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Effects of dehydration conditions on desiccation tolerance of developing pea seeds as related to oligosaccharide content and cell membrane properties

Published online by Cambridge University Press:  22 February 2007

Françoise Corbineau ,
Mari Ange Picard ,
Jean-Albert Fougereux ,
Fabienne Ladonne  and
Daniel Côme
Françoise Corbineau*
Affiliation:
Physiologie Végétale Appliquée, Université Pierre et Marie Curie, Tour 53, 1er étage, 4 place Jussieu, 75252 Paris cédex 05, France
Mari Ange Picard
Affiliation:
Physiologie Végétale Appliquée, Université Pierre et Marie Curie, Tour 53, 1er étage, 4 place Jussieu, 75252 Paris cédex 05, France
Jean-Albert Fougereux
Affiliation:
FNAMS-LABOSEM, Le Verger, 49800 Brain-sur-l’Authion, France
Fabienne Ladonne
Affiliation:
FNAMS-LABOSEM, Le Verger, 49800 Brain-sur-l’Authion, France
Daniel Côme
Affiliation:
Physiologie Végétale Appliquée, Université Pierre et Marie Curie, Tour 53, 1er étage, 4 place Jussieu, 75252 Paris cédex 05, France
*
*Correspondence Fax: +33-1-44275927 Email: corbi@ccr.jussieu.fr
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Abstract

Germination and carbohydrate metabolism were studied in fresh developing pea (Pisum sativum L., cv Baccara) seeds and after artificial drying at 25°C and various relative humidities (20, 75 and 99% RH) to investigate whether the occurrence of desiccation tolerance was related to sucrose, raffinose and stachyose contents. Seeds became completely tolerant to fast drying at 25°C and 20% RH a few days after the end of reserve accumulation, i.e. when their moisture content dropped to approx. 50% (fresh weight basis). This acquisition of desiccation tolerance was associated with an accumulation of raffinose and stachyose, the latter being more abundant in the embryonic axis than in the cotyledons. The (raffinose+stachyose)/sucrose ratio increased during seed development and reached 1.1 in the axis and 0.2 in the cotyledons just before the onset of desiccation tolerance. When the natural acquisition of desiccation tolerance occurred on the mother plant, artificial drying of isolated seeds induced an increase in oligosaccharide content in the cotyledons. Immature seeds, the moisture content of which was higher than about 60% (fresh weight basis), did not tolerate fast drying (25°C and 20 or 75% RH). Such drying did not result in the synthesis of stachyose and induced an increase in electrolyte leakage, a decrease in the ability of seeds to convert 1-aminocyclopropane 1-carboxylic acid (ACC) to ethylene and an increase in ethane synthesis, thus indicating a deterioration of cell membrane properties and lipid peroxidation. In contrast, immature seeds tolerated drying either in the pods or at 25°C and 99% RH, and such drying induced a decrease in sucrose content, an increase in oligosaccharide content and a (raffinose+stachyose)/sucrose ratio higher than around 1. Soluble sugar contents of dried immature seeds depended on the conditions of dehydration. In cotyledons, the (raffinose+stachyose)/sucrose ratio reached 0.61 when seeds were dried at 25°C and 99% RH, whereas it was as low as 0.15 when drying was performed at 25°C and 20% RH. All the results obtained are consistent with the concept that oligosaccharides may well be involved in the protection of membranes during dehydration.

Keywords

Desiccation tolerancemembrane propertiespea seedPisum sativumraffinoseseed dehydrationseed developmentstachyosesucrose
Type
Research Article
Information
Seed Science Research , Volume 10 , Issue 3 , September 2000 , pp. 329 - 339
Copyright
Copyright © Cambridge University Press 2000

