The bryophyte paradox: tolerance of desiccation, evasion of drought

Abstract

Vascular plants represent one strategy of adaptation to the uneven and erratic supply of water on land. Desiccation-tolerant (DT) bryophytes represent an alternative, photosynthesising and growing when water is freely available, and suspending metabolism when it is not. By contrast with vascular plants, DT bryophytes are typically ectohydric, carrying external capillary water which can vary widely in quantity without affecting the water status of the cells. External water is important in water conduction, and results in bryophyte leaf cells functioning for most of the time at full turgor; water stress is a relatively brief transient phase before full desiccation. All bryophytes are C3 plants, and their cells are essentially mesophytic in important physiological respects. Their carbohydrate content shows parallels with that of maturing embryos of DT seeds. Initial recovery from moderate periods of desiccation is very rapid, and substantial elements of it appear to be independent of protein synthesis. Desiccation tolerance in effect acts as a device that evades the problems of drought, and in various adaptive features DT bryophytes are more comparable with (mesic) desert ephemerals or temperate winter annuals (but on a shorter time scale, with DT vegetative tissues substituting for DT seeds) than with drought-tolerant vascular plants.

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References

  1. Abel, W. O. 1956. Die Austrocknungsresistenz der Laubmoose. Sitzungsberichte. Österreische Akademie der Wissenschaften. Mathematisch-naturwissenschaftliche Klasse, Abt.I 165: 619–707.

    Google Scholar 

  2. Anderson, J. M., Park, Y.-I. & Chow, W. S. 1997. Photoinactivation and photoprotection of photosystem II in nature. Physiol. Plant. 100: 214–223.

    Google Scholar 

  3. Bain, J. T. & Proctor, M. C. F. 1980. The requirement of aquatic bryophytes for free CO2 as an inorganic carbon source: some experimental evidence. New Phytol. 86: 393–400.

    Google Scholar 

  4. Beadle, C. L., Ludlow, M. M. & Honeysett, J. L. 1993. Water relations. Pp. 113–128. In: Hall, D. O., Scurlock, J. M. O., Bolhàr-Nordenkampf, H. R., Leegood, R. C. & Long, S. P. (eds), Photosynthesis and production in a changing environment. Chapman & Hall, London.

    Google Scholar 

  5. Bewley, J. D. & Oliver, M. J. 1992. Desiccation tolerance in vegetative plant tissues and seeds: protein synthesis in relation to desiccation and a potential role for protection and repair mechanisms. Pp. 141–160. In: Osmond, C. B. & Somero, G. (eds), Water and life: a comparative analysis of water relationships at the organismic, cellular and molecular levels. Springer-Verlag, Berlin.

    Google Scholar 

  6. Björkman, O. & Demmig-Adams, B. 1995. Regulation of light energy capture, conversion, and dissipation in leaves of higher plants. Pp. 17–47. In: Schulze, E. D. & Caldwell, M. M. (eds), Ecophysiology of photosynthesis. Springer-Verlag, Berlin.

    Google Scholar 

  7. Blockeel, T. L. & Long, D. G. 1998. A check list and census catalogue of British and Irish bryophytes. British Bryological Society, Cardiff.

    Google Scholar 

  8. Brown, D. H. & Buck, G. W. 1979. Desiccation effects and cation distribution in bryophytes. New Phytol. 82: 115–125.

    Google Scholar 

  9. Buch, H. 1945. Ñber die Wasser-und Mineralstoffversorgung der Moose (Part 1). Commentationes Biologici Societas Scientiarum Fennicae 9(16): 1–44.

    Google Scholar 

  10. Buch, H. (1947). Ñber die Wasser-und Mineralstoffversorgung der Moose (Part 2). Commentationes Biologici Societas Scientiarum Fennicae 9(20): 1–61.

    Google Scholar 

  11. Clausen, E. 1952. Hepatics and humidity. A study of the occurrence of hepatics in a Danish tract and the influence of relative humidity on their distribution. Dansk Botanisk Arkiv 15: 1–80.

