An atlas of Caenorhabditis elegans chemoreceptor expression

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.
Author summary Maps of gene expression patterns in nervous systems provide an important resource for neuron classification, for functional analysis, and for developmental studies that ask how different neurons acquire their unique identities. By analyzing transgenic GFP reporter strains, we describe here the expression pattern of 244 putative chemosensory receptor-encoding genes, which constitute the largest gene family in Caenorhabditis elegans. As expected, chemoreceptor expression is enriched in chemosensory neurons. Putative chemoreceptors are also expressed in a wide range of interneurons and motor neurons, as well as non-neuronal cells, suggesting that these receptors may sense internal cues in addition to environmental signals. Each chemoreceptor is expressed sparsely, often in just one neuron type, but each neuron type can express many chemoreceptors. Chemoreceptor expression is remarkably plastic, particularly in the context of the environmentally induced dauer diapause stage. Taken together, this molecular atlas of chemosensory receptors provides an entry point for functional studies and offers a host of markers for studying neuronal patterning and plasticity.