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Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis

Author

Listed:
  • Meetali Singh

    (Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, Institut Pasteur, UMR3738, CNRS)

  • Eric Cornes

    (Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, Institut Pasteur, UMR3738, CNRS)

  • Blaise Li

    (Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, Institut Pasteur, UMR3738, CNRS
    Hub de Bioinformatique et Biostatistique—Département Biologie Computationnelle, Institut Pasteur)

  • Piergiuseppe Quarato

    (Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, Institut Pasteur, UMR3738, CNRS
    Sorbonne Université, Collège Doctoral)

  • Loan Bourdon

    (Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, Institut Pasteur, UMR3738, CNRS)

  • Florent Dingli

    (Institut Curie, PSL Research University, Centre de Recherche, Laboratoire de Spectrométrie de Masse Protéomique)

  • Damarys Loew

    (Institut Curie, PSL Research University, Centre de Recherche, Laboratoire de Spectrométrie de Masse Protéomique)

  • Simone Proccacia

    (Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, Institut Pasteur, UMR3738, CNRS
    Università di Trento)

  • Germano Cecere

    (Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, Institut Pasteur, UMR3738, CNRS)

Abstract

In the Caenorhabditis elegans germline, thousands of mRNAs are concomitantly expressed with antisense 22G-RNAs, which are loaded into the Argonaute CSR-1. Despite their essential functions for animal fertility and embryonic development, how CSR-1 22G-RNAs are produced remains unknown. Here, we show that CSR-1 slicer activity is primarily involved in triggering the synthesis of small RNAs on the coding sequences of germline mRNAs and post-transcriptionally regulates a fraction of targets. CSR-1-cleaved mRNAs prime the RNA-dependent RNA polymerase, EGO-1, to synthesize 22G-RNAs in phase with translating ribosomes, in contrast to other 22G-RNAs mostly synthesized in germ granules. Moreover, codon optimality and efficient translation antagonize CSR-1 slicing and 22G-RNAs biogenesis. We propose that codon usage differences encoded into mRNA sequences might be a conserved strategy in eukaryotes to regulate small RNA biogenesis and Argonaute targeting.

Suggested Citation

  • Meetali Singh & Eric Cornes & Blaise Li & Piergiuseppe Quarato & Loan Bourdon & Florent Dingli & Damarys Loew & Simone Proccacia & Germano Cecere, 2021. "Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23615-w
    DOI: 10.1038/s41467-021-23615-w
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    Cited by:

    1. Wenjun Chen & Jordan S. Brown & Tao He & Wei-Sheng Wu & Shikui Tu & Zhiping Weng & Donglei Zhang & Heng-Chi Lee, 2022. "GLH/VASA helicases promote germ granule formation to ensure the fidelity of piRNA-mediated transcriptome surveillance," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Susanne Bornelöv & Benjamin Czech & Gregory J. Hannon, 2022. "An evolutionarily conserved stop codon enrichment at the 5′ ends of mammalian piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Shihui Chen & Carolyn M. Phillips, 2024. "HRDE-2 drives small RNA specificity for the nuclear Argonaute protein HRDE-1," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    4. Maxim V. Zagoskin & Jianbin Wang & Ashley T. Neff & Giovana M. B. Veronezi & Richard E. Davis, 2022. "Small RNA pathways in the nematode Ascaris in the absence of piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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