Cell type-specific expression profiling unravels the development and evolution of stinging cells in sea anemone.

BACKGROUND: Cnidocytes are specialized cells that define the phylum Cnidaria. They possess an "explosive" organelle called cnidocyst that is important for prey capture and anti-predator defense. An extraordinary morphological and functional complexity of the cnidocysts has inspired numerous studies to investigate their structure and development. However, the transcriptomes of the cells bearing these unique organelles are yet to be characterized, impeding our understanding of the genetic basis of their biogenesis. RESULTS: In this study, we generated a nematocyte reporter transgenic line of the sea anemone Nematostella vectensis using the CRISPR/Cas9 system. By using a fluorescence-activated cell sorter (FACS), we have characterized cell type-specific transcriptomic profiles of various stages of cnidocyte maturation and showed that nematogenesis (the formation of functional cnidocysts) is underpinned by dramatic shifts in the spatiotemporal gene expression. Among the genes identified as upregulated in cnidocytes were Cnido-Jun and Cnido-Fos1-cnidarian-specific paralogs of the highly conserved c-Jun and c-Fos proteins of the stress-induced AP-1 transcriptional complex. The knockdown of the cnidocyte-specific c-Jun homolog by microinjection of morpholino antisense oligomer results in disruption of normal nematogenesis. CONCLUSIONS: Here, we show that the majority of upregulated genes and enriched biochemical pathways specific to cnidocytes are uncharacterized, emphasizing the need for further functional research on nematogenesis. The recruitment of the metazoan stress-related transcription factor c-Fos/c-Jun complex into nematogenesis highlights the evolutionary ingenuity and novelty associated with the formation of these highly complex, enigmatic, and phyletically unique organelles. Thus, we provide novel insights into the biology, development, and evolution of cnidocytes.

NF-κB is required for cnidocyte development in the sea anemone Nematostella vectensis.

The sea anemone Nematostella vectensis (Nv) is a leading model organism for the phylum Cnidaria, which includes anemones, corals, jellyfishes and hydras. A defining trait across this phylum is the cnidocyte, an ectodermal cell type with a variety of functions including defense, prey capture and environmental sensing. Herein, we show that the Nv-NF-κB transcription factor and its inhibitor Nv-IκB are expressed in a subset of cnidocytes in the body column of juvenile and adult anemones. The size and distribution of the Nv-NF-κB-positive cnidocytes suggest that they are in a subtype known as basitrichous haplonema cnidocytes. Nv-NF-κB is primarily cytoplasmic in cnidocytes in juvenile and adult animals, but is nuclear when first detected in the 30-h post-fertilization embryo. Morpholino-mediated knockdown of Nv-NF-κB expression results in greatly reduced cnidocyte formation in the 5 day-old animal. Taken together, these results indicate that NF-κB plays a key role in the development of the phylum-specific cnidocyte cell type in Nematostella, likely by nuclear Nv-NF-κB-dependent activation of genes required for cnidocyte development.