Photosynthesis Research

, 73:139 | Cite as

Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications

  • John F. Allen
Article

Abstract

Chloroplast thylakoid protein phosphorylation was discovered, and the most conspicuous phosphoproteins identified, by John Bennett at Warwick University. His initial findings were published in 1977. The phosphoproteins included apoproteins of chloroplast light harvesting complex II. Thylakoid protein phosphorylation was shown to influence distribution of excitation energy between Photosystems I and II in 1979, during a visit by Bennett to the laboratory of Charles J. Arntzen at the University of Illinois at Urbana-Champaign. That work was published by Bennett, Katherine E. Steinback and Arntzen in 1980. Control of both protein phosphorylation and excitation energy distribution by the redox state of the plastoquinone pool was first established in 1980 during the author's visit to Arntzen's laboratory. The experiments were prompted by the realization that coupling between redox state of an inter-photosystem electron carrier and excitation energy distribution provides a concrete mechanism for adaptations known as state transitions. This work was published by Allen, Bennett, Steinback, and Arntzen in 1981. This discovery and its background are discussed, together with some implications for photosynthesis and for research generally. This minireview is a personal account of the Urbana-Warwick and related collaborations in 1979–83: it includes impressions, conjectures, and acknowledgements for which the author is solely responsible.

John F. Allen Charles J. Arntzen John Bennett Robert Emerson enhancement Peter Horton light harvesting complex II photosystem plastoquinone protein phosphorylation redox control state transitions Katherine E. Steinback Alison Telfer W. Patrick Williams 

