A single point mutation causes one-way alteration of pheromone receptor function in two Heliothis species

Cao, Song; Liu, Yang; Wang, Bing; Wang, Guirong

doi:10.1016/j.isci.2021.102981

Cited by 15 publications

(14 citation statements)

References 51 publications

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“…2), which is similar to the 2 Heliothis moths, H. virescens , and H. subflexa (Cao et al. , 2021). The amino acid sequences of OR11 were highly conserved among the 3 species, only slightly lower than the sequences conservation among Orco genes.…”

Section: Resultssupporting

confidence: 55%

Functional characterization of sex pheromone receptors in Spodoptera frugiperda, S. exigua, and S. litura moths

et al. 2022

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Moths possess an extremely sensitive and diverse sex pheromone processing system, in which pheromone receptors (PRs) are essential to ensure communication between mating partners. Functional properties of some PRs are conserved among species, which is important for reproduction. However, functional differentiation has occurred in some homologous PR genes, which may drive species divergence. Here, using genome analysis, 17 PR genes were identified from Spodoptera frugiperda, S. exigua, and S. litura, which belong to 6 homologous groups (odorant receptor [OR]6, 11, 13, 16, 56, and 62); of which 6 PR genes (OR6, OR11, OR13, OR16, OR56, and OR62) were identified in S. frugiperda and S. exigua, and 5 PR genes were identified in S. litura, excluding OR62. Using heterologous expression in Xenopus oocytes, we characterized the functions of PR orthologs including OR6, OR56, and OR62, which have not been clarified in previous studies. OR6 orthologs were specifically tuned to (Z,E)-9,12-tetradecadienyl acetate (Z9,E12-14:OAc), and OR62 orthologs were robustly tuned to Z7-12:OAc in S. frugiperda and S. exigua. The optimal ligand for OR56 was Z7-12:OAc in S. frugiperda, but responses were minimal in S. exigua and S. litura. In addition, SfruOR6 was male antennae-specific, whereas SfruOR56 and SfruOR62 were male antennae-biased. Our study further clarified the functional properties of PRs in 3 Spodoptera moth species, providing a comprehensive understanding of the mechanisms of intraspecific communication and interspecific isolation in Spodoptera.

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Section: Resultssupporting

confidence: 55%

Functional characterization of sex pheromone receptors in Spodoptera frugiperda, S. exigua, and S. litura moths

et al. 2022

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“…Our mutation studies demonstrated that a single amino acid residue substitution in two narrowly tuned ORs from the southern house mosquito can revert their specificity to the oviposition attractants skatole and indole. Amino acid residues leading to one-way alterations of insect ORs have been previously reported ( Auer et al, 2020 ; Cao et al, 2021 ; Hughes et al, 2014 ; Leary et al, 2012 ; Pellegrino et al, 2011 ; Yang et al, 2017 ; Yuvaraj et al, 2021 ). Here, we demonstrated that switching a single amino acid residue in two mosquito ORs reverses the specificity of these receptors to two physiologically and ecologically significant odorants.…”

Section: Discussionmentioning

confidence: 96%

“…Subsequently, the structure for a promiscuous OR from the evolutionarily primitive (Apterygota, wingless) jumping bristletail, Machilis hrabei , MhraOR5, was solved ( DelMarmol et al, 2021 ). Although structures of ORs from winged insects (Pterygota) have not been solved to date, amino acid residues critical for OR specificity have been reported ( Auer et al, 2020 ; Cao et al, 2021 ; Hughes et al, 2014 ; Leary et al, 2012 ; Pellegrino et al, 2011 ; Yang et al, 2017 ; Yuvaraj et al, 2021 ). These studies focused on one-way alteration of specificity but did not examine how an insect detects two odorants with reverse specificity.…”

Section: Introductionmentioning

confidence: 99%

Single amino acid residue mediates reciprocal specificity in two mosquito odorant receptors

