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Oxygen, free radical processes and seed longevity

Published online by Cambridge University Press:  19 September 2008

George A. F. Hendry
George A. F. Hendry*
Affiliation:
NERC Unit of Comparative Plant Ecology, Department of Animal and Plant Sciences, The University, Sheffield S10 2TN, UK
*
* Correspondence
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Abstract

The origin and significance of free radicals is described in the broad setting of animal and plant biology and in the specific context of seeds and seed viability. Evidence is given that free radicals play a central if not causal role in promoting molecular damage under the widest range of environmental stresses and induced ageing in mature plant tissuesIn ungerminated seeds, the evidence is less certain. The reason, we argue, is that many attempts to measure free radical processes in seeds are set not against gradients of damage or ageing (as they are in most other biological tissues) but against one of only two options, either seed germinability or mortality. Because free radical reactions differ quantitatively and qualitatively in living and dead tissues attempts to correlate radicalmediated damage with the viability of a population of seeds may be unreliable particularly when measurements are made at uncertain intervals after death. Despite this, the evidence that seeds, uniquely, are exempt from the ravages of oxygen assault is weak. Instead it ismore probable that oxygen plays a central role in seed mortality and may have significance in the evolution of seed persistence.

Keywords

Free radicalslipid peroxidationseed viabilityoxygen
Type
Invited Review
Information
Seed Science Research , Volume 3 , Issue 3 , September 1993 , pp. 141 - 153
Copyright
Copyright © Cambridge University Press 1993

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References

Apostol, I., Heinstein, P.F. and Low, P.S. (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiology 90, 109–116.CrossRefGoogle ScholarPubMed
Babbs, C.F., Pham, J.A. and Coolbaugh, R.C. (1989) Lethal hydroxyl radical production in paraquat treated plants. Plant Physiology 90, 1267–1270.CrossRefGoogle ScholarPubMed
Becana, M. and Klucas, R.V. (1992) Transition metals in legume root nodules: Iron-dependent free radical production increases during nodule senescence. Proceedings of the National Academy of Sciences, USA 89, 8958–8962.CrossRefGoogle ScholarPubMed
Benson, E.E. (1990) Free Radical Damage in Stored Plant Germplasm. International Board for Plant Genetic Resources. Rome.Google Scholar
Benson, E.E., Lynch, P.T. and Jones, J. (1992) The detection of lipid peroxidation products in cryoprotected and frozen rice cells: consequences for post-thaw survival. Plant Science 85, 107–114.CrossRefGoogle Scholar
Berjak, P. and Villiers, T.A. (1972) Ageing in plant embryos. II. Age-induced damage and its repair during early germination. New Phytologist 71, 135–144.CrossRefGoogle Scholar
Berner, R.A. and Canfield, D.E. (1989) A new model for atmospheric oxygen over Phanerozoic time. American Journal of Science 289, 333–361.CrossRefGoogle ScholarPubMed
Berner, R.A. and Landis, G.P. (1988) Gas bubbles in fossil amber as possible indicators of the major gas composition of ancient air. Science 239, 1406–1409.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1985) Seeds: physiology of development and germination. Plenum Press, New York.CrossRefGoogle Scholar
