Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-04T21:56:22.144Z Has data issue: false hasContentIssue false

A critical update on seed dormancy. I. Primary dormancy1

Published online by Cambridge University Press:  19 September 2008

Henk W. M. Hilhorst*
Affiliation:
Dept. of Plant Physiology, Wageningen Agricultural University, Arboretumlaan 4, NL-6703 BD Wageningen, Netherlands
*
*Correspondence

Abstract

The emphasis of modern dormancy research is almost entirely on the form of dormancy that is acquired during seed development, primary dormancy. Abscisic acid (ABA) appears to be intimately involved in its regulation. The action of abscisic acid has also been implied in many other developmental processes. The coincidence of developmental events, such as dehydration and completion of maturation, with the acquisition of primary dormancy suggests that dormancy is influenced by these processes. Germinability, both during development and after maturation, is sometimes directly correlated with ABA content. The lack of such a correlation may be explained by assuming a decisive role for the responsiveness to ABA or other overriding factors. ABA has been detected in all seed components. The different seed tissues may all contribute, to various extents, to the degree of whole seed dormancy. It is concluded that ABA action in dormancy regulation is not restricted to the embryo but is also located in endospermic tissue. In addition, a role of ABA in the morphological development of germination modifying seed tissues is proposed. The mechanism for ABA action appears to be associated with cell wall properties.

Type
Review Article
Copyright
Copyright © Cambridge University Press 1995

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.)

Footnotes

1

An update on secondary dormancy will be published in a later issue of the journal

