Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species

Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59717, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 08/2012; 109(35):14081-6. DOI: 10.1073/pnas.1204661109
Source: PubMed


Sex pheromone communication, acting as a prezygotic barrier to mating, is believed to have contributed to the speciation of moths and butterflies in the order Lepidoptera. Five decades after the discovery of the first moth sex pheromone, little is known about the molecular mechanisms that underlie the evolution of pheromone communication between closely related species. Although Asian and European corn borers (ACB and ECB) can be interbred in the laboratory, they are behaviorally isolated from mating naturally by their responses to subtly different sex pheromone isomers, (E)-12- and (Z)-12-tetradecenyl acetate and (E)-11- and (Z)-11-tetradecenyl acetate (ACB: E12, Z12; ECB; E11, Z11). Male moth olfactory systems respond specifically to the pheromone blend produced by their conspecific females. In vitro, ECB(Z) odorant receptor 3 (OR3), a sex pheromone receptor expressed in male antennae, responds strongly to E11 but also generally to the Z11, E12, and Z12 pheromones. In contrast, we show that ACB OR3, a gene that has been subjected to positive selection (ω = 2.9), responds preferentially to the ACB E12 and Z12 pheromones. In Ostrinia species the amino acid residue corresponding to position 148 in transmembrane domain 3 of OR3 is alanine (A), except for ACB OR3 that has a threonine (T) in this position. Mutation of this residue from A to T alters the pheromone recognition pattern by selectively reducing the E11 response ∼14-fold. These results suggest that discrete mutations that narrow the specificity of more broadly responsive sex pheromone receptors may provide a mechanism that contributes to speciation.

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    • "When the male moths detect the pheromone, they fly to the pheromonereleasing females and land near one of them to initiate a series of courtship behaviors (Nakano et al., 2006). The repertoire of genes involved in chemoreception in this species has been identified (Yang et al., 2015), including nine pheromone receptors (Miura et al., 2009, 2010; Wanner et al., 2010; Leary et al., 2012). Among them, the odorant receptor co-receptor, OfurOrco, is considered to serve as a common subunit of odorant receptor complex receptors involved in the recognition of a wide range of odorants (Vosshall et al., 1999; Larsson et al., 2004; Xia and Zwiebel, 2006; Stengl, 2010). "
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    ABSTRACT: Genome editing using transcription activator-like effector nuclease (TALEN) has been applied for various model organisms but not yet for agricultural pest insects. In this study, TALEN-mediated mutagenesis of the gene encoding odorant receptor co-receptor (Orco) of an important agricultural pest Ostrinia furnacalis (OfurOrco) was carried out. Of the two pairs of TALEN constructs designed, one generated somatic and germline mutations at rates of 70.8% and 20.8%, respectively. Physiological and behavioral analyses using a gas chromatograph-electroantennographic detector system and a wind tunnel, respectively, revealed that antennal responses to sex pheromone components were decreased to trace levels, and behavioral responses were abolished in OfurOrco mutants. This study demonstrated that TALEN-mediated mutagenesis is applicable to pest insects, and these results will open the way for a better understanding of chemosensory systems in wild insects.
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    • "Behavioral flight tunnel studies confirmed that there are 'rare' ECB and ACB males that can exhibit upwind oriented flight to both the ACB and ECB pheromones (Linn et al. 2003, 2007). Studies of the pheromone odorant receptors (ORs) in Ostrinia confirmed the presence of ORs capable of responding to both the ECB and ACB pheromone components in vitro (Leary et al. 2012; Miura et al. 2010; Wanner et al. 2010). The response profiles of the ORs corresponded well to the published electrophysiological responses of olfactory sensory neurons (OSNs) in vivo (Domingue et al. 2007a, b, 2008, 2010). "
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    • "ODEs from different families have been described, among which esterases (Ishida and Leal, 2005), cytochrome P450 (Maïbeche-Coisn e et al., 2004) and glutathione- S-transferase (GST) (Rogers et al., 1999). Changes in olfactory sensitivity can be driven by subtle mutations in key genes from these families (Leary et al., 2012;McBride et al., 2014), gene gains and losses (Gardiner et al., 2008;Guo and Kim, 2007;Vieira and Rozas, 2011), and/or variation in gene expression (Biessmann et al., 2005;Fox et al., 2001;McBride et al., 2014;Rinker et al., 2013). In this study, we investigated if local adaptation could be associated with transcriptional changes in the chemosensory organs. "
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