Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-18T11:20:10.126Z Has data issue: false hasContentIssue false
  • English
  • Français

The mechanisms of desiccation tolerance in developing seeds

Published online by Cambridge University Press:  19 September 2008

O. Leprince ,
G. A. F. Hendry  and
B. D. McKersie
O. Leprince*
Affiliation:
Plant Morphology Laboratory, Department of Botany, B22 Sart Tilman, B4000 Liège, Belgium
G. A. F. Hendry
Affiliation:
Unit of Comparative Plant Ecology, Department of Animal Sciences, The University, Sheffield, S10 2TN, UK
B. D. McKersie
Affiliation:
Department of Crop Science, University of Guelph, Guelph, Ontario, N1G 2W1, Canada
*
* Correspondence and present address Department of Crop Science, University of Guelph, Guelph, Ontario N1G 2W1Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

Desiccation tolerance is one of the most fundamental properties of seeds. It is acquired late in seed development and is considered necessary for the completion of the plant's life cycle, as an adaptive strategy to enable seed survival during storage or environmental stress, and to ensure better dissemination of the species. The role of water status in desiccated tissues and problems related to testing tolerance in seeds are reviewed. The molecular mechanisms of desiccation tolerance has received extensive consideration only during this past decade. There is a general consensus that desiccation tolerance involves the protection of cellular membranes from the deleterious effect of water removal and the resultant necessity to maintain the bilayer structure in the absence of an aqueous environment. Therefore, some aspects of desiccation-induced membrane injury are described. Several strategies for coping with cellular desiccation have been identified the presence of high amounts of non-reducing sugars, the efficiency of free radical-scavenging systems and the expression of desiccation- and/or ABA-regulated genes. These molecular mechanisms allowing cellular protection are reviewed together with their respective role in dessication tolerance. It is concluded that desiccation tolerance is not likely to be ascribed to a single mechanism but rather to a multifactorial property in which each component is equally critical.

Keywords

antioxidantscarbohydratesdesiccation tolerancegene expressionmembrane damageoxygen free radicalsseed developmentwater status
Type
Review Articles
Information
Seed Science Research , Volume 3 , Issue 4 , December 1993 , pp. 231 - 246
Copyright
Copyright © Cambridge University Press 1993

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

Ackerson, R C. (1984) Abscisic acid and precocious germination in soybeans. Journal of Experimental Botany 35, 414–421CrossRefGoogle Scholar
Adams, C.A and Rinne, R.W (1980) Moisture content as a controlling factor in seed development and germination International Review of Cytology 68, 1–8CrossRefGoogle Scholar
Almonguera, C. and Jordano, J. (1992) Developmental and environmental concurrent expression of sunflower dry-seed-stored low molecular-weight heat-shock protein and Lea mRNAs Plant Molecular Biology 19, 781–792CrossRefGoogle Scholar
Alscher, R G (1989) Biosynthesis and antioxidant function of glutathione in plants Physiologia Plantarum 77, 457–464CrossRefGoogle Scholar
Anandarajah, K and McKersie, B.D (1990) Manipulating the desiccation tolerance and vigor of dry somatic embryos of Medicago sativa L. with sucrose, heat shock and abscisic acid Plant Cell Reports 9, 451–455CrossRefGoogle ScholarPubMed
Baker, J., Steele, C and Dure, L. III. (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Molecular Biology 11, 277–291CrossRefGoogle ScholarPubMed
