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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):1419–1431. doi: 10.1098/rstb.2000.0703

The water-water cycle as alternative photon and electron sinks.

K Asada 1
PMCID: PMC1692883  PMID: 11127996

Abstract

The water-water cycle in chloroplasts is the photoreduction of dioxygen to water in photosystem I (PS I) by the electrons generated in photosystem II (PS II) from water. In the water-water cycle, the rate of photoreduction of dioxygen in PS I is several orders of magnitude lower than those of the disproportionation of superoxide catalysed by superoxide dismutase, the reduction of hydrogen peroxide to water catalysed by ascorbate peroxidase, and the reduction of the resulting oxidized forms of ascorbate by reduced ferredoxin or catalysed by either dehydroascorbate reductase or monodehydroascorbate reductase. The water-water cycle therefore effectively shortens the lifetimes of photoproduced superoxide and hydrogen peroxide to suppress the production of hydroxyl radicals, their interactions with the target molecules in chloroplasts, and resulting photoinhibition. When leaves are exposed to photon intensities of sunlight in excess of that required to support the fixation of CO2, the intersystem electron carriers are over-reduced, resulting in photoinhibition. Under such conditions, the water-water cycle not only scavenges active oxygens, but also safely dissipates excess photon energy and electrons, in addition to downregulation of PS II and photorespiration. The dual functions of the water-water cycle for protection from photoinhibition under photon excess stress are discussed, along with its functional evolution.

