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PMID: 6355117 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S. Review

Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components.

The Journal of cell biology ·Vol. 97 ·No. 5 Pt 1 ·1983-11-00 ·Pages 1327-37

Staehelin LA, Arntzen CJ

Abstract

A chlorophyll-protein complex of chloroplast membranes, which simultaneously serves as light-harvesting antenna and membrane adhesion factor, undergoes reversible, lateral diffusion between appressed and nonappressed membrane regions under the control of a protein kinase. The phosphorylation-dependent migration process regulates the amount of light energy that is delivered to the reaction centers of photosystems I and II (PS I and PS II), and thereby regulates their rate of turnover. This regulatory mechanism provides a rationale for the finding that the two photosystems are physically separated in chloroplast membranes (PS II in appressed, grana membranes, and PS I in nonappressed, stroma membranes). The feedback system involves the following steps: a membrane-bound kinase senses the rate of PS II vs. PS I turnover via the oxidation-reduction state of the plastoquinone pool, which shuttles electrons from PS II via cytochrome f to PS I. If activated, the kinase adds negative charge (phosphate) to a grana-localized pigment-protein complex. The change in its surface charge at a site critical for promoting membrane adhesion results in increased electrostatic repulsion between the membranes, unstacking, the lateral movement of the complex to adjacent stroma membranes, which differ in their functional composition. The general significance of this type of membrane regulatory mechanism is discussed.

