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Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes

Nature Plants volume 3, Article number: 17033 (2017) Cite this article

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Abstract

Oxygenic photoautotrophs require mechanisms for rapidly matching the level of chlorophyll excited states from light harvesting with the rate of electron transport from water to carbon dioxide. These photoprotective reactions prevent formation of reactive excited states and photoinhibition. The fastest response to excess illumination is the so-called non-photochemical quenching which, in higher plants, requires the luminal pH sensor PsbS and other yet unidentified components of the photosystem II antenna. Both trimeric light-harvesting complex II (LHCII) and monomeric LHC proteins have been indicated as site(s) of the heat-dissipative reactions. Different mechanisms have been proposed: energy transfer to a lutein quencher in trimers, formation of a zeaxanthin radical cation in monomers. Here, we report on the construction of a mutant lacking all monomeric LHC proteins but retaining LHCII trimers. Its non-photochemical quenching induction rate was substantially slower with respect to the wild type. A carotenoid radical cation signal was detected in the wild type, although it was lost in the mutant. We conclude that non-photochemical quenching is catalysed by two independent mechanisms, with the fastest activated response catalysed within monomeric LHC proteins depending on both zeaxanthin and lutein and on the formation of a radical cation. Trimeric LHCII was responsible for the slowly activated quenching component whereas inclusion in supercomplexes was not required. This latter activity does not depend on lutein nor on charge transfer events, whereas zeaxanthin was essential.

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Figure 1: Phenotype of wild-type and NoM plants.
Figure 2: Biochemical characterization of the NoM mutant.
Figure 3: Kinetics of rise and relaxation of photoprotective energy dissipation.
Figure 4: Kinetics of the formation and relaxation of photoprotective energy dissipation.
Figure 5: Spectral changes associated with the formation of NPQ in wild-type, npq4 and NoM genotypes.
Figure 6: TA spectroscopy on wild-type and NoM thylakoids.

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Acknowledgements

This work was supported by the EEC projects ACCLIPHOT (PITN-GA-2012-316427) and SE2B (675006–SE2B) to R.B. Work in Lund was supported by LaserLab Europe, the Swedish Research Council and the Knut and Alice Wallenberg Foundation. The work of K.K.N. and G.R.F. was supported by the Director, Office of Science, Office of Basic Energy Sciences, of the US Department of Energy under Contract No. DEAC02-05CH11231 and the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences under field work proposal 449B. L.D.'s work was supported by international mobility programme CooperInt 2011/2014, University of Verona.

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Author notes

  1. Luca Dall'Osto and Stefano Cazzaniga: These authors contributed equally to the work.

Authors and Affiliations

  1. Dipartimento di Biotecnologie, Università di Verona, Strada Le Grazie 15, 37134 Verona, Italy

    Luca Dall'Osto, Stefano Cazzaniga, Mauro Bressan & Roberto Bassi

  2. Department of Chemical Physics, Lund University, Getingevägen 60, Lund, S-22241, Sweden

    David Paleček, Karel Židek & Donatas Zigmantas

  3. Department of Plant and Microbial Biology, Howard Hughes Medical Institute, University of California, Berkeley 94720-3102, California, USA

    Krishna K. Niyogi

  4. Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley 94720, California, USA

    Krishna K. Niyogi & Graham R. Fleming

  5. Graduate Group in Applied Science and Technology, University of California, Berkeley 94720, California, USA

    Graham R. Fleming

  6. Department of Chemistry, Hildebrand B77, University of California, Berkeley 94720-1460, California, USA

    Graham R. Fleming

  7. Consiglio Nazionale delle Ricerche (CNR), Istituto per la Protezione delle Piante (IPP), Via Madonna del Piano 10, 50019 Sesto Fiorentino, Firenze, Italy

    Roberto Bassi

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  1. Luca Dall'Osto
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Contributions

R.B., K.K.N. and G.R.F. conceived the work and designed the experiments. L.D., S.C. and M.B. performed all the experiments for the isolation of mutants, and their physiological and biochemical characterization. D.Z. coordinated and performed the transient absorption spectroscopy experiments. D.P. and K.Z. contributed to the time resolved analysis experiments. All of the authors contributed to writing the manuscript. All of the authors discussed the results and commented on the manuscript.

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Correspondence to Roberto Bassi.

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Supplementary Figures 1–6, Supplementary Table 1 and Supplementary References. (PDF 1038 kb)

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Dall'Osto, L., Cazzaniga, S., Bressan, M. et al. Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nature Plants 3, 17033 (2017). https://doi.org/10.1038/nplants.2017.33

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