Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T22:03:59.103Z Has data issue: false hasContentIssue false

Martin's peripheral embryo – unique but not a phylogenetic ‘orphan’ at the base of his family tree: a tribute to the insight of a pioneer seed biologist

Published online by Cambridge University Press:  26 September 2019

Carol C. Baskin*
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546-0321, USA
Jerry M. Baskin
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA
*
Author for correspondence: Carol C. Baskin, Email: [email protected]

Abstract

As a tribute to A.C. Martin's classic work on embryos in seeds, we have attempted to gain a better understanding of the peripheral embryo, which puzzled Martin. The peripheral embryo is strongly curved and in contact with the inner surface of the seed coat, and Martin placed it at the base of his family tree of seed phylogeny and called it a ‘phylogenetic orphan’. We evaluated ovule/seed development, kind of embryo and occurrence of perisperm in families with and without a peripheral embryo. All families with a peripheral embryo occur in the Caryophyllales. Seeds with a peripheral embryo have a low cotyledon width:radicle width ratio that coincides with Martin's (full-sized) linear embryo. The peripheral embryo develops in campylotropous and/or amphitropous ovules and is pushed to the side of the seed as the perisperm develops. Linear-full embryos and perisperm are widely distributed across extant angiosperms but are rarely found together, except in core Caryophyllales. The non-core Caryophyllales with endosperm and various kinds of embryos, including the linear-full, diverged before the core Caryophyllales. Thus, the ancestral linear-full embryo appears to have been retained when the core lineage developed campylotropous and/or amphitropous ovules and perisperm. Seeds with a peripheral embryo merit a position on Martin's family tree; however, the position should be a side branch (‘orphan’) slightly above (more advanced than) his linear embryo and not at the base. We conclude that Martin had great insight into the relationships between the kinds of embryos and rightly questioned the position of the peripheral embryo.

Type
Review Paper
Copyright
Copyright © Cambridge University Press 2019 

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

Anderson, WR (1975) Dicella: a genus of Malpighiaceae new to Colombia. Acta Amazonica 5, 279283.Google Scholar
APG IV (Angiosperm Phylogeny Group) (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181, 120.Google Scholar
AP (Angiosperm Phylogeny) website www.mobot.org/mobot/research/apweb/oders/carophyllalesweb.html (accessed 26 March 2018).Google Scholar
Ayele, BT, Magnus, V, Mihaljević, S, Prebeg, T, Čož-Rakovac, R, Ozga, JA, Reinecke, DM, Mander, LN, Kamiya, Y, Yamaguchi, S and Salopek-Sondi, B (2010) Endogenous gibberellin profile during Christmas rose (Helleborus niger L.) flower and fruit development. Journal of Plant Growth Regulation 29, 194209.Google Scholar
Baskin, CC and Baskin, JM (2007) A revision of Martin's seed classification system, with particular reference to his dwarf-seed type. Seed Science Research 17, 1120.Google Scholar
Baskin, CC and Baskin, JM (2014) Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination, 2nd Edn. San Diego, CA, USA: Elsevier/Academic Press.Google Scholar
Bass, LN, Gunn, CR, Hesterman, OB and Roos, EE (1988) Seed physiology, seedling performance, and seed sprouting. Agronomy Monograph 29, 961983.Google Scholar
Behnke, H-D (1972) Sieve-tube plastids in relation to angiosperm systematics – an attempt towards a classification by ultrastructural analysis. The Botanical Review 38, 155197.Google Scholar
