Abstract
The ability of vegetative plant tissues to survive desiccation is an uncommon trait, although plants that are able to do this represent all major classes of plants. Two classes of vegetative desiccation-tolerant plants exist; those that are modified desiccation-tolerant and can only survive desiccation if drying rates are slow, and those that are fully desiccation-tolerant and can survive even rapid drying rates. Investigations into the cellular level responses of these two types of plants has lead to an understanding of the underlying mechanisms of desiccation-tolerance. The following proposed mechanisms for desiccation-tolerance are presented. Modified desiccation-tolerant plants utilize inducible cellular protection systems supplemented in part by a minor rehydration induced repair component. Fully desiccation-tolerant plants utilize a rehydration induced repair system that is complemented by a constitutive protection component. This minireview explores the evidence for these proposed mechanisms in an attempt to lay the theoretical ground work for future work in this area.
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Aalen RB, Opsahl-Ferstad HG, Linnestad C and Olsen OA (1994) Transcripts encoding an oleosin and a dormancy-related protein are present in both the aleurone layer and in the embryo of developing barley (Hordeum vulgare). Plant J 5: 385-396
Alpert P (1987) Morphological control of water relations in an assemblage of mosses. Abstracts of the XIV International Botanical Congress, p 378. Botanical Museum, Berlin-Dahlem, Germany
Bartels DR and Nelson D (1994) Approaches to improve stress tolerance using molecular genetics. Plant Cell Environ 17: 659-667
Bartels DR, Alexander K, Schneider R, Elster R, Velasco J, Alamillo G, Bianchi G, Nelson D and Salamini F (1993) Desiccation-related gene products analyzed in a resurrection plant and in barley embryos. In: Close TJ and Bray EA (eds) Plant responses to cellular dehydration during environmental stress. Current Topics in Plant Physiology: Am. Soc. Plant Physiol. Series Vol. 10, pp 119-127
Bartels DR, Hanke C, Schneider K, Michel D and Salamini F (1992) A desiccation-related Elip-like gene from the resurrection plant Craterostigma plantagineum is regulated by light and ABA. EMBO J 11: 277-2778
Bartels DR, Schneider K, Terstappen G, Piatkowski D and Salamini F (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181: 27-34
Bernacchia G, Salamini F and Bartels D (1996) Molecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineum. Plant Physiol 111: 1043- 1050
Bewley JD (1972) The conservation of polyribosomes in the moss Tortula ruralis during total desiccation. J Expt Bot 23: 692-698
Bewley JD (1973) Desiccation and protein synthesis in the moss Tortula ruralis. Can J Bot 51: 203-206
Bewley JD (1979) Physiological aspects of desiccationtolerance, Annu Rev Plant Physiol 30: 195-238
Bewley JD, Reynolds TL and Oliver MJ (1993) Evolving strategies in the adaptation to desiccation. In: Close TJ and Bray EA (eds) Plant responses to cellular dehydration during environmental stress. Current Topics in Plant Physiology: Am. Soc. Plant Physiol. Series Vol. 10, pp 193-201
Bewley JD, Halmer P, Krochko JE and Winner WE (1978) Metabolism of a drought-tolerant and a drought-sensitive moss: respiration, ATP synthesis and carbohydrate status. In: Crowe JH and Clegg JS (eds) Dry biological systems, pp 185- 203. New York: Academic Press
Bewley JD and Krochko JE (1982) Desiccation-tolerance. In: Lange OL, Nobel PS, Osmond CB, and Ziegler H (eds) Encyclopedia of plant physiology. Vol 12B, Physiological Ecology II, pp 325-378. Berlin: Springer-Verlag
Bewley JD and Oliver MJ (1992) Desiccation-tolerance in vegetative plant tissues and seeds: Protein synthesis in relation to desiccation and a potential role for protection and repair mechanisms. In: Osmond CB and Somero G (eds) Water and life: A comparative analysis of water relationships at the organismic, cellular and molecular levels, pp 141-160. Berlin: Springer-Verlag
Bianchi G, Gamba A, Limiroli R, Pozzi N, Elster R, Salamini F and Bartels DR (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiologia Plant 87: 223-226
Bianchi G, Gamba A, Murelli C, Salamini F and Bartels DR (1991a) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. Plant J 1: 355-359
Bianchi G, Murelli C, Bochicchio A and Vazzana C (1991b) Changes in low-molecular weight substances in Boea hygroscopica in response to desiccation and rehydration. Phytochemistry 30: 461-466
Blomstedt CK, Neale AD, Gianello RD, Hamill JD and Gaff DF (1997) Isolation and characterization of cDNAs associated with the onset of desiccation tolerance in the resurrection grass, Sporobolus stapfianus. Plant Growth Reg. In Press.
