Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-29T20:57:02.449Z Has data issue: false hasContentIssue false
  • English
  • Français

Structural aspects and trends in the evolution of recalcitrant seeds in dicotyledons

Published online by Cambridge University Press:  19 September 2008

I. von Teichman  and
A. E. van Wyk
I. von Teichman*
Affiliation:
Margaretha Mes Institute for Seed Research and H G W J Schweickerdt Herbarium, Department of Botany, University of Pretoria, Pretoria, 0002Republic of South Africa
A. E. van Wyk
Affiliation:
Margaretha Mes Institute for Seed Research and H G W J Schweickerdt Herbarium, Department of Botany, University of Pretoria, Pretoria, 0002Republic of South Africa
*
* Correspondence
Get access Rights & Permissions [Opens in a new window]

Abstract

This review focuses on the possible evolutionary status and functional significance of recalcitrance and certain associated ovule/seed characters, within the framework of modern systems of angiosperm classification. The presence of recalcitrant seed viability in 45 dicotyledonous families is significantly associated with bitegmic and crassinucellate ovules and with nuclear endosperm development, all considered ancestral (plesiomorphic) character states of the ovule; as well as with greater seed size, woody habit and tropical habitat, also regarded as ancestral character states in the dicotyledons. In many species with recalcitrant seeds, the predominant storage reserve is carbohydrate. Recalcitrance is significantly associated with the exalbuminous type of reserve storage. It is proposed that in large recalcitrant seeds, the transfer of the main storage function from endosperm to embryo was probably an early development. In many species with recalcitrance, the ovules/seeds are characterized by extensive vascularization of the integument(s)/seed coat or by a pachychalaza. Pachychalazy is proposed to be a significant functional adaptation for a more efficient transfer of nutrients to the embryo/seed. Recalcitrance and some of the other character states proposed to be plesiomorphic in dicotyledons are also present in some gymnosperms, including presumed sister groups of the dicotyledons. In relatively advanced dicotyledonous families, mostly with orthodox seeds, recalcitrance probably persisted only in isolated relict members. Determination of character polarity is particularly problematic at lower taxonomic levels, because there is always the possibility that, in some taxa, a character state such as recalcitrance may have arisen secondarily as a reversal. Available evidence supports our view that seed recalcitrance can be regarded as a relatively ancestral character state in dicotyledons.

Keywords

carbohydratesendospermevolutionovulepachychalazaseedtaxonomyvascularization
Type
Short Communication
Information
Seed Science Research , Volume 4 , Issue 2 , June 1994 , pp. 225 - 239
Copyright
Copyright © Cambridge University Press 1994

