Synchronization in epithelial tissue morphogenesis

Coordination of cell behavior is central to morphogenesis, when arrays of cells simultaneously undergo shape changes or dynamic rearrangements. In epithelia, cell shape changes invariably exert mechanical forces, which adjacent cells could sense to trigger an active response. However, molecular mechanisms for such mechano-transduction and especially their role for tissue-wide coordination in morphogenesis have remained ambiguous. Here, we investigate the function of Tmc, a key component of cellular mechano-transduction in vertebrate hearing, for coordination of cell dynamics in the epithelial amnioserosa of Drosophila embryos. We directly probed cell-cell mechano-transduction in vivo by opto-chemically inducing single-cell contractions and discovered a Tmc-dependent contraction response in neighboring cell groups. On the tissue scale, we uncover synchronization of neighboring cell area oscillations, which is impaired in Tmc mutants. A data-driven model of Tmc-dependent cell-cell interactions predicts that synchronization leads to an isotropic force map and effectively shields the tissue from external mechanical pulling. By microdissection, we detect equal junction tension along the axial and lateral axis in wild-type but increased lateral tension in Tmc mutants. Thus, Tmc transduces forces into an intracellular response that coordinates mechanical cell behavior in epithelial tissue.