Botanica Pacifica

Survey paper

Botanica Pacifica. A journal of plant science and conservation Preprint
Article first published online: 30 SEP 2015 | DOI: 10.17581/bp.2015.04208

Functional aspects of the origin and subsequent evolution of cotyledons

Dmitry D. Sokoloff 1, Paula J. Rudall 2, Richard M. Bateman 2 & Margarita V. Remizowa 1

1 Department of Higher Plants, Biological Faculty, Moscow State University, 119991 Moscow, Russia
2 Royal Botanic Gardens Kew, Richmond, Surrey, TW9 3DS, U.K.

In most seed plants, cotyledons formed within the seed act as haustorial organs, as well as playing a key role in releasing the shoot apex from the seed coat on germination. Emergence of the shoot apex often results from asymmetric intercalary growth of the cotyledon bases. This process avoids the principal spatial constraint on germination in seed plants, wherein the plumule is surrounded by cotyledons whose tips should be in contact with nutritive tissues. Cotyledons are commonly viewed as a synapomorphy of the seed-plant lineage and as the modified first leaves of a seedling. However, intercalary growth, which is crucial for the cotyledon’s role in releasing the plumule, had not yet been acquired by foliage leaves of the earliest seed plants. We explore the possibility that the program of intercalary growth in leaves first evolved in cotyledons and was subsequently recruited for foliage leaves in the seed-plant lineage. We also discuss whether early seed plants already possessed haustorial cotyledons.

Соколов Д.Д., Рудалл П.Дж., Бэйтман Р.М., Ремизова М.В. Функциональные аспекты происхождения и эволюции семядолей семенных растений. Семядоли большинства семенных растений выполняют гаусториальные функции, а также играют важную роль в высвобождении апекса побега из семени при его прорастании. Высвобождение апекса побега часто идет за счет асимметричного интеркалярного роста оснований семядолей. Этот процесс позволяет обойти ключевое пространственное ограничение при прорастании семенных растений, связанное с тем, что почечка окружена семядолями, верхушки которых связаны с питательными тканями семени. Семядоли обычно считают синапоморфией семенных растений и видоизмененными первыми листьями проростка. Однако интеркалярный рост, столь важный для роли семядолей в высвобождении почечки, еще не был приобретен листьями древнейших семенных растений. Из-за отсутствия прямых свидетельств мы обсуждаем четыре гипотетически возможных сценария происхождения семядолей. Мы рассматриваем возможность того, что интеркалярный рост впервые появился у семядолей, а затем эта программа развития распространилась и на обычные листья семенных растений. С другой стороны, возможно, что древнейшие семенные растения еще не имели гаусториальных семядолей.

Keywords: embryo development, haustorium, gymnosperms, intercalary growth, megaphyll, seed germination, spatial constraint, гаусторий, голосеменные растения, интеркалярный рост, мегафилл, прорастание семени, пространственное ограничение, развитие зародыша



Ball, E. 1956. Growth of the embryo of Ginkgo biloba under experimental conditions. I. Origin of the first root of the seedling in vitro. American Journal of Botany 43: 488–495.

Ball, E. 1959. Growth of the embryo of Ginkgo biloba under experimental conditions. III. Growth rates of root and shoot upon media absorbed through the cotyledons. American Journal of Botany 46: 130–139.

Barykina, R.P. 1971. Peculiarities of first stages of ontogeny of Podophyllum emodi Wall. and P. peltatum L. Botanicheskii Zhurnal 56: 921–931 (in Russian). [Барыкина Р.П. 1971. Особенности первых этапов онтогенеза Podophyllum emodi Wall. и P. peltatum L. // Ботанический журнал. Т. 56. С. 921–931].

Barykina, R.P. 1995. Morphological and ecological patterns of somatic evolution in the family Ranunculaceae Juss. Abstract of DSc Thesis (Biology). Moscow State University, Moscow, 46 pp. (in Russian). [Барыкина Р.П. 1995. Морфолого-экологическииие закономерности соматической эволюции в семействе лютиковых (Ranunculaceae Juss.). Автореф. дисс. … докт. биол. наук. М., 1995. 46 с.].

