The methylome of the marbled crayfish links gene body methylation to stable expression of poorly accessible genes

Abstract

BackgroundThe parthenogenetic marbled crayfish (Procambarus virginalis) is a novel species that has rapidly invaded and colonized various different habitats. Adaptation to different environments appears to be independent of the selection of genetic variants, but epigenetic programming of the marbled crayfish genome remains to be understood.ResultsHere, we provide a comprehensive analysis of DNA methylation in marbled crayfish. Whole-genome bisulfite sequencing of multiple replicates and different tissues revealed a methylation pattern that is characterized by gene body methylation of housekeeping genes. Interestingly, this pattern was largely tissue invariant, suggesting a function that is unrelated to cell fate specification. Indeed, integrative analysis of DNA methylation, chromatin accessibility and mRNA expression patterns revealed that gene body methylation correlated with limited chromatin accessibility and stable gene expression, while low-methylated genes often resided in chromatin with higher accessibility and showed increased expression variation. Interestingly, marbled crayfish also showed reduced gene body methylation and higher gene expression variability when compared with their noninvasive mother species, Procambarus fallax.ConclusionsOur results provide novel insights into invertebrate gene body methylation and its potential role in adaptive gene regulation.Electronic supplementary materialThe online version of this article (10.1186/s13072-018-0229-6) contains supplementary material, which is available to authorized users.

­­­­­­Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

“…Our results suggest that the most highly conserved feature of arthropod methylomes is enrichment of methylation at the exons of a subset of genes. Similar conclusions as to the dominance of methylation within genes in arthropods have been reached through a systematic analysis of insects [13] and in analyses of several individual arthropod species outside insects [24][25][26]30]. Across species, we asked whether there was any tendency for orthologous genes to be methylated in different species.…”

“…However, there was little difference between exons and introns for the two crustaceans, P. hawaiensis and A. vulgare (Fig 3C; S3 Fig). Methylation of genes has been described in the crayfish [26] and suggested in Daphnia [24] albeit at very low levels. Given that P. hawaiensis exons are depleted for methylation relative to the genome-wide background while A. vulgare exons are only slightly greater than the background, this may reflect an ancient loss of gene body methylation in the Peracaridian ancestor of these species.…”

Tracing animal genomic evolution with the chromosomal-level assembly of the freshwater sponge Ephydatia muelleri

“…19B) 37 . Promoters are strongly demethylated and repeats found within gene bodies tend to have higher methylation levels than those in intergenic regions, as seen in other invertebrates 38 , suggesting that not all repeats are actively targeted by DNA methylation in E. muelleri. Overall, the E. muelleri methylome shows many patterns similar to those of canonical "mosaic" invertebrate genomes, and may therefore provide a more appropriate comparison for future comparative epigenetics work than other existing sponge models.…”

Tracing animal genomic evolution with the chromosomal-level assembly of the freshwater sponge Ephydatia muelleri

“…19B) 37 . Promoters are strongly demethylated and repeats found within gene bodies tend to have higher methylation levels than those in intergenic regions, as seen in other invertebrates 38 , suggesting that not all repeats are actively targeted by DNA methylation in E. muelleri. In fact, repeat methylation level positively correlates with age of the repeat, and LTR retrotransposons are more likely targeted by DNA methylation irrespective of genome position ( Supplementary Fig.…”