Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Changes in topography and function of thylakoid membranes following membrane protein phosphorylation

Abstract

Changes in topography and function of pea (Pisum sativum L.) thylakoid membrane fractions following membrane protein phosphorylation have been studied. After protein phosphorylation the stromal membrane fraction had a higher chlorophyll a/b ratio, an increased content of light-harvesting chlorophyll protein and a higher ratio of chlorophyll to cytochrome f. This indicates that a pool of light-harvesting chlorophyll protein migrates from the photosystem II-enriched grana regions to the photosystem I-enriched stroma lamellae, in agreement with Kyle et al. (1984, Biochim. Biophys. Acta 765, 89–96) and Larsson et al. (1983, Eur. J. Biochem. 136, 25–29). Phosphorylation caused a stimulation in the rate of light-limited photosystem-I electron transfer in the unappressed membrane fraction, indicating that the translocated LHC-II becomes functionally associated with photosystem I.

This is a preview of subscription content, log in to check access.

Abbreviations

Fm:

fluorescence yield when all traps are closed

Fo:

fluorescence yield when all traps are open

Fv:

Fm-Fo

LHC-II:

light-harvesting chlorophyll protein associated with photosystem II

PSI, II:

photosystem I, II

P700:

primary donor of PSI

References

  1. Anderson, J.M., Melis, A. (1984) Localization of different photosystems in separate regions of chloroplast membranes. Proc. Natl. Acad. Sci. USA 80, 745–749

  2. Anderson, J.M., Waldron, J.C., Thorne, S.W. (1978) Chlorophyll-protein complexes of spinach and barley thylakoids. FEBS. Lett. 92, 227–233

  3. Andersson, B., Anderson, J.M. (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim. Biophys. Acta 539, 427–440

  4. Barber, J. (1982) The control of membrane organisation by electrostatic forces. Biosci. Rep. 2, 1–13

  5. Barber, J. (1983) Membrane conformational changes due to phosphorylation and the control of energy transfer in photosynthesis. Photochem. Photobiophys. 5, 181–190

  6. Barber, J. (1985) Thylakoid membrane structure and organisation of electron transport components. In: Photosynthetic mechanisms and the environment, pp. 91–134, Barber, J., Baker, N.R., eds. Elsevier Biomedical Press, Amsterdam

  7. Biggins, J. (1982) Thylakoid conformational changes accompanying membrane protein phosphorylation. Biochim. Biophys. Acta 679, 479–482

  8. Black, M.T. (1985) Phosphorylation of thylakoid proteins and the distribution of excitation energy in pea chloroplasts. Ph.D. thesis, University of Sheffield, UK

  9. Black, M.T., Foyer, C.H., Horton, P. (1984) An investigation into the ATP requirement for phosphorylation of thylakoid proteins and for the ATP-induced decrease in the yield of chlorophyll fluorescence in chloroplasts at different stages of development. Biochim. Biophys. Acta 767, 557–562

  10. Black, M.T., Horton, P. (1984) An investigation into the mechanistic aspects of excitation energy redistribution following thylakoid membrane protein phosphorylation. Biochim. Biophys. Acta 767, 568–573

  11. Bonaventura, C., Myers, J. (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim. Biophys. Acta 189, 363–383

  12. Canaani, O., Malkin, S. (1984) Distribution of light excitation in an intact leaf between the two photosystems of photosynthesis. Changes in absorption cross-sections following state 1-state 2 transitions. Biochim. Biophys. Acta 766, 513–524

  13. Cramer, W.A., Horton, P., Donnell, J.J. (1974) Inhibition of chemical oxidation and reduction of cytochromes f and b 559 by carbonylcyanide p-trifluoromethoxy phenylhydrazone. Biochim. Biophys. Acta 368, 361–370

  14. Cramer, W.A., Whitmarsh, J. (1977) Photosynthetic cytochromes. Annu. Rev. Plant Physiol. 28, 133–172

  15. Farchaus, J.W., Widger, W.R., Cramer, W.A., Dilley, R.A. (1982) Kinase induced changes in electron transport rates of spinach chloroplasts. Arch. Biochem. Biophys. 271, 362–367

  16. Haworth, P., Kyle, D.J., Arntzen, C.J. (1982) Protein phosphorylation and excitation energy distribution in normal, ImL grown and a chlorophyll b-less mutant of barley. Arch. Biochem. Biophys. 218, 199–206

  17. Haworth, P., Melis, A. (1983) Phosphorylation of chloroplast thylakoid membrane proteins does not increase the absorption cross-section of PSI. FEBS Lett. 160, 277–280

  18. Haworth, P., Watson, J.L., Arntzen, C.J. (1983) The detection, isolation and characterisation of a light-harvesting complex which is specifically associated with PSI. Biochim. Biophys. Acta 724, 151–158

  19. Horton, P. (1983) Control of chloroplast electron transport by phosphorylation of thylakoid proteins. FEBS Lett. 152, 47–52

