Drosophila melanogaster Male Somatic Cells Feminized Solely by TraF Can Collaborate With Female Germ Cells to Make Functional Eggs

Abstract

Abstract Female differentiation of Drosophila germ cells is induced by cell-nonautonomous signals generated in the gonadal soma that work with germ-cell-autonomous signals determined by germ-cell X chromosome dose. Generation of the nonautonomous feminizing signals was known to involve female-specific protein encoded by the master sex-determination gene Sex-lethal (Sxl) acting on its switch-gene target transformer (tra) to produce TraF protein. However, it was not known whether Sxl's action on tra alone would suffice to trigger a fully feminizing nonautonomous signal. We developed a constitutively feminizing tra transgene that allowed us to answer this question. In gynanders (XX//XO mosaics) feminized by this TraF transgene, functionally Sxl− haplo-X (chromosomally male) somatic cells collaborated successfully with diplo-X (chromosomally female) germ cells to make functional eggs. The fertility of such gynanders shows not only that TraF is sufficient to elicit a fully feminizing nonautonomous signal, but also that haplo-X somatic cells can execute all other somatic functions required for oogenesis, despite the fact that their genome is not expected to be dosage compensated for such diplo-X-specific functions. The unexpected observation that some TraF-feminized gynanders failed to lay their eggs showed there to be diplo-X cells outside the gonad for which TraF-feminized haplo-X cells cannot substitute.