Epigenomics of embryogenesis in turbot (Scophthalmus maximus)

Abstract

Embryogenesis is the crucial first step of ontogeny, where an organism with a complex body plan arises from a single undifferentiated totipotent cell. This process is orchestrated by dynamic changes in transcriptional regulation, influenced by chromatin accessibility and nucleotide and histone modifications constituting epigenetic signals enabling access to transcription factors. The epigenomic regulation of embryogenesis has been studied in model fishes, but little attention has been paid to farmed fish - where traits of importance to aquaculture rely on early developmental processes. This study, framed within the AQUA-FAANG consortium, reports a comprehensive regulatory atlas of embryogenesis for turbot (Scophthalmus maximus), a farmed flatfish representing order Pleuronectiformes. 14,560 genes were expressed in the embryonic transcriptome with > 90% showing differential expression across consecutive stages. By integrating multi-histone ChIP-Seq marks with ATAC-Seq, we built a genome-wide chromatin state model, defining promoter and enhancer activity across stages. Transcription factor binding motif (TFBM) analysis of differentially active promoters and enhancers revealed dynamism in regulated gene functions, with more than half the TFBM enriched in a single developmental transition. Significant shifts in chromatin accessibility occurred across stages, most notably during the transition from shield to early segmentation, suggesting a profound chromatin reorganization underpins somitogenesis and early organ development. Most changes in chromatin accessibility across stages did not involve promoter regions of differentially expressed genes, suggesting a trend of promoter accessibility preceding gene transcriptional activity. Comparative analyses with zebrafish revealed a global transcriptomic correlation of single copy orthologs at matched stages of embryogenesis across species. While conserved expression dynamics were revealed for many orthologous Hox genes, notable cross-species differences were identified from before zygotic genome activation leading up to hatching. This multi-omics investigation provides a novel atlas of non-coding regulatory elements controlling turbot development, with key applications for flatfish biology and enhancing sustainable aquaculture.