References

Albersheim, P. (1976) The primary cell wall. pp 225274 in Bonner, J. and Varner, J.E. (Eds) Plant biochemistry. New York, Academic Press.CrossRefGoogle Scholar
Anderberg, R.J. and Walker-Simmons, M.K. (1994) Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. Proceedings of the National Academy of Sciences, USA 89, 1018310187.CrossRefGoogle Scholar
Benech Arnold, R.L., Fenner, M. and Edwards, P.J. (1991) Changes in germinability, ABA content and ABA embryonic sensitivity in developing seeds of Sorghum bicolor (L.) Moench. induced by water stress during grain filling. New Phytologist 118, 339347.CrossRefGoogle ScholarPubMed
Berry, T. and Bewley, J.D. (1992) A role for the surrounding fruit tissues in preventing the germination of tomato (Lycopersicon esculentum) seeds. Plant Physiology 100, 951957.CrossRefGoogle ScholarPubMed
Berry, T. and Bewley, J.D. (1993) Comparisons between the roles of the fruit tissues, osmoticum and abscisic acid in maintaining tomato seed development and storage protein synthesis. Seed Science Research 3, 2534.CrossRefGoogle Scholar
Bewley, J.D. and Black, M. (1982) Physiology and biochemistry of seeds. Vol. 2. Viability, dormancy and environmental control. Berlin, Springer-Verlag.Google Scholar
Bewley, J.D. and Black, M. (1994) Seeds. Physiology of development and germination. New York, London, Plenum Press.CrossRefGoogle Scholar
Bianco, J., Garello, G. and Le Page-Degivry, M.T. (1994) Release of dormancy in sunflower embryos by dry storage: involvement of gibberellins and abscisic acid. Seed Science Research 4, 5762.CrossRefGoogle Scholar
Black, M. (1991) Involvement of ABA in the physiology of developing and mature seeds, pp 99124 in Davies, W.J. and Jones, H.G. (Eds) Absisic acid. Physiology and biochemistry. Oxford, BIOS Scientific Publishers.Google Scholar
Bowler, C. and Chua, N.M. (1994) Emerging themes of plant signal transduction. Plant Cell 6, 15291541.Google ScholarPubMed
Braun, J.W. and Khan, A.A. (1975) Endogenous abscisic acid levels in germinating and non-germinating lettuce seed. Plant Physiology 56, 731733.CrossRefGoogle Scholar
Bray, E.A. (1988) Drought- and ABA-induced changes in polypeptide and mRNA accumulation in tomato leaves. Plant Physiology 88, 12101214CrossRefGoogle ScholarPubMed
Carpita, N.C. and Gibeaut, D.M. (1993) Structural model of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant Journal 3, 130.CrossRefGoogle ScholarPubMed
Chandler, P.M. and Robertson, M. Gene expression regulated by abscisic acid and its relation to stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 45, 113141.CrossRefGoogle Scholar
Debeaujon, I., Léon-Kloosterziel, K., Peeters, T. and Koornneef, M. (1994) Genetics of seed dormancy in Arabidopsis thaliana. p 98 in Lang, G.A. (Ed.) Abstract. 1st International Symposium on Plant Dormancy, Corvallis (USA).Google Scholar
DeBruijn, S.M. (1993) Abscisic acid and assimilate partitioning during seed development. PhD Thesis, Wageningen Agricultural University, Netherlands.Google Scholar
DeBruijn, S.M., Ooms, J.J.J., Basra, A.S., van Lammeren, A.A.M. and Vreugdenhil, D. (1993) Influence of abscisic acid on storage of lipids and carbohydrates in developing Arabidopsis seeds. pp 103108 in Côme, D. and Corbineau, F. (Eds) Fourth International Workshop on Seeds. Basic and applied aspects of seed biology. Paris, ASFIS.Google Scholar
Dekker, J., Dekker, B., Hilhorst, H.W.M. and Karssen, C.M. (1994) Multiple germinability-dormancy states in Setaria faberii: changes in embryos with development from anthesis to after-ripening. p 196 in Lang, G.A. (Ed.) Abstract. 1st International Symposium on Plant Dormancy, Corvallis (USA).Google Scholar
Derkx, M.P.M. and Karssen, C.M. (1993) Variability in light-, gibberellin- and nitrate-requirement of Arabidopsis thaliana seeds due to harvest time and conditions of dry storage. Journal of Plant Physiology 141, 574582.CrossRefGoogle Scholar
