Membrane behavior during dehydration: Implications for desiccation tolerance

Russian Journal of Plant Physiology

Volumn 46, Issue 3, 1999, Pages 295-306

  Hoekstra, F A ^a   Golovina, E A ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b TIMIRYAZEV INSTITUTE OF PLANT PHYSIOLOGY   (Russian Federation)

Author keywords

Desiccation tolerance; Glassy state; Imbibitional injury; Membranes; Partitioning; Phase behavior

Indexed keywords

EID: 0033246811     PISSN: 10214437     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (84)

1. Crowe, J.H., Crowe, L.M., and Chapman, D., Preservation of Membranes in Anhydrobiotic Organisms: The Role of Trehalose, Science, 1984, vol. 223, pp. 701-703.
2. Crowe, J.H., Hoekstra, F.A., and Crowe, L.M., Anhydrobiosis, Annu. Rev. Physiol., 1992, vol. 54, pp. 579-599.
3. Crowe, J.H., Crowe, L.M., Carpenter, J.F., Prestrelski, S.J., Hoekstra, F.A., de Araujo, P.S., and Panek, A.D., Anhydrobiosis: Cellular Adaptations to Extreme Dehydration, Handbook of Physiology, Sec. 13, Comparative Physiology, vol. 2, Dantzler, W.H., Ed., Oxford: Oxford Univ. Press, 1997, pp. 1445-1477.
4. Berjak, P., Vertucci, C.W., and Pammenter, N.W., Effects of Developmental Status and Dehydration Rate on Characteristics of Water and Desiccation-Sensitivity in Recalcitrant Seeds of Camellia sinensis, Seed Sci. Res., 1993, vol. 3, pp. 155-166.
5. Salmen-Espindola, L., Noin, M., Corbineau, F., and Côme, D., Cellular and Metabolic Damage Induced by Desiccation in Recalcitrant Araucaria angustifolia Embryos, Seed Sci. Res., 1994, vol. 4, pp. 193-201.
6. Senaratna, T. and McKersie, B.D., Characterization of Solute Efflux from Dehydration-injured Soybean (Glycine max L. Merr) Seeds, Plant Physiol., 1983, vol. 72, pp. 911-914.
7. Hoekstra, F.A. and van Roekel, T., Desiccation Tolerance of Papaver dubium L. Pollen during Its Development in the Anther: Possible Role of Phospholipid Composition and Sucrose Content, Plant Physiol., 1988, vol. 88, pp. 626-632.
8. Hoekstra, F.A., Crowe, J.H., and Crowe, L.M., Membrane Behavior in Drought and Its Physiological Significance, Recent Advances in the Development and Germination of Seeds, Taylorson, R.B., Ed., New York: Plenum, 1989, pp. 77-88.
9. Webster, B.D. and Leopold, A.C., The Ultrastructure of Dry and Imbibed Cotyledons of Soybean, Am. J. Bot., 1977, vol. 6, pp. 1286-1293.
10. Morrison-Baird, L.A., Leopold, A.C., Bramlage, W.J., and Webster, B.D., Ultrastructural Modifications Associated with Imbibition of the Soybean Radicle, Bot. Gaz., 1979, vol. 140, pp. 371-377.
11. Buttrose, M.S., Rapid Water Uptake and Structural Changes in Imbibing Seed Tissues, Protoplasma, 1973, vol. 77, pp. 111-122.
12. Thomson, W.W., Ultrastructure of Dry Seed Tissue after a Non Aqueous Primary Fixation, New Phytol., 1979, vol. 82, pp. 207-212.
13. Öpik, H., The Ultrastructure of Coleoptile Cells in Dry Rice (Oryza sativa L.) Grains after Anhydrous Fixation with Osmium Tetroxide Vapour, New Phytol., 1980, vol. 85, pp. 521-529.
14. Öpik, H., The Fine Structure of Some Dry Seed Tissues Observed after Completely Anhydrous Chemical Fixation, Ann. Bot., 1985, vol. 56, pp. 453-466.
15. Chapman, D., Williams, R.M., and Ladbrooke, B.D., Physical Studies of Phospholipids: 6. Thermotropic and Lyotropic Mesomorphism of Some 1,2-Diacyl-Phosphatidylcholines (Lecithins), Chem. Phys. Lipids, 1967, vol. 1, pp. 445-475.
