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Membrane behaviour in seeds and other systems at low water content: the various effects of solutes

Published online by Cambridge University Press:  22 February 2007

Gary Bryant ,
Karen L. Koster  and
Joe Wolfe
Gary Bryant
Affiliation:
Department of Applied Physics, RMIT University, Melbourne 3001, Australia
Karen L. Koster*
Affiliation:
Department of Biology, The University of South Dakota, Vermillion, SD 57069, USA
Joe Wolfe
Affiliation:
School of Physics, The University of New South Wales, Sydney 2052, Australia
*
*Correspondence Fax: 1-605-677-6557 Email: kkoster@usd.edu
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Abstract

A common feature of desiccation-tolerant organisms, such as orthodox seeds, is the presence of large quantities of sugars, especially di- and oligosaccharides. These sugars may be one component of the suite of adaptations that allow anhydrobiotes to survive the loss of most of their cellular water. This paper describes the physical effects of dehydration on cellular ultrastructure, with particular emphasis on membranes, and explains quantitatively how sugars and other solutes can influence these physical effects. As a result of dehydration, the surfaces of membranes are brought into close approach, which causes physical stresses that can lead to a variety of effects, including demixing of membrane components and fluid-to-gel phase transitions of membrane lipids. The presence of small solutes, such as sugars, between membranes can limit their close approach and, thereby, diminish the physical stresses that cause lipid fluid-to-gel phase transitions to occur during dehydration. Thus, in the presence of intermembrane sugars, the lipid fluid-to-gel phase transition temperature (Tm) does not increase as much as it does in the absence of sugars. Vitrification of the intermembrane sugar solution has the additional effect of adding a mechanical resistance to the lipid phase transition; therefore, when sugars vitrify between fluid phase bilayers, Tm is depressed below its fully hydrated value (To). These effects occur only for solutes small enough to remain in very narrow spaces between membranes at low hydration. Large solutes, such as polymers, may be excluded from such regions and, therefore, do not diminish the physical forces that lead to membrane changes at low hydration.

Keywords

dehydrationdesiccationmembranesphasetransitionsolutessugarsvitrification
Type
Research Perspective
Information
Seed Science Research , Volume 11 , Issue 1 , March 2001 , pp. 17 - 25
Copyright
Copyright © Cambridge University Press 2001

