Yolk granule fusion and microtubule aster formation regulate cortical granule translocation and exocytosis in zebrafish oocytes

Dynamic reorganization of the cytoplasm is key to many core cellular processes, such as cell division, cell migration and cell polarization. Cytoskeletal rearrangements are thought to constitute the main drivers of cytoplasmic flows and reorganization. In contrast, remarkably little is known about how dynamic changes in size and shape of cell organelles affect large-scale cytoplasmic organization. Here, we show that within the maturing zebrafish oocyte, the surface localization of exocytosis-competent cortical granules upon germinal vesicle breakdown is achieved by the combined activities of yolk granule fusion and microtubule aster formation and translocation. We find that cortical granules are moved towards the oocyte surface through radially-outward cytoplasmic flows induced by yolk granules fusing within the oocyte center in response to GV breakdown. We further show that vesicles decorated with the small Rab GTPase Rab11, a master regulator of vesicular trafficking and exocytosis, accumulate together with cortical granules at the oocyte surface. This accumulation is achieved by Rab11-positive vesicles being transported by acentrosomal microtubule asters, the formation of which is induced by the release of CyclinB/Cdk1 upon GV breakdown, and which display a net movement towards the oocyte surface by preferentially binding to the oocyte actin cortex. We finally demonstrate that the decoration of cortical granules by Rab11 at the oocyte surface is needed for cortical granule release and subsequent chorion elevation, a process central in oocyte activation. Collectively, these findings unravel a yet unrecognized role of organelle fusion, functioning together with cytoskeletal rearrangements, in determining cytoplasmic organization during oocyte maturation.