A novel regulatory gene promotes novel cell fate by suppressing ancestral fate in the sea anemone Nematostella vectensis

Abstract

Cnidocytes (stinging cells) are an unequivocally novel cell type used by cnidarians (corals, jellyfish, and their kin) to immobilize prey. Although they are known to share a common evolutionary origin with neurons, the developmental program that promoted the emergence of cnidocyte fate is not known. Using functional genomics in the sea anemone, Nematostella vectensis, we show that cnidocytes evolved by suppression of neural fate in a subset of neurons expressing RFamide. We further show that a single regulatory gene, a C2H2-type zinc finger transcription factor (ZNF845), coordinates both the gain of novel (cnidocyte-specific) traits and the inhibition of ancestral (neural) traits during cnidocyte development and that this gene arose by domain shuffling in the stem cnidarian. Thus, we uncover a mechanism by which a truly novel regulatory gene (ZNF845) promoted the origin of a truly novel cell type (cnidocyte) through duplication of an ancestral cell lineage (neuron) and inhibition of its ancestral identity (RFamide).

The evolution of cnidarian stinging cells supports a Precambrian radiation of animal predators

“…However, the transfer of pgsAA from bacteria to animals is not cnidarian-specific, and is therefore not evidence that cnidocytes themselves arose through horizontal transfer. More recent analyses that look wholistically at gene expression show that the cnidocyte's transcriptional regulation is similar to the neuron (Chari et al, 2021;Link et al, 2023;Siebert et al, 2019;Steger et al, 2022) and that a small number of genes can change the cell fate from neuron to cnidocyte (Babonis et al, 2022). This is consistent with an alternative hypothesis that cnidocytes and neurons share a common ancestor (Galliot & Quiquand, 2011).…”

Microinjection, gene knockdown, and CRISPR-mediated gene knock-in in the hard coral,Astrangia poculata

“…We designed two single guide RNAs (sgRNAs) targeting the stop codon of the last exon of A. poculata and the appearance of mature cnidocytes in wild type larvae. Cnidocytes are thought to have evolved from a neural-like precursor in the ancestor of cnidarians (Babonis et al, 2022), yet our understanding of the complex regulatory interactions that drive diversification of cnidocyte form and function remains limited (Babonis et al, 2023). The ability to track early cnidocyte development in vivo using endogenously tagged proteins in A. poculata makes this animal a critical model for understanding diversification of this phylum-restricted cell type.…”