Boveris, A., Putarulo, S.A., Roy, A.H. and Sanchez, R.A. (1984) Spontaneous chemiluminescence of soybean axes during imbibition. Plant Physiology 76, 447–451.CrossRefGoogle ScholarPubMed
Brown, S.B., Houghton, J.D. and Hendry, G.A.F. (1991) Chlorophyll Breakdown, pp 465–489,in Scheer, H. (Ed.) The Chlorophylls. CRC Press, Boca Raton, Florida.Google Scholar
Buchvarov, P. and Gantcheff, T.S. (1984) Influence of accelerated and natural ageing on free radical levels in soybean seeds. Physiologia Plantarum 60, 53–56.CrossRefGoogle Scholar
Cakmak, I. and Horst, W.J. (1991) Effects of aluminium on lipid peroxidation, superoxide dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83, 463–468.CrossRefGoogle Scholar
Cakmak, I. and Marschner, H. (1988) Enhanced superoxide radical production in roots of zinc-deficient plants. Journal of Experimental Botany 39, 1449–1460.CrossRefGoogle Scholar
Cakmak, I. and Marschner, H. (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiology 98, 1222–1227.CrossRefGoogle ScholarPubMed
Chaloner, W.G. (1989) Fossil charcoal as an indicator of palaeoatmospheric oxygen levels. Journal of the Geological Society, London 146, 171–174.CrossRefGoogle Scholar
Chia, L.S., Mayfield, C.I. and Thompson, J.E. (1984) Simulated acid rain induces lipid peroxidation and membrane damage in foliage. Plant Cell and Environment 78, 333–338.CrossRefGoogle Scholar
Commoner, B., Heise, J.J. and Townsend, J. (1956) Light-induced paramagnetism in chloroplasts. Proceedings of the National Academy of Sciences, USA 42, 710–718.CrossRefGoogle ScholarPubMed
Conger, A.D. and Randolph, M.L. (1968) Is age-dependent genetic damage in seeds caused by free radicals? Radiation Botany 8, 193–196.CrossRefGoogle Scholar
Crawford, R.M.M. (1989) Studies in Plant Survival pp 105–106. Blackwell, Oxford.Google Scholar
Cross, A.R. and Jones, O.T.G. (1991) Enzymic mechanisms of superoxide production. Biochimica et Biophysica Acta 1057, 281–298.CrossRefGoogle ScholarPubMed
De Vos, C.H.R., Schat, H., Vooijs, R. and Ernst, W.H.O. (1989) Copper-induced damage to the permeability barrier in roots of Silene cucubalis. Journal of Plant Physiology 135, 164–169.CrossRefGoogle Scholar
Dhindsa, R.S. (1987) Glutathione status and protein synthesis during drought and subsequent rehydration in Tortula ruralis. Plant Physiology 83, 816–819.CrossRefGoogle ScholarPubMed
Droillard, M.J., Bureau, D. and Paulin, A. (1989) Changes in activities of superoxide dismutases during aging of petals of cut carnations (Dianthus caryophyllus). Physiologia Plantarum 76, 149–154.CrossRefGoogle Scholar
Elstner, E.F. (1982) Oxygen activation and oxygen toxicity. Annual Reviews of Plant Physiology 33, 73–96.CrossRefGoogle Scholar
Fielding, J.L. and Goldsworthy, A. (1980) Tocopherol levels and ageing in wheat grains. Annals of Botany 46, 453–456.CrossRefGoogle Scholar
Francis, A. and Coolbear, P. (1988) Changes in fatty acid content of the polar lipid fraction of tomato seeds induced by ageing and/or subsequent low temperature pre-sowing treatment. Seed Science and Technology 16, 87–95.Google Scholar
Fridovich, I. (1983) Superoxide radical: an endogenous toxicant. Annual Reviews of Pharmacology and Toxicology 23, 239–257.CrossRefGoogle ScholarPubMed
Fryer, M.J. (1992) The antioxidant effects of thylakoid vitamin E (alpha-tocopherol). Plant Cell and Environment 15, 381–392.CrossRefGoogle Scholar
Gidrol, X., Serghini, H., Noubhani, A., Mocout, B. and Mazliak, P. (1989) Biochemical changes induced by accelerated aging in sunflower seed. Lipid peroxidation and membrane damage. Physiologia Plantarum 76, 591–597.CrossRefGoogle Scholar
