Significance of the photosystem II Core phosphatase PBCP for plant viability and protein repair in thylakoid membranes

Plant and Cell Physiology

Volumn 55, Issue 7, 2014, Pages 1245-1254

  Puthiyaveetil, Sujith ^a   Woodiwiss, Timothy ^a   Knoerdel, Ryan ^a   Zia, Ahmad ^a   Wood, Magnus ^a   Hoehner, Ricarda ^a   Kirchhoff, Helmut ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

PBCP; Photoinhibition; PSII repair cycle; STN8

Indexed keywords

5' UNTRANSLATED REGION; ARABIDOPSIS PROTEIN; PHOSPHOPROTEIN PHOSPHATASE; PHOTOSYSTEM II; PHOTOSYSTEM II PHOSPHATASE, ARABIDOPSIS;

5' UNTRANSLATED REGION; ARABIDOPSIS; BIOMASS; DARKNESS; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; PHENOTYPE; PHOSPHORYLATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PROTOPLAST; RADIATION RESPONSE; SEEDLING; THYLAKOID;

5' UNTRANSLATED REGIONS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOMASS; DARKNESS; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; LIGHT; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTOPLASTS; SEEDLING; THYLAKOIDS;

EID: 84904010982     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu062     Document Type: Article

References (50)

1. Albertsson, P. (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6: 349-358.
2. Allen, J.F. (1992) Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098: 275-335.
3. Allen, J.F., Santabarbara, S., Allen, C.A. and Puthiyaveetil, S. (2011) Discrete redox signaling pathways regulate photosynthetic lightharvesting and chloroplast gene transcription. PLoS One 6: e26372.
4. Andersson, B. and Anderson, J.M. (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoidmembranes of spinach chloroplasts. Biochim. Biophys. Acta 593: 427-440.
5. Andreeva, A., Stoitchkova, K., Busheva, M. and Apostolova, E. (2003) Changes in the energy distribution between chlorophyll-protein complexes of thylakoid membranes from pea mutants with modified pigment content. I. Changes due to the modified pigment content. J. Photochem. Photobiol. B 70: 153-162.
6. Bellafiore, S., Barneche, F., Peltier, G. and Rochaix, J.D. (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892-895.
7. Bonardi, V., Pesaresi, P., Becker, T., Schleiff, E., Wagner, R., Pfannschmidt, T. et al. (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437: 1179-1182.
8. Cohen, P. (2002) The origins of protein phosphorylation. Nat. Cell Biol. 4: E127-E130.
9. Daum, B., Nicastro, D., Austin, J. 2nd, McIntosh, J.R. and Kuhlbrandt, W. (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22: 1299-1312.
10. Depege, N., Bellafiore, S. and Rochaix, J.D. (2003) Rote of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299: 1572-1575.
11. Elich, T.D., Edelman, M. and Mattoo, A.K. (1992) Identification, characterization, and resolution of the in vivo phosphorylated form of the D1 photosystem II reaction center protein. J. Biol. Chem. 267: 3523-3529.
12. Fristedt, R., Granath, P. and Vener, A.V. (2010) A protein phosphorylation threshold for functional stacking of plant photosynthetic membranes. PLoS One 5: e10963.
13. Fristedt, R. and Vener, A.V. (2011) High light induced disassembly of photosystem II supercomplexes in Arabidopsis requires STN7-dependent phosphorylation of CP29. PLoS One 6: e24565.
14. Fristedt, R., Willig, A., Granath, P., Crevecoeur, M., Rochaix, J.D. and Vener, A.V. (2009) Phosphorylation of photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell 21: 3950-3964.
15. Goral, T.K., Johnson, M.P., Brain, A.P., Kirchhoff, H., Ruban, A.V. and Mullineaux, C.W. (2010) Visualizing the mobility and distribution of chlorophyll proteins in higher plant thylakoid membranes: effects of photoinhibition and protein phosphorylation. Plant J. 62: 948-959.
16. Haferkamp, S., Haase, W., Pascal, A.A., van Amerongen, H. and Kirchhoff, H. (2010) Efficient light harvesting by photosystem II requires an optimized protein packing density in grana thylakoids. J. Biol. Chem. 285: 17020-17028.
17. Herbstova, M., Tietz, S., Kinzel, C., Turkina, M.V. and Kirchhoff, H. (2012) Architectural switch in plant photosynthetic membranes induced by light stress. Proc. Natl Acad. Sci. USA 109: 20130-20135.
18. Kargul, J., Turkina, M.V., Nield, J., Benson, S., Vener, A.V. and Barber, J. (2005) Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J. 272: 4797-4806.
19. Kirchhoff, H. (2013) Structural constraints for protein repair in plant photosynthetic membranes. Plant Signal. Behav. 8: e23634.
20. Kirchhoff, H., Borinski, M., Lenhert, S., Chi, L. and Buchel, C. (2004) Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 43: 14508-14516.
