Abstract
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.