Girard, J. and Le Meste, M. (1992) Absence de relation entre taux de radicaux libres mesuré par RPE viabilité des semences de blé. Comptes Rendus de l'Académie de Sciences, Series 3, Sciences de la Vie 314, 417–422.Google Scholar
Gorecki, R.J. and Harman, G.E. (1987) Effects of antioxidants on viability and vigour of ageing seeds. Seed Science and Technology 15, 109–117.Google Scholar
Gutteridge, J.M.C. and Halliwell, B. (1990) The measurement and mechanism of lipid peroxidation in biological systems. Trends in Biochemical Sciences 15, 129–135.CrossRefGoogle ScholarPubMed
Hailstones, M.D. and Smith, M.T. (1988) Lipid peroxidation in relation to declining vigour in seeds of soya (Glycine max L.) and cabbage (Brassica oleracea L.). Journal of Plant Physiology 133, 425–456.CrossRefGoogle Scholar
Hailstones, M.D. and Smith, M.T. (1991) Soya bean seed invigoration by ferrous sulphate: changes in lipid peroxidation, conductivity, tetrazolium reduction, DNA and protein synthesis. Plant Physiology 137, 307–311.CrossRefGoogle Scholar
Halliwell, B. (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chemistry and Physics of Lipids 44, 327–340.CrossRefGoogle Scholar
Halliwell, B. (1991) Oxygen radicals: their formation in plant tissues and their role in herbicide damage, pp 87–129,in Baker, N. R. and Percival, M. P.(Eds) Herbicides. Elsevier, Amsterdam.Google Scholar
Halliwell, B. and Gutteridge, J.M.C. (1984) Lipid peroxidation, oxygen radicals, cell damage and antioxidant therapy. Lancet June 23rd, 1396–1397.CrossRefGoogle ScholarPubMed
Halliwell, B. and Gutteridge, J.M.C. (1989) Free Radicals in Biology and Medicine. 2nd Edn.Clarendon Press, Oxford.Google Scholar
Harman, D. (1956) Aging: a theory based on free radical and radiation chemistry. Journal of Gerontology 11, 298–313.CrossRefGoogle ScholarPubMed
Harman, D. (1978) Free radical theory of aging: nutritional implications. Age 1, 145–152.CrossRefGoogle Scholar
Harman, G.E. and Mattick, L.R. (1976) Association of lipid oxidation with seed ageing and death. Nature 260, 323–324.CrossRefGoogle Scholar
Harrison, B.J. (1966) Seed deterioration in relation to storage conditions and its influence upon germination, chromosomal damage and plant performance. Journal of the National Institute of Agricultural Botany 10, 644–663.Google Scholar
Hendry, G.A.F. and Brocklebank, K.J. (1985) Iron-induced oxygen radical damage in waterlogged plants. New Phytologist 101, 199–206.CrossRefGoogle ScholarPubMed
Hendry, G.A.F., Houghton, J.D. and Brown, S. (1987) The degradation of chlorophyll—a biological enigma. New Phytologist 107, 255–302.CrossRefGoogle ScholarPubMed
Hendry, G.A.F., Price, A.H. and Brocklebank, K.J. (1990) Role of iron in chlorophyll destruction in stressed plants. Molecular Aspects of Medicine 11, 131–135.Google Scholar
Hendry, G.A.F., Baker, A.J.M. and Ewart, C.F. (1992a) Cadmium tolerance and toxicity; oxygen radical processes and molecular damage in cadmium-tolerant and cadmiumsensitive clones of Holcus lanatus L. Acta Botanica Neerlandica 41, 271–281.CrossRefGoogle Scholar
Hendry, G.A.F., Finch-Savage, W.E., Thorpe, P.C., Atherton, N.M., Buckland, S.M., Nilsson, K.A. and Seel, W. A. (1992b) Free radical processes and loss of seed viability during drying in the recalcitrant species Quercus robur L. New Phytologist 122, 273–279.CrossRefGoogle ScholarPubMed
Hepburn, H.A., Goodman, B.A., McPhail, D.B., Matthews, S. and Powell, A.A. (1986) An evaluation of EPR measurements of the organic free radical content of individual seeds in the non-destructive testing of seed viability. Journal of Experimental Botany 37, 1675–1684.CrossRefGoogle Scholar
