NEW GENOMIC DATA AND ANALYSES CHALLENGE THE TRADITIONAL VISION OF ANIMAL EPITHELIUM EVOLUTION

Abstract

The emergence of epithelia was the foundation of metazoan expansion. To investigate the early evolution of animal epithelia, we sequenced the genome and transcriptomes of two new sponge species to characterize epithelial markers such as the E-cadherin complex and the polarity complexes for all classes (Calcarea, Demospongiae, Hexactinellida, Homoscleromorpha) of sponges (phylum Porifera) and compare them with their homologs in Placozoa and in Ctenophora. We found that Placozoa and most sponges possess orthologs of all essential genes encoding proteins characteristic of bilaterian epithelial cells, as well as their conserved interaction domains. In stark contrast, we found that ctenophores lack several major polarity complex components such as the Crumbs complex and Scribble. Furthermore, the E-cadherin ctenophore ortholog exhibits a divergent cytoplasmic domain making it unlikely to interact with its canonical cytoplasmic partners. These unexpected findings challenge the current evolutionary paradigm on the emergence of epithelia.\n\nSIGNIFICANT STATEMENTEpithelial tissues are a hallmark of metazoans deeply linked to the evolution of the complex morphogenesis processes characterizing their development. However, studies on the epithelial features of non-bilaterians are still sparse and it remains unclear whether the last common metazoan ancestor possessed a fully functional epithelial toolkit or if it was acquired later during metazoan evolution. In this work, we demonstrate that if sponges have a well conserved and functionally predicted epithelial toolkit, Ctenophores have either divergent adhesion complexes or lack essential polarity complexes. Altogether, our results raise a doubt on the homology of protein complexes and structures involved in cell polarity and adhesive type junctions between Ctenophora and Bilateria epithelia.