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Cytochrome P450 gene CYP6BQ8 mediates terpinen-4-ol susceptibility in the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae)

Published online by Cambridge University Press:  13 January 2023

Shanshan Gao ,
Xinlong Guo ,
Shumei Liu ,
Siying Li ,
Jiahao Zhang ,
Shuang Xue ,
Qingbo Tang ,
Kunpeng Zhang  and
Ruimin Li Open the ORCID record for Ruimin Li [Opens in a new window]
Shanshan Gao
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
Xinlong Guo
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
Shumei Liu
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
Siying Li
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
Jiahao Zhang
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
Shuang Xue
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
Qingbo Tang
Affiliation:
Department of Entomology, College of Plant Protection, Henan Agricultural University, Zhengzhou, Henan 450002, China
Kunpeng Zhang*
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
Ruimin Li*
Affiliation:
College of Biology and Food Engineering, Innovation and Practice Base for Postdoctors, Anyang Institute of Technology, Anyang, Henan 455000, China
*
Authors for correspondence: Ruimin Li, Email: liruimin920130@163.com; Kunpeng Zhang, Email: zhangkunpengag@163.com
Authors for correspondence: Ruimin Li, Email: liruimin920130@163.com; Kunpeng Zhang, Email: zhangkunpengag@163.com
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Abstract

Cytochrome P450 proteins (CYPs) in insects can encode various detoxification enzymes and catabolize heterologous substances, conferring tolerance to insecticides. This study describes the identification of a P450 gene (CYP6BQ8) from Tribolium castaneum (Herbst) and investigation of its spatiotemporal expression profile and potential role in the detoxification of terpinen-4-ol, a component of plant essential oils. The developmental expression profile showed that TcCYP6BQ8 expression was relatively higher in early- and late-larval stages of T. castaneum compared with other developmental stages. Tissue expression profiles showed that TcCYP6BQ8 was mainly expressed in the head and integument of both larvae and adults. The expression profiling of TcCYP6BQ8 in developmental stages and tissues is closely related to the detoxification of heterologous substances. TcCYP6BQ8 expression was significantly induced after exposure to terpinen-4-ol, and RNA interference against TcCYP6BQ8 increased terpinen-4-ol-induced larval mortality from 47.78 to 66.67%. This indicates that TcCYP6BQ8 may be involved in T. castaneum's metabolism of terpinen-4-ol. Correlation investigation between the CYP6BQ8 gene and terpinen-4-ol resistance in T. castaneum revealed that the TcCYP6BQ8 gene was one of the factors behind T. castaneum's resistance to terpinen-4-ol. This discovery may provide a new theoretical foundation for future regulation of T. castaneum.

Keywords

Cytochrome P450RNA interference susceptibilityterpinen-4-olTribolium castaneum

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Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 2 , April 2023 , pp. 271 - 281
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Copyright © The Author(s), 2023. Published by Cambridge University Press

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References

Ahn, SJ, Vogel, H and Heckel, DG (2012) Comparative analysis of the UDP-glycosyltransferase multigene family in insects. Insect Biochemistry and Molecular Biology 42, 133–147.CrossRefGoogle ScholarPubMed
