Wnt/Frizzled signaling controls C. elegans gastrulation by activating actomyosin contractility

Embryonic patterning mechanisms regulate the cytoskeletal machinery that drives morphogenesis, but there are few cases where links between patterning mechanisms and morphogenesis are well understood. We have used a combination of genetics, in vivo imaging, and cell manipulations to identify such links in C. elegans gastrulation. Gastrulation in C. elegans begins with the internalization of endodermal precursor cells in a process that depends on apical constriction of ingressing cells.

We show that ingression of the endodermal precursor cells is regulated by pathways, including a Wnt-Frizzled signaling pathway, that specify endodermal cell fate. We find that Wnt signaling has a role in gastrulation in addition to its earlier roles in regulating endodermal cell fate and cell-cycle timing. In the absence of Wnt signaling, endodermal precursor cells polarize and enrich myosin II apically but fail to contract their apical surfaces. We show that a regulatory myosin light chain normally becomes phosphorylated on the apical side of ingressing cells at a conserved site that can lead to myosin-filament formation and contraction of actomyosin networks and that this phosphorylation depends on Wnt signaling.

We conclude that Wnt signaling regulates C. elegans gastrulation through regulatory myosin light-chain phosphorylation, which results in the contraction of the apical surface of ingressing cells. These findings forge new links between cell-fate specification and morphogenesis, and they represent a novel mechanism by which Wnt signaling can regulate morphogenesis.