Nonautonomous Sex Determination Controls Sexually Dimorphic Development of the Drosophila Gonad

Abstract

Sex determination in Drosophila is commonly thought to be a cell-autonomous process, where each cell decides its own sexual fate based on its sex chromosome constitution (XX versus XY). This is in contrast to sex determination in mammals, which largely acts nonautonomously through cell-cell signaling. Here we examine how sexual dimorphism is created in the Drosophila gonad by investigating the formation of the pigment cell precursors, a male-specific cell type in the embryonic gonad. Surprisingly, we find that sex determination in the pigment cell precursors, as well as the male-specific somatic gonadal precursors, is non-cell autonomous. Male-specific expression of Wnt2 within the somatic gonad triggers pigment cell precursor formation from surrounding cells. Our results indicate that nonautonomous sex determination is important for creating sexual dimorphism in the Drosophila gonad, similar to the manner in which sex-specific gonad formation is controlled in mammals.

Somatic gonadal cells: The supporting cast for the germline

“…However, the msSGPs are lost in later stages in these mutants, suggesting a requirement for the presence of SGPs for msSGP maintenance (DeFalco et al, 2003(DeFalco et al, , 2008. Consistent with these results, the survival of msSGPs is regulated in a cell non-autonomous manner by the sex determination genes, transformer (tra) and doublesex (dsx) (DeFalco et al, 2003(DeFalco et al, , 2008.…”

“…In addition, another male-specific cell type is observed around the periphery of the gonad at embryonic stage 17, called the pigment cells (Fig. 1;DeFalco et al, 2008). These cells persist to adult stages and may perform an important signaling role during pupal development to promote testis morphogenesis (Nanda et al, 2009).…”

“…Thus, not only is it important for the SGPs to communicate with the germline, but they also regulate the development of other cell types within the gonad, including the msSGPs. Pigment cells are also recruited to the gonad during embryogenesis (DeFalco et al, 2008;Hempel and Oliver, 2007). These cells are derived from the fat body, and express Sox100B (DeFalco et al, 2008).…”

Sexual Back Talk With Evolutionary Implications: Stimulation of the Drosophila Sex-Determination Gene Sex-lethal by Its Target transformer

“…Cell-nonautonomy in the sexual differentiation of Drosophila gonads was first reported by Fung and Gowen (1957) and shown most recently by Defalco et al (2008). However, because none of these examples seemed to involve effects on the sexually determined state of those cells in sensu stricto-the functional state of Sxl-there was no reason a priori to expect autonomous behavior more than nonautonomous behavior.…”

Current Topics in Organogenesis and Gametogenesis

“…This was supported by a recent study from the Van Doren lab (Johns Hopkins University) investigating how the pigment cells, which surround the testis, are specified. 2 These are male specific cells and there is no counterpart in female gonads. This cell type is induced non-autonomously by fat body mesoderm in male gonads during embryogenesis, the inducing factor being Wnt2.…”