Behnke, H-D (1976) Ultrastructure of sieve-element plastids in Caryophyllales (Centrospermae), evidence for the delimitation and classification of the order. Plant Systematics and Evolution 126, 3154.Google Scholar
Behnke, H-D (1991) Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. Aliso 13, 167182.Google Scholar
Behnke, H-D, Chang, C, Eifert, IJ and Mabry, TJ (1974) Betalains and P-type sieve-tube plastids in Petiveria and Agdestis (Phytolaccaceae). Taxon 23, 541542.Google Scholar
Bittrich, V (1993) Introduction to Centrospermae. In Kubitzki, K, Rohwer, JG and Bittrich, V (eds), The Families and Genera of Vascular Plants. II. Dicotyledons. Magnoliid, Hamamelid and Caryophyllid Families. Berlin, Germany: Springer-Verlag, pp. 1319.Google Scholar
Boesewinkel, FD and Bouman, F (1995) The seed: structure and function. In Kigel, J and Galili, G (eds), Seed Development and Germination. New York, USA: Marcel Dekker, pp. 124.Google Scholar
Bouman, F (1984) The ovule. In Johri, BM (ed), Embryology of Angiosperms. Berlin, Germany: Springer-Verlag, pp. 123157.Google Scholar
Brockington, SR, Alexandre, R, Ramdial, J, Moore, MJ, Crawley, S, Dhingra, A, Hilu, K, Soltis, DE and Soltis, PS (2009) Phylogeny of the Caryophyllales sensu lato: revisiting hypotheses on pollination biology and perianth differentiation in the core Caryophyllales. International Journal of Plant Sciences 170, 627643.Google Scholar
Brockington, SR, Walker, RH, Glover, BJ, Soltis, PS and Soltis, DE (2011) Complex pigment evolution in the Caryophyllales. New Phytologist 190, 854864.Google Scholar
Brockington, SR, Yang, Y, Gandia-Herrero, F, Covshoff, S, Hibberd, JM, Sage, RF, Wong, GKS, Moore, MJ and Smith, SA (2015) Lineage-specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales. New Phytologist 207, 11701180.Google Scholar
Buell, KM (1952) Developmental morphology in Dianthus. I. Structure of the pistil and seed development. American Journal of Botany 39, 194210.Google Scholar
Burrieza, HP, López-Fernández, MP and Maldonado, S (2014) Analogous reserve distribution and tissue characteristics in quinoa and grass seeds suggest convergent evolution. Frontiers in Plant Science 5, article 546.Google Scholar
Carlquist, S (1961) Comparative Plant Anatomy: A Guide to Taxonomic and Evolutionary Application of Anatomical Data in Angiosperms. New York, USA: Holt, Rinehart and Winston.Google Scholar
Carlquist, S (2010) Caryophyllales: a key group for understanding wood anatomy character states and their evolution. Botanical Journal of the Linnean Society 164, 342393.Google Scholar
Crawley, SS and Hilu, KW (2012) Caryophyllales: evaluating phylogenetic signal in trnK intron versus matK. Journal of Systematics and Evolution 50, 387410.Google Scholar
Cronquist, A (1988) The Evolution and Classification of Flowering Plants. Bronx, NY, USA: The New York Botanical Garden.Google Scholar
Cuénoud, P, Savolainen, V, Chatrou, LW, Powell, M, Grayer, RJ and Chase, MW (2002) Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB and matK DNA sequences. American Journal of Botany 89, 132144.Google Scholar
Dahlgren, R and Rasmussen, FN (1983) Monocotyledon evolution. In Hecht, MK, Wallace, B and Prance, GT (eds), Evolutionary Biology, volume 16. New York, USA: Plenum Press, pp. 255395.Google Scholar
Downie, SR, Katz-Downie, DS and Cho, K-J (1997) Relationships in the Caryophyllales as suggested by phylogenetic analyses of partial chloroplast DNA ORF2280 homolog sequences. American Journal of Botany 84, 253273.Google Scholar
Eckardt, T (1976) Classical morphological features of Centrospermous families. Plant Systematics and Evolution 126, 525.Google Scholar
Endress, PK (2010) Flower structure and trends of evolution in eudicots and their major subclades. Annals of the Missouri Botanical Garden 97, 541583.Google Scholar
Endress, PK (2011a) Evolutionary diversification of the flowers in angiosperms. Botany 98, 370396.Google Scholar
Endress, PK (2011b) Angiosperm ovules: diversity, development, and evolution. Annals of Botany 107, 14651489.Google Scholar
Eriksson, O and Kainulainen, K (2011) The evolutionary ecology of dust seeds. Perspectives in Plant Ecology, Evolution and Systematics 13, 7387.Google Scholar
Fahn, A (1974) Plant Anatomy, 2nd Edn. Oxford, UK: Pergamon Press.Google Scholar
Fay, MF, Cameron, KM, Prance, GT, Lledó, MD and Chase, MW (1997) Familial relationships of Rhabdodendron (Rhabdodendraceae): plastid rbcL sequences indicate a caryophyllid placement. Kew Bulletin 52, 923932.Google Scholar
Finch-Savage, WE and Leubner-Metzger, G (2006) Seed dormancy and the control of germination. New Phytologist 171, 501523.Google Scholar
Floyd, SK and Friedman, WE (2000) Evolution of endosperm developmental patterns among basal flowering plants. International Journal of Plant Sciences 161, S5781.Google Scholar
Forbis, TA, Floyd, SK and Queiroz, A (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56, 21122125.Google Scholar
Fryxell, PA (1978) The Natural History of the Cotton Tribe (Malvaceae, Tribe Gossypieae). College Station, Texas A & M University Press.Google Scholar
Giannasi, DE, Zurawski, G, Learn, G and Clegg, MT (1992) Evolutionary relationships of the Caryophyllidae based on comparative rbcL sequences. Systematic Botany 17, 115.Google Scholar
Gibbs, LS (1907) Notes on the developement and structure of the seed in the Alsinoideae. Annals of Botany 21, 2555 + plates V and VI.Google Scholar
Gillespie, WH, Rothwell, GW and Scheckler, SE (1981) The earliest seed. Nature 293, 462464.Google Scholar
Goldberg, A 1986. Classification, evolution and phylogeny of the families of dicotyledons. Smithsonian Contributions to Botany, Number 58.Google Scholar
Goldberg, A 1989. Classification, evolution and phylogeny of the families of monocotyledons. Smithsonian Contributions to Botany, Number 71.Google Scholar
Grabe, DF (ed) (1970) Tetrazolium Testing Handbook for Agricultural Seeds. Amherst, Association of Official Seed Analysts of North America. Tetrazolium Testing Committee.Google Scholar
Grayum, MH (1991) Systematic embryology of the Araceae. The Botanical Review 57, 167203.Google Scholar
Greenberg, AK and Donoghue, MJ (2011) Molecular systematics and character evolution in Caryophyllaceae. Taxon 60, 16371652.Google Scholar
Grushvitskii, IV (1961) Role of embryo underdevelopment in the evolution of flowering plants. Komarovskie Chteniya 4, 146 [in Russian].Google Scholar
Gunn, CR (1974) Seed characteristics of 42 economically important species of Solanaceae in the United States. Agricultural Research Service, Soil Conservation Service. United States Department of Agriculture Technical Bulletin 1471.Google Scholar
Haig, D and Westoby, M (1989) Parent-specific gene expression and the triploid endosperm The American Naturalist 134, 147155.Google Scholar
Hakki, MI (2013) On flower anatomy and embryology of Lophiocarpus polystachyus (Lophiocarpaceae). Willdenowia 43, 185194.Google Scholar
Harley, RM, Atkins, S, Budantsev, AL, Cantino, PD, Conn, BJ, Grayer, R, Harley, MM, de Kok, R, Krestovskaja, T, Morales, R, Paton, AJ, Ryding, O and Upson, T (2004) In Kadereit, JW (ed), Labiatae. The Families and Genera of Vascular Plants, Vol. VII. Flowering Plants – Dicotyledons. Berlin, Germany: Springer, pp. 167295.Google Scholar