Aronstein, K, Oppert, B and Lorenzen, MD (2011) RNAi in agriculturally-important arthropods. In Grabowski, P (ed.), RNA Processing. Rijeka, Croatia: InTech, pp. 157–180.Google Scholar
Awan, DA, Saleem, MA, Nadeem, MS and Shakoori, AR (2012) Toxicological and biochemical studies on spinosad and synergism with piperonyl butoxide in susceptible and resistant strains of Tribolium castaneum. Pakistan Journal of Zoology 44, 649–662.Google Scholar
Bautista, MA, Miyata, T, Miura, K and Tanaka, T (2009) RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochemistry and Molecular Biology 39, 38–46.CrossRefGoogle ScholarPubMed
Benelli, G (2015) Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitology Research 114, 3201–3212.CrossRefGoogle ScholarPubMed
Beran, F, Köllner, TG, Gershenzon, J and Tholl, D (2019) Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites. New Phytologist 223, 52–67.CrossRefGoogle ScholarPubMed
Berenbaum, MR (2002) Postgenomic chemical ecology: from genetic code to ecological interactions. Journal of Chemical Ecology 28, 873–896.CrossRefGoogle ScholarPubMed
Bergé, JB, Feyereisen, R and Amichot, M (1998) Cytochrome P450 monooxygenases and insecticide resistance in insects. Philosophical Transactions of the Royal Society of London B Biological Sciences 353, 1701–1705.CrossRefGoogle ScholarPubMed
Boevé, JL, Ducarme, V, Mertens, T, Bouillard, P and Angeli, S (2004) Surface structure, model and mechanism of an insect integument adapted to be damaged easily. Journal of Nanobiotechnology 2, 10.CrossRefGoogle ScholarPubMed
Boukouvala, MC, Kavallieratos, NG, Athanassiou, CG and Hadjiarapoglou, LP (2016 a) Biological activity of two new pyrrole derivatives against stored-product species: influence of temperature and relative humidity. Bulletin of Entomological Research 106, 446–456.CrossRefGoogle ScholarPubMed
Boukouvala, MC, Kavallieratos, NG, Athanassiou, CG, Losic, D, Hadjiarapoglou, LP and Elemes, Y (2016 b) Laboratory evaluation of five novel pyrrole derivatives as grain protectants against Tribolium confusum and Ephestia kuehniella larvae. Journal of Pest Science 90, 569–585.CrossRefGoogle Scholar
Boyer, S, Zhang, H and Lemperiere, G (2012) A review of control methods and resistance mechanisms in stored-product insects. Bulletin of Entomological Research 102, 213–229.CrossRefGoogle ScholarPubMed
Calla, B (2021) Signatures of selection and evolutionary relevance of cytochrome P450s in plant-insect interactions. Current Opinion in Insect Science 43, 92–96.Google ScholarPubMed
Chen, C, Shan, T, Liu, Y, Wang, C, Shi, X and Gao, X (2019) Identification and functional analysis of a cytochrome P450 gene involved in imidacloprid resistance in Bradysia odoriphaga Yang et Zhang. Pesticide Biochemistry and Physiology 153, 129–135.CrossRefGoogle ScholarPubMed
Dai, L, Wang, C, Zhang, X, Yu, J, Zhang, R and Chen, H (2014) Two CYP4 genes of the Chinese white pine beetle, Dendroctonus armandi (Curculionidae: Scolytinae), and their transcript levels under different development stages and treatments. Insect Molecular Biology 23, 598–610.CrossRefGoogle ScholarPubMed
Dey, D (2016) Impact of indiscriminate use of insecticide on environmental pollution. International Journal of Plant Protection 9, 264–267.Google Scholar
Dierick, HA and Greenspan, RJ (2006) Molecular analysis of flies selected for aggressive behavior. Nature Genetics 38, 1023–1031.Google ScholarPubMed
Dulbecco, AB, Moriconi, DE, Calderón-Fernández, GM, Lynn, S, McCarthy, A, Roca-Acevedo, G, Salamanca-Moreno, JA, Juárez, MP and Pedrini, N (2018) Integument CYP genes of the largest genome-wide cytochrome P450 expansions in triatomines participate in detoxification in deltamethrin-resistant Triatoma infestans. Scientific Reports 8, 10177.CrossRefGoogle ScholarPubMed
Dulbecco, AB, Moriconi, DE and Pedrini, N (2021) Knockdown of CYP4PR1, a cytochrome P450 gene highly expressed in the integument tissue of Triatoma infestans, increases susceptibility to deltamethrin in pyrethroid-resistant insects. Pesticide Biochemistry and Physiology 173, 104781.CrossRefGoogle ScholarPubMed
Feyereisen, R (2006) Evolution of insect P450. Biochemical Society Transactions 34, 1252–1255.CrossRefGoogle ScholarPubMed
Feyereisen, R (2011) Insect CYP genes and P450 enzymes. Insect Molecular Biology 8, 236–316.Google Scholar
Feyereisen, R (2020) Origin and evolution of the CYP4G subfamily in insects, cytochrome P450 enzymes involved in cuticular hydrocarbon synthesis. Molecular Phylogenetics and Evolution 143, 106695.CrossRefGoogle ScholarPubMed
Gao, SS, Zhang, K, Wei, L, Wei, G, Xiong, W, Lu, Y, Zhang, Y, Gao, A and Li, B (2020) Insecticidal activity of Artemisia vulgaris essential oil and transcriptome analysis of Tribolium castaneum in response to oil exposure. Frontiers in Genetics 11, 589.CrossRefGoogle ScholarPubMed
Gao, H, Lin, X, Yang, B and Liu, Z (2021) The roles of GSTs in fipronil resistance in Nilaparvata lugens: over-expression and expression induction. Pesticide Biochemistry and Physiology 177, 104880.CrossRefGoogle ScholarPubMed
Gao, S-S, Zhang, Y-L, Zhang, K-P, Wang, X-Y, Tang, Q-B and Zhang, Y-C (2022 a) Contact toxicity and transcriptomic analysis of terpinen-4-ol exposure in Tribolium castaneum. Journal of Asia-Pacific Entomology 25, 101950.CrossRefGoogle Scholar
Gao, S, Liu, K, Liu, H, Yin, S, Guo, X, Zhang, Y, Zhang, K and Li, R (2022 b) Functional analysis of a cytochrome P450 gene CYP9Z6 responding to terpinen-4-ol in the red flour beetle, Tribolium castaneum. Pesticide Biochemistry and Physiology 183, 105065.CrossRefGoogle ScholarPubMed
Golden, G, Quinn, E, Shaaya, E, Kostyukovsky, M and Poverenov, E (2018) Coarse and nano emulsions for effective delivery of the natural pest control agent pulegone for stored grain protection. Pest Management Science 74, 820–827.CrossRefGoogle ScholarPubMed
Guo, ZB, Ma, ZQ, Feng, JT and Zhang, X (2008) Inhibition of Na+, K+-ATPase in housefly (Musca domestica L.) by terpinen-4-ol and its ester derivatives. Agricultural Sciences in China 41, 3110–3115.Google Scholar
Heckel, DG (2018) Insect detoxification and sequestration strategies. In Annual Plant Reviews Online. Hoboken, NJ: John Wiley & Sons, pp. 77–114.CrossRefGoogle Scholar
Heidel-Fischer, HM and Vogel, H (2015) Molecular mechanisms of insect adaptation to plant secondary compounds. Current Opinion in Insect Science 8, 8–14.CrossRefGoogle ScholarPubMed
Helvig, C, Koener, JF, Unnithan, GC and Feyereisen, R (2004 a) CYP15A1, the cytochrome P450 that catalyzes epoxidation of methyl farnesoate to juvenile hormone III in cockroach corpora allata. Proceedings of the National Academy of Sciences of the United States of America 101, 4024–4029.CrossRefGoogle ScholarPubMed
Helvig, C, Tijet, N, Feyereisen, R, Walker, FA and Restifo, LL (2004 b) Drosophila melanogaster CYP6A8, an insect P450 that catalyzes lauric acid (omega-1)-hydroxylation. Biochemical and Biophysical Research Communications 325, 1495–1502.CrossRefGoogle ScholarPubMed
