Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1992 Oct 2;119(2):325–335. doi: 10.1083/jcb.119.2.325

Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids

PMCID: PMC2289643  PMID: 1400577

Abstract

The structural and topological stability of thylakoid components under photoinhibitory conditions (4,500 microE.m-2.s-1 white light) was studied on Mn depleted thylakoids isolated from spinach leaves. After various exposures to photoinhibitory light, the chlorophyll-protein complexes of both photosystems I and II were separated by sucrose gradient centrifugation and analysed by Western blotting, using a set of polyclonals raised against various apoproteins of the photosynthetic apparatus. A series of events occurring during donor side photoinhibition are described for photosystem II, including: (a) lowering of the oligomerization state of the photosystem II core; (b) cleavage of 32-kD protein D1 at specific sites; (c) dissociation of chlorophyll-protein CP43 from the photosystem II core; and (d) migration of damaged photosystem II components from the grana to the stroma lamellae. A tentative scheme for the succession of these events is illustrated. Some effects of photoinhibition on photosystem I are also reported involving dissociation of antenna chlorophyll-proteins LHCI from the photosystem I reaction center.

Full Text

The Full Text of this article is available as a PDF (2.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adir N., Shochat S., Ohad I. Light-dependent D1 protein synthesis and translocation is regulated by reaction center II. Reaction center II serves as an acceptor for the D1 precursor. J Biol Chem. 1990 Jul 25;265(21):12563–12568. [PubMed] [Google Scholar]
  2. Anderson J. M., Melis A. Localization of different photosystems in separate regions of chloroplast membranes. Proc Natl Acad Sci U S A. 1983 Feb;80(3):745–749. doi: 10.1073/pnas.80.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arnon D. I. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. Plant Physiol. 1949 Jan;24(1):1–15. doi: 10.1104/pp.24.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barbato R., Friso G., Giardi M. T., Rigoni F., Giacometti G. M. Breakdown of the photosystem II reaction center D1 protein under photoinhibitory conditions: identification and localization of the C-terminal degradation products. Biochemistry. 1991 Oct 22;30(42):10220–10226. doi: 10.1021/bi00106a021. [DOI] [PubMed] [Google Scholar]
  5. Barbato R., Frizzo A., Friso G., Rigoni F., Giacometti G. M. Photoinduced degradation of the D1 protein in isolated thylakoids and various photosystem II particles after donor-side inactivations. Detection of a C-terminal 16 kDa fragment. FEBS Lett. 1992 Jun 15;304(2-3):136–140. doi: 10.1016/0014-5793(92)80604-f. [DOI] [PubMed] [Google Scholar]
  6. Barbato R., Shipton C. A., Giacometti G. M., Barber J. New evidence suggests that the initial photoinduced cleavage of the D1-protein may not occur near the PEST sequence. FEBS Lett. 1991 Sep 23;290(1-2):162–166. doi: 10.1016/0014-5793(91)81250-c. [DOI] [PubMed] [Google Scholar]
  7. Barber J., Andersson B. Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci. 1992 Feb;17(2):61–66. doi: 10.1016/0968-0004(92)90503-2. [DOI] [PubMed] [Google Scholar]
  8. Bassi R., Ghiretti Magaldi A., Tognon G., Giacometti G. M., Miller K. R. Two-dimensional crystals of the photosystem II reaction center complex from higher plants. Eur J Cell Biol. 1989 Oct;50(1):84–93. [PubMed] [Google Scholar]
  9. Chua N. H., Gillham N. W. The sites of synthesis of the principal thylakoid membrane polypeptides in Chlamydomonas reinhardtii. J Cell Biol. 1977 Aug;74(2):441–452. doi: 10.1083/jcb.74.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dainese P., Bassi R. Subunit stoichiometry of the chloroplast photosystem II antenna system and aggregation state of the component chlorophyll a/b binding proteins. J Biol Chem. 1991 May 5;266(13):8136–8142. [PubMed] [Google Scholar]
  11. Diner B. A., Ries D. F., Cohen B. N., Metz J. G. COOH-terminal processing of polypeptide D1 of the photosystem II reaction center of Scenedesmus obliquus is necessary for the assembly of the oxygen-evolving complex. J Biol Chem. 1988 Jun 25;263(18):8972–8980. [PubMed] [Google Scholar]
  12. Giardi M. T., Rigoni F., Barbato R., Giacometti G. M. Relationships between heterogeneity of the PSII core complex from grana particles and phosphorylation. Biochem Biophys Res Commun. 1991 May 15;176(3):1298–1305. doi: 10.1016/0006-291x(91)90427-9. [DOI] [PubMed] [Google Scholar]
