Olfaction and Odor Discrimination Are Mediated by the C. elegans Guanylyl Cyclase ODR-1

Abstract

Animals in complex environments must discriminate between salient and uninformative sensory cues. Caenorhabditis elegans uses one pair of olfactory neurons called AWC to sense many different odorants, yet the animal can distinguish each odorant from the others in discrimination assays. We demonstrate that the transmembrane guanylyl cyclase ODR-1 is essential for responses to all AWC-sensed odorants. ODR-1 appears to be a shared signaling component downstream of odorant receptors. Overexpression of ODR-1 protein indicates that ODR-1 can influence odor discrimination and adaptation as well as olfaction. Adaptation to one odorant, butanone, is disrupted by ODR-1 overexpression. Olfactory discrimination is also disrupted by ODR-1 overexpression, probably by overproduction of the shared second messenger cGMP. We propose that AWC odorant signaling pathways are insulated to permit odor discrimination.

Generation and modulation of chemosensory behaviors in C. elegans

“…In the background of a high constant concentration of one chemical, animals fail to respond to a point source of that chemical, but continue to respond to other chemicals sensed by that neuron type [71]. Similarly, prolonged exposure to one odorant decreases the response to that odorant while sparing responses to other chemicals sensed by that neuron [142,[145][146][147]. These observations indicate that the chemosensory system is able to discriminate among chemicals sensed by one neuron type.…”

“…In the AWC olfactory neurons and in several other neuron types, G proteins may activate guanylyl cyclases, resulting in gating of the TAX-2/4 cGMP-gated channels [20,22,[141][142][143] (Fig. 2a).…”

“…In the case of the L/R asymmetric ASE and AWC neurons, this feat is achieved simply by segregating responsiveness to different chemicals to the left or the right neuron [98,99]. However, for cues sensed by both left and right neurons, one mechanism by which the signal transduction pathways could be insulated is via segregation of individual signaling pathways into signaling microdomains [142,[148][149][150][151]. It is also possible that while the core components of the signal transduction pathways are shared, additional molecules act in an odorant pathwayspecific manner [140], allowing the neuron to discriminate between multiple chemical cues.…”

“…a Molecules acting in the AWC neurons to modulate AWC neuron plasticity are shown in red. ARR-1 encodes an arrestin possibly playing a role in receptor desensitization [154]; overexpression of the ODR-1 receptor guanylyl cyclase alters adaptation to a subset of AWC-sensed odorants [142]; the TBX-2 transcription factor acts cytoplasmically to regulate olfactory adaptation via as yet unknown mechanisms [156]; the EGL-4 cGMP-dependent protein kinase phosphorylates the TAX-2 channel, and also translocates to the nucleus to regulate early and late steps in olfactory adaptation, respectively [145]; Ca 2+ entry through the OSM-9 TRPV channel is required for olfactory adaptation to a subset of AWC-sensed chemicals [146]; the TAX-6 Ca 2+ -dependent calcineurin phosphatase negatively regulates adaptation [155]. b Simplified summary of intercellular mechanisms proposed to mediate chemosensory behavioral plasticity.…”

Behavioral plasticity in C. elegans: Paradigms, circuits, genes

“…Another genetic manipulation that affects olfactory adaptation in an odor-specific manner is overexpression of the receptor-type guanylyl cyclase odr-1/ gcy-10 (L'Etoile and Bargmann, 2000). This activity is independent of the guanylyl-cyclase domain, and presumably occurs via the titration of a protein involved in the adaptation process.…”