Regionalized tissue fluidization by an actomyosin cable is required for epithelial gap closure during insect gastrulation

Many animal embryos pull and close an epithelial sheet around the spherical or ellipsoidal egg surface during a gastrulation process known as epiboly. The ovoidal geometry dictates that the epithelial sheet first expands and subsequently compacts. Moreover, the epithelial sheet spreading over the sphere is mechanically stressed and this stress needs to be released. Here we show that during extraembryonic tissue (serosa) epiboly in the red flour beetle Tribolium castaneum, the non-proliferative serosa becomes regionalized into two distinct territories: a dorsal region under higher tension away from the leading edge with larger non-rearranging cells, and a more fluid ventral region under lower tension surrounding the leading edge with smaller cells undergoing cell intercalation. Our results suggest that fluidization of the leading edge is caused by a heterogeneous actomyosin cable that drives sequential eviction and intercalation of individual cells away from the serosa margin. Since this developmental solution utilized during epiboly resembles the mechanism of wound healing in other systems, we propose actomyosin cable-driven local tissue fluidization as a conserved morphogenetic module for closure of epithelial gaps.