Abstract

The molecular basis of odorant detection and its corollary, the task of the odorant receptor, are fundamental to understanding olfactory coding and sensory ecology. Based on their molecular receptive range, olfactory receptors have been classified as pheromone and non-pheromone receptors, which are respectively activated by a single pheromone component (“specialist”) or by multiple odorant ligands (“generalist”). This functional distinction is unique among ligand-gated ion channels and has shaped how we model olfactory coding both at the peripheral and central levels. Here, we revisit the longstanding combinatorial theory of olfaction and argue, based on physiological, pharmacological, evolutionary and experimental grounds that the task of the odorant receptor is not different from that of neurotransmitter receptors localized in neuronal synapses.

Highlights

  • How insects process odorants is a central question in the field of olfactory neurobiology

  • They support an idea that both Odorant Receptors (ORs) and neurotransmitter receptors (NRs) are specialized in the detection of evolutionary meaningful chemical cues and their distinction may remain based on their ecological context rather than on their pharmacological properties

  • We have provided evidence that (i) narrow tuning is not the exclusive attribute of pheromone receptors (PRs), (ii) green leaf volatiles (GLVs) and other non-pheromonal volatile organic compounds (VOCs) activate non-pheromone receptors (nPRs), (iii) ORs are subjected to powerful selective pressures, and (iv) high concentrations of odorant stimuli cause broad non-specific OR responses

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Summary

Introduction

How insects process odorants is a central question in the field of olfactory neurobiology. Most recent studies report that GLVs (Dudareva et al, 2006; Knudsen et al, 2006) and VOCs number just below 2000 chemicals (Penn et al, 2007; Phillips et al, 2013; de Lacy Costello et al, 2014) (Figure 1A), which is likely an underestimate. Functional ORs are heteromeric complexes composed of an odorant-sensing unit belonging to a large and diverse family and a conserved OR co-receptor named ORco (for review, see Suh et al, 2014). These OR complexes are localized in the dendrites of olfactory receptor neurons (ORNs) embedded in sensilla, which project from the insect cuticular surface on olfactory appendages

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