Three Host Plant Volatiles, Hexanal, Lauric Acid, and Tetradecane, are Detected by an Antenna-Biased Expressed Odorant Receptor 27 in the Dark Black Chafer <i>Holotrichia parallela</i>

Wang, Xiao; Wang, Shang; Yi, Jiankun; Li, Yunshuo; Liu, Jianan; Wang, Jun; Xi, Jinghui

doi:10.1021/acs.jafc.0c00333

Cited by 41 publications

(49 citation statements)

References 44 publications

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“…Functional characterization of insect ORs has been biased towards moths [34][35][36], flies, and mosquitos [37,38]. In contrast, Coleoptera-arguably the largest order of the Metazoa-remains an understudied group with only five characterized ORs from a few species: the cerambycid Megacyllene caryae [39], the scarab Holotrichia parallela [40], and the curculionid Rhynchophorus ferrugineus [41]. The paucity of functional data is a bottleneck that severely limits our understanding of the molecular evolution of olfaction in this diverse taxon [42].…”

Section: Introductionmentioning

confidence: 99%

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

et al. 2021

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Background Bark beetles are major pests of conifer forests, and their behavior is primarily mediated via olfaction. Targeting the odorant receptors (ORs) may thus provide avenues towards improved pest control. Such an approach requires information on the function of ORs and their interactions with ligands, which is also essential for understanding the functional evolution of these receptors. Hence, we aimed to identify a high-quality complement of ORs from the destructive spruce bark beetle Ips typographus (Coleoptera, Curculionidae, Scolytinae) and analyze their antennal expression and phylogenetic relationships with ORs from other beetles. Using 68 biologically relevant test compounds, we next aimed to functionally characterize ecologically important ORs, using two systems for heterologous expression. Our final aim was to gain insight into the ligand-OR interaction of the functionally characterized ORs, using a combination of computational and experimental methods. Results We annotated 73 ORs from an antennal transcriptome of I. typographus and report the functional characterization of two ORs (ItypOR46 and ItypOR49), which are responsive to single enantiomers of the common bark beetle pheromone compounds ipsenol and ipsdienol, respectively. Their responses and antennal expression correlate with the specificities, localizations, and/or abundances of olfactory sensory neurons detecting these enantiomers. We use homology modeling and molecular docking to predict their binding sites. Our models reveal a likely binding cleft lined with residues that previously have been shown to affect the responses of insect ORs. Within this cleft, the active ligands are predicted to specifically interact with residues Tyr84 and Thr205 in ItypOR46. The suggested importance of these residues in the activation by ipsenol is experimentally supported through site-directed mutagenesis and functional testing, and hydrogen bonding appears key in pheromone binding. Conclusions The emerging insight into ligand binding in the two characterized ItypORs has a general importance for our understanding of the molecular and functional evolution of the insect OR gene family. Due to the ecological importance of the characterized receptors and widespread use of ipsenol and ipsdienol in bark beetle chemical communication, these ORs should be evaluated for their potential use in pest control and biosensors to detect bark beetle infestations.

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Section: Introductionmentioning

confidence: 99%

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

et al. 2021

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“…The electrophysiological and behavioral activities of these compounds have been reported in earlier studies. Hexanal from maize was electrophysiologically active in antennae of H. parallela female adults [18]. Among the 10 compounds isolated from H. parallela host plants [(Z)-3-hexen-1-ol, (E)-2-hexen-1-ol, (Z)-3-hexenyl acetate, (E)-2-hexenyl acetate, (R)-(+)-limonene, α-phellandrene, α-pinene, (Z)-β-ocimene, methyl benzoate, and benzaldehyde], (E)-2-hexenyl acetate, and (Z)-3-hexenyl acetate were found to elicit the strongest EAG responses in both female and male H. parallela [2].…”

Section: Discussionmentioning

confidence: 97%

Electrophysiological and Behavioral Responses of Holotrichia parallela to Volatiles from Peanut

