Hostname: page-component-669899f699-7xsfk Total loading time: 0 Render date: 2025-05-02T10:41:24.510Z Has data issue: false hasContentIssue false
  • English
  • Français

Free radical metabolism, pigment degradation and lipid peroxidation in leaves during senescence

Published online by Cambridge University Press:  05 December 2011

Mark N. Merzlyak  and
G.A.F. Hendry
Mark N. Merzlyak
Affiliation:
Department of Cell Physiology and Immunology, Faculty of Biology, Moscow State University, 119899 GSP Moscow W-234, Russia
G.A.F. Hendry
Affiliation:
NERC Unit of Comparative Plant Ecology, Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK
Get access

Synopsis

Various lines of evidence suggest that the controlled increase in the production of oxygen radicals is an important factor involved in phytohormone metabolism, selective changes in membrane permeability, degradation of photosynthetic pigments and unsaturated membrane lipids, oxidative modification and subsequent proteolytic degradation, and other events occurring in ageing and senescing leaves. Increased lipid peroxidation, appearance of chlorophyll allomerised products, as well as fluorescent ‘lipofuscin-like’ pigments have been documented in different systems of leaf senescence. On the other hand, the accumulation of peroxidised products may result from the alteration to native structural organisation and energy dissipation reactions of the photosynthetic apparatus. Although there are contradictory and incomplete data on the activity of the systems involved in the metabolism of oxygen radicals, it seems that senescing leaves retain, at least in part, their defence potential against both activated oxygen species and toxic lipid peroxidation products. This provides the plant with the ability to successfully dismantle its photosynthetic apparatus during senescence in a relatively safe manner.

Type
Research Article
Information
Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences , Volume 102: Oxygen and Environmental Stress in Plants , 1994 , pp. 459 - 471
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.)