16. Crowe, L.M. and Crowe, J.H., Effects of Water and Carbohydrates on Membrane Fluidity, Physiological Regulation of Membrane Fluidity, Aloia, R.C. et al., Eds., New York: Alan R. Liss, 1988, pp. 75-99.
17. Lynch, D.V. and Steponkus, P.L., Lyotropic Phase Behavior of Unsaturated Phosphatidylcholine Species: Relevance to the Mechanism of Plasma Membrane Destabilization and Freezing Injury, Biochim. Biophys. Acta, 1989, vol. 984, pp. 267-272.
18. II) Phase Transitions in Dialkyl-and Diacylphosphatidylethanolamines, Biochemistry, 1983, vol. 22, pp. 1280-1289.
19. Priestley, D.A. and Leopold, A.C., The Relevance of Seed Membrane Lipids to Imbibitional Chilling Effects, Physiol. Plant., 1980, vol. 49, pp. 198-204.
20. Cullis, P.R. and De Kruijff, B., Lipid Polymorphism and the Functional Roles of Lipids in Biological Membranes, Biochim. Biophys. Acta, 1979, vol. 559, pp. 399-420.
21. Aurell Wistrom, C., Rand, R.P., Crowe, L.M., Spargo, B.J., and Crowe, J.H., Direct Transition of Dioleoylphosphatidylethanolamine from Lamellar Gel to Inverted Hexagonal Phase Caused by Trehalose, Biochim. Biophys. Acta, 1989, vol. 984, pp. 238-242.
22. Crowe, J.H., Crowe, L.M., and Hoekstra, F.A., Phase Transitions and Permeability Changes in Dry Membranes during Rehydration, J. Bioenerg. Biomembr., 1989, vol. 21, pp. 77-91.
23. 31P-NMR and Fusion, Biochim. Biophys. Acta, 1981, vol. 645, pp. 102-114.
24. Luzzati, V. and Husson, F., The Structure of the Liquid-Crystalline Phases of Lipid-Water Systems, J. Cell Biol., 1962, vol. 12, pp. 207-219.
25. Simon, E.W., Phospholipids and Plant Membrane Permeability, New Phytol., 1974, vol. 73, pp. 377-420.
26. Hoekstra, F.A., Crowe, J.H., Crowe, L.M., and van Bilsen, D.G.J.L., Membrane Behaviour and Stress Tolerance in Pollen, Angiosperm Pollen and Ovules, Ottaviano, E. et al., Eds., New York: Springer-Verlag, 1992, pp. 177-186.
27. McKersie, B.D. and Stinson, R.H., Effect of Dehydration on Leakage and Membrane Structure in Lotus corniculatus L. Seeds, Plant Physiol., 1980, vol. 66, pp. 316-320.
28. 31P Nuclear Magnetic Resonance Study of Hydrating Typha latifolia Pollen, Plant Physiol., 1982, vol. 70, pp. 1075-1078.
29. Seewaldt, V., Priestley, D.A., Leopold, A.C., Feigenson, G.W., and Goodsaid-Zalduondo, F., Membrane Organization in Soybean Seeds during Hydration, Planta, 1981, vol. 152, pp. 19-23.
30. Singh, J., Blackwell, B.A., Miller, R.W., and Bewley, J.D., Membrane Organization of the Desiccation-Tolerant Moss Tortula ruralis in Dehydrated States, Plant Physiol., 1984, vol. 75, pp. 1075-1079.
31. Crowe, J.H., Crowe, L.M., Hoekstra, F.A., and Aurell Wistrom, C., Effects of Water on the Stability of Phospholipid Bilayers: The Problem of Imbibition Damage in Dry Organisms, Seed Moisture, CSSA Special Publication no. 14, Stanwood, P.C. and McDonald, M.B., Eds., Madison: Crop Science Society of America, 1989, pp. 1-14.
32. Hoekstra, F.A., Imbibitional Chilling Injury in Pollen. Involvement of the Respiratory Chain, Plant Physiol., 1984, vol. 74, pp. 815-821.
33. Hoekstra, F.A. and van der Wal, E.W., Initial Moisture Content and Temperature of Imbibition Determine Extent of Imbibitional Injury in Pollen, J. Plant Physiol., 1988, vol. 133, pp. 257-262.
