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Chlororespiratory Pathways and Their Physiological Significance

  • Peter J. Nixon
  • Peter R. Rich
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 23)

There is now overwhelming evidence that the thylakoid membrane of green plants contains, in addition to the photosynthetic electron-transfer complexes, a set of respiratory complexes that are capable of reducing and oxidising the plastoquinone pool. These “chlororespiratory” enzymes include the Ndh complex, which is related to complex I found in mitochondria and eubacteria, and the plastid terminal oxidase (PTOX), which is a distant member of the family of alternative oxidases found in mitochondria. In addition the molecular basis of other chlororespiratory activities, including the long sought after ferredoxin:plastoquinone reductase (FQR), implicated in cyclic electron flow around photosystem one, are now being uncovered using a combination of genetics, biochemistry and bioinformatics. Here we assess the possible components of the various chlororespiratory pathways and discuss their potential physiological importance. The emerging picture suggests that the main role of chlororespiratory enzymes, at least in mature chloroplasts, is not actually to participate in a classical respiratory chain to drive ATP synthesis. Instead, chlororespiratory activities play important auxiliary roles in various aspects of photosynthesis including cyclic electron flow around photosystem one, carotenoid biosynthesis and photoprotection. The detection of chlororespiratory enzymes in non-photosynthetic plastids suggests that their activities are not restricted to the chloroplast.

Keywords

Cyclic Electron Flow Cyclic Electron Transport Plastoquinone Pool Dark Reduction Cyclic Electron Transfer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Allen JF (2002) Plastoquinone redox control of chloroplast thy-lakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background and im- plications. Photosyn Res 73: 139-148CrossRefPubMedGoogle Scholar
  2. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophos-phorylation: new links in the chain. Trends Plant Sci 8: 15-19CrossRefPubMedGoogle Scholar
  3. Aluru MR and Rodermel SR (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol Plant 120: 4-11CrossRefPubMedGoogle Scholar
  4. Aluru MR, Bae H, Wu DY and Rodermel SR (2001) The Ara-bidopsis immutans mutation affects plastid differentiation and the morphogenesis of white and green sectors in variegated plants. Plant Physiol 127: 67-77CrossRefPubMedGoogle Scholar
  5. Andersson ME and Nordlund P (1999) A revised model of the active site of alternative oxidase. FEBS Lett 449: 17-22CrossRefPubMedGoogle Scholar
  6. Barth C and Krause GH (2002) Study of tobacco transformants to assess the role of chloroplastic NAD(P)H dehydrogenase in photoprotection of photosystems I and II. Planta 216: 273-279CrossRefPubMedGoogle Scholar
  7. Battchikova N, Zhang PP, Rudd S, Ogawa T and Aro E-M (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L, and NDH-1M complexes of Synechocystis sp PCC 6803. J Biol Chem 280: 2587-2595CrossRefPubMedGoogle Scholar
  8. B äumer S, Ide T, Jacobi C, Johann A, Gottschalk G and Deppenmeier U (2000) The F420 H2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases. J Biol Chem 275: 17968-17973CrossRefGoogle Scholar
  9. Bendall DS (1982) Photosynthetic cytochromes of oxygenic or-ganisms. Biochim Biophys Acta 683: 119-151Google Scholar
  10. Bendall DS and Manasse RS (1995) Cyclic phosphorylation and electron transport. Biochim Biophys Acta 1229: 23-38CrossRefGoogle Scholar
  11. Bennoun P (1982) Evidence for a respiratory chain in the chloro-plast. Proc Natl Acad Sci USA 79: 4352-4356CrossRefPubMedGoogle Scholar
  12. Bennoun P (1983) Effects of mutations and of ionophore on chlororespiration in Chlamydomonas reinhardtii. FEBS Lett 156: 363-365CrossRefGoogle Scholar
