A holistic quantitative understanding of state transition in plant photosynthesis

Efficient and safe harvesting of sunlight by photosynthesis in plant thylakoid membranes requires that both photosystems (PS)I and PSII operate with similar electron turnover rates. This is realized by state transition encompassing the redistribution of light-harvesting complexes II (LHCII) between the spatially separated PSII (mainly in stacked grana thylakoids) and PSI (mainly in unstacked domains). Here, we provide a quantitative holistic view on lateral protein and pigment reorganizations within the thylakoid membrane network induced by state transitions and the role of reversible protein phosphorylation for this process. The data reveals that plants can perfectly balance electron fluxes through both photosystems by the redistribution of a certain pool of hyperphosphorylated LHCII from PSII in stacked to PSI in unstacked thylakoid membranes. Force balance analysis predicts that the photosystems antenna reorganization is not realized by a phosphorylation induced stimulation of lateral mobility of LHCII but likely by vertical unstacking. Shuffling of phospho-LHCII during state transition results in remodeling of the PSI supercomplex landscape but not of the PSII landscape supporting the notion that only a loosely bound pool of LHCIIs is involved in state transition.