Skip to main content Accessibility help
×
Home

Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms

  • Patricia Berjak (a1)

Abstract

Desiccation-tolerant organisms, or life-cycle stages of particular taxa, occur among animals, higher and lower plants, terrestrial micro-algae, lichens and bacteria. Recent investigations have revealed that a number of mechanisms conferring desiccation tolerance appear to be common to the diversity of life forms able to survive extreme dehydration. In particular, parallel processes involving late embryogenic abundant (LEA) or LEA-like proteins, accumulation of sugars, aspects of active oxygen species (AOS) and non-enzymic and enzymic antioxidants have been the recent focus of attention, some across a diversity of organisms. The present contribution considers advances made from the study of these processes, particularly in enhancing current understanding of the composition of, and protection afforded by, the glassy state in desiccated organisms. Strong evidence that proteins, particularly LEAs, are implicated in glass formation is reviewed, and behaviour of such proteins upon dehydration is discussed in this context. The question of the ability of cells to survive complete water removal is considered in the context that it is unlikely, and that the basis of the deterioration of very dry seeds results from abstraction of water necessary to maintain the integrity of the intracellular glassy state. Finally, the revelation that desiccated seeds deteriorate with time, even under extremely good genebanking conditions, is discussed.

Copyright

Corresponding author

*Corresponding author:Email: berjak@ukzn.ac.za

References

Hide All
Aalen, R.B. (1999) Peroxiredoxin antioxidants in seed physiology. Seed Science Research 9, 285295.
Alpert, P. (2005) The limits and frontiers of desiccation-tolerant life. Integrative and Comparative Biology 45, 685695.
Angell, C.A. (1995) The old problems of glass and glass transition, and the many new twists. Proceedings of the National Academy of Sciences, USA 92, 66756682.
Bailly, C. (2004) Active oxygen species and antioxidants in seed biology. Seed Science Research 14, 93107.
Bailly, C., Bogatek-Leszczynska, R., Côme, D. and Corbineau, F. (2002) Changes in activities of antioxidant enzymes and lipoxygenase during growth of sunflower seedlings and seeds of different vigour. Seed Science Research 12, 4755.
Battista, J.R., Park, M.-J. and McLemore, A.E. (2001) Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology 43, 133139.
Benson, E.E. and Bremner, D. (2004) Oxidative stress in the frozen plant: A free radical point of view. 205241. in Fuller, B.J.;, Lane, N.;, Benson, E.E. (Eds.) Life in the frozen state. Boca Raton, CRC Press.
Berjak, P., Dini, M. and Gevers, H.O. (1986) Deteriorative changes in embryos of long-stored, uninfected maize caryopses. South African Journal of Botany 52, 109116.
Billi, D. and Potts, M. (2002) Life and death of dried prokaryotes. Research in Microbiology 153, 712.
Black, M. and Pritchard, H.W. (2002) Desiccation and survival in plants. Drying without dying. Wallingford, CABI Publishing.
Browne, J., Tunnacliffe, A. and Burnell, A. (2002) Anhydrobiosis: plant desiccation gene found in a nematode. Nature 416, 38
Bruni, F. and Leopold, A.C. (1992) Pools of water in anhydrobiotic organisms. A thermally stimulated depolarization current study. Biophysical Journal 63, 663672.
Bryant, G., Koster, K.L. and Wolfe, J. (2001) Membrane behaviour in seeds and other systems at low water content: the various effects of solutes. Seed Science Research 11, 1725.
Buitink, J. and Leprince, O. (2004) Glass formation in plant anyhdrobiotes: survival in the dry state. Cryobiology 48, 215228.
Buitink, J., Hemminga, M.A. and Hoekstra, F.A. (2000) Is there a role for oligosaccharides in seed longevity? An assessment of intracellular glass stability. Plant Physiology 122, 12171224.
Buitink, J., Hoekstra, F.A. and Leprince, O. (2002) Biochemistry and biophysics of tolerance systems. pp 293318. in Black, M.;, Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, CABI Publishing.
Burke, M.J. (1986) The glassy state and survival of anhydrous biological systems Membranes, metabolism and dry organisms 358363. Leopold A.C. Ithaca, New York Comstock Publishing Associates
