Abstract
Various odorants trigger complex animal behaviors across species in both quality- and quantity-dependent manners. However, how the intensity of olfactory input is encoded remains largely unknown. Here we report that isoamyl alcohol (IAA) induces bi-directional currents through a Gα- guanylate cyclase (GC)- cGMP signaling pathway in Caenorhabditis elegans olfactory neuron amphid wing “C” cell (AWC), while two opposite cGMP signaling pathways are responsible for odor-sensing in olfactory neuron amphid wing “B” cell (AWB): (1) a depolarizing Gα (GPA-3)- phosphodiesterase (PDE) – cGMP pathway which can be activated by low concentrations of isoamyl alcohol (IAA), and (2) a hyperpolarizing Gα (ODR-3)- GC- cGMP pathway sensing high concentrations of IAA. Besides, IAA induces Gα (ODR-3)-TRPV(OSM-9)-dependent currents in amphid wing “A” cell (AWA) and amphid neuron “H” cell with single ciliated sensory ending (ASH) neurons with different thresholds. Our results demonstrate that an elaborate combination of multiple signaling machineries encode the intensity of olfactory input, shedding light on understanding the molecular strategies on sensory transduction.
Highlights
Animals sense numerous volatile compounds from environmental cues to locate food sources, avoid predators and pathogens, and communicate with each other (Bargmann, 2006; DeMaria and Ngai, 2010; Wilson, 2013)
We tested the responses of AWCON and AWCOFF to butanone, 2, 3pentanedione, benzaldehyde, and isoamyl alcohol (IAA) using in vivo patch clamp recording (Supplementary Figure 2A)
A high affinity IAA receptor and a low affinity IAA receptor are likely expressed in amphid wing “A” cell (AWA) and ASH neurons, respectively, which are associated with ODR-3
Summary
Animals sense numerous volatile compounds from environmental cues to locate food sources, avoid predators and pathogens, and communicate with each other (Bargmann, 2006; DeMaria and Ngai, 2010; Wilson, 2013). The effects of one given odorant can be influenced by many factors including intensity, context and experience (Bargmann, 2006; Gottfried, 2009; Li and Liberles, 2015; Harris et al, 2019; Duan et al, 2020) It remains poorly understood how intensity of odorant signals are encoded by the olfactory system in higher organisms because of the complexity of their nervous systems. Previous studies have identified a number of genes including GPCRs, Gi/o-like G proteins, cGMP-gated CNG channel (TAX-2/TAX-4), TRP channel (OSM-9) and voltagegated calcium channel (EGL-19) that are involved in odorants detection and olfactory-related behaviors in C. elegans (Brenner, 1974; Bargmann et al, 1993; Bargmann and Kaplan, 1998; Bargmann, 2006; Chalasani et al, 2007; Harris et al, 2014; Ohno et al, 2014; Duan et al, 2020). Electrophysiology and calcium imaging at single neuron resolution, here we systematically identified the molecular strategies by which C. elegans encodes the intensity of odorant stimulus
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