Advertisement

Photophosphorylation and the chemiosmotic perspective

  • André T. Jagendorf
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 20)

Abstract

Photophosphorylation was discovered in chloroplasts by D. Arnon and coworkers, and in bacterial ‘chromatophores’ (intercytoplasmic membranes) by A. Frenkel. Initial low rates were amplified by adding electron-carrying compounds such as FMN, later shown to support the ‘pseudocyclic’ electron flow. ATP synthesis, and coupling to electron flow, was detected accompanying linear electron flow from H2O to either NADP+ or ferricyanide. Another pattern of electron flow supporting photophosphorylation was that of a cycle around Photosystem I (PS I). Isolation and analysis of the ATP synthase showed, as with mitochondrial and bacterial analogues, an intrinsic membrane complex (CF0) and an extrinsic complex (CF1). CF1 is a latent ATPase, activated additively by the high-energy state of the thylakoids, and by reduction of a disulfide bond on the gamma subunit. Once reduced, ATP synthesis occurs at lower energy levels. The search for an ‘intermediate’ linking electron flow and ATP synthesis led to the discovery of post-illumination ATP synthesis by thylakoids, where turnover occurs in the dark. Once interpreted by P. Mitchell’s chemiosmotic hypothesis, this led to the discovery of light-driven proton uptake into the thylakoid lumen, with accompanying Cl intake and Mg2+ and K+ output. Chemiosmosis was confirmed in several ways, including ATP synthesis in the dark due to an acid-to-base transition of thylakoids, and photophosphorylation accomplished in artificial lipid vesicles containing both the proton-pumping bacterial rhodopsin and a mitochondrial ATPase complex. The now generally accepted chemiosmotic interpretation is able to clarify some other aspects of photosynthesis as well.

Key words

D. Arnon M. Avron ATPase CF1 chemiosmotic hypothesis chloroplasts coupling factor A. Frenkel G. Hind A. Jagendorf R. McCarty P. Mitchell photophosphorylation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen MB, Whatley FR and Arnon DJ (1958) Photosynthesis by isolated chloroplasts. VI. Rates of conversion of light into chemical energy in photosynthetic phosphorylation. Biochim Biophys Acta 27: 16–23PubMedCrossRefGoogle Scholar
  2. Anthon GE and Jagendorf AT (1983) Effect of methanol on spinach thylakoid ATPase. Biochim Biophys Acta 723: 358–365CrossRefGoogle Scholar
  3. Arnon DI, Allen MB and Whatley FR (1954) Photosynthesis by isolated chloroplasts. II. Photophosphorylation, the conversion of light into phosphate bond energy. J Am Chem Soc 76: 6324–6329CrossRefGoogle Scholar
  4. Arnon DI, Whatley FR and Allen MB (1958a) Assimilatory power in photosynthesis. Science 127: 1026–1034PubMedGoogle Scholar
  5. Arnon DI, Whatley FR and Allen MB (1958b) Photosynthesis by isolated chloroplasts. VIII. Photosynthetic preparation and the generation of assimilatory power. Biochim Biophys Acta 32: 47–57CrossRefGoogle Scholar
  6. Arnon DI, Losada M, Whatley FR, Tsujimoto HY, Hall DO and Horton AA (1961) Photosynthetic phosphorylation and molecular oxygen. Proc Natl Acad Sci USA 47: 1314–1344.PubMedCrossRefGoogle Scholar
  7. Avron M (1963) A coupling factor in photophosphorylation. Biochim Biophys Acta 77: 699–702CrossRefGoogle Scholar
  8. Avron M and Jagendorf AT (1958) Co-factors and rates of photosynthetic phosphorylation by spinach chloroplasts. J Biol Chem 231: 277–290PubMedGoogle Scholar
  9. Avron M and Jagendorf AT (1959) Evidence concerning the mechanism of ATP formation by spinach chloroplasts. J Biol Chem 234: 967–972PubMedGoogle Scholar
  10. Avron M, Krogmann DW and Jagendorf AT (1958) The relation of photosynthetic phosphorylation to the Hill reaction. Biochim Biophys Acta 30: 144–153PubMedCrossRefGoogle Scholar
  11. Bakker-Grunwald T (1977) ATPase. In: Trebst A and Avron M (eds) Encyclopedia of Plant Physiology, New Series, Vol 5, pp 369–373. Springer-Verlag, BerlinGoogle Scholar
