The Regulation of Chloroplast ATP Synthase, CF0-CF1

  • John D. Mills
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 4)


\( \Delta \tilde \mu _{H^ + } \) – electrochemical potential difference of H+ across the thylakoid ΔpH – difference in pH across the thylakoid ΔΨ – difference in electric potential across the thylakoid ΔGp – Free energy change for ATP synthesis NEM – N-ethylmaleimide 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrahams JP, Leslie AGW, Lutter R, and Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370: 621–628PubMedCrossRefGoogle Scholar
  2. Andralojc PJ and Harris DA (1988) Two distinct types of ϥ-binding site exist in chloroplast coupling factor (CF1). FEBS Lett 233: 403–407CrossRefGoogle Scholar
  3. Anthon GE and Jagendorf AT (1986) Evidence for multiple effects in the methanol activation of chloroplast coupling factor 1. Biochim Biophys Acta 848: 92–98PubMedGoogle Scholar
  4. Arana JL and Vallejos RH (1982) Involvement of sulphydryl groups in the activation mechanism of the ATPase activity of chloroplast CF1. J Biol Chem 257: 1125–1127PubMedGoogle Scholar
  5. Austin PA, Ross IS and Mills JD (1992) Light/dark regulation of photosynthetic enzymes in intact cells of the cyanobacterium Nostoc sp Mac. Biochim Biophys Acta 1099: 226–232Google Scholar
  6. Bakker-Grunwald T and van Dam K (1974) On the mechanism of activation of the ATPase in chloroplasts. Biochim Biophys Acta 347: 290–298PubMedGoogle Scholar
  7. Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Nat Acad Sci USA 79: 4352–4356PubMedGoogle Scholar
  8. Biaudet P, de Kouchkovsky F and Haraux F (1988) ΔpH-activation of the thiol-modified chloroplast ATP hydrolase. Nucleotide binding effects. Biochim Biophys Acta 933: 487–500Google Scholar
  9. Bizouarn T, de Kouchkovsky Y and Haraux F (1991) Dependence of kinetic parameters of chloroplast ATP synthase on external pH, internal pH, and delta pH. Biochemistry 30: 6847–6853PubMedCrossRefGoogle Scholar
  10. Boekema EJ and Böttcher B (1992) The structure of ATP synthase from chloroplasts. Conformational changes of CF1 studied by electron microscopy. Biochim Biophys Acta 1098: 131–143Google Scholar
  11. Carmeli C and Lifschitz Y. (1972) Effects of Pi and ADP on ATPase activity in chloroplasts. Biochim Biophys Acta 267: 86–95PubMedGoogle Scholar
  12. Chiang G and Dilley RA (1987) Evidence for Ca2+-gated proton fluxes in chloroplast thylakoid membranes: Ca2+ controls a localized to delocalized proton switch. Biochemistry 26: 4911–4916CrossRefGoogle Scholar
  13. Crawford NA, Droux M, Kosower NS and Buchanan BB (1989) Evidence for function of the ferredoxin/thioredoxin system in the reductive activation of target enzymes in isolated intact chloroplasts. Arch Biochem Biophys 271: 223–239PubMedCrossRefGoogle Scholar
  14. Cséke C and Buchanan BB (1986) Regulation of the formation and utilization of photosynthate in leaves. Biochim Biophys Acta 853: 43–63Google Scholar
  15. Davenport JW and McCarty RE (1984) An analysis of proton fluxes coupled to electron transport and ATP synthesis in chloroplast thylakoids. Biochim Biophys Acta 766: 363–374Google Scholar
  16. Davenport JW and McCarty RE (1986) Relationships between rates of steady-state ATP synthesis and the magnitude of the proton activity across thylakoid membranes. Biochim Biophys Acta 851: 136–145Google Scholar
  17. Du ZY and Boyer PD (1990) On the mechanism of sulfite activation of chloroplast thylakoid ATPase and the relation of ADP tightly bound at a catalytic site to the binding change mechanism. Biochemistry 29: 402–407PubMedCrossRefGoogle Scholar
  18. Duhe RJ and Selman BR (1990) The dithiothreitol-stimulated dissociation of the chloroplast coupling factor 1 ε-subunit is reversible. Biochim Biophys Acta 1017: 70–78PubMedGoogle Scholar