Harms, H (1934) Centrospermae, pp. 16 in Engler, A and Harms, H (eds), Natürlichen Pflanzenfamilien. Berlin, Germany: Duncker and Humblot.Google Scholar
Harris, PJ and Hartley, RD (1980) Phenolic constituents of the cell walls of monocotyledons. Biochemical Systematics and Ecology 8, 153160.Google Scholar
Harris, PJ and Trethewey, JAK (2010) the distribution of ester-linked ferulic acid in the cell walls of angiosperms. Phytochemical Review 9, 1933.Google Scholar
Hartley, RD and Harris, PJ (1981) Phenolic constituents of the cell walls of dicotyledons. Biochemical Systematics and Ecology 9, 189203.Google Scholar
Hartman, HT and Kester, DE (1975) Plant Propagation: Principles and Practices, 3rd Edn. Boston, USA: Prentice-Hall.Google Scholar
Hernández-Ledesma, P, Berendsohn, WG, Bosch, T, Mering, SV, Akhani, H, Arias, S, Castañeda-Noa, I, Eggli, U, Eriksson, R, Flores-Olvera, H, Fuentes-Bazán, S, Kadereit, G, Klak, C, Korotkova, N, Nyffeler, R, Ocampo, G, Ochoterena, H, Oxelman, B, Rabeler, RK, Sanchez, A, Schlumpberger, BO and Uotila, P (2015) A taxonomic backbone for the global synthesis of species diversity in the angiosperm order Caryophyllales. Willdenowia 45, 281383.Google Scholar
Hilu, KW, Borsch, T, Müller, K, Soltis, DE, Soltis, PS, Savolainen, V, Chase, MW, Powell, MP, Alice, LA, Evans, R, Sauquet, H, Neinhuis, C, Slotta, TAB, Rohwer, JG, Campbell, CS and Chatrou, LW (2003) Angiosperm phylogeny based on MATK sequence information. American Journal of Botany 90, 17581776.Google Scholar
Hodgson, JG and Mackey, JML (1986) The ecological specialization of dicotyledonous families within a local flora: some factors constraining optimization of seed size and their possible evolutionary significance. New Phytologist 104, 497515.Google Scholar
Houk, WG (1938) Endosperm and perisperm of coffee with notes on the morphology of the ovule and seed development. American Journal of Botany 25, 5661.Google Scholar
Iwashina, T (2013) Flavonoid properties of five families newly incorporated into the order Cayophyllales (review). Bulletin of the National Museum of Natural Science, Series B 39, 2551.Google Scholar
Jiménez-Durán, K, Arias-Montes, S, Cortés-Palomec, A and Márquez-Guzmán, J (2014) Embryology and seed development in Pereskia lychnidiflora (Cactaceae). Haseltonia 19, 312.Google Scholar
Johansen, DA (1950) Plant Embryology. Embryology of the Spermatophytes. Waltham, MA, Chronica Botanica Company.Google Scholar
Justice, OL (1972) Essentials of seed testing. In Kozlowski, TT (ed), Seed Biology, Volume III: Insects, and Seed Collection, Storage, Testing, and Certification. Cambridge, MA, USA: Academic Press, pp. 330370.Google Scholar
Kajale, LB (1940) A contribution to the embryology of the Amaranthaceae. Proceedings of the National Institute of Sciences of India 6, 597625.Google Scholar
Kajale, LB (1954) A contribution to the embryology of the Phytolaccaceae. II. Fertilization and the development of embryo, seed and fruit in Rivina humilis Linn. and Phytolacca dioica Linn. The Journal of the Indian Botanical Society 33, 206225.Google Scholar
Keeley, JE (1991) Seed germination and life history syndromes in the California chaparral. The Botanical Review 57, 81116.Google Scholar
Kellmann-Sopyła, W, Koc, J, Górecki, RJ, Domaciuk, M and Giełwanowsak, I (2017) Development of generative structures of polar Caryophyllaceae plants: the Arctic Cerastium alpinum and Silene involucrata, and the Antarctic Colobanthus quitensis. Polish Polar Research 38, 83104.Google Scholar
