Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T14:28:15.036Z Has data issue: false hasContentIssue false

Relationship of the lateral embryo (in grasses) to other monocot embryos: a status up-grade

Published online by Cambridge University Press:  18 October 2021

Carol C. Baskin*
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY40506-0225, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY40506-0312, USA
Jerry M. Baskin
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY40506-0225, USA
*
*Author for Correspondence: Carol C. Baskin, E-mail: carol.baskin@uky.edu

Abstract

Martin placed the lateral embryo, which occurs only in grasses, adjacent to the broad embryo at the base of his family tree of seed phylogeny. Since Poales and Poaceae are derived monocots, we questioned the evolutionary relationship between the lateral embryo and other kinds of monocot embryos. Information was compiled on embryo and seed characteristics for the various families of monocots, kind of embryogenesis for families in Poales and germination morphology of families with lateral (only Poaceae) and broad embryos. The kinds of monocot embryos are broad, capitate, lateral, linear fully developed, linear underdeveloped and undifferentiated, but only broad and lateral embryos are restricted to Poales. Asterad embryogenesis occurs in Poaceae with a lateral embryo and in Eriocaulaceae, Rapataceae and Xyridaceae with a broad embryo. In developing grass seeds, the growing scutellum (cotyledon) pushes the coleoptile, mesocotyl and coleorhiza to the side. In the organless broad embryo, the cotyledonary sector is larger than the epicotyledonary sector. During germination of grass seeds, the coleorhiza and then the coleoptile emerge, while in a seed with a broad embryo the elongating cotyledon pushes the epicotyledonary sector outside the seed, after which a root–shoot axis is differentiated at a right angle to the cotyledon inside the seed. Broad and lateral embryos are closely related; however, the lateral embryo is more advanced in seed/embryo traits and germination morphology than the other kinds of monocot embryos, suggesting that its position on the family tree of seed phylogeny should be higher than of the other monocot embryos.

Type
Review Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andrews, M, Douglas, A, Jones, AV, Milburn, CE, Porter, C and McKenzie, BA (1997) Emergence of temperate pasture grasses from different sowing depths: importance of seed weight, coleoptile plus mesocotyl length and shoot strength. Annals of Applied Biology 130, 549560.CrossRefGoogle Scholar
Arber, A (1920) Water plants. A study of aquatic angiosperms. Cambridge, Cambridge University Press.Google Scholar
Arber, A (1925) Monocotyledons. A morphological study. Cambridge, Cambridge University Press.Google Scholar
Arekal, GD and Ramaswamy, SN (1980) Embryology of Eriocaulon hookerianum Stapf and the systematic position of Eriocaulaceae. Botaniska Notiser 133, 295309.Google Scholar
Avery, G Jr. (1930) Comparative anatomy and morphology of embryos and seedlings of maize, oats, and wheat. Botanical Gazette 89, 139.CrossRefGoogle Scholar
Baskin, CC and Baskin, JM (2018) Resolving the puzzle of Martin's broad embryo: a solution based on morphology, taxonomy and phylogeny. Perspectives in Plant Ecology, Evolution and Systematics 34, 6167.CrossRefGoogle Scholar
