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| Insecticide induction of O-demethylase activity and expression of cytochrome P450 genes in the red imported fire ant (Solenopsis invicta Buren) |
| ZHANG Bai-zhong, KONG Fan-chao, WANG Hua-tang, GAO Xi-wu, ZENG Xin-nian, SHI Xue-yan |
1、College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, P.R.China
2、Department of Entomology, China Agricultural University, Beijing 100193, P.R.China |
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摘要 The red imported fire ant (Solenopsis invicta) is a global major invasive pest, and has caused significant economic, social and environmental impacts since its invasion to mainland of China in 2004. To date, chemical control has been the most effective measure. However, the long-term use of chemicals would lead to an unexpected rebound. To understand the risks and explore the mechanisms of detoxification or induction to insecticides in S. invicta, the O-demethylase activity and expression of cytochrome P450 genes of workers and queens, and the effects of chlorpyrifos and fipronil exposure in workers were investigated. Biochemical assays showed the O-demethylase activity of cytochrome P450 was significantly higher in workers than in queens (1.66-fold), and was significantly induced in workers exposed to chlorpyrifos and fipronil, reaching a maximum (3.00- and 1.95-fold) at 48 h and then decreasing dramatically compared to controls (exposed to acetone counterpart). The relative expression levels of 12 cytochrome P450 expressed sequence tags (ESTs) in workers were significantly higher than in queens (from 2.3- to 36.4-fold). Multiple cytochrome P450 genes (except 9E4) were co-up-regulated (from 1.5- to 2.86-fold) in workers exposed to fipronil. These results indicated that the increased O-demethylase activity may result from the increased transcription levels of cytochrome P450 related to detoxification of insecticides in S. invicta. It appears that cytochrome P450 plays an important role in enhanced metabolic detoxification of insecticides. At the same time, it also provides the theoretical basis for resistance management and rational usage of insecticides to control S. invicta.
Abstract The red imported fire ant (Solenopsis invicta) is a global major invasive pest, and has caused significant economic, social and environmental impacts since its invasion to mainland of China in 2004. To date, chemical control has been the most effective measure. However, the long-term use of chemicals would lead to an unexpected rebound. To understand the risks and explore the mechanisms of detoxification or induction to insecticides in S. invicta, the O-demethylase activity and expression of cytochrome P450 genes of workers and queens, and the effects of chlorpyrifos and fipronil exposure in workers were investigated. Biochemical assays showed the O-demethylase activity of cytochrome P450 was significantly higher in workers than in queens (1.66-fold), and was significantly induced in workers exposed to chlorpyrifos and fipronil, reaching a maximum (3.00- and 1.95-fold) at 48 h and then decreasing dramatically compared to controls (exposed to acetone counterpart). The relative expression levels of 12 cytochrome P450 expressed sequence tags (ESTs) in workers were significantly higher than in queens (from 2.3- to 36.4-fold). Multiple cytochrome P450 genes (except 9E4) were co-up-regulated (from 1.5- to 2.86-fold) in workers exposed to fipronil. These results indicated that the increased O-demethylase activity may result from the increased transcription levels of cytochrome P450 related to detoxification of insecticides in S. invicta. It appears that cytochrome P450 plays an important role in enhanced metabolic detoxification of insecticides. At the same time, it also provides the theoretical basis for resistance management and rational usage of insecticides to control S. invicta.
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Received: 22 January 2015
Accepted:
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| Fund: The authors are highly obliged to the National Natural Science Foundation of China (31071712) for the financial support given to the present research work. |
| About author: ZHANG Bai-zhong, E-mail: baizhongok@163.com; |
Cite this article:
ZHANG Bai-zhong, KONG Fan-chao, WANG Hua-tang, GAO Xi-wu, ZENG Xin-nian, SHI Xue-yan.
2016.
Insecticide induction of O-demethylase activity and expression of cytochrome P450 genes in the red imported fire ant (Solenopsis invicta Buren). Journal of Integrative Agriculture, 15(1): 135-144.