Bartels, D., Singh, M. and Salamini, F (1988) Onset of desiccation tolerance during development of the barley embryo Planta 175, 485–492CrossRefGoogle ScholarPubMed
Bartels, D., Schneider, K., Terstappen, G., Piatkowski, D and Salamini, F. (1990) Molecular cloning of abscisic acid modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181, 27–34CrossRefGoogle ScholarPubMed
Berjak, P., Farrant, J.M and Pammenter, N W (1990) The basis of recalcitrant seed behavior 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 PressGoogle Scholar
Berjak, P, Pammenter, N.W and Vertucci, C (1992) Homoiohydrous (recalcitrant) seeds developmental status, desiccation sensitivity and the state of water in axes of Landolphia kirkii Dyer Planta 186, 249–261CrossRefGoogle ScholarPubMed
Berry, T and Bewley, J.D. (1991) Seeds of tomato (Lycoperiscon esculentum Mill.) which develop in a fully hydrated environment in the fruit switch from a developmental to a germinative mode without a requirement for desiccation Planta 186, 27–34CrossRefGoogle Scholar
Bewley, J D. (1979) Physiological aspects of desiccation tolerance Annual Review of Plant Physiology 30, 195–238CrossRefGoogle Scholar
Bewley, J.D., Kermode, A R and Misra, S (1989) Desiccation and minimal drying treatments of seeds of castor bean and Phaseolus vulgaris which terminate development and promote germination cause changes in protein and messenger RNA synthesis Annals of Botany 63, 3–17CrossRefGoogle Scholar
Blackman, S A., Wettlaufer, S.H., Obendorf, R.L and Leopold, A.C (1991) Maturation proteins associated with desiccation tolerance in soybean Plant Physiology 96, 868–874CrossRefGoogle ScholarPubMed
Blackman, S.A., Obendorf, R.L. and Leopold, A C (1992) Maturation proteins and sugars in desiccation tolerance of developing seeds Plant Physiology 100, 225–230CrossRefGoogle Scholar
Bochicchio, A, Vazzana, C, Raschi, A., Bartels, D and Salamini, F (1988) Effect of desiccation on isolated embryos of maize Onset of desiccation tolerance during development Agronomie 8, 29–36CrossRefGoogle Scholar
Bostock, R.M. and Quatrano, R S (1992) Regulation of Em gene expression in rice. Interaction between osmotic stress and abscisic acid Plant Physiology 98, 1356–1363CrossRefGoogle ScholarPubMed
Bradford, K J and Chandler, P.M. (1992) Expression of “dehydrin-like” proteins in embryos and seedlings of Zizania palustris and Oryza sativa during dehydration Plant Physiology 99, 488–494CrossRefGoogle ScholarPubMed
Bruni, F and Leopold, A.C. (1991) Glass transition in soybean seed Relevance to anhydrous biology. Plant Physiology 96, 660–663CrossRefGoogle ScholarPubMed
Bruni, F. and Leopold, A.C. (1992) Pools of water in anhydro-biotic organisms A thermally stimulated depolarization current study. Biophysical Journal 63, 663–672CrossRefGoogle ScholarPubMed
Buchvarov, P. and Gantcheff, Ts. (1984) Influence of accelerated and natural aging on free radical levels in soybean seeds. Physiologia Plantarum 60, 53–56CrossRefGoogle Scholar
Burke, M.J. (1986) The glassy state and survival of anhydrous biological systems. pp 358–363 in Leopold, A.C. (Ed.) Membrane, metabolism and dry organisms. Ithaca, Cornell University PressGoogle Scholar
Burton, G.W and Ingold, K.U. (1984) β-carotene: an unusual type of lipid antioxidant. Science 224, 569–573CrossRefGoogle ScholarPubMed
Caffrey, M., Fonseca, V. and Leopold, A.C. (1988) Lipidsugar interactions. Relevance to anhydrous biology. Plant Physiology 86, 754–758CrossRefGoogle ScholarPubMed
Cakmak, I, Strbac, D and Marschner, H. (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. Journal of Experimental Botany 44, 127–132CrossRefGoogle Scholar