  13. Berthold DA, Andersson ME and Nordlund P (2000) New in-sights into the structure and function of the alternative oxidase. Biochim Biophys Acta 1460: 241-254CrossRefPubMedGoogle Scholar
  14. Binder RG and Selman BR (1980) Two pathways of electron transfer in quinol-mediated cyclic phosphorylation in spinach chloroplasts. Biochim Biophys Acta 592: 314-322CrossRefPubMedGoogle Scholar
  15. Bock R, Kossel H and Maliga P (1994) Introduction of a heterol-ogous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype. EMBO J 13: 4623-4628PubMedGoogle Scholar
  16. Bondarava N, De Pascalis L, Al-Babili S, Goussias C, Golecki JR, Beyer P, Bock R and Krieger-Liszkay A (2003) Evidence that cytochrome b559 mediates the oxidation of reduced plas-toquinone in the dark. J Biol Chem 278: 13554-13560CrossRefPubMedGoogle Scholar
  17. Br üggemann H, Falinski F and Deppenmeier U (2000) Struc-ture of the F420 H2 : quinone oxidoreductase of Archaeoglobus fulgidus—Identification and overproduction of the F420 H2 -oxidizing subunit. Eur J Biochem 267: 5810-5814CrossRefGoogle Scholar
  18. Burrows PA, Sazanov LA, Svab Z, Maliga P and Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17: 868-876CrossRefPubMedGoogle Scholar
  19. Carol P and Kuntz M (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlorores-piration. Trends Plant Sci 6: 31-36CrossRefPubMedGoogle Scholar
  20. Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G and Kuntz M (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11: 57-68CrossRefPubMedGoogle Scholar
  21. Casano LM, Zapata JM, Martín M and Sabater B (2000) Chlororespiration and poising of cyclic electron transport. Plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. J Biol Chem 275: 942-948CrossRefPubMedGoogle Scholar
  22. Casano L M, Martin M and Sabater B (2001) Hydrogen perox-ide mediates the induction of chloroplastic Ndh complex un-der photooxidative stress in barley. Plant Physiol 125: 1450-1458CrossRefPubMedGoogle Scholar
  23. Corneille S, Cournac L, Guedeney G, Havaux M and Peltier G (1998) Reduction of the plastoquinone pool by exogenous NADH and NADPH in higher plant chloroplasts. Character-ization of a NAD(P)H-plastoquinone oxidoreductase activity. Biochim Biophys Acta 1363: 59-69CrossRefPubMedGoogle Scholar
  24. Cournac L, Redding K, Ravenel J, Rumeau D, Josse E M, Kuntz M and Peltier G (2000) Electron flow between photosys-tem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespi-ration. J Biol Chem 275: 17256-17262CrossRefPubMedGoogle Scholar
  25. Day DA and Wiskich JT (1976) Isolation and properties of the outer membrane of plant mitochondria. Arch Biochem Bio-phys 171: 117-123CrossRefGoogle Scholar
  26. Endo T, Shikanai T, Sato F and Asada K (1998) NAD(P)H dehydrogenase-dependent, antimycin A-sensitive electron do-nation to plastoquinone in tobacco chloroplasts. Plant Cell Physiol 39: 1226-1231Google Scholar
  27. Endo T, Shikanai T, Takabayashi A, Asada K and Sato F (1999) The role of chloroplastic NAD(P)H dehydrogenase in photo-protection. FEBS Lett 457: 5-8CrossRefPubMedGoogle Scholar
  28. Fearnley IM and Walker JE (1992) Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim Biophys Acta 1140: 105-134CrossRefPubMedGoogle Scholar
  29. Finazzi G (2005) The central role of the green alga Chlamy-domonas reinhardtii in revealing the mechanism of state tran-sitions. J Exp Bot 56: 383-388CrossRefPubMedGoogle Scholar
  30. Fisher N and Rich PR (2000) A motif for quinone binding sites in respiratory and photosynthetic systems. J Mol Biol 296: 1153-1162CrossRefPubMedGoogle Scholar
  31. Friedrich T, Steinm üller K and Weiss H (1995) The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett 367: 107-111CrossRefPubMedGoogle Scholar
  32. Garab G, Lajk ó F, Must árdy L and M árton L (1989) Respiratory control over photosynthetic electron transport in chloroplasts of higher-plant cells: evidence for chlororespiration. Planta 179: 349-358CrossRefGoogle Scholar