Horn, T and Panfilio, KA (2016) Novel functions for Dorsocross in epithelial morphogenesis in the beetle Tribolium castaneum. Development (Cambridge, England) 143, 3002–3011.Google ScholarPubMed
Huang, Y, Liao, M, Yang, Q, Shi, S, Xiao, J and Cao, H (2020) Knockdown of NADPH-cytochrome P450 reductase and CYP6MS1 increases the susceptibility of Sitophilus zeamais to terpinen-4-ol. Pesticide Biochemistry and Physiology 162, 15–22.CrossRefGoogle ScholarPubMed
Islam, W (2017) Eco-friendly approaches for the management of red flour beetle: Tribolium castaneum (Herbst). Science Letters 5, 105–114.Google Scholar
Isman, B (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology 51, 45–66.CrossRefGoogle Scholar
Jander, G (2014) Revisiting plant-herbivore co-evolution in the molecular biology era. Annual Plant Reviews 47, 361–384.CrossRefGoogle Scholar
Kaplanoglu, E, Chapman, P, Scott, IM and Donly, C (2017) Overexpression of a cytochrome P450 and a UDP-glycosyltransferase is associated with imidacloprid resistance in the Colorado potato beetle, Leptinotarsa decemlineata. Scientific Reports 7, 1762.CrossRefGoogle Scholar
Li, W, Berenbaum, MR and Schuler, MA (2001) Molecular analysis of multiple CYP6B genes from polyphagous Papilio species. Insect Biochemistry and Molecular Biology 31, 999–1011.CrossRefGoogle ScholarPubMed
Li, X, Schuler, MA and Berenbaum, MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231–253.CrossRefGoogle ScholarPubMed
Li, T, Liu, Y, Wei, DD, Shang, F, Smagghe, G, Dou, W, Wang, JJ and Smagghe, G (2016) Characterization and expression profiles of five possible cytochrome p450 genes from liposcelis entomophila (enderlein) (psocoptera: liposcelididae). Archives of Insect Biochemistry and Physiology 92, 259–273.CrossRefGoogle ScholarPubMed
Li, J, Ma, Y, Yuan, W, Xiao, Y and Liu, K (2017) FOXA transcriptional factor modulates insect susceptibility to Bacillus thuringiensis Cry1Ac toxin by regulating the expression of toxin-receptor ABCC2 and ABCC3 genes. Insect Biochemistry and Molecular Biology 88, 1–11.CrossRefGoogle ScholarPubMed
Li, F, Ma, K, Chen, X, Zhou, JJ and Gao, X (2019) The regulation of three new members of the cytochrome P450 CYP6 family and their promoters in the cotton aphid Aphis gossypii by plant allelochemicals. Pest Management Science 75, 152–159.CrossRefGoogle ScholarPubMed
Liao, M, Yang, QQ, Xiao, JJ, Huang, Y and Zhou, LJ (2018) Toxicity of Melaleuca alternifolia essential oil to the mitochondrion and NAD+/NADH dehydrogenase in Tribolium confusum. PeerJ 6, e5693.CrossRefGoogle Scholar
Lis, ŁB, Bakuła, T, Baranowski, M and Czarnewicz, A (2011) The carcinogenic effects of benzoquinones produced by the flour beetle. Polish Journal of Veterinary Sciences 14, 159–164.CrossRefGoogle ScholarPubMed
Liu, N, Li, M, Gong, Y, Liu, F and Li, T (2015) Cytochrome P450s–their expression, regulation, and role in insecticide resistance. Pesticide Biochemistry and Physiology 120, 77–81.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif.) 25, 402–408.CrossRefGoogle ScholarPubMed
Lu, Y, Park, Y, Gao, X, Zhang, X, Yao, J, Pang, Y-P, Jiang, H and Zhu, KY (2012) Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum. Scientific Reports 2, 1–7.CrossRefGoogle ScholarPubMed
Lu, K, Li, W, Cheng, Y, Ni, H, Chen, X, Li, Y, Tang, B, Sun, X, Li, Y, Liu, T, Qin, N, Chen, D, Zeng, R and Song, Y (2019) Copper exposure enhances Spodoptera litura larval tolerance to β-cypermethrin. Pesticide Biochemistry and Physiology 160, 127–135.CrossRefGoogle ScholarPubMed
Ma, MQ, He, WW, Xu, SJ, Xu, LT and Zhang, J (2020) RNA interference in Colorado potato beetle (Leptinotarsa decemlineata): a potential strategy for pest control. Journal of Integrative Agriculture 19, 428–437.CrossRefGoogle Scholar
