Hormetic response and co-expression of cytochrome P450 and cuticular protein reveal the tolerance to host-specific terpenoid defences in an emerging insect pest, Pagiophloeus tsushimanus (Coleoptera: Curculionidae)

Li, Shouyin; Li, Hui; Wang, Jingting; Chen, Cong; Hao, Dejun

doi:10.1007/s10340-022-01509-0

Cited by 9 publications

(7 citation statements)

References 77 publications

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“…Studies have shown that the secondary metabolites of C. camphora are considered to have a high degree of resistance to a variety of herbivorous insects ( Jiang et al 2016 , Wu et al 2020 ). In our previous study, however, low doses of exogenous camphor can instead promote growth and development of P. tsushimanus ( Li et al 2023 ), suggesting that this specialist weevil appears to have evolved a strategy adapted to its host-specific chemical defenses. Thus, this deserves in-depth studies to investigate whether the symbiotic gut bacteria in P. tsushimanus larvae play an important role in detoxifying and metabolizing these hosts’ toxins.…”

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confidence: 78%

Isolation and characterization of gut bacteria associated with the degradation of host-specific terpenoids in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) larvae

Qiao

Zhu

et al. 2023

Journal of Insect Science

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Insect intestinal bacteria play an important role in resisting defensive substances of host plants. Pagiophloeus tsushimanus (Coleoptera: Curculionidae) feeds exclusively on camphor trees (Cinnamomum camphora, Laurales: Lauraceae) in China, causing substantial economic and ecological losses. It is unclear how the larvae of P. tsushimanus outcome the main secondary metabolites of C. camphora such as D-camphor, eucalyptol, and linalool. In this study, we isolated terpenoid-degrading bacteria from the gut of P. tsushimanus larvae by using selective culture medium. Maximum likelihood phylogenetic analyses were performed with 16S rDNA sequences to identify the bacteria, and results showed ten strains belonged to four genera, including Pseudomonas, Enterobacter, Serratia, and Corynebacterium. Then, gas chromatography was employed to determine the degradability of D-camphor, eucalyptol, and linalool by the isolated strains, results showed that Z5 strain (i.e., Corynebacterium variabile, Actinomycetales: Corynebacteriaceae), F1 strain (i.e., Pseudomonas aeruginosa, Pseudomonadales: Pseudomonaceae), and A3 strain (i.e., Serratia marcescens, Enterobacterales: Enterobacteriaceae) had the highest degradation rates of D-camphor, linalool, and eucalyptol, respectively. The intestinal bacteria were capable of terpenoid degradation in vitro, which suggested that these gut bacteria associated with P. tsushimanus play an important role in overcoming host plant secondary metabolite defense, thereby facilitating the host specialization of this pest.

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confidence: 78%

Isolation and characterization of gut bacteria associated with the degradation of host-specific terpenoids in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) larvae

Qiao

Zhu

et al. 2023

Journal of Insect Science

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“…D-camphor and linalool from camphor trees) in insects remains poorly understood. Similarly, a bank of CYP450 transcripts in our former investigations were upregulated after D-camphor exposure [55]. We expected that there is a parallel CYP450-mediated metabolic process occurring in the detoxification of D-camphor and linalool since they are a group of isomers.…”

Section: A Global Picture Of Pagiophloeus Tsushimanus Transcriptomementioning

confidence: 68%

“…In our previous work, an emerging specialist pest, Pagiophloeus tsushimanus, feeding exclusively on camphor trees Cinnamomum camphora, has been reported that its tolerance performance on different host monoterpenoids including D-camphor and linalool varied [26]. Furthermore, a potential mechanism underlying the tolerance of this specialist to D-camphor exposure has been proposed [55]. In this work, we obtained a more comprehensive transcriptome of P. tsushimanus using a combination of RNA-seq and SMRT sequencing, and emphasized the functional transcripts involved in response to dietary linalool.…”

Section: Discussionmentioning

confidence: 99%

Tolerance to dietary linalool primarily involves co-expression of cytochrome P450s and cuticular proteins in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) larvae using SMRT sequencing and RNA-seq

