Electrophysiological and behavioural responses of Ips typographus (L.) to trans-4-thujanol—a host tree volatile compound

Blažytė‐Čereškienė, Laima; Apšegaitė, Violeta; Radžiūtė, Sandra; Mozūraitis, Raimondas; Būda, Vincas; Pečiulytė, Dalė

doi:10.1007/s13595-015-0494-5

Cited by 27 publications

(21 citation statements)

References 33 publications

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“…Thus, higher proportions of these compounds may indicate older fungal infection sites and hence older beetle invasion sites that may be less attractive to newly arriving beetles due to crowding. The lack of attraction and even repellency of higher concentrations of individual oxygenated monoterpenes seen in laboratory bioassays in our and in previous studies is consistent with this interpretation [65]. In fact, one oxygenated monoterpene derivative has been already reported to inhibit I. typographus attraction.…”

Section: Discussionsupporting

confidence: 93%

Bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes

Kandasamy

Zaman

Nakamura

et al. 2021

Preprint

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Outbreaks of bark beetles have decimated millions of hectares of conifer forest worldwide in recent years. The ability of these tiny 3-6 mm long insects to kill mature trees over a short period has been ascribed to two factors: (1) mass attacks on the host tree to overcome tree defenses and (2) the presence of fungal symbionts that support successful beetle development in the tree. While the role of pheromones in coordinating mass attacks has been well studied, the role of chemical communication in maintaining the fungal symbiosis is poorly understood. We previously demonstrated that Eurasian spruce bark beetles (Ips typographus) can recognize beneficial fungal symbionts of the genera Grosmannia, Endoconidiophora and Ophiostoma by their de novo synthesized volatile compounds. We hypothesized that the fungal symbionts of the bark beetles might metabolize spruce resin monoterpenes of the beetle host tree, Norway spruce (Picea abies), and that the volatile products could be used as cues by beetles for locating breeding sites with beneficial symbionts. Grosmannia penicillata and other fungal symbionts altered the profile of spruce bark volatiles by converting the major monoterpenes to oxygenated derivatives. Bornyl acetate was metabolized to camphor, and α- and β-pinene to trans-4-thujanol and other oxygenated products. Extensive electrophysiological measurements showed that bark beetles possess olfactory sensory neurons that are selective for these oxygenated symbiont metabolites. Compounds such as camphor and trans-4-thujanol attracted beetles at specific doses in olfactory experiments and stimulated the response of female beetles to a mixture of pheromones. Finally, the fungal symbiont was found to stimulate bark beetle tunneling on diets. Collectively, our results show that oxygenated metabolites of conifer monoterpenes produced by fungal symbionts are used by bark beetles as cues to find these essential microbial symbionts. The oxygenated metabolites may aid beetles in assessing the presence of the fungus, the defense status of the host tree and the density of conspecifics at potential feeding and breeding sites.

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Section: Discussionsupporting

confidence: 93%

Bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes

Kandasamy

Zaman

Nakamura

et al. 2021

Preprint

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“…It was recently shown that the fungi of I. typographus transform the host compounds (–)-β-pinene, (–)-α-pinene and (–)-bornyl acetate into oxygenated monoterpenoids, including the primary and secondary ligands of both ItypOR23 and ItypOR29 ( Kandasamy et al 2021 ). In lab bioassays, (+)- trans -4-thujanol and camphor were attractive to adult beetles at a relatively low dose (100 µg), however, (+)- trans -4-thujanol was repellent at higher doses (200 µg to 1 mg) ( Blažytė-Čereškienė et al 2016 ; Kandasamy et al 2021 ). This suggests concentration-dependent effects of these compounds and that changes in their emission over time may be used by new incoming bark beetles to evaluate the colonization status of the host tree.…”

Section: Discussionmentioning

confidence: 99%

Functional Evolution of a Bark Beetle Odorant Receptor Clade Detecting Monoterpenoids of Different Ecological Origins