Article purchase

Temporarily unavailable

References

Adams, W. W. III, Winter, K., Schreiber, U. & Schramer, P. 1990. Photosynthesis and chlorophyll fluorescence characteristics in relationships to changes in pigment and elemental composition of leaves of Platanus occidentalis L. during autumn leaf senescence. Plant Physiology 92, 1184–90.Google Scholar
Beevers, L. 1976. Senescence. In Bonner, J. & Varner, J. E. (Eds) Plant biochemistry (3rd edn), pp. 771–94. New York etc.: Academic Press.CrossRefGoogle Scholar
Bousquet, J.-F. & Thimann, K. 1984. Lipid peroxidation forms ethylene from 1-aminocyclopropane-1-carboxylic acid and operates in leaf senescence. Proceedings of the National Academy of Sciences of USA 81, 1724–7.CrossRefGoogle Scholar
Brown, S. B., Houghton, J. D. & Hendry, G. A. F. 1991. Chlorophyll breakdown. In Scheer, H. (Ed.) Chlorophyll, pp. 465–89. Boca Raton: CRC Press.Google Scholar
Chichester, C. O. & Nakayama, T. O. M. 1965. Pigment changes in senescent and stored tissues. In Goodwin, T. W. (Ed.) Chemistry and biochemistry of plant pigments, pp. 440–57. New York, London: Academic Press.Google Scholar
Davies, K. J. A. 1986. Intracellular proteolytic systems may function as a secondary antioxidant defences: an hypothesis. Journal of Free Radicals in Biology and Medicine 2, 155–73.CrossRefGoogle ScholarPubMed
Davies, K. J. A. 1988. Protein oxidation, protein cross-linking, and proteolysis in the formation of lipofuscin: Rationale and methods for the measurement of protein degradation. In Zs.-Nagy, I. (Ed.) Lipofuscin-1987: state of the art, pp. 109–33. Amsterdam, New York, Oxford: Excerpta Medica.Google ScholarPubMed
Dhindsa, R. S., Plumb-Dhindsa, P. L. & Thorpe, T. A. 1981. Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32, 93–101.CrossRefGoogle Scholar
Dhindsa, R. S., Plumb-Dhindsa, P. L. & Reid, D. M. 1982. Leaf senescence and lipid peroxidation: effects of some phytohormones, and scavengers of free radicals and singlet oxygen. Physiologia Plantarum 56, 453–7.CrossRefGoogle Scholar
Duggelin, Th., Gut, H., Matile, Ph. & Thomas, H. 1988. Leaf senescence in Festuca pratensis: Acummulation of lipofuscin-like compounds. Physiologia Plantarum 74, 131–6.CrossRefGoogle Scholar
Dupont, J. 1981. Lipoxygenase-mediated cleavage of fatty acids in plant mitochondria. Physiologia Plantarum 52, 225–32.CrossRefGoogle Scholar
Dupont, J., Rustin, P. & Lance, C. 1984. Effect of lipid peroxide on cytochrome composition during aging of plant mitochondria. In Siegenthaler, P. A. & Eichenberger, W. E. (Eds) Structure function metabolism of plant lipids, pp. 197–200. Amsterdam: Elsevier Science Publisher.Google Scholar
Endo, Y., Usuki, R. & Kaneda, I. 1984. The photooxidative alteration of chlorophylls in methyl linoleate and prooxidant activity of their decomposition products. Agricultural and Biological Chemistry 48, 985–99.Google Scholar
Frey, R. & Tevini, M. 1979. Lipids and lipolitic activities in spinach plastids during seasonal development. In AppeiqvistL,-A. L,-A. & Liljenberg, C. (Eds) Advances in biochemistry and physiology of plant lipids, pp. 225–9. Amsterdam, New York, Oxford: North Holland Biomedical Press.Google Scholar
Galliard, T. 1979. The enzymic degradation of membrane lipids in higher plants. In Appeiqvist, L.-A. & Liljenberg, C. (Eds) Advances in biochemistry and physiology of plant lipids. pp. 121–32. Amsterdam, New York, Oxford: North Holland Biomedical Press.Google Scholar
Halliwell, B. & Gutteridge, J. M. C. 1989. Free radicals in biology and medicine. (2nd edn). Oxford: Claredon Press.Google Scholar
Hancock, J. F., Antonio, T. M., Dalgarn, D. S. & Newman, D. W. 1983. Lipids of senescent leaf tissues induced by inhibition of synthesis and acceleration of breakdown. Ohio Journal of Science 83, 50–4.Google Scholar