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

Akoroda, M.O. (1986) Seed desiccation and recalcitrance in Telfairia occidentalis. Seed Science and Technology 14, 327–332.Google Scholar
Baker, H.G. and Baker, I. (1979) Starch in angiosperm pollen grains and its evolutionary significance. American Journal of Botany 66, 591–600.CrossRefGoogle Scholar
Berjak, P., Farrant, J.M. and Pammenter, N.W. (1989) The basis of recalcitrant seed behaviour. Cell biology of the homoiohydrous seed condition. pp. 89–108 in Taylorson, R.B. (Ed.) Recent advances in the development and germination of seeds. New York, Plenum Press.CrossRefGoogle Scholar
Berjak, P., Farrant, J.M., Pammenter, N.W., Vertucci, C.W. and Wesley-Smith, J. (1993) Current understanding of desiccation-sensitive (recalcitrant) seeds: development, states of water and responses to dehydration and freezing. pp 705–714 in Côme, D. and Corbineau, F. (Eds) Fourth international workshop on seeds: basic and applied aspects of seed biology. Paris, ASFIS.Google Scholar
Boesewinkel, F.D. and Bouman, F. (1984) The seed: structure, pp 567–610 in Johri, B.M. (Ed.) Embryology of angiosperms. Berlin, Springer Verlag.CrossRefGoogle Scholar
Boesewinkel, F.D. and Geenen, J. (1980) Development of ovule and seed-coat of Erythroxylum coca Lamk. Acta Botanica Neerlandica 29, 231–241.CrossRefGoogle Scholar
Bouman, F. (1984) The ovule. pp 123–157 in Johri, B.M. (Ed.) Embryology of angiosperms. Berlin, Springer Verlag.CrossRefGoogle Scholar
Chase, M.W., Soltis, D.E., Olmstead, R.G., Morgan, D., Les, D.H., Mishler, B.D., Duvall, M.R., Price, R.A., Hills, H.G., Qiu, Y.-L., Kron, K.A., Rettig, J.H., Conti, E., Palmer, J.D., Manhart, J.R., Sytsma, K.J., Michaels, H.J., Kress, W.J., Karol, K.G., Clark, W.D., Hedrén, M., Gaut, B.S., Jansen, R.K., Kim, K.-J., Wimpee, C.F., Smith, J.F., Furnier, G.R., Strauss, S.H., Xiang, Q.-Y., Plunkett, G.M., Soltis, P.S., Swensen, S.M., Williams, S.E., Gadek, P.A., Quinn, C.J., Eguiarte, L.E., Golenberg, E., Learn, G.H., Graham, S.W., Barrett, S.C.H., Dayanandan, S. and Albert, V.A. (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastic gene rbc L. Annals of the Missouri Botanical Garden 80, 528–580.CrossRefGoogle Scholar
Chin, H.F., Hor, Y.L. and Mohd Lassim, M.B. (1984) Identification of recalcitrant seeds. Seed Science and Technology 12, 429–436.Google Scholar
Corbineau, F. and Côme, D. (1989) Germination and storage of recalcitrant seeds of some tropical forest tree species. Annales des Sciences Forestières 46, 89s–91s.CrossRefGoogle Scholar
Corner, E.J.H. (1949) The durian theory or the origin of the modern tree. Annals of Botany 13, 367–414.CrossRefGoogle Scholar
Corner, E.J.H. (1976) The seeds of dicotyledons, vols 1 & 2. Cambridge, Cambridge University Press.Google Scholar
Corner, E.J.H. (1992) The pachychalaza in dicotyledons: primitive or advanced? Botanical Journal of the Linnean Society 108, 15–19.CrossRefGoogle Scholar
Corthout, J., Pieters, L.A., Claeys, M., Vanden Berghe, D.A. and Vlietinck, A.J. (1991) Antiviral ellagitannins from Spondias mombin. Phytochemistry 30, 1129–1130.CrossRefGoogle Scholar
Cronquist, A. (1981) An integrated system of classification of flowering plants. New York, Columbia University Press.Google Scholar
Cronquist, A. (1988) The evolution and classification of flowering plants. 2nd edn. Bronx, New York, New York Botanical Garden.Google Scholar
Dahlgren, R.M.T. (1980) A revised system of classification of the angiosperms. Botanical Journal of the Linnean Society 80, 91–124.CrossRefGoogle Scholar
Dahlgren, R. (1983) General aspects of angiosperm evolution and macrosystematics. Nordic Journal of Botany 3, 119–149.CrossRefGoogle Scholar
Dahlgren, R. and Bremer, K. (1985) Major clades of the angiosperms. Cladistics 1, 349–368.CrossRefGoogle ScholarPubMed
