Abstract
Many animal embryos pull and close an epithelial sheet around the 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 spreading epithelium is mechanically stressed and this stress needs to be released. Here we show that during extraembryonic tissue (serosa) epiboly in the insect Tribolium castaneum, the non-proliferative serosa becomes regionalized into a solid-like dorsal region with larger non-rearranging cells, and a more fluid-like ventral region surrounding the leading edge with smaller cells undergoing intercalations. Our results suggest that a heterogeneous actomyosin cable contributes to the fluidization of the leading edge by driving 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, we propose actomyosin cable-driven local tissue fluidization as a conserved morphogenetic module for closure of epithelial gaps.
Highlights
Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly
In the red flour beetle, Tribolium castaneum, extraembryonic serosal cells are initially specified as an anterior cap of the cellular blastoderm, which subsequently spreads over the gastrulating embryonic part of the blastoderm[11]
The epibolic expansion of the Tribolium serosa to envelop the entire egg surface is a dynamic morphogenetic process constrained by the ellipsoidal geometry of the egg and the mechanical properties of the tissue
Summary
Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly. The spreading serosal tissue expands over the posterior pole and eventually closes ventrally over the contracting embryo in a process known as serosa window closure[12,13,14] It is not understood how the leading serosal cells at the rim of the serosa window achieve final compaction. It is unknown if and how mechanical tension arises and gets released in the serosal tissue during spreading To address these questions, we use the Tribolium serosa epiboly and closure as a model to understand how the mechanical properties of serosal cells promote wrapping of a non-dividing epithelial sheet around an ellipsoidal egg. We find that serosal tissue becomes mechanically regionalized along the dorsal–ventral axis and that its ventral closure is facilitated by a local, actomyosin-cable-mediated fluidization at the leading edge
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