Evolutionary rewiring of the endomesoderm gene regulatory networks specify skeleton secreting cells in stony corals

Stony corals are the only cnidarians to secrete a robust calcium carbonate skeleton making them the critical keystone species for one of the most diverse marine ecosystems on earth: coral reefs. Despite their importance, very little is known about the genetic interactions that drive the earliest life history stages of corals during which coral-specific traits emerge, such as specification of coral skeletogenic cells. Here, we used a combination of chromatin profiling and gene expression assays to derive the cis-regulatory architectures of early coral development using the emerging model system Astrangia poculata. From this work we found that elements of the cnidarian endomesoderm gene regulatory network have been co-opted into a subnetwork underlying the specification of coral skeleton secreting cells. We further identified the cis-regulatory element responsible for the novel expression of the endomesodermal gene Brachyury in coral skeletogenic cells and demonstrated that this element is capable of reproducing similar expression patterns in Nematostella vectensis, a distantly related species that does not produce a skeleton. These findings support a novel dual role of the endomesodermal GRN in establishing germ layer identity and specifying skeleton secreting cells in stony corals and provide a gene-regulatory framework that underpins the evolution and diversification of stony corals from other cnidarian lineages.