  12. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31: 341–374CrossRefGoogle Scholar
  13. Carmeli C and Racker E (1973) Partial resolution of enzymes catalyzing photophosphorylation. XIV. Reconstitution of chlorophyll-deficient vesicles catalyzing phosphate-adenosine triphosphate exchange. J Biol Chem 248: 8281–8287PubMedGoogle Scholar
  14. Carrell CJ, Zhang H, Cramer WA and Smith JL (1997) Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein. Structure 5: 1613–1625PubMedCrossRefGoogle Scholar
  15. Chance B and Williams CR (1956) The respiratory chain and oxidative photophosphorylation. Adv Enzymol 17:65–134Google Scholar
  16. Deamer DW and Packer L (1969) Light-dependent anion transport in isolated spinach chloroplasts. Biochim Biophys Acta 172: 539PubMedCrossRefGoogle Scholar
  17. Dilley RA (1991) Energy coupling in chloroplasts: a calcium-gated switch controls proton fluxes between localized and delocalized proton gradients. Curr Topics Bioenerg 16: 265–318Google Scholar
  18. Dilley RA and Vernon LP (1965) Ion and water transport processes related to the light-dependent shrinkage of spinach chloroplasts. Arch Biochem Biophys 111: 365–373PubMedCrossRefGoogle Scholar
  19. Emerson R, Stauffer JS and Umbreit WW (1944) Relationships between photosynthesis and phosphorylation in Chlorella. Am J Bot 31: 107–120CrossRefGoogle Scholar
  20. Farron F (1970) Isolation and properties of a chloroplast coupling factor and heat-activated ATPase. Biochemistry 9: 3823–3828PubMedCrossRefGoogle Scholar
  21. Frenkel A (1954) Light-induced phosphorylation by cell-free preparations of photosynthetic bacteria. J Am Chem Soc 76: 5568–5569CrossRefGoogle Scholar
  22. Futai M, Noumi T and Maeda M (1989) ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu Rev Biochem 58: 111–136PubMedCrossRefGoogle Scholar
  23. Gest H and Kamen MD (1948) Studies on the phosphorus metabolism of green algae and purple bacteria in relation to photosynthesis. J Biol Chem 176: 299–318PubMedGoogle Scholar
  24. Good NE (1960) Activation of the Hill reaction by amines. Biochim Biophys Acta 40: 502–517PubMedCrossRefGoogle Scholar
  25. Hauska G, Reimer S and Trebst A (1974) Native and artificial energy-conserving sites in cyclic photophosphorylation systems. Biochim Biophys Acta 357: 1–13PubMedCrossRefGoogle Scholar
  26. Hauska G, Oettmeier W, Reimer S and Trebst A (1975) Energy conservation in photoreductions by Photosystem I. Shuttles of artificial electron donors for Photosystem I across the thylakoid membrane. Z Naturforsch C 30: 37–45PubMedGoogle Scholar
  27. Hightower KE and McCarty RE (1996) Influence of nucleotides on the cold stability of chloroplast coupling factor 1. Biochemistry 35: 10051–10057PubMedCrossRefGoogle Scholar
  28. Hind G and Jagendorf AT (1963) Separation of light and dark stages in photophosphorylation. Proc Nat Acad Sci USA 49: 715–722PubMedCrossRefGoogle Scholar
  29. Hind G and Jagendorf AT (1965) Light scattering changes associated with the production of a possible intermediate in photophosphorylation. J Biol Chem 240: 3195–3201PubMedGoogle Scholar
  30. Jackson JB and Crofts AR (1971) The kinetics of light induced carotenoid changes in Rhodopseudomonas spheroides and their relation to electrical field generation across the chromatophore membrane. Eur J Biochem 18: 120–130PubMedCrossRefGoogle Scholar
  31. Jagendorf AT (1962) Biochemistry of energy transformations during photosynthesis. In: Glass HB (ed) Survey of Biological Progress, Vol IV, pp 181–344. Academic Press, New YorkGoogle Scholar
  32. Jagendorf AT (1998) Chance, luck and photosynthesis research — an inside story. Photosynthesis Res 57: 215–229CrossRefGoogle Scholar
  33. Jagendorf AT and Hind G (1963) Studies on the mechanism of photophosphorylation, In: Kok B and Jagendorf AT (eds) Photosynthetic Mechanisms of Green Plants, pp 599–610. Publication 1145 of National Academy of Sciences-National Research Council, Washington, DCGoogle Scholar