Hudson, J.D. (1989) Palaeoatmospheres in the Phanerozoic. Journal of the Geological Society, London 146, 155–160.CrossRefGoogle Scholar
Justice, O.L. and Bass, L.N. (1978) Principles and practice of seed storage. U.S. Department of Agriculture Handbook 506, 57–77.Google Scholar
Knox, J.P. and Dodge, A.D. (1985) Singlet oxygen and plants. Phytochemistry 24, 889–896.CrossRefGoogle Scholar
Landis, G.P. and Snee, L.W. (1991) Ar40/Ar39 systematics and argon diffusion in amber: implications for ancient earth atmospheres. Palaeogeography, Palaeoclimatology, Palaeoecology (Global Change Section) 97, 63–67.CrossRefGoogle Scholar
Leprince, O., Deltour, R., Thorpe, P.C., Atherton, M.N. and Hendry, G.A.F. (1990) The role of free radicals and radical processing systems in loss of desiccation tolerance in germinating maize (Zea mays). New Phytologist 116, 573–580.CrossRefGoogle Scholar
Leprince, O., McKersie, B.D. and Hendry, G.A.F. (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Science Research (in press).CrossRefGoogle Scholar
Lesham, Y.Y. (1988) Plant senescence processes and free radicals. Free Radicals in Biology and Medicine 5, 39–42.CrossRefGoogle Scholar
Lesham, Y.Y. (1992) Plant Membranes: a biophysical approach to structure, development and senescence. Kluwer, Dordrecht.CrossRefGoogle Scholar
Liljenberg, C.S. (1992) The effects of water stress on plant membrane lipids. Progress in Lipid Research 31, 335–344.CrossRefGoogle ScholarPubMed
MacRae, E.A. and Ferguson, I.B. (1985) Changes in catalase activity and hydrogen peroxide concentration in plants in response to low temperatures. Physiologia Plantarum 65, 51–56.CrossRefGoogle Scholar
Marschner, H. and Cakmak, I. (1989) High light and intensity enhances chlorosis and necrosis in leaves of zinc, potassium and magnesium deficient bean (Phaseolus vulgaris) plants. Journal of Plant Physiology 134, 308–315.CrossRefGoogle Scholar
Maunders, M.J. and Brown, S.B. (1983) The effect of light on chlorophyll loss in senescing leaves of sycamore. Planta 158, 309–311.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Cottam, D.A., Lucas, P.W. and Wellburn, A.R. (1987) Induction of ascorbate peroxidase and glutathione reductase activities by interactions of mixtures of air pollutants. Free Radical Research Communications 3, 1–5.CrossRefGoogle ScholarPubMed
Merzlyak, M.N. (1990) Syndrome of lipid peroxidation in plants pp 281–288in Quinn, P. J. and Harwood, J. L. (Eds) Plant lipid biochemistry, structure and utilization. Portland Press, London.Google Scholar
Merzlyak, M.N. and Kovrizhnikh, V.A. (1986) Allomerization of chlorophyll in pea (Pisum sativum) plants treated with diquat and fumigated with SO2. Possible participation of free radical reactions in pigment degradation. Journal of Plant Physiology 123, 503–506.CrossRefGoogle Scholar
Merzylak, M.N., Hendry, G.A.F., Atherton, N.M., Zhigalova, T.V., Pavlov, V.K. and Zhitenva, O.V. (1993) Pigment destruction, lipid peroxidation and free radical formation in leaves during autumn senescence. Biokhimiya 58, 240–249.Google Scholar
Monk, L.S., Fagerstedt, K.V. and Crawford, R.M.M. (1989) Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Physiologia Plantarum 76, 456–459.CrossRefGoogle Scholar
Monk-Talbot, L.S., Davies, H.V., MacCaulay, M. and Forster, B.P. (1991) Superoxide dismutase and susceptibility of potato (Solanum tuberosum L.) tubers to calcium related disorders. Journal of Plant Physiology 137, 499–501.CrossRefGoogle Scholar
