Abstract
DNA methylation is a critical epigenetic regulator of development in mammals and social insects, but its significance in development outside these groups is not understood. Here we investigated the genome-wide dynamics of DNA methylation in a mollusc model, the oyster Crassostrea gigas, from the egg to the completion of organogenesis. Large-scale methylation maps reveal that the oyster genome displays a succession of methylated and non methylated regions, which persist throughout development. Differentially methylated regions (DMRs) are strongly regulated during cleavage and metamorphosis. The distribution and levels of methylated DNA within genomic features (exons, introns, promoters, repeats and transposons) show different developmental lansdscapes marked by a strong increase in the methylation of exons against introns after metamorphosis. Kinetics of methylation in gene-bodies correlate to their transcription regulation and to distinct functional gene clusters, and DMRs at cleavage and metamorphosis bear the genes functionally related to these steps, respectively. This study shows that DNA methylome dynamics underlie development through transcription regulation in the oyster, a lophotrochozoan species. To our knowledge, this is the first demonstration of such epigenetic regulation outside vertebrates and ecdysozoan models, bringing new insights into the evolution and the epigenetic regulation of developmental processes.
Highlights
The methylation of DNA is a prevalent epigenetic mark that is deeply rooted in evolution and found from bacteria to mammals
Large-scale genome-wide methylome dynamics were investigated by analyses of differentially methylated regions (DMRs) and physical maps
The mean distance from genomic features to the nearest Differentially methylated regions (DMRs) was drastically shorter at the M step than at other steps, indicating that DNA methylation is more evenly regulated throughout the genome at the M step than in the C step (S1B Fig)
Summary
The methylation of DNA is a prevalent epigenetic mark that is deeply rooted in evolution and found from bacteria to mammals. DNA methylation is an essential feature of mammalian development because meC patterns are associated with a wide range of cell processes whose subtle combination is required for the embryo to develop into a complex adult organism exhibiting differentiated cell types. CpG dinucleotides are overrepresented in promoters of development and housekeeping genes which are protected from methylation by transcription factor binding and subsequent DNA methyltransferase exclusion [2], reflecting poor methylation in the germline over evolutionary time. DNA methylation shapes cell differentiation (reviewed in [4]) notably through silencing of pluripotency factors [5, 6] and of germline specific genes in somatic cells [7] at lineage commitment by de novo methylation. DNA methylation stabilizes the chromatin context underlying cell fate decisions that are propagated through cell generations by maintenance of the meC landscapes (review in [4])
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