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A different perspective for nonphotochemical quenching in plant antenna complexes

Author

Listed:
  • Edoardo Cignoni

    (University of Pisa)

  • Margherita Lapillo

    (University of Pisa)

  • Lorenzo Cupellini

    (University of Pisa)

  • Silvia Acosta-Gutiérrez

    (University College London)

  • Francesco Luigi Gervasio

    (University College London
    University of Geneva)

  • Benedetta Mennucci

    (University of Pisa)

Abstract

Light-harvesting complexes of plants exert a dual function of light-harvesting (LH) and photoprotection through processes collectively called nonphotochemical quenching (NPQ). While LH processes are relatively well characterized, those involved in NPQ are less understood. Here, we characterize the quenching mechanisms of CP29, a minor LHC of plants, through the integration of two complementary enhanced-sampling techniques, dimensionality reduction schemes, electronic calculations and the analysis of cryo-EM data in the light of the predicted conformational ensemble. Our study reveals that the switch between LH and quenching state is more complex than previously thought. Several conformations of the lumenal side of the protein occur and differently affect the pigments’ relative geometries and interactions. Moreover, we show that a quenching mechanism localized on a single chlorophyll-carotenoid pair is not sufficient but many chlorophylls are simultaneously involved. In such a diffuse mechanism, short-range interactions between each carotenoid and different chlorophylls combined with a protein-mediated tuning of the carotenoid excitation energies have to be considered in addition to the commonly suggested Coulomb interactions.

Suggested Citation

  • Edoardo Cignoni & Margherita Lapillo & Lorenzo Cupellini & Silvia Acosta-Gutiérrez & Francesco Luigi Gervasio & Benedetta Mennucci, 2021. "A different perspective for nonphotochemical quenching in plant antenna complexes," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27526-8
    DOI: 10.1038/s41467-021-27526-8
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    References listed on IDEAS

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    1. Andrew A. Pascal & Zhenfeng Liu & Koen Broess & Bart van Oort & Herbert van Amerongen & Chao Wang & Peter Horton & Bruno Robert & Wenrui Chang & Alexander Ruban, 2005. "Molecular basis of photoprotection and control of photosynthetic light-harvesting," Nature, Nature, vol. 436(7047), pages 134-137, July.
    2. Lorenzo Cupellini & Dario Calvani & Denis Jacquemin & Benedetta Mennucci, 2020. "Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    3. Minjung Son & Alberta Pinnola & Samuel C. Gordon & Roberto Bassi & Gabriela S. Schlau-Cohen, 2020. "Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    4. Alexander V. Ruban & Rudi Berera & Cristian Ilioaia & Ivo H. M. van Stokkum & John T. M. Kennis & Andrew A. Pascal & Herbert van Amerongen & Bruno Robert & Peter Horton & Rienk van Grondelle, 2007. "Identification of a mechanism of photoprotective energy dissipation in higher plants," Nature, Nature, vol. 450(7169), pages 575-578, November.
    5. Nicoletta Liguori & Pengqi Xu & Ivo H.M. Stokkum & Bart Oort & Yinghong Lu & Daniel Karcher & Ralph Bock & Roberta Croce, 2017. "Different carotenoid conformations have distinct functions in light-harvesting regulation in plants," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
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    1. Audrey Short & Thomas P. Fay & Thien Crisanto & Ratul Mangal & Krishna K. Niyogi & David T. Limmer & Graham R. Fleming, 2023. "Kinetics of the xanthophyll cycle and its role in photoprotective memory and response," Nature Communications, Nature, vol. 14(1), pages 1-10, December.

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