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Disruption of carboxylesterase DaEST3 reduces tolerance to host allelochemicals in Dendroctonus armandi

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Abstract

Bark beetles mainly rely on detoxification enzymes to overcome the defensive oleoresin terpenes of their host. Insect Carboxylesterases (CarEs) play an important role in the detoxification of plant allelochemicals and insecticides. Nevertheless, the functions of specific CarE genes in metabolization of exogenous substances are still unclear in the Chinese white pine beetle, Dendroctonus armandi. In this study, we sequenced and characterized the full-length cDNAs of six CarE (DaEST1-DaEST6) genes from D. armandi. Spatiotemporal expression profiling showed that the expression of DaEST1, DaEST3 and DaEST4 in D. armandi was higher in the larval and adult stages, and these genes mainly expressed in fat body, Malpighian tubules and midgut. Moreover, the expression of DaEST1, DaEST3 and DaEST4 was significantly induced after treatment with four terpenoids. Importantly, disruption of DaEST3 significantly inhibited the CarE activity and reduced the tolerance of adults to host allelochemicals in D. armandi. Additionally, treatment with triphenyl phosphate to adults also reduced the tolerance after terpenoids exposure, which resulted in a significant decrease of CarE activity, leading to a significant improvement of mortality in D. armandi. These results indicate that DaEST3 plays an important role in determining the tolerance to host allelochemicals in D. armandi, which might be of great significance in developing new therapeutic methods to pest control.

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References

  • Bai LS, Zhao CX, Xu JJ, Feng C, Li YQ, Dong YL, Ma ZQ (2019) Identification and biochemical characterization of carboxylesterase 001G associated with insecticide detoxification in Helicoverpa armigera. Pestic Biochem Physiol 157:69–79

    Article  CAS  PubMed  Google Scholar 

  • Blomquist GJ, Tittiger C, MacLean M, Keeling CI (2021) Cytochromes P450: terpene detoxification and pheromone production in bark beetles. Curr Opin Insect Sci 43:97–102

    Article  PubMed  Google Scholar 

  • Bohlmann J (2012) Pine terpenoid defences in the mountain pine beetle epidemic and in other conifer pest interactions: specialized enemies are eating holes into a diverse, dynamic and durable defence system. Tree Physiol 32:943–945

    Article  PubMed  Google Scholar 

  • Campbell PM, Robin GCD, Court LN, Dorrian SJ, Russell RJ, Oakeshott JG (2003) Developmental expression and gene/enzyme identifications in the alpha esterase gene cluster of Drosophila melanogaster. Insect Mol Biol 12:459–471

    Article  CAS  PubMed  Google Scholar 

  • Cano-Ramirez C, Lopez MF, Cesar-Ayala AK, Pineda-Martinez V, Sullivan BT, Zuniga G (2013) Isolation and expression of cytochrome P450 genes in the antennae and gut of pine beetle Dendroctonus rhizophagus (Curculionidae: Scolytinae) following exposure to host monoterpenes. Gene 520:47–63

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Tang M, Gao J, Chen X, Li Z (2006) Changes in the composition of volatile monoterpenes and sesquiterpenes of Pinus armandi, P. tabulaeformis, and P. bungeana in Northwest China. Chem Nat Compd 42:534–538

    Article  CAS  Google Scholar 

  • Chen H, Li Z, Tang M (2010) Laboratory evaluation of flight activity of Dendroctonus armandi (Coleoptera: Curculionidae: Scolytinae). Can Entomol 142:378–387

    Article  Google Scholar 

  • Chiu CC, Keeling CI, Bohlmann J (2017) Toxicity of pine monoterpenes to mountain pine beetle. Sci Rep 7:8858

    Article  PubMed  PubMed Central  Google Scholar 

  • Cui F, Lin Z, Wang H, Liu S, Chang H, Reeck G, Qiao C, Raymond M, Kang L (2011) Two single mutations commonly cause qualitative change of nonspecific carboxylesterases in insects. Insect Biochem Mol Biol 41:1–8

    Article  CAS  PubMed  Google Scholar 

  • Cui F, Li MX, Chang HJ, Mao Y, Zhang HY, Lu LX, Yan SG, Lang ML, Liu L, Qiao CL (2015) Carboxylesterase-mediated insecticide resistance: quantitative increase induces broader metabolic resistance than qualitative change. Pestic Biochem Physiol 121:88–96

