Abstract
The heart of oxygenic photosynthesis is the water-splitting photosystem II (PSII), which forms supercomplexes with a variable amount of peripheral trimeric light-harvesting complexes (LHCII). Our knowledge of the structure of green plant PSII supercomplex is based on findings obtained from several representatives of green algae and flowering plants; however, data from a non-flowering plant are currently missing. Here we report a cryo-electron microscopy structure of PSII supercomplex from spruce, a representative of non-flowering land plants, at 2.8 Å resolution. Compared with flowering plants, PSII supercomplex in spruce contains an additional Ycf12 subunit, Lhcb4 protein is replaced by Lhcb8, and trimeric LHCII is present as a homotrimer of Lhcb1. Unexpectedly, we have found α-tocopherol (α-Toc)/α-tocopherolquinone (α-TQ) at the boundary between the LHCII trimer and the inner antenna CP43. The molecule of α-Toc/α-TQ is located close to chlorophyll a614 of one of the Lhcb1 proteins and its chromanol/quinone head is exposed to the thylakoid lumen. The position of α-Toc in PSII supercomplex makes it an ideal candidate for the sensor of excessive light, as α-Toc can be oxidized to α-TQ by high-light-induced singlet oxygen at low lumenal pH. The molecule of α-TQ appears to shift slightly into the PSII supercomplex, which could trigger important structure–functional modifications in PSII supercomplex. Inspection of the previously reported cryo-electron microscopy maps of PSII supercomplexes indicates that α-Toc/α-TQ can be present at the same site also in PSII supercomplexes from flowering plants, but its identification in the previous studies has been hindered by insufficient resolution.
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Data availability
The mass spectrometry proteomic data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the identifier PXD035272. The cryo-EM map of the spruce PSII supercomplex has been deposited in the Electron Microscopy Data Bank with accession code EMD-16389. The corresponding structure model has been deposited in the PDB under PDB code 8C29.
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Acknowledgements
This work was supported by the Grant Agency of the Czech Republic (project no. 21-05497S to M.O., P.I., P.P., I.I. and R.K.) and the European Regional Development Fund (ERDF) project ‘Plants as a tool for sustainable global development’ (no. CZ.02.1.01/0.0/0.0/16_019/0000827 to M.O., P.I., P.P., R.K., S.Ć.Z. and P.T.). We acknowledge support by the Federal Ministry for Education and Research (BMBF, ZIK programme) (grant nos. 03Z22HN23, 03Z22HI2 and 03COV04 to P.L.K.), Horizon Europe ERA Chair ‘hot4cryo’ project number 101086665 to P.L.K., the European Regional Development Funds for Saxony-Anhalt (grant no. EFRE: ZS/2016/04/78115 to P.L.K.), funding by the Deutsche Forschungsgemeinschaft (DFG) (project number 391498659 and RTG 2467 to P.L.K.), and the Martin-Luther University of Halle-Wittenberg. This work was also funded by project no. RO0423 to S.Ć.Z. and P.T. (Sustainable systems and technologies, improving crop production for higher quality of production of food, feed, and raw materials, under conditions of changing climate) funded by the Ministry of Agriculture, Czechia. CIISB, Instruct-CZ Centre of Instruct-ERIC EU consortium, funded by MEYS CR infrastructure project LM2023042 and European Regional Development Fund-Project ‘UP CIISB’ (no. CZ.02.1.01/0.0/0.0/18_046/0015974), is gratefully acknowledged for the financial support of the measurements at the CEITEC Proteomics Core Facility. We thank L. Hloušková and J. Bartoš for help with FRET rate calculation. This paper is dedicated to Professor Emeritus Jan Nauš for his outstanding contribution to the development of biophysics at Palacký University.
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M.O., D.K., P.I., P.P, P.L.K. and R.K., study design. M.O., D.A.S., F.L.K. and F.H., sample preparation for cryo-EM. D.A.S., image analysis of cryo-EM data. D.K. and R.K., model building. M.O. and I.I., amino acid sequence analysis. P.R., mass spectrometry analysis. P.T. and S.Ć.Z., fatty acid composition. P.T. and S.Ć.Z., α-tocopherol(quinone) analysis. M.O., D.K., P.I., P.P. I.I. and R.K., data interpretation. M.O., D.A.S., P.I., I.I. and R.K. wrote the main body of the paper, and all authors revised and approved it.
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A description of MS analysis and Supplementary Figs. 1–14, Tables 1–6 and References.
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Opatíková, M., Semchonok, D.A., Kopečný, D. et al. Cryo-EM structure of a plant photosystem II supercomplex with light-harvesting protein Lhcb8 and α-tocopherol. Nat. Plants 9, 1359–1369 (2023). https://doi.org/10.1038/s41477-023-01483-0
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DOI: https://doi.org/10.1038/s41477-023-01483-0
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