Baskin, JM, Hidayati, SN, Baskin, CC, Walck, JL, Huang, Z-Y and Chien, C-T (2006) Evolutionary considerations of the presence of both morphophysiological and physiological seed dormancy in the highly advanced euasterids II order Dipsacales. Seed Science Research 16, 233242.CrossRefGoogle Scholar
Becraft, PW (2007) Aleurone cell development. Plant Cell Monographs 8, 4556.CrossRefGoogle Scholar
Becraft, PW and Yi, G (2011) Regulation of aleurone development in cereal grains. Journal of Experimental Botany 62, 16691675.CrossRefGoogle ScholarPubMed
Begum, M (1968) Embryological studies in Eriocaulon quinquangulare Linn. Proceedings of the Indian Academy of Sciences A 67, 148156.CrossRefGoogle Scholar
Belzunce, M, Navarro, RM and Rapoport, HF (2005) Seed and early plantlet structure of the Mediterranean seagrass Posidonia oceanica. Aquatic Botany 82, 269283.CrossRefGoogle Scholar
Bessey, CE (1915) The phylogenetic taxonomy of flowering plants. Annals of the Missouri Botanical Garden 2, 109164.CrossRefGoogle Scholar
Bose, A and Paria, ND (2015) Seed and seedling morphology of Cheilocostus specious (Costaceae). Phytomorphology 65, 109113.Google Scholar
Bouchenak-Khelladi, Y, Muasya, AM and Linder, HP (2014) A revised evolutionary history of Poales: origins and diversification. Botanical Journal of the Linnean Society 175, 416.CrossRefGoogle Scholar
Boyd, L (1931) Evolution in the monocotyledonous seedling: a new interpretation of the morphology of the grass embryo. Transactions of the Botanical Society of Edinburgh 30, 286303.CrossRefGoogle Scholar
Brown, WV (1960) The morphology of the grass embryo. Phytomorphology 10, 215223.Google Scholar
Buttrose, MS (1963) Ultrastructure of the developing aleurone cells of wheat grain. Australian Journal of Biological Sciences 16, 768774.CrossRefGoogle Scholar
Caye, G and Meinesz, A (1986) Experimental study of seed germination in the seasgrass Cynodocea nodosa. Aquatic Botany 26, 7987.CrossRefGoogle Scholar
Chandler, J, Nardmann, J and Werr, W (2007) Plant development revolves around axes. Trends in Plant Science 13, 7884.CrossRefGoogle Scholar
Cheng, J, Khan, MA, Qiu, W-M, Li, J, Zhou, H, Zhang, Q, Guo, W, Zhu, T, Peng, J, Sun, F, Li, S, Korban, SS and Han, Y (2012) Diversification of genes encoding granule-bound starch synthase in monocots and dicots is marked by multiple genome-wide duplications events. PLoS One 7, e30088.Google Scholar
Clarke, B (1859) On the embryos of endogens and their germination. Transactions of the Linnean Society of London 22, 401419. +1 plate.CrossRefGoogle Scholar
Cocucci, AE and Astegiano, ME (1978) Interpretacion del embrion de las Poaceas. Kurtziana 11, 4154.Google Scholar
Corredor, BAD, Escobar, DFE and Scatena, VL (2015) Morfologia de semillas y Desarrollo post-seminal de especies de Comanthera (Eriocaulaceae). Revista de Biologia Tropical 63, 11271135.CrossRefGoogle Scholar
Coulter, JM (1915) The origin of monocotyledony. II. Monocotyledony in grasses. Annals of the Missouri Botanical Garden 2, 175183.CrossRefGoogle Scholar
Cronquist, A (1968) The evolution and classification of flowering plants. Boston, MA, Houghton Mifflin.Google Scholar
Dahlgren, RMT and Clifford, HT (1982) The monocotyledons: a comparative study. London, Academic Press.Google Scholar
Dahlgren, R and Rasmussen, FN (1983) Monocotyledon evolution. Characters and phylogenetic estimation, pp. 255395 in Hecht, MK; Wallace, B; and Prance, GT (Eds) Evolutionary biology, vol. 16. New York, Plenum Press.CrossRefGoogle Scholar
Dahlgren, RMT, Clifford, HT and Yeo, PF (1985) The families of the monocotyledons. Structure, evolution and taxonomy. Berlin, Springer-Verlag.CrossRefGoogle Scholar
