Hostname: page-component-5c6d5d7d68-sv6ng Total loading time: 0 Render date: 2024-08-21T05:20:03.350Z Has data issue: false hasContentIssue false

Enzymatic defence against post-anoxic injury in higher plants

Published online by Cambridge University Press:  05 December 2011

B. Wollenweber-Ratzer
Affiliation:
Plant Sciences Laboratories, Sir Harold Mitchell Building, St Andrews University, St Andrews, Fife KYI6 9AL, UK
R. M. M. Crawford*
Affiliation:
Plant Sciences Laboratories, Sir Harold Mitchell Building, St Andrews University, St Andrews, Fife KYI6 9AL, UK
*
**Corresponding author
Get access

Synopsis

Plants tolerant of long-term flooding and oxygen deprivation in their perennating organs such as rhizomes and tubers are able to avoid the deleterious effects of anoxia and minimise the dangers of re-entry to air by reactions with antioxidants such as ascorbic acid and glutathione. In processes of detoxification of oxygen radicals, ascorbic acid is oxidised to dehydroascorbic acid and reduced glutathione to oxidised glutathione. Through the action of enzymes such as monodehydroascorbate reductase (MR) and dehydroascorbate reductase (DHAR), glutathione and ascorbic acid may be regenerated to maintain sufficient levels of antioxidants within the tissue in order to quench oxygen radicals.

Type
Research Article
Copyright
Copyright © Royal Society of Edinburgh 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

*Now at: The Royal Veterinary and Agricultural University, Department of Agricultural Sciences, Thorvaldsensvej 40, DK 1871 Frederiksberg C, Copenhagen, Denmark.

