beta-Catenin asymmetries after all animal/vegetal- oriented cell divisions in Platynereis dumerilii embryos mediate binary cell-fate specification

Abstract

In response to Wnt signaling during animal development, beta-catenin accumulates in nuclei to mediate the transcriptional activation of target genes. Here, we show that a highly conserved beta-catenin in the annelid Platynereis dumerilii exhibits a reiterative, nearly universal embryonic pattern of nuclear accumulation remarkably similar to that observed in the nematode Caenorhabditis elegans. Platynereis exhibits beta-catenin sister-cell asymmetries after all cell divisions that occur along the animal/vegetal axis beginning early in embryogenesis, but not after two transverse divisions that establish bilateral symmetry in the trunk. Moreover, ectopic activation of nuclear beta-catenin accumulation in Platynereis causes animal-pole sister cells, which normally have low nuclear beta-catenin levels, to adopt the fate of their vegetal-pole sisters, which normally have high nuclear beta-catenin levels. The presence of reiterative and functionally important beta-catenin asymmetries in two distantly related animal phyla suggests an ancient metazoan origin of a beta-catenin-mediated binary cell-fate specification module.