34. Hoekstra, F.A., Crowe, J.H., and Crowe, L.M., Germination and Ion Leakage Are Linked with Phase Transitions of Membrane Lipids during Imbibition of Typha latifolia Pollen, Physiol. Plant., 1992, vol. 84, pp. 29-34.
35. Platt-Aloia, K.A., Lord, E.M., DeMason, D.A., and Thomson, W.W., Freeze-Fracture Observations on Membranes of Dry and Hydrated Pollen from Collomia, Phoenix, and Zea, Planta, 1986, vol. 168, pp. 291-298.
36. McKersie, B.D. and Thompson, J.E., Phase Properties of Senescing Plant Membranes: Role of the Neutral Lipids, Biochim. Biophys. Acta, 1979, vol. 550, pp. 48-58.
37. Crowe, J.H., Hoekstra, F.A., and Crowe, L.M., Membrane Phase Transitions Are Responsible for Imbibitional Damage in Dry Pollen, Proc. Natl. Acad. Sci. USA, 1989, vol. 86, pp. 520-523.
38. Hoekstra, F.A., Crowe, J.H., and Crowe, L.M., Effect of Sucrose on Phase Behavior of Membranes in Intact Pollen of Typha latifolia L. as Measured with Fourier Transform Infrared Spectroscopy, Plant Physiol., 1991, vol. 97, pp. 1073-1079.
39. Hoekstra, F.A., Bomal, C., and Tetteroo, F.A.A., Membrane Phase Transitions in Dry Seeds as Measured by FT-IR Spectroscopy, Proc. Fourth Int. Workshop on Seeds: Basic and Applied Aspects of Seed Biology, Come D. and Corbineau F., Eds., Paris: ASFIS, 1993, pp. 755-762.
40. Horbowicz, M. and Obendorf, R.L., Seed Desiccation Tolerance and Storability: Dependence on Flatulence-producing Oligosaccharides and Cyclitols, Review and Survey, Seed Sci. Res., 1994, vol. 4, pp. 385-405.
41. Fischer, W., Bergfeld, R., Plachy, C., Schafer, R., and Schopfer, P., Accumulation of Storage Materials, Precocious Germination and Development of Desiccation Tolerance during Seed Maturation in Mustard (Sinapis alba L.), Bot. Acta, 1988, vol. 101, pp. 344-354.
42. Leprince, O., Bronchart, R., and Deltour, R., Changes in Starch and Soluble Sugars in Relation to the Acquisition of Desiccation Tolerance during Maturation of Brassica campestris Seed, Plant, Cell, Environ., 1990, vol. 13, pp. 539-546.
43. Crowe, L.M., Womersley, C., Crowe, J.H., Reid, D., Appel, L., and Rudolph, A., Prevention of Fusion and Leakage in Freeze-Dried Liposomes by Carbohydrates, Biochim. Biophys. Acta, 1986, vol. 861, pp. 131-140.
44. Crowe, J.H., Hoekstra, F.A., Nguyen, K.H.N., and Crowe, L.M., Is Vitrification Involved in Depression of the Phase Transition Temperature in Dry Phospholipids? Biochim. Biophys. Acta, 1996, vol. 1280, pp. 187-196.
45. Franks, F., Long-Term Stabilization of Biologicals, Biotechnol., 1994, vol. 12, pp. 253-256.
46. Slade, L. and Levine, H., Water and the Glass Transition: Dependence of the Glass Transition on Composition and Chemical Structure: Special Implications for Flour Functionality in Cookie Baking, J. Food Eng., 1994, vol. 22, pp. 143-188.
47. Burke, M.J., The Glassy State and Survival of Anhydrous Biological Systems, Membranes, Metabolism and Dry Organisms, Leopold A.C., Ed., Ithaca: Cornell Univ. Press, 1986, pp. 358-363.
48. Green, J.L. and Angell, C.A., Phase Relations and Vitrification in Saccharide-Water Solutions and the Trehalose Anomaly, J. Phys. Chem., 1989, vol. 93, pp. 2880-2882.
49. Crowe, J.H., Oliver, A.E., Hoekstra, F.A., and Crowe, L.M., Stabilization of Dry Membranes by Mixtures of Hydroxyethyl Starch and Glucose: The Role of Vitrification, Cryobiology, 1997, vol. 35, pp. 20-30.
