Embryology in trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early-diverging flowering plants

American Journal of Botany

Volumn 99, Issue 6, 2012, Pages 1083-1095

  Friedman, William E ^a   Bachelier, Julien B ^a   Hormaza, José I ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

Author keywords

Aleurone; Cotyledons; Embryo; Germination; Hydatellaceae; Nymphaeales; Origin of angiosperms; Seed; Trithuria submersa

Indexed keywords

ANGIOSPERM; AQUATIC PLANT; BIOLOGICAL DEVELOPMENT; EMBRYO; EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; FERTILIZER APPLICATION; FLOWER; FRUIT; GERMINATION; HISTOLOGY; MORPHOLOGY; STARCH;

ANGIOSPERM; ARTICLE; CLASSIFICATION; COTYLEDON; ENDOSPERM; EVOLUTION; FERTILIZATION; FLOWER; GERMINATION; PHYSIOLOGY; PLANT SEED; PRENATAL DEVELOPMENT; REPRODUCTION; TIME;

ANGIOSPERMS; BIOLOGICAL EVOLUTION; COTYLEDON; ENDOSPERM; FERTILIZATION; FLOWERS; GERMINATION; REPRODUCTION; SEEDS; TIME FACTORS;

COTYLEDON (GENUS); HYDATELLACEAE; MAGNOLIOPHYTA; NYMPHAEALES; TRITHURIA SUBMERSA;

EID: 84862246162     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200066     Document Type: Article

References (93)

