Control of STN7 transcript abundance and transient STN7 dimerisation are involved in the regulation of STN7 activity

Planta

Volumn 237, Issue 2, 2013, Pages 541-558

  Wunder, Tobias ^a   Liu, Qiuping ^a   Aseeva, Elena ^a   Bonardi, Vera ^a   Leister, Dario ^a   Pribil, Mathias ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Arabidopsis; LHCII; Phosphorylation; Photosystems; Redox regulation; State transitions; STN7

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; CHLOROPHYTA; TRACHEOPHYTA;

EID: 84873084990     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1775-y     Document Type: Article

References (60)

1. Allen JF, Santabarbara S, Allen CA, Puthiyaveetil S (2011) Discrete redox signaling pathways regulate photosynthetic light-harvesting and chloroplast gene transcription. PLoS ONE 6: e26372.
2. Bassi R, Marquardt J, Lavergne J (1995) Biochemical and functional properties of photosystem II in agranal membranes from maize mesophyll and bundle sheath chloroplasts. Eur J Biochem 233: 709-719.
3. Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892-895.
4. Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437: 1179-1182.
5. 559 mediates the oxidation of reduced plastoquinone in the dark. J Biol Chem 278: 13554-13560.
6. Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17: 868-876.
7. Casano LM, Zapata JM, Martín M, Sabater B (2000) Chlororespiration and poising of cyclic electron transport. Plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. J Biol Chem 275: 942-948.
8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
9. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132: 273-285.
10. Depège N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299: 1572-1575.
11. Dietzel L, Bräutigam K, Pfannschmidt T (2008) Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry-functional relationships between short-term and long-term light quality acclimation in plants. FEBS J 275: 1080-1088.
12. Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42: 463-515.
13. 6f complex. In vitro control of kinase activity. J Biol Chem 265: 19742-19749.
14. Heinemeyer J, Eubel H, Wehmhöner D, Jänsch L, Braun HP (2004) Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. Phytochemistry 65: 1683-1692.
15. Hou CX, Rintamäki E, Aro EM (2003) Ascorbate-mediated LHCII protein phosphorylation-LHCII kinase regulation in light and in darkness. Biochemistry 42: 5828-5836.
16. Ihnatowicz A, Pesaresi P, Varotto C, Richly E, Schneider A, Jahns P, Salamini F, Leister D (2004) Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. Plant J 37: 839-852.
17. Ihnatowicz A, Pesaresi P, Leister D (2007) The E subunit of photosystem I is not essential for linear electron flow and photoautotrophic growth in Arabidopsis thaliana. Planta 226: 889-895.
18. Ihnatowicz A, Pesaresi P, Lohrig K, Wolters D, Müller B, Leister D (2008) Impaired photosystem I oxidation induces STN7-dependent phosphorylation of the light-harvesting complex I protein Lhca4 in Arabidopsis thaliana. Planta 227: 717-722.
19. Izawa S, Pan RL (1978) Photosystem I electron transport and phosphorylation supported by electron donation to the plastoquinone region. Biochem Biophys Res Commun 83: 1171-1177.
20. Jensen PE, Gilpin M, Knoetzel J, Scheller HV (2000) The PSI-K subunit of photosystem I is involved in the interaction between light-harvesting complex I and the photosystem I reaction center core. J Biol Chem 275: 24701-24708.
21. Kanervo E, Suorsa M, Aro EM (2005) Functional flexibility and acclimation of the thylakoid membrane. Photochem Photobiol Sci 4: 1072-1080.
22. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
23. Lemeille S, Rochaix JD (2010) State transitions at the crossroad of thylakoid signalling pathways. Photosynth Res 106: 33-46.
24. Lemeille S, Willig A, Depège-Fargeix N, Delessert C, Bassi R, Rochaix JD (2009) Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol 7: e45.
25. 6f complex in Arabidopsis. Plant Cell 13: 2539-2551.
26. Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408: 613-615.
27. Maiwald D, Dietzmann A, Jahns P, Pesaresi P, Joliot P, Joliot A, Levin JZ, Salamini F, Leister D (2003) Knock-out of the genes coding for the Rieske protein and the ATP-synthase delta-subunit of Arabidopsis: effects on photosynthesis, thylakoid protein composition, and nuclear chloroplast gene expression. Plant Physiol 133: 191-202.