  33. Godde D (1982) Evidence for a membrane bound NADH-plastoquinone-oxidoreductase in Chlamydomonas reinhardtii CW-15. Arch Microbiol 131: 197-202CrossRefGoogle Scholar
  34. Godde D and Trebst A (1980) NADH as electron donor for the photosynthetic membrane of Chlamydomonas reinhardtii. Arch Microbiol 127: 245-252CrossRefGoogle Scholar
  35. Goedheer JC (1963) A cooperation of two pigment systems and respiration in photosynthetic luminescence. Biochim Biophys Acta 66: 61-71CrossRefPubMedGoogle Scholar
  36. Gounaris K, Chapman DJ and Barber J (1988) Reconstitution of plastoquinone in the D1/D2/cytochrome b-559 photosystem II reaction centre complex. FEBS Lett 240: 143-147CrossRefGoogle Scholar
  37. Graan T and Ort DR (1984) Quantitation of the rapid electron donors to P700, the functional plastoquinone pool, and the ratio of the photosystems in spinach chloroplasts. J Biol Chem 259: 14003-14010PubMedGoogle Scholar
  38. Grohmann L, Rasmusson AG, Heiser V, Thieck O and Brennicke A (1996) The NADH-binding subunit of respiratory chain complex I is nuclear-encoded in plants and identified only in mitochondria. Plant J 10: 793-803CrossRefPubMedGoogle Scholar
  39. Gu éra A and Sabater B (2002) Changes in the protein and activ-ity levels of the plastid NADH- plastoquinone-oxidoreductase complex during fruit development. Plant Physiol Biochem 40: 423-429CrossRefGoogle Scholar
  40. Gu éra A, de Nova PG and Sabater B (2000) Identification of the Ndh (NAD(P)H-plastoquinone-oxidoreductase) complex in etioplast membranes of barley: changes during photomor-phogenesis of chloroplasts. Plant Cell Physiol 41: 49-59Google Scholar
  41. Gu éra A, Calatayud A, Sabater B and Barreno E (2005) Involve-ment of the thylakoidal NADH-plastoquinone-oxidoreductase complex in the early responses to ozone exposure of barley (Hordeum vulgare L.) seedlings. J Exp Bot 56: 205-218Google Scholar
  42. Hibberd JM and Quick WP (2002) Characteristics of C-4 photo-synthesis in stems and petioles of C-3 flowering plants. Nature 415: 451-454CrossRefPubMedGoogle Scholar
  43. Hirst JK, Carroll J, Fearnley IM, Shannon RJ and Walker JE (2003) The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim Biophys Acta 1604: 135-150CrossRefPubMedGoogle Scholar
  44. Horv áth EM, Peter SO, Jo ët T, Rumeau D, Cournac L, Horvath GV, Kavanagh TA, Schafer C, Peltier G and Medgyesy P (2000) Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiol 123: 1337-1350CrossRefGoogle Scholar
  45. Jo ët T, Cournac L, Peltier G and Havaux M (2002a) Cyclic elec-tron flow around photosystem I in C(3) plants. In vivo con-trol by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128: 760-769CrossRefGoogle Scholar
  46. Jo ët T, Genty B, Josse EM, Kuntz M, Cournac L and Peltier G (2002b) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J Biol Chem 277: 31623-31630CrossRefGoogle Scholar
  47. Joliot P, Beal D and Joliot A (2004) Cyclic electron flow un-der saturating excitation of dark- adapted Arabidopsis leaves. Biochim Biophys Acta 1656: 166-176CrossRefPubMedGoogle Scholar
  48. Josse EM, Simkin AJ, Gaffe J, Laboure AM, Kuntz M and Carol P (2000) A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol 123: 1427-1436CrossRefPubMedGoogle Scholar
  49. Josse EM, Alcaraz JP, Laboure AM and Kuntz M (2003) In vitro characterization of a plastid terminal oxidase (PTOX). Eur J Biochem 270: 3787-3794CrossRefPubMedGoogle Scholar
  50. Kofer W, Koop H-U, Wanner G and Steinm üller K (1998) Mu-tagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transfor-mation. Mol Gen Genet 258: 166-173CrossRefPubMedGoogle Scholar
  51. Kow YW, Erbes DL and Gibbs M (1982) Chloroplast respiration: a means of supplying oxidized pyridine nucleotide for dark chloroplastic metabolism. Plant Physiol 69: 442-447CrossRefPubMedGoogle Scholar
  52. Kruk J and Strzalka K (1999) Dark reoxidation of the plasto-quinone pool is mediated by the low-potential form of cy-tochrome b-559 in spinach thylakoids. Photosynth Res 62: 273-279CrossRefGoogle Scholar