1. APG III [ANGIOSPERM PHYLOGENY GROUP III]. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105-121.
2. BACHELIER, J. B., and W. E. FRIEDMAN. 2011. Female gamete competition in an ancient angiosperm lineage. Proceedings of the National Academy of Sciences, USA 108: 12360-12365.
3. BAILEY, I. W., and B. G. L. SWAMY. 1948. Amborella trichopoda Bail., a new morphological type of vesselless dicotyledon. Journal of the Arnold Arboretum 29: 245-254.
4. BASKIN, C. C., and J. M. BASKIN. 2007a. Nymphaeaceae: A basal angiosperm family (ANITA grade) with a fully developed embryo. Seed Science Research 17: 293-296.
5. BASKIN, C. C., and J. M. BASKIN. 2007b. A revision of Martin's seed classify cation system, with particular reference to his dwarf-seed type. Seed Science Research 17: 11-20.
6. BASKIN, J. M., and C. C. BASKIN. 2004. A classification system for seed dormancy. Seed Science Research 14: 1-16.
7. BATYGINA, T. B., I. I. SHAMROV, and G. E. KOLESOVA. 1982. Embryology of the Nymphaeales and Nelumbonales. II. The development of the female embryonic structures. Botanicheskii Zhurnal 67: 1179-1195.
8. BUELL, M. F. 1935. Seed and seedling of Acorus calamus. Botanical Gazette 96: 758-765.
9. CARLQUIST, S., and E. L. SCHNEIDER. 2009. Do tracheid microstructure and the presence of minute crystals link Nymphaeaceae, Cabombaceae and Hydatellaceae? Botanical Journal of the Linnean Society 159: 572-582.
10. CHIEN, C.-T., S.-Y. C HEN, J. M. BASKIN, and C. C. BASKIN. 2011. Morphophysiological dormancy in seeds of the ANA grade angiosperm Schisandra arisanensis (Schisandraceae). Plant Species Biology 26: 99-104.
11. CHIFFLOT, J.-B.-J. 1902. Contributions à l'étude de la classe des Nymphéinées. Annales de l'Université de Lyon, nouvelle série, I 10: 1-294.
12. COCUCCI, A. E. 1976. Estudios en el género P rosopanche (Hydnoraceae) III. Embriología. Kurtziana 9: 19-39.
13. CONARD, H. S. 1905. The waterlilies: A monograph of the genus Nymphaea. Carnegie Institution of Washington 4: 1-278.
14. COOK, M. T. 1902. Development of the embryo-sac of Castalia odorata and Nymphaea advena. Bulletin of the Torrey Botanical Club 29: 211-220.
15. COOK, M. T. 1906. The embryogeny of some Cuban Nymphaeaceae. Botanical Gazette 42: 376-392.
16. COOK, M. T. 1909. Notes on the embryology of the Nymphaeaceae. Botanical Gazette 48: 56-60.
17. CRONQUIST, A. 1988. The evolution and classification of flowering plants. New York Botanical Garden, Bronx, New York, USA.
18. DONOGHUE, M. J., and S. M. SCHEINER. 1992. The evolution of endosperm: A phylogenetic account. In R. Wyatt [ed.], Ecology and evolution of plant reproduction: New approaches, 356-389. Chapman and Hall, New York, New York, USA.
19. DOYLE, J. A. 1994. Origin of the angiosperm flower: A phylogenetic perspective. In P. K. Endress and E. M. Friis [eds.], Early evolution of flowers, 7-29. Springer, Vienna, Austria.
20. DOYLE, J. A., M. J. DONOGHUE, and E. A. ZIMMER. 1994. Integration of morphological and ribosomal RNA data on the origin of angiosperms. Annals of the Missouri Botanical Garden 81: 419-450.
21. ENDRESS, P. K. 1980. The reproductive structures and systematic position of the Austrobaileyaceae. Botanische Jahrbücher für Systematik, Pflflanzengeschichte und Pflanzengeographie 101: 393-433.
22. ENDRESS, P. K. 2010. The evolution of floral biology in basal angiosperms. Philosophical Transactions of the Royal Society, B, Biological Sciences 365: 411-421.
23. ENDRESS, P. K., and J. A. DOYLE. 2009. Reconstructing the ancestral flower and its initial specializations. American Journal of Botany 96: 22-66.
24. FLOYD, S. K., and W. E. FRIEDMAN. 2000. Evolution of endosperm developmental patterns among basal flowering plants. International Journal of Plant Sciences 161: S57-S81.
25. FLOYD, S. K., and W. E. FRIEDMAN. 2001. Developmental evolution of endosperm in basal angiosperms: Evidence from Amborella (Amborellaceae), Nuphar (Nymphaeaceae), and Illicium (Illiciaceae). Plant Systematics and Evolution 228: 153-169.
26. FORBIS, T. A., S. K. FLOYD, and 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.
