Ancestral role of Fat-like cadherins in planar cell polarity

Abstract

Fat family cadherins are enormous proteins that regulate planar cell polarity (PCP) and cell adhesion in bilaterian animals. Their evolutionary origin can be traced back to prebilaterian species, but their ancestral function(s) are unknown. We identified Fat-like and Dachsous cadherins in Hydra, a member of the earlydiverging metazoan phylum Cnidaria. Hydra has a simple body plan with only two epithelial layers and radial symmetry. We find that Hydra homologues of Fat-like (HyFat) and Dachsous (HyDs) co-localize at the apico-lateral membrane of ectodermal epithelial cells. Remarkably, HyFat is planar polarized perpendicular to the oral-aboral axis of the animal. Using knockdown approaches we found that HyFat is involved in the regulation of local cell alignment, but is dispensable for the global alignment of ectodermal myonemes along the oral-aboral axis. The intracellular domain (ICD) of HyFat is involved in the morphogenesis of ectodermal myonemes. Thus, Fat family cadherins have ancient, prebilaterian functions in cell adhesion, tissue organization and planar polarity.

Cell polarity signalling at the birth of multicellularity: What can we learn from the first animals

“…Planar cell polarity genes fat and fat -like genes are associated with cell directional migration and morphogenesis in asymmetric cell division in bilaterians ( Matis and Axelrod 2013 ). The Hydra fat and dachsous genes localise to the body of the animals where continuous growth and migration of cells occur supporting the theory of a similar role to that of bilaterians ( Brooun et al, 2019 ). Phylogenetic examination of frizzled in a variety of different poriferan, placozoan, cnidarian and ctenophore species show multiple orthologues of frizzled.…”

“…The Hydra fat and dachsous genes localise to the body of the animals where continuous growth and migration of cells occur supporting the theory of a similar role to that of bilaterians (Brooun et al, 2019). Phylogenetic examination of frizzled in a variety of different poriferan, placozoan, cnidarian and ctenophore species show multiple orthologues of frizzled.…”