  34. Jagendorf AT and Neumann J (1965) Effect of uncouplers on the light-induced pH rise with spinach chloroplasts. J Biol Chem 240: 3210–3214PubMedGoogle Scholar
  35. Jagendorf AT and Smith M (1962) Uncoupling phosphorylation in spinach chloroplasts by absence of cations. Plant Physiol 37: 135–141PubMedGoogle Scholar
  36. Jagendorf AT and Uribe E (1966) ATP formation caused by acidbase transition of spinach chloroplasts. Proc Nat Acad Sci USA 55: 170–177PubMedCrossRefGoogle Scholar
  37. Jagendorf AT, McCarty RE and Robertson D (1991) Coupling factor components: structure and function. In: Bogorad L and Vasil IK (eds) Cell Culture and Somatic Cell Genetics of Plants, Vol 7B, pp 225–254. Academic Press, New YorkGoogle Scholar
  38. Junesch U and Gräber P (1985) The rate of ATP synthesis as a function of DpH in normal and dithiothreitol-modified chloroplasts. Biochim Biophys Acta 809: 429–434CrossRefGoogle Scholar
  39. Junge W and Jackson JB (1982) The development of electrochemical potential gradients across photosynthetic membranes. In: Govindjee (ed) Photosynthesis: Energy Conversion by Plants and Bacteria, pp 589–646. Academic Press, New YorkGoogle Scholar
  40. Junge W and Witt HT (1968) On the ion transport system of photosynthesis. Investigations on a molecular level. Z Naturforsch 23b: 244–254Google Scholar
  41. Kamienietzky A and Nelson N (1975) Preparation and properties of chloroplasts depleted of chloroplast coupling factor 1 by sodium bromide treatment. Plant Physiol 55: 282–287PubMedGoogle Scholar
  42. Kandler O (1950) Über die Beziehungen zwischen Phosphathaushalt und Photosynthese. I. Phosphatspiegelschwenkungen bei Chlorella pyrenoidosa als Folde des Licht-Dunkel-Wechsels. Z Naturforsch 5b: 423–437Google Scholar
  43. Kobayashi Y, Neimanis S and Heber U (1995) Coupling ration H+/e = 3 vs H+/e = 2 in chloroplasts, and quantum requirements of oxygen exchange during the reduction of nitrite, ferricyanide or methylviologen. Plant Cell Physiol 6: 1613–1620Google Scholar
  44. Komatsu-Takaki M (1989) Energy-dependent conformational changes in the subunit of the chloroplast ATP synthase (CFoCF1). J Biol Chem 264: 17750–17753PubMedGoogle Scholar
  45. Krogmann DW, Jagendorf AT and Avron A (1959) Uncouplers of spinach chloroplast photosynthetic phosphorylation. Plant Physiol 34: 272–277PubMedGoogle Scholar
  46. Lardy HA and Wellman H (1952) Oxidative phosphorylations: role of inorganic phosphate and acceptorsystems in control of metabolic rates. J Biol Chem 195: 215–224PubMedGoogle Scholar
  47. Lien S and Racker E (1971) Partial resolution of the enzymes catalyzing photophosphorylation. VIII Properties of silico-tungstate treated particles. J Biol Chem 246: 4298–4307PubMedGoogle Scholar
  48. Loomis WF and Lipmann F (1948) Reversible inhibition of the coupling between phosphorylation and oxidation. J Biol Chem 173: 807–808PubMedGoogle Scholar
  49. Maclachlan GA and Porter HK (1959) Replacement of oxygen by light as the energy source for glucose metabolism in tobacco leaves. Proc Roy Soc London B 150: 460–473CrossRefGoogle Scholar
  50. McCarty RE (1969) The uncoupling of photophosphorylation by valinomycin and ammonium chloride. J Biol Chem 244: 4292–4298PubMedGoogle Scholar
  51. McCarty RE (1992) A plant biochemist’s view of H+-ATPases and ATP synthases. J Exp Bot 172: 431–441Google Scholar
  52. McCarty RE and Fagan J (1973) Light-stimulated incorporation of N-ethylmaleimide into coupling factor 1 in spinach chloroplasts. Biochem 12: 1503–1507CrossRefGoogle Scholar
  53. McCarty RE, Pittman PR and Tsuchiya Y (1972) Light-dependent inhibition of photophosphorylation by N-ethylmaleimide. J Biol Chem 247: 3048–3051PubMedGoogle Scholar
  54. Mehler AH (1951) Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33: 65–77CrossRefGoogle Scholar
  55. Miles CD and Jagendorf AT (1970) Evaluation of electron transport as the basis of ATP synthesis after acid-base transition by spinach chloroplasts. Biochemistry 9: 429–4341PubMedCrossRefGoogle Scholar