De Jussieu, A (1839) Sur les embryons monocotyledones. Annales des Sciences Naturelles: Botanique 11, 341361.Google Scholar
Deshpande, PK (1976) Development of embryo and endosperm in Eragrostis unioloides (Poaceae). Plant Systematics and Evolution 125, 253259.CrossRefGoogle Scholar
Duvall, MR, Learn, GH Jr., Eguiarte, LE and Clegg, MT (1993) Phylogenetic analysis of rbcL sequences identifies Acorus calamus as the primal extant monocotyledon. Proceedings of the National Academy of Sciences of the United States of America 90, 46414644.CrossRefGoogle ScholarPubMed
Eichemberg, MT and Scatena, VL (2013) Morphology and anatomy of the diaspores and seedling of Paspalum (Poaceae, Poales). Anais da Academia Brasileira de Ciências 85, 13891396.CrossRefGoogle Scholar
Fernando, DD and Cass, DD (1996) Development and structure of ovule, embryo sac, embryo, and endosperm in Butomus umbellatus (Butomaceae). International Journal of Plant Sciences 157, 269279.CrossRefGoogle Scholar
Gibbs, RE (1902) Phyllospadix as a beach-builder. The American Naturalist 36, 101109.CrossRefGoogle Scholar
Givnish, TJ, Ames, M, McNeal, JR, McKain, MR, Steele, PR, dePamphilis, CW, Graham, SW, Pires, JC, Stevenson, DW, Zomlefer, WB, Briggs, BG, Duvall, MR, Moore, MJ, Heaney, JM, Soltis, DE, Soltis, PS, Thiele, K and Leebens-Mack, JH (2010) Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales. Annals of the Missouri Botanical Garden 97, 584616.CrossRefGoogle Scholar
Givnish, TJ, Zuluaga, A, Spalink, D, Gomez, MS, Lam, VKY, Saarela, JM, Sass, C, Iles, WJD, de Sousa, DJL, Leebens-Mack, J, Pires, JC, Zomlefer, WB, Gandolfo, MA, Davis, JI, Stevenson, DW, dePamphilis, C, Specht, C, Graham, SW, Barrett, CF and Ané, C (2018) Monocot plastic phylogenomics, timeline, net rates of species diversification, the power of multi-gene analyses, and a functional model for the origin of monocots. American Journal of Botany 105, 18881910.CrossRefGoogle Scholar
Goebel, K (1905) Organography of plants, especially of the archegoniatae and spermophyta. Oxford, Clarendon Press.Google Scholar
Grayum, MH (1987) A summary of evidence and arguments supporting the removal of Acorus from the Araceae. Taxon 36, 723729.CrossRefGoogle Scholar
Grushvitzky, IV (1967) After-ripening of seeds of primitive tribes of angiosperms, conditions and peculiarities, pp. 329336+8 figures in Borriss, H (Ed) Physiologie, Okologie und Biochemie der Keimung. Greifswald, Ernst-Moritz-Arndt Universitat.Google Scholar
Guignard, JL (1975) Du cotylédon des monocotylédons. Phytomorphology 25, 193200.Google Scholar
Guignard, JL and Mestre, JC (1970) L'embryon des graminees. Phytomorphology 20, 190197.Google Scholar
Hare, CL (1950) The structure and development of Eriocaulon spetangulare with. Journal of the Linnean Society of London Botany 53, 422448.CrossRefGoogle Scholar
Hochbach, A, Linder, HP and Röser, M (2018) Nuclear genes, matK and the phylogeny of the Poales. Taxon 67, 521536.CrossRefGoogle Scholar
Hutchinson, J (1926) The families of flowering plants. I. Dicotyledons. London, Macmillan and Company.CrossRefGoogle Scholar
Itoh, J-I, Nonomura, K-I, Ikeda, K, Yamaki, S, Inukai, Y, Yamagishi, H, Kitano, H and Nagato, Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiology 46, 2347.CrossRefGoogle ScholarPubMed
Johansen, DA (1950) Plant embryology. Embryology of the spermatophyta. Waltham, MA, Chronica Botanica Company.Google Scholar
