Eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum types
Abstract Background Insects detect odours using odorant receptors (ORs) expressed in olfactory sensory neurons (OSNs) in the antennae. Ecologically important odours are often detected by selective and abundant OSNs; hence, ORs with high antennal expression. However, little is known about the functio...
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2024-11-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-024-02066-x |
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| author | Jothi Kumar Yuvaraj Dineshkumar Kandasamy Rebecca E. Roberts Bill S. Hansson Jonathan Gershenzon Martin N. Andersson |
| author_facet | Jothi Kumar Yuvaraj Dineshkumar Kandasamy Rebecca E. Roberts Bill S. Hansson Jonathan Gershenzon Martin N. Andersson |
| author_sort | Jothi Kumar Yuvaraj |
| collection | DOAJ |
| description | Abstract Background Insects detect odours using odorant receptors (ORs) expressed in olfactory sensory neurons (OSNs) in the antennae. Ecologically important odours are often detected by selective and abundant OSNs; hence, ORs with high antennal expression. However, little is known about the function of highly expressed ORs in beetles, since few ORs have been functionally characterized. Here, we functionally characterized the most highly expressed OR (ItypOR36) in the bark beetle Ips typographus L. (Coleoptera, Curculionidae, Scolytinae), a major pest of spruce. We hypothesized that this OR would detect a compound important to beetle fitness, such as a pheromone component. We next investigated the antennal distribution of this OR using single sensillum recordings (SSR) and in situ hybridization, followed by field- and laboratory experiments to evaluate the behavioural effects of the discovered ligand. Results We expressed ItypOR36 in HEK293 cells and challenged it with 64 ecologically relevant odours. The OR responded exclusively to the monoterpene-derived ketone lanierone with high sensitivity. Lanierone is used in chemical communication in North American Ips species, but it has never been shown to be produced by I. typographus, nor has it been studied in relation to this species’ sensory physiology. Single sensillum recordings revealed a novel and abundant lanierone-responsive OSN class with the same specific response as ItypOR36. Strikingly, these OSNs were co-localized in sensilla together with seven different previously described OSN classes. Field experiments revealed that low release rates of lanierone inhibited beetle attraction to traps baited with aggregation pheromone, with strongest effects on males. Female beetles were attracted to lanierone in laboratory walking bioassays. Conclusions Our study highlights the importance of the so-called ‘reverse chemical ecology’ approach to identify novel semiochemicals for ecologically important insect species. Our discovery of the co-localization pattern involving the lanierone OSN class suggests organizational differences in the peripheral olfactory sense between insect orders. Our behavioural experiments show that lanierone elicits different responses in the two sexes, which also depend on whether beetles are walking in the laboratory or flying in the field. Unravelling the source of lanierone in the natural environment of I. typographus is required to understand these context-dependent behaviours. |
| format | Article |
| id | doaj-art-7beba0c3a05644f9b0c6a6501bdac7ba |
| institution | Kabale University |
| issn | 1741-7007 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
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| series | BMC Biology |
| spelling | doaj-art-7beba0c3a05644f9b0c6a6501bdac7ba2024-11-24T12:43:06ZengBMCBMC Biology1741-70072024-11-0122111910.1186/s12915-024-02066-xEurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum typesJothi Kumar Yuvaraj0Dineshkumar Kandasamy1Rebecca E. Roberts2Bill S. Hansson3Jonathan Gershenzon4Martin N. Andersson5Department of Biology, Lund UniversityDepartment of Biology, Lund UniversityDepartment of Biology, Lund UniversityDepartment of Evolutionary Neuroethology, Max Planck Institute for Chemical EcologyDepartment of Biochemistry, Max Planck Institute for Chemical EcologyDepartment of Biology, Lund UniversityAbstract Background Insects detect odours using odorant receptors (ORs) expressed in olfactory sensory neurons (OSNs) in the antennae. Ecologically important odours are often detected by selective and abundant OSNs; hence, ORs with high antennal expression. However, little is known about the function of highly expressed ORs in beetles, since few ORs have been functionally characterized. Here, we functionally characterized the most highly expressed OR (ItypOR36) in the bark beetle Ips typographus L. (Coleoptera, Curculionidae, Scolytinae), a major pest of spruce. We hypothesized that this OR would detect a compound important to beetle fitness, such as a pheromone component. We next investigated the antennal distribution of this OR using single sensillum recordings (SSR) and in situ hybridization, followed by field- and laboratory experiments to evaluate the behavioural effects of the discovered ligand. Results We expressed ItypOR36 in HEK293 cells and challenged it with 64 ecologically relevant odours. The OR responded exclusively to the monoterpene-derived ketone lanierone with high sensitivity. Lanierone is used in chemical communication in North American Ips species, but it has never been shown to be produced by I. typographus, nor has it been studied in relation to this species’ sensory physiology. Single sensillum recordings revealed a novel and abundant lanierone-responsive OSN class with the same specific response as ItypOR36. Strikingly, these OSNs were co-localized in sensilla together with seven different previously described OSN classes. Field experiments revealed that low release rates of lanierone inhibited beetle attraction to traps baited with aggregation pheromone, with strongest effects on males. Female beetles were attracted to lanierone in laboratory walking bioassays. Conclusions Our study highlights the importance of the so-called ‘reverse chemical ecology’ approach to identify novel semiochemicals for ecologically important insect species. Our discovery of the co-localization pattern involving the lanierone OSN class suggests organizational differences in the peripheral olfactory sense between insect orders. Our behavioural experiments show that lanierone elicits different responses in the two sexes, which also depend on whether beetles are walking in the laboratory or flying in the field. Unravelling the source of lanierone in the natural environment of I. typographus is required to understand these context-dependent behaviours.https://doi.org/10.1186/s12915-024-02066-xIps typographusFunctional characterizationOlfactory sensory neuronHEK293 cellsColocalizationPheromone |
| spellingShingle | Jothi Kumar Yuvaraj Dineshkumar Kandasamy Rebecca E. Roberts Bill S. Hansson Jonathan Gershenzon Martin N. Andersson Eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum types BMC Biology Ips typographus Functional characterization Olfactory sensory neuron HEK293 cells Colocalization Pheromone |
| title | Eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum types |
| title_full | Eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum types |
| title_fullStr | Eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum types |
| title_full_unstemmed | Eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum types |
| title_short | Eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor, present in several functional sensillum types |
| title_sort | eurasian spruce bark beetle detects lanierone using a highly expressed specialist odorant receptor present in several functional sensillum types |
| topic | Ips typographus Functional characterization Olfactory sensory neuron HEK293 cells Colocalization Pheromone |
| url | https://doi.org/10.1186/s12915-024-02066-x |
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