Maïbèche-Coisne, M, Nikonov, AA, Ishida, Y, Jacquin-Joly, E and Leal, WS (2004) Pheromone anosmia in a scarab beetle induced by in vivo inhibition of a pheromone-degrading enzyme. Proceedings of the National Academy of Sciences of the United States of America 101, 11459–11464.CrossRefGoogle Scholar
Mangang, IB, Tiwari, A, Rajamani, M and Manickam, L (2020) Comparative laboratory efficacy of novel botanical extracts against Tribolium castaneum. Journal of the Science of Food and Agriculture 100, 1541–1546.CrossRefGoogle ScholarPubMed
Min, L, Xiao, JJ, Zhou, LJ, Yang, L, Wu, XW, Hua, RM, Wang, GR, Cao, HQ and Qiu, X (2016) Insecticidal activity of Melaleuca alternifolia essential oil and RNA-seq analysis of Sitophilus zeamais transcriptome in response to oil fumigation. PLoS One 11, e0167748.Google Scholar
Nelson, DR, Goldstone, JV and Stegeman, JJ (2013) The cytochrome P450 genesis locus: the origin and evolution of animal cytochrome P450s. Philosophical Transactions of the Royal Society of London B Biological Sciences 368, 20120474.CrossRefGoogle ScholarPubMed
Nishida, R (2014) Chemical ecology of insect-plant interactions: ecological significance of plant secondary metabolites. Bioscience Biotechnology and Biochemistry 78, 1–13.CrossRefGoogle ScholarPubMed
Ogendo, JO, Kostyukovsky, M, Ravid, U, Matasyoh, JC, Deng, AL, Omolo, EO, Kariuki, ST and Shaaya, E (2008) Bioactivity of Ocimum gratissimum L. oil and two of its constituents against five insect pests attacking stored food products. Journal of Stored Products Research 44, 328–334.CrossRefGoogle Scholar
Rewitz, KF, O'Connor, MB and Gilbert, LI (2007) Molecular evolution of the insect halloween family of cytochrome P450s: phylogeny, gene organization and functional conservation. Insect Biochemistry and Molecular Biology 37, 741–753.CrossRefGoogle ScholarPubMed
Rosner, J, Wellmeyer, B and Merzendorfer, H (2020) Tribolium castaneum: a model for investigating the mode of action of insecticides and mechanisms of resistance. Current Pharmaceutical Design 26, 3554–3568.CrossRefGoogle Scholar
Saad, MMG, El-Deeb, DA and Abdelgaleil, SAM (2019) Insecticidal potential and repellent and biochemical effects of phenylpropenes and monoterpenes on the red flour beetle, Tribolium castaneum Herbst. Environmental Science and Pollution Research International 26, 6801–6810.CrossRefGoogle ScholarPubMed
Song, X, Wen, X, He, J, Zhao, H, Li, S and Wang, M (2019) Phytochemical components and biological activities of Artemisia argyi. Journal of Functional Foods 52, 648–662.CrossRefGoogle Scholar
Sun, Z, Shi, Q, Li, Q, Wang, R, Xu, C, Wang, H, Ran, C, Song, Y and Zeng, R (2019) Identification of a cytochrome P450 CYP6AB60 gene associated with tolerance to multi-plant allelochemicals from a polyphagous caterpillar tobacco cutworm (Spodoptera litura). Pesticide Biochemistry and Physiology 154, 60–66.CrossRefGoogle ScholarPubMed
Suthisut, D, Fields, PG and Chandrapatya, A (2011) Contact toxicity, feeding reduction, and repellency of essential oils from three plants from the ginger family (Zingiberaceae) and their major components against Sitophilus zeamais and Tribolium castaneum. Journal of Economic Entomology 104, 1445–1454.CrossRefGoogle ScholarPubMed
Tang, B, Cheng, Y, Li, Y, Li, W, Ma, Y, Zhou, Q and Lu, K (2020) Adipokinetic hormone enhances CarE-mediated chlorpyrifos resistance in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology 29, 511–522.CrossRefGoogle ScholarPubMed
