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

Published online by Cambridge University Press:  22 February 2007

Patricia Berjak
Patricia Berjak*
Affiliation:
School of Biological and Conservation Sciences, University of KwaZulu-Natal, Durban, 4041, South Africa
*
*Corresponding author:Email: berjak@ukzn.ac.za
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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.

Keywords

active oxygen speciesantioxidantsdesiccation toleranceintracellular glassesLEAlocalized reactivityseed survivalsugars
Type
Invited Review
Information
Seed Science Research , Volume 16 , Issue 1 , March 2006 , pp. 1 - 15
Copyright
Copyright © Cambridge University Press 2006

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References

Aalen, R.B. (1999) Peroxiredoxin antioxidants in seed physiology. Seed Science Research 9, 285–295.CrossRefGoogle Scholar
Alpert, P. (2005) The limits and frontiers of desiccation-tolerant life. Integrative and Comparative Biology 45, 685–695.CrossRefGoogle ScholarPubMed
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, 6675–6682.CrossRefGoogle ScholarPubMed
Bailly, C. (2004) Active oxygen species and antioxidants in seed biology. Seed Science Research 14, 93–107.CrossRefGoogle Scholar
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, 47–55.CrossRefGoogle Scholar
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, 133–139.CrossRefGoogle ScholarPubMed
Benson, E.E. and Bremner, D. (2004) Oxidative stress in the frozen plant: A free radical point of view. 205–241. in Fuller, B.J.;, Lane, N.;, Benson, E.E. (Eds.) Life in the frozen state. Boca Raton, CRC Press.CrossRefGoogle Scholar
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, 109–116.CrossRefGoogle Scholar
Billi, D. and Potts, M. (2002) Life and death of dried prokaryotes. Research in Microbiology 153, 7–12.CrossRefGoogle ScholarPubMed
Black, M. and Pritchard, H.W. (2002) Desiccation and survival in plants. Drying without dying. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Browne, J., Tunnacliffe, A. and Burnell, A. (2002) Anhydrobiosis: plant desiccation gene found in a nematode. Nature 416, 38CrossRefGoogle Scholar
Bruni, F. and Leopold, A.C. (1992) Pools of water in anhydrobiotic organisms. A thermally stimulated depolarization current study. Biophysical Journal 63, 663–672.CrossRefGoogle ScholarPubMed
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, 17–25.CrossRefGoogle Scholar
Buitink, J. and Leprince, O. (2004) Glass formation in plant anyhdrobiotes: survival in the dry state. Cryobiology 48, 215–228.CrossRefGoogle ScholarPubMed
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, 1217–1224.CrossRefGoogle Scholar
Buitink, J., Hoekstra, F.A. and Leprince, O. (2002) Biochemistry and biophysics of tolerance systems. pp 293–318. in Black, M.;, Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Burke, M.J. (1986) The glassy state and survival of anhydrous biological systems Membranes, metabolism and dry organisms 358–363. Leopold A.C. Ithaca, New York Comstock Publishing AssociatesGoogle Scholar
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, 527–532.CrossRefGoogle Scholar
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 169–187. Leopold A.C. Ithaca, New York Comstock Publishing AssociatesGoogle Scholar
Clegg, J.S. (2005) Desiccation tolerance in encysted embryos of the animal extremophile. Artemia. Integrative and Comparative Biology 45, 715–724.CrossRefGoogle ScholarPubMed
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, 39–53.CrossRefGoogle Scholar
de Tullio, M.C. and Arrigoni, O. (2003) The ascorbic acid system in seeds: to protect and to serve. Seed Science Research 13, 249–260.CrossRefGoogle Scholar
Dietz, K.-J. (2003) Plant peroxiredoxins. Annual Review of Plant Biology 54, 93–107.CrossRefGoogle ScholarPubMed
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, 61–71.CrossRefGoogle Scholar
Finkel, T. and Holbrook, N.J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408, 239–247.CrossRefGoogle ScholarPubMed
Foyer, C. and Halliwell, B. (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21–25.CrossRefGoogle ScholarPubMed
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, 155–170.CrossRefGoogle ScholarPubMed
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, 12977–12984.CrossRefGoogle Scholar
Halliwell, B. (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chemistry and Physics of Lipids 44, 327–340.CrossRefGoogle Scholar
Hendry, G.A.F. (1993) Oxygen and free radical processes in seed longevity. Seed Science Research 3, 141–153.CrossRefGoogle Scholar
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, 449–460.CrossRefGoogle Scholar
