Skip to main content
Log in

Metabolism of activated oxygen in detached wheat and rye leaves and its relevance to the initiation of senescence

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The activities of several enzymes either generating or decomposing O -2 or H2O2, were investigated during the course of senescence of detached wheat (Triticum aestivum L.) and rye (Secale cereale L.) leaves in light and in darkness. Most of the activities, although not in full synchrony, declined with the degradation of chlorophyll and protein. The decline was slower in light than in darkness (e.g. glycolate oxidase, EC 1.1.3.1; urate oxidase, EC 1.7.3.3.; catalase, EC 1.11.1.6) and was further retarded after application of kinetin. The activity of superoxide dismutase (EC 1.15.1.1) declined only very little or, in detached rye leaves, even remained unchanged. For lipoxygenase (EC 1.13.11.12) the decline was enhanced in light and not affected by kinetin. Total peroxidase (EC 1.11.1.7) activity strikingly increased after excision of the leaves. The increase was higher in the dark than in light and further enhanced by kinetin. Activity of l-amino-acid oxidase (EC 1.4.3.2) was not detected. The peroxide content of the detached leaves slowly increased during senescence, being higher in light than in darkness. The malondialdehyde content strongly increased in light, but not in darkness. Application of several chemicals known as scavengers for oxygen radicals (1,4-diazobicyclo(2,2,2)octane, α-tocopherol acetate, p-benzoquinone, d-penicillamine copper, 2-amino-2-(hydroxymethyl)-1,3-propanediol, formate) did not notably retard chlorophyll degradation in senescencing leaves. Thiourea and urate retarded chlorophyll breakdown in light, obviously because they were used as nitrogen sources. Chlorophyll breakdown was greatly accelerated by D2O, particularly in light, presumably by enhancing photooxidative damage. The results indicate that increased peroxide metabolism accompanies the senescence of detached leaves. They do not, however, support the free-radical theory that an accumulation of activated oxygen initiates leaf senescence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ames, B.N., Cathcart, R., Schwiers, E., Hochstein, P. (1981) Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc. Natl. Acad. Sci. USA 78, 6858–6862

    Google Scholar 

  • Birecka, H., Chaskes, M.J., Goldstein, J. (1979) Peroxidase and senescence. J. Exp. Bot. 30, 565–573

    Google Scholar 

  • Birker, P.T.M.W.L., Freeman, H.C. (1977) Structure, properties, and function of a copper(I)-copper(II) complex of d-penicillamine: pentathallium (I) μ8-chloro-dodeca (d-penicillaminato)-octacuprate(I)hexacuprate(II)n-hydrate. J. Am. Chem. Soc. 99, 6890–6899

    Google Scholar 

  • Braber, J.M. (1980) Catalase and peroxidase in primary bean leaves during development and senescence. Z. Pflanzenphysiol. 97, 135–144

    Google Scholar 

  • Brennan, T., Frenkel, C. (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol. 59, 411–416

    Google Scholar 

  • Chance, B., Maehly, A.C. (1955) Assay of catalase and peroxidases. Methods Enzymol. 2, 764–775

    Google 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. Physiol. Plant. 56, 453–457

    Google Scholar 

  • Dhindsa, R.S., Plumb-Dhindsa, P., Thorpe, T.A. (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J. Exp. Bot. 32, 93–101

    Google Scholar 

  • Douillard, R., Bergeron, E. (1981) Lipoxygenase activities of young wheat leaves. Physiol. Plant. 51, 335–338

    Google Scholar 

  • Elstner, E.F. (1982) Oxygen activation and oxygen toxicity. Annu. Rev. Plant Physiol. 33, 73–96

    Google Scholar 

  • Feierabend, J., Beevers, H. (1972) Developmental studies on microbodies in wheat leaves. I. Conditions influencing enzyme development. Plant Physiol. 49, 28–32

    Google Scholar 

  • Feierabend, J., Schrader-Reichhardt, U. (1976) Biochemical differentiation of plastids and other organelles in rye leaves with a high-temperature-induced deficiency of plastid ribosomes. Planta 129, 133–145

    Google Scholar 

  • Feierabend, J., Winkelhüsener, T. (1982) Nature of photooxidative events in leaves treated with chlorosis-inducing herbicides. Plant Physiol. 70, 1277–1282

    Google Scholar 

  • Fridovich, I. (1976) Oxygen radicals, hydrogen peroxide and oxygen toxicity. In: Free radicals in biology, vol. 1, pp. 239–277, Pryor, W.A., ed. Academic Press, New York London

    Google Scholar 

  • Fujimori, E., Livingstone, R. (1957) Interactions of chlorophyll in its triplet state with oxygen, carotene, etc. Nature (London) 180, 1036–1038

    Google Scholar 

  • Galliard, T., Chan, H.W.-S. (1980) Lipoxygenases. In: The biochemistry of plants. A comprehensive treatise, vol. 4: Lipids: structure and function, pp. 131–161, Stumpf, P.K., ed. Academic Press, New York, London

    Google Scholar 

  • Gardner, H.W. (1979) Lipid hydroperoxide reactivity with proteins and amino acids; a review. J. Agric. Food Chem. 27, 220–229