Carpenter, J.F., Crowe, L M. and Crowe, J H. (1987) Stabilization of phosphofructokinase with sugars during freeze-drying: characterization of enhanced protection in the presence of divalent cations. Biochimica et Biophysica Acta 923, 109–115CrossRefGoogle ScholarPubMed
Carpenter, J.F., Crowe, J H. and Arakawa, T. (1990) Comparison of solute-induced protein stabilization in aqueous solution and in the frozen and dried states. Journal of Dairy Science 73, 3627–3636CrossRefGoogle Scholar
Chen, Y. and Burris, J.S. (1990) Role of carbohydrates in desiccation tolerance and membrane behavior in maturing maize seed Crop Science 30, 971–975CrossRefGoogle Scholar
Chia, L.S., McRae, D G. and Thompson, J.E. (1982) Light-dependence of paraquat-initiated membrane deterioration in bean plants Evidence for the involvement of super-oxide Physiologia Plantarum 56, 492–499CrossRefGoogle Scholar
Crèvecoeur, M., Deltour, R. and Bronchart, R (1976) Cytological study on water stress during germination of Zea mays. Planta 132, 31–41CrossRefGoogle Scholar
Crowe, J.H, Crowe, L.M. and Chapman, D. (1984a) Preservation of membranes in anhydriobiotic organisms the role of trehalose Science 223, 701–703CrossRefGoogle ScholarPubMed
Crowe, J.H., Crowe, L M. and Chapman, D. (1984b) Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Archives of Biochemistry and Biophysics 232, 400–407CrossRefGoogle ScholarPubMed
Crowe, L.M., Crowe, J.H. and Chapman, D (1985) Interaction of carbohydrates with dry dipalmitoylphos-phatidylcholine. Archives of Biochemistry and Biophysics 236, 289–296CrossRefGoogle Scholar
Crowe, L.M, Womersley, C, Crowe, J.H., Reid, D., Appel, L. and Rudolph, A.S (1986) Prevention of fusion and leakage in freeze-dried liposomes by carbohydrates Biochimica et Biophysica Acta 861, 131–140CrossRefGoogle Scholar
Crowe, J.H., Crowe, L.M, Carpenter, J F and Aurell Wistrom, C. (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochemical Journal 242, 1–10CrossRefGoogle ScholarPubMed
Crowe, J H, Crowe, L.M, Carpenter, J.F., Rudolph, A.S., Aurell Wistrom, C., Spargo, B J and Anchordoguy, T.J. (1988) Interactions of sugars with membranes Biochimica et Biophysica Acta 947, 367–384CrossRefGoogle ScholarPubMed
Crowe, J.H., Crowe, L.M., Hoekstra, F.A and Aurell Wistrom, C. (1989) Effects of water on the stability of phospholipid bilayers the problem of imbibition damage in dry organisms. pp 1–22 in Stanwood, P C and McDonald, M B (Eds) Seed moisture. CSSA Special Publication No 14. Madison, Crop Science Society of America IncGoogle Scholar
Darbyshire, B. (1974) The function of the carbohydrate units of three fungal enzymes in their resistance to dehydration. Plant Physiology 54, 717–721CrossRefGoogle ScholarPubMed
Dasgupta, J., Bewley, J.D and Yeung, E.C (1982) Desiccation-tolerant and desiccation-intolerant stages during the development and germination of Phaseolus vulgaris seeds. Journal of Experimental Botany 33, 1045–1057CrossRefGoogle Scholar
Dure, L. III, Crouch, M L., Harada, J.J., Ho, T.-H.D., Mundy, J., Quatrano, R.S., Thomas, T. and Sung, Z.R. (1989) Common amino sequence domains among the lea proteins of higher plants. Plant Molecular Biology 12, 475–486CrossRefGoogle ScholarPubMed
Ellis, R.H., Hong, T D. and Roberts, E.H (1987) The development of desiccation-tolerance and maximum seed quality during seed maturation in six grain legumes Annals of Botany 59, 23–29CrossRefGoogle Scholar
