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Boosting chloroplast ribosome biogenesis by a plastidial DEAD-box RNA helicase is critical for high light acclimation

El Batoul Djouani-Tahri, Sreedhar Nellaepalli, View ORCID ProfilePascaline Auroy, View ORCID ProfileEmmanuelle Billon, View ORCID ProfileAdrien Burlacot, Frédéric Chaux-Jukic, View ORCID ProfileStéphan Cuiné, View ORCID ProfileVirginie Epting, Marie Huleux, Bart Ghysels, View ORCID ProfileMiriam Schulz-Raffelt, View ORCID ProfileIsabelle Te, Sabine Brugière, View ORCID ProfileYohann Couté, View ORCID ProfileYuichiro Takahashi, View ORCID ProfileYonghua Li-Beisson, View ORCID ProfileGilles Peltier
doi: https://doi.org/10.1101/2022.05.16.492170
El Batoul Djouani-Tahri
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Sreedhar Nellaepalli
bResearch Institute for Interdisciplinary Science, Okayama University, 3-1-1 Tsushima-naka, Kita-ku, Okayama, 700-8530, Japan
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Pascaline Auroy
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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  • ORCID record for Pascaline Auroy
Emmanuelle Billon
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Adrien Burlacot
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Frédéric Chaux-Jukic
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Stéphan Cuiné
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Virginie Epting
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Marie Huleux
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Bart Ghysels
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Miriam Schulz-Raffelt
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Isabelle Te
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Sabine Brugière
cUniversité Grenoble Alpes, INSERM, CEA, UMR BioSanté U1292, CNRS, CEA, FR2048, 38000 Grenoble, France
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Yohann Couté
cUniversité Grenoble Alpes, INSERM, CEA, UMR BioSanté U1292, CNRS, CEA, FR2048, 38000 Grenoble, France
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Yuichiro Takahashi
bResearch Institute for Interdisciplinary Science, Okayama University, 3-1-1 Tsushima-naka, Kita-ku, Okayama, 700-8530, Japan
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Yonghua Li-Beisson
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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Gilles Peltier
aAix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint Paul-lez-Durance, France
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  • For correspondence: gilles.peltier@cea.fr
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ABSTRACT

Photosynthetic organisms have developed sophisticated strategies to fine-tune light energy conversion to meet the metabolic demand, thereby optimizing growth in fluctuating light environments. Although mechanisms such as energy dissipation, photosynthetic control, or the photosystem II (PSII) damage and repair have been widely studied, little is known about the regulation of protein synthesis capacity during light acclimation. By screening a Chlamydomonas reinhardtii insertional mutant library using chlorophyll fluorescence imaging, we isolated a high chlorophyll fluorescence mutant (hf0) defected in a gene encoding a putative plastid targeted DEAD-box RNA helicase called CreRH22. CreRH22 is rapidly induced upon illumination and belongs to the GreenCut, a set of proteins specific to photosynthetic organisms. While photosynthesis is slightly affected in the mutant under low light (LL), exposure to high light (HL) induces a marked decrease in both PSII and PSI, and a strong alteration of the light-induced gene expression pattern. These effects are explained by the inability of hf0 to increase plastid ribosome amounts under HL. We conclude that CreRH22, by promoting ribosomal RNA precursor maturation in a light-dependent manner, enables the assembly of extra-ribosomes required to synthesize photosystem subunits at a higher rate, a critical step in the acclimation of algae to HL.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The author(s) responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Gilles Peltier (gilles.peltier{at}cea.fr).

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 23, 2022.
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Boosting chloroplast ribosome biogenesis by a plastidial DEAD-box RNA helicase is critical for high light acclimation
El Batoul Djouani-Tahri, Sreedhar Nellaepalli, Pascaline Auroy, Emmanuelle Billon, Adrien Burlacot, Frédéric Chaux-Jukic, Stéphan Cuiné, Virginie Epting, Marie Huleux, Bart Ghysels, Miriam Schulz-Raffelt, Isabelle Te, Sabine Brugière, Yohann Couté, Yuichiro Takahashi, Yonghua Li-Beisson, Gilles Peltier
bioRxiv 2022.05.16.492170; doi: https://doi.org/10.1101/2022.05.16.492170
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Boosting chloroplast ribosome biogenesis by a plastidial DEAD-box RNA helicase is critical for high light acclimation
El Batoul Djouani-Tahri, Sreedhar Nellaepalli, Pascaline Auroy, Emmanuelle Billon, Adrien Burlacot, Frédéric Chaux-Jukic, Stéphan Cuiné, Virginie Epting, Marie Huleux, Bart Ghysels, Miriam Schulz-Raffelt, Isabelle Te, Sabine Brugière, Yohann Couté, Yuichiro Takahashi, Yonghua Li-Beisson, Gilles Peltier
bioRxiv 2022.05.16.492170; doi: https://doi.org/10.1101/2022.05.16.492170

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