Ecdysone Receptor Acts in fruitless- Expressing Neurons to Mediate Drosophila Courtship Behaviors

Abstract

Summary In Drosophila melanogaster, fruitless (fru) encodes male-specific transcription factors (FRUM; encoded by fru P1) required for courtship behaviors [reviewed in 1]. However, downstream effectors of FRUM throughout development are largely unknown [2-5]. During metamorphosis the nervous system is remodeled for adult function, the timing of which is coordinated by the steroid hormone 20-hydroxy ecdysone (ecdysone) through the ecdysone receptor, a heterodimer of the nuclear receptors EcR (isoforms are EcR-A, EcR-B1, or EcR-B2) and Ultraspiracle (USP) [reviewed in 6]. Here, we show that genes identified as regulated downstream of FRUM during metamorphosis are significantly overrepresented with genes known to be regulated in response to ecdysone or EcR. FRUM and EcR isoforms are co-expressed in neurons in the CNS during metamorphosis in an isoform-specific manner. Reduction of EcR-A levels in fru P1-expressing neurons of males caused a significant increase in male-male courtship activity and significant reduction in size of two antennal lobe glomeruli. Additional genes were identified that are regulated downstream of EcR-A in fru P1-expressing neurons. Thus, EcR-A is required in fru P1-expressing neurons for wild type male courtship behaviors and the establishment of male-specific neuronal architecture.

Sex-switching of theDrosophilabrain by two antagonistic chromatin factors

“…16 Similarly, numerous genes are up-or downregulated by individual Fru isoforms, Fru MA (156 genes), Fru MB (116 genes) or Fru MC (109 genes), in male pupae at 48 h APF. 16 Apart from the genes predicted by this microarray analysis, proapoptotic genes, head involution defective (hid), grim and reaper (rpr), are potential targets of Fru, because female-specific cell death is responsible for the smaller number of cells in the female mAL cluster. In females with MARCM clones that are homozygous for Df(3L)H99 in which the hid, grim and rpr genes are deleted, the number of mAL neurons increases to a level similar to that in wild-type males.…”

“…A reduction in EcR isoform-A (EcR-A) in males results in increased male-male courtship activity and a reduction in the sizes of two sexually dimorphic antennal lobe glomeruli, two phenotypes reminiscent of those induced by the loss of fru. 16,23 Moreover, genes associated with ecdysone signaling are overrepresented in fru modifiers isolated by genetic screens (ref. 24 and Ito H, unpublished data).…”

“…The courtship-stimulating effect of neurons coincides with the two ecdysone pulses at the early pupal stage. Dalton et al (2009) 16 reported that about one third of the genes regulated downstream from fru contain ecdysone receptor (EcR) binding sites. A reduction in EcR isoform-A (EcR-A) in males results in increased male-male courtship activity and a reduction in the sizes of two sexually dimorphic antennal lobe glomeruli, two phenotypes reminiscent of those induced by the loss of fru.…”

Socially-Responsive Gene Expression in MaleDrosophila melanogasterIs Influenced by the Sex of the Interacting Partner

“…The somatic sexdetermination pathway regulates these behaviors (reviewed in Cline 2005;Shirangi and McKeown 2007) and sexually dimorphic development, including that of the nervous system (Finley et al 1997;Kimura et al 2005;Manoli et al 2005;Stockinger et al 2005;Rideout et al 2007;Sanders and Arbeitman 2008;Mellert et al 2010;Rideout et al 2010;reviewed in Billeter et al 2006). Although target loci of the transcriptional regulatory members of this pathway are known (Burtis et al 1991;Cann et al 2000;Kopp et al 2000;Dauwalder et al 2002;Fujii and Amrein 2002;Drapeau et al 2003;Arbeitman et al 2004;Goldman and Arbeitman 2007;Lazareva et al 2007;Fujii et al 2008;Dalton et al 2009), few have clearly defined functions in behavior and neural development. Several Drosophila microarray studies were key to identifying most of these downstream targets (Arbeitman et al 2004;Goldman and Arbeitman 2007;Dalton et al 2009), but the strategies used do not allow us to distinguish target genes that affect development of the nervous system from those that impact physiology and behavior post development.…”

“…Although target loci of the transcriptional regulatory members of this pathway are known (Burtis et al 1991;Cann et al 2000;Kopp et al 2000;Dauwalder et al 2002;Fujii and Amrein 2002;Drapeau et al 2003;Arbeitman et al 2004;Goldman and Arbeitman 2007;Lazareva et al 2007;Fujii et al 2008;Dalton et al 2009), few have clearly defined functions in behavior and neural development. Several Drosophila microarray studies were key to identifying most of these downstream targets (Arbeitman et al 2004;Goldman and Arbeitman 2007;Dalton et al 2009), but the strategies used do not allow us to distinguish target genes that affect development of the nervous system from those that impact physiology and behavior post development.…”