Farrant, J M, Pammenter, N.W. and Berjak, P. (1986) The increasing desiccation sensitivity of recalcitrant Avicennia marina seeds with storage time. Plant Physiology 67, 291–298CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N W. and Berjak, P. (1992) Development of the recalcitrant (homoiohydrous) seeds of Avicenia marina: anatomical, ultrastructural and biochemical events associated with development from histodifferentiation to maturation. Annals of Botany 70, 75–86CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1993) 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, 1–13CrossRefGoogle Scholar
Finkelstein, R.R. and Crouch, M.L (1986) Rapeseed embryo development in culture on high osmoticum is similar to that in seeds Plant Physiology 81, 907–912CrossRefGoogle ScholarPubMed
Finkelstein, R.R., Tenbarge, K.M., Shumway, J.E. and Crouch, M.L. (1985) Role of ABA in maturation of rapeseed embryos Plant Physiology 78, 630–636CrossRefGoogle ScholarPubMed
Fischer, W., Bergfeld, R., Plachy, C., Schafer, R. and Schopfer, P. (1988) Accumulation of storage materials, precocious germination and development of desiccation tolerance during seed maturation in mustard (Sinapis alba L.) Botanica Acta 101, 344–354Google Scholar
Franzen, J. and Haas, M.M. (1991) Vitamin E content during development of some seedlings Phytochemistry 30, 2911–2913CrossRefGoogle Scholar
Gaber, B.P., Chandrasekhar, I. and Pattabiraman, N. (1986) The interaction of trehalose with the phospholipid bilayer a molecular study pp 231–241 in Leopold, A C (Ed.) Membranes, metabolism and dry organisms Ithaca, Cornell University PressGoogle Scholar
Galau, G.A., Hughes, D.W. and Dure, L. III. (1986) Abscisic acid induction of cloned late embryogenesis-abundant (Lea) mRNAs Plant Molecular Biology 7, 155–170CrossRefGoogle ScholarPubMed
Galau, G.A., Jakobsen, K.S. and Hughes, D W (1991) The controls of late dicot embryogenesis and early germination Physiologia Plantarum 81, 280–288CrossRefGoogle Scholar
Goldberg, R.B., Barker, S.J. and Perez-Grau, L (1989) Regulation of gene expression during plant embryogenesis Cell 56, 149–160CrossRefGoogle ScholarPubMed
Gomez, J., Sanchez-Martinez, D., Stiefel, V, Rigau, J., Puigdomenech, P and Pages, M. (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein Nature 334, 262–264CrossRefGoogle ScholarPubMed
Goodrich, R.P, Crowe, J H., Crowe, L M. and Baldeschwieler, J.D (1991) Alterations in membrane surfaces induced by attachment of carbohydrates Biochemistry 30, 5313–5318CrossRefGoogle ScholarPubMed
Halliwell, B (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts Chemistry and Physics of Lipids 44, 327–340CrossRefGoogle Scholar
Halliwell, B (1991) Oxygen radicals: their formation in plant tissues and their role in herbicide damage in Baker, N R and Percival, M P (Eds) Herbicides. Elsevier Science PublishersGoogle Scholar
Hendry, G.A.F. (1993) Oxygen, free radical processes and seed longevity Seed Science Research 3, 141–153CrossRefGoogle Scholar
Hendry, G.A.F., Finch-Savage, W.E., Thorpe, P C, Atherton, N.M., Buckland, S.H., Nilsson, K.A and Seel, W.E (1992) Free radical processes and loss of seed viability during desiccation in the recalcitrant species Quercus robur L New Phytologist 122, 273–279CrossRefGoogle ScholarPubMed
Hepburn, H.A., Goodman, B.A., McPhail, D.B., Matthews, S and Powell, A.A (1986) An evaluation of EPR measurements of the organic free radical content of individual seeds in the non-destructive testing of seed viability Journal of Experimental Botany 37, 1675–1684CrossRefGoogle Scholar
Hetherington, A.M and Quatrano, R S. (1991) Mechanisms of action of abscisic acid at the cellular level. New Phytologist 119, 9–32CrossRefGoogle ScholarPubMed