  19. Dunham KR and Selman BR (1981) Interactions of Pi with spinach CF1. Effects on ATPase and binding activities. J Biol Chem 256: 10044–10049PubMedGoogle Scholar
  20. Fearnley IM and Walker JE (1992) Conservation of sequences of subunits of complex I and their relationships with other proteins. Biochim Biophys Acta 1140: 105–134PubMedGoogle Scholar
  21. Feldman RI and Boyer PD (1985) The role of tightly bound ADP on chloroplast ATPase. J Biol Chem 260: 13088–13094PubMedGoogle Scholar
  22. Gabrys H, Kramer DM, Crofts AR and Ort DR (1994) Mutants of chloroplast coupling factor reduction in Arabidopsis. Plant Physiol 104: 769–776PubMedGoogle Scholar
  23. Galmiche JM, Girault G, Berger G, Jacquot JP, Miginiac-Maslow M and Wollman E. (1990) Induction by different thioredoxins of ATPase activity coupling factor 1 from spinach. Biochimie 72: 25–32PubMedCrossRefGoogle Scholar
  24. Giersch C, Heber U, Kobayashi Y, Innoue Y, Shibata K, and Heldt HW (1980) Energy storage, phosphorylation potential and protonmotive force in chloroplasts. Biochim Biophys Acta 590: 59–73PubMedGoogle Scholar
  25. Gräber P, Schlodder U and Witt, HT (1977) Conformational change of the chloroplast ATPase induced by transmembrane electric field and its correlation to phosphorylation. Biochim Biophys Acta 461: 426–440PubMedGoogle Scholar
  26. Gräber P, Schlodder U and Witt HT (1984) Mechanism of the regulation of ATP synthesis hydrolysis in chloroplasts. In: Papa S, Altendorf K, Ernster L and Packer L (eds) H+-ATPase: Structure, Function, Biogenesis. pp 431–440. Adriatic Editrice, BariGoogle Scholar
  27. Griwatz C and Junge W (1992) Cooperative transient trapping of protons by a distorted chloroplast ATPase. Evidence for a proton well? Biochim Biophys Acta 1101: 244–248Google Scholar
  28. Groom QJ, Kramer DM, Crofts AR and Ort DR (1993) The non-photochemical reduction of plastoquinone in leaves. Photosyn Res 36: 205–215Google Scholar
  29. Groth G and Junge W (1993) Proton slip of the chloroplast ATPase: Its nucleotide dependence, energetic threshold, and relation to an alternating site mechanism of catalysis. Biochemistry 32: 8103–8111PubMedCrossRefGoogle Scholar
  30. Hangarter RP and Ort DR (1986) The relationship between light-induced increases in the H+ conductivity of thylakoid membranes and activity of the coupling factor. Eur J Biochem 158: 7–12PubMedCrossRefGoogle Scholar
  31. Hangarter RP, Grandioni P and Ort DR (1987) The effects of chloroplast coupling factor reduction on the energetics of activation and on the energetics and efficiency of ATP formation. J Biol Chem 262: 13513–13519PubMedGoogle Scholar
  32. Harris DA and Crofts AR (1978) The initial stages of photophosphorylation. Studies using excitation by saturating short flashes of light. Biochim Biophys Acta 502: 87–102PubMedGoogle Scholar
  33. Harris GC and Heber U (1993) Effects of anaerobiosis on chlorophyll fluorescence yield in spinach leaf discs. Plant Physiol 101: 1169–1173PubMedGoogle Scholar
  34. Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge U-I and Heldt HW (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95: 1131–1137PubMedGoogle Scholar
  35. Holmgren A (1985) Thioredoxin. Ann Rev Biochem 54: 237–271PubMedGoogle Scholar
  36. Junesche U and Gräber P (1985) The rate of ATP synthesis as a function of ΔpH in normal and dithiothreitol-modified chloroplasts. Biochim Biophys Acta 809: 429–434Google Scholar
  37. Junesche U and Gräber P (1987) Influence of the redox state and the activation of the chloroplast ATP synthase on proton-transport coupled ATP synthesis/hydrolysis. Biochim Biophys Acta 893: 275–288Google Scholar
  38. Junesche U and Gräber P (1991) The rate of ATP synthesis as a function of ΔpH and ΔΨ catalysed by the active, reduced H+-ATPase from chloroplasts. FEBS Lett 294: 275–278Google Scholar
  39. Junge W (1970) The critical electric potential difference for photophosphorylation. Its relation to the chemiosmotic hypothesis and to triggering requirements of the ATPase system. Eur J Biochem 14: 582–592PubMedGoogle Scholar
