Apical constriction powers amnioserosa contraction during Drosophila dorsal closure. The nucleation, movement and dispersal of apicomedial actomyosin complexes generates pulsed apical constrictions during early closure. Persistent apicomedial and circumapical actomyosin complexes drive unpulsed constrictions that follow. Here, we show that the microtubule end-binding proteins EB1 and Patronin pattern constriction dynamics and contraction kinetics by coordinating the balance of actomyosin forces in the apical plane. We find that microtubule growth from moving Patronin platforms governs the spatiotemporal dynamics of apicomedial myosin through the regulation of RhoGTPase signaling by transient EB1-RhoGEF2 interactions. We uncover the dynamic reorganization of a subset of short non-centrosomally nucleated apical microtubules that surround the coalescing apicomedial myosin complex, trail behind it as it moves and disperse as the complex dissolves. We demonstrate that apical microtubule reorganization is sensitive to Patronin levels. Microtubule depolymerization compromised apical myosin enrichment and altered constriction dynamics. Together, our findings uncover the importance of reorganization of an intact apical microtubule meshwork, by moving Patronin platforms and growing microtubule ends, in enabling the spatiotemporal modulation of actomyosin contractility and, through it, apical constriction.

SummaryThe contraction of the amnioserosa by apical constriction provides the major force for Drosophila dorsal closure. The nucleation, movement and dispersal of apicomedial actomyosin complexes generate pulsed constrictions during early dorsal closure whereas persistent apicomedial and circumapical actomyosin complexes drive the unpulsed constrictions that follow. What governs the spatiotemporal assembly of these distinct complexes, endows them with their pulsatile dynamics, and directs their motility remains unresolved. Here we identify an essential role for microtubule growth in regulating the timely contraction of the amnioserosa. We show that a symmetric cage of apical microtubules forms around the coalescing apicomedial myosin complex. An asymmetric tail of microtubules then trails the moving myosin complex and disperses as the myosin complex dissolves. Perturbing microtubule growth reduced the coalescence and movement of apicomedial myosin complexes and redistributed myosin and its activator, Rho kinase to the circumapical pool and altered the cell constriction and tissue contraction dynamics of the amnioserosa. We show that RhoGEF2, the activator of the Rho1 GTPase, is transiently associated with microtubule plus end binding protein EB1 and the apicomedial actomyosin complex. Our results suggest that microtubule growth from moving patronin platforms modulates actomyosin contractility through the spatiotemporal regulation of Rho1 activity. We propose that microtubule reorganisation enables a self-organising, mechanosensitive feedback loop that buffers the tissue against mechanical stresses by modulating actomyosin contractility.