Johri, BM, Ambegaokar, KB and Srivastava, PS (1992) Comparative embryology of angiosperms, vols. 1 and 2. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Juguet, M (1993) Origin and stages of monocotyly in the Monocotyledons. II – Stages of monocotylyl. Acta Botanica Gallica 140, 479496.CrossRefGoogle Scholar
Kellogg, EA (2000) The grasses: a case study in macroevolution. Annual Review of Ecology and Systematics 31, 217238.CrossRefGoogle Scholar
Kubitzki, K (ed) (1998) The families and genera of vascular plants. Flowering plants. Monocotyledons, vols. III and IV. Berlin, Springer.Google Scholar
Kuo, J and Kirkman, H (1992) Fruits, seeds and germination in the seagrass Halophila ovalis (Hydrocharitaceae). Botanica Marina 35, 197204.CrossRefGoogle Scholar
Kuo, J, Long, WL and Coles, RG (1993) Occurrence and fruit and seed biology of Halophila tricostata Greenway (Hydrocharitaceae). Australian Journal of Freshwater Research 44, 4357.CrossRefGoogle Scholar
Li, C, Li, Q-G, Dunwell, JM and Zhang, Y-M (2012) Divergent evolutionary pattern of starch biosynthetic pathway genes in grasses and dicots. Molecular Biology and Evolution 29, 32273236.CrossRefGoogle ScholarPubMed
Li, J and Berger, F (2012) Endosperm: food for humankind and fodder for scientific discoveries. New Phytologist 195, 290305.CrossRefGoogle ScholarPubMed
Linder, HP (1987) The evolutionary history of the Poales/Restionales – a hypothesis. Kew Bulletin 42, 297318.CrossRefGoogle Scholar
Linder, HP and Rudall, PJ (2005) Evolutionary history of Poales. Annual Review of Ecology, Evolution and Systematics 36, 107124.CrossRefGoogle Scholar
Maheshwari, P (1950) An introduction to the embryology of angiosperms. New York, McGraw-Hill.CrossRefGoogle Scholar
Martin, AC (1946) The comparative internal morphology of seeds. The American Midland Naturalist 36, 513660.CrossRefGoogle Scholar
Martins, AR, Pütz, N, Novembre, ADLC, Piedade, SMS and Glória, BA (2011) Seed germination and seedling morphology of Smilax polyantha (Smilaceaceae). Biota Neotropica 11, 3137.CrossRefGoogle Scholar
Mas, MT and Verdú, MC (2016) Mesocotyl elongation in Digitaria sanguinalis during seedling development. Plant Biosystems 150, 11751181.CrossRefGoogle Scholar
McKain, MR, Tang, H, McNeal, JR, Ayyampalayam, S, Davis, JI, dePamphilis, CW, Givnish, TJ, Pires, JC, Stevenson, DW and Leebens-Mack, JH (2016) A phylogenomic assessment of ancient polyploidy and genome evolution across the Poales. Genome Biology and Evolution 8, 11501164.Google ScholarPubMed
McMillan, C (1981) Seed reserves and seed germination for two seagrasses, Halodule wrightii and Syringodium filiforme, from the western Atlantic. Aquatic Botany 11, 279296.CrossRefGoogle Scholar
Michelangeli, FA, Davis, JI and Stevenson, DW (2003) Phylogenetic relationships among Poaceae and related families as inferred from morphology, inversions in the plastid genome, and sequence data from the mitochondrial and plastid genomes. American Journal of Botany 90, 93106.CrossRefGoogle ScholarPubMed
Monteiro-Scanavacca, WR and Mazzoni, SC (1978) Embryological studies in Leiothrix fluitans (Mart.) Ruhl. (Eriocaulaceae). Revista Brasileira de Botanica 1, 5964.Google Scholar
Nardmann, J, Zimmermann, R, Durantini, D, Kranz, E and Werr, W (2007) WOX gene pathway in Poaceae: a comparative approach addressing leaf and embryo development. Molecular Biology and Evolution 24, 24742484.CrossRefGoogle Scholar
Natesh, S and Rau, MA (1984) The embryo, pp. 377443 in Johri, BM (Ed) Embryology of angiosperms, Berlin, Springer-Verlag.CrossRefGoogle Scholar