Bateman, R.M. & W.A. DiMichele 1994. Heterospory: the most iterative key innovation in the evolutionary history of the plant kingdom. Biological Reviews 69: 345–417. CrossRef

Bateman, R.M. & W.A. DiMichele 2002. Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited. In: Developmental genetics and plant evolution (Q.C.B. Cronk, R.M. Bateman & J.A. Hawkins, eds.), pp. 109–159, Taylor & Francis, London. CrossRef

Bauer, K., L. Grauvogel-Stamm, E. Kustatscher & M. Krings 2013. Fossil ginkgophyte seedlings from the Triassic of France resemble modern Ginkgo biloba. BMC Evolutionary Biology 13: 177. CrossRef

Beck, C.B. 1967. Eddya sullivanensis, gen. et sp. nov., a plant of gymnospermic morphology from the Upper Devonian of New York. Palaeontographica B 121: 1–22.

Bornman, C.H., V. Butler & W.A. Jensen 1979. Welwitschia mirabilis: fine structure of the germinating seed. I. Orientation. Zeitschrift für Pflanzenphysiologie 91:189–196.

Bower, F.O. 1881. On the germination and histology of the seedlings of Welwitschia mirabilis. Quarterly Journal of Microscopical Science 21: 15–30.

Bower, F.O. 1882. The germination and embryogeny of Gnetum gnemon. Quarterly Journal of Microscopical Science 87: 278–298.

Boyce, C.K. 2005. Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31: 117–140. CrossRef

Boyce, C.K. & A.H. Knoll 2002. Evolution and developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28: 70–100. CrossRef

Bulard, C. 1952. Culture aseptique d’embryons de Ginkgo biloba: Rôle des cotylédons dans l’absorption du sucre et la croissance de la tige. Comptes rendus hebdomadaires des séances de l’Académie des sciences 235: 739–741.

Burleigh, J.G. & S. Mathews 2004. Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed-plant tree of life. American Journal of Botany 91: 1599–1613. CrossRef

Butler, V., C.H. Bornman & R.F. Evert 1973. Welwitschia mirabilis: Morphology of the seedling. Botanical Gazette 134: 52–59. CrossRef

Celis, G. & G. Avalos 2013. Acclimation of seedlings of Gnetum leyboldii Tul. (Gnetaceae) to light changes in a tropical rain forest. International Journal of Tropical Biology and Conservation 61: 1859–1868.

Chamberlain, C.J. 1935. Gymnosperms. Structure and evolution. University of Chicago Press, Chicago. 484 pp.

Chandler, J.W. 2008 . Cotyledon organogenesis. Journal of Experimental Botany 59: 2917–2931. CrossRef

Crane, P.R. 1996. The fossil history of the Gnetales. International Journal of Plant Sciences 157 (Suppl.): S50–S57. CrossRef

Dilcher, D.L., M.E. Bernardes-De-Oliveira, D. Pons & T.A. Lott 2005. Welwitschiaceae from the Lower Cretaceous of northeastern Brazil. American Journal of Botany 92: 1294–1310. CrossRef

DiMichele, W.A., T.L. Phillips & H.W. Pfefferkorn 2006. Paleoecology of Late Paleozic pteridosperms from tropical Euramerica. Journal of the Torrey Botanical Society 133: 83–118. CrossRef

Dorety, H.A. 1909. Vascular anatomy of the seedling of Microcycas calocoma. Botanical Gazette 47: 139–147.

Dorety, H.A. 1919. Embryo and seedling of Dioon spinulosum. Botanical Gazette 67: 251–257.

