Active Cell Divisions Generate Exotic Fourfold Orientationally Ordered Phase in Living Tissue

Abstract

AbstractMorphogenesis, the process through which genes generate form, establishes tissue scale order as a template for constructing the complex shapes of the body plan. The extensive growth required to build these ordered substrates is fuelled by cell proliferation, which, naively, should destroy order. The active mechanisms that couple cellular and physical processes to generate and maintain global order, thereby reconciling this seeming contradiction, remain elusive. Using live imaging and tissue cartography, we quantitatively analyze the dynamics of fourfold tissue ordering in the crustacean Parhyale hawaiensis. We show that cell divisions are the main drivers of tissue flow leading to a fourfold orientationally ordered phase. Waves of anisotropic cell proliferation propagate across the embryo with precise choreography, such that defects introduced into the nascent lattice by cell divisions are healed by subsequent divisions through active defect climb. Orchestrating cell proliferation rates and orientations enables cell divisions to organize, rather than fluidize, the tissue. The result is a robust, active mechanism for generating global orientational order in a non-equilibrium system that sets the stage for the subsequent development of shape and form.