MeSH Terms
Cell Membrane/physiology Chloroplasts/ultrastructure Electrophoresis, Polyacrylamide Gel Light-Harvesting Protein Complexes Membrane Proteins/metabolism Microscopy, Electron Molecular Weight Phosphorylation Photosynthetic Reaction Center Complex Proteins Plant Proteins/metabolism
Chemicals
Light-Harvesting Protein Complexes Membrane Proteins Photosynthetic Reaction Center Complex Proteins Plant Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Staehelin L A
Arntzen C J
References (45)
45 references, click to expand
  1. Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by adenosine 5'-triphosphate.
    Biochim Biophys Acta. 1981 Mar 12;635(1):53-62 PMID: 7213677
  2. Control of light-activated phosphorylation in frog photoreceptor membranes.
    Biochemistry. 1977 Jun 14;16(12):2633-9 PMID: 302121
  3. Isolation of highly active photosystem II particles from a mutant of Chlamydomonas reinhardtii.
    Eur J Biochem. 1980 Sep;110(2):521-6 PMID: 7439172
  4. Organization of the photosystem II centers and their associated antennae in the thylakoid membranes: a comparative ultrastructural, biochemical, and biophysical study of Chlamydomonas wild type and mutants lacking in photosystem II reaction centers.
    J Cell Biol. 1980 Dec;87(3 Pt 1):728-35 PMID: 7462323
  5. The stacking of chloroplast thylakoids. Effects of cation screening and binding, studied by the digitonin method.
    Arch Biochem Biophys. 1980 Apr 15;201(1):347-55 PMID: 7396509
  6. Reconstruction of the chloroplast noncyclic electron transport pathway from water to NADP with three integral protein complexes.
    Proc Natl Acad Sci U S A. 1982 Sep;79(18):5494-8 PMID: 16593225
  7. Adhesion between liposomes mediated by the chlorophyll a/b light-harvesting complex isolated from chloroplast membranes.
    J Cell Biol. 1980 Jan;84(1):40-56 PMID: 7350170
  8. Kinase-induced changes in electron transport rates of spinach chloroplasts.
    Arch Biochem Biophys. 1982 Aug;217(1):362-7 PMID: 7125674
  9. Structure of the Thylakoids and Envelope Membranes of the Cyanelles of Cyanophora paradoxa.
    Plant Physiol. 1983 Feb;71(2):409-19 PMID: 16662839
  10. Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum.
    Biochim Biophys Acta. 1969 Feb 25;172(2):242-51 PMID: 5775694
  11. Phosphorylation of the light-harvesting chlorophyll-protein regulates excitation energy distribution between photosystem II and photosystem I.
    Arch Biochem Biophys. 1982 Jun;216(1):356-61 PMID: 7049089
  12. Analysis of the thylakoid outer surface. Coupling factor is limited to unstacked membrane regions.
    J Cell Biol. 1976 Jan;68(1):30-47 PMID: 812874
  13. Chloroplast phosphoproteins. Phosphorylation of polypeptides of the light-harvesting chlorophyll protein complex.
    Eur J Biochem. 1979 Aug 15;99(1):133-7 PMID: 488114
  14. Involvement of the light-harvesting complex in cation regulation of excitation energy distribution in chloroplasts.
    Arch Biochem Biophys. 1978 Apr 15;187(1):252-63 PMID: 655723
  15. Chemistry of visual adaptation in the rat.
    Nature. 1960 Oct 8;188:114-8 PMID: 13724150
  16. Proteolysis of chloroplast thylakoid membranes. II. Evidence for the involvement of the light-harvesting chlorophyll a/b-protein complex in thylakoid stacking and for effects of magnesium ions on photosystem II-light-harvesting complex aggregates in the absence of membrane stacking.
    Arch Biochem Biophys. 1980 Apr 1;200(2):374-86 PMID: 7002041
  17. Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants.
    Arch Biochem Biophys. 1983 Apr 15;222(2):527-41 PMID: 6847199
  18. The role of the light-harvesting chlorophyll a/b protein complex in chloroplast membrane stacking. Cation-induced aggregation of reconstituted proteoliposomes.
    Eur J Biochem. 1980 Jun;107(2):345-54 PMID: 7398645
  19. Protein phosphorylation and excitation energy distribution in normal intermittent-light-grown, and a chlorophyll b-less mutant of barley.
    Arch Biochem Biophys. 1982 Oct 1;218(1):199-206 PMID: 7149726
  20. The distribution and proportions of vitamin A compounds during the visual cycle in the rat.
    Vision Res. 1974 Sep;14(9):795-802 PMID: 4418913
  21. Chlorophyll proteins of photosystem I.
    Plant Physiol. 1980 May;65(5):814-22 PMID: 16661288
  22. Phosphorylation of chlamydomonas reinhardi chloroplast membrane proteins in vivo and in vitro.
    J Cell Biol. 1982 Jun;93(3):712-8 PMID: 6811597
  23. Structural analysis of the isolated chloroplast coupling factor and the N,N'-dicyclohexylcarbodiimide binding proteolipid.
    Biochim Biophys Acta. 1981 Mar 20;642(1):149-57 PMID: 6452905
  24. Phycobilisomes: structure and dynamics.
    Annu Rev Microbiol. 1982;36:173-98 PMID: 6816134
  25. Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro.
    J Cell Biol. 1976 Oct;71(1):136-58 PMID: 988028
  26. The stacking of chloroplast thylakoids. Quantitative analysis of the balance of forces between thylakoid membranes of chloroplasts, and the role of divalent cations.
    Arch Biochem Biophys. 1980 Apr 15;201(1):339-46 PMID: 7396508
  27. Environmental control of photosynthetic enhancement.
    Science. 1971 Jan 22;171(3968):284-6 PMID: 5538840
  28. A chloroplast membrane lacking photosystem I. Changes in unstacked membrane regions.
    Biochim Biophys Acta. 1980 Aug 5;592(1):143-52 PMID: 7397137
  29. Simulation of grana stacking in a model membrane system. Mediation by a purified light-harvesting pigment-protein complex from chloroplasts.
    Biochim Biophys Acta. 1980 Jan 4;589(1):100-17 PMID: 7356975
  30. Chloroplast phosphoproteins. The protein kinase of thylakoid membranes is light-dependent.
    FEBS Lett. 1979 Jul 15;103(2):342-4 PMID: 467680
  31. Evidence for a respiratory chain in the chloroplast.
    Proc Natl Acad Sci U S A. 1982 Jul;79(14):4352-6 PMID: 16593210
  32. Reconstitution of cytochrome f/b6 and CF0-CF1 ATP synthetase complexes into phospholipid and galactolipid liposomes.
    J Cell Biol. 1983 Aug;97(2):301-10 PMID: 6193124
  33. Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts.
    Biochim Biophys Acta. 1980 Dec 3;593(2):427-40 PMID: 7236643
  34. Energy transfer: a spectroscopic ruler.
    Proc Natl Acad Sci U S A. 1967 Aug;58(2):719-26 PMID: 5233469
  35. Effect of Salts and Electron Transport on the Conformation of Isolated Chloroplasts. II. Electron Microscopy.
    Plant Physiol. 1966 Mar;41(3):544-52 PMID: 16656286
  36. Evidence for the role of surface-exposed segments of the light-harvesting complex in cation-mediated control of chloroplast structure and function.
    Arch Biochem Biophys. 1979 Jul;195(2):546-57 PMID: 475400
  37. Fluorescence and oxygen evolution from Chlorella pyrenoidosa.
    Biochim Biophys Acta. 1969;189(3):366-83 PMID: 5370012
  38. Isolation of photosystem II enriched membrane vesicles from spinach chloroplasts by phase partition.
    Biochim Biophys Acta. 1976 Dec 6;449(3):525-35 PMID: 999851
  39. The role of protein phosphorylation in neural and hormonal control of cellular activity.
    Nature. 1982 Apr 15;296(5858):613-20 PMID: 6280056
  40. Vitamin A and the role of the pigment epithelium during bleaching and regeneration of rhodopsin in the frog eye.
    Exp Eye Res. 1976 May;22(5):435-55 PMID: 1084281
  41. Lateral and transverse organisation of cytochromes in the chloroplast thylakoid membrane.
    Biochem Biophys Res Commun. 1981 Dec 31;103(4):1336-42 PMID: 7332596
  42. Chloroplast phosphoproteins: regulation of excitation energy transfer by phosphorylation of thylakoid membrane polypeptides.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5253-7 PMID: 6933557
  43. Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites.
    Biochemistry. 1982 Jun 8;21(12):3014-22 PMID: 6980670
  44. Chloroplast phosphoproteins. Evidence for a thylakoid-bound phosphoprotein phosphatase.
    Eur J Biochem. 1980 Feb;104(1):85-9 PMID: 6245872
  45. Spatial relationship of photosystem I, photosystem II, and the light-harvesting complex in chloroplast membranes.
    J Cell Biol. 1977 May;73(2):400-18 PMID: 870501
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1983-11-00
Pages
1327-37
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2112674
Subset
IM
Grants
NIGMS NIH HHS · GM22912 · United States
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