Hoekstra, F.A, Crowe, J.H. and Crowe, L.M. (1990) Membrane behavior in drought and its physiological significance. pp 71–126 in Taylorson, R B (Ed.) Recent advances in the development and germination of seeds New York, Plenum PressGoogle Scholar
Hoekstra, F.A., Crowe, J.H. and Crowe, L M. (1991) Effect of sucrose on phase behavior of membranes in intact pollen of Typha latifola L. as measured with Fourier transform infrared spectroscopy Plant Physiology 97, 1073–1079CrossRefGoogle 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, 589–596CrossRefGoogle Scholar
Hong, T.D and Ellis, R.H. (1992) Development of desiccation tolerance in Norway maple (Acer platanoides L.) seeds during maturation drying Seed Science Research 2, 169–172CrossRefGoogle Scholar
Ishida, N., Kano, H., Kobayashi, T. and Yoshida, T. (1988) Analysis of physical states of water in soybean seeds by NMR Agricultural and Biological Chemistry 52, 2777–2781Google Scholar
Kermode, A.R. and Bewley, J.D (1985) The role of maturation drying in the transition from seed development to germination. I. Acquisition of desiccation-tolerance and germinability during development of Ricinus communis L. seeds Journal of Experimental Botany 36, 1906–1915CrossRefGoogle Scholar
Kermode, A R. and Bewley, J.D. (1989) Developing seeds of Ricinus communis L. when detached and maintained in an atmosphere of high relative humidity, switch to a germinative mode without the requirement for complete desiccation Plant Physiology 90, 702–707CrossRefGoogle Scholar
Kermode, A.R., Oishi, M.Y. and Bewley, J.D. (1989) Regulatory roles for desiccation and abscisic acid in seed development a comparison of the evidence from whole seeds and isolated embryos pp 23–50 in Stanwood, P.C. and McDonald, M.B. (Eds) Seed moisture. CSSA Special Publication No 14. Madison, Crop Science of America IncGoogle Scholar
King, R.W. (1976) Abscisic acid in developing wheat grains and its relationship to grain growth and maturation Planta 132, 43–51CrossRefGoogle ScholarPubMed
Klein, S. and Pollock, B.M. (1968) Cell fine structure of developing lima bean seeds related to seed desiccation American Journal of Botany 55, 658–672CrossRefGoogle 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 Arabidopis thaliana Plant Physiology 90, 463–469CrossRefGoogle Scholar
Koster, K.L (1991) Glass formation and desiccation tolerance in seeds Plant Physiology 96, 302–304CrossRefGoogle ScholarPubMed
Koster, K.L. and Leopold, A C (1988) Sugars and desiccation tolerance in seeds Plant Physiology 88, 829–832CrossRefGoogle ScholarPubMed
Kovach, D A. and Bradford, K J (1992) Imbibitional damage and desiccation tolerance of wild rice (Zizania palustris) seeds Journal of Experimental Botany 43, 747–757CrossRefGoogle Scholar
Kuo, T.M., VanMiddlesworth, J.F. and Wolf, W J. (1988) Content of raffinose oligosaccharides and sucrose in various plant seeds Journal of Agricultural and Food Chemistry 36, 32–36CrossRefGoogle Scholar
Lane, B.G. (1991) Cellular desiccation and hydration: developmentally regulated proteins, and the maturation and germination of seed embryos FASEB Journal 5, 2893–2901CrossRefGoogle ScholarPubMed
Leopold, A C (1990) Coping with desiccation pp 57–86 in Alscher, R G and Cumming, J R (Eds) Stress responses in plants: adaptation and acclimation mechanisms. New York, Wiley-Liss, IncGoogle Scholar
Leopold, A.C. and Vertucci, C.W. (1986) Physical attributes of desiccated seeds pp 22–34 in Leopold, A C (Ed.) Membranes, metabolism and dry organisms Ithaca, Cornell University PressGoogle Scholar
Leopold, A.C. and Vertucci, C.W. (1989) Moisture as a regulator of physiological reaction in seeds pp 51–67 in Stanwood, P C and McDonald, M B (Eds) Seed moisture. CSSA Special Publication No 14. Madison, Crop Science Society of America IncGoogle Scholar