Caprioli, M., Katholm, A.K., Melone, G., Ramløv, H., Ricci, C. and Santo, N. (2004) Trehalose in desiccated rotifers: a comparison between a bdelloid and a monogonont species. Comparative Biochemistry and Physiology A – Molecular and Integrative Physiology 139, 527532.
Clegg, J.S. (1986) The physical properties and metabolic status of Artemia cysts at low water contents: the ‘water replacement hypothesis’ Membranes, metabolism and dry organisms 169187. Leopold A.C. Ithaca, New York Comstock Publishing Associates
Clegg, J.S. (2005) Desiccation tolerance in encysted embryos of the animal extremophile. Artemia. Integrative and Comparative Biology 45, 715724.
Collett, H., Shen, A., Gardner, M., Farrant, J.M., Denby, K.J. and Illing, N. (2004) Towards transcript profiling of desiccation tolerance in Xerophyta humilis: Construction of a normalized 11k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration. Physiologia Plantarum 122, 3953.
de Tullio, M.C. and Arrigoni, O. (2003) The ascorbic acid system in seeds: to protect and to serve. Seed Science Research 13, 249260.
Dietz, K.-J. (2003) Plant peroxiredoxins. Annual Review of Plant Biology 54, 93107.
Elder, R.H., Dell'Aquila, A., Mezzina, M., Sarasin, A. and Osborne, D.J. (1987) DNA ligase in repair and replication in the embryos of rye. Secale cereale. Mutation Research 181, 6171.
Finkel, T. and Holbrook, N.J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408, 239247.
Foyer, C. and Halliwell, B. (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 2125.
Galau, G.A., Hughes, D.W. and Dure, L. (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (lea) mRNAs. Plant Molecular Biology 7, 155170.
Goyal, K., Tisi, L., Basran, A., Browne, J., Burnell, A., Zurdo, J. and Tunnacliffe, A. (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. Journal of Biological Chemistry 278, 1297712984.
Halliwell, B. (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chemistry and Physics of Lipids 44, 327340.
Hendry, G.A.F. (1993) Oxygen and free radical processes in seed longevity. Seed Science Research 3, 141153.
Hong, T.D., Ellis, R.H., Astley, D., Pinnegar, A.E., Groot, S.P.C. and Kraak, H.L. (2005) Survival and vigour of ultra-dry seeds after ten years of hermetic storage. Seed Science and Technology 33, 449460.
Hughes, D.W. and Galau, G.A. (1987) Translational efficiency of Lea mRNAs in cotton embryos: minor changes during embryogenesis and germination. Plant Molecular Biology 9, 301313.
Illing, N., Denby, K.J., Collett, H., Shen, A. and Farrant, J.M. (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integrative and Comparative Biology 45, 771787.
Koster, K.L. (1991) Glass formation and desiccation tolerance in seeds. Plant Physiology 96, 302304.
Koster, K.L. and Leopold, A.C. (1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829832.
Kranner, I., Birtić, S. (2005) A modulating role for antioxidants in desiccation tolerance. Integrative and Comparative Biology 45, 734740.
Kranner, I. and Grill, D. (1996) Significance of thiol-disulphide exchange in resting stages of plant development. Botanica Acta 109, 814.
Kranner, I., Beckett, R.P., Wornik, S., Zorn, M. and Pfeifhofer, H.W. (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant Journal 31, 1324.
Kranner, I., Cram, W.J., Zorn, M., Wornik, S., Yoshimura, I., Stabenheiner, E. and Pfeifhofer, H.W. (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proceedings of the National Academy of Sciences, USA 102, 31413146.
Laloi, C., Apel, K. and Danon, A. (2004) Reactive oxygen signalling: the latest news. Current Opinion in Plant Biology 7, 323328.
Lapinski, J. and Tunnacliffe, A. (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Letters 553, 387390.
Leubner-Metzger, G. (2005) β-1,3-glucanase gene expression in low-hydrated seeds as a mechanism for dormancy release during tobacco after-ripening. Plant Journal 41, 133145.
Levitt, J. (1962) A sulfhydryl-disulfide hypothesis of frost injury and resistance in plants. Journal of Theoretical Biology 3, 355391.
Mínguez, A., de la, Espina, S.M.D. (1993) Immunological characterization of lamins in the nuclear matrix of onion cells. Journal of Cell Science 106, 431439.
Obendorf, R.L. (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Science Research 7, 6374.
Oksanen, C.A. and Zografi, G. (1993) Molecular mobility in mixtures of absorbed water and solid poly(vinylpyrrolidone). Pharmaceutical Research 10, 791799.
Oliver, A.E., Leprince, O., Wolkers, W.F., Hincha, D.K., Heyer, A.G. and Crowe, J.H. (2001) Non-disaccharide-based mechanisms of protection during drying. Cryobiology 43, 151167.