27. FRIEDMAN, W. E. 2008. Hydatellaceae are water lilies with gymnospermous tendencies. Nature 453: 94-97.
28. FRIEDMAN, W. E., W. N. GALLUP, and J. H. WILLIAMS. 2003. Gametophyte development in Kadsura: Implications for Schisandraceae, Austrobaileyales, and the early evolution of flowering plants. International Journal of Plant Sciences 164: S293-S305.
29. FRIEDMAN, W. E., E. N. MADRID, and J. H. WILLIAMS. 2008. Origin of the fittest and survival of the fittest: Relating female gametophyte development to endosperm genetics. International Journal of Plant Sciences 169: 79-92.
30. FRIEDMAN, W. E., and J. H. WILLIAMS. 2003. Modularity in the angiosperm female gametophyte and its bearing on the early evolution of endosperm in flowering plants. Evolution 57: 216-230.
31. FRIEDMAN, W. E., and J. H. WILLIAMS. 2004. Developmental evolution of the sexual process in ancient flowering plants lineages. The Plant Cell 16: S119-S132.
32. GAIKWAD, S. P., and S. R. YADAV. 2003. Further morphotaxonomical contribution to the understanding of family Hydatellaceae. Journal of the Swamy Botanical Club 20: 1-10.
33. GUTTENBERG, H. V., and R. MÜLLER-SCHRÖDER. 1958. Untersuchungen über die Entwicklung des Embryos und der Keimpflanze von Nuphar luteum Smith. Planta 51: 481-510.
34. HALLIER, H. 1901. Über die Verwandtschaftsverhältnisse der Tubifloren und Ebenalen, den polyphyletischen Ursprung der Sympetalen und Apetalen, und die Anordnung der Angiospermen überhaupt: Vorstudien zum Entwurf eines Stammbaums der Blütenplanfzen. Abhandlungen und Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg 16: 1-112.
35. HAMANN, U. 1962. Beitrag zur Embryologie der Centrolepidaceae mit Bemerkungen über den Bau der Blüten und Blütenstände und die systematische Stellung der Familie. Berichte der Deutschen Botanischen Gesellschaft 75: 153-171.
36. HAMANN, U. 1975. Neue Untersuchungen zur Embryologie und Systematik der Centrolepidaceae. Botanische Jahrbücher für Systematik, Pflflanzengeschichte und Pflanzengeographie 96: 154-191.
37. HAMANN, U. 1976. Hydatellaceae-A new family of Monocotyledoneae. New Zealand Journal of Botany 14: 193-196.
38. HAMANN, U., K. KAPLAN, and T. RÜBSAMEN. 1979. Über die Samenschalenstruktur der Hydatellaceae (Monocotyledoneae) und die sys tematische Stellung von Hydatella filamentosa. Botanische Jahrbücher für Systematik, Pflflanzengeschichte und Pflanzengeographie 100: 555-563.
39. HUMPHREY, J. E. 1896. The development of the seed in the Scitaminae. Annals of Botany 10: 1-37.
40. ILES, W. J. D., P. J. RUDALL, D. D. SOKOLOFF, M. V. REMISOWA, T. D. MACFARLANE, M. D. LOGACHEVA, and S. W. GRAHAM. 2012. Molecular phylogenetics of Hydatellaceae (Nymphaeales): Sexual-system homoplasy and a new sectional classification. American Journal of Botany 99: 663-676.
41. JOHNSON, D. S. 1900a. On the development of Saururus cernuus L. Bulletin of the Torrey Botanical Club 27: 365-372.
42. JOHNSON, D. S. 1900b. On the endosperm and embryo of Peperomia pellucida. Botanical Gazette 30: 1-11.
43. JOHNSON, D. S. 1902. On the development of certain Piperaceae. Botanical Gazette 34: 321-340.
44. JOHNSON, D. S. 1914. Studies of the development of Piperaceae. II. The structure and seed-development of Peperomia hispidula. [continued] American Journal of Botany 1: 357-397.
45. KHANNA, P. 1964a. Morphological and embryological studies in Nymphaeaceae. I. Euryale ferox Salisb. Proceedings of the Indian Academy of Sciences 59: 237-243.
46. KHANNA, P. 1964b. Some interesting observations in Euryale ferox Salisb. Current Science 33: 152.
47. KHANNA, P. 1965. Morphological and embryological studies in Nymphaeaceae. II. Brasenia schreberei Gmel. and Nelumbo nucifera Gaertn. Australian Journal of Botany 13: 379-387.
48. KHANNA, P. 1967. Morphological and embryological studies in Nymphaeaceae. III. Victoria cruziana D'Orb. and Nymphaea stellata Willd. Botanical Magazine 80: 305-312.
49. LEI, L.-G., Z. Y. WU, and H. X. LIANG. 2002. Embryology of Zippelia begoniifolia (Piperaceae) and its systematic relationships. Botanical Journal of the Linnean Society 140: 49-64.
50. LERSTEN, N. R. 2008. Flowering plant embryology, 2nd ed. Blackwell, Oxford, UK.
