A Male-Specific Fatty Acid ω-Hydroxylase, SXE1, Is Necessary for Efficient Male Mating in Drosophila melanogaster

Abstract

In Drosophila, sexual differentiation, physiology, and behavior are thought to be mediated by numerous male-and female-specific effector genes whose expression is controlled by sex-specifically expressed transcriptional regulators. One such downstream effector gene, sex-specific enzyme 1 (sxe1, cyp4d21), has been identified in a screen for genes with sex-biased expression in the head. Sxe1 was also identified in another screen as a circadian regulated gene. Here, we analyzed the spatial and temporal regulation of sxe1 and identified a function for this gene in male courtship. We show that male-specific transcriptional regulator DSX M and the clock genes are necessary for cycling of sxe1 mRNA during the diurnal cycle. Similar to sxe1 mRNA, expression of SXE1 protein oscillates in a diurnal fashion, with highest protein levels occurring around midnight. SXE1 protein expression is restricted to nonneuronal cells associated with diverse sensory bristles of both the chemo-and mechanosensory systems. Suppression or knockout of sxe1 significantly reduces mating success throughout the diurnal cycle. Finally, the metabolomic profile of wild-type and sxe1 mutant males revealed that sxe1 likely functions as a fatty acid v-hydroxylase, suggesting that male courtship and mating success is mediated by small compounds generated by this enzyme. DEVELOPMENT and differentiation of sex-specific structures and organs, and the establishment of sex-specific physiological/neuroanatomical traits, are essential processes common to virtually all animals. In Drosophila melanogaster, somatic differentiation of male and female flies is regulated by sex-specific splicing regulators including SEX-LETHAL (SXL) and TRANS-FORMER (TRA) that lead to the expression of maleand female-specific spliced isoforms of the transcription factors, FRUITLESS (FRU

Under-Expression of Chemosensory Genes in Domiciliary Bugs of the Chagas Disease Vector Triatoma brasiliensis

“…For example, in D . melanogaster , a cytochrome P450 (cyp4d21) named sxe1 is differentially expressed between males and females and identified as a circadian-regulated gene involved in male courtship and mating success [72]. Differences in the ratio of cuticular proteins have also been found in the thoracic cuticle of male and female crickets ( Schistocerca gregaria and Locusta migratoria ).…”

Circadian Organization of Behavior and Physiology in Drosophila

“…sxe1 is much more strongly expressed in male flies than in female flies (140). Its transcript and protein are under circadian clock control, with protein levels peaking during the night (141). RNAi-mediated knockdown and disruption of sxe1 reduced male courtship levels but did not abolish circadian regulation (141).…”

“…Its transcript and protein are under circadian clock control, with protein levels peaking during the night (141). RNAi-mediated knockdown and disruption of sxe1 reduced male courtship levels but did not abolish circadian regulation (141). sxe1 is expressed in nonneuronal cells in association with sensory bristles, including those involved in chemosensation and potentially important for courtship behavior (141).…”

Characterization of Drosophila melanogaster cytochrome P450 genes

“…P450s involved in other important endogenous processes in D. melanogaster have also been identified, including Cyp303a1, required for the development and structure of sensory bristles (23), and Cyp4g1, an oenocytespecific P450 required for correct triacylglycerol composition (24). P450s are also involved in behavioral phenotypes in D. melanogaster, with Cyp6a20 associated with aggressive behavior in males (25,26) and Cyp4d21 necessary for efficient male mating (27). In the cockroach Diploptera punctata, Cyp15a1 is involved in the biosynthesis of juvenile hormone III (28).…”