Osborne, M. and Weber, K. (1987) Cytoplasmic intermediate filament proteins and nuclear lamins A, B and C share the IFA epitope. Experimental Cell Research 170, 195203.
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 1337.
Parsegian, V.A. (2002) Protein–water interactions. International Review of Cytology 215, 131.
Proctor, M.C.F. and Pence, V.C. (2002) Vegetative tissues: Bryophytes, vascular resurrection plants and vegetative propagules. pp. 207237. Black, M.;, Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, CABI Publishing.
Rinne, P.L.H., Kaikuranta, P.L.M., van der Plas, L.H.W. and van der Schoot, C. (1999) Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209, 377388.
Rogerson, N.E. and Matthews, S. (1977) Respiratory and carbohydrate changes in developing pea (Pisum sativum) seeds in relation to their ability to withstand desiccation. Journal of Experimental Botany 28, 304313.
Sinniah, U.R., Ellis, R.H. and John, P. (1998) Irrigation and seed quality development in rapid-cycling brassica: soluble carbohydrates and heat-stable proteins. Annals of Botany 82, 647655.
Solomon, A., Salomon, R., Paperna, I. and Glazer, I. (2000) Desiccation stress of entomopathogenic nematodes induces the accumulation of a novel heat-stable protein. Parasitology 121, 409416.
Stacy, R.A.P. and Aalen, R.B. (1998) Identification of a sequence homology between the internal hydrophilic repeated motifs of Group 1 late-embryogenesis-abundant proteins in plants and hydrophilic repeats of the general stress protein GsiB of Bacillus subtilis. Planta 206, 476478.
Stacy, R.A.P., Nordeng, T.W., Culiáñez-Maciá, F.A. and Aalen, R.B. (1999) The dormancy-related peroxiredoxin antioxidant PER1, is located to the nucleus in barley embryo and aleurone. Plant Journal 19, 18.
Steadman, K.J., Pritchard, H.W. and Dey, P.M. (1996) Tissue-specific soluble sugars in seeds as indicators of storage category. Annals of Botany 77, 667674.
Teeter, M.M., Yamano, A., Stec, B. and Mohanty, U. (2001) On the nature of a glassy state of matter in a hydrated protein: Relation to protein function. Proceedings of the National Academy of Sciences, USA 98, 1124211247.
Timasheff, S.N. (1982) Preferential interactions in protein–water co-solvent systems. pp. 7072. in Franks, F.;, Mathias, S.F.; (Eds) Biophysics of water. Chichester, Wiley.
Vertucci, C.W. and Farrant, J.M. (1995) Acquisition and loss of desiccation tolerance. pp. 237271. in Kigel, J.;, Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker.
Viner, R.I. and Clegg, J.S. (2001) Influence of trehalose on the molecular chaperone activity of p26, a small heat shock/α-crystallin protein. Cell Stress and Chaperones 6, 126135.
Walters, C. (1998) Understanding the mechanisms and kinetics of seed aging. Seed Science Research 7, 223244.
Walters, C. and Engels, J. (1998) The effects of storing seeds under extremely dry conditions. Seed Science Research 8, 38.
Walters, C., Ried, J.L. and Walker-Simmons, M.K. (1997) Heat-soluble proteins extracted from wheat embryos have tightly bound sugars and unusual hydration properties. Seed Science Research 7, 125134.
Walters, C., Wheeler, L. and Stanwood, P.C. (2004) Longevity of cryogenically stored seeds. Cryobiology 48, 229244.
Walters, C., Wheeler, L.M. and Grotenhuis, J.M. (2005a) Longevity of seeds stored in a genebank: Species characteristics. Seed Science Research 15, 120.
Walters, C., Hill, L.M. and Wheeler, L.M. (2005b) Dying while dry: kinetics and mechanisms of deterioration in desiccated organisms. Integrative and Comparative Biology 45, 751758.
Whitaker, C., Berjak, P., Kolberg, H. and Pammenter, W. (2004) Responses to various manipulations, and storage potential, of seeds of the unique desert gymnosperm, Welwitschia mirabilis Hook. fil. South African Journal of Botany 70, 622630.
Williams, R.J. and Leopold, A.C. (1989) The glassy state in corn embryos. Plant Physiology 89, 977981.
Wise, M.J. and Tunnacliffe, A. (2004) POPP the question: what do LEA proteins do?. Trends in Plant Science 9, 1317.
Wolkers, W.F., McCready, S., Brandt, W.F., Lindsey, G.G. and Hoekstra, F.A. (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochimica et Biophysica Acta 1544, 196206.

Keywords

Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms

  • Patricia Berjak (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed