Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution

Abstract

Background: Understanding the drivers of morphological diversity is a persistent challenge in evolutionary biology. Here, we investigate functional diversification of secretory cells in the sea anemone Nematostella vectensis to understand the mechanisms promoting cellular specialization across animals. Results: We demonstrate regionalized expression of gland cell subtypes in the internal ectoderm of N. vectensis and show that adult gland cell identity is acquired very early in development. A phylogenetic survey of trypsins across animals suggests that this gene family has undergone numerous expansions. We reveal unexpected diversity in trypsin protein structure and show that trypsin diversity arose through independent acquisitions of non-trypsin domains. Finally, we show that trypsin diversification in N. vectensis was effected through a combination of tandem duplication, exon shuffling, and retrotransposition. Conclusions: Together, these results reveal the numerous evolutionary mechanisms that drove trypsin duplication and divergence during the morphological specialization of cell types and suggest that the secretory cell phenotype is highly adaptable as a vehicle for novel secretory products.