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Review
. 2020 Feb 7;223(Pt Suppl 1):jeb208215.
doi: 10.1242/jeb.208215.

Evolution, developmental expression and function of odorant receptors in insects

Hua Yan  1   2 , Shadi Jafari  3   4 , Gregory Pask  5 , Xiaofan Zhou  6 , Danny Reinberg  7 , Claude Desplan  8
Affiliations
Review

Evolution, developmental expression and function of odorant receptors in insects

Hua Yan et al. J Exp Biol. .

Abstract

Animals rely on their chemosensory system to discriminate among a very large number of attractive or repulsive chemical cues in the environment, which is essential to respond with proper action. The olfactory sensory systems in insects share significant similarities with those of vertebrates, although they also exhibit dramatic differences, such as the molecular nature of the odorant receptors (ORs): insect ORs function as heteromeric ion channels with a common Orco subunit, unlike the G-protein-coupled olfactory receptors found in vertebrates. Remarkable progress has recently been made in understanding the evolution, development and function of insect odorant receptor neurons (ORNs). These studies have uncovered the diversity of olfactory sensory systems among insect species, including in eusocial insects that rely extensively on olfactory sensing of pheromones for social communication. However, further studies, notably functional analyses, are needed to improve our understanding of the origins of the Orco-OR system, the mechanisms of ORN fate determination, and the extraordinary diversity of behavioral responses to chemical cues.

Keywords: Ant; Development; Diversity; Drosophila; Evolution; Odorant Receptor; Olfaction; Orco.

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Conflict of interest statement

Competing interestsThe authors declare no competing or financial interests.

Figures

Fig. 1.
Fig. 1.
Evolution of chemosensory receptor genes in arthropods. The evolutionary relationships and divergence times among representative arthropod species are shown on the left; the cladogram is adapted from a recent phylogenomic analysis in insects (Misof et al., 2014). The number of chemosensory receptor genes (Or, odorant receptor; orco, odorant receptor co-receptor; Gr, gustatory receptor; Ir, ionotropic receptor) reported in each species is shown on the right, based on previous work (Armisen et al., 2018; Brand et al., 2018; Carey and Carlson, 2011; Croset et al., 2010; Hill et al., 2002; Howlett et al., 2012; McKenzie and Kronauer, 2018; Missbach et al., 2014; Oxley et al., 2014; Robertson, 2019; Terrapon et al., 2014; Wang et al., 2018; Wanner et al., 2007a; Wanner and Robertson, 2008; Zhou et al., 2015, 2012). Of note, in the water strider Gerris buenoi, 60 Gr genes encode 135 GR proteins via alternative splicing (Armisen et al., 2018).
Fig. 2.
Fig. 2.
Subunit contributions to channel properties of an Orco–OR complex. Heterotetrameric insect odorant receptors consist of two different subunits: (1) the obligate Orco co-receptor (purple), which is functionally conserved across insects and is necessary for OR dendritic localization; and (2) a variable ligand-binding (tuning) OR subunit responsible for odorant sensitivity (green), which affects the probability of pore opening and mediates excitatory or inhibitory responses. Note that Orco can also assemble as a homotetramer and is modulated by phosphorylation. Based on previous structure–function studies (Benton et al., 2006) and the cryo-EM structure of an Orco homomeric channel (Butterwick et al., 2018), Orco–OR complexes probably assemble with a 2:2 subunit stoichiometry; the complex forms a cation-conducting pore, influencing cation permeability. The contributions of each subunit to the overall channel properties are depicted.
Fig. 3.
Fig. 3.
Development of olfactory receptor neurons in Drosophila. (A) Early patterning of the antennal disc in second instar larvae: expression of Engrailed (En), Hedgehog (Hh), Wingless (Wg) and Decapentaplegic (Dpp) divides the antennal disc into different zones. Hh expression in the posterior disc is activated by En. Expression of Dpp and Wg is then initiated by Hh signals in the anterior disc. Epidermal growth factor (EGF) expression is activated where Dpp and Wg gradients meet. (B) The antennal disc in the third instar larvae is composed of seven rings of combinations and gradients of components of a gene regulatory network. Each ring gives rise to different types of sensilla. Later in the 3rd instar larvae, the two inner rings will divide further (dashed lines). Asterisks represent the rings that will continue to express Amos; rings without asterisks will express Atonal in the late third instar larvae. (C) Hedgehog-mediated Patch (Ptc) expression and the transcription factors Atonal (Ato), Amos (Am) and Lozenge (which is expressed in Amos-positive rings) specify sensory organ precursors (SOPs) which are selected at the onset of pupal formation (0 h after puparium formation, APF). (D) SOPs generate olfactory receptor neurons (ORNs) under the control of Notch (N) signaling. ORN classes are further diversified based on Notch signaling levels in each basal cell (pNa and pNb). Blue cells represent the Amos-positive lineage; green cells represent the Atonal-positive lineage. pNa cells are Notch positive, and these cells and their descendants are indicated with a darker outline. Lighter outlines indicate Notch-negative pNb cells and their descendants. The Notch-positive descendants of pNb cells can take alternative fates – usually, they undergo apoptosis, but in a few cases, they become either glia or another neuron.
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