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

ABSTRACT: The N6-methyladenosine (m6A) has recently emerged as an important layer of the gene expression regulatory network with critical implications in vertebrate and insect development. However, despite an m6A-RNA pathway is present in the pacific oyster Crassostrea gigas, the developmental significance of epitranscriptomes in lophotrochozoan organisms remains unknown. We performed RNA sequencing (RNA-seq) and m6A-RNA immunoprecipitation sequencing (MeRIP-seq) on 10 developmental stages, on two distinct developments, to covering the whole oyster developement. The m6A-RNA methylomes show the conservation of m6A consensus motif RRACH, a m6A peak around the stop codon and highlight specific m6A signatures according to RNA species between mRNAs, lncRNAs and transposable elements. The differentially methylated RNAs constitute developmental clusters that correspond to chronological steps of oyster development (cleavage, gastrulation, tissues differentiation and metamorphosis). They are marked with an overall drop of mRNA and lncRNA methylation at the morula stage followed by a global increase up to pre-metamorphosis. Messenger RNA m6A levels are correlated to transcript content and shifts in methyladenine profiles correspond to expression kinetics. The m6A of TE transcripts is also regulated and peaks during the gastrulation. Altogether our results indicate that m6A epitranscriptomes are an important regulator of oyster development. This first epitranscriptome profiling across the development of a lophotrochozoan model brings new insights into the epigenetic control of developmental processes and their evolution.

ORGANISM(S): Magallana gigas

PROVIDER: GSE180388 | GEO | 2021/07/20

REPOSITORIES: GEO

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Project description:The monitoring of global transcription patterns during development is a useful first step to understand mechanisms underlying growth, differentiation and patterning in a given species. However such large scale developmental studies are so far only available from a few selected model organisms such as mouse, Drosophila and the nematode C. elegans. Genomic scale information from the lophotrochozoa is now emerging. The recently characterized neuronal transcriptome of the sea hare Aplysia californica (~200’000 ESTs and ~40,000 unique non-redundant sequences representing about 55-70% of all neuronal transcripts including splice forms and non-coding RNAs) provides new insights and opportunities into problems of molluscan development and specifically neurogenesis. Regulatory genes used in development are recruited for the functions of adult nervous systems such as synaptogenesis, specific wiring in networks and structural changes underlying synaptic plasticity. While this similarity reflects a basic concept in biology, namely the recruitment of the same genes for different functions, it has never been tested on a large scale genomic level. We used representative oligo-arrays constructed from transcripts obtained from the Aplysia nervous system to explore the following two questions: 1) What neuronal genes are differentially expressed during embryonic development of the sea hare Aplysia. 2) What gene expression changes can be observed in correlation with gastrulation, metamorphosis, and larval neurogenesis. For this purpose we hybridized RNA from 3 embryonic (64 cells, gastrula, trochophore) and 4 larval stages (pre-hatching, post-hatching, pre-metamorphosis, postmetamorphosis) against a reference sample consisting of equal contributions from all stages. Our analysis revealed that all embryonic and larval stages can be distinguished based on their transcription profiles. A comparison of the Aplysia atlas with similar studies in Drosophila and mouse reveals interesting differences. We identified several new transcription factors which are differentially expressed during early embryonic development. Various other transcripts involved in metabolism and differentiation were characterized. These genes can be candidate targets for understanding neuronal growth, synaptogenesis and memory mechanisms. We conclude that the microarray technology provides us with a powerful tool for efficient survey and functional annotation of the neuronal transcriptome in Aplysia. We used a reference design for this study where we hybridized each of the 8 developmental stages of Aplysia (cleavage, gastrula, trochophore, first veliger, hatching veliger, pre-metamorphosis (stage 6), post-metamorphosis (stage 7), post-metamorphosis 60 hours (pm60)

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

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