Moore, P.D. (1989) Some ecological implications of palaeatmospheric variations. Journal of the Geological Society, London 146, 183–186.CrossRefGoogle Scholar
Muller, J. (1981) Fossil pollen records of extant angiosperms. Botanical Review 47, 1–142.CrossRefGoogle Scholar
Ohlrogge, J.B. and Kernan, T.P. (1982) Oxygen dependent aging of seeds. Plant Physiology 70, 791–796.CrossRefGoogle ScholarPubMed
Osborne, D.J. (1980) Senescence in seeds. pp 13–33in Thimann, K. V.(Ed.) Senescence in Plants. CRC Press, Boca Raton, Florida.Google Scholar
Parrish, D.J. and Leopold, A.C. (1978) On the mechanism of ageing in soybean seeds. Plant Physiology 61, 365–368.CrossRefGoogle ScholarPubMed
Pauls, K.P. and Thompson, J.E. (1984) Evidence for the accumulation of peroxidized lipids in membranes of senescing cotyledons. Plant Physiology 75, 1152–1157.CrossRefGoogle ScholarPubMed
Pearce, D.M.E. and Jackson, M.B. (1991) Comparison of growth responses of barnyard grass (Echinochloa oryzoides) and rice (Oryza sativa) to submergence, ethylene, carbon dioxide and oxygen shortage. Annals of Botany 68, 201–209.CrossRefGoogle Scholar
Pearce, R.S. and Samad, A. (1980) Changes in fatty acid content of the polar lipids during ageing of seeds of peanut (Arachis hypogea), Journal of Experimental Botany 31, 1283–1290.CrossRefGoogle Scholar
Ponquett, R.T., Smith, M.T. and Ross, G. (1992) Lipid autoxidation and seed ageing putative relationships between seed longevity and lipid stability.Seed Science Research 2, 51–54.CrossRefGoogle Scholar
Price, A.H. and Hendry, G.A.F. (1989) Stress and the role of activated oxygen scavengers and protective enzymes in droughted plants. Biochemical Society Transactions 17, 493–494.CrossRefGoogle Scholar
Price, A.H. and Hendry, G.A.F. (1991) Iron-catalysed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell and Environment 14, 477–484.CrossRefGoogle Scholar
Price, A.H., Atherton, N.M. and Hendry, G.A.F. (1989a) Superoxide formation and enhanced transition-metal uptake in drought-damaged wheat leaves, pp 467–479in Rice-Evans, C.(Ed.) Free radicals, diseased states and anti-oxidant interventions. Richlieu Press, London.Google Scholar
Price, A.H., Atherton, N.M. and Hendry, G.A.F. (1989b) Plants under drought-stress generate activated oxygen. Free Radical Research Communications 8, 61–66.CrossRefGoogle ScholarPubMed
Priestley, D.A. and Leopold, A.C. (1979) Absence of lipid oxidation during accelerated aging of soybean seeds. Plant Physiology 63, 726–729.CrossRefGoogle ScholarPubMed
Priestley, D.A., McBride, M.B. and Leopold, A.C. (1980) Tocopherol and organic free radical levels in soybean seeds during natural and accelerated aging. Plant Physiology 66, 715–719.CrossRefGoogle ScholarPubMed
Priestley, D.A., Werner, B.G., Leopold, A.C. and McBride, M.B. (1985) Organic free radical levels in soybean seeds and pollen: the effects of hydration and aging. Physiologia Plantarum 64, 88–94.CrossRefGoogle Scholar
Pukacka, S. (1991) Changes in membrane lipid components and antioxidant levels during natural ageing of seeds of Acer platanoides. Physiologia Plantarum 82, 306–310.CrossRefGoogle Scholar
Quartacci, M.F. and Navari-Izzo, F. (1992) Water stress and free radical mediated changes in sunflower seedlings. Journal of Plant Physiology 139, 621–625.CrossRefGoogle Scholar
Raven, J.A. (1991) Plant responses to high O2 concentrations: relevance to previous high O2 episodes. Palaeogeography, Palaeoclimatology, Palaeoecology (Global Change Section) 97, 19–38.CrossRefGoogle Scholar