Derkx, M.P.M., Vermeer, E. and Karssen, C.M. (1994) Gibberellins in seeds of Arabidopsis thaliana: biological activities, identification and effects of light and chilling on endogenous levels. Plant Growth Regulation 15, 223234.CrossRefGoogle Scholar
Dulson, J., Bewley, J.D. and Johnston, R.N. (1988) Abscisic acid is an endogenous inhibitor in the regulation of mannanase production by isolated lettuce (Lactuca sativa cv Grand Rapids) endosperms. Plant Physiology 87, 660666.CrossRefGoogle Scholar
Fanutti, C., Gidley, M.J. and Reid, J.S.G. (1993) Action of a pure xyloglucan endo-transglycolase (formerly called xyloglucan-specific endo-(14)-β-D-glucanase) from the cotyledons of germinated nasturtium seeds. Plant Journal 3, 691700.CrossRefGoogle Scholar
Fong, F., Smith, J.D. and Koehler, D.E. (1983) Early events in maize seed development: 1-methyl-3-phenyl-5-(3-[trifluoromethyl]phenyl)-4-(1H)-pyridinone induction of vivipary. Plant Physiology 73, 899901.CrossRefGoogle Scholar
Fry, S.C. (1989) Cellulases, hemicelluloses and auxin-stimulated growth: a possible relationship. Physiologia Plantarum 75, 532536.CrossRefGoogle Scholar
Fry, S.C., Smith, R.C., Renwick, K.F., Martin, D.J., Hodge, S.K. and Matthews, K.J. (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochemical Journal 282, 821828.CrossRefGoogle ScholarPubMed
Galau, G.A., Jakobsen, K.S. and Hughes, D.W. (1991) The controls of late dicot embryogenesis and early germination. Physiologia Plantarum 81, 280288.CrossRefGoogle Scholar
Garcia-Maya, M., Chapman, J.M. and Black, M. (1990) Regulation of -amylase formation and gene expression in the developing wheat embryo. Role of abscisic acid, the osmotic environment and gibberellin. Planta 181, 296303.CrossRefGoogle ScholarPubMed
Goldmark, P.J., Curry, J., Morris, C.F. and Walker-Simmons, M.K. (1992) Cloning and expression of an embryo-specific mRNA up-regulated in hydrated dormant seeds. Plant Molecular Biology 19, 433441.CrossRefGoogle ScholarPubMed
Groot, S.P.C. (1987) Hormonal regulation of seed development and germination in tomato. Studies on abscisic acid- and gibberellin-deficient mutants. PhD Thesis, Wageningen Agricultural University, Netherlands.Google Scholar
Groot, S.P.C. and Karssen, C.M. (1992) Dormancy and germination of abscisic acid-deficient tomato seeds. Studies with the sitiens mutant. Plant Physiology 99, 952958.CrossRefGoogle ScholarPubMed
Groot, S.P.C., Kieliszewska-Rokicka, B., Vermeer, E. and Karssen, C.M. (1988) Gibberellin-induced hydrolysis of endosperm cell walls in gibberellin-deficient tomato seeds prior to radicle protrusion. Planta 174, 500504.CrossRefGoogle ScholarPubMed
Groot, S.P.C., van Yperen, I.I. and Karssen, C.M. (1991) Strongly reduced levels of endogenous abscisic acid in developing seeds of tomato mutant sitiens do not influence in vivo accumulation of dry matter and storage proteins. Physiologia Plantarum 81, 7378.CrossRefGoogle Scholar
Halmer, P. (1985) The mobilization of storage carbohydrates in germinated seeds. Physiologie Végetale 23, 107125.Google Scholar
Hayashi, T. (1989) Xyloglucans in the primary cell wall. Annual Review of Plant Physiology and Plant Molecular Biology 40, 139168.CrossRefGoogle Scholar
Hilhorst, H.W.M. (1993) New aspects of seed dormancy. pp 571579 in Côme, D. and Corbineau, F. (Eds) Fourth International Workshop on Seeds. Basic and applied aspects of seed biology. Paris, ASFIS.Google Scholar
Hilhorst, H.W.M. and Downie, B. (1994) Dormancy and germination of abscisic acid-deficient tomato seeds. Further studies with the sitiens mutant. Plant Physiology (Supplement) 105, 167.Google Scholar
Hilhorst, H.W.M. and Karssen, C.M. (1992) Seed dormancy and germination: The role of abscisic acid and gibberellins and the importance of hormone mutants. Plant Growth Regulation 11, 225238.CrossRefGoogle Scholar