    Article  CAS  PubMed  Google Scholar 

  • Dai L, Ma M, Wang C, Shi Q, Zhang R, Chen H (2015) Cytochrome P450s from the Chinese white pine beetle, Dendroctonus armandi (Curculionidae: Scolytinae): expression profiles of different stages and responses to host allelochemicals. Insect Biochem Mol Biol 65:35–46

    Article  CAS  PubMed  Google Scholar 

  • Dow JAT, Davies SA (2006) The Malpighian tubule: rapid insights from post-genomic biology. J Insect Physiol 52:365–378

    Article  CAS  PubMed  Google Scholar 

  • Durand N, Chertemps T, Maibeche-Coisne M (2012) Antennal carboxylesterases in a moth, structural and functional diversity. Commun Integr Biol 5:284–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng X, Li M, Liu N (2018) Carboxylesterase genes in pyrethroid resistant house flies, Musca domestica. Insect Biochem Mol Biol 92:30–39

    Article  CAS  PubMed  Google Scholar 

  • Fernanda Lopez M, Cano-Ramirez C, Shibayama M, Zuniga G (2011) alpha-Pinene and myrcene induce ultrastructural changes in the midgut of Dendroctonus valens (Coleoptera: Curculionidae: Scolytinae). Ann Entomol Soc Am 104:553–561

    Article  Google Scholar 

  • Gao H, Dai L, Fu D, Sun Y, Chen H (2020a) Isolation, expression profifiling, and regulation via host allelochemicals of 16 glutathione S-transferases in the Chinese white pine beetle, Dendroctonus armandi. Front Physiol 11:546592

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao S, Zhang K, Wei L, Wei G, Xiong W, Lu Y, Zhang Y, Gao A, Li B (2020b) Insecticidal activity of Artemisia vulgaris essential oil and transcriptome analysis of Tribolium castaneum in response to oil exposure. Front Genet 11:589

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong YH, Yu XR, Shang QL, Shi XY, Gao XW (2014) Oral delivery mediated RNA interference of a carboxylesterase gene results in reduced resistance to organophosphorus insecticides in the Cotton Aphid, Aphis Gossypii Glover. PLoS ONE 9:e102823

    Article  PubMed  PubMed Central  Google Scholar 

  • Hawkes NJ, Hemingway J (2002) Analysis of the promoters for the beta-esterase genes associated with insecticide resistance in the mosquito Culex quinquefasciatus. Biochim Biophys Acta-Gene Struct Expr 1574:51–62

    Article  CAS  Google Scholar 

  • Huber DPW, Robert JA (2016) The proteomics and transcriptomics of early host colonization and overwintering physiology in the mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae). In: Tittiger C, Blomquist GJ (eds) Pine bark beetles. Elsevier, Amsterdam, pp 101–128

    Chapter  Google Scholar 

  • Jeon JH, Kim SJ, Lee HS, Cha SS, Lee JH, Yoon SH, Koo BS, Lee CM, Choi SH, Lee SH, Kang SG, Lee JH (2011) Novel metagenome-derived carboxylesterase that hydrolyzes beta-lactam antibiotics. Appl Environ Microbiol 77:7830–7836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamita SG, Hammock BD (2010) Juvenile hormone esterase: biochemistry and structure. J Pestic Sci 35:265–274

    Article  CAS  PubMed  Google Scholar 

  • Keeling CI, Yuen MMS, Liao NY, Docking TR, Chan SK, Taylor GA, Palmquist DL, Jackman SD, Anh N, Li M, Henderson H, Janes JK, Zhao Y, Pandoh P, Moore R, Sperling FAH, Huber DPW, Birol I, Jones SJM, Bohlmann J (2013) Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol 14:R27

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwon DH, Kim JH, Kim YH, Yoon KS, Clark JM, Lee SH (2014) Identification and characterization of an esterase involved in malathion resistance in the head louse Pediculus humanus capitis. Pestic Biochem Physiol 112:13–18

