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Evolution of the Animal-Vegetal Axis

The animal-vegetal (AV) axis is a cytoplasmic/cytoarchitectural polarity seen in oocytes and eggs of most animals, and this axis is specified maternally by largely unknown mechanisms. The AV axis strongly influences early pattern formation because maternally deposited developmental information that is asymmetrically distributed along this axis is used during embryogenesis to specify the primary germ layers. This axis clearly had an ancient origin since it is present in eggs from bilaterians, animals with bilateral symmetry that include over 95% of extant species, and in eggs of non-bilaterians, extant representatives of early diverging basal metazoan taxa that form outgroups to the bilaterians.

Classic embryological and more recent molecular studies in bilaterians and non-bilaterians have shown interesting similarities and differences in the pattern of germ later segregation and gastrulation, and in the molecular pathways that regulate these processes along the AV axes in these two animal clades. In ctenophores and cnidarians, the only two non-bilaterian taxa that show true gastrulation, endoderm specification and gastrulation occurs at the animal pole, while in many bilaterians, endomesoderm specification generally occurs in vegetal pole derived blastomeres.

We and others have shown that in sea urchins and in cnidarians, germ layer segregation is mediated by the asymmetric activation of the Wnt/beta-catenin pathway in cleavage stage embryos. Interestingly, while the Wnt/beta-catenin pathway is activated in vegetal blastomeres in the sea urchin, this pathway is activated in animal pole-derived blastomeres in Nematostella. We have further shown that in sea urchins the Wnt/beta-catenin pathway is selectively activated by the Disheveled (Dsh) protein at the vegetal pole, while in Nematostella, the Dsh protein is selectively activated at the animal pole. The Dsh protein, a key regulator of the Wnt signalling pathways, shows striking accumulation at the vegetal pole of unfertilized sea urchin eggs and at the animal pole of unfertilized Nematostella eggs. Based on these and other observations, we have recently hypothesized that the site of gastrulation was moved from the animal pole of the last common ancestor to the cnidarians and bilaterians, to the vegetal pole of the bilaterian last common ancestor (Lee et al. 2007; Kumburegama et al. 2011). We have further hypothesized that this major shift in the site of gastrulation was enabled by a shift of critical determinants necessary for localization and activation of Wnt signaling from the animal pole to the vegetal pole in the bilaterian lineage. We are currently using RNAseq and proteomic approaches in sea urchins and Nematostella to try to reconstruct the molecular mechanisms that may have led to the shift in the site of gastrulation along the AV axis in the bilaterian lineage.

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