Harbour, J. R. & Bolton, J. R. 1978. The involvement of hydroxyl radical in the destructive photooxidation of chlorophylls in vivo and in vitro. Photochemistry and Photobiology 28, 231–4.CrossRefGoogle Scholar
Harman, D. 1986. Free radical theory of aging: Role of free radicals in the origination and evolution of life, aging and disease processes. In Johnson, J. E. Jr, Walford, R., Harmen, D. & Miquel, J. (Eds) Free radicals, aging, and degenerative deseases, modern aging research, pp. 3–50. New York: Alan R. Liss Incorporated.Google Scholar
Harman, D. 1988. Free radical theory of aging: current status. In Zs.-Nagy, I. (Ed.) Lipifuscin-1987: state of the art, pp. 3–21. Amsterdam, New York, Oxford: Excerpta Medica.Google Scholar
Hendry, G. A. F., Houghton, J. D. & Brown, S. B. 1987. The degradation of chlorophyll a biological enigma. New Phytologist 107, 255–302.CrossRefGoogle ScholarPubMed
Hynninen, P. H. 1981. Mechanism of the allomerization of chlorophyll: inhibition of the allomerization by carotenoid pigments. Zeitschrift für Naturforschung 36b, 1010–6.Google Scholar
Kar, M. & Feierabend, J. 1984. Metabolism of activated oxygen in detached wheat and rye leaves and its relevance to the initiation of senescence. Planta 160, 385–91.Google Scholar
Kato, M. & Shimizu, S. 1987. Chlorophyll metabolism in higher plants. VII. Chlorophyll degradation in senescing tobacco leaves: phenolic-dependent peroxidative degradation. Canadian Journal of Botany 65, 729–35.Google Scholar
Krasnovsky, A. A. Jr 1986. Singlet oxygen in photosynthetizing organisms. Mendeleev Journal of the All-Union Chemical Society 31, 562–7.Google Scholar
Krautler, B., Jaun, B., Amrein, W., Bortlik, K., Schellenberg, M. & Matile, P. 1992. Breakdown of chlorophyll: Constitution of a secondary chlorophyll catabolite isolated from senescent barley leaves. Plant Physiology and Biochemistry 30, 333–46.Google Scholar
Kunert, K. J. & Ederer, M. 1985. Leaf aging and lipid peroxidation: the role of the antioxidants vitamin E and C. Physiologia Plantarum 65, 85–8.Google Scholar
Legge, R. L. & Thompson, J. E. 1983. Involvement of hydorperoxides and an ACC-derived free radical in the formation of ethylene. Phytochemistry 22, 2161–6.CrossRefGoogle Scholar
Leshem, Y. Y. 1987. Membrane phospholipid catabolism and Ca2+ activity in control of senescence. Physiologia Plantarum 69, 551–9.CrossRefGoogle Scholar
Leshem, Y. Y., Halevy, A. H. & Frenkel, C. 1986. Processes and control of senescence. New York: Elsevier.Google Scholar
Leshem, Y. Y., Wurzburger, J., Grossman, S. & Frimer, A. A. 1981. Cytokinin interaction with free radical metabolism and senescence: Effects of exogenous lipoxygenase and purine oxidation. Physiologia Plantarum 53, 9–12.CrossRefGoogle Scholar
Zhi-fang, Lin, shun, Li Shung, & Gui-zhu, Lin, 1984. Superoxide dismutase activity and lipid peroxidation in relation to senescence of rice leaves. Acta Botanica Sinensica 26, 605–15.Google Scholar
Lynch, D. V., Sridhara, S. & Thompson, J. E. 1985. Lipoxygenase generated hydroperoxides accounts for non-physiological features of ethylene formation from 1-aminocyclopropane-1-carboxylic acid by microsomal membranes of carnation. Planta 164, 121–5.Google Scholar
Lynch, D. V. & Thompson, J. E. 1984. Lipoxygenase-mediated production of superoxide anion in senescing plant tissue. FEBS Letters 173, 251–4.CrossRefGoogle Scholar
Maunders, M. J., Brown, S. B. & Woolhouse, H. W. 1983. The appearance of chlorophyll derivatives in senescing tissues. Phytochemistry 22, 2443–6.Google Scholar
Maquire, Y. P. & Haard, N. F. 1976. Fluorescent product accumulation in ripening fruit. Nature 258, 599–600.Google Scholar
Matile, P., Duggelin, T., Schellenberg, M., Rentsch, D., Bortlik, K., Peisker, C. & Thomas, H. 1989. How and why is chlorophyll broken down in senescent leaves. Plant Physiology and Biochemistry 27, 595–604.Google Scholar
