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Dynamical and allosteric regulation of photoprotection in light harvesting complex II

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Abstract

Major light-harvesting complex of photosystem II (LHCII) plays a dual role in light-harvesting and excited energy dissipation to protect photodamage from excess energy. The regulatory switch is induced by increased acidity, temperature or both. However, the molecular origin of the protein dynamics at the atomic level is still unknown. We carried out temperature-jump time-resolved infrared spectroscopy and molecular dynamics simulations to determine the energy quenching dynamics and conformational changes of LHCII trimers. We found that the spontaneous formation of a pair of local α-helices from the 310-helix E/loop and the C-terminal coil of the neighboring monomer, in response to the increased environmental temperature and/or acidity, induces a scissoring motion of transmembrane helices A and B, shifting the conformational equilibrium to a more open state, with an increased angle between the associated carotenoids. The dynamical and allosteric conformation change leads to close contacts between carotenoid lutein 1 and chlorophyll pigment 612, facilitating the fluorescence quenching. Based on these results, we suggest a unified mechanism by which the LHCII trimer controls the dissipation of excess excited energy in response to increased temperature and acidity, as an intrinsic result of intense sun light in plant photosynthesis.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (21433014, 11721404, 21533003), the Ministry of Science and Technology (2017YFB0203400), Chinese Academy of Sciences Innovation Program (KJCX2-YW-W25) and the National Institutes of Health (GM46736, GM64742). Y.W. thanks Prof. Tingyun Kuang for encouragement, Prof. Xinguang Zhu for in-depth discussion, Prof. Chunhong Yang for the single-site mutant S123G sample, and Miss Ju Wang and Prof. Shufeng Wang from Peking University for the help in streak camera measurement.

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  1. These authors contributed equally to this work.

Authors and Affiliations

  1. Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing, 100190, China

    Hao Li, Manping Ye, Shanshan Li, Deyong Li, Mohan Wang, Luchao Du, Heng Li & Yuxiang Weng

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Hao Li, Mohan Wang & Yuxiang Weng

  3. Shenzhen Bay Laboratory, Shenzhen, 518055, China

    Yingjie Wang & Jiali Gao

  4. Department of Chemistry and Supercomputing Institute, University of Minnesota, Minneapolis, MN, 55455, USA

    Yingjie Wang, Haisheng Ren, Gianluigi Veglia & Jiali Gao

  5. Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA

    Yingjie Wang & Gianluigi Veglia

  6. Laboratory of Computational Chemistry and Drug Design, State Key Laboratory of Chemical Oncogenomics, Peking University Shenzhen Graduate School, Shenzhen, 518055, China

    Jiali Gao

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  1. Hao Li
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Li, H., Wang, Y., Ye, M. et al. Dynamical and allosteric regulation of photoprotection in light harvesting complex II. Sci. China Chem. 63, 1121–1133 (2020). https://doi.org/10.1007/s11426-020-9771-2

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