  40. Kacser H and Burns JA (1973) The control of flux. In: Davies DD (ed) Rate Control of Biological Processes, pp 65–104. Cambridge University Press, CambridgeGoogle Scholar
  41. Ketcham SR, Davenport JW, Wernicke K and McCarty RE (1984) Role of the γ-subunit of the chloroplast coupling factor 1 in the light-dependent activation of photophosphorylation and ATPase activity by dithiothreitol. J Biol Chem 259: 7286–7293PubMedGoogle Scholar
  42. Kleefeld S, Lohse D, Mansy A and Strotmann H (1990) Activation and deactivation of the thiol-modulated chloroplast H+-ATPase during ATP hydrolysis. Biochim Biophys Acta 1019: 11–18Google Scholar
  43. Komatsu-Takaki M (1993) Energy-dependent changes in the conformation of the chloroplast ATP synthase and its catalytic activity. Eur J Biochem 214: 587–591.PubMedCrossRefGoogle Scholar
  44. Kostrzewa M and Zetsche K (1992) Large ATP synthase operon of the red alga Antithamnion sp. resembles the corresponding operon in cyanobacteria. J Mol Biol 227: 961–970PubMedCrossRefGoogle Scholar
  45. Krab K, Bakels RHA, Scholts MJC and van Walraven HS (1993) Activation of the H+-ATP synthase in thylakoid vesicles from cyanobacterium Synechococcus 6716 by \( \Delta \tilde \mu _{H^ + } \). Biochim Biophys Acta 1141: 197–205Google Scholar
  46. Kramer DM and Crofts AR (1989) Activation of the chloroplast ATPase measured by electrochromic change in leaves of intact plants. Biochim Biophys Acta 976: 28–41Google Scholar
  47. Kramer DM, Wise RR, Frederick JR, Alm DM, Hesketh JD, Ort DR and Crofts AR (1992) Regulation of coupling factor in field grown sunflower: A redox model relating coupling factor activity to activities of other thioredoxin-dependent enzymes. Photosyn Res 26: 213–222Google Scholar
  48. McCarty RE and Racker E (1968) Partial resolution of the enzymes catalysing photophosphorylation III. Activation of ATPase and 32Pi, ATP exchange in chloroplasts. J Biol Chem 243: 129–137PubMedGoogle Scholar
  49. Miki J, Maeda M, Mukohata Y and Futai M (1988) The γ subunit of ATP synthase from spinach chloroplasts. Primary structure deduced from cloned cDNA sequence. FEBS Lett 232: 221–226PubMedCrossRefGoogle Scholar
  50. Mills JD and Mitchell P (1982a) Modulation of coupling factor ATPase activity in intact chloroplasts. Reversal of thiol modulation in the dark. Biochim Biophys Acta 679: 75–83Google Scholar
  51. Mills JD and Mitchell P (1982b) Thiol modulation of CFo–CF1 stimulates acid/base dependent phosphorylation of ADP by broken pea chloroplasts. FEBS Lett 144: 63–67CrossRefGoogle Scholar
  52. Mills JD and Mitchell P (1984) Thiol modulation of the chloroplast ATPase and its effect on photophosphorylation. Biochim Biophys Acta 764: 93–104Google Scholar
  53. Mills JD, Mitchell P and Schürmann P (1980) Modulation of coupling factor ATPase activity in intact chloroplasts. The role of the thioredoxin system. FEBS Lett 112: 173–177CrossRefGoogle Scholar
  54. Mitchell P (1968) Chemiosmotic coupling and energy transduction. Glynn Research Ltd, Bodmin, UKGoogle Scholar
  55. Mitra B and Hammes GG (1988) Characterization of three-subunit chloroplast coupling factor. Biochemistry 27: 245–250PubMedCrossRefGoogle Scholar
  56. Morita S, Itoh S and Nishimura M (1983) Flash induced photophosphorylation in chloroplasts with activated ATPase. Biochim Biophys Acta 724: 411–415Google Scholar
  57. Moroney JV, Fullmer CS and McCarty RE (1984) Characterization of the cysteinyl-containing peptides of the γ subunit of coupling factor 1. J Biol Chem 259: 7281–7285PubMedGoogle Scholar
  58. Nalin CM and McCarty RE (1984) Role of a disulfide bond in the γ subunit in activation of the ATPase of chloroplast coupling factor 1. J Biol Chem 259: 7275–7280PubMedGoogle Scholar
