A Novel Function for the Hox Gene Abd-B in the Male Accessory Gland Regulates the Long-Term Female Post-Mating Response in Drosophila

摘要

In insects, products of the male reproductive tract are essential for initiating and maintaining the female post-mating response (PMR). The PMR includes changes in egg laying, receptivity to courting males, and sperm storage. In Drosophila , previous studies have determined that the main cells of the male accessory gland produce some of the products required for these processes. However, nothing was known about the contribution of the gland's other secretory cell type, the secondary cells. In the course of investigating the late functions of the homeotic gene, Abdominal-B (Abd-B) , we discovered that Abd-B is specifically expressed in the secondary cells of the Drosophila male accessory gland. Using an Abd-B BAC reporter coupled with a collection of genetic deletions, we discovered an enhancer from the iab-6 regulatory domain that is responsible for Abd-B expression in these cells and that apparently works independently from the segmentally regulated chromatin domains of the bithorax complex. Removal of this enhancer results in visible morphological defects in the secondary cells. We determined that mates of iab-6 mutant males show defects in long-term egg laying and suppression of receptivity, and that products of the secondary cells are influential during sperm competition. Many of these phenotypes seem to be caused by a defect in the storage and gradual release of sex peptide in female mates of iab-6 mutant males. We also found that Abd-B expression in the secondary cells contributes to glycosylation of at least three accessory gland proteins: ovulin (Acp26Aa), CG1656, and CG1652. Our results demonstrate that long-term post-mating changes observed in mated females are not solely induced by main cell secretions, as previously believed, but that secondary cells also play an important role in male fertility by extending the female PMR. Overall, these discoveries provide new insights into how these two cell types cooperate to produce and maintain a robust female PMR. Author Summary Similar to the prostate gland and seminal vesicle in mammals, the Drosophila male accessory gland produces seminal fluid proteins that are critical for individual male reproductive success. In Drosophila, many of these proteins function to induce a suite of long-lasting physiological changes in mated females, like increased egg laying and decreased receptivity to secondary courtships. While investigating the cis -regulatory region of the Hox gene, Abd-B , we found that Abd-B is specifically expressed in a mostly uncharacterized cell-type of the accessory gland, called the secondary cells. Using regulatory mutants of Abd-B , we were able to perturb the function of the secondary cells to show that the secondary cells play a critical role in extending the duration of the post-mating response in females. The induced physiological changes in the female result in a genetic advantage for the genes of the copulating male in populating the next generation. Interestingly, the function of the Abd-B class genes in seminal protein producing tissues seems to be an ancient and conserved function, as the orthologues of Abd-B in mammals, the hox9-13 class of genes, are expressed in the mammalian prostate and seminal vesicle.