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Damage to the oxygen-evolving complex by superoxide anion, hydrogen peroxide, and hydroxyl radical in photoinhibition of photosystem II

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Abstract

Under strong illumination of a photosystem II (PSII) membrane, endogenous superoxide anion, hydrogen peroxide, and hydroxyl radical were successively produced. These compounds then cooperatively resulted in a release of manganese from the oxygen-evolving complex (OEC) and an inhibition of oxygen evolution activity. The OEC inactivation was initiated by an acceptor-side generated superoxide anion, and hydrogen peroxide was most probably responsible for the transportation of reactive oxygen species (ROS) across the PSII membrane from the acceptor-side to the donor-side. Besides ROS being generated in the acceptor-side induced manganese loss; there may also be a ROS-independent manganese loss in the OEC of PSII. Both superoxide anion and hydroxyl radical located inside the PSII membrane were directly identified by a spin trapping-electron spin resonance (ESR) method in combination with a lipophilic spin trap, 5-(diethoxyphosphoryl)-5-phenethyl-1-pyrroline N-oxide (DEPPEPO). The endogenous hydrogen peroxide production was examined by oxidation of thiobenzamide.

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Abbreviations

CAT:

Catalase

Chl:

Chlorophyll

Cyt b559 :

Cytochrome b559

DCBQ:

2,5-dichloro-1,4-benzoquinone

DEPMPO:

5-(diethoxyphosphoryl)-5-methyl-1-pyrroline N-oxide

DEPPEPO:

5-(diethoxyphosphoryl)-5-phenethyl-1-pyrroline N-oxide

DMSO:

Dimethyl sulfoxide

ESR:

Electron spin resonance

HX:

Hypoxanthine

Mes:

2-(N-morpholino) ethanesulfonic acid

1O2 :

Singlet oxygen

OEC:

Oxygen-evolving complex

P680 :

Photosystem II primary electron donor chlorophyll

PSI:

Photosystem I

PSII:

Photosystem II

PSII RC:

Photosystem II reaction center

QA and QB :

Primary and secondary quinone electron acceptor of photosystem II, respectively

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TCNE:

Tetracyanoethylene

XOD:

Xanthine oxidase

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Acknowledgements

The research was supported by the National Natural Science Foundation of China (No. 20473098) and the Pilot Project of Knowledge Innovation Program of CAS. We are very grateful to Frances Thompson, SynZyme Technologies in Irvine, CA, for the careful reading and the correction of the manuscript.

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Authors and Affiliations

  1. State Key laboratory for Structural Chemistry of Unstable and Stable Species, Center for Molecular Science, Institute of Chemistry, The Chinese Academy of Sciences, Beijing, 100080, China

    Yu Guang Song, Bin Liu, Lan Fen Wang & Yang Liu

  2. Graduate School, The Chinese Academy of Sciences, Beijing, 100080, China

    Yu Guang Song, Bin Liu, Lan Fen Wang & Yang Liu

  3. Swiss Federal Research Institute WSL, Zuercherstrasse 111, CH-8903, Birmensdorf, Switzerland

    Mai He Li

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  1. Yu Guang Song
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  2. Bin Liu
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Correspondence to Yang Liu.

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Song, Y.G., Liu, B., Wang, L.F. et al. Damage to the oxygen-evolving complex by superoxide anion, hydrogen peroxide, and hydroxyl radical in photoinhibition of photosystem II. Photosynth Res 90, 67–78 (2006). https://doi.org/10.1007/s11120-006-9111-7

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