Dehgan, B. and Yuen, C.K.K.H. (1983) Seed morphology in relation to dispersal, evolution, and propagation of Cycas L. Botanical Gazette 144, 412–418.CrossRefGoogle Scholar
Dodd, M.C., van Staden, J. and Smith, M.T. (1989) Seed development in Podocarpus henkelii: an ultrastructural and biochemical study. Annals of Botany 64, 297–310.CrossRefGoogle Scholar
Doyle, J.A. and Donoghue, M.J. (1986) Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Botanical Review 52, 322–431.CrossRefGoogle Scholar
Doyle, J.A. and Donoghue, M.J. (1992) Fossil and seed plant phylogeny reanalysed. Brittonia 44, 89–106.CrossRefGoogle Scholar
Ellis, R.H., Hong, T.D. and Roberts, E.H. (1991a) Effect of storage temperature and moisture on the germination of papaya seeds. Seed Science Research 1, 69–72.CrossRefGoogle Scholar
Ellis, R.H., Hong, T.D., Roberts, E.H. and Soetisna, U. (1991b) Seed storage behaviour in Elaeis guineensis. Seed Science Research 1, 99–104.CrossRefGoogle Scholar
Endress, P.K. (1990) Evolution of reproductive structures and functions in primitive angiosperms (Magnoliidae). Memoirs of the New York Botanical Garden 55, 5–34.Google Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1988) Recalcitrance – a current assessment. Seed Science and Technology 16, 155–166.Google Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1992a) Development of the recalcitrant (homoiohydrous) seeds of Avicennia marina: anatomical, ultrastructural and biochemical events associated with development from histodifferentiation to maturation. Annals of Botany 70, 75–86.CrossRefGoogle Scholar
Farrant, J.M., Berjak, P. and Pammenter, N.W. (1992b) Proteins in development and germination of a desiccation sensitive (recalcitrant) seed species. Plant Growth Regulation 11, 257–265.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1993a) Seed development in relation to desiccation tolerance: a comparison between desiccation-sensitive (recalcitrant) seeds of Avicennia marina and desiccation-tolerant types. Seed Science Research 3, 1–13.CrossRefGoogle Scholar
Farrant, J.M., Berjak, P., Cutting, J.G.M. and Pammenter, N.W. (1993b) The role of plant growth regulators in the development and germination of the desiccation-sensitive seeds of Avicennia marina. Seed Science Research 3, 55–63.CrossRefGoogle Scholar
Favre-Duchartre, M. (1984) Homologies and phylogeny. pp 697–734 in Johri, B.M. (Ed.) Embryology of angiosperms. Berlin, Springer Verlag.CrossRefGoogle Scholar
Finch-Savage, W.E. (1992) Seed development in the recalcitrant species Quercus robur L.: germinability and desiccation tolerance. Seed Science Research 2, 17–22.CrossRefGoogle Scholar
Friedman, W.E. (1992) Evidence of a pre-angiosperm origin of endosperm: implications for the evolution of flowering plants. Science 255, 336–339.CrossRefGoogle ScholarPubMed
Grabe, D.F. (1989) Report of the Seed Moisture Committee 1986–1989. Seed Science and Technology 17 (Supplement 1), 87–93.Google Scholar
Gottsberger, G. (1990) Modes of reproduction and evolution of woody angiosperms in tropical environments: introduction. Memoirs of the New York Botanical Garden 55, 1–4.Google Scholar
Grobbelaar, N. (1992) A more realistic conservation strategy for the South African cycads. PlantLife 6, 14–17.Google Scholar
Heywood, V.H. (1978) Flowering plants of the world. Oxford, Oxford University Press.Google Scholar
Hill, C.R. and Crane, P.R. (1982) Evolutionary cladistics and the origin of angiosperms. pp 269–361 in Joysey, K.A. and Friday, A.E. (Eds) Problems of phylogenetic reconstruction. Systematics Association Special Vol. 21, London, Academic Press.Google Scholar
Hofmann, P. and Steiner, A.M. (1989) An updated list of recalcitrant seeds. Landwirtschaftliche Forschung 42, 310–323.Google Scholar
Hong, T.D. and Ellis, R.H. (1990) A comparison of maturation drying, germination, and desiccation tolerance between developing seeds of Acer pseudoplatanus L. and Acer platanoides L. New Phytologist 116, 589–596.CrossRefGoogle Scholar
