Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Dec;85(24):9524–9528. doi: 10.1073/pnas.85.24.9524

Cytochrome b-559 and proton conductance in oxygenic photosynthesis

Daniel I Arnon 1, George M-S Tang 1
PMCID: PMC282786  PMID: 16594007

Abstract

Although cytochrome b-559 has long been known as a membrane-bound redox component closely linked to the reaction center of the oxygen-generating photosystem (PSII), its role in photosynthesis has remained obscure. This paper reports evidence and outlines a hypothesis in support of a “b-559 cycle”—i.e., a light-induced, cytochrome b-559-dependent, cyclic electron transport pathway around PSII that promotes translocation of protons from plastoquinol into the aqueous domain (lumen) of photosynthetic membranes (thylakoids). Light-induced proton transport coupled to light-induced electron transport is an essential aspect of energy transduction in photosynthesis because it generates an electrochemical proton gradient that drives ATP synthesis by the process of photosynthetic phosphorylation. The principal carrier of electrons and protons in thylakoids is the plastoquinone/plastoquinol couple. We propose that the b-559 cycle functions as a redox-linked proton pump that may operate jointly with the Rieske iron-sulfur pathway in oxidizing plastoquinol. The overall effect of such concerted oxidation of plastoquinol would be the translocation into the thylakoid lumen of two protons for each electron transferred from water to plastocyanin via plastoquinone.

