Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths

Miura, Nami; Nakagawa, Terunaga; Touhara, Kazushige; Ishikawa, Yukio

doi:10.1016/j.ibmb.2009.12.011

Cited by 82 publications

(107 citation statements)

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“…Amino acid sequences of CpomORs clustering in the candidate PR clade (Bengtsson et al, 2012) were included in a dataset together with sequences of candidate PRs from the following Lepidoptera: Antheraea polyphemus (Forstner et al, 2009), Bombyx mori (Nakagawa et al, 2005), Danaus plexippus (Zhan et al, 2011), Diaphania indica (Mitsuno et al, 2008), Epiphyas postvittana (Jordan et al, 2009), Heliconius melpomene (Heliconius Genome Consortium, 2012), Helicoverpa armigera (Liu et al, 2012), Heliothis virescens (Grosse-Wilde et al, 2007;Wang et al, 2010), Manduca sexta (Grosse-Wilde et al, 2010), Mythimna separata (Mitsuno et al, 2008), Ostrinia furnacalis (Miura et al, 2010;Leary et al, 2012), O. nubilalis (Wanner et al, 2010;Leary et al, 2012), O. scapulalis (Miura et al, 2009(Miura et al, , 2010, Plutella xylostella (Mitsuno et al, 2008;Sun et al, 2013), Spodoptera exigua and S. littoralis (Legeai et al, 2011;Montagné et al, 2012). Sequences from B. mori (BmorOR6) and H. melpomene (HmelOR5, 6, and 7) were also included in the dataset as external groups, since they belong to the sister group to the PR clade (Poivet et al, 2013).…”

Section: Phylogenetic Analysismentioning

confidence: 99%

A predicted sex pheromone receptor of codling moth Cydia pomonella detects the plant volatile pear ester

et al. 2014

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Plant volatiles mediate host discrimination and host finding in phytophagous insects. Understanding how insects recognize these signals is a current challenge in chemical ecology research. Pear ester, ethyl (E,Z )-2,4-decadienoate, is a powerful, bisexual attractant of codling moth Cydia pomonella (Lepidoptera, Tortricidae) and strongly synergizes the male response to female-produced sex pheromone. We show here that the codling moth odorant receptor (OR) CpomOR3 is dedicated to detecting this plant volatile. Heterologous expression of CpomOR3 in Drosophila T1 trichoid and ab3A basiconic sensilla, followed by a screening with codling moth pheromone compounds and known plant volatile attractants, confirms that CpomOR3 binds to pear ester. Although CpomOR3 does not respond to any of the pheromone components tested, a phylogenetic analysis of lepidopteran chemosensory receptor genes reveals a close relationship of CpomOR3 with pheromone receptors (PRs) in moths. This corroborates the interaction of ecological and social chemosensory cues during premating communication. The finding that a plant volatile compound, pear ester, is a specific ligand for a PR-like lepidopteran receptor adds to our understanding of insect-plant interactions and emphasizes the interaction of natural and sexual selection during the phylogenetic divergence of insect herbivores.

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Section: Phylogenetic Analysismentioning

confidence: 99%

A predicted sex pheromone receptor of codling moth Cydia pomonella detects the plant volatile pear ester

et al. 2014

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“…Recent studies have identified genetic loci associated with pheromone production and detection that account for the segregation of closely related moth species or races (9,10). A lineage of conserved odorant receptor (OR) genes expressed in male moth antennae, represent the primary genes responsible for detecting and discriminating female-produced sex pheromones (11)(12)(13)(14). The response profile of the sex pheromone receptors (15), or their expression pattern (16), can directly account for the attractive behavioral response of transgenic male silk moths.…”

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confidence: 99%

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

Leary

Allen

Bunger

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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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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“…In moths, pheromone molecules are detected by specialized antennal ORNs that express particular pheromone receptor genes (4)(5)(6)(7)(8)(9)(10). The axons of ORNs convey pheromone information to the first olfactory center, the antennal lobe (AL; an analog of the vertebrate olfactory bulb).…”

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confidence: 99%

Pheromone responsiveness threshold depends on temporal integration by antennal lobe projection neurons

Tabuchi

Sakurai

Mitsuno

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The olfactory system of male moths has an extreme sensitivity with the capability to detect and recognize conspecific pheromones dispersed and greatly diluted in the air. Just 170 molecules of the silkmoth (Bombyx mori) sex pheromone bombykol are sufficient to induce sexual behavior in the male. However, it is still unclear how the sensitivity of olfactory receptor neurons (ORNs) is relayed through the brain to generate high behavioral responsiveness. Here, we show that ORN activity that is subthreshold in terms of behavior can be amplified to suprathreshold levels by temporal integration in antennal lobe projection neurons (PNs) if occurring within a specific time window. To control ORN inputs with high temporal resolution, channelrhodopsin-2 was genetically introduced into bombykol-responsive ORNs. Temporal integration in PNs was only observed for weak inputs, but not for strong inputs. Pharmacological dissection revealed that GABAergic mechanisms inhibit temporal integration of strong inputs, showing that GABA signaling regulates PN responses in a stimulus-dependent fashion. Our results show that boosting of the PNs' responses by temporal integration of olfactory information occurs specifically near the behavioral threshold, effectively defining the lower bound for behavioral responsiveness.optogenetics | pheromone orientation behavior | transgenic silkmoth | olfaction O lfaction is a key element in many aspects of animal behavior, such as foraging, oviposition, and mate recognition. In many moth species, a special class of odorants called sex pheromones plays a critical role for identification of and orientation to potential mates. Because sex pheromones emitted by females are greatly diluted and dispersed in the air, sophisticated olfactory systems to detect minute amounts of sex pheromones and processing systems to translate subtle peripheral sensory responses into appropriate behavioral responses have evolved in male moths. Theoretical calculations have shown that the detection of 170 molecules of the sex pheromone bombykol [(E,Z)-10,12-hexadecadienol] can trigger sexual behavioral responses in males of the silkmoth Bombyx mori (1). The physical and chemical mechanisms in the antennae, the sensilla, and the olfactory receptor neurons (ORNs) responsible for this remarkably high sensitivity, which can detect even a single molecule, are well understood (2, 3). However, it is unclear how a small number of spikes from a small number of ORNs is processed centrally to allow for high behavioral responsiveness.In moths, pheromone molecules are detected by specialized antennal ORNs that express particular pheromone receptor genes (4-10). The axons of ORNs convey pheromone information to the first olfactory center, the antennal lobe (AL; an analog of the vertebrate olfactory bulb). The AL is composed of a number of glomeruli where ORNs establish connections with two types of neurons: projection neurons (PNs), which relay olfactory information to higher brain regions, and local interneurons (LNs), which are involved ...

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Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths

Cited by 82 publications

References 49 publications

A predicted sex pheromone receptor of codling moth Cydia pomonella detects the plant volatile pear ester

A predicted sex pheromone receptor of codling moth Cydia pomonella detects the plant volatile pear ester

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

Pheromone responsiveness threshold depends on temporal integration by antennal lobe projection neurons

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