N6-Methyladenosine Profile Dynamics Indicates Regulation of Oyster Development by m6A-RNA Epitranscriptomes

Type Article
Acceptance Date 2022-12 IN PRESS
Language English
Author(s) Le Franc Lorane1, Petton BrunoORCID2, Favrel Pascal1, Rivière Guillaume1
Affiliation(s) 1 : Laboratoire de Biologie des Organismes et des Ecosystèmes Aquatiques (BOREA), Muséum d’Histoire Naturelle, Sorbonne Université, Université de Caen Normandie, Université des Antilles, CNRS UMR 8067, IRD, 14032 Caen, France
2 : Ifremer, Laboratoire des Sciences de l’Environnement Marin, UMR 6539 CNRS/UBO/IRD/Ifremer, Centre Bretagne, 29280 Plouzané, France
Source Genomics, Proteomics & Bioinformatics (1672-0229) (Elsevier BV) In Press
DOI 10.1016/j.gpb.2022.12.002
Keyword(s) RNA methylation, Transcription, Embryo, Metamorphosis, Evo-devo

The N6-methylation of RNA adenosines (N6-methyladenosine, 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 methylated RNA immunoprecipitation sequencing (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 messenger RNAs (mRNAs) and long non-coding RNAs (lncRNAs) exhibiting distinct profiles and being highly methylated compared to transposon transcripts. Epitranscriptomes are dynamic and correspond to the 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 methylation 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.

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