Matile, Ph., Schellenberg, M. & Peisker, C. 1992. Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187, 230–5.Google Scholar
Mazliak, P. 1983. Plant membrane lipids: changes and alterations during aging and senescence. In Post-harvest physiology and crop preservation pp. 123–40. New York, London: Proceedings of NATO Advance Study Institute.CrossRefGoogle Scholar
McRae, D. G. & Thompson, J. E. 1983. Senescence-dependent changes in superoxide anion production by illuminated chloroplasts from bean leaves. Planta 158, 185–93.Google Scholar
Merzlyak, M. N. 1989. Activated oxygen and oxidative processes in plant cell membranes. Account of Science and Technology, ser. Plant Physiology, vol. 6, Moscow: VINITI.Google Scholar
Merzlyak, M. N. 1991. Syndrome of lipid peroxidation in plants. In Quinn, P. J. & Harwood, J. L. (Eds) Plant lipid biochemistry, structure and utilization, pp. 281–8. London: Portland Press Limited.Google Scholar
Merzlyak, M. N., Hendry, G. A. F., Atherton, N. M., Zhigalova, T. V., Pavlov, V. K. & Zhiteneva, O. V. 1993. Pigment destruction, lipid peroxidation and free radical formation in leaves during autumn senescence. Biokhimiya 58, 240–9.Google Scholar
Merzlyak, M. N. & Kovrizhnikh, V. A. 1984. Chlorophyll allomerization in the systems, containing free radicals, and under illumination of isolated chloroplasts. Studia Biophysica 102, 81–8.Google Scholar
Merzlyak, M. N. & Kovrizhnikh, V. A. 1986. Allomerization of chlorophyll in pea plants treated with diquat and fumigated with sulfur dioxide: possible participation of free - radical reactions in pigment degradation. Journal of Plant Physiology 123, 503–6.CrossRefGoogle Scholar
Merzlyak, M. N., Rumyantseva, V. B., Pogosyan, S. I. & Gusev, M. V. 1981. ‘Aging pigments’ in plant cells: accumulation in detached pea leaves. Dokladv Akademii Nauk USSR 256, 1264–7.Google Scholar
Merzlyak, M. N., Rumyantseva, V. B. & Gusev, M. V. 1982. Accumulation and some properties of liposoluble fluorescent compounds in senescing leaves of Nicotiana sylvestris and in autumn leaves of deciduous plants. Physiologie Vegetale 20, 211–7.Google Scholar
Merzlyak, M. N., Rumyantseva, V. B., Shevyryova, V. V. & Gusev, M. V. 1983. Further investigations of liposoluble fluorescent compounds in senescing plant cells. Journal of Experimental Botany 34, 604–9.Google Scholar
Merzlyak, M. N., Kuprianova, N. S., Kovrizhnikh, V. A. & Afanas'ev, I. B. 1985. The allomerization of chlorophylls a and b with superoxide anion. Journal of Inorganic Biochemistry 24, 239–42.CrossRefGoogle Scholar
Merzlyak, M. N., Kovrizhnikh, V. A. Reshetnikova, I. V. & Gusev, M. V. 1986. Interaction of diphenylpicrylhydrazyl with chloroplast lipids and the antioxidant function of tocopherol and carotenoids in photosynthetic membranes. Photobiochemistry and Photobiophysics 11, 49–55.Google Scholar
Merzlyak, M. N., Kovrizhnikh, V. A. & Timofeev, K. N. 1991. Superoxide mediated chlorophyll allomerization in a dimethyl sulphoxide-water mixture. Free Radical Research Communications 15, 197–201.Google Scholar
Merzlyak, M. N., Pavlov, V. K. & Zhigalova, T. V. 1992a. Effect of dessication on chlorophyll high temperature chemiluminescence in Acer platanoides L. and Aesculus hippocastanum L. leaves. Journal of Plant Physiology 139, 629–31.Google Scholar
Merzlyak, M. N., Zhigalova, T. V. & Shevyryova, V. V. 1992b. Assay of the thiobarbituric acid-reactive products of lipid peroxidation in plants using derivative absorption spectroscopy. Phytochemical Analysis 3, 105–9.Google Scholar
Obukhova, L. K. & Emmanuel, N. M. 1983. Role of free radical oxidative reactions in molecular mechanisms of senescence of living organisms. Uspekhi Sovremennoi Biologii 52, 353–72.Google Scholar
Paliyath, G. & Thompson, J. E. 1987. Calcium- and calmodulin-regulated breakdown of phospholipids by microsomal membranes from bean cotyledons. Plant Physiology 83, 63–8.CrossRefGoogle ScholarPubMed
