Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes

Sea urchins are emblematic models in developmental biology and display several characteristics that set them apart from other deuterostomes. To uncover the genomic cues that may underlie these specificities, we generated a chromosome-scale genome assembly for the sea urchin Paracentrotus lividus and an extensive gene expression and epigenetic profiles of its embryonic development. We found that, unlike vertebrates, sea urchins retained ancestral chromosomal linkages but underwent very fast intrachromosomal gene order mixing. We identified a burst of gene duplication in the echinoid lineage and showed that some of these expanded genes have been recruited in novel structures (water vascular system, Aristotle’s lantern, and skeletogenic micromere lineage). Finally, we identified gene-regulatory modules conserved between sea urchins and chordates. Our results suggest that gene-regulatory networks controlling development can be conserved despite extensive gene order rearrangement. [Display omitted] •Ancestral linkages are retained in sea urchins, but local gene order is evolving rapidly•Genes duplicated in sea urchins are expressed in novel structures•A new family of Pmar1-related genes is involved in specifying the micromere lineage•Gene-regulatory modules are conserved between sea urchin and chordates The chromosome-scale genome and characterization of the genomic elements that control gene expression in development reveal distinct trends of genome evolution in sea urchins and vertebrates as well as conserved gene-regulatory modules in deuterostomes.