Left and right symmetry breaking is involved in many developmental processes that are important to form bodies and organs. One of them is the epithelial rotation of developing organs. However, how epithelial cells move, how they break symmetry to define common direction of their collective movement and what function rotational epithelial motions have in morphogenesis remain elusive. Here, we identified a dynamic actomyosin network with preferred retrograde contractility at the basal side of the rotating follicle epithelium in Drosophila oogenesis. We provide evidence that unidirectional epithelial rotation is a result of actomyosin asymmetry cue transmission onto a tissue plane synchronized by the atypical cadherin Fat2, a key planar cell polarity regulator in Drosophila oogenesis. We found that Fat2 directs actomyosin contractility to move the epithelial tissue in order to provide directed elongation of follicle cells. In contrast, loss of Fat2 results in anisotropic non-muscle Myosin II pulses that are disorganized in plane and deform cell shape, tissue and Drosophila eggs. Our data indicate that directed elongation of follicle cells is critical for proper Drosophila egg morphogenesis. Together, we demonstrate the importance of atypical cadherins in the control of cell mechanics, left/right symmetry breaking and its propagation onto the tissue scale to facilitate proper organ morphogenesis. This process may be evolutionarily conserved in rotating animal organs.
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