Dörken, V.M. 2013. Morphology, anatomy and vasculature in leaves of Ginkgo biloba L. (Ginkgoaceae, Ginkgoales) under functional and evolutionary aspects. Feddes Repertorium 124: 80–97. CrossRef

Doyle, J.A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169: 816–843. CrossRef

Doyle, J.A. 2013. Phylogenetic analyses and morphological innovations in land plants. Annual Plant Reviews 45: 1–50. CrossRef

Emberger, L. 1942. Sur les Ptéridospermées et les Cordaitales. Bulletin de la Société Botanique de France 89: 202–203.

Esau, K. 1977. Anatomy of seed plants. Ed. 2. John Wiley and Sons, New York, 550 pp.

Florin, R. 1951. Evolution in cordaites and conifers. Acta Horti Bergiani 15: 285–388.

Floyd, S.K. & J.L. Bowman 2006. Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Current Biology 16: 1911–1917. CrossRef

Forbis, T.A., S.K. Floyd & A. de Queiroz 2002. The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56: 2112–2125. CrossRef

Friedman, W.E., J.B. Bachelier & J.I. Hormaza 2012. Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early-diverging flowering plants. American Journal of Botany 99: 1083–1095. CrossRef

Galtier, J. 2010. The origins and early evolution of the megaphyllous leaf. International Journal of Plant Sciences 171: 641–661. CrossRef

Gerrienne, P., B. Meyer-Berthaud, M. Fairon-Demaret, M. Streel & P. Steemans 2004. Runcaria, a Middle Devonian seed plant precursor. Science 306: 856–858. CrossRef

Gifford, E.M. & A.S. Foster 1989. Morphology and evolution of vascular plants, 3rd ed. W. Freeman, New York, 626 pp.

Goebel, K. 1905. Organography of plants. Authorized English edition. Part 2. Clarendon Press, Oxford. 707 pp.

Goebel, K. 1932. Organographie der Pflanzen. Aufl. 3. Fischer, Jena. 1820 S.

Graham, L.E., M.E. Cook & J.S. Busse 2000. The origin of plants: Body plan changes contributing to a major evolutionary radiation. Proceedings of the National Academy of Sciences, USA 97: 4535–4540. CrossRef

Graham, L.K.E. & L.W. Wilcox 2000. The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport. Philosophical Transactions of the Royal Society of London B 355: 757–767. CrossRef

Graham, S.W. & W.J.D. Iles 2009. Different gymnosperm outgroups have (mostly) congruent signal regarding the root of flowering plant phylogeny. American Journal of Botany 96: 216–227. CrossRef

Groff, P.A. & D.R. Kaplan 1988. The relation of root systems to shoot systems in vascular plants. Botanical Review 54: 387–422. CrossRef

Grushvitzky, I.V. 1963. Subterranean germination and the functions of cotyledons. Botanicheskii Zhurnal 48: 906–915 (in Russian). [Грушвицкий И.В. 1963. Подземное прорастание и функции семядолей // Ботанический журнал. Т. 48, № 6. С. 906–915].

Guttenberg, H. von 1966. Histogenese der Pteridophyten. 312 S. In: Encyclopedia of plant anatomy. Traite d’Anatomie Vegetale. Ed. 2, (W. Zimmermann & P. Ozenda, eds.), Band 7. Teil 2. Spezieller Teil.

Haccius, B. 1952. Verbreitung und Ausbildung der Einkeimblättrigkeit bei den Umbelliferen. Österreichische Botanische Zeitschrift 99: 483–505.

Haccius, B. 1953. Histogenetische Untersuchungen an Wurzelhaube und Kotyledonarscheide geophiler Keimpflanzen (Podophyllum und Eranthis). Planta 41: 439–458.

Haines, R.W. & K.A. Lye 1979. Monocotylar seedlings: a review of evidence supporting an origin by fusion. Botanical Journal of the Linnean Society 78: 123–140.

Harrison, C.J., S.B. Corley, E.C. Moylan, D.L. Alexander, R.W. Scotland & J.A. Langdale 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434: 509–514. CrossRef

Hilton, J. 1998. Review of the fossil evidence for the origin and earliest evolution of the seed-plants. Acta Botanica Sinica 40: 981–987.