  53. Kruk J and Strzalka K (2001) Redox changes of cytochrome b-559 in the presence of plastoquinones. J Biol Chem 276: 86-91CrossRefPubMedGoogle Scholar
  54. Kubicki A, Funk E, Westhoff P and Steinm üller K (1996) Dif-ferential expression of plastome-encoded ndh genes in meso-phyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport. Planta 199: 276-281CrossRefGoogle Scholar
  55. Kuntz M (2004) Plastid terminal oxidase and its biological sig-nificance. Planta 218: 896-899CrossRefPubMedGoogle Scholar
  56. Kurisu G, Zhang H, Smith JL and Cramer WA (2003) Structure of the cytochrome b6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302: 1009-1014CrossRefPubMedGoogle Scholar
  57. Lennon AM, Prommeenate P and Nixon PJ (2003) Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta 218: 254-260CrossRefPubMedGoogle Scholar
  58. Luttik MAH, Overkamp KM, K ötter P, de Vries S, van Dijken JP and Pronk JT (1998) The Saccharomyces cerevisiae NDE1 and NDE2 genes encode separate mitochondrial NADH de-hydrogenases catalysing the oxidation of cytosolic NADH. J Biol Chem 273: 24529-24534CrossRefPubMedGoogle Scholar
  59. Martín M, Casano LM, Zapata JM, Guera A, del Campo EM, Schmitz-Linneweber C, Maier RM and Sabater B (2004) Role of thylakoid Ndh complex and peroxidase in the protection against photo-oxidative stress: fluorescence and enzyme ac-tivities in wild-type and ndhF-deficient tobacco. Physiol Plant 122: 443-452CrossRefGoogle Scholar
  60. Maxwell DP, Wang Y and McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96: 8271-8276CrossRefPubMedGoogle Scholar
  61. McCauley SW, Melis A, Tang GM-S and Arnon DI (1987) Protonophores induce plastoquinol oxidation and quench chloroplast fluorescence: evidence for a cyclic, proton-conducting pathway in oxygenic photosynthesis. Proc Natl Acad Sci USA 84: 8424-8428CrossRefPubMedGoogle Scholar
  62. Meyer TE, Zhao ZG, Cusanovich MA and Tollin G (1993) Tran-sient kinetics of electron transfer from a variety of c-type cy-tochromes to plastocyanin. Biochemistry 32: 4552-4559CrossRefPubMedGoogle Scholar
  63. Moss DA and Bendall DS (1984) Cyclic electron transport in chloroplasts: the Q cycle and the site of action of antimycin. Biochim Biophys Acta 767: 389-395CrossRefGoogle Scholar
  64. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M and Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371CrossRefPubMedGoogle Scholar
  65. Munekage Y, Hashimoto M, Miyaka C, Tomizawa KI, Endo T, Tasaka M and Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429: 579-582CrossRefPubMedGoogle Scholar
  66. Nixon PJ (2000) Chlororespiration. Philos Trans Roy Soc Lond B Biol Sci 355: 1541-1547CrossRefGoogle Scholar
  67. Ohyama K, Kohchi T, Sano T and Yamada Y (1988) Newly identified groups of genes in chloroplasts. Trends Biochem Sci 13: 19-22CrossRefPubMedGoogle Scholar
  68. Peltier G and Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53: 523-550CrossRefPubMedGoogle Scholar
  69. Peltier J-B, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I and van Wijk KJ (2000) Proteomics of the chloro-plast: systematic identification and targeting analysis of lume-nal and peripheral thylakoid proteins. Plant Cell 12: 319-341CrossRefPubMedGoogle Scholar
  70. Pfannschmidt T (2003) Chloroplast redox signals: how photo-synthesis controls its own genes. Trends Plant Sci 8: 33-41CrossRefPubMedGoogle Scholar
  71. Prommeenate P, Lennon AM, Markert C, Hippler M and Nixon PJ (2004) Subunit composition of NDH-1 complexes of Synechocystis sp PCC 6803—Identification of two new ndh gene products with nuclear-encoded homologues in the chloroplast Ndh complex. J Biol Chem 279: 28165-28173CrossRefPubMedGoogle Scholar
  72. Quiles MJ, Garcia A and Cuello J (2003) Comparison of the thy-lakoidal NAD(P)H dehydrogenase complex and the mitochon-drial complex I separated from barley leaves by blue-native PAGE. Plant Science 164: 541-547CrossRefGoogle Scholar
