SRD‐1 in AWA neurons is the receptor for female volatile sex pheromones in C. elegans males

Abstract

Pheromones are critical cues for attracting mating partners for successful reproduction. Sexually mature Caenorhabditis remanei virgin females and self‐sperm‐depleted Caenorhabditis elegans hermaphrodites produce volatile sex pheromones to attract adult males of both species from afar. The chemoresponsive receptor in males has remained unknown. Here, we show that the male chemotactic behavior requires amphid sensory neurons (AWA neurons) and the G‐protein‐coupled receptor SRD‐1. SRD‐1 expression in AWA neurons is sexually dimorphic, with the levels being high in males but undetectable in hermaphrodites. Notably, srd‐1 mutant males lack the chemotactic response and pheromone‐induced excitation of AWA neurons, both of which can be restored in males and hermaphrodites by AWA‐specific srd‐1 expression, and ectopic expression of srd‐1 in AWB neurons in srd‐1 mutants results in a repulsive behavioral response in both sexes. Furthermore, we show that the C‐terminal region of SRD‐1 confers species‐specific differences in the ability to perceive sex pheromones between C. elegans and C. remanei. These findings offer an excellent model for dissecting how a single G‐protein‐coupled receptor expressed in a dimorphic neural system contributes to sex‐specific behaviors in animals.

RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans

“…The nlp-2-expressing AWA neurons have ciliated sensory endings and are known to display pulsatile calcium transients, which are elicited by action potential bursts 88,89 . AWA neurons display sex-specific pheromone responses 90 and may share some functional similarity to chordate GnRH neurons that arise from the olfactory placode 91,92 and are also presumed to regulate non-reproductive functions in larval stages 93,94 . Our expression data suggest that NLP-2 neuropeptides from AWA neurons may act on GNRR-3 and GNRR-6 in neurons of the motor circuit to mediate wakefulness.…”

Genetic and functional diversification of chemosensory pathway receptors in mosquito-borne filarial nematodes

“…Historically, it has been difficult to identify endogenous ligands for nematode chemoreceptors. In C. elegans , only a small fraction of chemoreceptors have been linked to activating molecules, some of which are not likely to be the natural ligand (46,(69)(70)(71)(72)(73)(74)(75)(76)(77) . This is partly a function of the large number of chemoreceptors (> 1,400) and the large space of potentially relevant terrestrial cues in free-living clade V nematodes.…”

Defects in mating behavior and tail morphology are the primary cause of sterility in C. elegans males at high temperature

“…The other aspect of the male response to hermaphrodites is their ability to find the hermaphrodite. Male attraction to hermaphrodites is mediated through neural input from head neurons responding to mating pheromones, including several amphid neurons and the male-specific cephalic neurons (Narayan et al, 2016;Srinivasan et al, 2008;Wan et al, 2019;White et al, 2007). The AWA neurons are one of the primary amphid neuron pairs that function in the perception of mating pheromones (Wan et al, 2019).…”

“…The initial steps of mating require males to successfully find a hermaphrodite and subsequently locate the hermaphrodite vulva. Sensory neurons in the head allow males to find hermaphrodites in response to mating hormones (Narayan et al, 2016;Srinivasan et al, 2008;Wan et al, 2019;White et al, 2007). This is followed by signals through the nine pairs of sensory rays found in male-specific tail structures, which are necessary for maintaining contact with the hermaphrodite and finding the vulva (Garcia et al, 2001;Koo et al, 2011;Liu and Sternberg, 1995;Liu et al, 2011).…”