Leprince, O. (1992) Etude des mécanismes de la résistance à la déshydratation dans les embryos desplantes supérieures. Ph.D. Thesis. (Liège, University of Liège)Google Scholar
Leprince, O., Bronchart, R and Deltour, R. (1990a) Changes in starch and soluble sugars in relation to the acquisition of desiccation tolerance during maturation of Brassica campestris seed Plant, Cell and Environment 13, 539–546CrossRefGoogle Scholar
Leprince, O., Deltour, R., Thorpe, P.C., Atherton, N.M. and Hendry, G.A.F. (1990b) The role of free radicals and radical processing systems in loss of desiccation tolerance in germinating maize (Zea mays L.) New Phytologist 116, 573–580CrossRefGoogle Scholar
Leprince, O., van der Werf, A., Deltour, R and Lambers, H. (1992) Respiratory pathways in germining maize radicles correlated with desiccation tolerance and soluble sugars Physiologia Plantarum 84, 581–588CrossRefGoogle Scholar
Long, S R, Dale, R.M.K. and Sussex, I.M. (1981) Maturation and germination of Phaseolus vulgaris embryonic axes in culture Planta 153, 405–415CrossRefGoogle ScholarPubMed
Lynch, R.M and Clegg, J.S. (1986) A study of metabolism in dry seeds of Avena fatua L. evaluated by incubation with ethanol–1–14C pp 50–58 in Leopold, A C (Ed) Membranes, metabolism and dry organisms. Ithaca, Cornell University PressGoogle Scholar
Madin, K.A.C and Crowe, J.H. (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration Journal of Experimental Zoology 193, 335–342CrossRefGoogle Scholar
McCubbin, W.D. and Kay, C.M. (1985) Hydrodynamic and optical properties of the wheat Em protein Canadian Journal of Biochemistry 63, 803–810Google Scholar
McKersie, B D and Thompson, J.E (1979) Phase properties of senescing plant membranes Role of the neutral lipids Biochimica et Biophysica Acta 550, 48–58CrossRefGoogle ScholarPubMed
McKersie, B D., Senaratna, T., Walker, M.A., Kendall, E J and Hetherington, P.R. (1988) Deterioration of membranes during aging in plants: evidence for free radical mediation pp 441–464 in Noodén, L D and Leopold, A C (Eds) Senescence and aging in plants. San Diego, Academic PressGoogle Scholar
McKersie, B.D., Senaratna, T., Bowley, S R., Brown, D.C.W., Krochko, J.E. and Bewley, J.D. (1989) Application of artificial seed technology in the production of hydrid alfalfa (Medicago sativa L) In Vitro Cell and Development Biology 25, 1183–1188CrossRefGoogle Scholar
McKersie, B.D., Hoekstra, F.A. and Krieg, L.C. (1990) Differences in the susceptibility of plant membrane lipids to peroxidation Biochimica et Biophysica Acta 1030, 119–126CrossRefGoogle ScholarPubMed
Meurs, C., Basra, A.S., Karssen, C.M. and van Loon, L.C (1992) Role of abscisic acid in the induction of desiccation tolerance in developing seeds of Arabidopis thaliana. Plant Physiology 98, 1484–1493CrossRefGoogle Scholar
Mundy, J and Chua, N.H. (1988) Abscisic acid and waterstress induce a novel rice gene EMBO Journal 7, 2279–2286CrossRefGoogle ScholarPubMed
Oishi, M.Y. and Bewley, J.D. (1990) Distinction between the responses of developing maize kernels to fluridone and desiccation in relation to germinability, α-amylase activity and abscisic acid content Plant Physiology 94, 592–598CrossRefGoogle ScholarPubMed
Pammenter, N.W., Vertucci, CW and Berjak, P.(1991) Homeohydrous (recalcitrant) seeds, dehydration, the state of water and viability characteristics in Landolphia kirku Plant Physiology 96, 1093–1098CrossRefGoogle Scholar
Pauls, K P and Thompson, J.E. (1981) Effects of in vitro treatment with ozone on the physical and chemical properties of membranes Physiologia Plantarum 53, 255–262CrossRefGoogle Scholar
