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Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection

Nature Plants volume 7, pages 979–988 (2021)Cite this article

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Abstract

In photosynthetic thylakoid membranes the proton motive force (pmf) not only drives ATP synthesis, in addition it is central to controlling and regulating energy conversion. As a consequence, dynamic fine-tuning of the two pmf components, electrical (Δψ) and chemical (ΔpH), is an essential element for adjusting photosynthetic light reactions to changing environmental conditions. Good evidence exists that the Δψ/ΔpH partitioning is controlled by thylakoid potassium and chloride ion transporters and channels. However, a detailed mechanistic understanding of how these thylakoid ion transporter/channels control pmf partitioning is lacking. Here, we combined functional measurements on potassium and chloride ion transporter and channel loss-of-function mutants with extended mathematical simulations of photosynthetic light reactions in thylakoid membranes to obtain detailed kinetic insights into the complex interrelationship between membrane energization and ion fluxes across thylakoid membranes. The data reveal that potassium and chloride fluxes in the thylakoid lumen determined by the K+/H+ antiporter KEA3 and the voltage-gated Cl− channel VCCN1/Best1 have distinct kinetic responses that lead to characteristic and light-intensity-dependent Δψ/ΔpH oscillations. These oscillations fine-tune photoprotective mechanisms and electron transport which are particularly important during the first minutes of illumination and under fluctuating light conditions. By employing the predictive power of the model, we unravelled the functional consequences of changes in KEA3 and VCCN1 abundance and regulatory/enzymatic parameters on membrane energization and photoprotection.

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Fig. 1: NPQ characteristics in KEA3, VCCN1 and Clce mutants.
Fig. 2: Testing the independence of KEA3, VCCN1 and ClCe functionality.
Fig. 3: Computer model of photosynthetic light harvesting coupled to CO2 fixation in the Calvin–Benson cycle.
Fig. 4: Specific role of KEA3 and VCCN1 for thylakoid energization and ion fluxes calculated from our mathematical model.
Fig. 5: Computer simulation for the functional characterization and regulation of KEA3 and VCCN1.

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Data availability

The data sets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Code availability

The computer code for our model is available online. A link is provided in Supplementary Information.

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Acknowledgements

We thank M. Wood and Dr D. Schneider at the WSU Plant Phenomics facilities for their assistance in acquiring phenotyping data. The work was mainly supported by a US Department of Energy grant (DE-SC0017160) to H.K. and H.-H.K. Additional support from the National Science Foundation (MCB-1616982) and USDA-NIFA (#1005351 and #0119) to H.K. and by the 3rd ERA-CAPS call via the NSF PGRP programme (IOS-1847382, 1847193) to H.-H.K. and D.M.K. is acknowledged. Support for modelling work at MSU was supported by award #1847193 from the National Science Foundation. The project was also made possible thanks to a Murdock trust equipment grant (# SR-2016049) to H.-H.K. and H.K.

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  1. Meng Li

    Present address: School of Oceanography, University of Washington, Seattle, WA, USA

Authors and Affiliations

  1. Institute of Biological Chemistry, Washington State University, Pullman, WA, USA

    Meng Li, Vaclav Svoboda & Helmut Kirchhoff

  2. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA

    Geoffry Davis & David Kramer

  3. Department of Biochemistry, Michigan State University, East Lansing, MI, USA

    David Kramer

  4. School of Biological Sciences, Washington State University, Pullman, WA, USA

    Hans-Henning Kunz

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Contributions

M.L., V.S., G.D. and H.-H.K. performed experiments and analysed data. M.L. G.D., D.K. H.-H.K. and H.K. designed the study. H.K. wrote the manuscript.

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Correspondence to Helmut Kirchhoff.

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Peer review information Nature Plants thanks Conrad Mullineaux, Toshiharu Shikanai and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Methods, Supplementary Figs. 1–10, Supplementary References.

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Li, M., Svoboda, V., Davis, G. et al. Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection. Nat. Plants 7, 979–988 (2021). https://doi.org/10.1038/s41477-021-00947-5

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