Hilton, J. & R.M. Bateman 2006. Pteridosperms are the backbone of seed plant evolution. Journal of the Torrey Botanical Society 133: 119–168. CrossRef

Johansson, M. & B. Walles 1994. Functional anatomy of the ovule in broad bean (Vicia faba L.): ultrastructural seed development and nutrient pathways. Annals of Botany 74: 233–244. CrossRef

Kaplan, D.R. & T.J. Cooke 1997. Fundamental concepts in the embryogenesis of Dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9: 1903–1919. CrossRef

Kenrick, P. 2002. The telome theory. In: Developmental genetics and plant evolution (Q.C.B. Cronk, R.M. Bateman & J.A. Hawkins, eds.), pp. 365–387. Taylor & Francis, London. CrossRef

Kenrick, P. & P.R. Crane 1997. The origin and early diversification of land plants: a cladistic study (Smithsonian Series in Comparative Evolutionary Biology). Smithsonian Institution, Washington, DC, 441 pp.

Krassilov, V.A. 1972. Mesozoic flora of the river Bureya (Ginkgoales and Czekanowskiales). Nauka, Moscow, 151 pp. (in Russian). [Красилов В.А. 1972. Мезозойская флора реки Бурея (Ginkgoales и Czekanowskiales). Москва: Наука. 151 с.].

Krassilov, V.A. 1989. Origin and early evolution of flowering plants. Nauka, Moscow, 264 pp. (in Russian). [Красилов В.А. 1989. Происхождение и ранняя эволюция цветковых растений. Москва: Наука. 264 с.].

Krassilov, V.A. 1997. Angiosperm origins: morphological and ecological aspects. Pensoft Publishers, Sofia, 270 pp.

Krassilov, V.A. 2009. Diversity of Mesozoic gnetophytes and the first angiosperms. Paleontological Journal 43: 1272–1280. CrossRef

Ligrone, R., J.G. Duckett & K.S. Renzaglia 1993. The gametophyte-sporophyte junction in land plants. Advances in Botanical Research 19: 231–317. CrossRef

Linkies, A., K. Graebner, C. Knight & G. Leubner-Metzger 2010. The evolution of seeds. New Phytologist 186: 817–831. CrossRef

Lodkina, M.M. 1988. Evolutionary relations between mono- and dicotyledons based on embryo and seedling study. Botanicheskii Zhurnal 73: 617–628 (in Russian.) [Лодкина М.М. 1988. Эволюционные отношения однодольных и двудольных по данным изучения зародыша и проростков // Ботанический журнал. Т. 73, № 5. С. 617–628].

Long, A.G. 1975. Further observations on some Lower Carboniferous seeds and cupules. Transactions of the Royal Society of Edinburgh B 69: 267–293. CrossRef

Lyon, H.L. 1902. The phylogeny of cotyledons. Postelsia: the yearbook of the Minnesota Seaside Station 1901: 56–86.

Mapes, G., G.W. Rothwell & M.T. Haworth 1989. Evolution of seed dormancy. Nature 337: 645–646. CrossRef

Marshall, J.E.A. & A.R. Hemsley 2003. A Mid Devonian seed-megaspore from East Greenland and the origin of the seed plants. Palaeontology 46: 647–670. CrossRef

Mathews, S. 2009. Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. American Journal of Botany 96: 228–236. CrossRef

Mestre, J.-C. & M. Guédès 1983. Nature et signification phylogénétique du cotyledon. Bulletin de la Société Botanique de France. Actualités Botaniques 130: 7–22. CrossRef

Meyen, S.V. 1987. Fundamentals of palaeobotany. Chapman & Hall, N.Y. CrossRef

Meyer, K.I. 1958. Morphogeny of higher plants. Moscow University Press, Moscow, 254 pp. (in Russian). [Мейер К.И. 1958. Морфогения высших растений. Москва: Издательство Московского университета. 254 с.].