Hilhorst, H.W.M., Smitt, A.I. and Karssen, C.M. (1986) Gibberellin-biosynthesis and sensitivity mediated stimulation of seed germination of Sisymbrium officinale by red light and nitrate. Physiologia Plantarum 67, 285290.CrossRefGoogle Scholar
Hsu, F.C. (1979) Abscisic acid accumulation in developing seeds of Phaseolus vulgaris L. Plant Physiology 63, 552556.CrossRefGoogle ScholarPubMed
Karssen, C.M. (1982) Seasonal patterns of dormancy in weed seeds. pp 243270 in Khan, A.A. (Ed.) The physiology and biochemistry of seed development, dormancy and germination. Amsterdam, New York, Oxford, Elsevier Biomedical Press.Google Scholar
Karssen, C.M. and Laçka, E. (1986) A revision of the hormone balance theory of seed dormancy: studies on gibberellin and/or abscisic acid-deficient mutants of Arabidopsis thaliana. pp 315323 in Bopp, M. (Ed.) Plant growth substances 1985. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Karssen, C.M., Brinkhorst-van, der, Swan, D.L.C., Breekland, A.E. and Koornneef, M. (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana. Planta 157, 158165.CrossRefGoogle ScholarPubMed
Karssen, C.M., Groot, S.P.C. and Koornneef, M. (1987) Hormone mutants and seed dormancy in Arabidopsis and tomato. pp 119134 in Thomas, A.A. and Grierson, D. (Eds) Developmental mutants in higher plants. Cambridge, Cambridge University Press.Google Scholar
Kelly, K.M., Van Staden, J. and Bell, W.E. (1992) Seed coat structure and dormancy. Plant Growth Regulation 11, 201209.CrossRefGoogle Scholar
Kermode, A.R. (1990) Regulatory mechanisms involved in the transition from seed development to germination. Critical Reviews in Plant Science 9, 155195.CrossRefGoogle Scholar
Koornneef, M., Jorna, M.L., Brinkhorst-van der Swan, D.L.C. and Karssen, C.M. (1982) The isolation of abscisic acid (ABA)-deficient mutants by selection of induced revertants in non-germinating gibberellin-sensitive lines of Arabidopsis thaliana (L.) Heynh. Theoretical and Applied Genetics 61, 385393.CrossRefGoogle ScholarPubMed
Koornneef, M., Reuling, G. and Karssen, C.M. (1984) The isolation and characterization of abscisic acid insensitive mutants of Arabidopsis thaliana. Physiologia Plantarum 61, 377383.CrossRefGoogle Scholar
Koornneef, M., Cone, J.W., Karssen, C.M., Kendrick, R.E., Van der Veen, J.H. and Zeevaart, J.A.D. (1985) Plant hormone and photoreceptor mutants in Arabidopsis and tomato. pp 112 in Freeling, M. (Ed.) Plant genetics, UCLA symposia on molecular and cellular biology, New Series, Vol. 35. New York, Alan Liss Inc.Google Scholar
Koornneef, M., Hanhart, C.J., Hilhorst, H.W.M. and Karssen, C.M. (1989) In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiology 90, 463469.CrossRefGoogle ScholarPubMed
Kutschera, U. and Schopfer, P. (1986) Effect of auxin and abscisic acid on cell wall extensibility in maize coleoptiles. Planta 167, 527535.CrossRefGoogle ScholarPubMed
Lang, A.G., Early, J.D., Martin, G.C. and Darnell, R.L. (1987) Endo-, para- and ecodormancy; physiological terminology and classification for dormancy research. HortScience 22, 371377.CrossRefGoogle Scholar
Le Page-Degivry, M.T. and Garello, G. (1992) In situ abscisic acid synthesis. A requirement for induction of embryo dormancy in Helianthus annuus. Plant Physiology 98, 13861390.CrossRefGoogle ScholarPubMed
Léon-Kloosterziel, K.M., Keijzer, C. and Koornneef, M. (1994) A seed shape mutant of Arabidopsis that is affected in integument development. Plant Cell 6, 385392.CrossRefGoogle ScholarPubMed
Leung, J., Bouvier-Durand, M., Morris, P.C., Guerrier, D., Chefdor, F. and Giraudat, J. (1994) Arabidopsis ABA response gene ABI1: Features of a calcium-modulated protein phosphatase. Science 264, 14481452.CrossRefGoogle ScholarPubMed
Longland, J.M., Fry, S.C. and Trewavas, A.J. (1989) Developmental control of apiogalacturonan biosynthesis and UDP-apiose production in a duckweed. Plant Physiology 90, 972976.CrossRefGoogle Scholar
