Polarized Cortical Tension drives Zebrafish Epiboly Movements

Abstract

The physical principles underlying the biomechanics of morphogenetic processes are largely unknown. Epiboly is an essential embryonic event in which three distinct tissues coordinate to direct the expansion of the blastoderm. How and where forces are generated during epiboly and how these are globally coupled remains elusive. Here we first develop a method, Hydrodynamic Regression (HR), to infer 3D dynamic pressure fields, mechanical power densities and cortical surface tension profiles within living organisms. HR is based on velocity measurements retrieved from 2D+T microscopy time-lapses and their hydrodynamic modeling. We then applied this method to identify biomechanically active structures during epiboly in the zebrafish and the changes in the distribution of cortex local tension as epiboly progresses. Based on these results, we propose a novel simple physical description for epiboly, where tissue movements are directed by a polarized gradient of cortical tension. We found that this tensional gradient relies on local contractile forces at the cortex, differences in the elastic properties of cortex components and force passive transmission within the incompressible yolk cell. All in all, our work identifies a novel way to physically regulate concerted cellular movements that will be fundamental for the mechanical control of many morphogenetic processes.