References

  1. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335PubMedCrossRefGoogle Scholar
  2. Allen JF and Bennett J (1981) Photosynthetic protein phosphorylation in intact chloroplasts. Inhibition by DCMU and by the onset of CO2-fixation. FEBS Lett 123: 67–70CrossRefGoogle Scholar
  3. Allen JF and Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6: 317–326PubMedCrossRefGoogle Scholar
  4. Allen JF and Horton P (1981) Chloroplast protein phosphorylation and chlorophyll fluorescence quenching. Activation by tetramethyl-p-hydroquinone, an electron donor to plastoquinone. Biochim Biophys Acta 638: 290–295CrossRefGoogle Scholar
  5. Allen JF, Bennett J, Steinback KE and Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291: 25–29CrossRefGoogle Scholar
  6. Barraclough R and Ellis RJ (1980) Protein synthesis in chloroplasts. IX. Assembly of newly-synthesized large subunits into ribulose bisphosphate carboxylase in isolated intact pea chloroplasts. Biochim Biophys Acta 608: 19–31PubMedGoogle Scholar
  7. Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269: 344–346CrossRefGoogle Scholar
  8. Bennett J (1979a) Chloroplast phosphoproteins. The protein kinase of thylakoid membranes is light-dependent. FEBS Lett 103: 342–344PubMedCrossRefGoogle Scholar
  9. Bennett J (1979b) Chloroplast phosphoproteins: phosphorylation of polypeptides of the light-harvesting chlorophyll protein complex. Eur J Biochem 99: 133–137PubMedCrossRefGoogle Scholar
  10. Bennett J (1980) Chloroplast phosphoproteins: evidence for a thylakoid-bound phosphoprotein phosphatase. Eur J Biochem 104: 85–89PubMedCrossRefGoogle Scholar
  11. Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42: 281–331CrossRefGoogle Scholar
  12. Bennett J, Steinback KE and Arntzen CJ (1980) Chloroplast phosphoproteins: regulation of excitation energy transfer by phosphorylation of thylakoid membrane polypeptides. Proc Natl Acad Sci USA 77: 5253–5257PubMedCrossRefGoogle Scholar
  13. Bonaventura C and Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189: 366–383PubMedCrossRefGoogle Scholar
  14. Buchanan BB (1991) Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys 288: 1–9PubMedCrossRefGoogle Scholar
  15. Butler WL (1976) Energy distribution in the photosynthetic apparatus of plants. Brookhaven Symp Biol 28: 338–346PubMedGoogle Scholar
  16. Cuming AC and Bennett J (1981) Biosynthesis of the lightharvesting chlorophyll a/b protein. Control of messenger RNA activity by light. Eur J Biochem 118: 71–80PubMedCrossRefGoogle Scholar
  17. Duysens LNM (1972) 3-(3,4-Dichlorophenyl)-1,1-dimethyurea (DCMU) inhibition of system II and light-induced regulatory changes in energy transfer efficiency. Biophys J 12: 858–863PubMedCrossRefGoogle Scholar
  18. Emerson R and Rabinowitch E (1960) Red drop and role of auxiliary pigments in photosynthesis. Plant Physiol 35: 477–485PubMedGoogle Scholar
  19. Emerson R, Chalmers RV and Cederstrand CN (1957) Some factors influencing the long-wave limit of photosynthesis. Proc Natl Acad Sci USA 43: 133–14PubMedCrossRefGoogle Scholar
  20. Govindjee (1999) On the requirement of minimum number of four versus eight quanta of light for the evolution of one molecule of oxygen in photosynthesis: a historical note. Photosynth Res 59: 249–254CrossRefGoogle Scholar
  21. Govindjee and Rabinowitch E (1960) Two forms of chlorophyll a with distinct photochemical functions. Science 132: 355–356PubMedGoogle Scholar
  22. Govindjee R, Govindjee and Hoch G (1964) Emerson enhancement effect in chloroplast reactions. Plant Physiol 39: 10–14PubMedGoogle Scholar
  23. Horton P and Black MT (1980) Activation of adenosine-5?-triphosphate quenching of chlorophyll fluorescence by reduced plastoquinone. The basis of state I-state II transitions in chloroplasts. FEBS Lett 119: 141–144CrossRefGoogle Scholar
  24. Horton P and Black MT (1981) Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by adenosine-5?-triphosphate. Biochim Biophys Acta 635: 53–62PubMedCrossRefGoogle Scholar
  25. Horton P, Allen JF, Black MT and Bennett J (1981) Regulation of phosphorylation of chloroplast membrane polypeptides by the redox state of plastoquinone. FEBS Lett 125: 193–196CrossRefGoogle Scholar
  26. Murata N (1969a) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172: 242–251PubMedCrossRefGoogle Scholar
  27. Murata N (1969b) Control of excitation transfer in photosynthesis. II. Magnesium ion-dependent distribution of excitation energy between two pigment systems in spinach chloroplasts. Biochim Biophys Acta 189: 171–181PubMedCrossRefGoogle Scholar
  28. Myers J (1971) Enhancement studies in photosynthesis. Annu Rev Plant Physiol 22: 289–312CrossRefGoogle Scholar
  29. Pfannschmidt T, Nilsson A and Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397: 625–628CrossRefGoogle Scholar
  30. Pfister K, Steinback KE, Gardner G and Arntzen CJ (1981) Photoaffinity labeling of an herbicide receptor protein in chloroplast membranes. Proc Natl Acad Sci USA 78: 981–985PubMedCrossRefGoogle Scholar
  31. Ried A and Reinhardt B (1980) Distribution of excitation energy between Photosystem I and Photosystem II in red algae. III. Quantum requirements of the induction of a state 2-state 1 transition. Biochim Biophys Acta 592: 76–86PubMedCrossRefGoogle Scholar
  32. Saito K, Williams WP, Allen JF and Bennett J (1983) Comparison of ATP-induced and state 1-state 2 related changes in excitation energy distribution in Chlorella vulgaris. Biochim Biophys Acta 724: 94–103CrossRefGoogle Scholar
  33. Somerville CR and Ogren WL (1982) Mutants of the cruciferous plant Arabidopsis thaliana lacking glycine decarboxylase activity. Biochem J 202: 373–380PubMedGoogle Scholar
  34. Staehelin LA and Arntzen CJ (1979) Effects of ions and gravity forces on the supramolecular organization and excitation energy distribution in chloroplast membranes. In: Chlorophyll Organization and Energy Transfer in Photosynthesis. Ciba Foundation Symposium 61 (new series), pp 147–175. Elsevier/North Holland, AmsterdamGoogle Scholar
  35. Telfer A, Allen JF, Barber J and Bennett J (1983) Thylakoid protein phosphorylation during state 1-state 2 transitions in osmotically shocked pea chloroplasts. Biochim Biophys Acta 722: 176–181CrossRefGoogle Scholar
  36. The Times (May 11, 1981) Science report. Biology: How plants respond to colour (p. 16)Google Scholar
  37. Whatley FR (1995) Photosynthesis by isolated chloroplasts: the early work in Berkeley. Photosynth Res 46: 17–26CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • John F. Allen
    • 1
  1. 1.Plant BiochemistryLund UniversityLundSweden

Personalised recommendations