Jacobsen, J.V. (1984) The seed: germination. pp 611–646 in Johri, B.M. (Ed.) Embryology of angiosperms. Berlin, Springer Verlag.CrossRefGoogle Scholar
Jenkins, R. (1993) The origin of the fagaceous cupule. Botanical Reviews 59, 81–111.CrossRefGoogle Scholar
Johri, B.M., Ambegaokar, K.B. and Srivastava, P.S.(Eds) (1992) Comparative embryology of angiosperms, vols 1 & 2. Berlin, Springer Verlag.CrossRefGoogle Scholar
Kapil, R.N. and Bhatnagar, A.K. (1993) Nutritional mechanisms in the ovule and seed. Symposium Abstract 3.8.1-10 (p. 96),XV International Botanical Congress,Yokohama, Japan.Google Scholar
Khare, P.K., Yadav, V.K. and Mishra, G.P. (1989) Electrical conductivity as an indicator of orthodox and recalcitrant seed physiology in tropical forest trees. Current Science 58, 1336–1339.Google Scholar
King, M.W. and Roberts, E.H. (1979) The storage of recalcitrant seeds – achievements and possible approaches. Rome, IBPGR Secretariat.Google Scholar
King, M.W. and Roberts, E.H. (1980) Maintenance of recalcitrant seeds in storage. pp 53–89 in Chin, H.F. and Roberts, E.H. (Eds) Recalcitrant crop seeds. Kuala Lumpur, Tropical Press SDN. BHD.Google Scholar
Kramer, K.U. and Green, P.S.(Eds) (1990) Vol. 1, Pteridophytes and gymnosperms. In Kubitzki, K. (Ed.) The families and genera of vascular plants. Berlin, Springer Verlag.Google Scholar
Kubitzki, K. (1985) Ichthyochory in Gnetum venosum. Anais da Academia Brasileira de Ciencius 57, 513–516.Google Scholar
Lamont, B.B., Le Maitre, D.C., Cowling, R.M. and Enright, N.J. (1991) Canopy seed storage in woody plants. Botanical Review 57, 277–317.CrossRefGoogle Scholar
Lan, L.A. (1984) The reproductive biology of rambutan, Nephelium lappaceum L. (Sapindaceae). Gardens Bulletin 37, 181–192.Google Scholar
Loconte, H. and Stevenson, D.W. (1990) Cladistics of Spermatophyta. Brittonia 423, 197–211.CrossRefGoogle Scholar
Mabberley, D.J. (1987) The plant book. A portable dictionary of the higher plants. Cambridge, Cambridge University Press.Google Scholar
Mapes, G., Rothwell, G.W. and Haworth, M.T. (1989) Evolution of seed dormancy. Nature 377, 645–646.CrossRefGoogle Scholar
Mayer, A.M. and Poljakoff-Mayber, A. (1982) The germination of seeds, 3rd edn. Oxford, Pergamon Press.Google Scholar
Murray, D.R. (1988) Nutrition of the angiosperm embryo Taunton, Research Studies Press Ltd.Google Scholar
Natesh, S. and Rau, M.A. (1984) The embryo. pp 377–443 in Johri, B.M. (Ed.) Embryology of angiosperms. Berlin, Springer Verlag.CrossRefGoogle Scholar
Netolitzky, F. (1926) Anatomie der Angiospermen-Samen. 364 pp in Linsbauer, K. (Ed.) Handbuch der Pflanzenanatomie, Vol. 10. Berlin, Gebrüder Borntraeger.Google Scholar
Nkang, A. and Chandler, G. (1986) Changes during embryogenesis in rainforest seeds with orthodox and recalcitrant viability characteristics. Journal of Plant Physiology 126, 243–256.CrossRefGoogle Scholar
Oparka, K. J. (1990) What is phloem unloading? Plant Physiology 94, 393–396.CrossRefGoogle ScholarPubMed
Passioura, J.B. (1979) Accountability, philosophy and plant physiology. Search 10, 347–350.Google Scholar
Robbertse, P.J., von Teichman, I. and van Rensburg, H.J. (1986) A re-evaluation of the mango ovule in comparison with those of a few other Anacardiaceae species. South African Journal of Botany 52, 17–24.CrossRefGoogle Scholar
Scalbert, A. (1991) Antimicrobial properties of tannins. Phytochemistry 30, 3875–3883.CrossRefGoogle Scholar
Soepadmo, E. and Eow, B.K. (1977) The reproductive biology of Durio zibethinus Murr. Gardens Bulletin 29, 25–33.Google Scholar
Sporne, K.R. (1974) The morphology of gymnosperms, 2nd edn. London, Hutchinson & Co.Google Scholar
Sporne, K.R. (1980) A re-investigation of character correlations among dicotyledons. New Phytologist 85, 419–449.CrossRefGoogle Scholar
Sporne, K.R. (1982) The advancement index vindicated. New Phytologist 91, 137–145.CrossRefGoogle Scholar