    Google Scholar 

  12. Clayton-Greene, K. A., Collins, N. J., Green, T. G. A. & Proctor, M. C. F. 1985. Surface wax, structure and function in leaves of Polytrichaceae. J. Bryol. 13: 549–562.

    Google Scholar 

  13. Csintalan, Zs., Proctor, M. C. F. & Tuba, Z. 1999. Chlorophyll fluorescence during drying and rehydration in the mosses Rhytidiadelphus loreus (Hedw.)Warnst., Anomodon viticulosus (Hedw.) Hook & Tayl. and Grimmia pulvinata (Hedw.) Sm. Ann. Bot. 84: 235–244.

    Google Scholar 

  14. Dilks, T. J. K. & Proctor, M. C. F. 1974. The pattern of recovery of bryophytes after desiccation. J. Bryol. 8: 97–115.

    Google Scholar 

  15. Dilks, T. J. K. & Proctor, M. C. F. 1976. Effects of intermittent desiccation on bryophytes. J. Bryol. 9: 249–264.

    Google Scholar 

  16. Dilks, T. J. K. & Proctor, M. C. F. 1979. Photosynthesis, respiration and water content in bryophytes. New Phytol. 82: 97–114.

    Google Scholar 

  17. Eskling, M., Arvidsson, P.-A. & Åkerlund, H.-E. 1997. The xanthophyll cycle, its regulation and components. Physiol. Plant. 100: 806–816.

    Google Scholar 

  18. Gaff, D. F. 1980. Protoplasmic tolerance of extreme water stress. Pp. 207–230. In: Turner, N. C. & Kramer, P. J. (eds), Adaptation of plants to water and high temperature stress. Wiley, New York.

    Google Scholar 

  19. Gilmore, A. M. 1997. Mechanistic aspects of xanthophyll-cycle dependent photoprotection in higher-plant chloroplasts and leaves. Physiol. Plant. 99: 197–209.

    Google Scholar 

  20. Gimingham, C. H. & Birse, E. M. 1957. Ecological studies on growth-form in bryophytes. I. Correlations between growth-form and habitat. J. Ecol. 45: 522–545.

    Google Scholar 

  21. Hanson, A. D. & Hitz, W. D. 1982. Metabolic responses of mesophytes to plant water deficits. Ann. Rev. Plant Physiol. 33: 163–203.

    Google Scholar 

  22. Hébant, C. 1977. The conducting tissues of bryophytes. J. Cramer, Vaduz.

    Google Scholar 

  23. Hinshiri, H. M. & Proctor, M. C. F. 1971. The effect of desiccation on subsequent assimilation and respiration of the bryophytes Anomodon viticulosus and Porella platyphylla. New Phytol. 70: 527–538.

    Google Scholar 

  24. Höfler, K. 1946. Ñber Trockenhärtung und Härtungsgrenzen einiger Lebermoose. Anzeiger der Akademie der Wissenschaften in Wien. Mathematische-naturwissenschaftliche Klasse 1945: 5–8.

    Google Scholar 

  25. Hosokawa, T. & Kubota, H. 1957. On the osmotic pressure and resistance to desiccation of epiphytic mosses from a beech forest, south-west Japan. J. Ecol. 45: 579–591.

    Google Scholar 

  26. Jones, H. G. 1992. Plants and microclimate. 2nd ed. Cambridge University Press, Cambridge.

    Google Scholar 

  27. Kaiser, W. M. 1987. Effects of water deficit on photosynthetic capacity. Physiol. Plant. 71: 142–149.

    Google Scholar 

  28. Koide, R. T., Robichaux, R. H., Morse, S. R. & Smith, C. M. 1989. Plant water status, hydraulic resistance and capacitance. Pp. 161–183. In: Pearcy, R. W., Ehleringer, J., Mooney, H. A. & Rundel, P. W. (eds), Plant physiological ecology. Chapman & Hall, London.

