Subunit and chlorophyll organization of the plant photosystem II supercomplex

Abstract

Photosystem II (PSII) is a light-driven protein, involved in the primary reactions of photosynthesis. In plant photosynthetic membranes PSII forms large multisubunit supercomplexes, containing a dimeric core and up to four light-harvesting complexes (LHCs), which act as antenna proteins. Here we solved a three-dimensional (3D) structure of the C2S2M2 supercomplex from Arabidopsis thaliana using cryo-transmission electron microscopy (cryo-EM) and single-particle analysis at an overall resolution of 5.3 Å. Using a combination of homology modelling and restrained refinement against the cryo-EM map, it was possible to model atomic structures for all antenna complexes and almost all core subunits. We located all 35 chlorophylls of the core region based on the cyanobacterial PSII structure, whose positioning is highly conserved, as well as all the chlorophylls of the LHCII S and M trimers. A total of 13 and 9 chlorophylls were identified in CP26 and CP24, respectively. Energy flow from LHC complexes to the PSII reaction centre is proposed to follow preferential pathways: CP26 and CP29 directly transfer to the core using several routes for efficient transfer; the S trimer is directly connected to CP43 and the M trimer can efficiently transfer energy to the core through CP29 and the S trimer.

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Figure 1: Architecture of the C2S2M2 particle at an average resolution of 5.3 Å.
Figure 2: Location of all the different subunits of the C2S2M2 particle.
Figure 3: Chlorophylls of the supercomplex.
Figure 4: Flexibilities in the C2S2M2 supercomplex from Arabidopsis investigated by negative stain single-particle electron microscopy.
Figure 5: Energy flow within C2S2M2 particles.

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Acknowledgements

This work was supported by the FOM program ‘The thylakoid membrane—a dynamic switch (10TM02)’. S.C. is supported by the French National Research Agency Grant ANR-12-JSV8-0001-01. R.K. is supported by a Marie Curie Career Integration Grant call FP7-PEOPLE-2012-CIG and by grant LO1204 (Sustainable development of research in the Centre of the Region Haná). We acknowledge L. Franken and J. Dekker for discussions.

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L.S.v.B., G.T.O. and E.J.B. designed the research. S.C. isolated the supercomplex, L.S.v.B. and G.T.O. collected the data. L.S.v.B. performed the single-particle analysis. L.S.v.B., S.C., G.T.O. and A.-M.W.H.T. analysed the data. R.S.K and R.K. analysed the negative stain supercomplex data. L.S.v.B., S.C., G.T.O., A.-M.W.H.T. and E.J.B. wrote the article.

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Correspondence to Egbert J. Boekema.

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The authors declare no competing financial interests.

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van Bezouwen, L., Caffarri, S., Kale, R. et al. Subunit and chlorophyll organization of the plant photosystem II supercomplex. Nature Plants 3, 17080 (2017). https://doi.org/10.1038/nplants.2017.80

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