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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Oct 29;355(1402):1465–1475. doi: 10.1098/rstb.2000.0707

Peroxide processing in photosynthesis: antioxidant coupling and redox signalling.

G Noctor 1, S Veljovic-Jovanovic 1, C H Foyer 1
PMCID: PMC1692876  PMID: 11128000

Abstract

Photosynthesis has a high capacity for production of hydrogen peroxide (H2O2), but the intracellular levels of this relatively weak oxidant are controlled by the antioxidant system, comprising a network of enzymatic and non-enzymatic components that notably includes reactions linked to the intracellular ascorbate and glutathione pools. Mutants and transformed plants with specific decreases in key components offer the opp ortunity to dissect the complex system that maintains redox homeostasis. Since H2O2 is a signal-transducing molecule relaying information on intracellular redox state, the pool size must be rigorously controlled within each compartment of the cell. This review focuses on compartment-specific differences in the stringency of redox coupling between ascorbate and glutathione, and the significance this may have for the flexibility of the control of gene expression that is linked to photosynthetic H2O2 production.

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Selected References

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  1. Baier M., Dietz K. J. Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol. 1999 Apr;119(4):1407–1414. doi: 10.1104/pp.119.4.1407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baier M., Dietz K. J. The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J. 1997 Jul;12(1):179–190. doi: 10.1046/j.1365-313x.1997.12010179.x. [DOI] [PubMed] [Google Scholar]
  3. Baier M, Dietz KJ. Alkyl hydroperoxide reductases: the way out of the oxidative breakdown of lipids in chloroplasts. Trends Plant Sci. 1999 May;4(5):166–168. doi: 10.1016/s1360-1385(99)01398-9. [DOI] [PubMed] [Google Scholar]
  4. Bartling D., Radzio R., Steiner U., Weiler E. W. A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. Eur J Biochem. 1993 Sep 1;216(2):579–586. doi: 10.1111/j.1432-1033.1993.tb18177.x. [DOI] [PubMed] [Google Scholar]
  5. Bartoli C. G., Pastori G. M., Foyer C. H. Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol. 2000 May;123(1):335–344. doi: 10.1104/pp.123.1.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brisson L. F., Zelitch I., Havir E. A. Manipulation of catalase levels produces altered photosynthesis in transgenic tobacco plants. Plant Physiol. 1998 Jan;116(1):259–269. doi: 10.1104/pp.116.1.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bunkelmann J. R., Trelease R. N. Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiol. 1996 Feb;110(2):589–598. doi: 10.1104/pp.110.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Conklin P. L., Norris S. R., Wheeler G. L., Williams E. H., Smirnoff N., Last R. L. Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4198–4203. doi: 10.1073/pnas.96.7.4198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Conklin P. L., Pallanca J. E., Last R. L., Smirnoff N. L-ascorbic acid metabolism in the ascorbate-deficient arabidopsis mutant vtc1. Plant Physiol. 1997 Nov;115(3):1277–1285. doi: 10.1104/pp.115.3.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Conklin P. L., Williams E. H., Last R. L. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9970–9974. doi: 10.1073/pnas.93.18.9970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dron M., Clouse S. D., Dixon R. A., Lawton M. A., Lamb C. J. Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6738–6742. doi: 10.1073/pnas.85.18.6738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Foyer C. H., Mullineaux P. M. The presence of dehydroascorbate and dehydroascorbate reductase in plant tissues. FEBS Lett. 1998 Apr 3;425(3):528–529. doi: 10.1016/s0014-5793(98)00281-6. [DOI] [PubMed] [Google Scholar]
  13. Grace S. C., Logan B. A. Acclimation of Foliar Antioxidant Systems to Growth Irradiance in Three Broad-Leaved Evergreen Species. Plant Physiol. 1996 Dec;112(4):1631–1640. doi: 10.1104/pp.112.4.1631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Groden D., Beck E. H2O2 destruction by ascorbate-dependent systems from chloroplasts. Biochim Biophys Acta. 1979 Jun 5;546(3):426–435. doi: 10.1016/0005-2728(79)90078-1. [DOI] [PubMed] [Google Scholar]
  15. Hertwig B., Streb P., Feierabend J. Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions. Plant Physiol. 1992 Nov;100(3):1547–1553. doi: 10.1104/pp.100.3.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heupel R., Heldt H. W. Protein organization in the matrix of leaf peroxisomes. A multi-enzyme complex involved in photorespiratory metabolism. Eur J Biochem. 1994 Feb 15;220(1):165–172. doi: 10.1111/j.1432-1033.1994.tb18611.x. [DOI] [PubMed] [Google Scholar]