Bopp M and Werner O (1993) Abscisic acid and desiccationtolerance in mosses. Bot Acta 106: 103-106
Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103: 1035-1040
Burke MJ (1986) The glassy state and survival of anhydrous biological systems. In: Leopold AC (ed) Membranes, metabolism and dry organisms, pp 358-363. Ithaca, NY: Cornell Univ Press
Chandler PM, Munns R and Robertson M (1993) Regulation of dehydrin expression. In: Close TJ and Bray EA (eds) Plant responses to cellular dehydration during environmental stress. Current Topics in Plant Physiology. Am. Soc. Plant Physiol. Series Vol. 10, pp 159-166
Close TJ, Fenton RD, Yang A, Asghar R, DeMason DA, Crone DE, Meyer NC and Moonan F (1993) Dehydrin: The protein In: Close TJ and Bray EA (eds) Plant responses to cellular dehydration during environmental stress. Current Topics in Plant Physiology. Am Soc Plant Physiol Series Vol. 10, pp 104-118
Crowe JH, Hoekstra FA and Crowe LM (1992) Anhydrobiosis Annu Rev Physiol 54: 579-599
Dhindsa R and Bewley JD (1977) Water stress and protein synthesis: V. Protein synthesis, protein stability and membrane permeability in a drought-sensitive and drought-tolerant moss. Plant Physiol 59: 295-300
Drennan PM, Smith MT, Goldsworthy D and van Staden J (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. J Plant Physiol 142: 493-496
Dure L III (1993) A repeating 11-mer amino acid motif and plant desiccation, Plant J 3: 363-369
Farrant JM, Pammenter NW and Berjak P (1993) Seed desiccation in relation to desiccation-tolerance: a comparison between desiccation-sensitive (recalcitrant) seeds of Avencenia marina and desiccation-tolerant types. Seed Sci Res 3: 1-13
Gaff DF (1980) Protoplasmic tolerance to extreme water stress. In: Turner NC and Kramer PJ (eds) Adaptation of plants to water and high temperature stress, pp 207-230. New York: Wiley Interscience
Gaff DF (1989) Responses of desiccation-tolerant “resurrection” plants to water stress. In: Krebb KH, Richter H and Hinkley TM (eds) Structural and functional responses to environmental stresses, pp 255-268. SPB Academic The Hague Publishers
Gaff DF and Ellis RP (1974) South African grasses with foliage that revives after dehydration. Bothalia 11: 305-308
Gaff DF and Loveys BR (1994) Abscisic acid levels in drying plants of a resurrection grass. First Asia-Pacific Conf Plant Physiol., Kuala Lumpur. Nov 1992. Trans Malaysian Soc Plant Physiol 3: 286-287
Goldmark PJ, Curry J, Morris CF and Walker-Simmons MK (1992) Cloning and expression of an embryo-specific mRNA up-regulated in hydrated dormant seeds. Plant Mol Biol 19: 433-441
Henckel RA, Statrova NA and Shaposnikova SV (1977) Protein synthesis in poikiloxerophyte and wheat embryos during the initial period of swelling, Sov Plant Physiol 14: 754-762
Ingram J and Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 377-403
Kaiser K, Gaff DF and Outlaw WH Jr (1985) Sugar contents of leaves of desiccation sensitive and desiccation-tolerant plants. Naturwissenschaften 72: 608-609
Kuang J, Gaff DF, Gianello RD, Blomstedt CK, Neale AD and Hamill JD. (1995) Changes in in vivo protein complements in drying leaves of the desiccation-tolerant grass Sporobolus stapfianus and the desiccation-sensitive grass Sporobolus pyramidalis. Aust J Plant Physiol 22: 1027-1034
Leopold AC, Bruni F and Williams RJ (1992), Water in dry organisms. In: Somero GN, Osmond CB and Bolis CL (eds) Water and life. Comparative analysis of water relationships at the organismic, cellular and molecular levels, pp 161-169. Berlin: Springer-Verlag
Oliver MJ (1983) The role of desiccation in the control of transcription and translation in the moss Tortula ruralis. PhD Thesis, Univ. of Calgary. Calgary Canada
Oliver MJ (1991) Influence of protoplasmic water loss on the control of protein synthesis in the desiccation-tolerant moss Tortula ruralis: Ramifications for a repair-based mechanism of desiccation-tolerance. Plant Physiol 97: 1501-1511
Oliver MJ (1996), Desiccation-tolerance in vegetative plant cells. Physiol Plant 97: 779-787
Oliver MJ and Bewley JD (1984a) Desiccation and ultrastructure in bryophytes. Adv Bryol 2: 91-131
Oliver MJ and Bewley JD (1984b) Plant desiccation and protein synthesis: IV. RNA synthesis, stability, and recruitment of RNA into protein synthesis upon rehydration of the desiccation-tolerant moss Tortula ruralis. Plant Physiol 74: 21-25
