Gatekeeper function for Short stop at the ring canals of the Drosophila ovary

Abstract

Growth of the Drosophila oocyte requires transport of cytoplasmic materials from the interconnected sister cells (nurse cells) through ring canals, the cytoplasmic bridges that remained open after incomplete germ cell division. Given the open nature of the ring canals, it is unclear how the direction of transport through the ring canal is controlled. In this work, we show that a single Drosophila spectraplakin Short stop (Shot) controls the direction of flow from nurse cells to the oocyte. Knockdown of shot changes the direction of transport through the ring canals from unidirectional (toward the oocyte) to bidirectional. After shot knockdown, the oocyte stops growing, resulting in a characteristic small oocyte phenotype. In agreement with this transport-directing function of Shot, we find that it is localized at the asymmetric actin baskets on the nurse cell side of the ring canals. In wild-type egg chambers, microtubules localized in the ring canals have uniform polarity (minus ends toward the oocyte), while in the absence of Shot, these microtubules have mixed polarity. Together, we propose that Shot functions as a gatekeeper directing transport from nurse cells to the oocyte via the organization of microtubule tracks to facilitate the transport driven by the minus-end-directed microtubule motor cytoplasmic dynein. VIDEO ABSTRACT.