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Proton-mediated photoprotection mechanism in photosystem II.

ABSTRACT: Photo-induced charge separation, which is terminated by electron transfer from the primary quinone Q_A to the secondary quinone Q_B, provides the driving force for O₂ evolution in photosystem II (PSII). However, the backward charge recombination using the same electron-transfer pathway leads to the triplet chlorophyll formation, generating harmful singlet-oxygen species. Here, we investigated the molecular mechanism of proton-mediated Q_A ^⋅- stabilization. Quantum mechanical/molecular mechanical (QM/MM) calculations show that in response to the loss of the bicarbonate ligand, a low-barrier H-bond forms between D2-His214 and Q_A ^⋅-. The migration of the proton from D2-His214 toward Q_A ^⋅- stabilizes Q_A ^⋅-. The release of the bicarbonate ligand from the binding Fe²⁺ site is an energetically uphill process, whereas the bidentate-to-monodentate reorientation is almost isoenergetic. These suggest that the bicarbonate protonation and decomposition may be a basis of the mechanism of photoprotection via Q_A ^⋅-/Q_AH^⋅ stabilization, increasing the Q_A redox potential and activating a charge-recombination pathway that does not generate the harmful singlet oxygen.

SUBMITTER: Sugo Y

PROVIDER: S-EPMC9490181 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Proton-mediated photoprotection mechanism in photosystem II.

Sugo Yu Y Ishikita Hiroshi H

Frontiers in plant science 20220907

Photo-induced charge separation, which is terminated by electron transfer from the primary quinone QA to the secondary quinone QB, provides the driving force for O2 evolution in photosystem II (PSII). However, the backward charge recombination using the same electron-transfer pathway leads to the triplet chlorophyll formation, generating harmful singlet-oxygen species. Here, we investigated the molecular mechanism of proton-mediated QA ⋅- st ...[more]

PMID: 36161009

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Project description:Although light is essential for photosynthesis, when in excess, it may damage the photosynthetic apparatus, leading to a phenomenon known as photoinhibition. Photoinhibition was thought as a light-induced damage to photosystem II; however, it is now clear that even photosystem I may become very vulnerable to light. One main characteristic of light induced damage to photosystem II (PSII) is the increased turnover of the reaction center protein, D1: when rate of degradation exceeds the rate of synthesis, loss of PSII activity is observed. With respect to photosystem I (PSI), an excess of electrons, instead of an excess of light, may be very dangerous. Plants possess a number of mechanisms able to prevent, or limit, such damages by safe thermal dissipation of light energy (non-photochemical quenching, NPQ), slowing-down of electron transfer through the intersystem transport chain (photosynthesis-control, PSC) in co-operation with the Proton Gradient Regulation (PGR) proteins, PGR5 and PGRL1, collectively called as short-term photoprotection mechanisms, and the redistribution of light between photosystems, called state transitions (responsible of fluorescence quenching at PSII, qT), is superimposed to these short term photoprotective mechanisms. In this manuscript we have generated a number of higher order mutants by crossing genotypes carrying defects in each of the short-term photoprotection mechanisms, with the final aim to obtain a direct comparison of their role and efficiency in photoprotection. We found that mutants carrying a defect in the ΔpH-dependent photosynthesis-control are characterized by photoinhibition of both photosystems, irrespectively of whether PSBS-dependent NPQ or state transitions defects were present or not in the same individual, demonstrating the primary role of PSC in photoprotection. Moreover, mutants with a limited capability to develop a strong PSBS-dependent NPQ, were characterized by a high turnover of the D1 protein and high values of Y(NO), which might reflect energy quenching processes occurring within the PSII reaction center.

Dataset Information

Proton-mediated photoprotection mechanism in photosystem II.

Publications

Proton-mediated photoprotection mechanism in photosystem II.

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