References

Akerboom, T. P. M. & Sies, H. 1981. Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods in Enzymology 11, 373–82.Google Scholar
Alscher, R. G. 1989. Biosynthesis and antioxidant functions of glutathione in plants. Physiologia Plantarum 77, 457–64.Google Scholar
Aono, M., Kubo, A., Saji, H., Natori, T., Tanaka, K. & Kondo, N. 1991. Resistance to active oxygen toxicity of transgenic Nicotiana tabacum that express the gene for glutathione reductase from Escherkhia coli. Plant and Cell Physiology 32, 691–7.Google Scholar
Arrigoni, O., Dipierro, S. & Borraccino, G. 1981. Ascorbate free radical reductase, a key enzyme of the asorobic acid system. FEBS Letters 125, 242–4.Google Scholar
Bielski, B. H. J. 1982. Chemistry of asocrbic acid radicals. In Seib, P. A. & Tolbert, B. M. (eds) Advances in chemistry, No. 200, Ascorbic acid: chemistry, metabolism, anduses pp. 81100. New York: American Chemical Society.Google Scholar
Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–54.CrossRefGoogle ScholarPubMed
Braendle, R. & Crawford, R. M. M. 1987. Rhizome anoxia tolerance and habitat specialization in wetland plants. In Crawford, R. M. M. (Eds) Plant life in aquatic and amphibous habitats pp. 397410. London: Blackwell Science Publications.Google Scholar
Chen, Y., Lucas, P. W. & Wellburn, A. R. 1991. Relationship between foliar injury and changes in antioxidant levels in red and Norway spruce exposed to acidic mist. Environmental Pollution 69, 115.CrossRefGoogle Scholar
Chinoy, J. J. 1984. The role of ascorbic acid in growth, differentiation and metabolism of plants. The Hague: Martinus Nijhoff Publishers.CrossRefGoogle Scholar
Crawford, R. M. M. 1992. Oxygen availability as an ecological limit to plant distribution. Advances in Ecological Research 23, 93185.CrossRefGoogle Scholar
Crawford, R. M. M. & Wollenweber-Ratzer, B. 1992. Influence of L-ascorbic acid on post-anoxic growth and survival of chickpea seedlings (Cicer arienetum L.). Journal of Experimental Botany 43, 703–8.Google Scholar
Crawford, R. M. M., Lindsay, D. A., Walton, J. C., & Wollenweber-Ratzer, B. 1994. Towards the characterisation of radicals formed in rhizomes of Iris germanica L. Phytochemistry (in press),CrossRefGoogle Scholar
Crawford, R. M. M., Walton, J. C. & Wollenweber-Ratzer, B. 1994. Similarities between post-ischaemic injury to annual tissues and post-anoxic injury to plants. Proceedings of the Royal Society of Edinburgh 102B, 325–32.Google Scholar
Dipierro, S. & Borraccino, G. 1991. Dehydroascorbate reductase from potato tubers. Phytochemistry 30, 427–9.CrossRefGoogle Scholar
Elstner, E. F., Wagner, G. A. & Schütz, W. 1988. Activated oxygen in green plants in relation to stress situations. Current Topics in Plant Biochemistry and Physiology 7, 159–87.Google Scholar
Esterbauer, H. & Grill, D. 1978. Seasonal variation of glutathione and glutathione reductase in needles of Picea abies. Plant Physiology 61, 119121.Google Scholar
Foyer, C. H. & Halliwell, B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta 133, 21–5.Google Scholar
Foyer, C., Rowell, J. & Walker, D. 1983. Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157, 239–44.Google Scholar
Fridovich, I. 1976. Oxygen radicals, hydrogen peroxide, and oxygen toxicity. In Pryor, W. A. (Ed.) Free radicals in biology pp. 239–77. London: Academic Press.Google Scholar
Fridovich, I. 1988. The biology of oxygen radicals: general concept. In Halliwell, B. (Ed.) Oxygen radicals and tissue injury. Proceedings of a Brook Lodge Symposium, Aupusta, Michigan, pp. 15. New York: Proc. Upjohn Symp.Google Scholar
Griffith, O. W. 1980. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vilylpyridine. Analytical Biochemistry 106, 207–12.CrossRefGoogle Scholar
Gutteridge, J. M. C. 1988. Lipid peroxidation: Some problems and concepts. In Halliwell, B. (Ed.) Oxygen radicals and tissue injury. Proceedings of a Brook Lodge Symposium, Augusta, Michigan. pp. 919. New York: Proc. Upjohn Symp.Google Scholar
Halliwell, B. 1974. Superoxide dismutase, catalase and glutathione peroxidase: solutions to the problems of living with oxygen. New Phytologist 73, 1075–86.CrossRefGoogle Scholar
Halliwell, B. & Gutteridge, M. C. 1984. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochemical Journal 219, 114.Google Scholar
Hetherington, A. M., Hunter, M. I. S. & Crawford, R. M. M. 1982. Contrasting effects of anoxia on rhizome lipids in Iris species. Phytochemistry 21, 1275–8.CrossRefGoogle Scholar
Hippeli, S. & Elstner, E. 1991. Oxygen radicals and air pollution. In Sies, H. (Ed.) Oxidative stress: oxidants and antioxidants pp. 155. London: Academic Press.Google Scholar