Hou

Yuvaraj

Roberts

et al. 2021

Molecular Biology and Evolution

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Insects detect odors using an array of odorant receptors (ORs), which may expand through gene duplication. How and which new functions may evolve among related ORs within a species remain poorly investigated. We addressed this question by functionally characterizing ORs from the Eurasian spruce bark beetle Ips typographus, in which physiological and behavioral responses to pheromones, volatiles from host and non-host trees, and fungal symbionts are well described. In contrast, knowledge of OR function is restricted to two receptors detecting the pheromone compounds (S)-(–)-ipsenol (ItypOR46) and (R)-(–)-ipsdienol (ItypOR49). These receptors belong to an Ips-specific OR-lineage comprising seven ItypORs. To gain insight into the functional evolution of related ORs, we characterized the five remaining ORs in this clade using Xenopus oocytes. Two receptors responded primarily to the host tree monoterpenes (+)-3-carene (ItypOR25) and p-cymene (ItypOR27). Two receptors responded to oxygenated monoterpenoids produced in larger relative amounts by the beetle-associated fungi, with ItypOR23 specific for (+)-trans-(1R, 4S)-4-thujanol, and ItypOR29 responding to (+)-isopinocamphone and similar ketones. ItypOR28 responded to the pheromone E-myrcenol from the competitor Ips duplicatus. Overall, the OR responses match well with those of previously characterized olfactory sensory neuron classes except that neurons detecting E-myrcenol have not been identified. The characterized ORs are under strong purifying selection and demonstrate a shared functional property in that they all primarily respond to monoterpenoids. The variation in functional groups among OR ligands and their diverse ecological origins suggest that neofunctionalization has occurred early in the evolution of this OR-lineage following gene duplication.

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“…The strong sensitivity to compounds present at low levels may have evolved to detect small shifts in the host odor bouquet as an important indicator of host state for attacking beetles, possibly detectable after landing but before committing to enter the bark. It has been reported that trans -4-thujanol is found in higher amounts in young spruce trees in Lithuania, and is therefore a tentative host-age indicator (Blažytė-Čereškienė et al 2016 ). Such a function might range from indicating a dangerous, defending host, or a host with impaired defenses, to a host unsuitable due to degradation or to intra- or interspecific competition.…”

Section: Discussionmentioning

confidence: 99%

Styrene, (+)-trans-(1R,4S,5S)-4-Thujanol and Oxygenated Monoterpenes Related to Host Stress Elicit Strong Electrophysiological Responses in the Bark Beetle Ips typographus

et al. 2019

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Bark beetles kill apparently vigorous conifers during epidemics by means of pheromone-mediated aggregation. During non-endemic conditions the beetles are limited to use trees with poor defense, like wind-thrown. To find olfactory cues that help beetles to distinguish between trees with strong or weak defense, we collected volatiles from the bark surface of healthy felled or standing Picea abies trees. Furthermore, living trees were treated with methyl jasmonate in order to induce defense responses. Volatiles were analyzed by combined gas chromatography and electroantennographic detection (GC-EAD) on Ips typographus antennae. Compounds eliciting antennal responses were characterized by single sensillum recording for identification of specific olfactory sensory neurons (OSN). Release of monoterpene hydrocarbons decreased, while oxygenated compounds increased, from spring to early summer in felled trees. In both beetle sexes particular strong EAD activity was elicited by trace amounts of terpene alcohols and ketones. 4-Thujanol gave a very strong response and the absolute configuration of the tested natural product was assigned to be (+)- trans -(1 R, 4 S, 5 S )-thujanol by stereoselective synthesis and enantioselective gas chromatography. One type of OSN responded to all ketones and five other OSN were characterized by the type of compounds that elicited responses. Three new OSN classes were found. Of the eight EAD-active compounds found in methyl jasmonate-treated bark, the known anti-attractant 1,8-cineole was the one most strongly induced. Our data support the hypothesis that highly active oxygenated host volatiles could serve as positive or negative cues for host selection in I. typographus and in other bark beetles.

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Electrophysiological and behavioural responses of Ips typographus (L.) to trans-4-thujanol—a host tree volatile compound

Cited by 27 publications

References 33 publications

Bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes

Bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes

Functional Evolution of a Bark Beetle Odorant Receptor Clade Detecting Monoterpenoids of Different Ecological Origins

Styrene, (+)-trans-(1R,4S,5S)-4-Thujanol and Oxygenated Monoterpenes Related to Host Stress Elicit Strong Electrophysiological Responses in the Bark Beetle Ips typographus

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