Ionic Effects on the Lateral Segregation of Chlorophyll-Proteins during Restacking of Thylakoid Membranes

  • Cecilia Sundby
  • Ulla K. Larsson
  • Bertil Andersson


The photosynthetic membrane of chloroplasts is differentiated into appressed and non-appressed (stroma exposed) areas. This structural differentiation is accompanied by a functional heterogeneity in the lateral plane of the membrane1. The photosystem 1 complex and the ATP synthase are mainly excluded from the appressed membrane regions and localized in the non-appressed regions. Most of the photosystem 2 complexes and its light-harvesting chlorophyll a/b complex (LHC-II) is located in the appressed regions. This lateral segregation of the thylakoid protein complexes has been postulated to involve repulsive electrostatic and attractive van der Waals forces at closely appressed membrane surfaces2. Under low salt conditions the thylakoid membranes destack and the membrane components are randomized along the membrane3. Readdition of cations reverses this process and restacking accompanied by lateral segregation of the complexes occurs.


Thylakoid Membrane Stroma Lamella Lateral Segregation Intact Thylakoid Control Thylakoid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    J.M. Anderson and B. Andersson, The architecture of photosynthetic membranes: lateral and transverse organization, Trends Biochem. Sci. 7: 288 (1982)CrossRefGoogle Scholar
  2. 2.
    J. Barber, Influence of surface charges on thylakoid structure and function, Annu. Rev. Plant Physiol. 33: 261 (1982)CrossRefGoogle Scholar
  3. 3.
    L.A. Staehelin, Reversible particle movements associated with un-stacking and restacking of chloroplast membranes in vitro, J. Cell. Biol. 71: 136 (1976)CrossRefGoogle Scholar
  4. 4.
    L.A. Staehelin and C.J. Arntzen, Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components, J. Cell Biol. 97: 1327 (1983).CrossRefGoogle Scholar
  5. 5.
    P.V. Sane, D.J. Goodchild and R.B. Park, Characterization of chloroplast photosystem 1 and 2 separated by a non-detergent method, Biochim. Biophys. Acta 216: 162 (1970).CrossRefGoogle Scholar
  6. 6.
    B. Andersson, C. Sundby, H.-E. Akerlund and P.-A. Albertsson, Inside-out thylakoid vesicles: important tools for the characterization of the photosynthetic membrane, Physiol. Plant. in press (1985).Google Scholar
  7. 7.
    B. Andersson, C. Sundby and P.-A. Albertsson, A mechanism for the formation of inside-out membrane vesicles, Biochim. Biophys. Acta 599: 391 (1980).CrossRefGoogle Scholar
  8. 8.
    B. Andersson and H.-E. Akerlund, Inside-out membrane vesicles isolated from spinach thylakoids, Biochim. Biophys. Acta 503: 462 (1978).CrossRefGoogle Scholar
  9. 9.
    D.J. Arnon, Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris, Plant Physiol. 24: 1 (1949).CrossRefGoogle Scholar
  10. 10.
    J.M. Anderson, J.C. Waldron and S.W. Thorne, Chlorophyll-protein complexes of spinach and barley thylakoids, FEBS Lett. 92: 227 (1978).CrossRefGoogle Scholar
  11. 11.
    J.E. Mullet and G.J. Arntzen, Simulation of grana stacking in a model membrane system, Biochim. Biophys. Acta 589: 100 (1980).CrossRefGoogle Scholar
  12. 12.
    I.J. Ryrie, Freeze-fracture analysis of membrane appression and protein segregation in model membranes containing the chlorophyll-protein complexes from chloroplasts, Eur. J. Biochem. 137: 203 (1983).CrossRefGoogle Scholar
  13. 13.
    J.M. Briantais, C. Vernotte, J. Olive and F.-A. Wollman, Kinetics of cation-induced changes of photosystem II fluorescence and of lateral distribution of the two photosytems in the thylakoid membranes of pea chloroplasts, Biochim. Biophys. Acta 766: 1 (1984).CrossRefGoogle Scholar
