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Submitted on February 22, 2006
Division of Cell Biology, Linköping University, Linköping SE-581 85
Corresponding Author: aleve{at}ibk.liu.se
Mapping of in vivo protein phosphorylation sites in photosynthetic membranes of the green alga Chlamydomonas reinhardtii revealed that the major environmentally-dependent changes in phosphorylation are clustered at the interface between the photosystem II (PSII) core and its light-harvesting antennae (LHCII, CP26 and CP29). The photosynthetic membranes were isolated form the algal cells exposed to four distinct environmental conditions affecting photosynthesis: (i) dark aerobic, corresponding to photosynthetic State 1; (ii) dark under nitrogen atmosphere, corresponding to photosynthetic State 2; (iii) moderate light; (iv) high light. The surface-exposed phosphorylated peptides were cleaved from the membrane by trypsin, methyl-esterified, enriched by immobilized metal affinity chromatography and sequenced by nanospray-quadrupole-time-of-flight mass spectrometry. A total of nineteen in vivo phosphorylation sites have been mapped in the proteins corresponding to fifteen genes in C. reinhardtii. N-terminal acetylation of seven proteins has been concomitantly determined. Sequenced N-termini of six mature LHCII proteins differed from the predicted ones. The State 1-to-State 2 transition induced phosphorylation of the PSII core components D2 and PsbR, quadruple phosphorylation of a minor LHCII antennae subunit CP29, as well as phosphorylation of constituents of a major LHCII complex, Lhcbm1 and Lhcbm10. Exposure of the algal cells to either moderate or high light caused additional phosphorylation of the D1 and CP43 proteins of the PSII core. The high light treatment led to specific hyperphosphorylation of CP29 at seven distinct residues, phosphorylation of another minor LHCII constituent CP26 at a single threonine, and double phosphorylation of additional subunits of a major LHCII complex including Lhcbm4, Lhcbm6, Lhcbm9 and Lhcbm11. Environmentally-induced protein phosphorylation at the interface of PSII core and the associated antenna proteins, particularly multiple differential phosphorylation of CP29 linker protein, suggests the mechanisms for control of photosynthetic State transitions and for LHCII uncoupling from PSII under high light stress to allow thermal energy dissipation.
Revised on April 21, 2006
Accepted on May 2, 2006
Environmentally-modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii
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