Figure 8. Schemes for the trans-thylakoid Δψ-induced acceleration of recombination reactions in PSII and subsequent production of 1O2.
(A) The relative positions of PSII electron transfer cofactors with respect to the electric field (double-headed arrow) imposed across the thylakoid membrane (dotted lines). The red and blue arrows indicate the Δψ-induced changes in the equilibrium constant for the sharing of electrons (−) between QA and Pheo, and electron holes (+) among P+ and the oxygen evolving complex. Excitation of PSII by light leads to formation of excited chlorophyll states (P*), the excitation is shared over the 4 chlorophylls and the 2 pheophytins. Charge separation occurs between more than one pair of pigments, so at short times the situation is not well defined, but ChlD1+Pheo D1− appears to be the dominant radical pair. Secondary electron transfer events occur forming PD1+PheoD1−, the second radical pair, which is present in nearly all centers. This radical pair is stabilized by electron transfer from Pheo− to QA forming PD1+QA−. This radical pair is further stabilized by electron transfer from D1Tyr161 (TyrZ) forming a neutral tyrosyl radical, which oxidizes the Mn cluster of the oxygen evolving complex to form the state Sn+1QA−. Finally, QA− reduces QB to form Sn+1QB-. Upon a second PSII turnover the double reduced and protonated QB plastohydroquinone becomes protonated and is exchanged with an oxidized plastoquinone from the membrane pool (black arrows). The illustration was based on crystal structure 3WU2 (Umena et al., 2011). (B) The charge separation states described above are unstable and recombination competes with the energy-storing reactions. When PD1+ is present, recombination reactions can occur by several pathways as indicated by the dashed lines: (1) direct electron transfer from QA− to P+ (R1); (2) by the back reaction to form the P+Pheo− state, which can then recombine directly (R2) or, (3) when the P+Pheo− radical pair is present as a triplet state, 3[P+Pheo−], the dominant state when formed by the back-reaction, 3[P+Pheo−] charge recombination forms 3P (R3), a long lived chlorophyll triplet that can easily interact with O2 to form 1O2; (4) complete reversal of electron transfer can also occur, repopulating P* (R4), which can return to the ground state by emitting fluorescence (luminescence) or heat. Route 3, the triplet generating pathway, is the dominant recombination route in fully functional PSII. For simplicity the 3[P+Phe-] is not distinguised from the singlet form in this scheme. A Δψ across the membrane should destabilize P+QA− relative to the other states (see dotted blue lines), affecting the rates of reactions indicated in the green versus red. A Δψ across the membrane should also destabilize P+Pheo−, but because of the smaller dielectric span across the membrane, to a lesser extent than P+QA−. Thus, the buildup of Δψ should shift the equilibrium constant for sharing electrons between QA− and Pheo, favoring the formation of Pheo− and thus increasing the rate of recombination through R3 (as well as the R2 and R4), resulting in increased production of 3P and 1O2. Destabilization of P+QA− will also increase the driving force for P+QA− recombination via R1, however this recombination is already driven by 1.4eV and it is thus likely to be in the Marcus inverted region. Thus increasing the driving force will slow recombination by this route.