Chen

et al. 2023

BMC Genomics

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Background Pagiophloeus tsushimanus (Coleoptera: Curculionidae), an emerging forest pest exclusively infesting camphor trees, has recently caused severe ecological and economic damage in localized areas in China. Its population outbreak depends largely on the capacity to overcome the pressure of terpenoid-derived metabolites (e.g. linalool) from camphor trees. At present, the molecular basis of physiological adaptation of P. tsushimanus to dietary linalool is poorly understood, and there is no available reference genome or transcriptome. Results Herein, we constructed the transcriptome profiling of P. tsushimanus larvae reared on linalool-infused diets using RNA sequencing and single-molecule real-time sequencing. A total of 20,325 high-quality full-length transcripts were identified as a reference transcriptome, of which 14,492 protein-coding transcripts including 130 transcription factors (TFs), and 5561 long non-coding RNAs (lncRNAs) were detected. Also, 30 alternative splicing events and 8049 simple sequence repeats were captured. Gene ontology enrichment of differential expressed transcripts revealed that overall up-regulation of both cytochrome P450s (CYP450s) and cuticular proteins (CPs), was the primary response characteristic against dietary linalool. Other physiological effects possibly caused by linalool exposure, such as increase in Reactive Oxygen Species (ROS) and hormetic stimulation, were compensated by a handful of induced genes encoding antioxidases, heat shock proteins (HSPs), juvenile hormone (JH) epoxide hydrolases, and digestive enzymes. Additionally, based on co-expression networks analysis, a diverse array of hub lncRNAs and TFs co-expressed with CYP450s and CPs were screened as the potential gene regulators. Temporal expression of candidate transcripts determined by quantitative real-time PCR also indicated a cooperative relationship between the inductions of CYP450s and CPs upon exposure to linalool. Conclusions Our present study provides an important transcriptome resource of P. tsushimanus, and lays a valuable foundation for understanding how this specialist pest copes with chemical challenges in its specific host environments.

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“…Such anomalies are not uncommon in studies where a large number of insecticide bioassays were conducted [57][58][59][60] and may be due to hormesis, a phenomenon in which sublethal insecticide exposure may increase inset survival via a range of mechanisms including stimulating insecticide metabolism. 61,62 Recently, some researchers have recommended that a bottle assay's measure of KD over time could be augmented with a second endpoint to determine mortality. [44][45][46] In this study we held mosquitoes for 24 h after insecticide exposure to determine final mortality and to monitor recovery from KD.…”

Section: Discussionmentioning

confidence: 99%

“…The effect did not persist at 10× the deltamethrin dose and the relationship did not hold true for permethrin. Such anomalies are not uncommon in studies where a large number of insecticide bioassays were conducted 57–60 and may be due to hormesis, a phenomenon in which sublethal insecticide exposure may increase inset survival via a range of mechanisms including stimulating insecticide metabolism 61,62 …”

Section: Discussionmentioning

confidence: 99%

Insecticide resistance compromises the control of Aedes aegypti in Bangladesh

Al-Amin

Gyawali

Graham

et al. 2023

Pest Management Science

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BACKGROUND With no effective drugs or widely available vaccines, dengue control in Bangladesh is dependent on targeting the primary vector Aedes aegypti with insecticides and larval source management. Despite these interventions, the dengue burden is increasing in Bangladesh, and the country experienced its worst outbreak in 2019 with 101 354 hospitalized cases. This may be partially facilitated by the presence of intense insecticide resistance in vector populations. Here, we describe the intensity and mechanisms of resistance to insecticides commonly deployed against Ae. aegypti in Dhaka, Bangladesh. RESULTS Dhaka Ae. aegypti colonies exhibited high‐intensity resistance to pyrethroids. Using CDC bottle assays, we recorded 2–24% mortality (recorded at 24 h) to permethrin and 48–94% mortality to deltamethrin, at 10× the diagnostic dose. Bioassays conducted using insecticide–synergist combinations suggested that metabolic mechanisms were contributing to pyrethroid resistance, specifically multi‐function oxidases, esterases, and glutathione S‐transferases. In addition, kdr alleles were detected, with a high frequency (78–98%) of homozygotes for the V1016G mutation. A large proportion (≤ 74%) of free‐flying and resting mosquitoes from Dhaka colonies survived exposure to standard applications of pyrethroid aerosols in an experimental free‐flight room. Although that exposure affected the immediate host‐seeking behavior of Ae. aegypti, the effect was transient in surviving mosquitoes. CONCLUSION The intense resistance characterized in this study is likely compromising the operational effectiveness of pyrethroids against Ae. aegypti in Dhaka. Switching to alternative chemical classes may offer a medium‐term solution, but ultimately a more sustainable and effective approach to controlling dengue vectors is required. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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Hormetic response and co-expression of cytochrome P450 and cuticular protein reveal the tolerance to host-specific terpenoid defences in an emerging insect pest, Pagiophloeus tsushimanus (Coleoptera: Curculionidae)

Cited by 9 publications

References 77 publications

Isolation and characterization of gut bacteria associated with the degradation of host-specific terpenoids in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) larvae

Isolation and characterization of gut bacteria associated with the degradation of host-specific terpenoids in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) larvae

Tolerance to dietary linalool primarily involves co-expression of cytochrome P450s and cuticular proteins in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) larvae using SMRT sequencing and RNA-seq

Insecticide resistance compromises the control of Aedes aegypti in Bangladesh

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