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Selected References

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  1. Asada K., Urano M., Takahashi M. Subcellular location of superoxide dismutase in spinach leaves and preparation and properties of crystalline spinach superoxide dismutase. Eur J Biochem. 1973 Jul 2;36(1):257–266. doi: 10.1111/j.1432-1033.1973.tb02908.x. [DOI] [PubMed] [Google Scholar]
  2. Asada Kozi. THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons. Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50(NaN):601–639. doi: 10.1146/annurev.arplant.50.1.601. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Behrens P. W., Marsho T. V., Radmer R. J. Photosynthetic o(2) exchange kinetics in isolated soybean cells. Plant Physiol. 1982 Jul;70(1):179–185. doi: 10.1104/pp.70.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Biehler K., Fock H. Evidence for the Contribution of the Mehler-Peroxidase Reaction in Dissipating Excess Electrons in Drought-Stressed Wheat. Plant Physiol. 1996 Sep;112(1):265–272. doi: 10.1104/pp.112.1.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bokemeyer C., Nowak P., Haupt A., Metzner B., Köhne H., Hartmann J. T., Kanz L., Schmoll H. J. Treatment of brain metastases in patients with testicular cancer. J Clin Oncol. 1997 Apr;15(4):1449–1454. doi: 10.1200/JCO.1997.15.4.1449. [DOI] [PubMed] [Google Scholar]
  7. Brechignac F., Andre M. Oxygen Uptake and Photosynthesis of the Red Macroalga, Chondrus crispus, in Seawater: Effects of Oxygen Concentration. Plant Physiol. 1985 Jul;78(3):545–550. doi: 10.1104/pp.78.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Canvin D. T., Berry J. A., Badger M. R., Fock H., Osmond C. B. Oxygen exchange in leaves in the light. Plant Physiol. 1980 Aug;66(2):302–307. doi: 10.1104/pp.66.2.302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen G. X., Blubaugh D. J., Homann P. H., Golbeck J. H., Cheniae G. M. Superoxide contributes to the rapid inactivation of specific secondary donors of the photosystem II reaction center during photodamage of manganese-depleted photosystem II membranes. Biochemistry. 1995 Feb 21;34(7):2317–2332. doi: 10.1021/bi00007a028. [DOI] [PubMed] [Google Scholar]
  10. Farrington J. A., Ebert M., Land E. J., Fletcher K. Bipyridylium quaternary salts and related compounds. V. Pulse radiolysis studies of the reaction of paraquat radical with oxygen. Implications for the mode of action of bipyridyl herbicides. Biochim Biophys Acta. 1973 Sep 26;314(3):372–381. doi: 10.1016/0005-2728(73)90121-7. [DOI] [PubMed] [Google Scholar]
  11. Flexas J, Badger M, Chow WS, Medrano H, Osmond CB. Analysis of the relative increase in photosynthetic O(2) uptake when photosynthesis in grapevine leaves is inhibited following low night temperatures and/or water stress. Plant Physiol. 1999 Oct;121(2):675–684. doi: 10.1104/pp.121.2.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR. Relationship between CO2 Assimilation, Photosynthetic Electron Transport, and Active O2 Metabolism in Leaves of Maize in the Field during Periods of Low Temperature. Plant Physiol. 1998 Feb 1;116(2):571–580. doi: 10.1104/pp.116.2.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Hideg E., Kálai T., Hideg K., Vass I. Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry. 1998 Aug 18;37(33):11405–11411. doi: 10.1021/bi972890+. [DOI] [PubMed] [Google Scholar]
  15. Ishikawa T., Yoshimura K., Tamoi M., Takeda T., Shigeoka S. Alternative mRNA splicing of 3'-terminal exons generates ascorbate peroxidase isoenzymes in spinach (Spinacia oleracea) chloroplasts. Biochem J. 1997 Dec 15;328(Pt 3):795–800. doi: 10.1042/bj3280795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jablonski P. P., Anderson J. W. Light-dependent reduction of dehydroascorbate by ruptured pea chloroplasts. Plant Physiol. 1981 Jun;67(6):1239–1244. doi: 10.1104/pp.67.6.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kaiser W. The effect of hydrogen peroxide on CO2 fixation of isolated intact chloroplasts. Biochim Biophys Acta. 1976 Sep 13;440(3):476–482. doi: 10.1016/0005-2728(76)90035-9. [DOI] [PubMed] [Google Scholar]
  18. Kanematsu S., Asada K. Crystalline ferric superoxide dismutase from an anaerobic green sulfur bacterium, Chlorobium thiosulfatophilum. FEBS Lett. 1978 Jul 1;91(1):94–98. doi: 10.1016/0014-5793(78)80025-8. [DOI] [PubMed] [Google Scholar]
  19. Kanematsu S., Asada K. Superoxide dismutase from an anaerobic photosynthetic bacterium, Chromatium vinosum. Arch Biochem Biophys. 1978 Jan 30;185(2):473–482. doi: 10.1016/0003-9861(78)90191-1. [DOI] [PubMed] [Google Scholar]
  20. Kobayashi K., Tagawa S., Sano S., Asada K. A direct demonstration of the catalytic action of monodehydroascorbate reductase by pulse radiolysis. J Biol Chem. 1995 Nov 17;270(46):27551–27554. doi: 10.1074/jbc.270.46.27551. [DOI] [PubMed] [Google Scholar]
  21. Laisk A., Loreto F. Determining Photosynthetic Parameters from Leaf CO2 Exchange and Chlorophyll Fluorescence (Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Specificity Factor, Dark Respiration in the Light, Excitation Distribution between Photosystems, Alternative Electron Transport Rate, and Mesophyll Diffusion Resistance. Plant Physiol. 1996 Mar;110(3):903–912. doi: 10.1104/pp.110.3.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MARRE E., ARRIGONI O. Ascorbic acid and photosynthesis. I. Monodehydroascorbic acid reductase of chloroplasts. Biochim Biophys Acta. 1958 Dec;30(3):453–457. doi: 10.1016/0006-3002(58)90089-1. [DOI] [PubMed] [Google Scholar]
  23. MEHLER A. H. Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys. 1951 Aug;33(1):65–77. doi: 10.1016/0003-9861(51)90082-3. [DOI] [PubMed] [Google Scholar]
  24. Miller A. G., Hunter K. J., O'Leary S. J., Hart L. J. The photoreduction of H(2)O(2) by Synechococcus sp. PCC 7942 and UTEX 625. Plant Physiol. 2000 Jun;123(2):625–636. doi: 10.1104/pp.123.2.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mir N. A., Salon C., Canvin D. T. Inorganic Carbon-Stimulated O2 Photoreduction Is Suppressed by NO2- Assimilation in Air-Grown Cells of Synechococcus UTEX 625. Plant Physiol. 1995 Dec;109(4):1295–1300. doi: 10.1104/pp.109.4.1295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miyagawa Y., Tamoi M., Shigeoka S. Evaluation of the defense system in chloroplasts to photooxidative stress caused by paraquat using transgenic tobacco plants expressing catalase from Escherichia coli. Plant Cell Physiol. 2000 Mar;41(3):311–320. doi: 10.1093/pcp/41.3.311. [DOI] [PubMed] [Google Scholar]
  27. Miyake C., Yokota A. Determination of the rate of photoreduction of O2 in the water-water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesis. Plant Cell Physiol. 2000 Mar;41(3):335–343. doi: 10.1093/pcp/41.3.335. [DOI] [PubMed] [Google Scholar]
  28. Mutsuda M., Ishikawa T., Takeda T., Shigeoka S. The catalase-peroxidase of Synechococcus PCC 7942: purification, nucleotide sequence analysis and expression in Escherichia coli. Biochem J. 1996 May 15;316(Pt 1):251–257. doi: 10.1042/bj3160251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Palatnik J. F., Valle E. M., Carrillo N. Oxidative stress causes ferredoxin-NADP+ reductase solubilization from the thylakoid membranes in methyl viologen-treated plants. Plant Physiol. 1997 Dec;115(4):1721–1727. doi: 10.1104/pp.115.4.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Radmer R. J., Kok B. Photoreduction of O(2) Primes and Replaces CO(2) Assimilation. Plant Physiol. 1976 Sep;58(3):336–340. doi: 10.1104/pp.58.3.336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Radmer R., Kok B., Ollinger O. Kinetics and Apparent K(m) of Oxygen Cycle under Conditions of Limiting Carbon Dioxide Fixation. Plant Physiol. 1978 Jun;61(6):915–917. doi: 10.1104/pp.61.6.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sano S., Miyake C., Mikami B., Asada K. Molecular characterization of monodehydroascorbate radical reductase from cucumber highly expressed in Escherichia coli. J Biol Chem. 1995 Sep 8;270(36):21354–21361. doi: 10.1074/jbc.270.36.21354. [DOI] [PubMed] [Google Scholar]
  33. Tel-Or E., Huflejt M. E., Packer L. Hydroperoxide metabolism in cyanobacteria. Arch Biochem Biophys. 1986 Apr;246(1):396–402. doi: 10.1016/0003-9861(86)90485-6. [DOI] [PubMed] [Google Scholar]
  34. Yamamoto H., Miyake C., Dietz K. J., Tomizawa K., Murata N., Yokota A. Thioredoxin peroxidase in the Cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 1999 Mar 26;447(2-3):269–273. doi: 10.1016/s0014-5793(99)00309-9. [DOI] [PubMed] [Google Scholar]

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