Paliyath, G., Lynch, D. V. & Thompson, J. E. 1987. Regulation of membrane phospholipids catabolism in senescing carnation flowers. Physiologia Plantarum 71, 503–11.CrossRefGoogle Scholar
Parida, K. K., Kar, M. & Mishra, D. 1978. Enhancement of senescence in excised leaves by hydrogen peroxide. Canadian Journal of Botany 56, 2937–41.Google Scholar
Pauls, K. P. & Thompson, J. E. 1984. Evidence for the accumulation of peroxidized lipids in membranes of senescing cotyledons. Plant Physiology 75, 1152–7.CrossRefGoogle ScholarPubMed
Peiser, G. D. & Yang, S. F. 1978. Chlorophyll destruction in the presence of bisulfite and linoleic acid hydroperoxide. Phytochemistry 12, 79–84.Google Scholar
Peterman, T. K. & Siedow, J. N. 1985. Behavior of lipoxygenase during establishment, senescence, and rejuvenation of soybean cotyledons. Plant Physiology 78, 690–5.Google Scholar
Platt-Aloia, K. A. & Thompson, W. W. 1985. Freeze-fracture evidence of gel-phase lipid in membranes of senescing cowpea cotyledons. Planta 163, 360–9.Google Scholar
Rustin, P., Dupont, J. & Lance, C. 1984. Involvement of lipid peroxy radicals in the cyanide-resistant electron transport pathway. Physiologie Vegetale 22, 643–63.Google Scholar
Schoch, S., Rudiger, W., Luthy, B. & Matile, Ph. 1984. 132-hydroxy-chlorophyll a, the first product of the reaction of chlorophyll oxidase. Journal of Plant Physiology 115, 85–9.Google Scholar
Shimokawa, K., Hashizume, A. & Shioi, Y. 1990. Pyropheophorbide a, a catabolite of ethylene-induced chlorophyll a degradation. Phytochemistry 29, 2105–6.Google Scholar
Shurtz-Swirski, R. & Gepstein, S. 1985. Proteolysis of endogenous substrates in senescing oat leaves. I. Specific degradation of ribulose bisphosphate carboxylase. Plant Physiology 78, 121–5.Google Scholar
Simon, E. W. 1974. Phospholipids and plant membrane permeability. New Phytologist 73, 337–420.CrossRefGoogle Scholar
Spikes, J. D. & Bommer, J. C. 1991. Chlorophyll and related pigments as photosensitizers in biology and medicine. In Scheer, H. (Ed.) Chlorophylls, pp. 1181–204. Boca Raton, Ann Arbor, Boston, London: CRC Press.Google Scholar
Tevini, M. & Steinmuller, D. 1985. Composition and function of plastoglobuli. II. Lipid composition of leaves and plastoglobuli during senescence. Planta 163, 91–6.CrossRefGoogle ScholarPubMed
Thomas, H. 1986. The role of polyunsaturated fatty acids in. Journal of Plant Physiology 123, 97–105.CrossRefGoogle Scholar
Thomas, H. & Stoddart, K. 1980. Leaf senescence. Annual Review of Plant Physiology 31, 83–111.Google Scholar
Thompson, J. E., Pauls, K. P., Chia, L. S. & Sridhara, S. 1983. Free radical-mediated changes in the organization of membrane lipid bilayers: a simulation of senescence. In Thompson, W. W., Mudd, J. B. & Gibbs, M. (Eds) Biosynthesis and function of plant lipids, pp. 173–94. Monograph Ser.: Proceedings of the 6th Annual Symposium in Botany, American Society of Plant Physiology.Google Scholar
Thompson, J. E., Legg, C. S. & Barger, R. F. 1987. The role of free radicals in senescence and wounding. New Phytologist 105, 317–44.Google Scholar
van Hasselt, Ph. R. 1972. Photooxidation of leaf pigments in Cucumis leaf discs during chilling. Acta Botanica Neerlandica 21, 539–48.CrossRefGoogle Scholar
van Hasselt, Ph. R. 1974. Photo-oxidation of unsaturated lipids in Cucumis leaf discs during chilling. Acta Botanica Neerlandica 23, 159–69.Google Scholar
Vogelman, T. C. & Bjorn, L. O. 1986. Plants as light traps. Physiologia Plantarum 68, 704–8.Google Scholar
Wilhelm, J. & Wilhelmova, N. 1981. Accumulation of lipofuscin- like pigments in chloroplasts from senescing leaves of Phaseolus vulgaris. Photosynthetica 15, 55–60.Google Scholar
Young, A. J. 1991. The protective role of carotenoids in higher plants. Phytochemistry 83, 702–8.Google Scholar