Regionalized Regulation of Actomyosin Organization Influences Cardiomyocyte Cell Shape Changes During Chamber Curvature Formation

Cardiac chambers emerge from a heart tube that balloons and bends to create expanded ventricular and atrial structures, each containing a convex outer curvature (OC) and a recessed inner curvature (IC). A comprehensive understanding of the cellular and molecular mechanisms underlying the formation of these characteristic curvatures remains lacking. Here, we demonstrate in zebrafish that the initially similar populations of OC and IC ventricular cardiomyocytes diverge in the organization of their actomyosin cytoskeleton and subsequently acquire distinct OC and IC cell shapes. Altering actomyosin dynamics hinders cell shape changes in the OC, and mosaic analyses indicate that actomyosin regulates cardiomyocyte shape in a cell-autonomous manner. Additionally, both blood flow and the transcription factor Tbx5a influence the basal enrichment of actomyosin and squamous cell morphologies in the OC. Together, our findings demonstrate that intrinsic and extrinsic factors intersect to control actomyosin organization in OC cardiomyocytes, which in turn promotes the cell shape changes that drive curvature morphogenesis.