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| Abbas N, Khan H A A, Shad S A. 2014. Cross-resistance,genetics, and realized heritability of resistance to fipronilin the house fly, Muscado mestica (Diptera: Muscidae):A potential vector for disease transmission. ParasitologyResearch, 113, 1343-1352Alexia C P, Jaclyn B, Myriam R K, Jessica R, Emilie G C,Rodolphe P, Muhammad A R, Mark P, Chantal D V,Stéphane R, Jean P D 2013. The central role of mosquitocytochrome P450 CYP6Zs in insecticide detoxificationrevealed by functional expression and structural modelling.Biochemical Journal, 455, 75-85Avicor S W, Wajidi M F F, El-garj F M A, Jaal Z, Yahaya Z S.2014. Insecticidal activity and expression of cytochromeP450 family 4 genes in aedesalbopictus after exposure topyrethroid Mosquito coils. The Protein Journal, 33, 457-464Ay R, Yorulmaz S. 2010. Inheritance and detoxification enzymelevels in Tetranychus urticae Koch (Acari: Tetranychidae)strain selected with chlorpyrifos. Journal of Pest Science, 83, 85-93Bloch G, Shpigler H, Wheeler D E, Robinson, G E. 2009.Endocrine influences on the organization of insect societies.Hormones, 2, 1027-1068Bradford M M. 1976. A rapid sensitive method for thequantization of microgram quantities of protein utilizingthe principle of protein binding. Analytical Biochemistry,72, 248-254Bradfield J Y, Lee Y H, Keeley L L 1991. Cytochrome P450family 4 in a cockroach: Molecular cloning and regulationby regulation by hypertrehalosemic hormone. Proceedingsof the National Academy of Sciences of the United Statesof America, 88, 4558-4562Cornette R, Koshikawa S, Hojo M, Matsumoto T, Miura T. 2006.Caste-specific cytochrome P450 in the damp-wood termiteHodotermopsis sjostedti (Isoptera, Termopsidae). InsectMolecular Biology, 15, 235-244Drees B M. 2006. A new technique for laboratory assessmentof red imported fire ant mound drench treatments.Southwestern Entomologist, 27, 177-183Durham E W, Siegfried B D, Scharf M E. 2002. In vivo andin vitro metabolism of fipronil by larvae of the Europeancorn borer Ostrinia nubilalis. Pest Management Science,58, 799-804El-Latif A O A, Kranthi K R, KranthiS, Sarwar A, SubrahmanyamB. 2014. Overexpression of cytochrome P450 CYP6B7mediated pyrethroid resistance in Indian strains of the cottonbollworm, Helicoverpa armigera (Hübner). Journal of PlantProtection Research, 54, 287-293Festucci-Buselli R A, Carvalho-Dias A S, Oliveira-Andrade D,Caixeta-Nunes C, Li H M, Stuart J J, Muir W, Scharf M E,Pittendrigh B R. 2005. Expression of Cyp6g1 and Cyp12d1in DDT resistant and susceptible strains of Drosophilamelanogaster. Insect Molecular Biology, 14, 69-77Feyereisen R. 2005. Insect cytochrome P450. ComprehensiveMolecular Insect Science, 4, 1-77Gonzalez F J, Nebert D W. 1990. Evolution of the P450 genesuperfamily: Animal-plant ‘warfare’, molecular drive andhuman genetic differences in drug oxidation. Trends inGenetics, 6, 182-186Greenberg L, Reierson D, Rust M K. 2003. Fipronil trials inCalifornia against the red imported fire ant, Solenopsisinvicta Buren, using sugar water consumption andmound counts as measures of ant abundance. Journal ofAgricultural and Urban Entomology, 20, 221-233Guo Y, Zhang J, Ma E. 2014. Effect of sub-lethal doses ofchlorpyrifos on cytochrome P450 enzyme. Chinese Journalof Applied Entomology, 51, 702-707 (in Chinese)Harrison T L, Zangerl A