    Article  CAS  PubMed  Google Scholar 

  • Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253

    Article  PubMed  Google Scholar 

  • Liu B, Chen H (2022a) Disruption of CYP6DF1 and CYP6DJ2 increases the susceptibility of Dendroctonus armandi to (+)-α-pinene. Pestic Biochem Physiol 188:105270

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Chen H (2022b) Identification and functional characterization of the transcription factors AhR/ARNT in Dendroctonus armandi. Cells 11:3856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Yangb B, Go J, Yao X, Zhang Y, Song F, Liu Z (2008) Molecular cloning and characterization of a juvenile hormone esterase gene from brown planthopper, Nilaparvata lugens. J Insect Physiol 54:1495–1502

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Liu H, Liu S, Wang S, Jiang RJ, Li S (2009) Hormonal and nutritional regulation of insect fat body development and function. Arch Insect Biochem Physiol 71:16–30

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Fu D, Gao H, Ning H, Sun Y, Chen H, Tang M (2021a) Cloning and expression of the neuropeptide F and neuropeptide F receptor genes and their regulation of food intake in the Chinese white pine beetle Dendroctonus armandi. Front Physiol 12:662651

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu B, Fu D, Ning H, Tang M, Chen H (2021b) Identification of the short neuropeptide F and short neuropeptide F receptor genes and their roles of food intake in Dendroctonus armandi. InSects 12:844

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu B, Tang M, Chen H (2022) Activation of the ROS/CncC signaling pathway regulates cytochrome P450 CYP4BQ1 responsible for (+)-alpha-pinene tolerance in Dendroctonus armandi. Int J Mol Sci 23:11578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lopez MF, Cano-Ramirez C, Cesar-Ayala AK, Ruiz EA, Zuniga G (2013) Diversity and expression of P450 genes from Dendroctonus valens LeConte (Curculionidae: Scolytinae) in response to different kairomones. Insect Biochem Mol Biol 43:417–432

    Article  CAS  PubMed  Google Scholar 

  • Lü FG, Fu KY, Li Q, Guo WC, Ahmat T, Li GQ (2015) Identification of carboxylesterase genes and their expression profiles in the Colorado potato beetle Leptinotarsa decemlineata treated with fipronil and cyhalothrin. Pestic Biochem Physiol 122:86–95

    Article  PubMed  Google Scholar 

  • Mao K, Ren Z, Li W, Cai T, Qin X, Wan H, Jin BR, He S, Li J (2021) Carboxylesterase genes in nitenpyram-resistant brown planthoppers, Nilaparvata lugens. Insect Sci 28:1049–1060

    Article  CAS  PubMed  Google Scholar 

  • Marshall SDG, Putterill JJ, Plummer KM, Newcomb RD (2003) The carboxylesterase gene family from Arabidopsis thaliana. J Mol Evol 57:487–500

    Article  CAS  PubMed  Google Scholar 

  • Nishida R (2014) Chemical ecology of insect-plant interactions: ecological significance of plant secondary metabolites. Biosci Biotechnol Biochem 78:1–13

    Article  CAS  PubMed  Google Scholar 

  • Oakeshott J, Claudianos C, Campbell PM, Newcomb RD, Russell R (2005) Biochemical genetics and genomics of insect esterases. Compr Mol Insect Sci 5:309–381

    Article  CAS  Google Scholar 

  • Oakeshott JG, Johnson RM, Berenbaum MR, Ranson H, Cristino AS, Claudianos C (2010) Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis. Insect Mol Biol 19:147–163

    Article  CAS  PubMed  Google Scholar 

  • Prates HT, Santos JP, Waquil JM, Fabris JD, Oliveira AB, Foster JE (1998) Insecticidal activity of monoterpenes against Rhyzopertha dominica (F.) and Tribolium castanum (Herbst). J Stored Prod Res 34:243–249

    Article  CAS  Google Scholar 

  • Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, Sharakhova MV, Unger MF, Collins FH, Feyereisen R (2002) Evolution of supergene families associated with insecticide resistance. Science 298:179–181

    Article  CAS  PubMed  Google Scholar 

  • Robert JA, Pitt C, Bonnett TR, Yuen MMS, Keeling CI, Bohlmann J, Huber DPW (2013) Disentangling detoxification: gene expression analysis of feeding mountain pine beetle illuminates molecular-level host chemical defense detoxification mechanisms. PLoS ONE 8:e77777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sayyed AH, Wright DJ (2006) Genetics and evidence for an esterase-associated mechanism of resistance to indoxacarb in a field population of diamondback moth (Lepidoptera: Plutellidae). Pest Manag Sci 62:1045–1051

