A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development

Type Article
Date 2021-03
Language English
Author(s) Le Franc Lorane1, 2, Bernay Benoit3, Petton Bruno4, Since Marc5, Favrel Pascal1, 2, Rivière Guillaume1, 2
Affiliation(s) 1 : UNICAEN CNRS BOREA Normandie Univ Caen, France
2 : Laboratoire Biologie des organismes et Ecosystèmes aquatiques (BOREA) Muséum d’Histoire naturelle CNRS IRD Sorbonne Université, Université de Caen NormandieUniversité des Antilles Caen ,France
3 : UNICAEN, ICOREPROTEOGEN Core Facility Caen SF ,France
4 : Ifremer, Laboratoire des Sciences de l’Environnement Marin UMR 6539 CNRS/UBO/IRD/Ifremer Centre Bretagne Normandie Univ Plouzané, France
5 : UNICAEN ,Comprehensive Cancer Center F. Baclesse, SF ICORE PRISMM Core Facility Normandie Univ Caen ,France
Source Febs Journal (1742-464X) (Wiley), 2021-03 , Vol. 288 , N. 5 , P. 1696-1711
DOI 10.1111/febs.15500
Keyword(s) development, epitranscriptomics, methylation, oyster, RNA
Abstract

N6‐methyladenosine (m6A) is a prevalent epitranscriptomic mark in eukaryotic RNA, with crucial roles for mammalian and ecdysozoan development. Indeed, m6A‐RNA and the related protein machinery are important for splicing, translation, maternal‐to‐zygotic transition and cell differentiation. However, to date, the presence of an m6A‐RNA pathway remains unknown in more distant animals, questioning the evolution and significance of the epitranscriptomic regulation. Therefore, we investigated the m6A‐RNA pathway in the oyster Crassostrea gigas, a lophotrochozoan model whose development was demonstrated under strong epigenetic influence. Using mass spectrometry and dot blot assays, we demonstrated that m6A‐RNA is actually present in the oyster and displays variations throughout early oyster development, with the lowest levels at the end of cleavage. In parallel, by in silico analyses, we were able to characterize at the molecular level a complete and conserved putative m6A machinery. The expression levels of the identified putative m6A writers, erasers and readers were strongly regulated across oyster development. Finally, RNA pull‐down coupled to LC‐MS/MS allowed us to prove the actual presence of readers able to bind m6A‐RNA and exhibiting specific developmental patterns. Altogether, our results demonstrate the conservation of a complete m6A‐RNA pathway in the oyster and strongly suggest its implication in early developmental processes including MZT. This first demonstration and characterization of an epitranscriptomic regulation in a lophotrochozoan model, potentially involved in the embryogenesis, bring new insights into our understanding of developmental epigenetic processes and their evolution.

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Le Franc Lorane, Bernay Benoit, Petton Bruno, Since Marc, Favrel Pascal, Rivière Guillaume (2021). A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development. Febs Journal, 288(5), 1696-1711. Publisher's official version : https://doi.org/10.1111/febs.15500 , Open Access version : https://archimer.ifremer.fr/doc/00648/76026/