Tissue spreading reorganises the extracellular matrix to establish the pre-gastrulation avian blastoderm architecture

Pre-gastrulation vertebrate embryos develop a polarised blastoderm through collective cell spreading (epiboly). The formation and role of this tissue architecture are not well understood. Here, we identify extensive reorganisation of extracellular matrix (ECM) driven by the outward migration of blastoderm edge cells during epiboly in chicken. Proliferation of inner cells and cytoskeleton dynamics of edge cells cooperatively sustain tissue expansion, which remodels the ECM to establish a basal lamina and blastoderm polarity. Blocking edge cell migration by substrate modification or disrupting the basal lamina causes tissue polarity loss and thickening across the blastoderm, prohibiting subsequent gastrulation movements. Biochemical perturbations suggest that remodelling depends on cell-ECM binding. Our findings show a vital role of the mechanical coupling between cell movement and ECM in creating and sustaining the pre-gastrulation tissue architecture.