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State transitions redistribute rather than dissipate energy between the two photosystems in Chlamydomonas

Nature Plants volume 2, Article number: 16031 (2016) Cite this article

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Abstract

Photosynthesis converts sunlight into biologically useful compounds, thus fuelling practically the entire biosphere. This process involves two photosystems acting in series powered by light harvesting complexes (LHCs) that dramatically increase the energy flux to the reaction centres. These complexes are the main targets of the regulatory processes that allow photosynthetic organisms to thrive across a broad range of light intensities. In microalgae, one mechanism for adjusting the flow of energy to the photosystems, state transitions, has a much larger amplitude than in terrestrial plants, whereas thermal dissipation of energy, the dominant regulatory mechanism in plants, only takes place after acclimation to high light. Here we show that, at variance with recent reports, microalgal state transitions do not dissipate light energy but redistribute it between the two photosystems, thereby allowing a well-balanced influx of excitation energy.

Oxygenic photosynthesis requires two photosystems, photosystem II (PSII) and I (PSI), acting in series to catalyse the transfer of electrons from water to CO2. These two membrane-bound complexes convert light energy, by means of electron and proton transfer reactions, into electrochemical energy and ultimately into biologically useful free energy1. But before being converted, light energy must be captured, and the catalytic feat that these complexes achieve would be limited without the LHCs that increase the flux they sustain by more than two orders of magnitude funnelling light energy to the photochemical converters and thereby enhancing their absorption cross-section (reviewed in ref. 2).

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Figure 1: Kinetics of P700 oxidation in a ΔPC C. reinhardtii mutant.
Figure 2: Comparison of the changes in the PSII and PSI antenna size on state I to state II transitions using different approaches as detailed in the main text.
Figure 3: Evolution, as a function of the time after induction of state transitions, of the fast and slow components in the oxidation kinetics of P700 in the ΔPC mutant.
Figure 4: A quantitative schematic of photosystem and antenna distribution heterogeneity, and of its change during state transitions, in C. reinhardtii.

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Acknowledgements

We thank S. Bujaldon for the ΔPC-WT cross. W.J.N., F.-A.W. and F.R. acknowledge the support of CNRS and Université Pierre et Marie Curie. This work was supported by the Initiative d'Excellence programme from the French State (grant DYNAMO, ANR-11-LABX-0011-01) and by the programme PHC PROCOPE 2014 PROJET no. 30729YB. W.J.N. is a recipient of a PhD fellowship from the Université Pierre et Marie Curie. S.S. acknowledges the support from the DYNAMO ANR-11-LABX-0011-01 grant for travel. L.M. was a recipient of the Studienstiftung des Deutschen Volkes fellowship for her Master studies. Fabrice Rappaport deceased before final acceptance of this manuscript. His co-authors wish to acknowledge his remarkable contributions to our current understanding of photosynthesis regulations.

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Author notes

  1. Laura Mosebach

    Present address: †Present address: Munster University, Institute of Plant Biology & Biotechnology, D-48143 Muenster, Germany,

  2. Wojciech J. Nawrocki and Stefano Santabarbara: These authors contributed equally to the work

  3. Fabrice Rappaport: Deceased.

Authors and Affiliations

  1. Institut de Biologie Physico-Chimique, UMR 7141 CNRS-UPMC, 13 rue P. et M. Curie 75005, Paris, France

    Wojciech J. Nawrocki, Laura Mosebach, Francis-André Wollman & Fabrice Rappaport

  2. Istituto di Biofisica, Consiglio Nazionale delle Ricerche, Via Celoria 26, 20133 Milan, Italy

    Stefano Santabarbara

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  1. Wojciech J. Nawrocki
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Contributions

W.J.N., S.S., L.M. performed the experiments. F.-A.W. and F.R. conceived and designed the research. All of the authors discussed, analysed the data and wrote the paper.

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Correspondence to Francis-André Wollman.

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Nawrocki, W., Santabarbara, S., Mosebach, L. et al. State transitions redistribute rather than dissipate energy between the two photosystems in Chlamydomonas. Nature Plants 2, 16031 (2016). https://doi.org/10.1038/nplants.2016.31

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