Piatkowski, D., Schneider, K., Salamim, F and Bartels, D. (1990) Characterization of five abscisic acid-responsive cDNA clones isolated from the desiccation-tolerant plant Craterostigma plantagineum and their relationship to other water-stress genes Plant Physiology 94, 1682–1688CrossRefGoogle ScholarPubMed
Prevost, I and Le Page-Degivry, M.T (1985) Inverse correlation between ABA content and germinability throughout the maturation and the in vitro culture of the embryo of Phaseolus vulgaris Journal of Experimental Botany 36, 1457–1464CrossRefGoogle Scholar
Price, A.H and Hendry, G.A F. (1991) Iron-catalyzed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals Plant, Cell and Environment 14 477–484CrossRefGoogle Scholar
Price, A.H., Atherton, N M and Hendry, G.A F (1989) Plants under drought-stress generate activated oxygen Free Radical Research Communications 8, 61–66CrossRefGoogle ScholarPubMed
Priestley, D A., Werner, B.G., Leopold, A.C and McBnde, M.B. (1985) Organic free radical levels in seeds and pollen the effects of hydration and aging Physiologia Plantarum 64, 88–94CrossRefGoogle Scholar
Pntchard, H.W. (1991) Water potential and embryonic, axis viability in recalcitrant seeds of Quercus rubra Annals of Botany 67, 43–49CrossRefGoogle Scholar
Probert, R.J. and Longley, P.L (1989) Recalcitrant seed storage physiology in three aquatic grasses (Zizania palustris, Spartina anglica and Porteresia coarctata) Annals of Botany 63, 53–63CrossRefGoogle Scholar
Puntarulo, S, Galleano, M., Sanchez, R.A and Boveris, A. (1991) Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination Biochimica et Biophysica Acta 1074, 277–283CrossRefGoogle ScholarPubMed
Quatrano, R S (1986) Regulation of gene expression of abscisic acid during angiosperm embryo development Oxford Survey of Plant Molecular and Cell Biology 3, 467–477Google Scholar
Raghavan, V. (1986) Embryogenesis in Angiosperms A developmental and experimental study Cambridge, Cambridge University PressGoogle Scholar
Ramarathnam, N, Osawa, T., Namiki, M. and Tashiro, T (1986) Studies on the relationship between antioxidative activity of rice hull and germination ability of rice seeds Journal of the Science of Food and Agriculture 37, 719–726CrossRefGoogle Scholar
Roberton, M and Chandler, P.M. (1992) Pea dehydrins identification, characterisation and expression Plant Molecular Biology 19 1031–1044CrossRefGoogle ScholarPubMed
Roberts, E.H. and Ellis, R.H. (1989) Water and seed survival Annals of Botany 63, 39–52CrossRefGoogle Scholar
Rogerson, N.E. and Matthews, S (1977) Respiratory and carbohydrate changes in developing pea (Pisum sativum L) seeds in relation to their ability to withstand desiccation Journal of Experimental Botany 28, 304–313CrossRefGoogle Scholar
Sargent, J.A., Mandi, S.S. and Osborne, D (1981) The loss of desiccation tolerance during germination, an ultrastructural and biochemical approach Protoplasma 105, 225–229CrossRefGoogle Scholar
Seel, W., Hendry, G.A.F., Atherton, N.M. and Lee, J. (1991) Radical formation and accumulation in vivo, in desiccation tolerant and intolerant mosses Free Radical Research Communications 15, 133–141CrossRefGoogle ScholarPubMed
Senaratna, T and McKersie, B D. (1983) Characterization of solute efflux from dehydration injured soybean (Glycine max L Merr) seeds Plant Physiology 72, 911–914CrossRefGoogle ScholarPubMed
Senaratna, T. and McKersie, B.D. (1986) Loss of desiccation tolerance during seed germination a free radical mechanism of injury pp 85–101 in Leopold, A C (Ed) Membranes, metabolism and dry organisms Ithaca, Cornell University PressGoogle Scholar