  20. Horton, P. (1985a) Regulation of photochemistry and its interaction with carbon metabolism. In: Regulation of sources and sinks in crop plants (Monograph 12) pp. 19–33. Jeffcoat, B., Hawkins, A.F., Stead, A.D., eds. British Plant Growth Regulator Group, Bristol

  21. Horton, P. (1985b) Interactions between electron transfer and carbon assimilation. In: Photosynthetic mechanisms and the environment, pp. 135–187, Barber, J., Baker, N.R. eds. Elsevier Science Publishers B.V. (Biomedical Division), Amsterdam

  22. Horton, P., Black, M.T. (1980) Activation of adenosine triphosphate-induced quenching of chlorophyll fluorescence by reduced plastoquinone. The basis of the state I-state II transition in chloroplast. FEBS Letters 119, 141–144

  23. Horton, P., Black, M.T. (1981a) Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by ATP. Biochim. Biophys. Acta 635, 53–62

  24. Horton, P., Black, M.T. (1981b) Light-induced redox changes in chloroplast cytochrome f after phosphorylation of membrane proteins. FEBS Lett. 132, 75–77

  25. Horton, P., Black, M.T. (1982) On the nature of the fluorescence decrease due to phosphorylation of chloroplast membrane proteins. Biochim. Biophys. Acta 680, 22–27

  26. Horton, P., Black, M.T. (1983) A comparison between cation and protein phosphorylation effects on the fluorescence induction curve in chloroplasts treated with 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Biochim. Biophys. Acta 722, 214–218

  27. Horton, P., Croze, E. (1977) The relationship between the activity of chloroplast photosystem II and the mid-point oxidation reduction potential of cytochrome b-559. Biochim. Biophys. Acta 462, 86–101

  28. Krause, G.H., Behrend, U. (1983) Characterisation of chlorophyll fluorescence quenching in chloroplasts by fluorescence spectroscopy at 77K. II. ATP-dependent quenching. Biochim. Biophys. Acta 723, 176–181

  29. Kyle, D.J., Haworth, P., Arntzen, C.J. (1982) Thylakoid membrane protein phosphorylation leads to a decrease in connectivity between PS2 reaction centres. Biochim. Biophys. Acta 680, 336–342

  30. Kyle, D.J., Kuang, T.-Y., Watson, J.L., Arntzen, C.J. (1984) Movement of a sub-population of LHC-II from grana to stroma lamellae as a consequence of its phosphorylation. Biochim. Biophys. Acta 765, 89–96

  31. Kyle, D.J., Staehelin, L.A., Arntzen, C.J. (1983) Lateral mobility of the light-harvesting chlorophyll protein in chloroplast membranes controls excitation energy distribution in higher plants. Arch. Biochem. Biophys. 222, 527–541

  32. Larsson, U.K., Jergil, B., Andersson, B. (1983) Changes in the lateral distribution of the LHC a/b protein complex induced by its phosphorylation. Eur. J. Biochem. 136, 25–29

  33. Markwell, J.P., Baker, N.R., Bradbury, M., Thorber, J.P. (1984) Use of zinc ions to study thylakoid protein phosphorylation and the state 1 to state 2 transition in vitro. Plant Physiol. 74, 348–354

  34. Simpson, D.J. (1983) Freeze-fracture studies on barley plastid membranes. VII. Structural changes associated with phosphorylation of the LHC. Biochim. Biophys. Acta 725, 113–120

  35. Staehelin, L.A., Arntzen, C.J. (1983) Regulation of chloroplast membrane function: Protein phosphorylation changes the spatial organisation of membrane components. J. Cell. Biol. 97, 1327–1337

  36. Steinback, K.E., Bose, S., Kyle, D.J. (1982) Phosphorylation of the light-harvesting chlorophyll protein regulates excitation energy distribution between PS2 and PS1. Arch. Biochem. Biophys. 216, 356–361

  37. Telfer, A., Hodges, M., Millner, P.A., Barber, J. (1984a) The cation-dependence of the degree of protein phosphorylation-induced unstacking of pea thylakoids. Biochim. Biophys. Acta 766, 554–562

  38. Telfer, A., Bottin, H., Barber, J., Mathis, P. (1984b) The effect of magnesium and phosphorylation of the light-harvesting chlorophyll a/b protein on the yield of P700 photooxidation in pea chloroplasts. Biochim. Biophys. Acta 764, 324–330

  39. Whitmarsh, J., Ort, D.R. (1984) Stoichiometries of electron transport complexes in spinach chloroplast. Arch. Biochem. Biophys. 231, 378–389

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Black, M.T., Lee, P. & Horton, P. Changes in topography and function of thylakoid membranes following membrane protein phosphorylation. Planta 168, 330–336 (1986). https://doi.org/10.1007/BF00392357

Download citation

Key words

  • Chlorophyll protein complex
  • Photosystem I, II
  • Pisum (thylakoid)
  • Protein kinase
  • Thylakoid fractionation