Scientia Agricultura Sinica ›› 2015, Vol. 48 ›› Issue (19): 3857-3865.doi: 10.3864/j.issn.0578-1752.2015.19.008

• PLANT PROTECTION • Previous Articles     Next Articles

Tissue Specific Expression of Genes Encoding Detoxification Enzymes in the Larvae of Bactrocera dorsalis Under β-Cypermethrin Stress

SHEN Guang-mao1, WANG Xiao-na2, HUANG Yong1, DOU Wei1, WANG Jin-jun1   

  1. 1College of Plant Protection, Southwest University/Key Laboratory of Entomology and Pest Control Engineering, Chongqing 400715
    2Flower Garden Management Office of Chongqing, Chongqing 401147
  • Received:2015-04-17 Online:2015-10-01 Published:2015-10-01

Abstract: 【Objective】Based on the transcriptome data of Bactrocera dorsalis, the aim of this study is to systematically analyze the expression of genes in larvae encoding detoxification enzymes under β-cypermethrin exposure, identify important detoxification genes, and focus on the discussion of biological significance of tissue specific expression of these genes. 【Method】 The expressions of 30 detoxification genes in the whole body of larvae, midgut, and fat body were detected under β-cypermethrin exposure by using qPCR.【Result】Under the stress of β-cypermethrin, the qPCR results of 8 GSTs genes showed that the mRNA levels of 4 Delta class genes significantly increased. The expressions of genes from Delta class were up-regulated to 5.6-32.5 folds in the midgut and fat body, but the expressions of other GST genes did not show very active reaction when exposed to β-cypermethrin. Meanwhile, although the expressions of Delta class GSTs genes significantly increased in midgut and fat body, the expression changes of these genes were not so apparent in the whole body. As for the 6 CCEs genes, their expressions were up-regulated in some degree in the whole body, and α-E3 was up-regulated to 4.1 folds. However, in the midgut and fat body, the expressions of these genes did not increase significantly. The qPCR results of 16 P450s genes showed that the expressions of most P450s genes were up-regulated, especially the genes from CYP4 and CYP6 families. In CYP4 family, the expressions of CYP4D47 (midgut), CYP4E9 (whole body and fat body), CYP4P5 (whole body and fat body) were highly up-regulated. The expression of CYP4AD1 increased in some degree in the midgut and fat body, but no significant changes were found in the whole body. CYP4S18 and CYP4AC4 did not show any positive reaction or their expression changes were not apparent. In CYP6 family, the expressions of CYP6A48 and CYP6A41 had a significant increase in the fat body, 18.0 and 9.6 folds up-regulated, respectively. The expression of others like CYP6G6 and CYP6A50 also increased. The expression of CYP6EK1 was up-regulated by 4.8 folds in the whole body, but did not change in midgut and fat body. The expressions of the other genes, such as CYP12C2, CYP12N1, CYP9F6, and CYP309B1 also significantly increased in the fat body when exposed to β-cypermethrin. But the expression of CYP317B1 did not change under the stress.【Conclusion】When under the stress of β-cypermethrin, the detoxification genes in B. dorsalis larvae were highly enriched in midgut and fat body, but showed a balance in the whole body. It suggests that when under the toxic stress, the pests may have special strategy for efficient use and proper distribution of energy, which increase the energy efficiency to decrease the extra energy cost to resist the damage of exogenous toxin. This kind of strategy might be an important acclimation of insects to avoid fitness cost when under the environmental pressures.

Key words: Bactrocera dorsalis, GSTs, P450s, CCEs, toxic stress, tissue specificity