  59. Nelson N, Nelson H and Racker E (1972) Partial resolution of the enzymes catalysing photophosphorylation XII. Purification and properties of an inhibitor isolated from coupling factor 1. J Biol Chem 259: 7275–7280Google Scholar
  60. Nichols P, Obinger C, Niederhauser H and Peschek GA (1992) Cytochrome oxidase in Anacystis nidulans. Stoichiometries and possible functions in the cytoplasm and thylakoid membranes. Biochim Biophys Acta 1098: 184–190Google Scholar
  61. Noctor GD and Mills JD (1988) Thiol-modulation of the chloroplast ATPase. Lack of oxidation of the enzyme in the presence of \( \Delta \tilde \mu _{H^ + } \) and a possible explanation of the physiological requirement for thiol regulation of the enzyme. Biochim Biophys Acta 935: 53–60Google Scholar
  62. Ort DR and Oxborough K (1992) In situ regulation of chloroplast coupling factor activity. Ann Rev Plant Physiol Plant Mol Biol 43: 269–291CrossRefGoogle Scholar
  63. Pancic PG and Strotmann H (1993) Structure of the nuclear encoded gamma subunit of CF0CF1 of the diatom Odontella sinensis including its presequence. FEBS Lett 320: 61–66PubMedCrossRefGoogle Scholar
  64. Pancic PG, Strotmann H and Kowallik KV (1992) Chloroplast ATPase genes in the diatom Odontella sinensis reflect cyanobacterial characters in structure and arrangement. J Mol Biol 224: 529–536PubMedCrossRefGoogle Scholar
  65. Petrack B, Caston A, Sheppy F and Farron F (1965) Studies on the hydrolysis of ATP by spinach chloroplasts. J Biol Chem 240: 906–914PubMedGoogle Scholar
  66. Pettersson G and Ryde-Pettersson U (1988) A mathematical model of the Calvin photosynthesis cycle. Eur J Biochem 175: 661–672PubMedCrossRefGoogle Scholar
  67. Possmayer FE and Gräber P (1994) The pHin and pHout dependence of the rate of ATP synthesis catalysed by the chloroplast H+-ATPase, CF0CF1, in proteoliposomes. J Biol Chem 269: 1896–1904PubMedGoogle Scholar
  68. Quick WP and Mills JD (1986) Thiol modulation of chloroplast CFo–CF1 in isolated barley protoplasts and its significance to the regulation of carbon dioxide fixation. Biochim Biophys Acta 861: 166–172Google Scholar
  69. Quick WP and Mills JD (1987) Changes in the apparent Michaelis constant for ADP during photophosphorylation are consistent with a delocalized chemiosmotic energy coupling. Biochim Biophys Acta 893: 197–207Google Scholar
  70. Reimer S and Selman BR (1978) Tentoxin-induced energy independent adenine nucleotide exchange and ATPase activity with chloroplast coupling factor 1. J Biol Chem 253: 7249–7255PubMedGoogle Scholar
  71. Richter ML and McCarty RE (1987) Energy-dependent changes in the conformation of the ε-subunit of the chloroplast ATP synthase. J Biol Chem 262: 15037–15040PubMedGoogle Scholar
  72. Rumberg B and Becher U (1984) Multiple ΔpH control of H+-ATP synthase function in chloroplasts. In: Papa S, Altendorf K, Ernster L and Packer L (eds) H+-ATPase Structure, Function, Biogenesis. pp 421–430. Adriatic Editrice, BariGoogle Scholar
  73. Ryrie IJ and Jagendorf AT (1972) Correlation between a conformational change in the coupling factor protein and the high energy state in chloroplasts. J Biol Chem 247: 4453–4459PubMedGoogle Scholar
  74. Scheibe (1981) Thioredoxinm in pea chloroplasts: Concentration and redox status under light and dark conditions. FEBS Lett 133: 301–304CrossRefGoogle Scholar
  75. Scheibe R (1987) NADP+-malate dehydrogenase in C3 plants: Regulation and role of a light-activated enzyme. Physiol Plantarum 71: 393–400Google Scholar
  76. Schlodder E, Gräber P and Witt HT (1982) Mechanism of phosphorylation in chloroplasts. In: Barber J (ed) Topics in Photosynthesis, Vol 4, pp 105–175. Elsevier, AmsterdamGoogle Scholar
  77. Schumann J and Strotmann H (1981) The mechanism of induction and deactivation of light triggered ATPase. In: Akoyunoglou G (ed) Photosynthesis II, Electron Transport and Phosphorylation, pp 881–892. Balaban Int Sci Serv, PhiladelphiaGoogle Scholar