Niklas, K.J. 2008. Embryo morphology and seedling evolution. In: Seedling ecology and evolution (M.A. Leck, V.T. Parker & R.L. Simpson, eds.), pp. 103–129, Cambridge University Press, Cambridge. CrossRef

Niklas, K.J. & U. Kutschera 2009. The evolutionary development of plant body plans. Functional Plant Biology 36: 682–695. CrossRef

Pant, D.D. & D.D. Nautiyal 1987. Diphyllopteris verticillata Srivastava, the probable seedling of Glossopteris from the Palaeozoic of India. Review of Palaeobotany and Palynology 51: 31–36. CrossRef

Pearson, H.H.W. 1929. Gnetales. Cambridge University Press, Cambridge, 194 pp.

Pettitt, J.M. & C.B. Beck 1968. Archaeosperma arnoldii – a cupulate seed from the Upper Devonian of North America. Contributions from the Museum of Paleontology, the University of Michigan 22: 139–154.

Prestianni, C. & P. Gerrienne 2010. Early seed plant radiation: an ecological hypothesis. Geological Society, London, Special Publications 33: 71–80. CrossRef

Raven, J.E. 1999. The minimum size of seeds and spores in relation to the ontogeny of homoiohydric plants. Functional Ecology 13: 5–14. CrossRef

Rothwell, G.W. & S.E. Scheckler 1988. Biology of ancestral gymnosperms. In: Origin and evolution of the gymnosperms (C.B. Beck, ed.), pp. 85–134, Columbia University Press, New York.

Rothwell, G.W., S.E. Scheckler & W.H. Gillespie 1989. Elkinsia gen. nov., a Late Devonian gymnosperm with cupulate ovules. Botanical Gazette 150: 170–189. CrossRef

Rudall, P.J. & R.M. Bateman 2007. Developmental bases for key innovations in the seed-plant microgametophyte. Trends in Plant Science 12: 317–326. CrossRef

Rydin, C., B. Mohr & E.M. Friis 2003. Cratonia cotyledon gen. et sp. nov.: a unique Cretaceous seedling related to Welwitschia. Proceedings of the Royal Society of London B (Suppl.) 270: S29–S32. CrossRef

Sachs, J. 1863. Über die Keimung des Samens von Allium cepa. Botanische Zeitung 21: 57–62, 65–70.

Sanders, H., G.W. Rothwell & S.E. Wyatt 2009. Morphological alterations in the evolution of leaves. International Journal of Plant Sciences 170: 860–868. CrossRef

Scatizzi, A. 1937. Ricerche sulla germinazione di Ephedra altissima. Nuovo Giornale botanico italiano (Nuova serie) 44: 345–375.

Schneckenburger, S. 1993. Embryology and germination in gymnosperms. Academia Nacional De Ciencias (Córdoba, Argentina). Miscelanea 91: 1–22.

Seward, A.C. & S.O. Ford 1906. The Araucarieae, recent and extinct. Philosophical Transactions of the Royal Society of London, B 198: 305–411. CrossRef

Siegert, A. 1989. Zur Phylogenie der Wurzel. Teil 1. Die Radicula. Koeltz Scientific Books, Königstein. 105 S.

Sokoloff, D.D., M.V. Remizowa, A.S. Beer, S.R. Yadav, T.D. Macfarlane, M.M. Ramsay & P.J. Rudall 2013. Impact of spatial constraints during seed germination on the evolution of angiosperm cotyledons: a case study from tropical Hydatellaceae (Nymphaeales). American Journal of Botany 100: 824–843. CrossRef

Sokoloff, D.D., M.V. Remizowa, J.G. Conran, T.D. Macfarlane, M.M. Ramsay & P.J. Rudall 2014. Embryo and seedling morphology in Trithuria lanterna (Hydatellaceae, Nymphaeales): new data for infrafamilial systematics and a novel type of syncotyly. Botanical Journal of the Linnean Society 174: 551–573. CrossRef

Spurr, A.R. 1949. Histogenesis and organization of the embryo in Pinus strobus L. American Journal of Botany 36: 629–641. CrossRef