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References

Bryant, G. and Wolfe, J. (1992) Interfacial forces in cryobiology and anhydrobiology. Cryo-Letters 13, 23–36.Google Scholar
Caffrey, M., Fonseca, V. and Leopold, A.C. (1988) Lipid-sugar interactions: relevance to anhydrous biology. Plant Physiology 86, 754–758.CrossRefGoogle ScholarPubMed
Chapman, D., Williams, R.M. and Ladbrooke, B.D. (1967) Physical studies of phospholipids. VI. Thermotropic and lyotropic mesomorphism of some 1,2-diacylphosphatidylcholines (lecithins). Chemistry and Physics of Lipids 1, 445–475.CrossRefGoogle Scholar
Crowe, J.H. and Clegg, J.S. (1978) Dry biological systems. New York, Academic Press.Google Scholar
Crowe, J.H., Crowe, L.M. and Chapman, D. (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223, 701–703.CrossRefGoogle ScholarPubMed
Crowe, J.H., Hoekstra, F.A., Nguyen, K.H.N. and Crowe, L.M. (1996) Is vitrification involved in depression of the phase transition temperature in dry phospholipids? Biochimica et Biophysica Acta 1280, 187–196.CrossRefGoogle ScholarPubMed
Crowe, J.H., Carpenter, J.F. and Crowe, L.M. (1998) The role of vitrification in anhydrobiosis. Annual Review of Physiology 60, 73–103.CrossRefGoogle ScholarPubMed
Crowe, L.M. and Crowe, J.H. (1982) Hydration-dependent hexagonal phase lipid in a biological membrane. Archives of Biochemistry and Biophysics 217, 582–587.CrossRefGoogle Scholar
Crowe, L.M. and Crowe, J.H. (1988) Trehalose and dry dipalmitoylphosphatidylcholine revisited. Biochimica et Biophysica Acta 946, 193–201.CrossRefGoogle ScholarPubMed
Evans, E. and Needham, D. (1987) Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion and colloidal interactions. Journal of Physical Chemistry 91, 4219–4228.Google Scholar
Gordon-Kamm, W.J. and Steponkus, P.L. (1984) Lamellarto- hexagonal II phase transitions in the plasma membrane of isolated protoplasts after freeze-induced dehydration. Proceedings of the National Academy Sciences, USA 81, 6373–6377.Google Scholar
Hoekstra, F.A., Crowe, J.H. and Crowe, L.M. (1992) Germination and ion leakage are linked with phase transitions of membrane lipids during imbibition of Typha latifolia pollen. Physiologia Plantarum 84, 29–34.CrossRefGoogle Scholar
Hoekstra, F.A., Golovina, E.A., Van Aelst, A.C. and Hemminga, M.A. (1999) Imbibitional leakage from anhydrobiotes revisited. Plant, Cell and Environment 22, 1121–1131.CrossRefGoogle Scholar
Karmas, R., Buera, M.P. and Karel, M. (1992) Effect of glass transition on rates of nonenzymatic browning in food systems. Journal of Agriculture and Food Chemistry 40, 873–879.Google Scholar
Kjellander, R. and Marèelja, S. (1985 a) Perturbation of hydrogen bonding in water near polar surfaces. Chemical Physics Letters 120, 393–396.CrossRefGoogle Scholar
Kjellander, R. and Marèelja, S. (1985b) Polarization of water between molecular surfaces: a molecular dynamics study. Chemica Scripta 25, 73–80.Google Scholar
Koster, K.L., Webb, M.S., Bryant, G. and Lynch, D.V. (1994) Interactions between soluble sugars and POPC (1-palmitoyl-2-oleoylphosphatidylcholine) during dehydration: vitrification of sugars alters the phase behaviour of the phospholipid. Biochimica et Biophysica Acta 1193, 143–150.CrossRefGoogle ScholarPubMed
Koster, K.L., Sommervold, C.L. and Lei, Y.P. (1996) The effect of storage temperature on the interactions between dehydrated sugars and phosphatidylcholine. Journal of Thermal Analysis 47, 1581–1596.CrossRefGoogle Scholar
Koster, K.L., Lei, Y.P., Anderson, M., Martin, S. and Bryant, G. (2000) Effects of vitrified and non-vitrified sugars on phosphatidylcholine fluid-to-gel phase transitions. Biophysical Journal 78, 1932–1946.CrossRefGoogle Scholar
Leopold, A.C. (1986) Membranes, metabolism and dry organisms. Ithaca, NY, Comstock Publishing Associates.Google Scholar
Lis, L.J., McAlister, M., Fuller, N., Rand, R.P. and Parsegian, V.A. (1982) Measurement of the lateral compressibility of several phospholipid bilayers. Biophysical Journal 37, 667–672.Google Scholar
Lynch, D.V. and Steponkus, P.L. (1989) Lyotropic phase behavior of unsaturated phosphatidylcholine species: relevance to the mechanism of plasma membrane destabilization and freezing injury. Biochimica et Biophysica Acta 984, 267–272.Google Scholar
Marra, J. and Israelachvili, J. (1985) Direct measurements of forces between phosphatidylcholine and phosphatidylethanolamine bilayers in aqueous electrolyte solutions. Biochemistry 24, 4608–4618.Google Scholar
McMullen, T.P., Lewis, R.N. and McElhaney, R.N. (1994)Comparative differential scanning calorimetric and FTIR and 31P-NMR spectroscopic studies of the effects of cholesterol and androstenol on the thermotropic phase behavior and organization of phosphatidylcholine bilayers. Biophysical Journal 66, 741–752.Google Scholar
Oliver, A.E., Crowe, L.M. and Crowe, J.H. (1998) Methods for dehydration-tolerance: depression of the phase transition temperature in dry membranes and carbohydrate vitrification. Seed Science Research 8, 211–221.Google Scholar
Parsegian, A., Rau, D. and Zimmerberg, J. (1986) Structural transitions induced by osmotic stress. pp. 306–317 in Leopold, A.C. (Ed.) Membranes, metabolism and dry organisms. Ithaca, NY, Comstock Publishing Associates.Google Scholar
Platt-Aloia, K.A. (1988) Freeze fracture evidence of stressinduced phase separations in plant cell membranes. pp. 259–2921in Aloia, R.C.Curtain, C.C.Gordon, L.C. (Eds) Physiological regulation of membrane fluidity. New York, Alan R. Liss, Inc.Google Scholar
Rand, R.P. and Parsegian, V.A. (1989) Hydration forces between phospholipid bilayers. Biochimica et Biophysica Acta 988, 351–376.CrossRefGoogle Scholar
Slade, L. and Levine, H. (1995) Glass transitions and water-food structure interactions. Advances in Food and Nutrition Research 38, 103–269.Google Scholar
Sun, W.Q., Irving, T.C. and Leopold, A.C. (1994) The role of sugar, vitrification and membrane phase transition in seed desiccation tolerance. Physiologia Plantarum 90, 621–628.Google Scholar
Sun, W.Q., Davidson, P. and Chan, H.S.O. (1998) Protein stability in the amorphous carbohydrate matrix: relevance to anhydrobiosis. Biochimica et Biophysica Acta 1425, 245–254.CrossRefGoogle ScholarPubMed
Webb, M.S., Hui, S.W. and Steponkus, P.L. (1993) Dehydration-induced lamellar-to-hexagonal-II phase transitions in DOPE/DOPC mixtures. Biochimica et Biophysica Acta 1145, 93–104.CrossRefGoogle ScholarPubMed
Wolfe, J. (1987) Lateral stresses in membranes at low water potential. Australian Journal of Plant Physiology 14, 311–318.Google Scholar
Wolfe, J. and Bryant, G. (1999) Freezing, drying, and/or vitrification of membrane-solute-water systems. Cryobiology 39, 103–129.CrossRefGoogle ScholarPubMed
Zhang, J. and Steponkus, P.L. (1995) Effects of sugars on the dehydration-induced increase in the T m of DPPC dehydrated over a continuum of osmotic pressures. Cryobiology 32, 60A.Google Scholar
Zhang, J. and Steponkus, P.L. (1996) Proposed mechanism for depression of the liquid-crystalline-to-gel phase transition temperature of phospholipids in dehydrated sugar-phospholipid mixtures. Cryobiology 33, 21A.Google Scholar