An atlas of Caenorhabditis elegans chemoreceptor expression

Abstract

One goal of modern day neuroscience is the establishment of molecular maps that assign unique features to individual neuron types. Such maps provide important starting points for neuron classification, for functional analysis, and for developmental studies aimed at defining the molecular mechanisms of neuron identity acquisition and neuron identity diversification. In this resource paper, we describe a nervous system-wide map of the potential expression sites of 244 members of the largest gene family in the C. elegans genome, rhodopsin-like (class A) G-protein-coupled receptor (GPCR) chemoreceptors, using classic gfp reporter gene technology. We cover representatives of all sequence families of chemoreceptor GPCRs, some of which were previously entirely uncharacterized. Most reporters are expressed in a very restricted number of cells, often just in single cells. We assign GPCR reporter expression to all but two of the 37 sensory neuron classes of the sex-shared, core nervous system. Some sensory neurons express a very small number of receptors, while others, particularly nociceptive neurons, coexpress several dozen GPCR reporter genes. GPCR reporters are also expressed in a wide range of inter- and motorneurons, as well as non-neuronal cells, suggesting that GPCRs may constitute receptors not just for environmental signals, but also for internal cues. We observe only one notable, frequent association of coexpression patterns, namely in one nociceptive amphid (ASH) and two nociceptive phasmid sensory neurons (PHA, PHB). We identified GPCRs with sexually dimorphic expression and several GPCR reporters that are expressed in a left/right asymmetric manner. We identified a substantial degree of GPCR expression plasticity; particularly in the context of the environmentally-induced dauer diapause stage when one third of all tested GPCRs alter the cellular specificity of their expression within and outside the nervous system. Intriguingly, in a number of cases, the dauer-specific alterations of GPCR reporter expression in specific neuron classes are maintained during postdauer life and in some case new patterns are induced post-dauer, demonstrating that GPCR gene expression may serve as traits of life history. Taken together, our resource provides an entry point for functional studies and also offers a host of molecular markers for studying molecular patterning and plasticity of the nervous system.

Sex‐specific pheromone responses in Caenorhabditis elegans

“…To identify the GPCR involved in volatile sex pheromone perception, Wan et al immunoprecipitated mRNA from AWA to uncover a handful of AWAexpressed GPCRs. In concordance with previous GPCR reporter gene studies [6,7], most appeared to be non-dimorphically expressed but one, SRD-1, the GPCR previously noted to be expressed dimorphically in the ADF neurons [6], showed expression only in male, but not hermaphrodite AWA (Fig 1), thereby providing a mirror image of hermaphroditespecific ODR-10 expression. Chemoattraction assays showed that loss of SRD-1 from AWA impaired male attraction to the hermaphrodite sex pheromone (Fig 1).…”

Selection and gene flow shape niche-associated copy-number variation of pheromone receptor genes

“…Our observation that the srg-37 deletion is enriched in rotting fruits provides evidence that selection can act on CNVs in a niche-specific manner. Although our studies focus on the ascr#5 receptors, approximately 1,300 chemoreceptor genes and 400 pseudogenes are annotated in the reference C. elegans genome 44,45 . By contrast, parasitic nematodes tend to have fewer chemoreceptors 46 , and these species inhabit less heterogeneous niches.…”

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

“…Filarial nematode genomes contain a reduced subset of chemoreceptors when compared to other parasitic and free-living nematodes, including C. elegans and C. briggsae , both of which contain over 1200 chemoreceptors (clade V) ( Figure 1B) (33,37,38) . While it is known that parasitic nematodes contain fewer chemoreceptor genes than C. elegans (40,41) , and indeed often fewer genes in total (42) , our pan-phylum analysis revealed a significant correlation between chemoreceptor gene count and the presence and nature of free-living or environmental stages of each nematode species life cycle ( Figure 1C).…”

“…G protein-coupled receptors (GPCRs) function as chemoreceptors at the amphid cilia, and activation leads to signaling through cyclic nucleotide-gated channels (CNGs) or transient receptor potential channels (TRPs), depending on cell type (27)(28)(29)(30) . Each amphid neuron expresses a diverse array of GPCRs, in contrast to the one-receptor-per-cell model in vertebrates (31)(32)(33) . These pathways have likely evolved to reflect the diversity of nematode life-history traits and environmental cues encountered by different parasite species (12,(17)(18)(19) .…”