QA and QB reduction states induce protein dynamics underlying the dual phase fluorescence rise in Photosystem II.

Abstract

In photosystem II (PSII) chlorophyll (Chl) fluorescence yield (F) rises during low-to-high light induction. Based on a critical review of the literature, the following evidence is summarized. (1) As the primary acceptor quinone Q_A gets reduced, fluorescence immediately rises to F_c =1.8 F_o. (2) During microseconds of illumination following Q_A reduction, F_c rises to F_f where excitation is terminated via carotenoid triplet states (³Car). (3) After many milliseconds of illumination, as the secondary acceptor quinone Q_B is reduced, fluorescence rises to a maximum F_m, wherein excitation is still terminated via ³Car. This dual phase fluorescence rise is driven by protein conformation changes. The two phases suggest that the C2S2M2 structure of the PSII dimer (Caffarri et al. 2009) may be rewritten as 2SCM such that for a monomer the arrangement is S - CP43 - D1D2 - CP47 - M. The D1- and D2- antenna branches are excitonically separated. Fluorescence of the D1 pigment-protein branch rises during microseconds after Q_A reduction, that of the D2 branch rises on a time scale of milliseconds during Q_B reduction. A hypothesis is proposed here based on electrostatic profiling of photosynthetic pigments (Sirohiwal et al. 2021; Saito et al. 2023). When acceptor quinones are oxidized excitation flows through the stromal Chl layer of Chl-proteins CP43 and CP47 to the photochemical Pheophytin/Chl based reaction center. As Q_A gets reduced during microseconds in CP43, and Q_B gets reduced during milliseconds in CP47, an associated dynamic signal induces protein conformation changes shifting excitations from the stromal to the lumenal Chl layer. With this, excitation becomes diverted from the photosynthetic reaction center and connected to the characteristically lumenal ChlZ_D1 and ChlZ_D2. Together with their nearby Car_D1 and Car_D2 these ChlsZ form quenching centers, terminating excitation via ³Car with a lifetime of about 1 ns, sufficient to induce the maximum F_m fluorescence.