Deep conservation of cis-regulatory elements and chromatin organization in echinoderms uncover ancestral regulatory features of animal genomes

Despite the growing abundance of sequenced animal genomes, we only have detailed knowledge of regulatory organization for a handful of lineages, particularly flies and vertebrates. These two taxa show contrasting trends in the molecular mechanisms of 3D chromatin organization and long-term evolutionary dynamics of cis-regulatory element (CRE) conservation. Here we study the evolution and organization of the regulatory genome of echinoderms, a lineage whose phylogenetic position and relatively slow molecular evolution have proven particularly useful for evolutionary studies. We generated new reference genome assemblies for two species belonging to two different echinoderm classes: the purple sea urchin Strongylocentrotus purpuratus and the bat sea star Patiria miniata using PacBio and HiC data and characterize their 3D chromatin architecture. We show that these echinoderms have TAD-like domains that, such as in flies, do not seem to be associated with CTCF motif orientation. We systematically profiled CREs during sea star and sea urchin development using ATAC-seq, comparing their regulatory logic and dynamics over multiple developmental stages. Finally, our analysis of sea urchin and sea star CRE evolution across multiple evolutionary distances and timescales showed several thousand elements conserved for hundreds of millions of years, revealing a vertebrate-like pattern of CRE evolution that probably constitutes an ancestral property of the regulatory evolution of animals.