Evolution of two receptors detecting the same pheromone compound in crop pest moths of the genus Spodoptera

Abstract

In moths, mate finding strongly rely on the detection of sex pheromones by pheromone receptors (PRs). Any modification in the functional properties of these receptors can have a drastic impact on reproduction. In the course of characterizing candidate PRs in the noctuid moth Spodoptera littoralis, we expressed them in Drosophila olfactory sensory neurons and stimulated them with a large panel of moth pheromone compounds. We found that two PRs detect (Z,E)-9,12-14:OAc, a minor component of the female pheromone blend. Whereas SlitOR6 is highly specific to this component, SlitOR13 is less sensitive and not strictly specific as it also detects (Z)9-14:OAc, another minor component of the sex pheromone. Interestingly, SlitOR13 expression is restricted to the distal part of male antennae, where we could identify a novel functional class of pheromone-sensitive neurons whose response spectrum matches that of SlitOR13. Based on a phylogenetic analysis of Lepidoptera PRs, we found that the ability to bind (Z,E)-9,12-14:OAc appeared independently within three paralogous lineages, and an analysis of selective pressures revealed sites under positive selection that could have played a role in the emergence of functional properties of OR6 and OR13 in Spodoptera species.

Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire

“…3), despite the fact that the sets of SlitORs and S. littoralis OSNs compared here were partial. Furthermore, the response spectra of two sex pheromone receptors characterized here (SlitOR6 and SlitOR13) were previously shown to correlate with S. littoralis male OSNs29. Other deorphanized SlitORs may correspond to yet uncharacterized OSNs or, alternatively, OSN response profiles may lack ligands included in the present panel.…”

Functional Characterization of Sex Pheromone Receptors in the Fall Armyworm (Spodoptera frugiperda)

“…Very recently, we showed that sympatric S. exigua and S. litura can both perceive specific components, reinforcing behavioral isolation between the two species [68]. To analyze the correlation between PR amino acid sequence identity and the ligand specificity, we summarized the results of previous studies from these four Spodoptera species [18,19,69], and a clear correlation was shown ( Figure 6). For example, four OR13 homologs, sharing 93.15% identity, all have a strong response to Z9-14:OAc and Z9,E12-14:OAc.…”

“…Whether PBPs or SNMPs are required for the function of these candidate PRs needs to be further explored. (Figures 4 and 5), S. exigua [18], S. littoralis [15,69], and S. litura [19]). The dots represent the responses obtained by the Xenopus oocytes system, and the stars represent responses by in vivo heterologous expression in Drosophila OSNs.…”

Proceeding From in vivo Functions of Pheromone Receptors: Peripheral-Coding Perception of Pheromones From Three Closely Related Species, Helicoverpa armigera, H. assulta, and Heliothis virescens

“…In addition to Noctuidae species, seven PRs (OR1, 3, 4, 5, 6, 7, 9) were identified and characterized in Bombyx mori , belonging to Bombycidae (Nakagawa et al, 2005; Wanner et al, 2007; Wang et al, 2010, 2016; Liu et al, 2012; Montagné et al, 2012; Liu et al, 2013a,b; Jiang et al, 2014; de Fouchier et al, 2015; Zhang et al, 2015a,b; Chang et al, 2016) ( Figure 1A and Supplementary Table S1 ).…”