Multiple contact sites between cells and the vitelline envelope coordinate tissue flows in Drosophila gastrulation

Gastrulation is thought to be driven primarily by forces generated within individual cells. These cell-intrinsic forces collectively induce tissue-scale flows and transform the monolayered embryo into a multilayered structure. However, as the embryo constitutes a mechanically closed system, these flows must be balanced by regions of resistance or anchoring to enable asymmetric morphogenesis. In the Drosophila embryo, integrin-mediated attachment of the blastoderm to the vitelline envelope has been shown to stabilize germ band extension at the organismal scale. Disrupting such an attachment leads to a characteristic twisting phenotype. Yet, how this attachment shapes concurrent global morphogenetic events remains unclear. We discovered that the integrin -subunit scab, which mediates the attachment, is expressed in three different regions of the cellular blastoderm near prominent invagination events. Through a combination of light-sheet imaging, genetic and mechanical perturbations, we demonstrate that integrin-enhanced friction is essential for unidirectional tissue flows in those regions, with effects including cephalic furrow positioning and epithelial stability. Guided by a minimal physical model, we further show that multiple attachment sites enhance the robustness and reproducibility of global tissue movements. Together, our results indicate that Drosophila gastrulation emerges from a balance between cell-intrinsic force generation and spatially distributed adhesion to the surrounding envelope, which together shape tissue flows at the embryo scale.