Adhesion-driven tissue rigidification triggers epithelial cell polarity

Abstract

The active regulation of tissue material properties via phase transitions is central in morphogenesis. Transitions abruptly occur at critical points in diverse control parameters, including cell density, shape or adhesion. Whether these parameters are interdependent, performing redundant or distinct functions, is unknown. Here we show that co-regulation of multiple control parameters impacts not only tissue deformability, but also cell polarization. We theoretically define a new phase diagram capturing the material states of zebrafish pluripotent tissues and show that they cross simultaneously critical points in cell density, connectivity and adhesion strength. Combining optogenetics, biophysical measurements and quantitative morphometrics, we independently modulate each parameter, identifying adhesion as the main determinant of tissue rheology. Unexpectedly, uncoupling adhesion-driven from density-driven rigidification in amorphous tissues triggers epithelial organization via tricellular junction formation, followed by luminogenesis and apicobasal polarization. Altogether, this work reveals the non-linear dynamics of emergent tissue mechanics as instructive mechanisms of tissue organization.