Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-25T20:54:55.910Z Has data issue: false hasContentIssue false
  • English
  • Français

DNA and desiccation tolerance

Published online by Cambridge University Press:  19 September 2008

D. J. Osborne  and
I. I. Boubriak
D. J. Osborne*
Affiliation:
Oxford Research Unit, The Open University, Foxcombe Hall, Boars Hill, Oxford, OX1 5HR, UK
I. I. Boubriak
Affiliation:
Oxford Research Unit, The Open University, Foxcombe Hall, Boars Hill, Oxford, OX1 5HR, UK
*
* Correspondence
Get access Rights & Permissions [Opens in a new window]

Abstract

This article reviews mechanisms by which specialized cells of different life forms have overcome the lethal effects of dehydration and considers how the maintenance of genetic information is central to survival. As a dynamic and hydrated molecule in vivo, DNA can assume different conformational structures depending upon the water activity, the base sequence and the presence of specific binding proteins. The attainment of stable secondary structures that are resistant to degradation in vivo at low water potentials is proposed as a likely accompaniment to desiccation tolerance. In addition, chemical modification of bases in DNA, the extent of methylation and conformational changes could determine the expression of different gene sequences as cells pass from desiccation-tolerant to desiccation-intolerant states. We monitored the integrity of extracted DNA in embryos of seeds and in wind-dispersed pollen during transition from their desiccation tolerance to desiccation intolerance on hydration and germination. We present evidence to show that the DNA of these two stages is different and that it is the DNA from desiccation-tolerant cells only that retains integrity when the cells are subjected to desiccation regimes. We discuss these findings in relation to certain hydration-sensitive DNA structures and to other relevant biological systems.

Keywords

desiccation toleranceDNA integrityDNA repairpollenseedembryos
Type
Short Communication
Information
Seed Science Research , Volume 4 , Issue 2 , June 1994 , pp. 175 - 185
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Permanent address: Institute of Cell Biology and Genetic Engineering, Ukrainian Academy of Sciences, Zabolotnogo Street 148, Kiev, 252650, Ukraine.