    Google Scholar 

  29. Mägdefrau, K. 1982. Life-forms of bryophytes. Pp. 45–58. In: Smith, A. J. E. (ed.), Bryophyte ecology. Chapman & Hall, London.

    Google Scholar 

  30. Marschall, M. 1998. Nitrate reductase activity during desiccation and rehydration of the desiccation-tolerant moss Tortula ruralis and the leafy liverwort Porella platyphylla. J. Bryol. 20: 273–285.

    Google Scholar 

  31. Marschall, M. & Proctor, M. C. F. 1999. Desiccation tolerance and recovery of the leafy liverwort Porella platyphylla (L.) Pfeiff.: chlorophyll-fluorescence measurements. J. Bryol. 21: 261–267.

    Google Scholar 

  32. Marschall, M., Proctor, M. C. F. & Smirnoff, N. 1998. Carbohydrate composition and invertase activity of the leafy liverwort Porella platyphylla. New Phytol. 138: 343–353.

    Google Scholar 

  33. Moore, C. J., Luff, S. E. & Hallam, N. D. 1982. Fine structure and physiology of the desiccation-tolerant mosses, Barbula torquata Tayl. and Triquetrella papillata (Hook. f. & Wils.) Broth., during desiccation and rehydration. Bot. Gazette 243: 358–367.

    Google Scholar 

  34. Oliver, M. J. 1996. Desiccation-tolerance in vegetative plant cells. Physiol. Plant. 97: 779–787.

    Google Scholar 

  35. Oliver, M. J. & Bewley, J. D. 1984. Desiccation and ultrastructure in bryophytes. Adv. Bryol. 2: 91–131.

    Google Scholar 

  36. Oliver, M. J. & Bewley, J. D. 1997. Desiccation-tolerance of plant tissues: a mechanistic overview. Hort. Rev. 18: 171–213.

    Google Scholar 

  37. Oliver, M. J., Velten, J & Wood, A. J. 2000. Bryophytes as experimental models for the study of environmental stress tolerance: desiccation tolerance in mosses. Plant Ecol. 151(1) in this issue.

  38. Oliver, M. J., Wood, A. J. & O.'Mahony, P. 1998. 'To dryness and beyond' -preparation for the dried state and rehydration in vegetative desiccation-tolerant plants. Plant Growth Regul. 24: 193–201.

    Google Scholar 

  39. Proctor, M. C. F. 1979a. Structure and eco-physiological adaptation in bryophytes. Pp. 479–509. In: Clarke, G. C. S. & Duckett, J. G. (eds), Bryophyte systematics. Systematics Association special volume No. 14. Academic Press, London.

    Google Scholar 

  40. Proctor, M. C. F. 1979b. Surface wax on the leaves of some mosses. J. Bryol. 10: 531–538.

    Google Scholar 

  41. Proctor, M. C. F. 1981a. Diffusion resistances in bryophytes. Pp. 219–229. In: Grace, J., Ford, E. D. & Jarvis, P. G. (eds), Plants and their atmospheric environment. 21st Symposium of the British Ecological Society. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  42. Proctor, M. C. F. 1981b. Physiological ecology of bryophytes. Adv. Bryol. 1: 79–166.

    Google Scholar 

  43. Proctor, M. C. F. 1990. The physiological basis of bryophyte production. Bot. J. Linnean Soc. 104: 61–77.

    Google Scholar 

  44. Proctor, M. C. F. 1999. Water-relations parameters of some bryophytes evaluated by thermocouple psychrometry. J. Bryol. 21: 269–277.

    Google Scholar 

  45. Proctor, M.C.F. & Smirnoff, N. 2000. Rapid recovery of photosystems on re-wetting desiccation-tolerant mosses: chlorophyll-fluorescence and inhibitor experiments. J. Exp. Bot. 51 (in press).