51. MADDISON, D. R., and W. P. MADDISON. 2000. MacClade version 4: Analysis of phylogeny and character evolution. Sinauer, Sunderland Massachusetts, USA.
52. MARTIN, A. C. 1946. The comparative internal morphology of seeds. American Midland Naturalist 36: 513-660.
53. MEYER, K. 1960. On the embryology of Nuphar luteum Sm. Bulletin of Moscow Society of Naturalists. Biological Series 65: 48-59.
54. MORAT, P. H., and H. S. MACKEE. 1977. Quelques précisions sur le Trimenia neocaledonica Bak. f. et la famille des Triméniacées en Nouvelle-Calédonie. Adansonia, série 2 17: 205-213.
55. OSBORN, J. M., and E. L. SCHNEIDER. 1988. Morphological studies of the Nymphaeaceae sensu lato. XVI. The floral biology of Brasenia schreberi. Annals of the Missouri Botanical Garden 75: 778-794.
56. PRAKASH, N., and H. K. BAK. 1982. Flower and fruit development in Piper nigrum L. cv. Kuching. Malaysian Journal of Science 7: 11-19.
57. PRYCHID, C. J., D. D. SOKOLOFF, M. V. REMIZOWA, R. E. TUCKETT, S. R. YADAV, and P. J. RUDALL. 2011. Unique stigmatic hairs and pollentube growth within the stigmatic cell wall in the early-divergent angiosperm family Hydatellaceae. Annals of Botany 108: 599-608.
58. REMIZOWA, M. V., D. D. SOKOLOFF, T. D. MACFARLANE, S. R. YADAV, P. C. PRYCHID, and P. J. RUDALL. 2008. Comparative pollen morphology in the early-divergent angiosperm family Hydatellaceae reveals variation at the infraspecific level. Grana 47: 81-100.
59. RUDALL, P. J., and C. A. FURNESS. 1997. Systematics of Acorus: Ovule and anther. International Journal of Plant Sciences 158: 640-651.
60. RUDALL, P. J., D. D. SOKOLOFF, M. V. REMIZOWA, J. G. C ONRAN, J. I. DAVIS, T. D. MACFARLANE, and D. W. STEVENSON. 2007. Morphology of Hydatellaceae, an anomalous aquatic family recently recognized as an early-divergent angiosperm lineage. American Journal of Botany 94: 1073-1092.
61. RUDALL, P. J., M. V. REMIZOWA, A. S. BEER, E. BRADSHAW, D. W. STEVENSON, T. D. MACFARLANE, R. E. TUCKETT, S. R. YADAV, and D. D. SOKOLOFF. 2008. Comparative ovule and megagametophyte development in Hydatellaceae and water lilies reveal a mosaic of features among the earliest angiosperms. Annals of Botany 101: 941-956.
62. RUDALL, P. J., M. V. REMIZOWA, G. PRENNER, C. J. PRYCHID, R. E. TUCKETT, and D. D. SOKOLOFF. 2009a. Nonflowers near the base of extant angiosperms? Spatiotemporal arrangement of organs in reproductive units if Hydatellaceae and its bearing on the origin of the flower. American Journal of Botany 96: 67-82.
63. RUDALL, P. J., T. E LDRIDGE, J. T RATT, M. M. RAMSAY, R. E. TUCKETT, S. Y. SMITH, M. E. COLLINSON, M. V. REMIZOWA, and D. D. SOKOLOFF. 2009b. Seed fertilization, development, and germination in Hydatellaceae (Nymphaeales): Implications for endosperm evolution in early angiosperms. American Journal of Botany 96: 1581-1593.
64. SAARELA, J. M., H. S. RAI, J. A. DOYLE, P. K. ENDRESS, S. MATHEWS, A. D. MARCHANT, B. G. BRIGGS, and S. W. GRAHAM. 2007. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446: 312-315.
65. SARGANT, E. 1900. Recent works on the results of fertilization in angiosperms. Annals of Botany 14: 689-712.
66. SAUNDERS, R. M. K. 1998. Monograph of K adsura (Schisandraceae). Systematic Botany Monographs 54: 1-106.
67. SCHNEIDER, E. L. 1978. Morphological studies of the Nymphaeaceae. IX. The seed of Barclaya longifolia Wall. Botanical Gazette 139: 223-230.
68. SCHNEIDER, E. L., and E. G. FORD. 1978. Morphological studies of the Nymphaeaceae. X. The seed of Ondinea purpurea Den Hartog. Bulletin of the Torrey Botanical Club 105: 192-200.
69. SCHNEIDER, E. L., and J. M. JETER. 1982. Morphological studies of the Nymphaeaceae. XII. The floral biology of Cabomba caroliniana. American Journal of Botany 69: 1410-1419.
70. SEATON, S. 1908. The development of the embryo-sac of Nymphaea advena. Bulletin of the Torrey Botanical Club 35: 283-290.
71. SHAMROV, I. I. 1998. Formation of hypostase, podium and postament in the ovule of Nuphar lutea (Nymphaeaceae) and Ribes aureum (Grossulariaceae). Botanicheskii Zhurnal 83: 3-14.
72. SHAMROV, I. I. 2006. Morphological nature of ovule and its evolutionary lineages in flowering plants. Botanicheskii Zhurnal 91: 1601-1635.