Tunç, İ, Berger, BM, Erler, F and Dağlı, F (2000) Ovicidal activity of essential oils from five plants against two stored-product insects. Journal of Stored Products Research 36, 161–168.CrossRefGoogle Scholar
Wang, L, Dankert, H, Perona, P and Anderson, DJ (2008) A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 105, 5657–5663.CrossRefGoogle ScholarPubMed
Xie, J, Hu, XX, Zhai, MF, Yu, XJ, Song, XW, Gao, SS, Wu, W and Li, B (2019) Characterization and functional analysis of hsp18. 3 gene in the red flour beetle, Tribolium castaneum. Insect Science 26, 263–273.CrossRefGoogle ScholarPubMed
Xiong, W, Gao, S, Mao, J, Wei, L, Xie, J, Liu, J, Bi, J, Song, X and Li, B (2019) CYP4BN6 and CYP6BQ11 mediate insecticide susceptibility and their expression is regulated by latrophilin in Tribolium castaneum. Pest Management Science 75, 2744–2755.Google ScholarPubMed
Xu, X, Li, X, Liu, Z, Wang, F, Fan, L, Wu, C and Yao, Y (2021) Knockdown of CYP301B1 and CYP6AX1v2 increases the susceptibility of the brown planthopper to beta-asarone, a potential plant-derived insecticide. International Journal of Biological Macromolecules 171, 150–157.CrossRefGoogle ScholarPubMed
Yu, L, Tang, W, He, W, Ma, X, Vasseur, L, Baxter, SW, Yang, G, Huang, S, Song, F and You, M (2015) Characterization and expression of the cytochrome P450 gene family in diamondback moth, Plutella xylostella (L.). Scientific Reports 5, 8952.CrossRefGoogle ScholarPubMed
Zhang, WJ, Yang, K, You, CX, Wang, Y, Wang, CF, Wu, Y, Geng, ZF, Su, Y, Du, SS and Deng, ZW (2015) Bioactivity of essential oil from Artemisia stolonifera (Maxim.) Komar. and its main compounds against two stored-product insects. Journal of Oleo Science 64, 299–307.CrossRefGoogle ScholarPubMed
Zhang, X, Kang, X, Wu, H, Silver, K, Zhang, J, Ma, E and Zhu, KY (2018) Transcriptome-wide survey, gene expression profiling and exogenous chemical-induced transcriptional responses of cytochrome P450 superfamily genes in migratory locust (Locusta migratoria). Insect Biochemistry and Molecular Biology 100, 66–77.CrossRefGoogle ScholarPubMed
Zhang, X, Dong, J, Wu, H, Zhang, H, Zhang, J and Ma, E (2019) Knockdown of cytochrome P450 CYP6 family genes increases susceptibility to carbamates and pyrethroids in the migratory locust, Locusta migratoria. Chemosphere 223, 48–57.CrossRefGoogle ScholarPubMed
Zhang, YC, Gao, SS, Xue, S, Gu, LB and Zhang, KP (2020) Controlling effects of essential oils on Artemisia vulgaris (L.) against Tribolium Castaneum (Herbst) λ. J Chin Cereal Oil Ass 9, 117–123.Google Scholar
Zhang, YC, Gao, SS, Xue, S, An, SH and Zhang, KP (2021) Disruption of the cytochrome P450 CYP6BQ7 gene reduces tolerance to plant toxicants in the red flour beetle, Tribolium castaneum. International Journal of Biological Macromolecules 172, 263–269.CrossRefGoogle ScholarPubMed
Zhu, F, Li, T, Zhang, L and Liu, N (2008) Co-up-regulation of three P450 genes in response to permethrin exposure in permethrin resistant house flies, Musca domestica. BMC Physiology 8, 18.CrossRefGoogle ScholarPubMed
Zhu, F, Parthasarathy, R, Bai, H, Woithe, K, Kaussmann, M, Nauen, R, Harrison, DA and Palli, SR (2010) A brain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum. Proceedings of the National Academy of Sciences of the United States of America 107, 8557–8562.CrossRefGoogle ScholarPubMed
Zhu, F, Moural, TW, Shah, K and Palli, SR (2013) Integrated analysis of cytochrome P450 gene superfamily in the red flour beetle, Tribolium castaneum. BMC Genomics 14, 174.CrossRefGoogle ScholarPubMed