Accessibility and activity of transcriptional regulatory elements during sea urchin embryogenesis and differentiation

Transcriptional regulatory elements (TREs) are the primary nodes of the gene regulatory networks that control development. TREs are identified by PRO-seq and their accessibility by ATAC-seq during sea urchin embryonic development and differentiation. Our analysis identifies surprisingly early accessibility in 4-cell cleavage embryo TREs that is not necessarily followed by subsequent transcription, and an excess of ATAC-seq peaks transcriptionally disengaged during the stages analyzed. Embryonic accessibility shifts are driven by transcriptionally engaged TREs, and PRO-seq transcriptional differences at TREs provide more contrast among embryonic stages than ATAC-seq accessibility differences. TRE accessibility reaches a maximum around the 20-hour late blastula, which coincides with major embryo regionalizations. At the same time, a large number of distal TREs become transcriptionally disengaged, in support of an early Pol II primed model for developmental gene regulation that eventually resolves in transcriptional activation or silencing. A transcriptional potency model based on labile nucleosome TRE occupancy driven by DNA sequences and the prevalence of histone variants is proposed in order to explain the basal accessibility of transcriptionally inactive TREs during early embryogenesis. Summary statement Genomic profiles deciphering the location and activity of regulatory elements that control gene expression suggest general mechanisms of regulatory potency in early sea urchin embryos.