Niu, L, Hao, R, Wu, X and Wang, W (2020) Maize mesocotyl: role in response to stress and deep-sowing tolerance. Plant Breeding 139, 466473.CrossRefGoogle Scholar
Patel, CM and Patel, DS (1964) The morphological and embryological studies in Eriocaulon cinereum R. Br.Vidya 7, 5870.Google Scholar
Pereira, TS (1987) Commelinaceae: estudo do desenvolvimento pos-seminal de algumas especies. Acta Biologica Leopoldensia 9, 4980.Google Scholar
Radoeva, T, Vaddepalli, P, Zhang, Z and Weijer, D (2019) Evolution, initiation, and diversity in early plant embryogenesis. Developmental Cell 50, 533543.CrossRefGoogle ScholarPubMed
Raju, MVS and Steeves, TA (1998) Growth, anatomy and morphology of the mesocotyl and the growth of appendages of the wild oat (Avena fatua L.) seedling. Journal of Plant Research 111, 7385.CrossRefGoogle Scholar
Ramaswamy, SN and Arekal, GD (1981) Embryology of Eriocaulon setaceum (Eriocaulaceae). Plant Systematics and Evolution 138, 175188.CrossRefGoogle Scholar
Ramaswamy, SN and Arekal, GD (1982a) On the embryology of three taxa of Paepalanthoideae (Eriocaulaceae). Annals of Botany 49, 99102.CrossRefGoogle Scholar
Ramaswamy, SN and Arekal, GD (1982b) Embryology of Eriocaulon xeranthemum Mart. (Eriocaulaceae). Acta Botanical Neerlandica 31, 4154.CrossRefGoogle Scholar
Ramaswamy, SN, Swamy, BGL and Govindappa, DA (1981) From zygote to seedlings in Eriocaulon robusto-brownianum Ruhl. (Eriocaulaceae). Beiträge zur Biologie der Pflanzen 55, 179188.Google Scholar
Reeder, JR (1957) The embryo in grass systematics. American Journal of Botany 44, 756768.CrossRefGoogle Scholar
Ritchie, S, Swanson, SJ and Gilroy, S (2000) Physiology of the aleurone layer and starchy endosperm during grain development and early seedling growth: new insights from cell and molecular biology. Seed Science Research 10, 193212.CrossRefGoogle Scholar
Rudall, PJ and Sajo, MG (1999) Systematic position of Xyris: flower and seed anatomy. International Journal of Plant Sciences 160, 795808.CrossRefGoogle Scholar
Rudall, PJ, Stuppy, W, Cunniff, J, Kellogg, EA and Briggs, BG (2005) Evolution of reproductive structures in grasses (Poaceae) inferred by sister-group comparison with their putative closest living relatives, Ecdeiocoleaceae. American Journal of Botany 92, 14321443.CrossRefGoogle ScholarPubMed
Scatena, VL, Menezes, NL and Stützel, T (1993) Embryology and seedling development in Syngonanthus rufipes Silveira (Eriocaulaceae). Beiträge zur Biologie der Pflanzen 67, 333343.Google Scholar
Schleiden, MJ (1839) Sur la formation de l'ovule et l'origine de l'embryon dans les phanerogames. Annales des Sciences Naturelle Botanique II 11, 129141.Google Scholar
Shuma, JM and Raju, MVS (1991) Is the wild oat embryo monocotylous? Botanical Magazine of Tokyo 104, 1523.CrossRefGoogle Scholar
Simão, DG, Scatena, VL and Bouman, F (2006) Developmental anatomy and morphology of the ovule and seed of Heliconia (Heliconiaceae, Zingiberales). Plant Biology 8, 143154.CrossRefGoogle Scholar
Smith, RW (1910) The floral development and embryogeny of Eriocaulon septangulare. Botanical Gazette 49, 281289 + plates XIX and XX.CrossRefGoogle Scholar
Sokoloff, DD, von Mering, S, Jacobs, SWL and Remizowa, MV (2013) Morphology of Maundia supports its isolated phylogenetic position in the early-divergent monocot order Alismatales. Botanical Journal of the Linnean Society 173, 1245.CrossRefGoogle Scholar
Soltis, DE, Gitzendanner, MA and Soltis, PS (2007) A 567-taxon data set for angiosperms: the challenges posed by Bayesian analyses of large data sets. International Journal of Plant Sciences 168, 137157.CrossRefGoogle Scholar