[1]    Le Goff G, Hilliou F, Siegfried B D, Boundy S, Wajnberg E, Sofer L, Audant P, ffrench-Constant R H, Feyereisen R. Xenobiotic response in Drosophila melanogaster: Sex dependence of P450 and GST gene induction. Insect Biochemistry and Molecular Biology, 2006, 36(8): 674-682.
[2]    Montella I R, Schama R, Valle D. The classification of esterases: an important gene family involved in insecticide resistance-A review. Memorias do Instituto Oswaldo Cruz, 2012, 107(4): 437-449.
[3]    Li X C, Schuler M A, Berenbaum M R. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 2007, 52(1): 231-253.
[4]    Zhang L, Gao X, Liang P. Beta-cypermethrin resistance associated with high carboxylesterase activities in a strain of house fly, Musca domestica (Diptera: Muscidae). Pesticide Biochemistry and Physiology, 2007, 89(1): 65-72.
[5]    Jin T, Zeng L, Lin Y Y, Lu Y Y, Liang G W. Insecticide resistance of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in mainland China. Pest Management Science, 2011, 67(3): 370-376.
[6]    Hsu J C, Wu W J, Haymer D S, Liao H Y, Feng H T. Alterations of the acetylcholinesterase enzyme in the oriental fruit fly Bactrocera dorsalis are correlated with resistance to the organophosphate insecticide fenitrothion. Insect Biochemistry and Molecular Biology, 2008, 38(2): 146-154.
[7]    Hsu J C, Feng H T, Wu W J, Geib S M, Mao C H, Vontas J. Truncated transcripts of nicotinic acetylcholine subunit gene Bdα6 are associated with spinosad resistance in Bactrocera dorsalis. Insect Biochemistry and Molecular Biology, 2012, 42(10): 806-815.
[8]    Hu F, Dou W, Wang J J, Jia F X, Wang J J. Multiple glutathione S-transferase genes: identification and expression in oriental fruit fly, Bactrocera dorsalis. Pest Management Science, 2013, 70(2): 295-303.
[9]    Huang Y, Shen G M, Jiang H B, Jiang X Z, Dou W, Wang J J. Multiple P450 genes: Identification, tissue-specific expression and their responses to insecticide treatments in the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidea). Pesticide Biochemistry and Physiology, 2013, 106(1): 1-7.
[10]   申光茂, 豆威, 王进军. 橘小实蝇羧酸酯酶基因BdCAREB1的克隆及其表达模式解析. 中国农业科学, 2014, 47(10): 1947-1955.
Shen G M, Dou W, Wang J J. ?Cloning and expression analysis of a carboxylesterase gene BdCAREB1 from Bactrocera dorsalis. Scientia Agricultura Sinica, 2014, 47(10): 1947-1955. (in Chinese)
[11]   Shen G M, Dou W, Niu J Z, Jiang H B, Yang W J, Jia F X, Hu F, Cong L, Wang J J. Transcriptome analysis of the oriental fruit fly (Bactrocera dorsalis). PLoS One, 2011, 6(12): e29127.
[12]   Shen G M, Dou W, Huang Y, Jiang X Z, Smagghe G, Wang J J. In silico cloning and annotation of genes involved in the digestion, detoxification and RNA interference mechanism in the midgut of Bactrocera dorsalis [Hendel (Diptera: Tephritidae)]. Insect Molecular Biology, 2013, 22(4): 354-365.
[13]   Shen G M, Huang Y, Jiang X Z, Dou W, Wang J J. Effect of β-cypermethrin exposure on the stability of nine housekeeping genes in Bactrocera dorsalis (Diptera: Tephritidae). Florida Entomologist, 2013, 96(2): 442-450.
[14]   Shen G M, Jiang H B, Wang X N, Wang J J. Evaluation of endogenous references for gene expression profiling in different tissues of the oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae). BMC Molecular Biology, 2010, 11(1): 76.
[15]   Qin G H, Liu T X, Guo Y P, Zhang X Y, Ma E B, Zhang J Z. Effects of chlorpyrifos on glutathione S-transferase in migratory locust, Locusta migratoria. Pesticide Biochemistry and Physiology, 2014, 109(6): 1-5.
[16]   Zhou W W, Li X W, Quan Y H, Cheng J, Zhang C X, Gurr G, Zhu Z R. Identification and expression profiles of nine glutathione S-transferase genes from the important rice phloem sap-sucker and virus vector Laodelphax striatellus (Fallen) (Hemiptera: Delphacidae). Pest Management Science, 2012, 68(9): 1296-1305.
[17]   Wang S P, He G L, Chen R R, Li F, Li G Q. The involvement of cytochrome P450 monooxygenases in methanol elimination in Drosophila melanogaster larvae. Archives of Insect Biochemistry and Physiology, 2012, 79(4/5): 264-275.
[18]   Wang J J, Wei D, Dou W, Hu F, Liu W F, Wang J J. Toxicities and synergistic effects of several insecticides against the oriental fruit fly (Diptera: Tephritidae). Journal of Economic Entomology, 2013, 106(2): 970-978.
[19]   Sheehan D, Meade G, Foley V M, Dowd C A. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochemical Journal, 2001, 360(1): 1-16.
[20]   Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, Sharakhova M V, Unger M F, Collins F H, Feyereisen R. Evolution of supergene families associated with insecticide resistance. Science, 2002, 298(5591): 179-181.
[21]   Willoughby L, Chung H, Lumb C, Robin C, Batterham P, Daborn P J. A comparison of Drosophila melanogaster detoxification gene induction responses for six insecticides, caffeine and phenobarbital. Insect Biochemistry and Molecular Biology, 2006, 36(12): 934-942.
[22]   Liu N, Li T, Reid W R, Yang T, Zhang L. Multiple cytochrome P450 genes: their constitutive overexpression and permethrin induction in insecticide resistant mosquitoes, Culex quinquefasciatus. PLoS One, 2011, 6(8): e23403.
[23]   Zhang L, Shi J, Shi X, Liang P, Gao J, Gao X. Quantitative and qualitative changes of the carboxylesterase associated with beta- cypermethrin resistance in the housefly, Musca domestica (Diptera: Muscidae). Comparative Biochemistry and Physiology: Part B, 2010, 156(1): 6-11.
[24]   Kakani E G, Bon S, Massoulie J, Mathiopoulos K D. Altered GPI modification of insect AChE improves tolerance to organophosphate insecticides. Insect Biochemistry and Molecular Biology, 2011, 41(3): 150-158.
[25]   Karban R, Agrawal A A. Herbivore offense. Annual Review of Ecology and Systematics, 2002, 33: 641-664.
[26]   Castañeda L E, Figueroa C C, Fuentes-Contreras E, Niemeyer H M, Nespolo R F. Physiological approach to explain the ecological success of ‘superclones’ in aphids: Interplay between detoxification enzymes, metabolism and fitness. Journal of Insect Pathology, 2010, 56(9): 1058-1064.
[27]   Silva L, Reis A, Pereira E, Oliveira M, Guedes R. Altered cysteine proteinase activity in insecticide-resistant strains of the maize weevil: Purification and characterization. Comparative Biochemistry and Physiology: Part B, 2010, 157(1): 80-87.
[28]   Ahmed S, Wilkins R M, Mantle D. Comparison of proteolytic enzyme activities in adults of insecticide resistant and susceptible strains of the housefly M. domestica L. Insect Biochemistry and Molecular Biology, 1998, 28(9): 629-639.
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