“To dryness and beyond” – Preparation for the dried state and rehydration in vegetative desiccation-tolerant plants

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.

This is a preview of subscription content, access via your institution.

References

  1. 1.

    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

    Google Scholar 

  2. 2.

    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

    Google Scholar 

  3. 3.

    Bartels DR and Nelson D (1994) Approaches to improve stress tolerance using molecular genetics. Plant Cell Environ 17: 659-667

    Google Scholar 

  4. 4.

    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

  5. 5.

    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

    Google Scholar 

  6. 6.

    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

    Google Scholar 

  7. 7.

    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

    Google Scholar 

  8. 8.

    Bewley JD (1972) The conservation of polyribosomes in the moss Tortula ruralis during total desiccation. J Expt Bot 23: 692-698

    Google Scholar 

  9. 9.

    Bewley JD (1973) Desiccation and protein synthesis in the moss Tortula ruralis. Can J Bot 51: 203-206

    Google Scholar 

  10. 10.

    Bewley JD (1979) Physiological aspects of desiccationtolerance, Annu Rev Plant Physiol 30: 195-238

    Google Scholar 

  11. 11.

    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

  12. 12.

    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

    Google Scholar 

  13. 13.

    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

    Google Scholar 

  14. 14.

    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

    Google Scholar 

  15. 15.

    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

    Google Scholar 

  16. 16.

    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

    Google Scholar 

  17. 17.

    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

    Google Scholar 

  18. 18.

    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.

  19. 19.

    Bopp M and Werner O (1993) Abscisic acid and desiccationtolerance in mosses. Bot Acta 106: 103-106

    Google Scholar 

  20. 20.

    Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103: 1035-1040

    Google Scholar 

  21. 21.

    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

    Google Scholar 

  22. 22.

    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

  23. 23.

    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

  24. 24.

    Crowe JH, Hoekstra FA and Crowe LM (1992) Anhydrobiosis Annu Rev Physiol 54: 579-599

    Google Scholar 

  25. 25.

    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

    Google Scholar 

  26. 26.

    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

    Google Scholar 

  27. 27.

    Dure L III (1993) A repeating 11-mer amino acid motif and plant desiccation, Plant J 3: 363-369

    Google Scholar 

  28. 28.

    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

    Google Scholar 

  29. 29.

    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

    Google Scholar 

  30. 30.

    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

  31. 31.

    Gaff DF and Ellis RP (1974) South African grasses with foliage that revives after dehydration. Bothalia 11: 305-308

    Google Scholar 

  32. 32.

    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

    Google Scholar 

  33. 33.

    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

    Google Scholar 

  34. 34.

    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

    Google Scholar 

  35. 35.

    Ingram J and Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 377-403

    Google Scholar 

  36. 36.

    Kaiser K, Gaff DF and Outlaw WH Jr (1985) Sugar contents of leaves of desiccation sensitive and desiccation-tolerant plants. Naturwissenschaften 72: 608-609

    Google Scholar 

  37. 37.

    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

    Google Scholar 

  38. 38.

    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

    Google Scholar 

  39. 39.

    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

    Google Scholar 

  40. 40.

    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

    Google Scholar 

  41. 41.

    Oliver MJ (1996), Desiccation-tolerance in vegetative plant cells. Physiol Plant 97: 779-787

    Google Scholar 

  42. 42.

    Oliver MJ and Bewley JD (1984a) Desiccation and ultrastructure in bryophytes. Adv Bryol 2: 91-131

    Google Scholar 

  43. 43.

    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

    Google Scholar 

  44. 44.

    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

    Google Scholar 

  45. 45.

    Oliver MJ and Bewley JD (1997) Desiccation-tolerance of plant tissues: a mechanistic overview. Hort Rev 18: 171-213

    Google Scholar 

  46. 46.

    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

    Google Scholar 

  47. 47.

    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

    Google Scholar 

  48. 48.

    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

    Google Scholar 

  49. 49.

    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

    Google Scholar 

  50. 50.

    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

    Google Scholar 

  51. 51.

    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

    Google Scholar 

  52. 52.

    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

    Google Scholar 

  53. 53.

    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

    Google Scholar 

  54. 54.

    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

    Google Scholar 

  55. 55.

    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

    Google Scholar 

  56. 56.

    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.

    Google Scholar 

  57. 57.

    Skriver K and Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2: 503-512

    Google Scholar 

  58. 58.

    Smirnoff N (1992) The carbohydrates of bryophytes in relation to desiccation-tolerance. J Bryol 17: 185-191

    Google Scholar 

  59. 59.

    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

    Google Scholar 

  60. 60.

    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

    Google Scholar 

  61. 61.

    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

    Google Scholar 

  62. 62.

    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

    Google Scholar 

  63. 63.

    Werner O, Espin RMR, Bopp M and Atzorn R (1991) Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186: 99-103

    Google Scholar 

  64. 64.

    Willis AJ (1964) Investigations on the physiological ecology of Tortula ruraliformis. Trans Brit Bryol Soc 4: 668-683

    Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • cellular protection
  • cellular repair
  • desiccation
  • tolerance mechanism
  • vegetative tissues