  78. Schumann J, Richter ML and McCarty RE (1985) Partial proteolysis as a probe of the conformation of the γ subunit in activated soluble and membrane-bound chloroplast coupling factor 1. J Biol Chem 260: 11817–11823PubMedGoogle Scholar
  79. Schürmann P, Maeda K and Tsugita A. (1981) Isomers of thioredoxins in spinach leaves. Eur J Biochem 116: 37–45PubMedGoogle Scholar
  80. Selman-Reimer S and Selman BR (1988) The activation and inactivation of the Dunaliella salina chloroplast coupling factor 1 (CF1) in vivo and in situ. FEBS Lett 230: 17–20PubMedGoogle Scholar
  81. Selman-Reimer S, Duhe RJ, Stockman BJ and Selman BR (1991) L-1-N-methyl-4-mercaptohistidine disulfide, a potential endogenous regulator in the redox control of chloroplast coupling factor 1 in Dunaliella. J Biol Chem 266: 182–188PubMedGoogle Scholar
  82. Shahak Y (1985) Differential effect of thiol oxidants on the chloroplast H+-ATPase in the light and in the dark. J Biol Chem 260: 1459–1464PubMedGoogle Scholar
  83. Sigalat C, de Kouchkovski Y, Haraux F and de Kouchkovski F (1988) Shift from localized to delocalized energy coupling in thylakoids by permeant amines. Biochim Biophys Acta 934: 375–388Google Scholar
  84. Soteropoulos P, Süss KH and McCarty RE (1992) Modifications of the γ subunit of chloroplast coupling factor 1 alter interactions with the inhibitory ε subunit. J Biol Chem 267: 10348–10354PubMedGoogle Scholar
  85. Stitt M, McLilley R and Heldt HW (1982) Adenosine nucleotide levels in the cytosol, chloroplasts and mitochondria of wheat protoplasts. Plant Physiol 70: 971–977PubMedCrossRefGoogle Scholar
  86. Strelow F and Rumberg B (1993) Kinetics and energetics of redox regulation of ATP synthase from chloroplasts. FEBS Lett 323: 19–22PubMedCrossRefGoogle Scholar
  87. Strotmann H and Bickel-Sandkötter S (1977) Energy dependent exchange of adenine nucleotides on chloroplast coupling factor 1. Biochim Biophys Acta 460: 126–135PubMedGoogle Scholar
  88. Strotmann H, Kleefeld S and Lohse D (1987) Control of ATP synthesis in chloroplasts. FEBS Lett 221: 265–269CrossRefGoogle Scholar
  89. Tager JM, Wanders RJA, Groen AK, Kunz W, Bohnensack R, Kuster U, Letko G, Bohme G, Duszynski J and Wojtczak L (1983) Control of mitochondrial respiration. FEBS Lett 151: 1–9PubMedCrossRefGoogle Scholar
  90. Ting CS and Owens TG (1993) Photochemical and nonphotochemical fluorescence quenching processes in the diatom Phaeodactylum tricornutum. Plant Physiol 101: 1323–1330PubMedGoogle Scholar
  91. Turina P, Melandri BA and Gräber P (1991) ATP synthesis in chromatophores driven by artificially induced ion gradients. Eur J Biochem 196: 225–229PubMedCrossRefGoogle Scholar
  92. Turina P, Melandri BA and Gräber P (1992) Activation of the H+-ATP synthase in photosynthetic bacterium Rhodobacter capsulatus. J Biol Chem 267: 11057–11063PubMedGoogle Scholar
  93. Valerio M, de Kouchkovsky Y and Haraux F (1992) An attempt to discriminate catalytic and regulatory proton binding sites in membrane-bound, thiol-reduced chloroplast ATPase. Biochemistry 31: 4239–4247PubMedCrossRefGoogle Scholar
  94. Vallejos RH, Arana JL and Ravizzini (1983) Changes in activity and structure of chloroplast proton ATPase induced by illumination of spinach leaves. J Biol Chem 258: 7317–7321.PubMedGoogle Scholar
  95. Werner S, Schumann J and Strotmann H (1990) The primary structure of the γ-subunit of the ATPase from Synechocystis 6803. FEBS Lett 261: 204–208PubMedCrossRefGoogle Scholar
  96. Zhou JM, Xue ZX, Du ZY, Melese T and Boyer PD (1988) Relationship of tightly bound ADP and ATP to control and catalysis by chloroplast ATP synthase. Biochemistry 27: 5129–5135PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • John D. Mills
    • 1
  1. 1.Plant Biochemistry and Microbiology Group, Department of Biological SciencesKeele UniversityUK

Personalised recommendations