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, 301–313.CrossRefGoogle ScholarPubMed
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, 771–787.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.CrossRefGoogle ScholarPubMed
Kranner, I., Birtić, S. (2005) A modulating role for antioxidants in desiccation tolerance. Integrative and Comparative Biology 45, 734–740.CrossRefGoogle ScholarPubMed
Kranner, I. and Grill, D. (1996) Significance of thiol-disulphide exchange in resting stages of plant development. Botanica Acta 109, 8–14.CrossRefGoogle Scholar
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, 13–24.CrossRefGoogle ScholarPubMed
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, 3141–3146.CrossRefGoogle Scholar
Laloi, C., Apel, K. and Danon, A. (2004) Reactive oxygen signalling: the latest news. Current Opinion in Plant Biology 7, 323–328.CrossRefGoogle ScholarPubMed
Lapinski, J. and Tunnacliffe, A. (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Letters 553, 387–390.CrossRefGoogle ScholarPubMed
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, 133–145.CrossRefGoogle ScholarPubMed
Levitt, J. (1962) A sulfhydryl-disulfide hypothesis of frost injury and resistance in plants. Journal of Theoretical Biology 3, 355–391.CrossRefGoogle Scholar
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, 431–439.CrossRefGoogle ScholarPubMed
Obendorf, R.L. (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Science Research 7, 63–74.CrossRefGoogle Scholar
Oksanen, C.A. and Zografi, G. (1993) Molecular mobility in mixtures of absorbed water and solid poly(vinylpyrrolidone). Pharmaceutical Research 10, 791–799.CrossRefGoogle ScholarPubMed
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, 151–167.CrossRefGoogle ScholarPubMed
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, 195–203.CrossRefGoogle Scholar
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 13–37.CrossRefGoogle Scholar
Parsegian, V.A. (2002) Protein–water interactions. International Review of Cytology 215, 1–31.CrossRefGoogle ScholarPubMed
Proctor, M.C.F. and Pence, V.C. (2002) Vegetative tissues: Bryophytes, vascular resurrection plants and vegetative propagules. pp. 207–237. Black, M.;, Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, CABI Publishing.CrossRefGoogle Scholar
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, 377–388.CrossRefGoogle ScholarPubMed
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, 304–313.CrossRefGoogle Scholar
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, 647–655.CrossRefGoogle Scholar
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, 409–416.CrossRefGoogle ScholarPubMed
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, 476–478.CrossRefGoogle ScholarPubMed
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, 1–8.CrossRefGoogle Scholar
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, 667–674.CrossRefGoogle Scholar
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, 11242–11247.CrossRefGoogle Scholar
Timasheff, S.N. (1982) Preferential interactions in protein–water co-solvent systems. pp. 70–72. in Franks, F.;, Mathias, S.F.; (Eds) Biophysics of water. Chichester, Wiley.Google Scholar
Vertucci, C.W. and Farrant, J.M. (1995) Acquisition and loss of desiccation tolerance. pp. 237–271. in Kigel, J.;, Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker.Google Scholar
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, 126–135.2.0.CO;2>CrossRefGoogle ScholarPubMed
Walters, C. (1998) Understanding the mechanisms and kinetics of seed aging. Seed Science Research 7, 223–244.CrossRefGoogle Scholar
Walters, C. and Engels, J. (1998) The effects of storing seeds under extremely dry conditions. Seed Science Research 8, 3–8.Google Scholar
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, 125–134.CrossRefGoogle Scholar
Walters, C., Wheeler, L. and Stanwood, P.C. (2004) Longevity of cryogenically stored seeds. Cryobiology 48, 229–244.CrossRefGoogle ScholarPubMed
Walters, C., Wheeler, L.M. and Grotenhuis, J.M. (2005a) Longevity of seeds stored in a genebank: Species characteristics. Seed Science Research 15, 1–20.CrossRefGoogle Scholar
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, 751–758.CrossRefGoogle ScholarPubMed
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, 622–630.CrossRefGoogle Scholar
Williams, R.J. and Leopold, A.C. (1989) The glassy state in corn embryos. Plant Physiology 89, 977–981.CrossRefGoogle Scholar
Wise, M.J. and Tunnacliffe, A. (2004) POPP the question: what do LEA proteins do?. Trends in Plant Science 9, 13–17.CrossRefGoogle Scholar
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, 196–206.CrossRefGoogle ScholarPubMed