A Pheromone Receptor Mediates 11-cis-Vaccenyl Acetate-Induced Responses inDrosophila

Abstract

Insect pheromones elicit stereotypic behaviors that are critical for survival and reproduction. Defining the relevant molecular mechanisms mediating pheromone signaling is an important step to manipulate pheromone-induced behaviors in pathogenic or agriculturally important pests. The only volatile pheromone identified in Drosophila is 11-cis-vaccenyl acetate (VA), a male-specific lipid that mediates aggregation behavior. VA activates a few dozen olfactory neurons located in T1 sensilla on the antenna of both male and female flies. Here, we identify a neuronal receptor required for VA sensitivity. We identified two mutants lacking functional T1 sensilla and show that the expression of the VA receptor is dramatically reduced or eliminated. Importantly, we show misexpression of this receptor in non-T1 neurons, normally insensitive to VA, confers pheromone sensitivity at physiologic concentrations. Sensitivity of T1 neurons to VA requires LUSH, an extracellular odorant-binding protein (OBP76a) present in the sensillum lymph bathing trichoid olfactory neuron dendrites. Here, we show LUSH are also required in non-T1 neurons misexpressing the receptor to respond to VA. These data provide new insight into the molecular components and neuronal basis of volatile pheromone perception.

SNMP is a signaling component required for pheromone sensitivity in Drosophila

“…The results presented here, together with recent work (2,3,23), indicate that cVA perception in Drosophila requires supplemental factors not required for the detection of general food odorants. General food odorants are thought to activate odorant receptors through direct interactions with receptor proteins.…”

“…CD36 ͉ olfaction ͉ olfactory ͉ sexual behavior ͉ signal transduction C VA (11-cis-vaccenyl acetate) mediates social behaviors in Drosophila, and its reception requires the odorant receptor Or67d and the extracellular pheromone-binding protein LUSH (1)(2)(3)(4). Misexpression of Or67d receptors in trichoid neurons that are normally insensitive to pheromone confers cVA sensitivity but only if LUSH is present (3).…”

“…Misexpression of Or67d receptors in trichoid neurons that are normally insensitive to pheromone confers cVA sensitivity but only if LUSH is present (3). However, Or67d and LUSH are not sufficient to confer cVA sensitivity to basiconic neurons (T.S.H.…”

“…We screened Ϸ3,000 mutagenized third-chromosome lines selected for homozygous viability (5). We screened each mutant line for T1 electrophysiological responses to cVA using single sensillum electrophysiological recordings (2,3,6). We identified five complementation groups that were cVA-insensitive yet retained spontaneous activity in the pheromone-sensing neurons (the vains phenotype) ( Fig.…”

Taste and pheromone perception in the fruit fly Drosophila melanogaster

“…Some odorantbinding proteins are also expressed in taste organs [8,[27][28][29]. In the olfactory system, a mutation in one of these proteins, LUSH, has been shown to affect behavioral responses to cis-vaccenyl acetate, a volatile pheromone involved in aggregation behavior [8,30]. Finally, a member of a new class of membrane proteins, CheB42a, is malebiased expressed in support cells of taste bristles also associated with the only known pheromone receptor, Gr68a, and plays a role in male courtship [31,32].…”