Abstract
Redox dependent protein phosphorylation in chloroplast thylakoids regulates distribution of excitation energy between the two photosystems of photosynthesis, PS I and PS II. Several thylakoid phosphoproteins are known to be phosphorylated on N-terminal threonine residues exposed to the chloroplast stroma. Phosphorylation of light harvesting complex II (LHC II) on Thr-6 is thought to account for redistribution of light energy from PS II to PS I during the transition to light state 2. Here, we present evidence that a protein tyrosine kinase activity is required for the transition to light state 2. With an immunological approach using antibodies directed specifically towards either phospho-tyrosine or phospho-threonine, we observed that LHC II became phosphorylated on both tyrosine and threonine residues. The specific protein tyrosine kinase inhibitor genistein, at concentrations causing no direct effect on threonine kinase activity, was found to prevent tyrosine phosphorylation of LHC II, the transition to light state 2, and associated threonine phosphorylation of LHC II. Possible reasons for an involvement of tyrosine phosphorylation in light state transitions are proposed and discussed.
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References
Akiyama T and Ogawara H (1991) Use and specificity of genistein as inhibitor of protein-tyrosine kinases. In: Hunter T and Sefton BM (eds) Methods in Enzymology 201 B, pp 362–370. Academic Press, San Diego, California
Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M and Fukami Y (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262: 5592–5595
Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. BiochiBiophys Acta 1098: 275–335
Allen JF, Bennett J, Steinback KE and Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291: 25–29
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1–15
Barizza E, Lo Schiavo F, Terzi M and Filippini F (1999) Evidence suggesting protein tyrosine phosphorylation in plants depends on the developmental conditions. FEBS Lett 447: 191–194
Bennett J (1979) Chloroplast phosphoproteins. Phosphorylation of polypeptides of the light-harvesting chlorophyll protein complex. Eur J Biochem 99: 133–137
Bennett J (1980) Chloroplast phosphoproteins. Evidence for a thylakoid-bound phosphoprotein phosphatase. Eur J Biochem 104: 85–89
Bennett J, Steinback KE and Arntzen CJ (1980) Chloroplast phosphoproteins: Regulation of excitation energy transfer by phosphorylation of thylakoid membrane polypeptides. Proc Natl Acad Sci USA 77: 5253–5257
Bjerrum OJ and Schafer-Nielsen C (1986) Buffer systems and transfer parameters for semi-dry electroblotting with a horizontal apparatus. In: Dunn MJ (ed) Electrophoresis'86, pp 315–327. VCH Publishers, Weinheim, Germany
Dilly-Hartwig H, Allen JF, Paulsen H and Race HL (1998) Truncated recombinant light harvesting complex II proteins are substrates for a protein kinase associated with Photosystem II core complexes. FEBS Lett 435: 101–104
Edelman AM, Blumenthal DK and Krebs EG (1987) Protein serine/ threonine kinases. Annu Rev Biochem 56: 567–613
Hirayama T and Oka A (1992) Novel protein kinase of Arabidopsis thaliana (APK1) that phosphorylates tyrosine, serine and threonine. Plant Mol Biol 20: 653–662
Huang J, Nasr M, Kim Y and Matthews HR (1992) Genistein inhibits protein histidine kinase. J Biol Chem 267: 15511–15515
Hunter T and Cooper JA (1985) Protein-tyrosine kinases. Annu Rev Biochem 54: 897–930
Johnson GL and Vaillancourt RR (1994) Sequential protein kinase reactions controlling cell growth and differentiation. Curr Opin Cell Biol 6: 230–238
Johnson LN and Barford D (1993) The effects of phosphorylation on the structure and function of proteins. Annu Rev Biophys Biomol Struct 22: 199–232
Kemp BE and Pearson RB (1990) Protein kinase recognition sequence motifs. Trends Biochem Sci 15: 342–346
Kühlbrandt W (1994) Structure and function of the plant lightharvesting complex, LHC-II. Curr Opin Struct Biol 4: 519–528
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685
Michel H, Hunt DF, Shabanowitz J and Bennett J (1988) Tandem mass spectrometry reveals that three Photosystem II proteins of spinach chloroplasts contain N-acetyl-O-phosphothreonine at their NH2 termini. J Biol Chem 263: 1123–1130
Mullet J (1983) The amino acid sequence of the polypeptide segment which regulates membrane adhesion (grana stacking) in chloroplasts. J Biol Chem 258: 9941–9948
Nilsson A, Stys D, Drakenberg T, Spangfort MD, Forsén S and Allen JF (1997) Phosphorylation controls the three-dimensional structure of plant light harvesting complex II. J Biol Chem 272: 18350–18357
Pearson RB and Kemp BE (1991) Protein kinase phosphorylation site sequences and consensus specificity motifs: Tabulations. In: Hunter T and Sefton BM (eds) Methods in Enzymology 200, pp 62–81. Academic Press, San Diego, California
Silverstein T, Cheng L and Allen JF (1993) Chloroplast thylakoid protein phosphatase reactions are redox-independent and kinetically heterogeneous. FEBS Lett 334: 101–105
Telfer A, Allen JF, Barber J and Bennett J (1983) Thylakoid protein phosphorylation during state 1-state 2 transitions in osmotically shocked pea chloroplasts. Biochim Biophys Acta 722: 176–181
Thornber JP (1975) Chlorophyll proteins light harvesting and reaction center components of plants. Ann Rev Plant Physiol 26: 127–158
Trojanek J, Ek P, Scoble J, Muszynska G and Engström L (1996) Phosphorylation of plant proteins and the identification of protein-tyrosine kinase activity in maize seedlings. Eur J Biochem 235: 338–344
Tullberg A, Håkansson G and Race HL (1998) A protein tyrosine kinase of chloroplast thylakoid membranes phosphorylates light harvesting complex II proteins. Biochem Biophys Res Commun 250: 617–622
Walker DA (1971) Chloroplasts (and grana): Aqueous (including high carbon fixation ability). In: San-Pietro A(ed) Methods in Enzymology 23, pp 211–220. Academic Press, London
Warner KM and Bullerjahn GS (1994) Light-dependent tyrosine phosphorylation in the cyanobacterium Prochlorothrix hollandica. Plant Physiol 105: 629–633
Xu Q, Fu HH, Gupta R and Luan S (1998) Molecular characterization of a tyrosine-specific protein phosphatase encoded by a stress-responsive gene in Arabidopsis [published erratum appears in Plant Cell 10: 1769]. Plant Cell 10: 849–857
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Forsberg, J., Allen, J.F. Protein tyrosine phosphorylation in the transition to light state 2 of chloroplast thylakoids. Photosynthesis Research 68, 71–79 (2001). https://doi.org/10.1023/A:1011891017067
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DOI: https://doi.org/10.1023/A:1011891017067