Lang, A (1965) Effects of some internal and external conditions on seed germination. Encyclopedia of Plant Physiology 15, 24952540.Google Scholar
Lee, J, Kim, SY, Park, SH and Ali, MA (2013) Molecular phylogenetic relationships among members of the family Phytolaccaceae sensu lato inferred from internal transcribed spacer sequences of nuclear ribosomal DNA. Genetics and Molecular Research 12, 45154525.Google Scholar
Liao, J-P and Wu, Q-G (2000) A preliminary study of the seed anatomy of Zingiberaceae. Botanical Journal of the Linnean Society 134, 287300.Google Scholar
Liu, K, Baskin, JM, Baskin, CC and Du, G (2013) Very fast-germinating seeds of desert species are cryptoviviparous-like. Seed Science Research 23, 163167.Google Scholar
López-Fernández, MP and Maldonado, S (2013) Programmed cell death during quinoa perisperm development. Journal of Experimental Botany 64, 33133325.Google Scholar
Lu, A-M (1985) Embryology and probable relationships of Eriospermum (Eriospermaceae). Nordic Journal of Botany 5, 229240.Google Scholar
Mabberley, DJ (2008) Mabberley's Plant-Book. A Portable Dictionary of Plants, Their Classification and Uses, 3rd Edn. Cambridge, UK: Cambridge University Press.Google Scholar
Mabry, TJ (1976) Pigment dichotomy and DNA-RNA hybridization data for centrospermous families. Plant Systematics and Evolution 126, 7994.Google Scholar
Mabry, TJ (1977) The order Centrospermae. Annals of the Missouri Botanical Garden 64, 210220.Google Scholar
Mabry, TJ and Dreiding, AS (1969). The betalains. Recent Advances in Phytochemistry 1, 145160.Google Scholar
Mabry, TJ, Taylor, A and Turner, BL (1963) The betacyanins and their distribution. Phytochemistry 2, 6164.Google Scholar
Magallón, S, Gómez-Acevedo, S, Sánchez-Reyes, LL and Hernández-Hernández, T (2015) A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist 207, 437453.Google Scholar
Maheshwari, P and Chopra, RN (1955) The structure and development of the ovule and seed of Opuntia dillenii Haw. Phytomorphology 5, 112122.Google Scholar
Martin, AC (1946) The comparative internal morphology of seeds. The American Midland Naturalist 36, 513660.Google Scholar
Martin, AC and Barkley, WD (1961) Seed Identification Manual. Berkeley and Los Angeles: University of California Press.Google Scholar
Martin, AC, Hotchkiss, N, Uhler, FM, Bourn, WS and the U.S. Fish and Wildlife Service Wetlands Classification Committee (1953) Classification of wetlands in the United States. U.S. Fish and Wildlife Service. Special Scientific Report No. 20.Google Scholar
Martin, AC, Zim, HS and Nelson, AL (1951) American Wildlife and Plants. New York, USA: McGraw-Hill.Google Scholar
Mohana Rao, PR, Guignard, J-L and Duret, S (1988) An ultrastructural study of perisperm and endosperm in Silene alba Miller E.H.L. Krause. Bulletin de la Société Botanique de France. Lettres Botaniques 135, 123130.Google Scholar
Moore, MJ, Soltis, PS, Bell, CD, Burleigh, JG and Soltis, DE (2010) Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proceedings of the National Academy of Sciences of the USA 107, 46234628.Google Scholar
Morton, CM, Karol, KG and Chase, MW (1997) Taxonomic affinities of Physena (Physenaceae) and Asteropeia (Theaceae). The Botanical Review 63, 231239.Google Scholar
Netolitzky, F (1926) Anatomie der Angiospermen-Samen. Berlin, Germany: Verlag von Gebrüder Borntrager.Google Scholar
Pal, A, Singh, RP and Pal, M (1990) Development and structure of seeds in Amaranthus hypochondriacus L. and its wild progenitor A. hybridus L. Phytomorphology 40, 145150.Google Scholar
Palser, BF (1951) Studies of floral morphology in the Ericales. I. Organography and vascular anatomy in the Andromedeae. Botanical Gazette 112, 447485.Google Scholar