Roberts, E.H. and Ellis, R. (1982) Physiological, ultrastructural and metabolic aspects of seed viability, pp 465–483in, Khan, A. A. (Ed.) The physiology and biochemistry of seed development, dormancy and germination. Elsevier, New York.Google Scholar
Robinson, J.M. (1989) Phanerozoic O2 variation, fire and terrestrial ecology. Palaeogeography, Palaeoclimatology, Palaeoecology (Global Change Section) 75, 223–240.CrossRefGoogle Scholar
Robinson, J.M. (1991) Phanerozoic atmospheric reconstructions: a terrestrial perspective. Palaeogeography, Palaeoclimatology, Palaeoecolgy (Global Change Section) 97, 51–56.CrossRefGoogle Scholar
Rudrupal, D. and Nakamura, S. (1988) The effect of hydration—dehydration pretreatments on eggplant and radish seed viability. Seed Science and Technology 16, 123–130.Google Scholar
Rumpho, M.E. and Kennedy, R.A. (1981) Anaerobic metabolism in germinating seeds of Echinochloa crusgalli (barnyard grass): metabolism and enzyme studies. Plant Physiology 68, 165–168.CrossRefGoogle ScholarPubMed
Runeckles, V.C. and Vaartnou, M. (1992) Observations on the in situ detection of free radicals in leaves using electron paramagnetic resonance spectroscopy. Canadian Journal of Botany 70, 192–199.CrossRefGoogle Scholar
Saxena, O.P. (1984) Plant physiological systems as studied by EPR. XI International Conference on Magnetic Resonance in Biological Systems, Abstract P112, London.Google Scholar
Schoner, S. and Krause, G.H. (1990) Protective systems against active oxygen species in spinach: responses to cold acclimation in excess light. Planta 180, 383–389.CrossRefGoogle ScholarPubMed
Seel, W., Hendry, G.A.F., Atherton, N.M. and Lee, J. (1991) Radical formation and accumulation in vivo in desiccation tolerant and intolerant mosses. Free Radical Research Communications 15, 133–141.CrossRefGoogle ScholarPubMed
Seel, W.E., Hendry, G.A.F. and Lee, J.A. (1992) The combined effects of desiccation and irradiance on mosses from xeric and hydrid habitats. Journal of Experimental Botany 43, 1023–1030.CrossRefGoogle Scholar
Senaratna, T., McKersie, B.D. and Stinson, R.H. (1985) Antioxidant levels in germinating soybean seed axes in relation to free radical and dehydration tolerance. Plant Physiology 78, 168–171.CrossRefGoogle ScholarPubMed
Senaratna, T., Gusse, J.F. and McKersie, B.D. (1988) Ageinduced changes in cellular membranes of imbibed soybean seed axes. Physiologia Plantarum 73, 85–91.CrossRefGoogle Scholar
Simola, L.K. (1976) Ultrastructure of non-viable seeds. Zeitschrift fur Pfanzenphysiologie 78, 245–252.CrossRefGoogle Scholar
Smirnoff, N. and Colombe, S.V. (1988) Drought influences the activity of enzymes of the chloroplast hydrogen peroxide scavenging system. Journal of Experimental Botany 39, 1097–1108.CrossRefGoogle Scholar
Sootha, G.D. and Gupta, S.K. (1976) Electron spin resonance study of manganese (II) and free radicals in pulses. Indian Journal of Biochemistry and Biophysics 13, 304–305.Google ScholarPubMed
Stewart, R.R.C. and Bewley, J.D. (1980) Lipid peroxidation associated with accelerated ageing of soybean axes. Plant Physiology 65,245–248.CrossRefGoogle ScholarPubMed
Thompson, J.C., Legge, R.L. and Barber, R.F. (1987) The role of free radicals in senescence and wounding. New Phytologist 105, 317–333.CrossRefGoogle ScholarPubMed
Villiers, T.A. (1973) Ageing and the longevity of seeds. pp 265–268in, Heydecker, W. (Ed.) Seed Ecology. Pennsylvania State University Press, Pennsylvania.Google Scholar
Wilson, D.O. Jr. and McDonald, M.B. Jr. (1986) The lipid peroxidation model of seed ageing. Seed Science and Technology 14, 269–300Google Scholar