Souèges, R (1924) Embryogenie des Graminees. Developpement de l'embryon chez le Poa annua L. Comptes Rendus Academie des Sciences Paris 178, 13071310.Google Scholar
Stebbins, GL (1974) Flowering plants. Evolution above the species level. Cambridge, MA, Harvard University Press.CrossRefGoogle Scholar
Stoutamire, WP (1964) Seeds and seedlings of native orchids. The Michigan Botanist 3, 107119.Google Scholar
Takhtajan, A (1954[1958]) Origins of angiospermous plants. English translation by O.H. Gankin. Washington, DC, American Institute of Biological Sciences.Google Scholar
Takhtajan, A (1980) Outline of the classification of flowering plants (Magnoliophyta). The Botanical Review 46, 225359.CrossRefGoogle Scholar
Takhtajan, A (1997) Diversity and classification of flowering plants. New York, Columbia University Press.Google Scholar
Taylor, ARA (1957) Studies of the development of Zostera marina L. I. The embryo and seed. Canadian Journal of Botany 35, 477499.CrossRefGoogle Scholar
Thorne, RF (1963) Some problems and guiding principles of angiosperm phylogeny. The American Naturalist 97, 287305.CrossRefGoogle Scholar
Tillich, H-J (1992) Bauprinzipien und Evolutionslinien bei monocotylen Keimflranzen. Botanische Jahrbücher Systematik 114, 91132.Google Scholar
Tillich, H-J (1994) Untersuchungen zum Bau der Keimflanzen der Philydraceae und Pontederiaceae (Monocotyledoneae). Sendtnera 2, 171186.Google Scholar
Tillich, H-J (1995) Seedlings and systematics in monocotyledons, pp. 305352 in Rudall, PJ; Cribb, PJ; Cutler, DF and Humphries, CJ (Eds) Monocotyledons: systematics and evolution, Kew, Royal Botanic Gardens.Google Scholar
Tillich, H-J (1996) Seeds and seedlings in Hanguanaceae and Flagellariaceae (Monocotyledons). Sendtnera 3, 187197.Google Scholar
Tillich, H-J (2000) Ancestral and derived character states in seedlings of monocotyledons, pp. 221229 in Wilson, KL and Morrison, DA (Eds) Monocots. Systematics and evolution, Collingwood, CSIRO.Google Scholar
Tillich, H-J (2003a) Seedling diversity in Araceae and its systematic implications. Feddes Repertorium 114, 454487.CrossRefGoogle Scholar
Tillich, H-J (2003b) Seedling morphology in Iridaceae: indications for reslationships within the family and to related families. Flora 198, 220242.CrossRefGoogle Scholar
Tillich, H-J (2007) Seedling diversity and the homologies of seedling organs in the order Poales (monocotyledons). Annals of Botany 100, 14131429.CrossRefGoogle Scholar
Tillich, H-J (2014) A new look at seedlings of Araceae. Aroideana 37, 4760.Google Scholar
Watson, L and Dallwitz, MJ (1992 onwards) The families of flowering plants: descriptions, illustrations, identification, and information retrieval. Version: 25th December 2020. Available at: Delta-intkey.com. (accessed 28 December 2020).Google Scholar
Werker, E (1997) Seed anatomy. Berlin, Gebrüder Borntraeger.Google Scholar
Wiedenroth, EM, Wernicke, G and Hoffman, P (1990) Morphological and anatomical characterization of the coleoptile and Triticum aestivum with regard to the evolution of forms with different ploidy levels. Annals of Botany 66, 531540.CrossRefGoogle Scholar
Xu, J-J, Zhang, X-F and Xue, H-W (2016) Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. Journal of Experimental Botany 67, 63996411.CrossRefGoogle ScholarPubMed
Yan, D, Wang, L-J, Zhao, C-H, Zhao, Y-Y and Liu, J-X (2017) Embryology of Hemerocallis L. and its systematic significance. Plant Systematics and Evolution 303, 663673.CrossRefGoogle Scholar