Oliver MJ and Bewley JD (1984c) Plant desiccation and protein synthesis: VI. Changes in protein synthesis elicited by desiccation of the moss Tortula ruralis are effected at the translational level. Plant Physiol 74: 923-927
Oliver MJ and Bewley JD (1997) Desiccation-tolerance of plant tissues: a mechanistic overview. Hort Rev 18: 171-213
Piatkowski D, Schneider K, Salamini F and Bartels DR (1990) Characterization of five abscisic acid-responsive cDNA clones from the desiccation-tolerant plant Craterostigma plantagineum and their relationship to other water-stress genes. Plant Physiol 94: 1682-1688
Platt KA, Oliver MJ and Thomson WW (1994) Membranes and organelles of dehydrated Selaginella and Tortula retain their normal configuration and structural integrity: freeze fracture evidence. Protoplasma 178: 57-65
Reynolds TL and Bewley JD (1993a) Characterization of protein synthetic changes in a desiccation-tolerant fern, Polypodium virginianum.Comparison of the effects of drying, rehydration and abscisic acid. J Expt Bot 44: 921-928
Reynolds TL and Bewley JD (1993b) Abscisic acid enhances the ability of the desiccation-tolerant fern Polypodium virginianum to withstand drying. J Expt Bot 44: 1771-1779
Schneider K, Wells B, Schmelzer E, Salamini F and Bartels DR (1993) Desiccation leads to the rapid accumulation of both cytosolic and chloroplastic proteins in the resurrection plant Craterostigma plantagineum Hoscht. Planta 189: 120-131
Schonbeck MW and Bewley JD(1981a) Responses of themoss Tortula ruralis to desiccation treatments. I. Effects of minimum water content and rates of dehydration and rehydration. Can J Bot 59: 2698-2706
Schonbeck MW and Bewley JD (1981b) Responses of the moss Tortula ruralis to desiccation treatments. II. Variations in desiccation tolerance. Can J Bot 59: 2707-2712
Scott HB II, and Oliver MJ, (1994) Accumulation and polysomal recruitment of transcripts in response to desiccation and rehydration of themoss Tortula ruralis. J Expt Bot 45: 577-583
Siebert G, Loris J, Zollner B, Frenzel B and Zahn RK (1976) The conservation of poly (A) containing RNA during the dormant state of the moss Polytrichum commune. Nucl Acid Res 3: 1997-2003
Simon EW (1978) Membranes in dry and imbibing seeds. In: Crowe JH and Clegg JS (eds) Dry biological systems, pp 205- 224. New York: Academic Press
Simon EW and Mills LK (1983) Imbibition, leakage, and membranes. In: Nozzolillo C, Lee PJ, and Loewus FA (eds) Mobilization of reserves in germination, pp 9-27. New York: Plenum Publ. Corp.
Skriver K and Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2: 503-512
Smirnoff N (1992) The carbohydrates of bryophytes in relation to desiccation-tolerance. J Bryol 17: 185-191
Strauss G and Hauser H (1986) Stabilization of small unilamellar phospholipid vesicles by sucrose during freezing and dehydration. In: Leopold AC (ed) Membranes, metabolismand dry organisms, pp 318-326. Ithaca, NY: Cornell Univ Press
Tuba Z, Lichtenthaler HK, Csintalan Z and Pócs T (1993a) Regreening of desiccated leaves of the poikilochlorophyllous Xerophyta scabrida upon rehydration. J Plant Physiol 142: 103-108
Tuba Z, Lichtenthaler HK, Maroti I and Csintalan Z (1993b) Resynthesis of thylakoids and functional chloroplasts in the desiccated leaves of the poikilochlorophyllous plant Xerophyta scabrida upon rehydration. J Plant Physiol 142: 742-748
Valasco R, Salamini F and Bartels DR (1994) Dehydration and ABA increase mRNA levels and enzyme activity of cytolsolic GAPDHin the resurrection plant Craterostigma plantagineum. Plant Mol Biol 26: 541-546
Werner O, Espin RMR, Bopp M and Atzorn R (1991) Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186: 99-103
Willis AJ (1964) Investigations on the physiological ecology of Tortula ruraliformis. Trans Brit Bryol Soc 4: 668-683
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Oliver, M.J., O'Mahony, P. & Wood, A.J. “To dryness and beyond” – Preparation for the dried state and rehydration in vegetative desiccation-tolerant plants. Plant Growth Regulation 24, 193–201 (1998). https://doi.org/10.1023/A:1005863015130
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DOI: https://doi.org/10.1023/A:1005863015130