50. Hoekstra, F.A., Wolkers, W.F., Buitink, J., Golovina, E.A., Crowe, J.H., and Crowe, L.M., Membrane Stabilization in the Dry State, Comp. Biochem. Physiol., A Comp. Physiol., 1997, vol. 117, pp. 335-341.
51. Hoekstra, F.A., Crowe, J.H., Crowe, L.M., van Roekel, T., and Vermeer, E., Do Phospholipids and Sucrose Determine Membrane Phase Transitions in Dehydrating Pollen Species? Plant, Cell Environ., 1992, vol. 15, pp. 601-606.
52. Leslie, S.B., Israeli, E., Lighthart, B., Crowe, J.H., and Crowe, L.M., Trehalose and Sucrose Protect both Membranes and Proteins in Intact Bacteria during Drying, Appl. Environ. Microbiol., 1995, vol. 61, pp. 3592-3597.
53. Golovina, E.A., Hoekstra, F.A., and Hemminga, M.A., Drying Increases Intracellular Partitioning of Amphipathic Substances into the Lipid Phase: Impact on Membrane Permeability and Significance for Desiccation Tolerance, Plant Physiol., 1998, vol. 118, pp. 975-986.
54. Ceska, O. and Styles, E.D., Flavonoids from Zea mays Pollen, Phytochemistry, 1984, vol. 23, pp. 1822-1823.
55. Liao, M.C., Liu, Y.L., and Xiao, P.G., Studies on the Flavonoids from the Pollens of Typha davidiana, T. latifolia, and T. angustata, Acta Bot. Sinica, 1989, vol. 31, pp. 939-947.
56. Rizk, A.M., Ismail, S.I., Azzam, S.A., and Wood, G., Constituents of Green Beans Phaseolus vulgaris, Qatar Univ. Sci. J., 1992, vol. 12, pp. 69-72.
57. Ylstra, B., Touraev, A., Benito Moreno, R.M., Stoger, E., van Tunen, A.J., Vicente, O., Mol, J.N.M., and Heberle-Bors, E., Flavonols Stimulate Development, Germination and Tube Growth of Tobacco Pollen, Plant Physiol., 1992, vol. 100, pp. 902-907.
58. Hoekstra, F.A., Water Content in Relation to Stress in Pollen, Membranes, Metabolism and Dry Organisms, Leopold A.C., Ed., Ithaca: Cornell Univ. Press, 1986, pp. 102-122.
59. Leprince, O. and Hoekstra, F.A., The Responses of Cytochrome Redox State and Energy Metabolism to Desiccation Support a Role for Cytoplasmic Viscosity in Desiccation Tolerance, Plant Physiol., 1998, vol. 118, pp. 1253-1264.
60. Williams, R.J. and Leopold, A.C., The Glassy State in Corn Embryos, Plant Physiol., 1989, vol. 89, pp. 977-981.
61. Dzuba, S.A., Golovina, E.A., and Tsvetkov, Yu.D., Echo-induced EPR Spectra of Spin Probes as a Method for Identification of Glassy State in Biological Objects, J. Magn. Reson., 1993, vol. 101, pp. 134-138.
62. Buitink, J., Walters-Vertucci, C., Hoekstra, F.A., and Leprince, O., Calorimetric Properties of Dehydrating Pollen, Analysis of a Desiccation-Tolerant and an Intolerant Species, Plant Physiol., 1996, vol. 111, pp. 235-242.
63. Lee, C.W.B., Das Gupta, S.K., Mattai, J., Shipley, G.G., Abdel-Mageed, O.H., Makriyannis, A., and Griffin, R.G., Characterization of the Lambda Phase in Trehalose-stabilized Dry Membranes by Solid-State NMR and X-Ray Diffraction, Biochemistry, 1989, vol. 28, pp. 5000-5009.
64. Lee, C.W.B., Waugh, J.S., and Griffin, R.G., Solid-State NMR Study of Trehalose/1,2-Dipalmitoyl-sn-Phosphatidylcholine Interactions, Biochemistry, 1986, vol. 25, pp. 3737-3742.
65. Sack, F.D., Leopold, A.C., and Hoekstra, F.A., Structural Correlates of Imbibitional Injury in Typha Pollen, Am. J. Bot., 1988, vol. 75, pp. 570-578.
