Conserved and lineage-restricted gene regulatory programs modulate developmental cnidocyte specification in Nematostella vectensis.

Abstract

Cnidocytes are a synapomorphy of cnidarians that have evolved a range of morphologies and functions within and across extant species, which makes them an excellent model to investigate how novel cell types emerge and radiate in evolution. One way to gain insight into how cell types evolve is to investigate the gene regulatory networks (GRNs) that pattern them, leading to the identification of shared and divergent programs that likely represent components of the ancestral and evolved phenotypes. Efforts to identify early acting transcription factors in the sea anemone Nematostella vectensis revealed that NvfoxE-like is a lineage-restricted cnidocyte transcription factor. Expression and functional studies confirmed that NvfoxE-like and its targets are found exclusively in cnidocytes. By investigating interactions with regulators of the known cnidogenesis GRN and comparing the targets of known cnidocyte regulators, we identified at least four regulatory programs contributing to the cnidogenic GRN in Nematostella. The previously identified cnidocyte regulators Nvznf845 and NvpaxA represent two core pan-cnidarian regulatory programs, while the NvfoxE-like dependent program appears to be restricted to Hexacorallia or Actinaria, where we hypothesize it functions to pattern the unique capsule features present in those lineages. Here, we confirm the hypothesized core conserved transcriptional program, as well as demonstrate how a novel transcription factor was co-opted into cnidogenesis in a subset of cnidarians, thus contributing to the diversification and continued evolution of cnidocytes.