R, Schuler M A, Berenbaum M R. 2001.Developmental variation in cytochrome P450 expressionin Papilio polyxenes in response to xanthotoxin, a hostplant allelochemical. Archives of Insect Biochemistry andPhysiology, 48, 179-189Huang C, Yao H, Ye G, Cheng J. 2006. Effects of sublethaldose of fipronil on detoxifying enzymes in the larvae of Chilosuppressalis and Sesamia inferens. Chinese Journal of RiceScience, 20, 447-450 (in Chinese)Hu X P, Song D L, Scherer C W. 2005. Transfer of indoxacarbamong workers of Coptotermes formosanus (Isoptera:Rhinotermitidae): effects of dose, donor: Recipient ratioand post-exposure time. Pest Management Science, 61,1209-1214Johnson R M, Pollock H S, Berenbaum M R 2009. Synergisticinteractions between in-hive miticides in Apis mellifera.Journal of Economic Entomology, 102, 474-479Johnson R M, Wen Z, Schuler M A, Berenbaum M R. 2006.Mediation of pyrethroid insecticide toxicity to honeybees (Hymenoptera: Apidae) by cytochrome P450monooxygenases. Journal of Economic Entomology, 99,1046-1050Kuriachan I, Vinson S B. 2000. A queen’s worker attractivenessinfluences her movement in polygynous colonies of the redimported fire ant (Hymenoptera: Formicidae) in responseto adverse temperatures. Environmental Entomology, 29,943-949Liu N, Li T, Reid W R, Yang T, Zhang L. 2011. Multiplecytochrome P450 genes: Their constitutive overexpressionand permethrin induction in insecticide resistant mosquitoes,Culex quinquefasciatus. PLoS One, 6, e23403.Liu N, Scott J G. 1998. Increased transcription of CYP6D1causes cytochrome P450-mediated insecticide resistancein house fly. Insect Biochemistry and Molecular Biology,28, 531-535Liu N, Zhang L. 2004. CYP4AB1, CYP4AB2, and Gp-9 geneoverexpression associated with workers of the red importedfire ant, Solenopsis invicta Buren. Gene, 327, 81-87Liu N, Zhu F. 2012. House fly ctyochrome P450s: Their rolein insecticide resistance and strategies in the isolation andcharacterization. In: Liu T X, Kang L, eds., Recent Advancesin Entomological Research. Springer, Berlin Heidelberg.pp. 246-257Liu X, Liang P, Gao X, Shi X. 2006. Induction of the cytochromeP450 activity by plant allelochemicals in the cotton bollworm,Helicoverpa armigera (Hübner). Pesticide Biochemistry andPhysiology, 84, 127-134Li X, Berenbaum M R, Schuler M A. 2002. Cytochrome P450and act in genes expressed in Helicoverpa zea andHelicoverpa armigera: paralogy/orthology identification,gene conversion and evolution. Insect Biochemistry andMolecular Biology, 32, 311-320Li X, Schuler M A, Berenbaum M R. 2007. Molecularmechanisms of metabolic resistance to synthetic and naturalxenobiotics. Annual Review of Entomology, 52, 231-253Loftin K, Hopkins J, Gavin J, Shanklin D. 2003. Evaluationof broadcast applications of various contact insecticidesagainst red imported fire ants, Solenopsis invicta Buren.Journal of Agricultural and Urban Entomology, 20, 151-156Lu K H, Bradfield J Y, Keeley L L. 1995. Hypertrehalosemichormone-regulated gene expression for cytochrome P4504C1 in the fat body of the cockroach, Blaberus discoidalis.Archives of Insect Biochemistry and Physiology, 28, 79-90Lu K H, Bradfield J Y, Keeley L L. 1999. Juvenile hormone inhibition of gene expression for cytochrome P4504C1 inadult females of the cockroach, Blaberusdis coidalis. InsectBiochemistry and Molecular Biology, 29, 667-673Mao W, Rupasinghe S