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Germline inherited small RNAs facilitate the clearance of untranslated maternal mRNAs in C. elegans embryos

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  • Piergiuseppe Quarato

    (Institut Pasteur, Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, UMR3738, CNRS, 75724
    Sorbonne Université, Collège Doctoral, F-75005)

  • Meetali Singh

    (Institut Pasteur, Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, UMR3738, CNRS, 75724)

  • Eric Cornes

    (Institut Pasteur, Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, UMR3738, CNRS, 75724)

  • Blaise Li

    (Institut Pasteur, Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, UMR3738, CNRS, 75724
    Hub de Bioinformatique et Biostatistique - Département Biologie Computationnelle, Institut Pasteur, 75724)

  • Loan Bourdon

    (Institut Pasteur, Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, UMR3738, CNRS, 75724)

  • Florian Mueller

    (Institut Pasteur, Imaging and Modeling Unit, UMR 3691 CNRS, C3BI USR 3756 IP CNRS, 75724)

  • Celine Didier

    (Institut Pasteur, Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, UMR3738, CNRS, 75724)

  • Germano Cecere

    (Institut Pasteur, Mechanisms of Epigenetic Inheritance, Department of Developmental and Stem Cell Biology, UMR3738, CNRS, 75724)

Abstract

Inheritance and clearance of maternal mRNAs are two of the most critical events required for animal early embryonic development. However, the mechanisms regulating this process are still largely unknown. Here, we show that together with maternal mRNAs, C. elegans embryos inherit a complementary pool of small non-coding RNAs that facilitate the cleavage and removal of hundreds of maternal mRNAs. These antisense small RNAs are loaded into the maternal catalytically-active Argonaute CSR-1 and cleave complementary mRNAs no longer engaged in translation in somatic blastomeres. Induced depletion of CSR-1 specifically during embryonic development leads to embryonic lethality in a slicer-dependent manner and impairs the degradation of CSR-1 embryonic mRNA targets. Given the conservation of Argonaute catalytic activity, we propose that a similar mechanism operates to clear maternal mRNAs during the maternal-to-zygotic transition across species.

Suggested Citation

  • Piergiuseppe Quarato & Meetali Singh & Eric Cornes & Blaise Li & Loan Bourdon & Florian Mueller & Celine Didier & Germano Cecere, 2021. "Germline inherited small RNAs facilitate the clearance of untranslated maternal mRNAs in C. elegans embryos," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-21691-6
    DOI: 10.1038/s41467-021-21691-6
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    Cited by:

    1. Dafne Ibarra-Morales & Michael Rauer & Piergiuseppe Quarato & Leily Rabbani & Fides Zenk & Mariana Schulte-Sasse & Francesco Cardamone & Alejandro Gomez-Auli & Germano Cecere & Nicola Iovino, 2021. "Histone variant H2A.Z regulates zygotic genome activation," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Xiangyang Chen & Ke Wang & Farees Ud Din Mufti & Demin Xu & Chengming Zhu & Xinya Huang & Chenming Zeng & Qile Jin & Xiaona Huang & Yong-hong Yan & Meng-qiu Dong & Xuezhu Feng & Yunyu Shi & Scott Kenn, 2024. "Germ granule compartments coordinate specialized small RNA production," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. 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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