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Surface charge dynamics in photosynthetic membranes and the structural consequences

Nature Plants volume 3, Article number: 17020 (2017) Cite this article

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Matters Arising to this article was published on 11 March 2021

Abstract

The strict stacking of plant photosynthetic membranes into granal structures plays a vital role in energy conversion. The molecular forces that lead to grana stacking, however, are poorly understood. Here we evaluate the interplay between repulsive electrostatic (Fel) and attractive van der Waals (FvdWaals) forces in grana stacking. In contrast to previous reports, we find that the physicochemical balance between attractive and repulsive forces fully explains grana stacking. Extending the force balance analysis to lateral interactions within the oxygen-evolving photosystem II (PSII)–light harvesting complex II (LHCII) supercomplex reveals that supercomplex stability is very sensitive to Fel changes. Fel is highly dynamic, increasing up to 1.7-fold on addition of negative charges by phosphorylation of grana-hosted proteins. We show that this leads to specific destabilization of the supercomplex, and that changes in Fel have contrasting effects on vertical stacking and lateral intramembrane organization. This enables discrete biological control of these central structural features.

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Figure 1: Approach for σ quantification at the stromal side of the grana membrane.
Figure 2: Interaction forces involved in grana stacking.
Figure 3: Lateral interaction forces within C2S2M2.
Figure 4: The calculated equilibrium membrane–membrane separation distances in grana.

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Acknowledgements

This work was supported by grants to H.K. from the National Science Foundation (NSF-MCB-1616982) the US Department of Energy (DE-SC 0017160), the US Department of Agriculture (ARC grant WNP00775) and Washington State University. B.v.O. acknowledges financial support by the Netherlands Organisation for Scientific Research (NWO) through a Veni grant to B.v.O and a Vici grant to R. Croce. We thank P. Malý for help with calculating intermembrane electrostatic force. Finally, we thank G. Schoenknecht (Stillwater, OK, USA) and R. Fristedt (Amsterdam, The Netherlands) for their valuable comments and helpful suggestions.

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  1. Sujith Puthiyaveetil

    Present address: †Present address: Department of Biochemistry, Purdue University, 175 South University Street, West Lafayette, Indiana 47907, USA,

  2. Sujith Puthiyaveetil and Bart van Oort: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Biological Chemistry, Washington State University, PO Box 646340, Pullman, 99164-6340, Washington, USA

    Sujith Puthiyaveetil & Helmut Kirchhoff

  2. Department of Physics and Astronomy, Biophysics of Photosynthesis, Faculty of Sciences, Vrije Universiteit Amsterdam, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands

    Bart van Oort

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S.P., B.v.O., H.K. designed and performed the research. H.K. wrote the paper.

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Correspondence to Helmut Kirchhoff.

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Puthiyaveetil, S., van Oort, B. & Kirchhoff, H. Surface charge dynamics in photosynthetic membranes and the structural consequences. Nature Plants 3, 17020 (2017). https://doi.org/10.1038/nplants.2017.20

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