Stebbins, G.L. (1974) Flowering plants. Evolution above the species level. Cambridge (MA), Harvard University Press.CrossRefGoogle Scholar
Steyn, E.M.A. and Robbertse, P.J. (1992) Is aril development in the litchi triggered by pollen tube growth? South African Journal of Botany 58 258–262.CrossRefGoogle Scholar
Steyn, E.M.A., Robbertse, P.J. and Smith, D. (1993) An anatomical study of ovary-to-cuke development in consistently low-producing trees of the ‘Fuerte’ avocado (Persea americana Mill.) with special reference to seed abortion. Sexual Plant Reproduction 6, 87–97.CrossRefGoogle Scholar
Sytnik, K.M. and Martyn, G.I. (1993) The cell ultrastructure of Acer saccharinum L. and Acer tataricum L. seed embryos differing in deepness of dormancy. Poster Abstract 6085 (p. 441), XV International Botanical Congress, Yokohama, Japan.Google Scholar
Takhtajan, A. (1991) Evolutionary trends in flowering plants. New York, Columbia University Press.Google Scholar
Terui, K. and Okagami, N. (1993) Temperature effects on seed germination of East Asian and Tertiary relict species of Dioscorea (Dioscoreaceae). American Journal of Botany 80, 493–499.CrossRefGoogle ScholarPubMed
Thorne, R.F. (1992) Classification and geography of the flowering plants. Botanical Review 58, 225–348.CrossRefGoogle Scholar
Tompsett, P.B. (1982) The effect of desiccation on the longevity of seeds of Araucaria hunsteinii and A. cunninghamii. Annals of Botany 50, 693–704.CrossRefGoogle Scholar
Tompsett, P.B. (1984) Desiccation studies in relation to the storage of Araucaria seed. Annals of Applied Biology 105, 581–586.CrossRefGoogle Scholar
Tompsett, P.B. (1992) A review of the literature on the storage of dipterocarp seeds. Seed Science and Technology 20, 251–267.Google Scholar
van Wyk, A.E. and Botha, R. (1984) The genus Eugenia (Myrtaceae) in southern Africa: ontogeny and taxonomic value of the seed. South African Journal of Botany 3, 63–80.CrossRefGoogle Scholar
van Wyk, A.E. and von Teichman, I. (1993) Evolutionary status of pachychalazy in angiosperm ovules and seed. Symposium Abstract 3.8.1-9 (p. 96), XV International Botanical Congress, Yokohama, Japan.Google Scholar
Vaughan, J.G. (1970) The structure and utilization of oil seeds. London, Chapman & Hall Ltd.Google Scholar
Vivrette, N.J. (1993) The relationship between embryo development and germination in seeds. Poster Abstract 2099 (p. 277), XV International Botanical Congress, Yokohama, Japan.Google Scholar
von Teichman, I. (1993) Development and structure of the seed of Ozoroa paniculosa (Anacardiaceae) and taxonomic notes. Botanical Journal of the Linnean Society 111, 463–470.CrossRefGoogle Scholar
von Teichman, I. and van Wyk, A.E. (1991) Trends in the evolution of dicotyledonous seeds based on character associations, with special reference to pachychalazy and recalcitrance. Botanical Journal of the Linnean Society 105, 211–237.CrossRefGoogle Scholar
von Teichman, I., Robbertse, P.J. and Schoonraad, E. (1988) The structure of the seed of Mangifera indica L. and notes on seed characters of the tribe Mangifereae (Anacardiaceae). South African Journal of Botany 54, 472–476.CrossRefGoogle Scholar
Whitmore, T.C. (1991) An introduction to tropical rain forests, reprinted. Oxford, Clarendon Press.Google Scholar
Wing, S.L. and Tiffney, B.H. (1987) The reciprocal interaction of angiosperm evolution and tetrapod herbivory. Review of Palaeobotany and Palynology 50, 179–210.CrossRefGoogle Scholar
Wolswinkel, P. (1992) Transport of nutrients into developing seeds: a review of physiological mechanisms. Seed Science Research 2, 59–73.CrossRefGoogle Scholar
Zavaleta-Mancera, H.A. and Engleman, E.M. (1991) Structure and development of ovule and seed in Manilkara zapota (Sapotaceae). Abstract 97, Botanical Society of America Conference. American Journal of Botany 78 (Supplement), p. 38.Google Scholar