Drosophila Pheromone-Sensing Neurons Expressing the ppk25 Ion Channel Subunit Stimulate Male Courtship and Female Receptivity

Abstract

As in many species, gustatory pheromones regulate the mating behavior of Drosophila. Recently, several ppk genes, encoding ion channel subunits of the DEG/ENaC family, have been implicated in this process, leading to the identification of gustatory neurons that detect specific pheromones. In a subset of taste hairs on the legs of Drosophila, there are two ppk23-expressing, pheromone-sensing neurons with complementary response profiles; one neuron detects female pheromones that stimulate male courtship, the other detects male pheromones that inhibit male-male courtship. In contrast to ppk23, ppk25, is only expressed in a single gustatory neuron per taste hair, and males with impaired ppk25 function court females at reduced rates but do not display abnormal courtship of other males. These findings raised the possibility that ppk25 expression defines a subset of pheromone-sensing neurons. Here we show that ppk25 is expressed and functions in neurons that detect female-specific pheromones and mediates their stimulatory effect on male courtship. Furthermore, the role of ppk25 and ppk25-expressing neurons is not restricted to responses to female-specific pheromones. ppk25 is also required in the same subset of neurons for stimulation of male courtship by young males, males of the Tai2 strain, and by synthetic 7-pentacosene (7-P), a hydrocarbon normally found at low levels in both males and females. Finally, we unexpectedly find that, in females, ppk25 and ppk25-expressing cells regulate receptivity to mating. In the absence of the third antennal segment, which has both olfactory and auditory functions, mutations in ppk25 or silencing of ppk25-expressing neurons block female receptivity to males. Together these results indicate that ppk25 identifies a functionally specialized subset of pheromone-sensing neurons. While ppk25 neurons are required for the responses to multiple pheromones, in both males and females these neurons are specifically involved in stimulating courtship and mating.

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.…”

“…Leg Aphrodisiac for intraspecific males, female receptivity promotion Liu et al, 2012;Lu et al, 2012;Thistle et al, 2012;Toda et al, 2012;Vijayan et al, 2014 IR52c-IR52d…”

“…These chemical cues are principally sexual pheromones (Gomez-Diaz and Benton, 2013) although recently it has been demonstrated that food-derived odors can modulate courtship as well . Members of ppk Lu et al, 2012;Thistle et al, 2012;Toda et al, 2012;Vijayan et al, 2014), OR (Kurtovic et al, 2007;Van der Goes van Naters and Carlson, 2007;Wang et al, 2011), IR (Koh et al, 2014), and GR (Bray and Amrein, 2003;Miyamoto and Amrein, 2008;Moon et al, 2009;Koganezawa et al, 2010) receptor families have been identified or proposed as sexual pheromones receptors; plus, IR84 is involved in the foododor-mediated modulation of courtship . In the last few years important advances have been made on the field of chemoreception in sexual behavior, hence in the next section we will present an updated view of the relevance of specific pheromone and food odor receptors involved in courtship.…”

“…These 3 channels are expressed in Fru + gustatory neurons of both sexes although males have around double the amount of ppk + cells in the leg compared to females Lu et al, 2012;Vijayan et al, 2014) (Figure 2A). Different subpopulations of ppk23 + -FruM + neurons in the leg respond to male and female pheromones, and both ppk23 and ppk29 are required for the pheromone-evoked effects on courtship (Lu et al, 2012;Thistle et al, 2012;Toda et al, 2012).…”