High light-dependent phosphorylation of photosystem II inner antenna CP29 in monocots is STN7 independent and enhances nonphotochemical quenching

Plant Physiology

Volumn 167, Issue 2, 2015, Pages 457-471

  Betterle, Nico ^a   Ballottari, Matteo ^a   Baginsky, Sacha ^b   Bassi, Roberto ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LILIOPSIDA; ORYZA SATIVA;

CP29 LIGHT HARVESTING COMPLEX; LIGHT HARVESTING SYSTEM; PHOTOSYSTEM II; PROTEIN KINASE INHIBITOR; VEGETABLE PROTEIN; ZEAXANTHIN;

BIOASSAY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; INTRACELLULAR MEMBRANE; KINETICS; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; MUTATION; ORYZA; PHOSPHORYLATION; PHOTOCHEMISTRY; PHOTOSYSTEM II; RADIATION RESPONSE; THYLAKOID;

BIOLOGICAL ASSAY; ENZYME ACTIVATION; INTRACELLULAR MEMBRANES; KINETICS; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; MUTATION; ORYZA; PHOSPHORYLATION; PHOTOCHEMICAL PROCESSES; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; PROTEIN KINASE INHIBITORS; THYLAKOIDS; ZEAXANTHINS;

EID: 84921975433     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.252379     Document Type: Article

References (78)

1. Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320: 794-797
2. Allorent G, Tokutsu R, Roach T, Peers G, Cardol P, Girard-Bascou J, Seigneurin-Berny D, Petroutsos D, Kuntz M, Breyton C, et al (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25: 545-557
3. Anderson JM, Horton P, KimEH, ChowWS (2012) Towards elucidation of dynamic structural changes of plant thylakoid architecture. Philos Trans R Soc Lond B Biol Sci 367: 3515-3524
4. Andersson J, Walters RG, Horton P, Jansson S (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13: 1193-1204
5. Aro E, Mccaffery S, Anderson JM (1994) Recovery from photoinhibition in peas (Pisum sativum L.) acclimated to varying growth irradiances. Plant Physiol 104: 1033-1041
6. Aro EM, Rokka A, Vener AV (2004) Determination of phosphoproteins in higher plant thylakoids. Methods Mol Biol 274: 271-285
7. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601-639
8. Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR (2008) Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 283: 3550-3558
9. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59: 89-113
10. Barbato R, Bergo E, Szabò I, Dalla Vecchia F, Giacometti GM (2000) Ultraviolet B exposure of whole leaves of barley affects structure and functional organization of photosystem II. J Biol Chem 275: 10976- 10982
11. Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892-895
12. Bergantino E, Dainese P, Cerovic Z, Sechi S, Bassi R (1995) A posttranslational modification of the photosystem II subunit CP29 protects maize from cold stress. J Biol Chem 270: 8474-8481
13. Bergantino E, Sandonà D, Cugini D, Bassi R (1998) The photosystem II subunit CP29 can be phosphorylated in both C3 and C4 plants as suggested by sequence analysis. Plant Mol Biol 36: 11-22
14. Betterle N, Ballottari M, Hienerwadel R, Dall'Osto L, Bassi R (2010) Dynamics of zeaxanthin binding to the photosystem II monomeric antenna protein Lhcb6 (CP24) and modulation of its photoprotection properties. Arch Biochem Biophys 504: 67-77
15. Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall'osto L, Morosinotto T, Bassi R (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284: 15255-15266
16. Bi FC, Zhang QF, Liu Z, Fang C, Li J, Su JB, Greenberg JT, Wang HB, Yao N (2011) A conserved cysteine motif is critical for rice ceramide kinase activity and function. PLoS ONE 6: e18079
17. 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
18. Caffarri S, Broess K, Croce R, van Amerongen H (2011) Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys J 100: 2094-2103
19. Caffarri S, Kouril R, Kereïche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28: 3052-3063
20. Casazza AP, Tarantino D, Soave C (2001) Preparation and functional characterization of thylakoids from Arabidopsis thaliana. Photosynth Res 68: 175-80
21. Chen YE, Yuan S, Du JB, Xu MY, Zhang ZW, Lin HH (2009) Phosphorylation of photosynthetic antenna protein CP29 and photosystem II structure changes in monocotyledonous plants under environmental stresses. Biochemistry 48: 9757-9763
22. Chen YE, Zhao ZY, Zhang HY, Zeng XY, Yuan S (2013) The significance of CP29 reversible phosphorylation in thylakoids of higher plants under environmental stresses. J Exp Bot 64: 1167-1178
23. Crimi M, Dorra D, Bösinger CS, Giuffra E, Holzwarth AR, Bassi R (2001) Time-resolved fluorescence analysis of the recombinant photosystem II antenna complex CP29. Effects of zeaxanthin, pH and phosphorylation. Eur J Biochem 268: 260-267
24. Croce R, Breton J, Bassi R (1996) Conformational changes induced by phosphorylation in the CP29 subunit of photosystem II. Biochemistry 35: 11142-11148
25. Dall'Osto L, Caffarri S, Bassi R (2005) A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17: 1217-1232
26. Dall'Osto L, Cazzaniga S, Havaux M, Bassi R (2010) Enhanced photoprotection by protein-bound vs. free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Mol Plant 3: 576-593
27. Dall'Osto L, Cazzaniga S, North H, Marion-Poll A, Bassi R (2007) The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell 19: 1048-1064
28. de Bianchi S, Ballottari M, Dall'osto L, Bassi R (2010) Regulation of plant light harvesting by thermal dissipation of excess energy. Biochem Soc Trans 38: 651-660
29. de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall'Osto L (2011) Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23: 2659-2679
30. 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
31. Drop B, Yadav KN S, Boekema EJ, Croce R (2014) Consequences of state transitions on the structural and functional organization of photosystem I in the green alga Chlamydomonas reinhardtii. Plant J 78: 181-191
32. Flors C, Fryer MJ, Waring J, Reeder B, Bechtold U, Mullineaux PM, Nonell S, Wilson MT, Baker NR (2006) Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J Exp Bot 57: 1725-1734
33. Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol 152: 1219-1250
34. Fristedt R, Vener AV (2011) High light-induced disassembly of photosystem II supercomplexes in Arabidopsis requires STN7-dependent phosphorylation of CP29. PLoS ONE 6: e24565
35. Galka P, Santabarbara S, Khuong TTH, Degand H, Morsomme P, Jennings RC, Boekema EJ, Caffarri S (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24: 2963-2978
36. Gilmore AM, Yamamoto HY (1991) Zeaxanthin formation and energydependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol 96: 635-43
37. Gobets B, van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1507: 80-99
38. Hansson M, Vener AV (2003) Identification of three previously unknown in vivo protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Mol Cell Proteomics 2: 550-559