Malek, L. and Bewley, J.D. (1991) Endo-β-mannanase activity and reserve mobilization in excised endosperms of fenugreek is affected by volume of incubation and abscisic acid. Seed Science Research 1, 4549.CrossRefGoogle Scholar
McCarty, D.R. and Carson, C.B. (1991) The molecular genetics of seed maturation in maize. Physiologia Plantarum 81, 267272.CrossRefGoogle Scholar
McLeary, B.V. (1988) β-D-Mannanase. Methods in enzymology 160, 596610.CrossRefGoogle Scholar
Meurs, C., Basra, A.S., Karssen, C.M. and VanLoon, L.C. (1992) Role of abscisic acid in the induction of desiccation tolerance in developing seeds of Arabidopsis thaliana. Plant Physiology 98, 14841493.CrossRefGoogle ScholarPubMed
Meyer, K., Leube, M.P. and Grill, E. (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264, 14521455.CrossRefGoogle ScholarPubMed
Morris, C.F., Anderberg, R.J., Goldmark, P.J. and Walker-Simmons, M.K. (1991) Molecular cloning and expression of abscisic acid responsive genes in embryos of dormant wheat seeds. Plant Physiology 95, 814821.CrossRefGoogle ScholarPubMed
Ni, B.R. and Bradford, K.J. (1992) Quantitative models describing the sensitivity of tomato seed germination to abscisic acid and osmoticum. Plant Physiology 98, 10571068.CrossRefGoogle ScholarPubMed
Ni, B.R. and Bradford, K.J. (1993) Germination and dormancy of abscisic acid- and gibberellin-deficient mutant tomato (Lycopersicon esculentum) seeds. Plant Physiology 101, 607617.CrossRefGoogle ScholarPubMed
Nikolaeva, M.G. (1977) Factors controlling the seed dormancy pattern. pp 5174 in Khan, A.A. (Ed.) The physiology and biochemistry of seed dormancy and germination. Amsterdam, New York, Oxford, North-Holland Publishing Company.Google Scholar
Ooms, J.J.J., van der Veen, R. and Karssen, C.M. (1994) Abscisic acid and osmotic stress or slow drying independently induce desiccation tolerance in mutant seeds of Arabidopsis thaliana. Physiologia Plantarum 92, 506510.CrossRefGoogle Scholar
Ooms, J.J.J., Léon-Kloosterziel, K.M., Bartels, D., Koornneef, M. and Karssen, C.M. (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana. A comparative study using ABA-insensitive abi3 mutants. Plant Physiology 102, 11851191CrossRefGoogle ScholarPubMed
Perry, T.O. and Byrne, O.R. (1969) Turion induction in Spirodela polyrrhiza by abscisic acid. Plant Physiology 44, 784785.CrossRefGoogle ScholarPubMed
Reid, J.S.G. (1985) Cell wall storage carbohydrate in seeds: biochemistry of the seed ‘gums and hemicelluloses’. Advances in Botanical Research 11, 125155.CrossRefGoogle Scholar
Robertson, M., Walker-Simmons, M., Munro, D. and Hill, R.D. (1989) Induction of α-amylase inhibitor synthesis in barley embryos and young seedlings by abscisic acid and dehydration stress. Plant Physiology 91, 415420.CrossRefGoogle Scholar
Sánchez, R.A., De Miguel, L. and Mercuri, O. (1986) Phytochrome control of cellulase activity in Datura ferox L. seeds and its relationship with germination. Journal of Experimental Botany 37, 15741580.Google Scholar
Sánchez, R.A., Sunell, S., Labavitch, J.M. and Bonner, B.A. (1990) Changes in the endosperm cell walls of two Datura species before radicle protrusion. Plant Physiology 93, 8997.CrossRefGoogle ScholarPubMed
Schopfer, P. and Plachy, C. (1984) Control of seed germination by abscisic acid. II. Effect on embryo water uptake in Brassica napus. Plant Physiology 64, 822827.CrossRefGoogle Scholar
Schopfer, P. and Plachy, C. (1985) Control of seed germination by abscisic acid. III. effect on embryo growth potential (minimum turgor pressure) and growth coefficient (cell wall extensibility) in Brassica napus L. Plant Physiology 77, 676686.CrossRefGoogle Scholar
Simpson, G.M. (1990) Seed dormancy in grasses. Cambridge, New York Melbourne, Cambridge University Press.CrossRefGoogle Scholar
Smith, R.C., Matthews, P.R. and Chandler, P.M. (1994) Gibberellin regulation of xyloglucan endotransglycolase in barley. Plant Physiology (Supplement) 105, 56.Google Scholar