Keywords: photosystem II, plastoquinol oxidation, uncouplers

Full text

PDF
9524

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arnon D. I. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. Plant Physiol. 1949 Jan;24(1):1–15. doi: 10.1104/pp.24.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arnon D. I. The discovery of ferredoxin: the photosynthetic path. Trends Biochem Sci. 1988 Jan;13(1):30–33. doi: 10.1016/0968-0004(88)90016-3. [DOI] [PubMed] [Google Scholar]
  3. Arnon D. I., Tsujimoto H. Y., McSwain B. D. Ferredoxin and photosynthetic phosphorylation. Nature. 1967 May 6;214(5088):562–566. doi: 10.1038/214562a0. [DOI] [PubMed] [Google Scholar]
  4. Arnon D. I., Tsujimoto H. Y., Tang G. M. Proton transport in photooxidation of water: A new perspective on photosynthesis. Proc Natl Acad Sci U S A. 1981 May;78(5):2942–2946. doi: 10.1073/pnas.78.5.2942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boardman N. K., Anderson J. M., Hiller R. G. Photooxidation of cytochromes in leaves and chloroplasts at liquid-nitrogen temperature. Biochim Biophys Acta. 1971 Apr 6;234(1):126–136. doi: 10.1016/0005-2728(71)90137-x. [DOI] [PubMed] [Google Scholar]
  6. Cramer W. A., Böhme H. High-potential cytochrome b-559 as a secondary quencher of chloroplast fluorescence in the presence of 3-(3,4-dichlorophenyl)-I,I-dimethylurea. Biochim Biophys Acta. 1972 Feb 28;256(2):358–369. doi: 10.1016/0005-2728(72)90066-7. [DOI] [PubMed] [Google Scholar]
  7. Dutton P. L., Wilson D. F. Redox potentiometry in mitochondrial and photosynthetic bioenergetics. Biochim Biophys Acta. 1974 Oct 31;346(2):165–212. doi: 10.1016/0304-4173(74)90008-1. [DOI] [PubMed] [Google Scholar]
  8. HEYTLER P. G. uncoupling of oxidative phosphorylation by carbonyl cyanide phenylhydrazones. I. Some characteristics of m-Cl-CCP action on mitochondria and chloroplasts. Biochemistry. 1963 Mar-Apr;2:357–361. doi: 10.1021/bi00902a031. [DOI] [PubMed] [Google Scholar]
  9. Hauska G., Hurt E., Gabellini N., Lockau W. Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim Biophys Acta. 1983 Jul 15;726(2):97–133. doi: 10.1016/0304-4173(83)90002-2. [DOI] [PubMed] [Google Scholar]
  10. Heber U., Kirk M. R., Boardman N. K. Photoreactions of Cytochrome b-559 and cyclic electron flow in photosystem II of intact chloroplasts. Biochim Biophys Acta. 1979 May 9;546(2):292–306. doi: 10.1016/0005-2728(79)90047-1. [DOI] [PubMed] [Google Scholar]
  11. Kallas T., Spiller S., Malkin R. Primary structure of cotranscribed genes encoding the Rieske Fe-S and cytochrome f proteins of the cyanobacterium Nostoc PCC 7906. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5794–5798. doi: 10.1073/pnas.85.16.5794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Knaff D. B., Arnon D. I. LIGHT-INDUCED OXIDATION OF A CHLOROPLAST B-TYPE CYTOCHROME AT -189 degrees C. Proc Natl Acad Sci U S A. 1969 Jul;63(3):956–962. doi: 10.1073/pnas.63.3.956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McCauley S. W., Melis A., Tang G. M., Arnon D. I. Protonophores induce plastoquinol oxidation and quench chloroplast fluorescence: Evidence for a cyclic, proton-conducting pathway in oxygenic photosynthesis. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8424–8428. doi: 10.1073/pnas.84.23.8424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McSwain B. D., Arnon D. I. Enhancement effects and the identity of the two photochemical reactions of photosynthesis. Proc Natl Acad Sci U S A. 1968 Nov;61(3):989–996. doi: 10.1073/pnas.61.3.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mitchell P. Keilin's respiratory chain concept and its chemiosmotic consequences. Science. 1979 Dec 7;206(4423):1148–1159. doi: 10.1126/science.388618. [DOI] [PubMed] [Google Scholar]
  16. Mitchell P. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol. 1976 Oct 21;62(2):327–367. doi: 10.1016/0022-5193(76)90124-7. [DOI] [PubMed] [Google Scholar]
  17. Miyoshi H., Nishioka T., Fujita T. Quantitative relationship between protonophoric and uncoupling activities of analogs of SF6847 (2,6-di-t-butyl-4-(2',2'-dicyanovinyl)phenol). Biochim Biophys Acta. 1987 May 6;891(3):293–299. doi: 10.1016/0005-2728(87)90224-6. [DOI] [PubMed] [Google Scholar]
  18. Nanba O., Satoh K. Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci U S A. 1987 Jan;84(1):109–112. doi: 10.1073/pnas.84.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Papa S. Proton translocation reactions in the respiratory chains. Biochim Biophys Acta. 1976 Apr 30;456(1):39–84. doi: 10.1016/0304-4173(76)90008-2. [DOI] [PubMed] [Google Scholar]
  20. STRAUB J. P., COLPA-BOONSTRA J. P. The effect of pH on the oxidation-reduction potential of cytochrome b in heart-muscle preparations. Biochim Biophys Acta. 1962 Jul 16;60:650–652. doi: 10.1016/0006-3002(62)90887-9. [DOI] [PubMed] [Google Scholar]
  21. Terada H. The interaction of highly active uncouplers with mitochondria. Biochim Biophys Acta. 1981 Dec 30;639(3-4):225–242. doi: 10.1016/0304-4173(81)90011-2. [DOI] [PubMed] [Google Scholar]
  22. Urban P. F., Klingenberg M. On the redox potentials of ubiquinone and cytochrome b in the respiratory chain. Eur J Biochem. 1969 Jul;9(4):519–525. doi: 10.1111/j.1432-1033.1969.tb00640.x. [DOI] [PubMed] [Google Scholar]
  23. Wada K., Arnon D. I. Three forms of cytochrome b 559 and their relation to the photosynthetic activity of chloroplasts. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3064–3068. doi: 10.1073/pnas.68.12.3064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wikström M. K. The different cytochrome b components in the respiratory chain of animal mitochondria and their role in electron transport and energy conservation. Biochim Biophys Acta. 1973 Dec 7;301(2):155–193. doi: 10.1016/0304-4173(73)90003-7. [DOI] [PubMed] [Google Scholar]
  25. Wilson D. F., Erecińska M., Leigh J. S., Jr, Koppelman M. The properties of the mitochondrial succinate-cytochrome c reductase. Arch Biochem Biophys. 1972 Jul;151(1):112–121. doi: 10.1016/0003-9861(72)90479-1. [DOI] [PubMed] [Google Scholar]
  26. el-Demerdash M., Salnikow J., Vater J. Evidence for a cytochrome f-Rieske protein subcomplex in the cytochrome b6f system from spinach chloroplasts. Arch Biochem Biophys. 1988 Jan;260(1):408–415. doi: 10.1016/0003-9861(88)90464-x. [DOI] [PubMed] [Google Scholar]
  27. van Gorkom H. J., Tamminga J. J., Haveman J. Primary reactions, plastoquinone and fluorescence yield in subchloroplast fragments prepared with deoxycholate. Biochim Biophys Acta. 1974 Jun 28;347(3):417–438. doi: 10.1016/0005-2728(74)90080-2. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES