. Gene 253:31–43.CrossRefPubMedGoogle Scholar
  72. Tanabe, Y., Uchida, M., Hasebe, M., and Ito, M. 2003. Characterization of the Selaginella ­remotifolia MADS-box gene. Journal of Plant Research 116:69–73.Google Scholar
  73. Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J. T., Munster, T., Winter, K.-U., and Saedler, H. 2000. A short history of MADS-box genes in plants. Plant Molecular Biology 42:115–149.CrossRefPubMedGoogle Scholar
  74. Thompson, J. M. 1920. New stelar facts, and their bearing on the stelar theories for the ferns. Transactions of the Royal Society of Edinburgh 52:715–735.Google Scholar
  75. Tomescu, A. M. F. 2008. The endodermis: a horsetail’s tale. New Phytologist 177:291–295.PubMedGoogle Scholar
  76. Tomescu, A. M. F. 2009. Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science 14:5–12.CrossRefPubMedGoogle Scholar
  77. Tomescu, A. M. F., Rothwell, G. W., and Trivett M. L. 2008. Reiterative growth in the complex adaptive architecture of the Paleozoic (Pennsylvanian) filicalean fern Kaplanopteris clavata. Plant Systematics and Evolution 270:209–216.CrossRefGoogle Scholar
  78. Troop, J. E., and Mickel, J. T. 1968. Petiolar shoots in the dennstaedtioid and related ferns. American Fern Journal 58:64–70.Google Scholar
  79. von Guttenberg, H. 1966. Histogenese der Pteridophyten. Berlin: Gebruder BorntraegerGoogle Scholar
  80. Wardlaw, C. W. 1944. Experimental and analytical studies of pteridophytes. IV. Stelar morphology: experimental observations on the relation between leaf development and stelar morphology in species of Dryopteris and Onoclea. Annals of Botany 8:387–399.Google Scholar
  81. Wardlaw, C. W. 1946. Experimental and analytical studies of pteridophytes. VII. Stelar morphology: the effect of defoliation on the stele of Osmunda and Todea. Annals of Botany 9:97–107.Google Scholar
  82. Wardlaw, C. W. 1955. Embryogenesis in plants. London: MethuenGoogle Scholar
  83. White, R. A. 1984. Comparative development of vascular tissue patterns in the shoot apex of ferns. In Contemporary problems in plant anatomy, eds. R. A. White and W. C. Dickison, pp. 53–107. Orlando: Academic PressGoogle Scholar
  84. White, R. A., and Weidlich, W. H. 1995. Organization of the vascular system in the stems of Diplazium and Blechnum (Filicales). American Journal of Botany 82:982–991.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biological SciencesHumboldt State UniversityArcataUSA

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