Cnidarians are the only non-bilaterian group to evolve ciliated larvae with an apical sensory organ, which is possibly homologous to the apical organs of bilaterian primary larvae. Here, we generated transcriptomes of the apical tissue in the sea anemone Nematostella vectensis and showed that it has a unique neuronal signature. By integrating previously published larval single-cell data with our apical transcriptomes, we discovered that the apical domain comprises a minimum of six distinct cell types. We show that the apical organ is compartmentalised into apical tuft cells (spot) and larval-specific neurons (ring). Finally, we identify ISX-like (NVE14554), a PRD class homeobox gene specifically expressed in apical tuft cells, as an FGF signalling-dependent transcription factor responsible for the formation of the apical tuft domain via repression of the neural ring fate in apical cells. With this study, we contribute a comparison of the molecular anatomy of apical organs, which must be carried out across phyla to determine whether this crucial larval structure evolved once or multiple times.
The apical pole of eumetazoan ciliated larvae acts as a neurosensory structure and is principally composed of sensory-secretory cells. Cnidarians like the sea anemone Nematostella vectensis are the only non-bilaterian group to evolve ciliated larvae with a neural integrated sensory organ that is likely homologous to bilaterians. Here, we uncovered the molecular signature of the larval sensory organ in Nematostella by generating a transcriptome of the apical tissue. We characterised the cellular identity of the apical domain by integrating larval single-cell data with the apical transcriptome and further validated this through in-situ hybridisation. We discovered that the apical domain comprises a minimum of 6 distinct cell types, including apical cells, neurons, peripheral flask-shaped gland/secretory cells, and undifferentiated cells. By profiling the spatial expression of neuronal genes, we showed that the apical region has a unique neuronal signature distinct from the rest of the body. By combining the planula cilia proteome with the apical transcriptome data, we revealed the sheer complexity of the non-motile apical tuft. Overall, we present comprehensive spatial/molecular data on the Nematostella larval sensory organ and open new directions for elucidating the functional role of the apical organ and larval nervous system.
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