PVF1/PVR signaling and apoptosis promotes the rotation and dorsal closure of the Drosophila male terminalia

Abstract

The <i>Drosophila</i> adult male terminalia originate from the genital disc. During the pupal stages, the external parts of terminalia evert from two ventral stalks; the everted left and right dorsal halves fuse at the dorsal midline. At the same time the male terminalia perform a 360 clockwise rotation. Several mutations are known to affect the rotation of the male terminalia, while none is known to affect dorsal closure. We show here that the <i>Pvf1</i> gene, encoding one of the three <i>Drosophila</i> homologues of the mammalian VEGF/PDGF growth factors, is required for both processes. Males either mutant for <i>Pvf1</i> or bearing a dominant negative form of <i>Pvr</i> or<i> stasis (stai), </i>the unique PVF<i> </i>receptor, do not complete either rotation or dorsal closure.<i> Pvf1</i> expression in the genital disc is restricted to the A8 cells. However, PVF1/PVR<i> </i>signaling influences A8, A9 and A10 cells, suggesting that the PVF1 protein diffuses from its source. Flies hemizygous for the apoptotic genes <i>hid, reaper </i>and <i>grim, </i>or mutant for <i>puckered </i>which encodes a phosphatase that down-regulates the n-Jun-N<i> </i>terminal kinase pathway, lead to the same phenotypes as mutations in PVF1/PVR. Our results indicate that PVF1/PVR signaling functions not only in apoptotic phenomena but are also required during rotation and dorsal closure of the <i>Drosophila</i> male genital disc.