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Light-independent regulation of algal photoprotection by CO2 availability

Author

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  • M. Águila Ruiz-Sola

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
    Consejo Superior de Investigaciones Científicas-Universidad de Sevilla)

  • Serena Flori

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Yizhong Yuan

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Gaelle Villain

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Emanuel Sanz-Luque

    (The Carnegie Institution for Science, Department of Plant Biology
    University of Cordoba, Department of Biochemistry and Molecular Biology)

  • Petra Redekop

    (The Carnegie Institution for Science, Department of Plant Biology)

  • Ryutaro Tokutsu

    (Division of Environmental photobiology, National Institute for Basic Biology (NIBB))

  • Anika Küken

    (University of Potsdam
    Max-Planck-Institute of Molecular Plant Physiology)

  • Angeliki Tsichla

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Georgios Kepesidis

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Guillaume Allorent

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Marius Arend

    (University of Potsdam
    Max-Planck-Institute of Molecular Plant Physiology)

  • Fabrizio Iacono

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Giovanni Finazzi

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

  • Michael Hippler

    (Westfälische Wilhelms Universität)

  • Zoran Nikoloski

    (University of Potsdam
    Max-Planck-Institute of Molecular Plant Physiology)

  • Jun Minagawa

    (Division of Environmental photobiology, National Institute for Basic Biology (NIBB))

  • Arthur R. Grossman

    (The Carnegie Institution for Science, Department of Plant Biology)

  • Dimitris Petroutsos

    (Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV)

Abstract

Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO2 conditions. When light energy exceeds CO2 fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO2 Concentrating Mechanism (CCM). How light and CO2 signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO2 concentrations and that depletion of CO2 drives these responses, even in total darkness. High CO2 levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3/CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO2 and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO2 levels.

Suggested Citation

  • M. Águila Ruiz-Sola & Serena Flori & Yizhong Yuan & Gaelle Villain & Emanuel Sanz-Luque & Petra Redekop & Ryutaro Tokutsu & Anika Küken & Angeliki Tsichla & Georgios Kepesidis & Guillaume Allorent & M, 2023. "Light-independent regulation of algal photoprotection by CO2 availability," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37800-6
    DOI: 10.1038/s41467-023-37800-6
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    References listed on IDEAS

    as
    1. Dimitris Petroutsos & Ryutaro Tokutsu & Shinichiro Maruyama & Serena Flori & Andre Greiner & Leonardo Magneschi & Loic Cusant & Tilman Kottke & Maria Mittag & Peter Hegemann & Giovanni Finazzi & Jun M, 2016. "A blue-light photoreceptor mediates the feedback regulation of photosynthesis," Nature, Nature, vol. 537(7621), pages 563-566, September.
    2. Victoria L. Linthwaite & Joanna M. Janus & Adrian P. Brown & David Wong-Pascua & AnnMarie C. O’Donoghue & Andrew Porter & Achim Treumann & David R. W. Hodgson & Martin J. Cann, 2018. "Author Correction: The identification of carbon dioxide mediated protein post-translational modifications," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
    3. Victoria L. Linthwaite & Joanna M. Janus & Adrian P. Brown & David Wong-Pascua & AnnMarie C. O’Donoghue & Andrew Porter & Achim Treumann & David R. W. Hodgson & Martin J. Cann, 2018. "The identification of carbon dioxide mediated protein post-translational modifications," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    4. Graham Peers & Thuy B. Truong & Elisabeth Ostendorf & Andreas Busch & Dafna Elrad & Arthur R. Grossman & Michael Hippler & Krishna K. Niyogi, 2009. "An ancient light-harvesting protein is critical for the regulation of algal photosynthesis," Nature, Nature, vol. 462(7272), pages 518-521, November.
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