Pre-bilaterian roots of the chordate body plan

Abstract Similarity of body-plan features across distant phyla provides striking testimony to the Darwinian concept of common descent throughout Metazoa. In both the cnidarian Nematostella and chordates, gastrula organizers direct the initial establishment of embryonic axes. Whether these domains share a common evolutionary origin is a fundamental question for understanding the origin of the chordate body plan. To address this question, we combine trans-species transgenesis, perturbations of signaling pathways, cross-phylum single-cell transcriptomic comparisons, and transplantation assays. We show that cis-regulatory elements that recapitulate NvBmp2/4 and NvChordin expression in Nematostella —and therefore report the endogenous cnidarian organizer regulatory environment—also drive organizer-restricted activity in vertebrate embryos, consistent with vertebrate organizer gene-regulatory logic. Moreover, we show that, as in vertebrates, Smad2/3-mediated signaling is active in the Nematostella organizer and is required for organizer-specific expression of NvBmp2/4 and NvChordin . Together, our data support remarkable homology between cnidarian and chordate gastrula organizers and are consistent with the idea that the cnidarian–bilaterian ancestor possessed a blastopore organizer with the potential to generate dorsal–anterior chordate fates. On this basis, we propose a “skewed evo-schistostomy” scenario for the evolution of the chordate body plan from a cnidarian–bilaterian ancestor.