References

Bartels, D., Singh, M. and Salamini, F. (1988) Onset of desiccation tolerance during development of the barley embryo. Planta 175, 485–492.CrossRefGoogle ScholarPubMed
Berjak, P., Farrant, J.M. and Pammenter, N.W. (1989) The basis of recalcitrant seed behaviour: cell biology of the homoiohydrous seed condition. pp 89–108 in Taylorson, R.B. (Ed.) Recent advances in the development and germination of seeds. New York, Plenum Press.CrossRefGoogle Scholar
Berjak, P., Vertucci, C.W. and Pammenter, N.W. (1992) Homoiohydrous (recalcitrant) seeds: developmental status, desiccation sensitivity and the state of water in axes of Landolphia kirkii Dyer. Planta 186, 249–261.CrossRefGoogle ScholarPubMed
Beswick, H.T. and Harding, J.J. (1985) Aldehydes or dicarbonyls in non-enzymic glycosylation of proteins. Biochemical Journal 226, 385–389.CrossRefGoogle ScholarPubMed
Bewley, J.D. (1979) Physiological aspects of desiccation tolerance. Annual Review of Plant Physiology 30, 195–238.CrossRefGoogle Scholar
Bianchi, M. and Viotti, A. (1988) DNA methylation and tissue-specific transcription of the storage protein genes of maize. Plant Molecular Biology 11, 203–214.CrossRefGoogle ScholarPubMed
Blackman, S.A., Wettlaufer, S.H., Obendorf, R.L. and Leopold, A.C. (1991) Maturation proteins associated with desiccation tolerance in soybean. Plant Physiology 96, 868–874.CrossRefGoogle ScholarPubMed
Bostock, R.M. and Quatrano, R.S. (1992) Regulation of Em gene expression in rice. Interaction between osmotic stress and abscisic acid. Plant Physiology 98, 1356–1363.CrossRefGoogle ScholarPubMed
Boubriak, I.I. (1986) Ecophysiological role of DNA repair systems in pollen. PhD Thesis, Kiev, Ukraine [in Russian].Google Scholar
Bradford, K.J. and Chandler, P.M. (1992) Expression of ‘dehydrin-like’ proteins in embryos and seedlings of Zizania palustris and Oryza sativa during dehydration. Plant Physiology 99, 488–494.CrossRefGoogle ScholarPubMed
Bruni, F. and Leopold, A.C. (1991) Glass transition in soybean seed. Relevance to anhydrous biology. Plant Physiology 96, 660–663.CrossRefGoogle ScholarPubMed
Brunori, A. (1967) A relationship between DNA synthesis and water content during ripening of Vicia faba seed. Caryologia 20, 333–338.CrossRefGoogle Scholar
Clegg, J.S. (1974) Biochemical adaptations associated with the embryonic dormancy of Artemia salina. Transactions of the American Microscopical Society 93, 481–490.CrossRefGoogle Scholar
Crowe, J.H. and Clegg, J.S. (1973) Anhydrobiosis. Stroudsberg, PA, Dowden, Hutchinson and Ross Inc.Google Scholar
Dickerson, R.E. and Drew, H.R. (1981) Structure of B-DNA dodecamer II. Influence of base sequence in helix structure. Journal of Molecular Biology 149, 761–786.CrossRefGoogle ScholarPubMed
Doerfler, W. (1983) DNA methylation and gene activity. Annual Review of Biochemistry 52, 93–124.CrossRefGoogle ScholarPubMed
Elder, R.H. and Osborne, D.J. (1993) Function of DNA synthesis and DNA repair in the survival of embryos during early germination and in dormancy. Seed Science Research 3, 43–53.CrossRefGoogle Scholar
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
Farrant, J.M., Berjak, P. and Pammenter, N.W. (1992a) Proteins in development and germination of a desiccation-sensitive (recalcitrant) seed species. Plant Growth Regulation 11, 257–265.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1992b) Development of the recalcitrant (homoiohydrous) seeds of Avicennia marina: anatomical, ultrastructural and biochemical events associated with development from histodifferentiation to maturation. Annals of Botany 70, 75–86.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1993) Seed development in relation to desiccation tolerance: a comparison between desiccation-sensitive (recalcitrant) seeds of Avicennia marina and desiccation-tolerant types. Seed Science Research 3, 1–13.CrossRefGoogle Scholar
Gómez, J., Sánchez-Martínez, D., Stiefel, V., Rigau, J., Puigdomènech, P. and Pagès, M. (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 334, 262–264.CrossRefGoogle ScholarPubMed
Hagerman, P.J. (1990) Sequence-directed curvature of DNA. Annual Review of Biochemistry 59, 755–781.CrossRefGoogle ScholarPubMed
Hinton, H.E. (1960) Cryptobiosis in the larva of Polydedilum vanderplanki Hint (Chironomidae). Journal of Insect Physiology 5, 286–300.CrossRefGoogle Scholar
Howlett, S.K. and Reik, W. (1991) Methylation levels of maternal and paternal genomes during pre-implantation development. Development 113, 119–127.CrossRefGoogle Scholar
Kabakov, A.E. and Poverenny, A.M. (1993) Immunological probing of DNA structure with monoclonal antibody to OsO4/2,2′bipyridine adduct. Analytical Biochemistry 211, 224–232.CrossRefGoogle Scholar
Kermode, A.R. (1990) Regulatory mechanisms involved in the transition from seed development to germination. Critical Reviews in Plant Sciences 9, 155–195.CrossRefGoogle Scholar
Kuo, T.M., van Middlesworth, J.F. and Wolf, W.J. (1988) Content of raffinose, oligosaccharides and sucrose in various plant seeds. Journal of Agricultural and Food Chemistry 36, 32–36.CrossRefGoogle 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.CrossRefGoogle Scholar
Li, E., Bestor, T.H. and Jaenisch, R. (1992) Targeted mutation of the methyltransferase gene results in embryonic lethality. Cell 69, 915–926.CrossRefGoogle ScholarPubMed
Lindahl, T. (1993) Instability and decay of the primary structure of DNA. Nature 362, 709–715.CrossRefGoogle ScholarPubMed
Madin, K.A.C. and Crowe, J.H. (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration. Journal of Experimental Zoology 193, 335–342.CrossRefGoogle Scholar
Mansingh, A. (1974) Studies in insect dormancy. II. Relationship of cold-hardiness to diapause and quiescence in the eastern leaf caterpillar, Malacosoma americanum (Fab.), Lasiocampidae: Lepidoptera. Canadian Journal of Zoology 52, 629–637.CrossRefGoogle Scholar
Nordheim, A., Pardue, M.L., Weiner, L.M., Lowenhauft, K., Scholton, P., Möller, A., Rich, A. and Stoller, B.D. (1986) Analysis of Z-DNA in fixed polytene chromosomes with monoclonal antibodies that show base sequence-dependent selectivity in reactions with super-coiled plasmids and polynucleotides. Journal of Biological Chemistry 261, 468–476.CrossRefGoogle Scholar
Palmgren, G., Mattsson, O. and Okkels, F.T. (1991) Specific levels of DNA methylation in various tissues, cell lines and cell types of Daucus carota. Plant Physiology 95, 174–178.CrossRefGoogle ScholarPubMed
Saenger, W., Hunter, W.N. and Kennard, O. (1986) DNA conformation is determined by economics in the hydration of phosphate groups. Nature 324, 385–388.CrossRefGoogle ScholarPubMed
Setlow, P. (1992a) I will survive: protecting and repairing spore DNA. Journal of Bacteriology 174, 2737–2741.CrossRefGoogle ScholarPubMed
Setlow, P. (1992b) DNA in dormant spores of Bacillus species is in an A-like conformation. Molecular Microbiology 6, 563–567.CrossRefGoogle Scholar
Spena, A., Viotti, A. and Pirrotta, V. (1983) Two adjacent genomic zein sequences: structure, organization and tissue-specific restriction pattern. Journal of Molecular Biology 169, 799–811.CrossRefGoogle ScholarPubMed
Vertucci, C.W. and Leopold, A.C. (1987) The relationship between water binding and desciccation tolerance in tissues. Plant Physiology 85, 232–238.CrossRefGoogle ScholarPubMed
Villiers, T.A. and Edgcumbe, D.J. (1975) On the cause of seed deterioration in dry storage. Seed Science and Technology 3, 761–774.Google Scholar
Wells, R.D. and Harvey, S.C. (1988) Unusual DNA structures. New York, Springer Verlag.CrossRefGoogle ScholarPubMed