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References

Adams, C.A., Fjerstad, M.C. and Rinne, R.W. (1983) Characteristics of soybean seed maturation: necessity for slow dehydration. Crop Science 23, 265–267.CrossRefGoogle Scholar
Bartels, D., Singh, M. and Salamini, F. (1988) Onset of desiccation tolerance during development of the barley embryo. Planta 175, 485–492.Google Scholar
Black, M., Corbineau, F., Gee, H. and Côme, D. (1999) Water content, raffinose, and dehydrins in the induction of desiccation tolerance in immature wheat embryos. Plant Physiology 120, 463–471.CrossRefGoogle ScholarPubMed
Black, M., Corbineau, F., Grzesik, M., Guy, P. and Côme, D. (1996) Carbohydrate metabolism in the developing and maturing wheat embryo in relation to its desiccation tolerance. Journal of Experimental Botany 47, 161–169.CrossRefGoogle Scholar
Blackman, S.A., Obendorf, R.L. and Leopold, A.C. (1992) Maturation proteins and sugars in desiccation tolerance of developing soybean seeds. Plant Physiology 100, 225–230.Google Scholar
Bochicchio, A., Vernieri, P., Puliga, S., Murelli, C. and Vazzana, C. (1997) Desiccation tolerance in immature embryos of maize: sucrose, raffinose and the ABA–sucrose relation. pp. 13–22in Ellis, R.H.; Black, M.; Murdoch, A.J.; Hong, T.D. (Eds) Basic and applied aspects of seed biology. Dordrecht, Kluwer Academic.CrossRefGoogle Scholar
Brenac, P., Horbowicz, M., Downer, S.M., Dickerman, A.M., Smith, M.E. and Obendorf, R.L. (1997) Raffinose accumulation related to desiccation tolerance during maize (Zea mays L.) seed development and maturation. Journal of Plant Physiology 150, 481–488.Google Scholar
Castillo, E.M., de Lumen, B.O., Reyes, P.S. and de Lumen, H.Z. (1990) Raffinose synthase and galactinol synthase in developing seeds and leaves of legumes. Journal of Agricultural and Food Chemistry 38, 351–355.CrossRefGoogle Scholar
Chen, Y. and Burris, J.S. (1990) Role of carbohydrates in desiccation tolerance and membrane behavior in maturing maize seed. Crop Science 30, 971–975.CrossRefGoogle Scholar
Chen, Y.Z. and Patterson, B.D. (1985) Ethylene and 1-aminocyclopropane-1-carboxylic acid as indicators of chilling sensitivity in various plant species. Australian Journal of Plant Physiology 12, 377–385.Google Scholar
Côme, D. and Corbineau, F. (1996) Metabolic damage related to desiccation sensitivity. pp. 107–120in Ouédraogo, A.S.; Poulsen, K.; Stubsgaard, F. (Eds) Intermediate/recalcitrant tropical forest tree seeds. Rome, IPGRI.Google Scholar
Compton, M.E., Benton, C.M., Gray, D.J. and Songstad, D.D. (1992) Plant recovery from maize somatic embryos subjected to controlled relative humidity dehydration. In Vitro Cellular and Developmental Biology 28, 197–201.Google Scholar
Corbineau, F., Bailly, C., Audigier, C., Ladonne, F., Wagner, M.-H. and Côme, D. (1998) Elaboration de la qualité germinative des semences au cours de leur développement sur la plante en relation avec la synthèse d'oligosaccharides: exemple du haricot. pp. 103–109in Lefort, P.-L. (Ed.) Biologie et qualité des semences. Angers, Presses de l'Université d'Angers.Google Scholar
Corbineau, F., Bogatek, R., Picard, M.A. and Côme, D. (1999) Chilling injury in Vigna radiata seedlings and its evaluation by ethylene biosynthesis. pp. 241–248in Sanchez-Diaz, M.; Irigoyen, J.J.; Aguirreolea, J.; Pithan, K. (Eds) Crop development for cool and wet climate of Europe. Luxembourg, Office for Publications of the European Communities.Google Scholar
Crowe, J.H., Hoekstra, F.A. and Crowe, L.M. (1992) Anhydrobiosis. Annual Review of Physiology 54, 579–599.Google Scholar
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, 23–29.CrossRefGoogle Scholar
Golovina, E.A., Hoekstra, F.A. and Hemminga, M.A. (1998) Drying increases intracellular partitioning of amphiphilic substances into the lipid phase. Impact on membrane permeability and significance for desiccation tolerance. Plant Physiology 118, 975–986.CrossRefGoogle ScholarPubMed
Gorecki, R.J., Ashino, H., Satoh, S. and Esashi, Y. (1991) Ethylene production in pea and cocklebur seeds of differing vigor. Journal of Experimental Botany 42, 407–414.Google Scholar
