Physical and functional cell-matrix uncoupling in a developing tissue under tension

Tissue mechanics play a crucial role in organ development. It relies on cells and extracellular matrix (ECM) mechanical properties, but also on their reciprocal interaction. The relative physical contribution of cells and ECM to morphogenesis is poorly understood. Here, we dissected the mechanics of the envelope of the Drosophila developing leg, an epithelium submitted to a number of mechanical stresses: first stretched, it is then torn apart and withdrawn to free the leg. During stretching, we found that mechanical tension is entirely borne by the ECM at first, then by the cellular monolayer as soon as they detach themselves from one another. Then, each envelope layer is removed by an independent mechanism: while ECM withdraws following local proteolysis, cellular monolayer withdrawal is independent of ECM degradation and driven by an autonomous myosin-II-dependent contraction. These results reveal a physical and functional cell-matrix uncoupling that could timely control tissue dynamics during development.