Using their senses of taste and smell, animals recognize a wide variety of chemicals. The nematode C. elegans has only fourteen types of chemosensory neurons, but it responds to dozens of chemicals, because each chemosensory neuron detects several stimuli. Here we describe over 40 highly divergent members of the G protein-coupled receptor family that could contribute to this functional diversity. Most of these candidate receptor genes are in clusters of two to nine similar genes. Eleven of fourteen tested genes appear to be expressed in small subsets of chemosensory neurons. A single type of chemosensory neuron can potentially express at least four different receptor genes. Some of these genes might encode receptors for water-soluble attractants, repellents, and pheromones.
Although cyclic nucleotide-gated channels mediate sensory transduction in olfaction and vision, other forms of sensory transduction are independent of these channels. Caenorhabditis elegans cyclic nucleotide-gated channel mutants respond normally to some olfactory stimuli and to osmotic stimuli, suggesting that these chemosensory responses use an alternative sensory transduction pathway. One gene that may act in this pathway is osm-9, which is required for each of these responses as well as a mechanosensory response to nose touch. osm-9 encodes a protein with ankyrin repeats and multiple predicted transmembrane domains that has limited similarity to the Drosophila phototransduction channels transient receptor potential (TRP) and TRP-like (TRPL). The sequence of OSM-9 and other TRP-like genes reveals a previously unsuspected diversity of mammalian and invertebrate genes in this family. osm-9 is required for the activity of the predicted G-proteincoupled odorant receptor ODR-10, which acts in the AWA olfactory neurons; its similarity to other G-protein-regulated transduction channels suggests that OSM-9 is involved in AWA signaling. osm-9::GFP fusion genes are expressed in a subset of chemosensory, mechanosensory, and osmosensory neurons. osm-9 also affects olfactory adaptation within neurons that require the cyclic nucleotide-gated channel for olfaction; in these neurons, the gene has a regulatory function and not a primary role in sensory transduction.Key words: olfaction; C. elegans; mechanosensation; sensory transduction; signaling pathways; olfactory adaptation; TRP channels Sensory neurons transduce environmental stimuli via the activation of channels that differ by organism and by sensory system. One important class of sensory channels includes cAMP-and cGM P-gated channels. In the vertebrate visual system, photoactivation of the G-protein-coupled receptor rhodopsin results in closure of cGM P-gated channels (Stryer, 1991). Olfactory transduction in vertebrates also begins with the activation of Gprotein-coupled receptors and is mediated by opening of cAM P-gated channels (Reed, 1992). Mice mutant for the olfactory cyclic nucleotide-gated channel fail to generate electrical responses to all tested odorants, although the olfactory neurons are present and have normal passive membrane properties (Brunet et al., 1996). C yclic nucleotide-gated channels have also been implicated in chemosensation in the nematode Caenorhabditis elegans. C. elegans senses a large number of volatile attractants with two pairs of olfactory neurons designated AWA and AWC (Bargmann et al., 1993). AWC olfactory responses may be mediated by a putative cyclic nucleotide-gated channel encoded by the tax-2 and tax-4 genes (Coburn and Bargmann, 1996;Komatsu et al., 1996). The TAX-2/TAX-4 channel also participates in chemotaxis to water-soluble attractants (Dusenbery et al., 1975) and in thermotaxis (Mori and Ohshima, 1995). TAX-2 and TAX-4 gene fusions are expressed in the sensory neurons that mediate these responses.By contrast, sensory tr...
Following prolonged exposure to an odorant, C. elegans exhibits a diminished response to the odorant for several hours. This olfactory adaptation is odorant selective; animals can adapt independently to different odorants sensed by a single pair of olfactory neurons, the AWC neurons. The mechanism of olfactory adaptation is genetically complex, with different genes required for adaptation to different odorants. Animals mutant for the gene adp-1 fail to adapt to a subset of AWC-sensed odorants; adp-1 affects a calcium-dependent process required for adaptation. Mutations in another gene, osm-9, affect adaptation to a different but overlapping subset of AWC-sensed odorants. Mutations in adp-1 and osm-9 do not diminish the ability of unadapted animals to respond to odorants, indicating that odorant sensation and odorant adaptation are distinct processes.
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