39. Havaux M, Dall'osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145: 1506-1520
40. Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307: 433-436
41. Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macroorganisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275: 1069-1079
42. Horton P, Ruban A (2005) Molecular design of the photosystem II lightharvesting antenna: photosynthesis and photoprotection. J Exp Bot 56: 365-373
43. Hwang H, Xu C, Moon B, Lee C (2003) Recovery from low-temperature photoinhibition is related to dephosphorylation of phosphorylated CP29 rather than zeaxanthin epoxidation in rice leaves. J Plant Biol 46: 122- 129
44. 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
45. Kargul J, Turkina MV, Nield J, Benson S, Vener AV, 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
46. Külheim C, Agren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91-93
47. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
48. Larmande P, Gay C, Lorieux M, Périn C, Bouniol M, Droc G, Sallaud C, Perez P, Barnola I, Biderre-Petit C, et al (2008) Oryza Tag Line, a phenotypic mutant database for the Genoplante rice insertion line library. Nucleic Acids Res 36: D1022-D1027
49. 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
50. Leoni C, Pietrzykowska M, Kiss AZ, Suorsa M, Ceci LR, Aro EM, Jansson S (2013) Very rapid phosphorylation kinetics suggest a unique role for Lhcb2 during state transitions in Arabidopsis. Plant J 76: 236-246
51. Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395
52. Liu WJ, Chen YE, Tian WJ, Du JB, Zhang ZW, Xu F, Zhang F, Yuan S, Lin HH (2009) Dephosphorylation of photosystem II proteins and phosphorylation of CP29 in barley photosynthetic membranes as a response to water stress. Biochim Biophys Acta 1787: 1238-1245
53. Mauro S, Dainese P, Lannoye R, Bassi R (1997) Cold-resistant and coldsensitive maize lines differ in the phosphorylation of the photosystem II subunit, CP29. Plant Physiol 115: 171-180
54. Morosinotto T, Baronio R, Bassi R (2002) Dynamics of chromophore binding to Lhc proteins in vivo and in vitro during operation of the xanthophyll cycle. J Biol Chem 277: 36913-36920
55. Morosinotto T, Segalla A, Giacometti GM, Bassi R (2010) Purification of structurally intact grana from plants thylakoids membranes. J Bioenerg Biomembr 42: 37-45
56. Nath K, Poudyal RS, Eom JS, Park YS, Zulfugarov IS, Mishra SR, Tovuu A, Ryoo N, Yoon HS, Nam HG, et al (2013) Loss-of-function of OsSTN8 suppresses the photosystem II core protein phosphorylation and interferes with the photosystem II repair mechanism in rice (Oryza sativa). Plant J 76: 675-686
57. Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5: 971-982
58. Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth AR, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophys Acta 1797: 466-475
59. Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134
60. Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16: 307-314
61. 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
62. Pursiheimo S, Martinsuo P, Rintamäki E, Aro E (2003) Photosystem II protein phosphorylation follows four distinctly different regulatory patterns induced by environmental cues. Plant Cell Environ 26: 1995-2003
63. 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
64. Rintamäki E, Salonen M, Suoranta UM, Carlberg I, Andersson B, Aro EM (1997) Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. J Biol Chem 272: 30476-30482
65. Ruban AV, Johnson MP (2010) Xanthophylls as modulators of membrane protein function. Arch Biochem Biophys 504: 78-85
66. Ruegg UT, Burgess GM (1989) Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends Pharmacol Sci 10: 218-220
67. Savitch LV, Ivanov AG, Gudynaite-Savitch L, Huner NP, Simmonds J (2011) Cold stress effects on PSI photochemistry in Zea mays: differential increase of FQR-dependent cyclic electron flow and functional implications. Plant Cell Physiol 52: 1042-1054
68. 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
69. Sirpiö S, Allahverdiyeva Y, Suorsa M, Paakkarinen V, Vainonen J, Battchikova N, Aro EM (2007) TLP18.3, a novel thylakoid lumen protein regulating photosystem II repair cycle. Biochem J 406: 415-425
70. Suorsa M, Regel RE, Paakkarinen V, Battchikova N, Herrmann RG, Aro EM (2004) Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. Eur J Biochem 271: 96-107
71. Testi MG, Croce R, Polverino-De Laureto P, Bassi R (1996) A CK2 site is reversibly phosphorylated in the photosystem II subunit CP29. FEBS Lett 399: 245-250
72. Tikkanen M, Grieco M, Aro EM (2011) Novel insights into plant lightharvesting complex II phosphorylation and 'state transitions'. Trends Plant Sci 16: 126-131
73. 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
74. Tikkanen M, Piippo M, Suorsa M, Sirpiö S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM, Paula M, et al (2006) State transitions revisited: a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62: 779-793
75. Vainonen JP, Hansson M, Vener AV (2005) STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. J Biol Chem 280: 33679-33686
76. Wunder T, Liu Q, Aseeva E, Bonardi V, Leister D, Pribil M (2013) Control of STN7 transcript abundance and transient STN7 dimerisation are involved in the regulation of STN7 activity. Planta 237: 541- 558
77. Zhang J, Li C, Wu C, Xiong L, Chen G, Zhang Q, Wang S (2006) RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Res 34: D745-D748
78. Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA (1999) The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J 18: 2961-2969