Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana

FEBS Journal

Volumn 275, Issue 8, 2008, Pages 1767-1777

  Vainonen, Julia P ^a   Sakuragi, Yumiko ^b   Stael, Simon ^a   Tikkanen, Mikko ^a   Allahverdiyeva, Yagut ^a   Paakkarinen, Virpi ^a   Aro, Eveliina ^a   Suorsa, Marjaana ^a   Scheller, Henrik V ^b   Vener, Alexander V ^c   Aro, Eva Mari ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

High light; Protein phosphorylation; STN8 kinase; Stress response; Thylakoid membrane

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM SENSING RECEPTOR; MEMBRANE PROTEIN; PHOSPHOPROTEIN; PROTEIN 14 3 3; PROTEIN KINASE; PROTEIN STN8; THREONINE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CELL FRACTIONATION; CHLOROPLAST; CONFOCAL LASER MICROSCOPY; LIGHT EXPOSURE; LIGHT INTENSITY; LIGHT STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEVELOPMENT; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THYLAKOID MEMBRANE;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; LIGHT; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MUTATION; PHENOTYPE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; RECEPTORS, CALCIUM-SENSING; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; THYLAKOIDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 41549103343     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06335.x     Document Type: Article

References (41)

1. Vener AV (2007) Environmentally modulated phosphorylation and dynamics of proteins in photosynthetic membranes. Biochim Biophys Acta 6, 449 457.
2. Michel H, Griffin PR, Shabanowitz J, Hunt DF Bennett J (1991) Tandem mass spectrometry identifies sites of three post-translational modifications of spinach light-harvesting chlorophyll protein II. Proteolytic cleavage, acetylation, and phosphorylation. J Biol Chem 266, 17584 17591.
3. Vener AV, Harms A, Sussman MR Vierstra RD (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J Biol Chem 276, 6959 6966.
4. 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.
5. Rintamaki E, Kettunen R Aro EM (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.
6. Baena-Gonzalez E, Barbato R Aro EM (1999) Role of phosphorylation in the repair cycle and oligomeric structure of photosystem II. Planta 208, 196 204.
7. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098, 275 335.
8. Rintamaki 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.
9. Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20, 3623 3630.
10. Aro EM Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antiox Redox Signal 1, 55 67.
11. Tikkanen M, Piippo M, Suorsa M, Sirpio 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.
12. Khrouchtchova A, Hansson M, Paakkarinen V, Vainonen JP, Zhang S, Jensen PE, Scheller HV, Vener AV, Aro EM Haldrup A (2005) A previously found thylakoid membrane protein of 14 kDa (TMP14) is a novel subunit of plant photosystem I and is designated PSI-P. FEBS Lett 579, 4808 4812.
13. Hamel P, Olive J, Pierre Y, Wollman FA de Vitry C (2000) A new subunit of cytochrome b6f complex undergoes reversible phosphorylation upon state transition. J Biol Chem 275, 17072 17079.
14. Rinalducci S, Larsen MR, Mohammed S Zolla L (2006) Novel protein phosphorylation site identification in spinach stroma membranes by titanium dioxide microcolumns and tandem mass spectrometry. J Proteome Res 5, 973 982.
15. Carlberg I, Hansson M, Kieselbach T, Schroder WP, Andersson B Vener AV (2003) A novel plant protein undergoing light-induced phosphorylation and release from the photosynthetic thylakoid membranes. Proc Natl Acad Sci USA 100, 757 762.
16. Turkina MV, Kargul J, Blanco-Rivero A, Villarejo A, Barber J Vener AV (2006) Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 5, 1412 1425.
17. Bellafiore S, Barneche F, Peltier G Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892 895.
18. Bonardi V, Pesaresi P, Becker T, Schleiff T, 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.
19. 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.
20. Han S, Tang R, Anderson LK, Woerner TE Pei ZM (2003) A cell surface receptor mediates extracellular Ca(2+) sensing in guard cells. Nature 425, 196 200.
21. Tang RH, Han S, Zheng H, Cook CW, Choi CS, Woerner TE, Jackson RB Pei ZM (2007) Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315, 1423 1426.
22. Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q Wijk KJ (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16, 478 499.
23. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjölander K, Gruissem W Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14, 354 362.
24. Peltier JB, Ytterberg AJ, Sun Q van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279, 49367 49383.
25. Hammet A, Pike BL, McNees CJ, Conlan LA, Tenis N Heierhorst J (2003) FHA domains as phospho-threonine binding modules in cell signaling. IUBMB Life 55, 23 27.
26. Alexandersson E, Saalbach G, Larsson C Kjellbom P (2004) Arabidopsis plasma membrane proteomics identifies components of transport, signal transduction and membrane trafficking. Plant Cell Physiol 45, 1543 1556.
27. Millar AH, Sweetlove LJ, Giege P Leaver CJ (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127, 1711 1727.
28. Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N Aro EM (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25, 142 152.
29. Kanervo E, Suorsa M Aro EM (2007) Assembly of protein complexes in plastids. In Cell and Molecular Biology of Plastids (Bock R, ed pp 283 313. Springer-Verlag, Berlin.
30. Bordo D Bork P (2002) The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations. EMBO Rep 3, 741 746.
31. Azumi Y Watanabe A (1991) Evidence for a senescence-associated gene induced by darkness. Plant Physiol 95, 577 583.
32. Fulgosi H, Soll J, de Faria Maraschin S, Korthout HA, Wang M Testerink C (2002) 14-3-3 proteins and plant development. Plant Mol Biol 50, 1019 1029.
33. Li J, Lee G, Van Doren SR Walker JC (2000) The FHA domain mediates phosphoprotein interactions. J Cell Sci 113, 4143 4149.
34. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653 657.
35. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53, 247 259.
36. Palmgren MG, Askerlund P, Fredrikson K, Widell S, Sommarin M Larsson C (1990) Sealed inside-out and right-side-out plasma membrane vesicles: optimal conditions for formation and separation. Plant Physiol 92, 871 880.
37. Cline K (1986) Import of proteins into chloroplasts. J Biol Chem 261, 14804 14810.
38. 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.
39. Ficarro S, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, Shabanowitz J, Hunt DF White FM (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechol 20, 301 305.
40. Shevchenko A, Jensen ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O, Mortensen P, Shevchenko A, Boucherie H Mann M (1996) Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci USA 93, 14440 14445.
41. Nour-Eldin HH, Hansen BG, Norholm MHH, Jensen JK Halkier BA (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 34, doi:.