Zhang

Cui

Xie

et al. 2021

Insects

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Holotrichia parallela (Coleoptera: Scarabaeidae: Melolonthinae) is a notorious pest of many crops, especially peanuts. In this study, volatiles from peanut plants were analyzed using both gas chromatographic-electroantennographic detection (GC-EAD) and gas chromatography/mass spectrometry (GC/MS) techniques, and tested for adult attraction with field trapping bioassays in Hebei Province, China. GC-EAD analyses indicated that H. parallela antennae strongly responded to twelve GC peaks, including eight identified compounds, (Z)-β-ocimene, hexanal, 6-methyl-5-hepten-2-one, nonanal, dihydromyrcenol, linalool, β-caryophyllene, methyl salicylate, and four unidentified compounds. When tested individually in field conditions from 24 to 31 July, 2020, β-caryophyllene and hexanal significantly attracted both sexes of H. parallela, whereas all other compounds were unattractive. A blend of β-caryophyllene and hexanal at a ratio of 2:1, close to the natural ratio of these two compounds from the intact peanut plant, was most attractive to the beetles. The remaining identified compounds, (Z)-β-ocimene, 6-methyl-5-hepten-2-one, nonanal, dihydromyrcenol, linalool, and methyl salicylate had no synergistic effects on H. parallela attraction when tested in combination with the blend of β-caryophyllene and hexanal. These results demonstrated that β-caryophyllene and hexanal in the volatiles from peanut plants have strong attraction to H. parallela. These two compounds have the potential to be used for monitoring H. parallela and its management programs.

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“…Functionally characterized odorant receptors from the beetles Megacyllene caryae (Gahan. ), Ips typographus L. and Rhyncophorus ferrugineus (Olivier) were included [66][67][68][69] as well as gustatory receptors from D. melanogaster [13]. Similarly, sequences of functionally characterized odorant-and pheromone-binding proteins were considered from beetles, i.e., Anomala cuprea (Hope) and Anomala octiescostata Burmeister [70], Agrilus mali Matsumura [71], Cyrtotrachelus buqueti Guérin-Méneville [72], Holotrichia oblita Faldermannor [73,74], Holotrichia parallela (Motschulsky) [75], Phyllopertha diversa Waterhouse [76], Popillia japonica Newman [77], R. ferrugineus [78], and from the aphid Acyrthosiphon pisum (Harris) [79].…”

Section: Identification Of Chemosensory Genes and Phylogenetic Analysesmentioning

confidence: 99%

Antennal transcriptome analysis and identification of candidate chemosensory genes of the harlequin ladybird beetle,Harmonia axyridis(Pallas) (Coleoptera: Coccinellidae)

Rondoni

Roman

Meslin

et al. 2021

Preprint

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In predatory ladybirds (Coleoptera: Coccinellidae), antennae are important for chemosensory reception used during food and mate location, and for finding a suitable oviposition habitat. Based on NextSeq 550 Illumina sequencing, we assembled the antennal transcriptome of mated Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) males and females and described the first chemosensory gene repertoire expressed in this species. We annotated candidate chemosensory sequences encoding 26 odorant receptors (including the coreceptor, Orco), 17 gustatory receptors, 27 ionotropic receptors, 31 odorant-binding proteins, 12 chemosensory proteins and 4 sensory neuron membrane proteins. Maximum-likelihood phylogenetic analyses allowed to assign can-didate H. axyridis chemosensory genes to previously described groups in each of these families. Differential expression analysis between males and females revealed low variability between sexes, possibly reflecting the known absence of relevant sexual dimorphism in the structure of the antennae and in the distribution and abundance of the sensilla. However, we revealed significant differences in expression of three chemosensory genes, namely 2 male-biased odorant-binding proteins and 1 male-biased odorant receptor, suggesting their possible involvement in pheromone detection. Our data pave the way for improving the understanding of the molecular basis of chemosensory reception in Coccinellidae.

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Three Host Plant Volatiles, Hexanal, Lauric Acid, and Tetradecane, are Detected by an Antenna-Biased Expressed Odorant Receptor 27 in the Dark Black Chafer Holotrichia parallela

Cited by 41 publications

References 44 publications

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

Electrophysiological and Behavioral Responses of Holotrichia parallela to Volatiles from Peanut

Antennal transcriptome analysis and identification of candidate chemosensory genes of the harlequin ladybird beetle,Harmonia axyridis(Pallas) (Coleoptera: Coccinellidae)

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