Senaratna, T., McKersie, B.D. and Stinson, R.H (1984) Association between membrane phase properties and dehydration injury in soybean axes Plant Plant Physiology 76, 759–762CrossRefGoogle Scholar
Senaratna, T., McKersie, B.D. and Stinson, R.H. (1985a) Simulation of dehydration injury to membranes from soybean axes by free radicals Plant Physiology 77, 472–474CrossRefGoogle ScholarPubMed
Senaratna, T., McKersie, B D. and Stinson, R.H (1985b) Antioxidant levels in germinating soybean seed axes in relation to free radical and dehydration tolerance Plant Physiology 78, 168–171CrossRefGoogle ScholarPubMed
Senaratna, T., McKersie, B D. and Borochov, A (1987) Desiccation and free radical mediated changes in plant membranes Journal of Experimental Botany 38, 2005–2014CrossRefGoogle Scholar
Senaratna, T., McKersie, B D. and Bowley, S.R. (1989) Desiccation tolerance of alfalfa (Medicago sativa L ) somatic embryos Influence of abscisic acid, stress pretreatments and drying rates Plant Science 65 253–259Google Scholar
Simontacchi, M. and Puntarulo, S. (1992) Oxygen radical generation by isolated microsomes from soybean seedlings Plant Physiology 100, 1263–1268CrossRefGoogle ScholarPubMed
Skriver, K. and Mundy, J (1990) Gene expression in response to abscisic acid and osmotic stress Plant Cell 2, 503–512Google ScholarPubMed
Strauss, G. and Hauser, H. (1986) Stabilization of lipid bilayer vesicles by sucrose during freezing Proceedings of the National Academy of Sciences, USA 83, 2422–2426CrossRefGoogle ScholarPubMed
Symons, S J., Angold, R.E., Black, M. and Chapman, J.M. (1983) Changes in the growth capacity of the developing wheat embryo I The influences of the enveloping tissues and premature drying Journal of Experimental Botany 34, 1541–1550CrossRefGoogle Scholar
Thomann, E.B, Sollinger, J., White, C and Rivin, C.J. (1992) Accumulation of group 3 embryogenesis abundant proteins in Zea mays embryos Roles of abscisic acid and the viviparous-1 gene product Plant Physiology 99, 607–614CrossRefGoogle ScholarPubMed
Van Acker, S.D. and McKersie, B D. (1994) Water binding characteristics of developing seeds, zygotic and somatic embryos of Medicago sativa Seed Science Research (in press)Google Scholar
Vertucci, C.W (1989) The effects of low water contents on physiological activities of seeds Physiologia Plantarum 77, 172–176CrossRefGoogle Scholar
Vertucci, C.W. (1990) Calorimetric studies of the state of water in seed tissues Biophysical Journal 58, 1463–1471CrossRefGoogle ScholarPubMed
Vertucci, C.W. and Leopold, A.C. (1987a) Water binding in legume seeds Plant Physiology 85, 224–231CrossRefGoogle ScholarPubMed
Vertucci, C.W. and Leopold, A.C (1987b) The relationship between water binding and desiccation tolerance in tissues Plant Physiology 85, 232–238CrossRefGoogle ScholarPubMed
Welbaum, G.E. and Bradford, K.J (1989) Water relations of seed development and germination in muskmelon (Cucumis melo L.). II. Development of germinability, vigour, and desiccation tolerance Journal of Experimental Botany 40, 1355–1362CrossRefGoogle Scholar
Williams, R J. and Leopold, A.C. (1989) The glassy state in corn embryos Plant Physiology 89, 977–981CrossRefGoogle Scholar
Williamson, J.D. and Quatrano, R.S. (1988) ABA-regulation of two classes of embryo-specific sequences in mature wheat embryos Plant Physiology 86, 208–215CrossRefGoogle ScholarPubMed
Winston, G.W. (1990) Physiochemical basis for free radical formation in cells: production and defenses pp 57–86 in Alscher, R G and Cumming, J R (Eds) Stress responses in plants: adaptation and acclimation mechanisms New York, Wiley-Liss IncGoogle Scholar
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, 821–826CrossRefGoogle Scholar