G, Johnson R M, Zangerla A R, SchulerbM A, Berenbaum M R. 2009. Quercetin-metabolizingCYP6AS enzymes of the pollinator Apis mellifera(Hymenoptera: Apidae). Comparative Biochemistry andPhysiology Part B (Biochemistry and Molecular Biology),154, 427-434Mao W, Schuler M A, Berenbaum M R. 2011. CYP9Q-mediateddetoxification of acaricides in the honey bee (Apis mellifera).Proceedings of the National Academy of Sciences of theUnited States of America, 108, 12657-12662Marr B, Schiuma G. 2003. Business performance measurement- Past, present and future. Management Decision, 41,680-687Mata J, Marguerat S, Bähler J. 2005. Post-transcriptional controlof gene expression: a genome-wide perspective. Trends inBiochemical Sciences, 30, 506-514Morrison L W, Porter S D. 2003. Positive association betweendensities of the red imported fire ant, Solenopsis invicta(Hymenoptera: Formicidae), and generalized ant andarthropod diversity. Environmental Entomology, 32,548-554Nebert D W, Gonzalez F J. 1987. P450 genes: structure,evolution, and regulation. Annual Review of Biochemistry,56, 945-993Okey A B. 1990. Enzyme induction in the cytochrome P-450system. Pharmacology &Therapeutics, 45, 241-298Passera L, Aron S, Vargo E L, Keller L. 2001. Queen control ofsex ratio in fire ants. Science, 293, 1308-1310Pavek P, Dvorak Z. 2008. Xenobiotic-induced transcriptionalregulation of xenobiotic metabolizing enzymes of thecytochrome P450 superfamily in human extrahepatictissues. Current Drug Metabolism, 9, 129-143Pennisi E. 2001. Queens, not workers, rule the ant nest.Science, 293, 1239-1241Pfaffl M W. 2001. A new mathematical model for relativequantification in real-time RT-PCR. Nucleic Acids Research,29, e45-e45.Pilling E D, Bromleychallenor K A C, Walker C H, Jepson PC. 1995. Mechanism of synergism between the pyrethroidinsecticide λ-cyhalothrin and the imidazole fungicideprochloraz, in the honeybee (Apis mellifera L.). PesticideBiochemistry and Physiology, 51, 1-11Rakotondravelo M L, Anderson T D, Charlton R E, Zhu K Y.2006. Sublethal effects of three pesticides on activity ofselected target and detoxification enzymes in the aquaticmidge, Chironomus tentans (Diptera: Chironomidae).Archives of Environmental Contamination and Toxicology,51, 360-366Rao A, Vinson S B. 2004. Ability of resident ants to destructsmall colonies of Solenopsis invicta (Hymenoptera:Formicidae). Environmental Entomology, 33, 587-598Rose R L, Barbhaiya L, Roe R M, Rock G C, Hodgson E. 1995.Cytochrome P450-associated insecticide resistance andthe development of biochemical diagnostic assays inHeliothis virescens. Pesticide Biochemistry and Physiology,51, 178-191Saner C, Weibel B, Würgler F E, Sengstag C. 1996.Metabolism of promutagens catalyzed by Drosophilamelanogaster CYP6A2 enzyme in Saccharomycescerevisiae. Environmental and Molecular Mutagenesis,27, 46-58Scharf M E, Parimi S, Meinke L J, Chandler L D, Siegfried B D.2001. Expression and induction of three family 4 cytochromeP450 (CYP4) genes identified from insecticide-resistant andsusceptible western corn rootworms, Diabrotica virgiferavirgifera. Insect Molecular Biology, 10, 139-146Scott J G. 2008. Insect cytochrome P450s: thinking beyonddetoxification. Recent Advances in Insect Physiology,Toxicology and Molecular Biology, 1, 17-124Shang Q, Pan Y, Fang K, Xi J, Brennana J A. 2012. Biochemicalcharacterization of