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Profiling of N6-methyladenosine dynamics indicates regulation of oyster development by m6A-RNA epitranscriptomes

Lorane Le Franc, Bruno Petton, Pascal Favrel, Guillaume Rivière
doi: https://doi.org/10.1101/2021.08.30.458180
Lorane Le Franc
1Normandie Univ, UNICAEN, CNRS, BOREA, 14000 Caen, France. Laboratoire Biologie des organismes et Ecosystèmes aquatiques (BOREA), Muséum d’Histoire naturelle, Sorbonne Université, Université de Caen Normandie, Université des Antilles, CNRS UMR 8067, IRD, Esplanade de la paix, 14032 Caen, France
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Bruno Petton
2Ifremer, Laboratoire des Sciences de l’Environnement Marin, UMR 6539 CNRS/UBO/IRD/Ifremer, Centre Bretagne, 29280, Plouzané, France
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Pascal Favrel
1Normandie Univ, UNICAEN, CNRS, BOREA, 14000 Caen, France. Laboratoire Biologie des organismes et Ecosystèmes aquatiques (BOREA), Muséum d’Histoire naturelle, Sorbonne Université, Université de Caen Normandie, Université des Antilles, CNRS UMR 8067, IRD, Esplanade de la paix, 14032 Caen, France
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Guillaume Rivière
1Normandie Univ, UNICAEN, CNRS, BOREA, 14000 Caen, France. Laboratoire Biologie des organismes et Ecosystèmes aquatiques (BOREA), Muséum d’Histoire naturelle, Sorbonne Université, Université de Caen Normandie, Université des Antilles, CNRS UMR 8067, IRD, Esplanade de la paix, 14032 Caen, France
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  • For correspondence: guillaume.riviere@unicaen.fr
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Abstract

The N6-methylation of RNA adenosines (m6A) is an important regulator of gene expression with critical implications in vertebrate and insect development. However, the developmental significance of epitranscriptomes in lophotrochozoan organisms remains unknown.

Using MeRIP-seq, we generated transcriptome-wide m6A-RNA methylomes covering the whole development of the oyster from oocytes to juveniles. Oyster RNA classes display specific m6A signatures, with mRNAs and lncRNAs exhibiting distinct profiles and being highly methylated compared to transposon transcripts. Epitranscriptomes are dynamic and correspond to chronological steps of development (cleavage, gastrulation, organogenesis and metamorphosis), with a minimal mRNA and lncRNA methylation at the morula stage followed by a global increase. mRNA m6A levels are correlated to transcript levels and shifts in methyladenine profiles correspond to expression kinetics. Differentially methylated transcripts cluster according to embryo-larval stages and bear the corresponding developmental functions (cell division, signal transduction, morphogenesis and cell differentiation). The m6A level of transposon transcripts is also regulated and peaks during the gastrulation.

We demonstrate that m6A-RNA methylomes are dynamic and associated to gene expression regulation during oyster development. The putative epitranscriptome implication in the cleavage, maternal-to-zygotic transition and cell differentiation in a lophotrochozoan model brings new insights into the control and evolution of developmental processes

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations

    (m6A)
    N6-methyladenosine
    (TE)
    Transposable elements
    (UTR)
    Untranslated transcribed region
    (CDS)
    Coding sequences
    (mRNA)
    messenger RNA
    (lncRNA)
    long non-coding RNA
    (misc. RNA)
    miscellaneous RNA
    (tRNA)
    transfer RNA
    (SSW)
    Sterile sea water
    (egg, E)
    Oocyte
    (FE)
    Fertilized oocyte
    (2/8 C)
    Two to eight cell embryo
    (M)
    Morula
    (B)
    Blastula
    (G)
    Gastrula
    (T)
    Trochophore
    (D)
    D larvae
    (P)
    Pedeveliger
    (S)
    Spat
    (hpf)
    Hours post fertilization
    (dpf)
    Days post fertilization
    (GO)
    Gene ontology
    (MZT)
    Maternal-to-zygotic transition
    (DM)
    Differentially methylated
    (Input)
    Input fraction
    (IP)
    Immunoprecipitated fraction
    (TPM)
    Transcripts per million
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    Posted August 31, 2021.
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    Profiling of N6-methyladenosine dynamics indicates regulation of oyster development by m6A-RNA epitranscriptomes
    Lorane Le Franc, Bruno Petton, Pascal Favrel, Guillaume Rivière
    bioRxiv 2021.08.30.458180; doi: https://doi.org/10.1101/2021.08.30.458180
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    Profiling of N6-methyladenosine dynamics indicates regulation of oyster development by m6A-RNA epitranscriptomes
    Lorane Le Franc, Bruno Petton, Pascal Favrel, Guillaume Rivière
    bioRxiv 2021.08.30.458180; doi: https://doi.org/10.1101/2021.08.30.458180

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