  46. Proctor, M. C. F. & Smith, A. J. E. 1993. Ecological and systematic implications of branching patterns in bryophytes. Pp. 87–110. In: Hoch, P. C. & Stephenson, A. G. (eds), Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St Louis, Mo.

    Google Scholar 

  47. Proctor, M. C. F., Nagy, Z., Csintalan, Zs. & Takács, Z. 1998.Watercontent components in bryophytes: analysis of pressure-volume curves. J. Exp. Bot. 49: 1845–1854.

    Google Scholar 

  48. Proctor, M. C. F., Raven, J. A. & Rice, S. K. 1992. Stable carbon isotope measurements in Sphagnum and other bryophytes: physiological and ecological implications. J. Bryol. 17: 193–202.

    Google Scholar 

  49. Raven, J. A. 1977. The evolution of land plants in relation to supracellular transport processes. Adv. Bot. Res. 5: 152–219.

    Google Scholar 

  50. Raven, J. A. 1984. Physiological correlates of the morphology of early vascular plants. Bot. J. Linnean Soc. 88: 105–126.

    Google Scholar 

  51. Raven, J. A. 1999. The minimum size of seeds and spores in relation to the ontogeny of homoihydric plants. Funct. Ecol. 13: 5–14.

    Google Scholar 

  52. Richards, P. W. 1984. The ecology of tropical forest bryophytes. Pp. 1233–1270. In: Schuster, R. M. (ed.), New manual of bryology. Hattori Botanical Laboratory, Nichinan.

    Google Scholar 

  53. Rundel, P. W., Stichler, W., Zander, R.H. & Ziegler, H. 1979. Carbon and hydrogen isotope ratios of bryophytes from arid and humid regions. Oecologia 4: 91–94.

    Google Scholar 

  54. Schreiber, U., Bilger, W. & Neubauer, C. 1995. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. Pp. 49–70. In: Schulze, E. D. & Caldwell, M. M. (eds), Ecophysiology of photosynthesis. Springer-Verlag, Berlin.

    Google Scholar 

  55. Slavik, B. 1965. The influence of decreasing hydration level on photosynthetic rate in the thalli of the hepatic Conocephalum conicum. Pp. 195–201. In: Slavik, B. (ed.), Water stress in plants. Proceedings of a symposium held in Prague, September 30- October 4, 1963. W. Junk, The Hague.

    Google Scholar 

  56. Smirnoff, N. 1992. The carbohydrates of bryophytes in relation to desiccation tolerance. J. Bryol. 17: 185–191.

    Google Scholar 

  57. Smith, E. C. & Griffiths, H. 1996. The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO2-concentrating mechanism and carbon isotope discrimination in lichens and bryophytes. Planta 198: 6–16.

    Google Scholar 

  58. Smith, E. C. & Griffiths, H. 1997. A pyrenoid-based carbonconcentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae. Planta 200: 203–212.

    Google Scholar 

  59. Tuba, Z., Csintalan, Zs. Badacsonyi, A. & Proctor, M. C. F. 1997. Chlorophyll fluorescence as an exploratory tool for ecophysiological studies on mosses and other small poikilohydric plants. J. Bryol. 19: 401–407.

    Google Scholar 

  60. Tuba, Z., Csintalan, Zs. & Proctor, M. C. F. 1996. Photosynthetic responses of a moss, Tortula ruralis ssp. ruralis, and the lichens Cladonia convoluta and C. furcata to water deficit and short periods of desiccation: a baseline study at present-day CO2 concentration. New Phytol. 133: 353–361.

    Google Scholar 

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Proctor, M.C. The bryophyte paradox: tolerance of desiccation, evasion of drought. Plant Ecology 151, 41–49 (2000). https://doi.org/10.1023/A:1026517920852

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  • Ectohydry
  • Photosynthesis
  • Poikilohydry
  • Protein synthesis
  • Rehydration
  • Water relations