acetylcholinesterase, cytochrome P450and cross-resistance in an omethoate-resistant strain ofAphis gossypii Glover. Crop Protection, 31, 15-20Sutherland T D, Unnithan G C, Feyereisen R. 2000. Terpenoidω-hydroxylase (CYP4C7) messenger RNA levels in thecorpora allata: A marker for ovarian control of juvenilehormone synthesis in Diploptera punctata. Journal of InsectPhysiology, 46, 1219-1227Tang J, Li J, Shao Y, Yang B, Liu Z. 2010. Fipronil resistancein the whitebacked planthopper (Sogatella furcifera):possible resistance mechanisms and cross-resistance. PestManagement Science, 66, 121-125Tarver M R, Coy M R, Scharf M E. 2012. Cyp15F1: A novelcytochrome p450 gene linked to juvenile hormonedependentcaste differention in the termite reticulitermesflavipes. Archives of Insect Biochemistry and Physiology,80, 92-108Tay J W, Neoh K B, Lee C Y. 2014. The roles of the queen,brood, and worker castes in the colony growth dynamicsof the pharaoh ant Monomorium pharaonis (Hymenoptera:Formicidae). Myrmecological News, 20, 87-94Terriere L C .1983. Enzyme induction gene amplification, andinsect resistance to insecticides. In: Georghiou G P, SaitoT, eds., Pest Resistance to Pesticides. Plenum Press, NewYork. pp. 265-297Terriere L C. 1984. Induction of detoxication enzymes in insects.Annual Review of Entomology, 29, 71-88Tufts D M, Hunter W B, Bextine B. 2014. Solenopsis invictavirus (sinv-1) infection and insecticide interactions in thered imported fire ant (Hymenoptera: Formicidae). FloridaEntomologist, 97, 1251-1254Vinson S B. 1997. Invasion of the red imported fire ant(Hymenoptera: Formicidae ) spread, biology and impact.American Entomologist, 43, 23-39Wang L, Lu Y, Xu Y, Zeng L. 2013. The current status ofresearch on Solenopsis invicta Buren (Hymenoptera:Formicidae) in Mainland China. Journal of InvertebratePathology, 114, 1-6Wee C W, Lee S F, Robin C, Heckel D G. 2008. Identification of candidate genes for fenvalerate resistance in Helicoverpaarmigera using cDNA-AFLP. Insect Molecular Biology, 17,351-360Wu Y. 2011. Direct electrochemistry of cytochrome P450 6A1in mimic bio-membrane and its application for pesticidessensing. Sensors and Actuators (B Chemical),156,773-778Xie M, You M. 2011. Effects of fipronil on detoxifying enzymeactivity in Plutella xylostella. Chinese Journal of AppliedEntomology, 48, 1728-1733. (in Chinese)Yang X, Li X, Zhang Y. 2013. Molecular cloning and expressionof CYP9A61: Achlorpyrifos-ethyl and lambda-cyhalothrininduciblecytochrome P450 cDNA from Cydia pomonella.International Journal of Molecular Sciences, 14, 24211-24229Yang Y, Yue L, Chen S, Wu Y. 2008. Functional expressionof Helicoverpa armigera CYP9A12 and CYP9A14 inSaccharomyces cerevisiae. Pesticide Biochemistry andPhysiology, 92, 101-105Yu R, Guo Y, Ma E, Guo Y. 2012. Effect of sublethal dosesof malathion and carbaryl on the P450 genes of Locustamigratoria. Chinese Journal of Applied Entomology, 49,693-699. (in Chinese)Zhou J, Zhang G, Zhou Q. 2012. Molecular characterizationof cytochrome P450 CYP6B47 cDNAs and 5′-flankingsequence from Spodoptera litura (Lepidoptera: Noctuidae):Its response to lead stress. Journal of Insect Physiology,58, 726-736.Zhu F, Li T, Zhang L, Liu N. 2008. Co-up-regulation of threeP450 genes in response to permethrin exposure inpermethrin resistant house flies, Muscado mestica. 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