Parsons, RF (2012) Incidence and ecology of very fast germination. Seed Science Research 22, 161167.Google Scholar
Parsons, RR, Vandelook, F and Janssens, SB (2014) Very fast germination: additional records and relationship to embryo size and phylogeny. Seed Science Research 24, 159163.Google Scholar
Philipson, WR (1974) Ovular morphology and the major classification of the dicotyledons. Botanical Journal of the Linnean Society 68, 89108.Google Scholar
Pires, ND (2014) Seed evolution: parental conflicts in a multi-generational household. Biomolecular Concepts 5, 7186.Google Scholar
Plakhine, D, Tadmor, Y, Ziadne, H and Joel, DM (2012) Maternal tissue is involved in stimulant reception by seeds of the parasitic plant Orobanche. Annals of Botany 109, 979986.Google Scholar
Povilus, RA, Diggle, PK and Friedman, WE (2018) Evidence for parent-of-origin effects and interparental conflict in seeds of an ancient flowering plant lineage. Proceedings of the Royal Society B 285, 20172491.Google Scholar
Queller, DC (1983) Kin selection and conflict in seed maturation. Journal of Theoretical Biology 100, 153172.Google Scholar
Raghaven, V (1986) Embryogenesis in Angiosperms. A Developmental and Experimental Study. London, UK: Cambridge University Press.Google Scholar
Rau, MA (1940) An embryological study of Suriana maritima Linn. Indian Academy of Sciences Proceedings Section B 11, 100106.Google Scholar
Reeder, JR (1957) The embryo in grass systematics. American Journal of Botany 44, 756768.Google Scholar
Retting, JH, Wilson, HD and Manhart, JR (1992) Phylogeny of the Caryophyllales – gene sequence data. Taxon 41, 201209.Google Scholar
Rothwell, GW, Scheckler, SE and Gillespie, WH (1989) Elkinsia gen. nov., a Late Devonian gymnosperm with cupulate ovules. Botanical Gazette 150, 170189.Google Scholar
Shepherd, KA, Macfarlane, TD and Colmer, TD (2005) Morphology, anatomy and histochemistry of Salicornioideae (Chenopodiaceae) fruits and seeds. Annals of Botany 95, 917933.Google Scholar
Smith, SA, Brown, JW, Yang, Y, Bruenn, R, Drummond, CP, Brockington, SF, Walker, JF, Last, N, Douglas, NA and Moore, MJ (2018) Disparity, diversity, and duplications in the Caryophyllales. New Phytologist 217, 836854.Google Scholar
Soltis, DE, Soltis, PS, Endress, PK and Chase, MW (2005) Phylogeny and evolution of angiosperms. Sunderland, Sinauer Associates.Google Scholar
Soltis, DE, Soltis, PS, Chase, MW, Mort, ME, Albach, DC, Zanis, M, Savolainen, V, Hahn, WH, Hoot, SB, Fay, MF, Axtell, M, Swensen, SM, Prince, LM, Kress, WJ, Nixon, KC and Farris, JS (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133, 381461.Google Scholar
Soltis, PE, Soltis, DE and Chase, MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402404.Google Scholar
Stafford, HA (1994) Anthocyanins and betalains: evolution of the mutually exclusive pathways. Plant Science 101, 9198.Google Scholar
Stevens, NE (1912) The morphology of the seed of buckwheat. Botanical Gazette 53, 5966.Google Scholar
Sukhorukov, AP, Mavrodiev, EV, Struwig, M, Nilova, MV, Dzhalilova, KK, Balandin, SA, Erst, A and Krinitsyna, AA (2015) One-seeded fruits in the core Caryophyllales: their origin and structural diversity. PLoS ONE 10, e0117974.Google Scholar
Takaso, T and Bouman, F (1984) Ovule ontogeny and seed development in Potamogeton natans L. (Potamogetonaceae), with a note on the campylotropous ovule. Acta Botanica Neerlandica 33, 519533.Google Scholar
Takhtajan, A (1980) Outline of the classification of flowering plants (Magnoliophyta). The Botanical Review 46, 225359.Google Scholar