Stidd, B.M. & K. Cosentino 1976. Nucellangium: gametophytic structure and relationship to cordaites. Botanical Gazette 137: 242–249. CrossRef

Stockey, R.A. 1975. Seeds and embryos of Araucaria mirabilis. American Journal of Botany 62: 856–868. CrossRef

Stockey, R.A. 1977. Reproductive biology of the Cerro Cuadrado (Jurassic) fossil conifers: Pararaucaria patagonica. American Journal of Botany 64: 733–744. CrossRef

Stockey, R.A. & T.N. Taylor 1978. On the structure and evolutionary relationships of the Cerro Cuadrado fossil conifer seedlings. Botanical Journal of the Linnean Society 76: 161–176. CrossRef

Takhtajan, A. 1991. Evolutionary trends in flowering plants. Columbia University Press, New York, 241 pp.

Taylor T.N., E.L. Taylor & M. Krings 2009. Paleobotany: the biology and evolution of fossil plants. Elsevier, Amsterdam. 1230 pp.

Tillich, H.-J. 1990. Die Keimpflanzen der Nymphaeaceae – monocotyl oder dicotyl? Flora 184: 169–176.

Tillich, H.-J. 1995. Seedlings and systematics in monocotyledons. In: Monocotyledons: systematics and evolution (P.J. Rudall, P.J. Cribb, D.F. Cutler & C.J. Humphries, eds.), pp. 303–352. Royal Botanic Gardens, Kew.

Tillich, H.-J. 2007. Seedling diversity and the homologies of seedling organs in the order Poales (Monocotyledons). Annals of Botany 100: 1413–1429. CrossRef

Timonin, A.C. 1989. On the root lateral branching. Bulleten' Moskovskogo obshchestva ispytatelei prirody. Otdel biol. 94(6): 38–48 (in Russian). [Тимонин А.К. 1989. О боковом ветвлении корней // Бюллетень МОИП. Отдел биол. Т. 94, № 6. С. 38–48].

Titova, G.E. 2006. Variations in cotyledon apparatus development. In: Embryology of flowering plants: Terminology and concepts, vol. 2, Seed, (T.B. Batygina, ed.), pp. 230–258, Science Publishers, Enfield & Plymouth.

Tzvelev, N.N. 2000. Embryos of Magnoliophyta as primary phytomers. Bulleten' Moskovskogo obshchestva ispytatelei prirody. Otdel biol. 105(4): 60–64 (in Russian). [Цвелев H.H. 2000. Зародыши семян покрытосеменных растений (Magnoliophyta) как первичные фитомеры // Бюллетень МОИП. Отдел биол. Т. 105, вып. 4. С. 60–64].

Tomescu, A.M.F. 2009. Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science 14: 5–12. CrossRef

Troll, W. 1943. Vergleichende Morphologie der höheren Pflanzen. Band 1. Teil 3. Borntraeger, Berlin.

Vasilchenko, I.T. 1937. A remarkable case of seed germination in Ephedra ciliata C.A.M. Priroda 26(3): 95–97 (in Russian). [Васильченко И.Т. 1937. Замечательный случай прорастания семян эфедры (Ephedra ciliata C.A.M.) // Природа. № 3. С. 95-97].

Vasilchenko, I.T. 1960. Seedlings of trees and shrubs (a manual). Izdatel'stvo Akademii nauk SSSR, Moscow, Leningrad, 302 pp. (in Russian). [Васильченко И.Т. 1960. Всходы деревьев и кустарников. Определитель. М.; Л.: Издательство Академии наук СССР. 302 с.].

Ye, N.-G., G.-Q. Gou, H.-M. Liao & Z.-L. Zhang 1993. The seedling types of gymnosperms and their evolutionary relationships. Acta Phytotaxonomica Sinica 31: 505–516.

Zhou, Z.-Y. 2009. An overview of fossil Ginkgoales. Palaeoworld 18: 1–22. CrossRef

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