ADrosophilaDEG/ENaC Subunit Functions Specifically in Gustatory Neurons Required for Male Courtship Behavior

Abstract

Detection of specific female pheromones stimulates courtship behavior in Drosophila melanogaster males, but the chemosensory molecules, cells and mechanisms involved remain poorly understood. Here we show that ppk25, a DEG/ENaC ion channel subunit required for normal male response to females, is expressed at highest levels in a single sexually dimorphic gustatory neuron of most taste hairs on legs and wings, but not in neurons that detect courtship-inhibiting pheromones or food. Synaptic inactivation of ppk25-expressing neurons, or knockdown of ppk25 expression in all gustatory neurons significantly impairs male response to females, whereas gustatory expression of ppk25 rescues the courtship behavior of ppk25 mutant males. Remarkably, the only other detectable albeit significantly weaker expression of ppk25 occurs in olfactory neurons implicated in modulation of courtship behavior. However, expression of ppk25 in olfactory neurons is not required for male courtship under our experimental conditions. These data show that ppk25 functions specifically in peripheral taste neurons involved in activation of courtship behavior, an unexpected function for this type of channel. Furthermore, our work identifies a small subset of gustatory neurons with an essential role in activation of male courtship behavior, most likely in response to female pheromones.

Genes and circuits of courtship behaviour in Drosophila males

“…It remains to be determined how a single sensory cell responds to both volatile (cVA) and non-volatile (7-T) ligands, and whether this cell contributes to the interaction between olfaction and gustation in modulating courtship behaviour. Interestingly, these ppk23-and ppk29-expressing sensory neurons in the leg are also positive for fru and have sexually dimorphic projections in the thoracic ganglia; in females their axons terminate exclusively on the ipsilateral side, whereas in males some axons cross the midline to form contralateral terminals [60][61][62][63][64][65][66][67] , which could potentially contribute to the control of lateralized male behaviours, such as unilateral wing vibration during courtship [3][4][5] and scanning by zigzag walking 68 . The zigzag walk is a strategy that males adopt under conditions of darkness in order to find females through chemical cues (visual tracking of a courtship target is impossible in the dark) 68 .…”

“…An additional protein group implicated in gustatory reception is the degenerin/epithelial Na + channel (DEG/ENaC) family encoded by pickpocket (ppk) and related genes [60][61][62][63][64][65] . Although some of the DEG/ENaCs have been shown to be ligand-gated channels, it remains to be determined whether the channels encoded by D. melanogaster ppk-family genes are similarly gated upon ligand binding.…”

Chemicals and chemoreceptors: ecologically relevant signals driving behavior in Drosophila

“…Liu et al, 2003aLiu et al, ,b, 2012Lu et al, 2012;Starostina et al, 2012;Thistle et al, 2012;Toda et al, 2012;Zelle et al, 2013;Guo et al, 2014;Mast et al, 2014;Vijayan et al, 2014 Larval terminal organ…”

“…In addition, at least three members of the TRP channels, TRP1, Painless, and TRPL are expressed in bitter neurons in the labellum where they are involved in detection of aversive compounds (Al-Anzi et al, 2006;Kim et al, 2010;Zhang et al, 2013b). Also, several ppk channels are expressed in taste neurons where they are required for relevant taste modalities such as low-salt detection (Liu et al, 2003b) and intraspecific chemical communication in larvae (Mast et al, 2014), and water perception (Cameron et al, 2010) and chemical communication during courtship in adults Lu et al, 2012;Starostina et al, 2012;Thistle et al, 2012;Toda et al, 2012;Vijayan et al, 2014). Finally, DmXR, a receptor homologous to metabotropic glutamate receptors that has lost the ability to bind glutamate (Mitri et al, 2004), may also act as a taste receptor.…”

The role of cVA and the Odorant binding protein Lush in social and sexual behavior in Drosophila melanogaster

“…The female-specific 7,11-HD pheromone, which is important for species-recognition, seems to be detected by gustatory neurons on the legs. Gustatory neurons expressing the ion-channels pickpocket-23 and −25 (ppk-23 and −25) respond physiologically to this pheromone (Starostina et al, 2012;Thistle et al, 2012;Toda et al, 2012). However, the role of ppk is not yet known: it may act as CH receptors or as effectors downstream of receptors for 7,11-HD and other CHs.…”