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Li W, Zhou Y, Liao X, Shi L (2022) Contribution of multiple overexpressed carboxylesterase genes to indoxacarb resistance in Spodoptera litura. Pest Manag Sci 78:1903–1914

    Article  CAS  PubMed  Google Scholar 

  • Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I (1991) Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253:872–879

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang B, Dai W, Qi L, Du S, Zhang C (2020) Functional characterization of an alpha-esterase gene associated with malathion detoxification in Bradysia odoriphaga. J Agric Food Chem 68:6076–6083

    Article  CAS  PubMed  Google Scholar 

  • Turner JM, Larsen NA, Basran A, Barbas CF, Bruce NC, Wilson IA, Lerner RA (2002) Biochemical characterization and structural analysis of a highly proficient cocaine esterase. Biochemistry 41:12297–12307

    Article  CAS  PubMed  Google Scholar 

  • Wang HL (2019) Study on the artificial feeding of Dendroctonus armandi. Dissertation Northwest A&F University, Yangling

    Google Scholar 

  • Wang J, Kean L, Yang JL, Allan AK, Davies SA, Herzyk P, Dow JAT (2004) Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol 5:R69

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang LL, Huang Y, Lu XP, Jiang XZ, Smagghe G, Feng ZJ, Yuan GR, Wei D, Wang JJ (2015) Overexpression of two α-esterase genes mediates metabolic resistance to malathion in the oriental fruit fly, Bactrocera dorsalis (Hendel). Insect Mol Biol 24:467–479

    Article  PubMed  Google Scholar 

  • Wang LL, Lu XP, Meng LW, Huang Y, Wei D, Jiang HB, Smagghe G, Wang JJ (2016) Functional characterization of an alpha-esterase gene involving malathion detoxification in Bactrocera dorsalis (Hendel). Pestic Biochem Physiol 130:44–51

    Article  CAS  PubMed  Google Scholar 

  • Wei P, Shi L, Shen G, Xu Z, Liu J, Pan Y, He L (2016) Characteristics of carboxylesterase genes and their expression-level between acaricide-susceptible and resistant Tetranychus cinnabarinus (Boisduval). Pestic Biochem Physiol 131:87–95

    Article  CAS  PubMed  Google Scholar 

  • Wei DD, He W, Miao ZQ, Tu YQ, Wang L, Dou W, Wang JJ (2020) Characterization of esterase genes involving malathion detoxification and establishment of an RNA interference method in Liposcelis bostrychophila. Front Physiol 11:274

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu S, Yang Y, Yuan G, Campbell PM, Teese MG, Russell RJ, Oakeshott JG, Wu Y (2011) Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. Insect Biochem Mol Biol 41:14–21

    Article  CAS  PubMed  Google Scholar 

  • Yang XQ (2016) Gene expression analysis and enzyme assay reveal a potential role of the carboxylesterase gene CpCE-1 from Cydia pomonella in detoxification of insecticides. Pestic Biochem Physiol 129:56–62

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li S, Xu L, Guo HF, Zi J, Wang L, He P, Fang J (2013) Overexpression of carboxylesterase-1 and mutation (F439H) of acetylcholinesterase-1 are associated with chlorpyrifos resistance in Laodelphax striatellus. Pestic Biochem Physiol 106:8–13

    Article  CAS  Google Scholar 

  • Zhu JY, Zhao N, Yang B (2012) Global transcriptome profiling of the pine shoot beetle, Tomicus yunnanensis (Coleoptera: Scolytinae). PLoS ONE 7:e32291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are thankful to the National Natural Science Foundation of China (31870636) and the Laboratory of Lingnan Modern Agriculture Project (NZ2021025).

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This research was supported by the National Natural Science Foundation of China, 31870636, to Hui Chen.

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Liu, B., Chen, H. Disruption of carboxylesterase DaEST3 reduces tolerance to host allelochemicals in Dendroctonus armandi. Arthropod-Plant Interactions 17, 673–685 (2023). https://doi.org/10.1007/s11829-023-09990-9

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