  56. Mills JD and Mitchell P (1984) Thiol modulation of the chloroplast protonmotive ATPase and its effect on photophosphorylation. Biochim Biophys Acta 764: 93–104CrossRefGoogle Scholar
  57. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature (London) 191: 144–148PubMedCrossRefGoogle Scholar
  58. Mitchell P (1975) The proton-motive Q cycle: a general formulation. FEBS Lett 59: 137–139PubMedCrossRefGoogle Scholar
  59. Morita S, Itoh S and Nishimura M (1983) Flash-induced photophosphorylation in chloroplasts with activated ATPase. Biochim Biophys Acta 724: 411–415CrossRefGoogle Scholar
  60. Moroney and McCarty RE (1982) Light-dependent cleavage of the g subunit of coupling factor 1 by trypsin causes activation of Mg2+ ATPase activity and uncoupling of photophosphorylation in spinach chloroplasts. J Biol Chem 257: 5915–5920PubMedGoogle Scholar
  61. Moroney JV, Lopresti L, McEwen BF, McCarty RE and Hammes GG (1983) The Mr value of chloroplast coupling factor 1. FEBS Lett 158: 58–62CrossRefGoogle Scholar
  62. Nelson N, Eytan E, Notsani B, Sigrist H, Sigrist-Nelson K and Gitler C (1977) Isolation of a chloroplast N,N’-dicyclohexylcarbodiimide-binding proteolipid, active in proton translocation. Proc Natl Acad Sci USA 74: 2375–2378PubMedCrossRefGoogle Scholar
  63. Neumann J and Jagendorf AT (1964) Light-induced pH changes related to phosphorylation by chloroplasts. Arch Biochem Biophys 107: 109–119PubMedCrossRefGoogle Scholar
  64. Ouitrakul R and Izawa S (1973) Electron transport and photophosphorylation in chloroplasts as a function of the electron acceptor. I. A receptor-specific inhibition by KCN. Biochim Biophys Acta 305: 105–118PubMedCrossRefGoogle Scholar
  65. Petrack B and Lipmann F (1961) Photophosphorylation and photohydrolysis in cell-free preparations of blue-green algae. In: McElroy WD and Glass HB (eds) Light and Life, pp 621–630. Johns Hopins Press, BaltimoreGoogle Scholar
  66. Pick U and Bassilian S (1981) Octyl glucoside stimulates a Mg2+-specific ATPase activity in chloroplast CF1. In: Selman BR and Selman-Reimer S (eds) Energy Coupling in Photosynthesis, pp 251–260. Elsevier/North Holland, AmsterdamGoogle Scholar
  67. Racker E (1970) Function and structure of the inner membranes of mitochondria and chloroplasts. In: Racker E (ed) Membranes of Mitochondria and Chloroplasts, pp 127–171. Van Nostrand Reinhold, New YorkGoogle Scholar
  68. Racker E and Stoeckenius W (1974) Reconstitution of purple membrane vesicles catalyzing light driven proton uptake and adenosine triphosphate formation. Biochemistry 20: 662–663Google Scholar
  69. Racker E, Hauska GA, Lien S, Berzborn RG and Nelson N (1972) Resolution and reconstitution of the system of photophosphorylation. In: Forti G (ed) Proceedings of the 2nd International Congress on Photosynthesis Research, Vol III, pp 1097–1112. Dr W Junk Publishers, The HagueGoogle Scholar
  70. Richter ML, Patrie WJ and McCarty RE (1984) Preparation of the e subunit and e-deficient chloroplast coupling factor 1 in reconstitutively active forms. J Biol Chem 259: 7371–7373PubMedGoogle Scholar
  71. Rottenberg H (1985) Proton-coupled energy conversion: chemiosmotic and intramembrane coupling. Modern Cell Biol. 4: 47–83Google Scholar
  72. Ruben S (1943) Photosynthesis and phosphorylation. J Am Chem Soc 65: 279–282CrossRefGoogle Scholar
  73. Rumberg B (1977) Field Changes. In: Trebst A and Avron M (eds) Encyclopedia of Plant Physiology, New Series, Vol 5, pp 405–415. Springer-Verlag, BerlinGoogle Scholar
  74. Ryrie I and Jagendorf AT (1971) An energy-linked conformational change in the coupling factor protein in chloroplasts. Studies with hydrogen exchange. J Biol Chem 246: 3771–3774PubMedGoogle Scholar
  75. Sakurai H, Shinohara K, Hisabori T and Shinohara K (1981) Enhancement of adenosine triphosphatase activity of purified chloroplast coupling factor 1. J Biochem (Tokyo) 90: 95–102PubMedGoogle Scholar
  76. Schwartz M (1968) Light induced proton gradient links electron transport and photophosphorylation. Nature (London) 219: 915–919PubMedCrossRefGoogle Scholar