Spyropoulos, C.G. and Reid, J.S.G. (1988) Water stress and galactomannan breakdown in germinated fenugreek seeds. Stress affects the production and the activities in vivo of galactomannan-hydrolysing enzymes. Planta 174, 473478.CrossRefGoogle ScholarPubMed
Taiz, L. (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annual Review of Plant Physiology 35, 585657.CrossRefGoogle Scholar
Totterdell, S. and Roberts, E.H. (1979) Effects of low temperature on the loss of innate dormancy and the development of induced dormancy in seeds of Rumex obtusifolius L. and Rumex crispus. Plant, Cell & Environment 2, 131138.CrossRefGoogle Scholar
Toyomasu, T., Tsuji, H., Yamane, H., Nakayama, M., Yamaguchi, I., Murofushi, N., Takahashi, N. and Inoue, Y. (1993) Light effects on endogenous levels of gibberellins in photoblastic lettuce seeds. Journal of Plant Growth Regulation 12, 8590.CrossRefGoogle Scholar
Toyomasu, T., Yamane, H., Murofushi, N. and Inoue, Y. (1994) Effects of exogenously applied gibberellin and red light on the endogenous levels of abscisic acid in photoblastic lettuce seeds. Plant & Cell Physiology 35, 127129.Google Scholar
Trewavas, A.J. and Jones, H.G. (1991) An assessment of the role of ABA in plant development. pp 169188 in Davies, W.J. and Jones, H.G. (Eds) Absisic acid. Physiology and biochemistry. Oxford, BIOS Scientific Publishers.Google Scholar
Vögeli-Lange, R., Fründt, C., Hart, C.M., Beffe, R., Nagy, F. and Meins, F. (1994) Evidence for a role of β-1, 3-glucanase in dicot seed germination. Plant Journal 5, 273278.CrossRefGoogle Scholar
Wakabayashi, K., Sakurai, N. and Kuraishi, S. (1989) Effects of ABA on synthesis of cell-wall polysaccharides in segments of etiolated squash hypocotyl. I. Changes in incorporation of glucose and myo-inositol into cell-wall components. Plant Cell Physiology 30, 99105.CrossRefGoogle Scholar
Wakabayashi, K., Sakurai, N. and Kuraishi, S. (1991) Effects of abscisic acid on synthesis of cell-wall polysaccharides in segments of etiolated squash hypocotyl. II. Levels of UDP-neutral sugars. Plant Cell Physiology 32, 427432.CrossRefGoogle Scholar
Walker-Simmons, M. (1987) ABA levels and sensitivity in developing wheat embryos of sprouting resistant and susceptible cultivars. Plant Physiology 84, 6166.CrossRefGoogle ScholarPubMed
Walker-Simmons, M. (1988) Enhancement of ABA responsiveness in wheat embryos by high temperature. Plant, Cell and Environment 11, 769775.CrossRefGoogle Scholar
Wang, T.L., Cook, S.K., Francis, R.J., Ambrose, M.J. and Hedley, C.L. (1987) An analysis of seed development in Pisum sativum. VI. Abscisic acid accumulation. Journal of Experimental Botany 38, 19211932.CrossRefGoogle Scholar
Watkins, J.T. and Cantliffe, D.J. (1983) Mechanical resistance of the seed coat and endosperm during germination of Capsicum annuum at low temperature. Plant Physiology 72, 146150.CrossRefGoogle ScholarPubMed
Welbaum, G.E., Tissaoui, T. and Bradford, K.J. (1990) Water relations of seed development and germination in muskmelon (Cucumis melo L.). III. Sensitivity of germination to water potential and abscisic acid during development. Plant Physiology 92, 10291037.CrossRefGoogle ScholarPubMed
Wilen, R.W., Mandel, R.M., Pharis, R.P., Holbrook, L.A. and Moloney, M.M. (1990) Effects of abscisic acid and high osmoticum on storage protein gene expression in microspore embryos of Brassica napus. Plant Physiology 94, 875881.CrossRefGoogle ScholarPubMed
Xu, N. and Bewley, J.D. (1991) Sensitivity to abscisic acid and osmoticum changes during embryogenesis of alfalfa (Medicago sativa). Journal of Experimental Botany 42, 821826.CrossRefGoogle Scholar
Xu, N., Coulter, K.M. and Bewley, J.D. (1990) Abscisic acid and osmoticum prevent germination of developing alfalfa embryos, but only osmoticum maintains the synthesis of developmental proteins. Planta 182, 382390.CrossRefGoogle ScholarPubMed