28. Meurer J, Plücken H, Kowallik KV, Westhoff P (1998) A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J 17: 5286-5297.
29. Motohashi K, Hisabori T (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem 281: 35039-35047.
30. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371.
31. 6f complex in Arabidopsis chloroplasts. J Biol Chem 279: 32474-32482.
32. Pesaresi P, Varotto C, Meurer J, Jahns P, Salamini F, Leister D (2001) Knock-out of the plastid ribosomal protein L11 in Arabidopsis: effects on mRNA translation and photosynthesis. Plant J 27: 179-189.
33. Pesaresi P, Lunde C, Jahns P, Tarantino D, Meurer J, Varotto C, Hirtz RD, Soave C, Scheller HV, Salamini F, Leister D (2002) A stable LHCII-PSI aggregate and suppression of photosynthetic state transitions in the psae1-1 mutant of Arabidopsis thaliana. Planta 215: 940-948.
34. Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, Pfannschmidt T, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21: 2402-2423.
35. Pesaresi P, Hertle A, Pribil M, Schneider A, Kleine T, Leister D (2010) Optimizing photosynthesis under fluctuating light: the role of the Arabidopsis STN7 kinase. Plant Signal Behav 5: 21-25.
36. 559 in photosystem II. J Photochem Photobiol, B 104: 341-347.
37. Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol 8: e1000288.
38. Puthiyaveetil S (2011) A mechanism for regulation of chloroplast LHC II kinase by plastoquinol and thioredoxin. FEBS Lett 585: 1717-1721.
39. Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150: 889-903.
40. Rintamäki E, Martinsuo P, Pursiheimo S, Aro EM (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97: 11644-11649.
41. Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581: 2768-2775.
42. Ruban AV, Johnson MP (2009) Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynth Res 99: 173-183.
43. Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant, Cell Environ 30: 1041-1051.
44. Sazanov LA, Burrows PA, Nixon PJ (1998) The chloroplast Ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves. FEBS Lett 429: 115-118.
45. Schwenkert S, Umate P, Dal Bosco C, Volz S, Mlçochová L, Zoryan M, Eichacker LA, Ohad I, Herrmann RG, Meurer J (2006) PsbI affects the stability, function, and phosphorylation patterns of photosystem II assemblies in tobacco. J Biol Chem 281: 34227-34238.
46. Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci USA 107: 4782-4787.
47. Shinopoulos KE, Brudvig GW (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta 1817: 66-75.
48. Tikkanen M, Piippo M, Suorsa M, Sirpiö S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM (2006) State transitions revisited-a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62: 779-793.
49. Tikkanen M, Nurmi M, Kangasjärvi S, Aro EM (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta 1777: 1432-1437.
50. Tikkanen M, Grieco M, Kangasjärvi S, Aro EM (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152: 723-735.
51. Tikkanen M, Grieco M, Aro EM (2011) Novel insights into plant light-harvesting complex II phosphorylation and 'state transitions'. Trends Plant Sci 16: 126-131.
52. Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93: 193-203.
53. Varotto C, Pesaresi P, Meurer J, Oelmüller R, Steiner-Lange S, Salamini F, Leister D (2000) Disruption of the Arabidopsis photosystem I gene psaE1 affects photosynthesis and impairs growth. Plant J 22: 115-124.
54. Vener AV, van Kan PJ, Rich PR, Ohad I, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci USA 94: 1585-1590.
55. Wagner R, Dietzel L, Bräutigam K, Fischer W, Pfannschmidt T (2008) The long-term response to fluctuating light quality is an important and distinct light acclimation mechanism that supports survival of Arabidopsis thaliana under low light conditions. Planta 228: 573-587.
56. Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56: 435-447.
57. White CC, Chain RK, Malkin R (1978) Duroquinol as an electron donor for chloroplast electron transfer reactions. Biochim Biophys Acta 502: 127-137.
58. Willig A, Shapiguzov A, Goldschmidt-Clermont M, Rochaix JD (2011) The phosphorylation status of the chloroplast protein kinase STN7 of Arabidopsis affects its turnover. Plant Physiol 157: 2102-2107.
59. Winger AM, Taylor NL, Heazlewood JL, Day DA, Millar AH (2007) Identification of intra- and intermolecular disulphide bonding in the plant mitochondrial proteome by diagonal gel electrophoresis. Proteomics 7: 4158-4170.
60. 6f complexes controls the activation of the LHCII kinase. EMBO J 18: 2961-2969.