Molecular mechanisms of olfactory detection in insects: beyond receptors

Abstract

Insects thrive in diverse ecological niches in large part because of their highly sophisticated olfactory systems. Over the last two decades, a major focus in the study of insect olfaction has been on the role of olfactory receptors in mediating neuronal responses to environmental chemicals. In vivo , these receptors operate in specialized structures, called sensilla, which comprise neurons and non-neuronal support cells, extracellular lymph fluid and a precisely shaped cuticle. While sensilla are inherent to odour sensing in insects, we are only just beginning to understand their construction and function. Here, we review recent work that illuminates how odour-evoked neuronal activity is impacted by sensillar morphology, lymph fluid biochemistry, accessory signalling molecules in neurons and the physiological crosstalk between sensillar cells. These advances reveal multi-layered molecular and cellular mechanisms that determine the selectivity, sensitivity and dynamic modulation of odour-evoked responses in insects.

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“…It is found useful in providing insights into the relationship between OSN anatomy and olfactory physiology [ 83 , 84 ]. A recent review of these new molecular tools and mechanisms of olfactory detection in insects has been published [ 85 ].…”

Transduction and Adaptation Mechanisms in the Cilium or Microvilli of Photoreceptors and Olfactory Receptors From Insects to Humans

“…The invertebrate phototransduction cascade has also been reviewed extensively (Hardie, 2012 ; Montell, 2012 ; Hardie and Juusola, 2015 ), while olfactory transduction is still under active investigation (Touhara and Vosshall, 2009 ; Schmidt and Benton, 2020 ). In this review we will focus on Drosophila olfactory and visual transduction for simplicity, however several studies have identified many differences between invertebrate species including different receptors and transduction signaling mechanisms (for recent reviews, see Honkanen et al, 2017 ; Schmidt and Benton, 2020 ). The main steps of the transduction are shown in Figures 4 , 5 , and described below, with the main components listed in Table 1 for comparison.…”

“…Invertebrate olfactory transduction appears to use a diverse set of pathways across species, within a single species, and even within a single OSN (for a recent review, see Schmidt and Benton, 2020 ). The receptors can be divided into two different classes; (1) seven transmembrane domain odorant receptors (ORs) (Clyne et al, 1999 ) and (2) three transmembrane domain ionotropic receptors (IRs, see Table 1 ; Benton et al, 2009 ).…”

“…Phototransduction and olfaction have been widely investigated in both invertebrate (Hardie and Raghu, 2001 ; Touhara and Vosshall, 2009 ; Yau and Hardie, 2009 ; Hardie and Juusola, 2015 ; Honkanen et al, 2017 ; Fleischer et al, 2018 ; Schmidt and Benton, 2020 ) and vertebrate (Schild and Restrepo, 1998 ; Burns and Baylor, 2001 ; Fain et al, 2001 ; Arshavsky et al, 2002 ; Luo et al, 2008 ; Kaupp, 2010 ; Pifferi et al, 2010 ; Vinberg et al, 2018 ) species. Signal transduction in vertebrate olfactory sensory neurons (OSNs) and photoreceptors (PRs) both rely upon G protein signaling cascades, while using distinct classes of G and effector proteins: A G-protein-coupled receptor (GPCR) detects a stimulus and modulates the open probability of cyclic nucleotide-gated (CNG) ion channels via classical GPCR signaling cascades involving the activation of an effector enzyme (E), adenylyl cyclase (AC) in the OSN and phosphodiesterase (PDE) in photoreceptors.…”

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“…pheromone) to the environment that provokes a physiological and/or behavioral reaction in the receiver 11 . So far, most research on chemical communication has been done in insects, for which the chemical nature of specific molecules and their mechanism of action is known to some extent 12 , 13 . Although many vertebrates are adept at detecting odoriferous stimuli, much less research has been done in this group compared to insects 13 .…”