Yolk polypeptide secretion and vitelline membrane deposition in a female sterile Drosophila mutant

Ovarian follicle cells of wild type Drosophila melanogaster simultaneously secrete yolk polypeptides (YP1, YP2 and YP3) and vitelline membrane proteins. In order to understand the relationship between these two secretory activities, we have investigated the ultrastructure of a female sterile mutation that alters YP1 secretion and vitelline membrane deposition. Homozygous fs(1)1163 females lay eggs that collapse and contain reduced quantities of YP1. Secretory granules in follicle cells contain an electron-translucent component that is assembled into the developing vitelline membrane in both mutant and wild-type ovaries, and an electron-dense component that disperses after secretion in wild-type ovaries. Mutant ovaries differ from wild-type by (1) having larger secretory granules (2) forming clumps of the dense secretory component within the developing vitelline membrane (3) accumulating more tubules in the cortical ooplasm of vitellogenic oocytes, and (4) possessing altered yolk spheres. Mutant ovaries implanted into wild-type hosts showed no improvement in the secretory granules and slight improvement in the vitelline membrane clumps but amelioration of the oocyte phenotypes. Since genetic evidence suggests that the fs(1)1163 mutation resides in or near the Yp1 gene and biochemical data show that the mutation alters YP1 structure, we conclude that the ultrastructural phenotypes are due to a structurally abnormal YP1 in the mutant. The alteration in vitelline membrane structure caused by the dense clumps could account for collapsed eggs and, hence, the female sterility of the mutant.