The Fat-Dachsous planar polarity pathway competes with hinge contraction to orient polarized cell behaviors during Drosophila wing morphogenesis

During tissue morphogenesis, an interplay of biochemical pathways and mechanical cues regulates polarized cell behaviors, the balance of which leads to tissues reaching their correct shape and size.1,2,3,4 A well-studied example of a biochemical regulator is the highly conserved Fat-Dachsous (Ft-Ds) pathway that coordinates planar polarized cell behaviors and growth in epithelial tissues.5,6 For instance, in the Drosophila larval wing disc, the Ft-Ds pathway acts via the atypical myosin Dachs to control tissue shape by promoting the orientation of cell divisions primarily in a proximodistal (PD) direction.7,8 Here, we investigate interactions between Ft-Ds planar polarity and mechanical forces in the developing Drosophila pupal wing. We show that in the early stages of pupal wing development (16-18 h after puparium formation), anteroposterior (AP)-oriented cell divisions and T1 transitions are controlled by the Ft-Ds pathway acting via Dachs. Shortly thereafter, PD-oriented tissue tension is induced across the wing blade by the process of hinge contraction. This opposes the control of Dachs over polarized cell behaviors in a tug-of-war fashion, resulting in more PD-oriented cell divisions and T1s. Furthermore, increased PD tissue tension stabilizes Ft along PD-oriented junctions, suggesting that biomechanical feedback on the Ft-Ds pathway resists the effects of hinge contraction on cell shape. We also show that loss of Dachs results in increased myosin-II stability at cell junctions, revealing compensatory interactions between these two myosins. Overall, we propose that Ft-Ds pathway function constitutes a mechanism whereby tissues are buffered against mechanical perturbations.