Gorecki, R.J., Piotrowicz-Cieslak, A.I., Lahuta, L.B. and Obendorf, R.L. (1997) Soluble carbohydrates in desiccation tolerance of yellow lupin seeds during maturation and germination. Seed Science Research 7, 107–115.CrossRefGoogle Scholar
Hoekstra, F.A., Haigh, A.M., Tetteroo, F.A.A. and van Roekel, T. (1994) Changes in soluble sugars in relation to desiccation tolerance in cauliflower seeds. Seed Science Research 4, 143–147.CrossRefGoogle Scholar
Horbowicz, M. and Obendorf, R.L. (1994) Seed desiccation tolerance and storability: Dependence on flatulenceproducing oligosaccharides and cyclitols–Review and survey. Seed Science Research 4, 385–405.CrossRefGoogle Scholar
ISTA (International Seed Testing Association) (1993) International rules for seed testing. Rules 1993. Annexe to chapter 5. Seed Science and Technology 21 (Suppl.), 141–186.Google Scholar
Kermode, A.R. (1997) Approaches to elucidate the basis of desiccation-tolerance in seeds. Seed Science Research 7, 75–95.CrossRefGoogle Scholar
Khan, A.A. (1994) ACC-derivated ethylene production, a sensitive test for seed vigor. Journal of the American Society for Horticultural Science 119, 1083–1090.Google Scholar
Kimmerer, T.W. and Kozlowski, T.T. (1982) Ethylene, ethane, acetaldehyde, and ethanol production by plants under stress. Plant Physiology 69, 840–847.CrossRefGoogle ScholarPubMed
Koster, K.L. (1991) Glass formation and desiccation tolerance in seeds. Plant Physiology 96, 302–304.CrossRefGoogle ScholarPubMed
Koster, K.L. and Leopold, A.C. (1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829–832.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, 539–546.CrossRefGoogle 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, 573–580.Google Scholar
Leprince, O., Hendry, G.A.F. and McKersie, B.D. (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Science Research 3, 231–246.Google Scholar
Lin, T.-P, Yen, W.-L. and Chien, C.-T. (1998) Disappearance of desiccation tolerance of imbibed crop seeds is not associated with the decline of oligosaccharides. Journal of Experimental Botany 49, 1203–1212.Google Scholar
Lowell, C.A. and Kuo, T.M. (1989) Oligosaccharide metabolism and accumulation in developing soybean seeds. Crop Science 29, 459–465.CrossRefGoogle Scholar
Matthews, S. (1973) Changes in developing pea (Pisum sativum L.) seeds in relation to their ability to withstand desiccation. Annals of Applied Biology 75, 93–105.CrossRefGoogle Scholar
Obendorf, R.L. (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Science Research 7, 63–74.Google Scholar
Odawara, S., Watanabe, A. and Imaseki, H. (1977) Involvement of cellular membrane in regulation of ethylene production. Plant and Cell Physiology 18, 569–575.Google Scholar
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccationtolerance mechanisms. Seed Science Research 9, 13–37.Google Scholar
Peterbauer, T., Puschenreiter, M. and Richter, A. (1998) Metabolism of galactosylononitol in seeds of Vigna umbellata. Plant and Cell Physiology 39, 334–341.CrossRefGoogle Scholar
Porter, A.J.R., Borlakoglu, J.T. and John, P. (1986) Activity of the ethylene-forming enzyme in relation to plant cell structure and organization. Journal of Plant Physiology 125, 207–216.CrossRefGoogle Scholar
Salmen Espindola, L., Noin, M., Corbineau, F. and Côme, D. (1994) Cellular and metabolic damage induced by desiccation in recalcitrant Araucaria angustifolia embryos. Seed Science Research 4, 193–201.CrossRefGoogle Scholar
Sanhewe, A.J. and Ellis, R.H. (1996) Seed development and maturation in Phaseolus vulgaris. I. Ability to germinate and to tolerate desiccation. Journal of Experimental Botany 47, 949–958.Google Scholar
Saravitz, D.M., Pharr, D.M. and Carter, T.E. (1987) Galactinol synthase activity and soluble sugars in developing seeds of four soybean genotypes. Plant Physiology 83, 185–189.Google 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, 253–259.Google Scholar
Sun, W.Q. and Leopold, A.C. (1993) Acquisition of desiccation tolerance in soybeans. Physiologia Plantarum 87, 403–409.CrossRefGoogle Scholar
Vertucci, C.W. and Farrant, J.M. (1995) Acquisition and loss of desiccation tolerance. pp. 237–271in Kigel, J.ˇ; Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker.Google Scholar