Chlorophyll <i>a</i> is the crucial redox sensor and transmembrane signal transmitter in the cytochrome <i>b</i>₆<i>f</i> complex. Components and mechanisms of state transitions from the hydrophobic mismatch viewpoint

The cytochrome (cyt) <i>b</i>₆<i>f</i> complex is involved in the transmembrane redox signaling that triggers state transitions in cyanobacteria and chloroplasts. However, the components and molecular mechanisms are still unclear. In an attempt to solve this long-standing problem, we first focused on the unknown role of a single chlorophyll <i>a</i> (Chl<i>a</i>) in cyt <i>b</i>₆<i>f</i> with a new approach based on Chl<i>a</i> structural properties. Various <i>b</i>₆<i>f</i> X-ray crystal structures were analyzed to identify their differences, which correlate with differences in Chl<i>a</i> molecular volume. We found that the distance of the Rieske [2Fe-2S] cluster to Chl<i>a</i> correlates with the distance between a pair of residues at the <i>Q</i>_o-site and the distance between a pair of residues at the opposite membrane side. These correlations were accompanied by the rotation of a key peripheral residue and by changes in the hydrophobic thickness of cyt <i>b</i>₆<i>f</i>. Parallel analysis of cyt <i>bc</i>₁ crystal structures allowed us to conclude that Chl<i>a</i> acts as the crucial redox sensor and transmembrane signal transmitter in <i>b</i>₆<i>f</i> for changes in the plastoquinone pool redox state. The hydrophobic mismatch induced by the changed hydrophobic thickness of cyt <i>b</i>₆<i>f</i> is the driving force for the structural reorganizations of the photosynthetic apparatus during induction and the progression of state transitions in cyanobacteria and chloroplasts. A mechanism for LHCII kinase activation in chloroplasts is also proposed. Our understanding of the dynamic structural changes in <i>bc</i>-complexes during turnover at the <i>Q</i>_o-site and state transitions is augmented by the time-sequence ordering of 56 <i>bc</i> crystal structures.