  13. Grebanier A. E., Coen D. M., Rich A., Bogorad L. Membrane proteins synthesized but not processed by isolated maize chloroplasts. J Cell Biol. 1978 Sep;78(3):734–746. doi: 10.1083/jcb.78.3.734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Greenberg B. M., Gaba V., Mattoo A. K., Edelman M. Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem II. EMBO J. 1987 Oct;6(10):2865–2869. doi: 10.1002/j.1460-2075.1987.tb02588.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jegerschöld C., Styring S. Fast oxygen-independent degradation of the D1 reaction center protein in photosystem II. FEBS Lett. 1991 Mar 11;280(1):87–90. doi: 10.1016/0014-5793(91)80210-t. [DOI] [PubMed] [Google Scholar]
  16. Jegerschöld C., Virgin I., Styring S. Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction. Biochemistry. 1990 Jul 3;29(26):6179–6186. doi: 10.1021/bi00478a010. [DOI] [PubMed] [Google Scholar]
  17. Kyle D. J., Ohad I., Arntzen C. J. Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4070–4074. doi: 10.1073/pnas.81.13.4070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Marder J. B., Goloubinoff P., Edelman M. Molecular architecture of the rapidly metabolized 32-kilodalton protein of photosystem II. Indications for COOH-terminal processing of a chloroplast membrane polypeptide. J Biol Chem. 1984 Mar 25;259(6):3900–3908. [PubMed] [Google Scholar]
  19. Mattoo A. K., Edelman M. Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1497–1501. doi: 10.1073/pnas.84.6.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mattoo A. K., Pick U., Hoffman-Falk H., Edelman M. The rapidly metabolized 32,000-dalton polypeptide of the chloroplast is the "proteinaceous shield" regulating photosystem II electron transport and mediating diuron herbicide sensitivity. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1572–1576. doi: 10.1073/pnas.78.3.1572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Michel H., Hunt D. F., Shabanowitz J., Bennett J. Tandem mass spectrometry reveals that three photosystem II proteins of spinach chloroplasts contain N-acetyl-O-phosphothreonine at their NH2 termini. J Biol Chem. 1988 Jan 25;263(3):1123–1130. [PubMed] [Google Scholar]
  22. Mullet J. E., Burke J. J., Arntzen C. J. Chlorophyll proteins of photosystem I. Plant Physiol. 1980 May;65(5):814–822. doi: 10.1104/pp.65.5.814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nanba O., Satoh K. Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci U S A. 1987 Jan;84(1):109–112. doi: 10.1073/pnas.84.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ohad I., Adir N., Koike H., Kyle D. J., Inoue Y. Mechanism of photoinhibition in vivo. A reversible light-induced conformational change of reaction center II is related to an irreversible modification of the D1 protein. J Biol Chem. 1990 Feb 5;265(4):1972–1979. [PubMed] [Google Scholar]
  25. Ohad I., Kyle D. J., Hirschberg J. Light-dependent degradation of the Q(B)-protein in isolated pea thylakoids. EMBO J. 1985 Jul;4(7):1655–1659. doi: 10.1002/j.1460-2075.1985.tb03833.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Peter G. F., Thornber J. P. Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Biol Chem. 1991 Sep 5;266(25):16745–16754. [PubMed] [Google Scholar]
  27. Reisfeld A., Mattoo A. K., Edelman M. Processing of a chloroplast-translated membrane protein in vivo. Analysis of the rapidly synthesized 32 000-dalton shield protein and its precursor in Spirodela oligorrhiza. Eur J Biochem. 1982 May;124(1):125–129. doi: 10.1111/j.1432-1033.1982.tb05914.x. [DOI] [PubMed] [Google Scholar]
  28. Rögner M., Chisholm D. A., Diner B. A. Site-directed mutagenesis of the psbC gene of photosystem II: isolation and functional characterization of CP43-less photosystem II core complexes. Biochemistry. 1991 Jun 4;30(22):5387–5395. doi: 10.1021/bi00236a009. [DOI] [PubMed] [Google Scholar]
  29. Schuster G., Dewit M., Staehelin L. A., Ohad I. Transient inactivation of the thylakoid photosystem II light-harvesting protein kinase system and concomitant changes in intramembrane particle size during photoinhibition of Chlamydomonas reinhardtii. J Cell Biol. 1986 Jul;103(1):71–80. doi: 10.1083/jcb.103.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shipton C. A., Barber J. Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem II: evidence for an autoproteolytic process triggered by the oxidizing side of the photosystem. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6691–6695. doi: 10.1073/pnas.88.15.6691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. de Vitry C., Olive J., Drapier D., Recouvreur M., Wollman F. A. Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii. J Cell Biol. 1989 Sep;109(3):991–1006. doi: 10.1083/jcb.109.3.991. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES