Regulation of light harvesting in Chlamydomonas: two protein phosphatases are involved in state transitions

Protein phosphorylation plays important roles in short-term regulation of photosynthetic electron transfer. In a mechanism known as state transitions, the kinase STATE TRANSITION 7 (STT7) of Chlamydomonas reinhardtii phosphorylates components of light-harvesting antenna complex II (LHCII). This reversible phosphorylation governs the dynamic allocation of a part of LHCII to photosystem I or photosystem II, depending on light conditions and metabolic demands. Little is however known in the green alga on the counteracting phosphatase(s). In Arabidopsis, the homologous kinase STN7 is specifically antagonized by PROTEIN PHOSPHATASE 1/THYLAKOID-ASSOCIATED PHOSPHATASE 38 (PPH1/TAP38). Furthermore, the paralogous kinase STN8 and the countering phosphatase PHOTOSYSTEM II PHOSPHATASE (PBCP), which count subunits of PSII amongst their major targets, influence thylakoid architecture and high-light tolerance. Here we analyze state transitions in C. reinhardtii mutants of the two homologous phosphatases, CrPPH1 and CrPBCP. The transition from state 2 to state 1 is retarded in pph1, and surprisingly also in pbcp. However both mutants can eventually return to state 1. In contrast, the double mutant pph1;pbcp appears strongly locked in state 2. The complex phosphorylation patterns of the LHCII trimers and of the monomeric subunits are affected in the phosphatase mutants. Their analysis indicates that the two phosphatases have different yet overlapping sets of protein targets. The dual control of thylakoid protein de-phosphorylation and the more complex antenna phosphorylation patterns in Chlamydomonas compared to Arabidopsis are discussed in the context of the stronger amplitude of state transitions and the more diverse LHCII isoforms in the alga.