Abstract
The development of sexually dimorphic morphology and the potential for sexually dimorphic behavior in Drosophila are regulated by the Fruitless (Fru) and Doublesex (Dsx) transcription factors. Several direct targets of Dsx have been identified, but direct Fru targets have not been definitively identified. We show that Drosophila leucine-rich repeat G protein-coupled receptor 3 (Lgr3) is regulated by Fru and Dsx in separate populations of neurons. Lgr3 is a member of the relaxin-receptor family and a receptor for Dilp8, necessary for control of organ growth. Lgr3 expression in the anterior central brain of males is inhibited by the B isoform of Fru, whose DNA binding domain interacts with a short region of an Lgr3 intron. Fru A and C isoform mutants had no observed effect on Lgr3 expression. The female form of Dsx (Dsx(F)) separately up- and down-regulates Lgr3 expression in distinct neurons in the abdominal ganglion through female- and male-specific Lgr3 enhancers. Excitation of neural activity in the Dsx(F)-up-regulated abdominal ganglion neurons inhibits female receptivity, indicating the importance of these neurons for sexual behavior. Coordinated regulation of Lgr3 by Fru and Dsx marks a point of convergence of the two branches of the sex-determination hierarchy.
Highlights
The development of sexually dimorphic morphology and the potential for sexually dimorphic behavior in Drosophila are regulated by the Fruitless (Fru) and Doublesex (Dsx) transcription factors
We examined the expression of the leucine-rich repeat G protein-coupled receptor 3 (Lgr3) gene using a bacterial artificial chromosome (BAC) reporter, Lgr3-GAL4::VP16, encompassing the Lgr3 locus, with the GAL4 DNA-binding domain and VP16 activation domain inserted in place of the first coding exon of Lgr3 (Fig. 1A)
In the fruit fly Drosophila melanogaster, this process is carried out by a series of genes ending with fruitless and doublesex. We found that both Fru and Dsx regulate the expression of the leucine-rich repeat G protein-coupled receptor 3 (Lgr3) gene in separate sets of neurons, including neurons important for female sexual behavior
Summary
The development of sexually dimorphic morphology and the potential for sexually dimorphic behavior in Drosophila are regulated by the Fruitless (Fru) and Doublesex (Dsx) transcription factors. The male-specific forms of Fru (FruM) act in a subset of the neurons within the male’s nervous system to establish the potential for social interactions such as courtship behavior and aggression Dsx acts in subsets of both neural and nonneural tissues of males and females to regulate behavioral and nonbehavioral aspects of sexual development Many Dsx target genes encode well-known transcription factors and cell–cell signaling molecules that function sex-nonspecifically in most tissues in which they are expressed. In other tissues, Dsx directs the sexspecific expression of these genes to generate sex-specific aspects of development. Our understanding of how FruM specifies the potential for sex-specific behavior remains limited
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