Hook, D. D. 1984. Adaptations to flooding with fresh water. In Kozlowski, T. T. (Ed.) Flooding and plant growth (Ed. by T. T. Kozlowski, pp. 265–94. London: Academic Press.Google Scholar
Hossain, M. A. & Asada, K. 1984. Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme. Plant and Cell Physiology 25, 8592.Google Scholar
Hossain, M. A., Nakano, Y. & Asada, K. 1984. Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant and Cell Physiology 25, 385–95.Google Scholar
Jackson, M. B. & Drew, M. C. 1984. Effects of flooding on growth and metabolism of herbaceous plants, pp. 47128. London: Academic Press.Google Scholar
Jahnke, L. S., Hull, M. R. & Long, S. P. 1991. Chilling stress and oxygen metabolizing enzymes in Zea mays and Zea diploperennis. Plant, Cell and Environment 14, 97104.CrossRefGoogle Scholar
Klaphek, S. & Rennenberg, H. 1990. Sulphur Metabolism E. Synthesis of glutathione. In Lea, P. J. (Ed.) Methods in plant biochemistry, vol. 3, Enzymes of primary metabolism, pp. 335–59. London: Academic Press.Google Scholar
Klapheck, S., Zimmer, I. & Cosse, H. 1990. Scavenging of hydrogen peroxide in the endosperm of Ricinus communis by ascorbate peroxidase. Plant and Cell Physiology 31, 1005–13.Google Scholar
Krause, G. H. 1988. Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Plant Physiology 74, 566–74.CrossRefGoogle Scholar
Laan, P., Smolders, A. & Blom, C. W. P. M. 1991. The relative importance of anaerobiosis and high iron levels in the flood tolerance of Rumex species. Plant and Soil 136, 153–61.Google Scholar
Larson, R. A. 1988. The antioxidants of higher plants. Phytochemistry 27, 969–78.Google Scholar
Leprince, O., Deltour, R., Thorpe, P. C., Atherton, N. M. & Hendry, G. A. F. 1990. The role of free radicals and radical processing system in loss of desiccation tolerance in germinating maize. New Phytologist 116, 573–80.Google Scholar
Luwe, M. W. F., Takahama, U. & Heber, U. 1993. Role of Ascorbate in detoxifying ozone in the apoplast of Spinach (Spinacea oleracea L.) leaves. Plant Physiology 101, 969–76.Google Scholar
Mehlhorn, H. & Kunert, K. J. 1986. Ascorbic acid, phenolic compounds, and plant peroxidases: a natural defence against peroxidative stress in higher plants? In Greppin, H., Penel, C. & Gaspar, T. (Eds.) Molecular and physiological aspects of plant peroxidases pp. 437–40. Geneva: University Geneva Press.Google Scholar
Mehlhorn, H., O'Shea, J. M. & Wellburn, A. R. 1991. Atmospheric ozone interacts with stress ethylene formation by plants to cause visible plant injury. Journal of Experimental Botany 42, 1724.Google Scholar
Mishra, N. P., Mishra, R. K. & Singhal, G. S. 1993. Changes in the activities of anti-oxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiology 102, 903–10.CrossRefGoogle ScholarPubMed
Monk, L. S., Fagerstedt, K. V. & Crawford, R. M. M. 1989. Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Physiologia Plantarum 76, 456–9.CrossRefGoogle Scholar
Nakano, Y. & Asada, K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867–80.Google Scholar
Polle, A. & Rennenberg, H. 1991. Superoxide dismutase activity in needles of Scots pine and Norway spruce under field and chamber conditions: lack of ozone effects. New Phytologist 117, 335–43.Google Scholar
Salin, M. L. 1988. Plant superoxide dismutases: A means of coping with oxygen radicals. Current Topics in Plant Biochemistry and Physiology 7, 188200.Google Scholar
Schmidt, A. & Kunert, K. J. 1986. Lipid peroxidation in higher plants. The role of glutathione reductase. Plant Physiology 82, 700–2.Google Scholar
Sieber, M. & Brändle, R. 1991. Energy metabolism in rhizomes of Acorus calamus (L.) and in tubers of Solanum tuberosum (L.) with regard to their anoxia tolerance. Botanica Acta 104, 279–82.CrossRefGoogle Scholar
Smith, G. S., Buwalda, J. G., Green, T. G. A. & Clark, C. J. 1989. Effect of oxygen supply and temperature at the root on the physiology of kiwifruit vines. New Phytologist 113, 431–7.CrossRefGoogle Scholar
Takahama, U., Egashira, T. & Wakamatsu, K. 1989. Hydrogen peroxide-dependent synthesis of flavonols in mesophyll cells of Vicia faba L. Plant and Cell Physiology 30, 951–5.Google Scholar
Thompson, J. E.. Legge, R. L. & Barber, R. F. 1987. The role of free radicals in senescence and wounding. New Phytologist 105, 317–44.CrossRefGoogle ScholarPubMed
Wingsle, G. & Haellgren, J.-E. 1993. Influence of SO2 and NO2 exposure on gluthatione, superoxide dismutase and gluthatione reductase activities in Scots pine needles. Journal of Experimental Botany 44, 463–70.CrossRefGoogle Scholar
Wise, R. R. & Naylor, A. W. 1987. Chilling-enhanced photoautoxidation. Evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiology 83, 278–82.Google Scholar