    Google Scholar 

  • Grossman, S., Leshem, Y.Y. (1978) Lowering of endogenous lipoxygenase activity in Pisum sativum foliage by cytokinin as related to senescence. Physiol. Plant. 43, 359–362

    Google Scholar 

  • Grossman, S., Zakut, R. (1978) Determination of the activity of lipoxygenase (lipoxidase). Methods Biochem. Anal. 25, 303–329

    Google Scholar 

  • Halliwell, B. (1978) Biochemical mechanisms accounting for the toxic action of oxygen on living organisms: the key role of superoxide dismutase. Cell. Biol. Int. Rep. 2, 113–128

    Google Scholar 

  • Harman, D. (1981) The aging process. Proc. Natl. Acad. Sci. USA 78, 7124–7128

    Google Scholar 

  • Heath, R.L., Packer, L. (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125, 189–198

    Google Scholar 

  • Kar, M., Mishra, D. (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol. 57, 315–319

    Google Scholar 

  • Krinsky, N.I. (1978) Non-photosynthetic functions of carotenoids. Phil. Trans. R. Soc. Lond. Ser. B 284, 581–590

    Google Scholar 

  • Lengfelder, E., Elstner, E.F. (1978) Determination of the superoxide dismutating activity of d-penicillamine copper. Z. Physiol. Chem. 359, 751–757

    Google Scholar 

  • Leshem, Y.Y. (1981) Oxy free radicals and plant senescence. What's New In Plant Physiol. 12, 1–4

    Google Scholar 

  • Leshem, Y.Y., Grossman, S., Frimer, A., Ziv, J. (1979) Endogenous lipoxygenase control and lipid-associated free radical scavenging as modes of cytokinin action in plant senescence retardation. In: Advances in the biochemistry and physiology of plant lipids. pp. 193–198, Appelqvist, L.-A., Liljenberg, C., eds. Elsevier/North Holland Biomedical Press, Amsterdam

    Google Scholar 

  • Leshem, Y.Y., Wurzburger, J., Grossman, S., Frimer, A.A. (1981) Cytokinin interaction with free radical metabolism and senescence: effects on endogenous lipoxygenase and purine oxidation. Physiol. Plant. 53, 9–12

    Google Scholar 

  • Marshall, M.J., Worsfeld, M. (1978) Superoxide dismutase: a direct, continuous assay using the oxygen electrode. Anal. Biochem. 86, 561–573

    Google Scholar 

  • Martinoia, E., Dalling, M.J., Matile, Ph. (1982) Catabolism of chlorophyll: demonstration of chloroplast-localized peroxidative and oxidative activities. Z. Pflanzenphysiol. 107, 269–279

    Google Scholar 

  • Matile, Ph. (1980) Catabolism of chlorophyll: involvement of peroxidase? Z. Pflanzenphysiol. 99, 475–478

    Google Scholar 

  • Merkel, P.B., Nilsson, R., Kearns, D.R. (1972) Deuterium effects on singlet oxygen lifetimes in solutions. A new test of singlet oxygen reactions. J. Am. Chem. Soc. 94, 1030–1031

    Google Scholar 

  • Mondal, R., Choudhuri, M.A. (1981) Role of hydrogen peroxide in senescence of excised leaves of rice and maize. Biochem. Physiol. Pflanz. 176, 700–709

    Google Scholar 

  • Mondal, R., Choudhuri, M.A. (1982) Regulation of senescence of excised leaves of some C3 and C4 species by endogenous H2O2. Biochem. Physiol. Pflanz 177, 403–417

    Google Scholar 

  • Müller, M., Møller, K.M. (1969) Urate oxidase and its association with peroxisomes in Acanthamoeba sp. Eur. J. Biochem. 9, 424–430

    Google Scholar 

  • Nguyen, J., Feierabend, J. (1978) Some properties and subcellular localization of xanthine dehydrogenase in pea leaves. Plant Sci. Lett. 13, 125–132

    Google Scholar 

  • Parida, R.K., Kar, M., Mishra, D. (1978) Enhancement of senescence in excised rice leaves by hydrogen peroxide. Can. J. Bot. 56, 2937–2941

    Google Scholar 

  • Percival, M.P., Dodge, A.D. (1983) Photodynamic effects of Rose Bengal on senescent flax cotyledons. J. Exp. Bot. 34, 47–54

    Google Scholar 

  • Sarkar, U., Choudhuri, M.A. (1981) Effects of some oxidants and antioxidants on senescence of isolated leaves of sunflower with special reference to glycolate content, glycolate oxidase, and catalase activities. Can. J. Bot. 59, 392–396

    Google Scholar 

  • Thimann, K.V. (1980) The senescence of leaves. In: Senescence in plants, pp. 86–115, Thimann, K.V., ed. CRC Press, Boca Raton, Fla.

    Google Scholar 

  • Thomas, H., Stoddart, J.L. (1980) Leaf senescence. Annu. Rev. Plant Physiol. 31, 83–111

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kar, M., Feierabend, J. Metabolism of activated oxygen in detached wheat and rye leaves and its relevance to the initiation of senescence. Planta 160, 385–391 (1984). https://doi.org/10.1007/BF00429753

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00429753

Key words

Navigation