21. Kirchhoff, H., Haferkamp, S., Allen, J.F., Epstein, D.B. and Mullineaux, C.W. (2008) Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol. 146: 1571-1578.
22. Kirchhoff, H., Hall, C., Wood, M., Herbstova, M., Tsabari, O., Nevo, R. et al. (2011) Dynamic control of protein diffusion within the granal thylakoid lumen. Proc. Natl Acad. Sci. USA 108: 20248-20253.
23. Koivuniemi, A., Aro, E.M. and Andersson, B. (1995) Degradation of the D1- and D2-proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34: 16022-16029.
24. Krause, G.H. and Jahns, P. (eds) (2003) Pulse Amplitude Modulated Fluorometry and its Application in Plant Science. Kluwer Academic Publishers, Dordrecht.
25. Kyle, D.J., Ohad, I. and Arntzen, C.J. (1984) Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc. Natl Acad. Sci. USA 81: 4070-4074.
26. Lavergne, J. and Trissl, H.W. (1995) Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys. J. 68: 2474-2492.
27. Lazar, D. (1999) Chlorophyll a fluorescence induction. Biochim. Biophys. Acta 1412: 1-28.
28. Melis, A. (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage? Trends Plant Sci. 4: 130-135.
29. Mullineaux, C.W. (2008) Factors controlling the mobility of photosynthetic proteins. Photochem. Photobiol. 84: 1310-1316.
30. Nath, K., Poudyal, R.S., Eom, J.S., Park, Y.S., Zulfugarov, I.S., Mishra, S.R. et al. (2013) Loss-of-function of OsSTN8 suppresses the photosystem (PS) II core protein phosphorylation and interferes with PSII repair mechanism in rice (Oryza sativa). Plant J. 76: 675-686.
31. Nixon, P.J., Michoux, F., Yu, J., Boehm, M. and Komenda, J. (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. 106: 1-16.
32. Pesaresi, P., Hertle, A., Pribil, M., Kleine, T., Wagner, R., Strissel, H. et al. (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21: 2402-2423.
33. Pesaresi, P., Pribil, M., Wunder, T. and Leister, D. (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38. Biochim. Biophys. Acta 1807: 887-896.
34. Pribil, M., Pesaresi, P., Hertle, A., Barbato, R. and Leister, D. (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol 8: e1000288.
35. Puthiyaveetil, S., Ibrahim, I.M. and Allen, J.F. (2012) Oxidation-reduction signalling components in regulatory pathways of state transitions and photosystem stoichiometry adjustment in chloroplasts. Plant Cell Environ. 35: 347-359.
36. Puthiyaveetil, S. and Kirchhoff, H. (2013) A phosphorylation map of the photosystem II supercomplex C2S2M2. Front. Plant Sci 4: 459.
37. Rappaport, F., Beal, D., Joliot, A. and Joliot, P. (2007) On the advantages of using green light to study fluorescence yield changes in leaves. Biochim. Biophys. Acta 1767: 56-65.
38. Rintamaki, E., Kettunen, R. and Aro, E.M. (1996) Differential D1 dephosphorylation in functional and photodamaged photosystem II centers. Dephosphorylation is a prerequisite for degradation of damaged D1. J. Biol. Chem. 271: 14870-14875.
39. Rochaix, J.D. (2013) Redox regulation of thylakoid protein kinases and photosynthetic gene expression. Antioxid. Redox Signal. 18: 2184-2201.
40. Rokka, A., Aro, E.M., Herrmann, R.G., Andersson, B. and Vener, A.V. (2000) Dephosphorylation of photosystem II reaction center proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature. Plant Physiol. 123: 1525-1536.
41. Samol, I., Shapiguzov, A., Ingelsson, B., Fucile, G., Crevecoeur, M., Vener, A.V. et al. (2012) Identification of a photosystem II phosphatase involved in light acclimation in Arabidopsis. Plant Cell 24: 2596-2609.
42. Sun, G., Bailey, D., Jones, M.W. and Markwel, J. (1989) Chloroplast thylakoid protein phosphatase is a membrane surface-associated activity. Plant Physiol. 89: 238-243.
43. Takahashi, H., Iwai, M., Takahashi, Y. and Minagawa, J. (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 103: 477-482.
44. Tikkanen, M. and Aro, E.M. (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim. Biophys. Acta 1817: 232-238.
45. Tikkanen, M. and Aro, E.M. (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci. 19: 10-17.
46. Tikkanen, M., Grieco, M., Kangasjarvi, S. and Aro, E.M. (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol. 152: 723-735.
47. Tikkanen, M., Nurmi, M., Kangasjarvi, S. and Aro, E.M. (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim. Biophys. Acta 1777: 1432-1437.
48. Tyystjarvi, E. (2013) Photoinhibition of photosystem II. Int. Rev. Cell Mol. Biol. 300: 243-303.
49. Tyystjarvi, E. and Aro, E.M. (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc. Natl Acad. Sci. USA 93: 2213-2218.
50. Vener, A.V., Rokka, A., Fulgosi, H., Andersson, B. and Herrmann, R.G. (2000) A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry 39: 2130.