Franco

Harris

et al. 2022

eLife

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The southern house mosquito, Culex quinquefasciatus, utilizes two odorant receptors, CquiOR10 and CquiOR2, narrowly tuned to oviposition attractants and well conserved among mosquito species. They detect skatole and indole, respectively, with reciprocal specificity. We swapped the transmembrane (TM) domains of CquiOR10 and CquiOR2 and identified TM2 as a specificity determinant. With additional mutations, we showed that CquiOR10A73L behaved like CquiOR2. Conversely, CquiOR2L74A recapitulated CquiOR10 specificity. Next, we generated structural models of CquiOR10 and CquiOR10A73L using RoseTTAFold and AlphaFold and docked skatole and indole using RosettaLigand. These modeling studies suggested space-filling constraints around A73. Consistent with this hypothesis, CquiOR10 mutants with a bulkier residue (Ile, Val) were insensitive to skatole and indole, whereas CquiOR10A73G retained the specificity to skatole and showed a more robust response than the wildtype receptor CquiOR10. On the other hand, Leu to Gly mutation of the indole receptor CquiOR2 reverted the specificity to skatole. Lastly, CquiOR10A73L, CquiOR2, and CquiOR2L74I were insensitive to 3-ethylindole, whereas CquiOR2L74A and CquiOR2L74G gained activity. Additionally, CquiOR10A73G gave more robust responses to 3-ethylindole than CquiOR10. Thus, we suggest the specificity of these receptors is mediated by a single amino acid substitution, leading to finely tuned volumetric space to accommodate specific oviposition attractants.

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“…Pheromone receptors (PRs) are a subset of Ors responsible for olfactory detection of sex pheromone compounds. In general, the tuning spectrum of PRs is specific [35,36]. For example, BmOr1 and BmOr3 are specifically tuned to bombykol and bombykal, respectively, in Bombyx mori [37,38].…”

Section: Introductionmentioning

confidence: 99%

Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera

Fan

et al. 2022

BMC Biol

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Background Odorant receptors (ORs) as odorant-gated ion channels play a crucial role in insect olfaction. They are formed by a heteromultimeric complex of the odorant receptor co-receptor (Orco) and a ligand-selective Or. Other types of olfactory receptor proteins, such as ionotropic receptors (IRs) and some gustatory receptors (GRs), are also involved in the olfactory system of insects. Orco as an obligatory subunit of ORs is highly conserved, providing an opportunity to systematically evaluate OR-dependent olfactory responses. Results Herein, we successfully established a homozygous mutant (Orco−/−) of Helicoverpa armigera, a notorious crop pest, using the CRISPR/Cas9 gene editing technique. We then compared the olfactory response characteristics of wild type (WT) and Orco−/− adults and larvae. Orco−/− males were infertile, while Orco−/− females were fertile. The lifespan of Orco−/− females was longer than that of WT females. The expressions of most Ors, Irs, and other olfaction-related genes in adult antennae of Orco−/− moths were not obviously affected, but some of them were up- or down-regulated. In addition, there was no change in the neuroanatomical phenotype of Orco−/− moths at the level of the antennal lobe (including the macroglomerular complex region of the male). Using EAG and SSR techniques, we discovered that electrophysiological responses of Orco−/− moths to sex pheromone components and many host plant odorants were absent. The upwind flight behaviors toward sex pheromones of Orco−/− males were severely reduced in a wind tunnel experiment. The oviposition selectivity of Orco−/− females to the host plant (green pepper) has completely disappeared, and the chemotaxis toward green pepper was also lost in Orco−/− larvae. Conclusions Our study indicates that OR-mediated olfaction is essential for pheromone communication, oviposition selection, and larval chemotaxis of H. armigera, suggesting a strategy in which mate searching and host-seeking behaviors of moth pests could be disrupted by inhibiting or silencing Orco expression.

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A single point mutation causes one-way alteration of pheromone receptor function in two Heliothis species

Cited by 15 publications

References 51 publications

Functional characterization of sex pheromone receptors in Spodoptera frugiperda, S. exigua, and S. litura moths

Functional characterization of sex pheromone receptors in Spodoptera frugiperda, S. exigua, and S. litura moths

Single amino acid residue mediates reciprocal specificity in two mosquito odorant receptors

Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera

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