  14. 14.
    D.J. Kyle, L.A. Staehelin and C.J. Arntzen, Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants, Arch. Biochem. Biophys. 222: 527 (1983).CrossRefGoogle Scholar
  15. 15.
    L.A. Staehelin and M. DeWit, Correlation of structure and function of chloroplast membranes at the supramolecular level, J. Cell Biochem. 24: 261 (1984).CrossRefGoogle Scholar
  16. 16.
    P. Rand, Interacting phospholipid bilayers: Measured forces and induced structural changes, Annu. Rev. Biophys. Bioeng. 10: 277 (1981).CrossRefGoogle Scholar
  17. 17.
    J.T. Duniec, J.N. Israelachvilli, B.W. Ninham, R.M. Pashley and S.W. Thorne, An ion-exchange model for thylakoid stacking in chloroplasts, FEBS Lett. 129: 193 (1981).CrossRefGoogle Scholar
  18. 18.
    H.-E. Akerlund, B. Andersson, A. Persson and P.-A. Albertsson, Isoelectric points of spinach thylakoid membrane surfaces as determined by cross partition, Biochim. Biophys. Acta 552: 238 (1979).CrossRefGoogle Scholar
  19. 19.
    P.D. Gerola, R.C. Jennings, G. Forti and F.M. Garlaschi, Influence of protons on thylakoid membrane stacking, Plant Sci. Lett. 16: 249 (1979).CrossRefGoogle Scholar
  20. 20.
    J. Barber, An explanation for the relationship between salt-induced thylakoid stacking and the chlorophyll fluorescence changes associated with changes in spillover of energy from photosystem 1 to photosystem 11, FEBS Lett. 118: 1 (1980).CrossRefGoogle Scholar
  21. 21.
    J. Bennet, Phosphorylation of chloroplast membrane polypeptides, Nature 269: 344 (1977).CrossRefGoogle Scholar
  22. 22.
    U.K. Larsson, B. Jergil and B. Andersson, Changes in the lateral distribution of the light-harvesting chlorophyll-a/b-protein complex induced by its phosphorylation, Eur. J. Biochem. 136: 25 (1983).CrossRefGoogle Scholar
  23. 23.
    D.J. Kyle, T.-Y. Kuang, J.L. Watson and C.J. Arntzen, Movement of a sub-population of the light-harvesting complex (LHC-II) from grana to stroma lamellae as a consequence of its phosphorylation, Biochim. Biophys. Acta 765: 89 (1984).CrossRefGoogle Scholar
  24. 24.
    A. Telfer, M. Hodges, P.A. Millner and J. Barber, The cation-dependence of the degree of protein phosphorylation-induced unstacking of pea thylakoids, Biochim. Biophsy. Acta 766: 554 (1984).CrossRefGoogle Scholar
  25. 25.
    F.-A. Wollman and B.A. Diner, Cation-control of fluorescence emission, light scatter and membrane stacking in pigment mutants of Chlamydomonas reinhardi, Arch. Biochem. Biophys. 201: 646 (1980).CrossRefGoogle Scholar
  26. 26.
    J.H. Argyroudi-Akoyunoglou, Effect of cations on the reconstitution of heavy subchloroplast fractions (grana) in disorganized low-salt agranal chloroplasts, Arch. Biochem. Biophys. 176: 267 (1976).CrossRefGoogle Scholar
  27. 27.
    W.S. Chow and J. Barber, Further studies of the relationship between cation-induced chlorophyll fluorescence and thylakoid membrane stacking changes, Biochim. Biophys. Acta 593: 149 (1980).CrossRefGoogle Scholar
  28. 28.
    H.-E. Akerlund, B. Andersson and P.-A. Albertsson, Isolation of photosystem II enriched membrane vesicles from spinach chloroplasts by phase partition, Biochim. Biophys. Acta 449: 525 (1976).CrossRefGoogle Scholar
  29. 29.
    C. Tanford, “The hydrophobic effect”, Wiley-Interscience, New York (1973).Google Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • Cecilia Sundby
    • 1
  • Ulla K. Larsson
    • 1
  • Bertil Andersson
    • 1
  1. 1.Department of BiochemistryUniversity of LundLundSweden

Personalised recommendations