  17. Hérouart D., Van Montagu M., Inzé D. Redox-activated expression of the cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3108–3112. doi: 10.1073/pnas.90.7.3108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jimenez A., Hernandez J. A., Del Rio L. A., Sevilla F. Evidence for the Presence of the Ascorbate-Glutathione Cycle in Mitochondria and Peroxisomes of Pea Leaves. Plant Physiol. 1997 May;114(1):275–284. doi: 10.1104/pp.114.1.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Karpinski S., Escobar C., Karpinska B., Creissen G., Mullineaux P. M. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell. 1997 Apr;9(4):627–640. doi: 10.1105/tpc.9.4.627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kingston-Smith A. H., Foyer C. H. Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures. J Exp Bot. 2000 Jan;51(342):123–130. [PubMed] [Google Scholar]
  21. Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
  22. Meister A. Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem. 1994 Apr 1;269(13):9397–9400. [PubMed] [Google Scholar]
  23. Mittler R., Zilinskas B. A. Purification and characterization of pea cytosolic ascorbate peroxidase. Plant Physiol. 1991 Nov;97(3):962–968. doi: 10.1104/pp.97.3.962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mullineaux P. M., Karpinski S., Jiménez A., Cleary S. P., Robinson C., Creissen G. P. Identification of cDNAS encoding plastid-targeted glutathione peroxidase. Plant J. 1998 Feb;13(3):375–379. doi: 10.1046/j.1365-313x.1998.00052.x. [DOI] [PubMed] [Google Scholar]
  25. Ninomiya Y., Urano Y., Yoshimoto K., Iwahana H., Sasaki S., Arase S., Itakura M. p53 gene mutation analysis in porokeratosis and porokeratosis-associated squamous cell carcinoma. J Dermatol Sci. 1997 Mar;14(3):173–178. doi: 10.1016/s0923-1811(96)00569-5. [DOI] [PubMed] [Google Scholar]
  26. Noctor Graham, Foyer Christine H. ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):249–279. doi: 10.1146/annurev.arplant.49.1.249. [DOI] [PubMed] [Google Scholar]
  27. Takahashi H., Chen Z., Du H., Liu Y., Klessig D. F. Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant J. 1997 May;11(5):993–1005. doi: 10.1046/j.1365-313x.1997.11050993.x. [DOI] [PubMed] [Google Scholar]
  28. Trümper S., Follmann H., Häberlein I. A novel-dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Lett. 1994 Sep 26;352(2):159–162. doi: 10.1016/0014-5793(94)00947-3. [DOI] [PubMed] [Google Scholar]
  29. Vanacker H, Carver TL, Foyer CH. Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves . Plant Physiol. 1998 Jul;117(3):1103–1114. doi: 10.1104/pp.117.3.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wheeler G. L., Jones M. A., Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature. 1998 May 28;393(6683):365–369. doi: 10.1038/30728. [DOI] [PubMed] [Google Scholar]
  31. Willekens H., Chamnongpol S., Davey M., Schraudner M., Langebartels C., Van Montagu M., Inzé D., Van Camp W. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 1997 Aug 15;16(16):4806–4816. doi: 10.1093/emboj/16.16.4806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wingate V. P., Lawton M. A., Lamb C. J. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 1988 May;87(1):206–210. doi: 10.1104/pp.87.1.206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Winkler B. S. Unequivocal evidence in support of the nonenzymatic redox coupling between glutathione/glutathione disulfide and ascorbic acid/dehydroascorbic acid. Biochim Biophys Acta. 1992 Oct 27;1117(3):287–290. doi: 10.1016/0304-4165(92)90026-q. [DOI] [PubMed] [Google Scholar]
  34. Yamaguchi K., Mori H., Nishimura M. A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol. 1995 Sep;36(6):1157–1162. doi: 10.1093/oxfordjournals.pcp.a078862. [DOI] [PubMed] [Google Scholar]
  35. Yoshimura K., Ishikawa T., Nakamura Y., Tamoi M., Takeda T., Tada T., Nishimura K., Shigeoka S. Comparative study on recombinant chloroplastic and cytosolic ascorbate peroxidase isozymes of spinach. Arch Biochem Biophys. 1998 May 1;353(1):55–63. doi: 10.1006/abbi.1997.0612. [DOI] [PubMed] [Google Scholar]
  36. Zhang H., Wang J., Nickel U., Allen R. D., Goodman H. M. Cloning and expression of an Arabidopsis gene encoding a putative peroxisomal ascorbate peroxidase. Plant Mol Biol. 1997 Aug;34(6):967–971. doi: 10.1023/a:1005814109732. [DOI] [PubMed] [Google Scholar]

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