  77. Schwink L (1956) Nachweis von Adenosinetriphosphosauer (ATP) in Grünalgen und Helodea sowie Einbau von radioaktivem Phosphor (32P) bei der Photosynthese. Planta 47: 165–218CrossRefGoogle Scholar
  78. Sebald W and Hoppe J (1981) On the structure and genetics of the proteolipid subunit of the ATP synthase complex. In: Sanadi DR (ed) Current Topics in Bioenergetics, Vol 12, pp 1–64. Academic Press, New YorkGoogle Scholar
  79. Shavit N, Skye GE and Boyer PD (1967) Occurrence and possible mechanism of 32P and 18O exchange reactions of photophosphorylation. J Biol Chem 242: 5125–5130PubMedGoogle Scholar
  80. Shen YK and Shen GM (1962) The’ light intensity effect’ and intermediate steps of photophosphorylation. Scientia Sinica 11: 1097–1106Google Scholar
  81. Simonis W and Grube KH (1952) Untersuchungen über den Zusammenhang von Phosphathaushalt und Photosynthese. Z Naturforsch 7b: 194–196Google Scholar
  82. Steele JA, Uchytil RF and Durbin RB (1978) The stimulation of coupling factor 1 ATPase by tentoxin. Biochim Biophys Acta 504: 136–141PubMedCrossRefGoogle Scholar
  83. Strehler BL (1953) Firefly luminescence in the study of energy transfer mechanisms. II. Adenosine triphosphate and photosynthesis. Arch Biochem Biophys 43: 67–79PubMedCrossRefGoogle Scholar
  84. Stroop SD and Boyer PD (1985) Characteristics of the ATP synthase as revealed by reaction at low ADP concentrations. Biochem 24: 2304–2310CrossRefGoogle Scholar
  85. Tagawa K, Tsujimoto HY and Arnon DI (1963) Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc Natl Acad Sci USA 49: 567–572PubMedCrossRefGoogle Scholar
  86. Telfer A, Barber J and Jagendorf AT (1980) Electrostatic control of chloroplast coupling factor binding to thylakoid membranes as indicated by cation effects on electron transport and reconstitution of photophosphorylation Biochim Biophys Acta 591: 331–345PubMedCrossRefGoogle Scholar
  87. Thayer WS and Hinkle PC (1975) Synthesis of adenosine triphosphate by an artificially imposed electrochemical proton gradient in bovine heart submitochondrial particles. J Biol Chem 250: 5330–5335PubMedGoogle Scholar
  88. Trebst A and Reimer S (1973) Properties of photoreductions by Photosystem II in isolated chloroplasts. An energy-conserving step in the photoreduction of benzoquinone by Photosystem II in the presence of dibromothymoquinone. Biochim Biophys Acta 305: 129–139PubMedCrossRefGoogle Scholar
  89. Uribe E and Jagendorf AT (1967) On the localization of organic acids in acid-induced ATP synthesis. Plant Physiol 42: 697–705PubMedCrossRefGoogle Scholar
  90. Vambutas VK and Racker E (1965) Partial resolution of the enzymes catalyzing photophosphorylation. I. Stimulation of photophosphorylation by a preparation of a latent, Ca2+-dependent adenosine triphosphatase from chloroplasts. J Biol Chem 240: 2660–2667PubMedGoogle Scholar
  91. Vambutas V, Beattie DS and Bittman R (1984) Isolation of chloride ion transport active protein(s) from thylakoid membranes. Arch Biochem Biophys 232: 538–548PubMedCrossRefGoogle Scholar
  92. Van Walraven HS, Strotmann H, Schwarz O and Rumberg B (1996) The H+/ATP coupling ratio of the ATP synthase from thiolmodulated chloroplasts and two cyanobacterial strains is four. FEBS Lett 379: 309–313PubMedCrossRefGoogle Scholar
  93. Wassink EC (1957) Phosphate in the photosynthetic cycle in Chlorella. In: Gaffron H, Brown AH, French CS, Livingston R, Rabinowitch E, Strehler BL and Tolbert NE (eds) Research in Photosynthesis, pp 333–339. Interscience, New YorkGoogle Scholar
  94. Williams AM (1956) Light-induced uptake of inorganic phosphate in cell-free extracts of obligately anaerobic photosynthetic bacteria. Biochim Biophys Acta 19: 570PubMedCrossRefGoogle Scholar
  95. Yoshida M, Muneyukis E and Hisabori T (2001) ATP synthase-a marvelous rotary engine of the cell. Nature Rev Mol Biol 2: 669–677CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • André T. Jagendorf
    • 1
  1. 1.Plant Biology DepartmentCornell UniversityIthacaUSA

Personalised recommendations