Skip to main content
SpringerLink
Log in

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

  • Published:
Planta Aims and scope Submit manuscript

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 via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

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

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Author notes

  1. M. T. Black

    Present address: Department of Biological Sciences, Purdue University, 47907, West Lafayette, Indiana, USA

Authors and Affiliations

  1. Research Institute for Photosynthesis, University of Sheffield, S10 2TN, Sheffield, UK

    M. T. Black, P. Lee & P. Horton

  2. Department of Biochemistry, University of Sheffield, S10 2TN, Sheffield, UK

    M. T. Black, P. Lee & P. Horton

Authors
  1. M. T. Black
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Horton
    View author publications

    You can also search for this author in PubMed Google Scholar

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

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00392357

Key words

Search

Navigation