Cell-intrinsic compliance mechanism enables release of tensile stress to prevent tissue rupture

Abstract Contractile forces are necessary to sculpt tissue structures and organ shapes during morphogenesis. In the early embryo, this presents an engineering challenge as the deforming tissue can be relatively large, while the forces thus generated might be poorly compartmentalized, generating tensile stresses that can cause damage if unmitigated. Here we show that during Drosophila gastrulation, the squamous morphogenesis of the extraembryonic amnioserosa functions mechanically to release tensile stresses yielded from the neighboring ectodermal convergent-extension and mesodermal invagination. Amnioserosa master regulator Zen transcriptionally silences shroom to endow it with low junctional actomyosin stresses, thereby ensuring high mechanical compliance. Loss of Zen, or targeted ectopic expression of Shroom in the amnioserosa using a novel optogenetic Gal4 system, leads to increased junctional myosin, thereby causing load-dependent tissue ruptures. Our data establish a previously unknown function for the Drosophila extraembryonic tissue, whereby cell-intrinsic mechanical compliance prevents tissue rupture to mitigate inter-tissue mechanical conflicts.