  73. Rasmusson AG and Moller IM (1991) Effect of calcium ions and inhibitors on internal NAD(P)H dehydrogenases in plant mitochondria. Eur J Biochem 202: 617-623CrossRefPubMedGoogle Scholar
  74. Rasmusson AG, Heiser V, Irrgang KD, Brennicke A and Grohmann L (1998) Molecular characterisation of the 76 kDa iron-sulphur protein subunit of potato mitochondrial com-plex I. Plant Cell Physiol 39: 373-381PubMedGoogle Scholar
  75. Ravanel P, Creuzet S and Tisset M (1990) Inhibitory effect of hydroxyflavones on the exogenous NADH dehydrogenase of plant mitochondrial inner membranes. Phytochemistry 29: 441-445CrossRefGoogle Scholar
  76. Rebeille F and Gans P (1988) Interaction between chloroplasts and mitochondria in microalgae. Role of glycolysis. Plant Physiol 88: 973-975CrossRefPubMedGoogle Scholar
  77. Rich PR (1984) Electron and proton transfers through quinones and cytochrome bc complexes. Biochim Biophys Acta 768: 53-79PubMedGoogle Scholar
  78. Rich PR, Hoefnagel MHN and Wiskich JT (1998) Possi-ble chlororespiratory reactions of thylakoid membranes. In: Moller IM, Gardstrom P, Glimelius K and Glase E (eds) Plant Mitochondria: From Gene to Function, pp 17-23. Backhuys Publishers, Leiden, the NetherlandsGoogle Scholar
  79. Rich PR, Fisher N, Lennon A, Prommeenate P, Purton S, Jassal J and Nixon PJ (2001) An assessment of the pathways of dark reduction and oxidation of the plastoquinone pool in thylakoid membranes of higher plants and green algae. In: Proceedings of the XII Congress on Photosynthesis, Brisbane, Australia. CSIRO Publishing, Melbourne, AustraliaGoogle Scholar
  80. Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inze D and Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32: 329-342CrossRefPubMedGoogle Scholar
  81. Rumeau D, Becuwe-Linka N, Beyly A, Louwagie M, Garin J and Peltier G (2005) New subunits NDH-M, -N and -O, en-coded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17: 219-232CrossRefPubMedGoogle Scholar
  82. Sazanov LA, Burrows PA and Nixon PJ (1998) The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes. Proc Natl Acad Sci USA 95: 1319-1324CrossRefPubMedGoogle Scholar
  83. Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K and Yokota A. (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95: 9705-9709CrossRefPubMedGoogle Scholar
  84. Slater EC (1973) The mechanism of action of the respiratory inhibitor, antimycin. Biochim Biophys Acta 301: 129-154PubMedGoogle Scholar
  85. Soole KL and Menz RI (1995) Functional molecular aspects of the NADH dehydrogenases of plant mitochondria. J Bioenerg Biomemb 27: 397-406CrossRefGoogle Scholar
  86. Stroebel D, Choquet Y, Popot J-L and Picot D (2003) An atypical haem in the cytochrome b6 f complex. Nature 426: 413-418CrossRefPubMedGoogle Scholar
  87. Tagawa K, Tsujimoto HY and Arnon DI (1963) Role of chloro-plast ferredoxin in the energy conversion process of photosyn-thesis. Proc Natl Acad Sci USA 49: 567-572CrossRefPubMedGoogle Scholar
  88. Turpin DH and Bruce D (1990) Regulation of photosynthetic light-harvesting by nitrogen assimilation in the green alga Se-lenastrum minutum. FEBS Lett 263: 99-103CrossRefGoogle Scholar
  89. Wu D, Wright DA, Wetzel C, Voytas DF and Rodermel S (1999) The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11: 43-55CrossRefPubMedGoogle Scholar
  90. Yagi T (1993) The bacterial energy-transducing NADH-quinone oxidoreductases. Biochim Biophys Acta 1141: 1-17CrossRefPubMedGoogle Scholar
  91. Zhang H, Whitelegge JP and Cramer WA (2001) Ferredoxin:NADP+ oxidoreductase is a subunit of the chloro-plast cytochrome b6 f complex. J Biol Chem 276: 38159-3816PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Peter J. Nixon
    • 1
  • Peter R. Rich
    • 2
  1. 1.Division of BiologyImperial College LondonUK
  2. 2.Glynn Laboratory of Bioenergetics, Department of BiologyImperial College LondonUK

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