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Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution

Nature volume 534, pages 6974 (02 June 2016) | Download Citation

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Abstract

During photosynthesis, the plant photosystem II core complex receives excitation energy from the peripheral light-harvesting complex II (LHCII). The pathways along which excitation energy is transferred between them, and their assembly mechanisms, remain to be deciphered through high-resolution structural studies. Here we report the structure of a 1.1-megadalton spinach photosystem II–LHCII supercomplex solved at 3.2 Å resolution through single-particle cryo-electron microscopy. The structure reveals a homodimeric supramolecular system in which each monomer contains 25 protein subunits, 105 chlorophylls, 28 carotenoids and other cofactors. Three extrinsic subunits (PsbO, PsbP and PsbQ), which are essential for optimal oxygen-evolving activity of photosystem II, form a triangular crown that shields the Mn4CaO5-binding domains of CP43 and D1. One major trimeric and two minor monomeric LHCIIs associate with each core-complex monomer, and the antenna–core interactions are reinforced by three small intrinsic subunits (PsbW, PsbH and PsbZ). By analysing the closely connected interfacial chlorophylls, we have obtained detailed insights into the energy-transfer pathways between the antenna and core complexes.

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Change history

  • 01 June 2016

    The received date year was corrected from 2015 to 2016.

Accessions

Primary accessions

Electron Microscopy Data Bank

Protein Data Bank

Data deposits

The cryo-EM map of the spinach PSII–LHCII supercomplex has been deposited in the Electron Microscopy Data Bank with accession code EMD-6617. The corresponding structure model has been deposited in the Protein Data Bank under accession code 3JCU.

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Acknowledgements

We thank J. P. Zhang and X. L. Zhao for their assistance in preparing thylakoid samples. Cryo-EM data collection was carried out at the Center for Biological Imaging, Core Facilities for Protein Science at the Institute of Biophysics (IBP), Chinese Academy of Sciences (CAS), and at the National Center for Protein Science Shanghai (NCPSS), Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences/Shanghai Science Research Center, Chinese Academy of Sciences, Shanghai, China. We thank X. J. Huang, G. Ji, W. Ding, F. Sun, and other staff members at the Center for Biological Imaging (IBP, CAS); L. L. Kong, X. Y. Shi, Y. N. He, J. P. Ding, and M. Lei for their support during data collection; X. B. Liang and X. M. An for support in organizing data collection trips; F. L. Zhang, J. Zhou, and Y. Li for support in measuring the oxygen evolution activity; L. L. Niu and X. Ding for mass spectrometry; J. H. Li for assistance in fluorescence measurement; R. Bassi, A. Pinnola and R. Croce for sharing experiences in purifying plant PSII–LHCII supercomplexes; and Y. Xiang for advice on cryo-EM sample preparation and structure refinement. The project was funded by National 973 project grant 2011CBA00900, the Strategic Priority Research Program of CAS (XDB08020302) and National Natural Science Foundation of China (31570724, 31270793 and 31170703). Z.L. and X.Z. received scholarships from the ‘National Thousand (Young) Talents Program’ from the Office of Global Experts Recruitment in China.

Author information

Author notes

    • Xuepeng Wei
    •  & Xiaodong Su

    These authors contributed equally to this work.

Affiliations

  1. National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China

    • Xuepeng Wei
    • , Xiaodong Su
    • , Peng Cao
    • , Xiuying Liu
    • , Wenrui Chang
    • , Mei Li
    • , Xinzheng Zhang
    •  & Zhenfeng Liu
  2. University of Chinese Academy of Sciences, Beijing 100049, China

    • Xuepeng Wei
    •  & Xiuying Liu

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Contributions

X.W., X.S., P.C. and X.L. purified the spinach PSII–LHCII supercomplex; M.L. and P.C. characterized the spectroscopic features, protein and pigment contents, and oxygen-evolving activity of the samples; X.W., X.S. and X.Z. collected and processed cryo-EM data; X.Z. reconstructed the 3.2 Å resolution map and supervised cryo-EM structure determination; X.W. and Z.L. built and refined the structure model; X.W., M.L., X.Z. and Z.L. analysed the structure; Z.L. and W.C. conceived and coordinated the project; and the manuscript was written by X.W., M.L., X.Z. and Z.L.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Mei Li or Xinzheng Zhang or Zhenfeng Liu.

Reviewer Information Nature thanks Roberta Croce, Jian-Ren Shen and Thomas Walz for their contribution to the peer review of this work.

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    Supplementary Figure 1

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https://doi.org/10.1038/nature18020

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