66. Hobbs, P.R. and Obendorf, R.L., Interaction of Initial Seed Moisture and Imbibitional Temperature on Germination and Productivity of Soybean, Crop Sci., 1972, vol. 12, pp. 664-667.
67. Bramlage, W.J., Leopold, A.C., and Parrish, D.J., Chilling Stress to Soybeans during Imbibition, Plant Physiol., 1978, vol. 61, pp. 525-529.
68. Priestley, D.A., Seed Aging: Implications for Seed Storage and Persistence in Soil, Ithaca: Comstock, 1986.
69. Crowe, J.H., O'Dell, S.J., and Armstrong, D.A., Anhydrobiosis in Nematodes: Permeability during Rehydration, J. Exp. Zool., 1979, vol. 207, pp. 431-438.
70. Crowe, J.H., Crowe, L.M., and O'Dell, S.J., Ice Formation during Freezing of Artemia Cysts of Variable Water Contents, Mol. Physiol., 1981, vol. 1, pp. 145-152.
71. Moore, D., Langewald, J., and Obognon, F., Effects of Rehydration on the Conidial Viability of Metarhizium flavoviride Mycopesticide Formulations, Biocontrol Sci. Technol., 1997, vol. 7, pp. 87-94.
72. Van Steveninck, J. and Ledeboer, A.M., Phase Transitions in the Yeast Cell Membrane: The Influence of Temperature on the Reconstitution of Active Dry Yeast, Biochim. Biophys. Acta, 1974, vol. 352, pp. 64-70.
73. Duke, S.H. and Kakefuda, G., Role of the Testa in Preventing Cellular Rupture during Imbibition of Legume Seeds, Plant Physiol., 1981, vol. 67, pp. 449-456.
74. Powell, A.A. and Matthews, S., The Influence of Testa Condition on the Imbibition and Vigour of Pea Seeds, J. Exp. Bot., 1979, vol. 30, pp. 193-197.
75. Herner, R.C., Germination under Cold Soil Conditions, HortScience, 1986, vol. 21, pp. 1118-1122.
76. Tully, R.E., Musgrave, M.E., and Leopold, A.C., The Seed Coat as a Control of Imbibitional Chilling Injury, Crop Sci., 1981, vol. 21, pp. 312-317.
77. Prusinski, J. and Borowska, M., Imbibitional Injury during Seed Germination of Pea (Pisum sativum L.) Cultivars, Plant Breed. Seed Sci., 1996, vol. 40, pp. 149-157.
78. Taylor, A.J. and Dickson, M.N., Seed Coat Permeability in Semi-Hard Snap Bean Seeds: Its Influence on Imbibitional Chilling Injury, J. Hort. Sci., 1987, vol. 62, pp. 183-189.
79. Bedi, S. and Basra, A.S., Chilling Injury in Germinating Seeds: Basic Mechanisms and Agricultural Implications, Seed Sci. Res., 1993, vol. 3, pp. 219-229.
80. Crowe, J.H., Hoekstra, F.A., Crowe, L.M., Anchordoguy, T.J., and Drobnis, E., Lipids Phase Transitions Measured in Intact Cells with Fourier Transform Infrared Spectroscopy, Cryobiology, 1989, vol. 26, pp. 76-84.
81. Leprince, O., Hendry, G.A.F., and McKersie, B.D., The Mechanisms of Desiccation Tolerance in Developing Seeds, Seed Sci. Res., 1993, vol. 3, pp. 231-246.
82. Tetteroo, F.A.A., de Bruijn, A.Y., Henselmans, R.N.M., Wolkers, W.F., van Aelst, A.C., and Hoekstra, F.A., Characterization of Membrane Properties in Desiccation-Tolerant and -Intolerant Carrot Somatic Embryos, Plant Physiol., 1996, vol. 111, pp. 403-412.
83. Timasheff, S.N., Preferential Interactions in Protein-Water-Cosolvent Systems, Biophysics of Water, Franks, F. and Mathias, S.F., Eds., New York: Wiley and Sons, 1982, pp. 70-72.
84. Anchordoguy, T.J., Rudolph, A.S., Carpenter, J.F., and Crowe, J.H., Modes of Interaction of Cryoprotectants with Membrane Phospholipids during Freezing, Cryobiology, 1987, vol. 24, pp. 324-331.