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

EMBO Rep. 2019 Mar;20(3):e46288. doi: 10.15252/embr.201846288. Epub 2019 Feb 21.

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.

Keywords: AWA neuron; SRD‐1 chemoreceptor; nematode volatile sex pheromone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / metabolism*
  • Calcium / metabolism
  • Female
  • Gene Expression Regulation
  • Male
  • Receptors, Cell Surface / chemistry
  • Receptors, Cell Surface / metabolism*
  • Receptors, G-Protein-Coupled / chemistry
  • Receptors, G-Protein-Coupled / metabolism*
  • Sensory Receptor Cells / metabolism*
  • Sex Attractants / metabolism*
  • Sex Characteristics
  • Signal Transduction
  • Species Specificity
  • Volatilization

Substances

  • Caenorhabditis elegans Proteins
  • Receptors, Cell Surface
  • Receptors, G-Protein-Coupled
  • SRD-1 protein, C elegans
  • Sex Attractants
  • Calcium