Takhtajan, A (1997) Diversity and Classification of Flowering Plants. New York, USA: Columbia University Press.Google Scholar
Thorne, RF (2000) The classification and geography of the flowering plants: dicotyledons of the class Angiospermae. The Botanical Review 66, 441647.Google Scholar
Thulin, M, Moore, AJ, El-Seedi, H, Larsson, A, Christin, P-A and Edwards, EJ (2016) Phylogeny and generic delimitation in Molluginaceae, new pigment data in Caryophyllales, and the new family Corbichoniaceae. Taxon 65, 775793.Google Scholar
Vaughan, JG and Whitehouse, JM (1971) Seed structure and the taxonomy of the Cruciferae. Botanical Journal of the Linnean Society 64, 383409.Google Scholar
Vyshenskaya, TD (2006) Morphological classification of embryo in mature seed: critical review of main systems. In Batygina, TB (ed), Embryology of Flowering Plants. Terminology and Concepts. Volume 2. Seed. Enfield, NH, USA: Science Publishers, pp. 264273.Google Scholar
Wagner, J and Tengg, G (1993) Embryology of two high-mountain plants, Saxifraga oppositifolia and Cerastium uniflorum, in relation to phenology. Flora 188, 203212.Google Scholar
Walker, JF, Yang, Y, Feng, T, Timondea, A, Mikenas, J, Hutchison, V, Edwards, C, Wang, N, Ahluwalia, S, Olivieri, J, Walker-Hale, N, Majure, LD, Puente, R, Kadereeit, G, Lauterbach, M, Eggli, U, Flores-Olvera, H, Ochoterena, H, Brockington, SF, Moore, MJ and Smith, SA (2018) From cacti to carnivores: improved phylotranscriptomic sampling and hierarchical homology inference provide further insight into the evolution of Caryophyllales. American Journal of Botany 105, 446462.Google Scholar
Watson, L and Dallwitz, MJ (1992 onwards) The Families of Flowering Plants: Descriptions, Illustrations, Identification, and Information Retrieval. Version: 14 October 2018, http://www1.biologie.uni-hamburg.de/b-online/delta/angio/index.htm (accessed 10 January 2019).Google Scholar
Werker, D (1997) Seed Anatomy. Berlin, Germany: Gebrüde Borntraeger .Google Scholar
Westoby, M and Rice, B (1982) Evolution of the seed plants and inclusive fitness of plant tissues. Evolution 36, 713724.Google Scholar
West, MM, Flannigan, DT and Lott, JNA (1995) Elemental composition of globoids in the perisperm tissue of various seeds. Canadian Journal of Botany 73, 954957.Google Scholar
Williams, SE, Albert, VA and Chase, MW (1994) Relationships of Droseraceae: a cladistics analysis of rbcL sequence and morphological data. American Journal of Botany 81, 10271037.Google Scholar
Willis, CG, Baskin, CC, Baskin, JM, Auld, JR, Venable, DL, Cavender-Bares, J, Donohue, K, Rubio de Casas, R; NESCent Germination Working Group (2014) The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants. New Phytologist 203, 300309.Google Scholar
Wilms, HJ (1980) Development and composition of the spinach ovule. Acta Botanica Neerlandica 29, 243260.Google Scholar
Woodcock, EF (1914) Observations on the development and germination of the seed in certain Polygonaceae. American Journal of Botany 1, 454476.Google Scholar
Yang, Y, Moore, MJ, Brockington, SF, Soltis, DE, Wong, G.K.-S., Carpenter, EJ, Zhang, Y, Chen, L, Yan, Z, Xie, Y, Sage, RF, Covshoff, S, Hibberd, JM, Nelson, MN and Smith, SA (2015) Dissecting molecular evolution in the highly diverse plant clade Caryophyllales using transcriptome sequencing. Molecular Biology and Evolution 32, 20012014.Google Scholar
Zheng, H-C, Ma, S-W and Chai, T-Y (2010) Ovular development and perisperm formation in Phytolacca americana (Phytolaccaceae) and their systematic significance in Caryophyllales. Journal of Systematics and Evolution 48, 318325.Google Scholar