73. SOKOLOFF, D. D., M. V. REMIZOWA, B. G. BRIGGS, and P. J. RUDALL. 2009. Shoot architecture and branching pattern in perennial Hydatellaceae (Nymphaeales). International Journal of Plant Sciences 170: 869-884.
74. SOKOLOFF, D. D., M. V. REMIZOWA, T. D. MACFARLANE, and P. J. RUDALL. 2008a. Classification of the early-divergent angiosperm family Hydatellaceae: One genus instead of two, four new species and sexual dimorphism in dioecious taxa. Taxon 57: 179-200.
75. SOKOLOFF, D. D., M. V. REMIZOWA, T. D. MACFARLANE, R. E. TUCKETT, M. M. RAMSAY, A. S. BEER, S. R. YADAV, and P. J. RUDALL. 2008b. Seedling diversity in Hydatellaceae: Implications for the evolution of angiosperm cotyledons. Annals of Botany 101: 153-164.
76. SOKOLOFF, D. D., M. V. REMIZOWA, T. D. MACFARLANE, S. R. YADAV, and P. J. RUDALL. 2011. Hydatellaceae: A historical review of systematics and ecology. Rheedea 21: 115-138.
77. SOKOLOFF, D. D., M. V. REMIZOWA, S. R. YADAV, and P. J. RUDALL. 2010. Development of reproductive structures in the sole Indian species of Hydatellaceae, Trithuria konkanensis, and its morphological differences from Australian taxa. Australian Systematic Botany 23: 217-228.
78. STEVENS, P. F. 2001 [onwards]. Angiosperm Phylogeny Website, version 9, une 2008 [and more or less continuously updated since]. Website http://www.mobot.org/MOBOT/research/APweb/ [accessed March 2012].
79. SWAMY, B. G. L., and N. PARAMESWARAN. 1962. The helobial endosperm. Biological Reviews of the Cambridge Philosophical Society 38: 1-50.
80. TAYLOR, M. L., T. D. MACFARLANE, and J. H. WILLIAMS. 2010. Reproductive ecology of the basal angiosperm Trithuria submersa (Hydatellaceae). Annals of Botany 106: 909-920.
81. TAYLOR, M. L., and J. H. WILLIAMS. 2012. Pollen tube development in two species of Trithuria (Hydatellaceae) with contrasting breeding systems. Sexual Plant Reproduction 25: 83-96.
82. TILLICH, H. J. 1990. The seedlings of Nymphaeaceae-Monocotylar or icotylar? Flora 184: 169-176.
83. TILLICH, H.-J., R. TUCKETT, and E. FACHER. 2007. Do Hydatellaceae belong to the monocotyledons or basal angiosperms? Evidence from seedling morphology. Willdenowia 37: 399-406.
84. TRATT, J., C. J. PRYCHID, H.-D. BEHNKE, and P. J. RUDALL. 2009. Starchaccumulating (S-type) sieve-element plastids in Hydatellaceae: Implications for plastid evolution in flowering plants. Protoplasma 237: 19-26.
85. TUCKETT, R. E., D. J. MERRITT, F. R. HAY, S. D. HOPPER, and K. W. DIXON. 2010a. Comparative longevity and low-temperature storage of seeds of Hydatellaceae and temporary pool species of south-west Australia. Ustralian Journal of Botany 58: 327-334.
86. TUCKETT, R. E., D. J. MERRITT, P. J. RUDALL, F. HAY, S. D. HOPPER, C. C. BASKIN, J. M. BASKIN, J. TRATT, and K. W. DIXON. 2010b. A new type of specialized morphophysiological dormancy and seed storage behaviour in Hydatellaceae, an early-divergent angiosperm family. Anals of Botany 105: 1053-1061.
87. VALTZEVA, O. V., and E. I. SAVICH. 1965. Development of embryo in Nymphaea candida Presl. and N. tetragona Georgi. Botanicheskii Zhurnal 50: 1323-1326.
88. WHEELER HAINES, R., and K. A. LYE. 1975. Seedlings of Nymphaeaceae. Botanical Journal of the Linnean Society 70: 255-265.
89. WILLIAMS, J. H., and W. E. FRIEDMAN. 2002. Identification of diploid endosperm in an early angiosperm lineage. Nature 415: 522-526.
90. WILLIAMS, J. H., and W. E. FRIEDMAN. 2004. The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): Implications for understanding the origin and early evolution of monocots, eumagnoliids, and eudicots. American Journal of Botany 91: 332-351.
91. YAMADA, T., R. IMAICHI, and M. KATO. 2001. Developmental morphology of ovules and seeds of Nymphaeales. American Journal of Botany 88: 963-974.
92. YAMADA, T., R. IMAICHI, N. PRAKASH, and M. KATO. 2003. Developmental morphology of ovules and seeds of Austrobaileyales. Australian Journal of Botany 51: 555-564.
93. YAMADA, T., H. NISHIDA, M. UMEBAYASHI, K. UEMURA, and M. KATO. 2008. Oldest record of Trimeniaceae from the Early Cretaceous of northern Japan. BMC Evolutionary Biology 8: 135.