Regulation of tensile stress in response to external forces coordinates epithelial cell shape transitions with organ growth and elongation

While cell-autonomous roles for actomyosin contractility and adherens junction regulation in epithelial morphogenesis have been studied extensively, little is understood about how contractility and adhesion in epithelial tissue respond to external forces, for example arising from growth of neighboring tissues. Epithelial cells must adjust their mechanical properties and accommodate external forces to maintain tissue integrity and their desired 3D cell shape. We use the Drosophila egg chamber to address how growth of a neighboring tissue is accommodated by an epithelial sheet while also undergoing 3D cell shape transitions. The developing egg chamber is composed of a growing germline which serves as the source of external forces acting on the enveloping follicle epithelium. We demonstrate that adherens junction lengthening and junctional exclusion of Myosin II (Myo II) correlate with a decrease in tension at adherens junctions (AJs) of the follicle epithelium while the germline grows. As the tension in the junctional network decreases, the epithelium undergoes a cuboidal to columnar cell shape transition which correlates with contact to specific germline cells. Strikingly, despite the decrease in tension in the junctions, the epithelium locally reinforces its Myo II and AJ levels dependent on contact with specific germline cells to stabilize cuboidal cell shape against external forces arising from germline growth and shape. We furthermore implicate Myo II and AJ reinforcement in sculpting the overall shape of the egg chamber by imposing local circumferential constraints on germline. This work provides insight into how 3D epithelial cell shapes arise in the context of external forces, how relaxation and resistance to forces coordinates expansion of two neighbouring tissues and how isotropic growth can be redirected into polarized organ morphogenesis