Abstract
In triploblastic animals, Par-proteins regulate cell-polarity and adherens junctions of both ectodermal and endodermal epithelia. But, in embryos of the diploblastic cnidarian Nematostella vectensis, Par-proteins are degraded in all cells in the bifunctional gastrodermal epithelium. Using immunohistochemistry, CRISPR/Cas9 mutagenesis, and mRNA overexpression, we describe the functional association between Par-proteins, ß-catenin, and snail transcription factor genes in N. vectensis embryos. We demonstrate that the aPKC/Par complex regulates the localization of ß-catenin in the ectoderm by stabilizing its role in cell-adhesion, and that endomesodermal epithelial cells are organized by a different cell-adhesion system than overlying ectoderm. We also show that ectopic expression of snail genes, which are expressed in mesodermal derivatives in bilaterians, is sufficient to downregulate Par-proteins and translocate ß-catenin from the junctions to the cytoplasm in ectodermal cells. These data provide molecular insight into the evolution of epithelial structure and distinct cell behaviors in metazoan embryos.
Highlights
Bilaterian animals comprise more than the 95% of the extant animals on earth and exhibit enormous body plan diversity (Martindale and Lee, 2013)
Components of the Par system are not present in the cells of endomesodermal epithelium of N. vectensis during gastrulation, even though the very same cells express these proteins during the blastula stage (Salinas-Saavedra et al, 2015) (Figure 1)
When N. vectensis embryos are stained with antibodies to ß-catenin (Figure 1) or if Nvß-catenin::GFP mRNA is expressed in uncleaved zygotes (Figure 1—figure supplement 1B), clear localization of ß-catenin can be seen in the cortex of ectodermally derived epithelial cells (Figures 1B, C, D, G and I), but not in endomesodermal cells (Figure 1B and C)
Summary
Bilaterian animals comprise more than the 95% of the extant animals on earth and exhibit enormous body plan diversity (Martindale and Lee, 2013). Mesodermal cells segregate from an embryonic endomesodermal precursor to form both endoderm and a third tissue layer (mesoderm) not present in the embryos of diploblastic cnidarians (Martindale et al, 2004; Rodaway and Patient, 2001; Davidson et al, 2002; Maduro and Rothman, 2002; Solnica-Krezel and Sepich, 2012). How mesodermal cells originally segregated from an ancestral endomesodermal epithelium during animal evolution is still unclear (Martindale and Lee, 2013; Martindale, 2005; Technau and Scholz, 2003), because virtually all of the genes required for mesoderm formation are present in cnidarian genomes
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