Novel cytochrome P450 Genes, CYP6EB1 and CYP6EC1, are over-expressed in acrinathrin-resistant Frankliniella occidentalis (Thysanoptera: Thripidae)

Journal of Economic Entomology

Volumn 105, Issue 3, 2012, Pages 1006-1018

  Cifuentes, D ^a   Chynoweth, R ^a   Guillen J ^a   De La Rua P ^b   Bielza, P ^a  

^a TECHNICAL UNIVERSITY OF CARTAGENA   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

acrinathrin; cytochrome P450; insecticide resistance; overexpression; Western flower thrip

Indexed keywords

ACRINATHRIN; CYTOCHROME P450; INSECTICIDE; PYRETHROID;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; DNA SEQUENCE; ENZYMOLOGY; GENE EXPRESSION; GENETICS; INSECTICIDE RESISTANCE; LARVA; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; THYSANOPTERA;

AMINO ACID SEQUENCE; ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION; INSECTICIDE RESISTANCE; INSECTICIDES; LARVA; MOLECULAR SEQUENCE DATA; PYRETHRINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; THYSANOPTERA;

EID: 84862229804     PISSN: 00220493     EISSN: None     Source Type: Journal    
DOI: 10.1603/EC11335     Document Type: Article

References (68)

1. Amenya, D. A., L. L. Koekemoer, A. Vaughan, J. C. Morgan, B. D. Brooke, R. H. Hunt, H. Ranson, J. Hemingway, and M. Coetzee. 2005. Isolation and sequence analysis of P450 genes from a pyrethroid resistant colony of the major malaria vector Anopheles funestus. DNA Sequence 16: 437-445.
2. Amenya, D. A., R. Naguran, T.C.M. Lo, H. Ranson, B. L. Spillings, O. R. Wood, B. D. Brooke, M. Coetzee, and L. L. Koekemoer. 2008. Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles funestus, resistant to pyrethroids. Insect Mol. Biol. 17: 19-25.
3. Baek, J. H., J. M. Clark, and S. H. Lee. 2010. Cross-strain comparison of cypermethrin-induced cytochrome P450 transcription under different induction conditions in diamondback moth. Pest Biochem. Physiol. 96: 43-50.
4. Bautista, M.A.M., T. Tanaka, and T. Miyata. 2007. Identification of permethrin-inducible cytochrome P450s from the diamondback moth, Plutella xylostella (L.) and the possibility of involvement in permethrin resistance. Pestic. Biochem. Physiol. 87: 85-93.
5. Bielza, P. 2008. Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag. Sci. 64: 1131-1138.
6. Bielza, P., V. Quinto, E. Fernández, C. Grávalos, and J. Contreras. 2007. Genetics of spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae). J. Econ. Entomol. 100: 916-920.
7. Bielza, P., V. Quinto, E. Fernández, C. Grávalos, J. Abellán, and D. Cifuentes. 2008. Inheritance of resistance to acrinathrin in Frankliniella occidentalis (Thysanoptera: Thripidae). Pest Manag. Sci. 64: 584-588.
8. Bielza, P., V. Quinto, J. Contreras, M. Torné, A. Martín, and P. J. Espinosa. 2007a. Resistance to spinosad in the western flower thrips, Frankliniella occidentalis (Pergande), in greenhouses of south-eastern Spain. Pest Manag. Sci. 63: 682-687.
9. Brandt, A., M. Scharf, J. H. Pedra, G. Holmes, A. Dean, M. Kreitman, and B. R. Pittendrigh. 2002. Differential expression and induction of two Drosophila cytochrome P450 genes near the Rst(2)DDT locus. Insect Mol. Biol. 11: 337-341.
10. Cariño, F. A., J. F. Koener, F. W. Plapp, and R. Feyereisen. 1994. Constitutive overexpression of the cytochrome P450 gene CYP6A1 in a house fly strain with metabolic resistance to insecticides. Insect Biochem. Mol. Biol. 24: 411-418.
11. Chen, S., Y. Yang, and Y. Wu. 2005. Correlation between fenvalerate resistance and cytochrome P450 mediated O-demethylation activity in Helicoverpa armigera (Lepidoptera, Noctuidae). J. Econ. Entomol. 98: 943-946.
12. Cohen, M. B., and R. Feyereisen. 1995. A cluster of cytochrome P450 genes of the CYP6 family in the house fly. DNA Cell Biol. 14: 73-82.
13. Contreras, J., D. Moreno, M. D. Hernández, P. Bielza, and A. Lacasa. 2001. Preliminary study on insecticide resistance in Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in sweet pepper crops in Campo de Cartagena (Murcia), SE of Spain. Acta Hortic. 559: 745-752.
14. Contreras, J., P. J. Espinosa, V. Quinto, C. Grávalos, E. Fernández, and P. Bielza. 2008. Stability of insecticide resistance in Frankliniella occidentalis to acrinathrin, formetanate and methiocarb. Agric. For. Entomol. 10: 273-278.
15. Contreras, J., P. J. Espinosa, V. Quinto, J. Abellán, C. Grávalos, E. Fernández, and P. Bielza. 2010. Life-stage variation in insecticide resistance of the Western Flower Thrips (Thysanoptera: Thripidae). J. Econ. Entomol. 103: 2164-2168. (doi:10.1603/EC09391).
16. Danielson, P. B., J.L.M. Foster, S. K. Cooper, and J. C. Fogleman. 1999. Diversity of expressed cytochrome P450 genes in Ceratitis capitata. Insect Mol. Biol. 8: 149-159.
17. David, J. P., C. Strode, J. Vontas, D. Nikou, A. Vaughan, P. M. Pignatelli, C. Louis, J. Hemingway, and H. Ranson. 2005. The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proc. Natl. Acad. Sci. U.S.A. 102: 4080-4084.
18. Espinosa, P. J., J. Contreras, V. Quinto, C. Grávalos, E. Fernández, and P. Bielza. 2005. Metabolic mechanisms of insecticide resistance in the western flower thrips, Frankliniella occidentalis (Pergande). Pest Manag. Sci. 61: 1009-1015.
19. Espinosa, P. J., P. Bielza, J. Contreras, and A. Lacasa. 2002a. Field and laboratory selection of Frankliniella occidentalis (Pergande) for resistance to insecticides. Pest Manag. Sci. 58: 920-927.
20. Espinosa, P. J., P. Bielza, J. Contreras, and A. Lacasa. 2002b. Insecticide resistance in field populations of Frankliniella occidentalis (Pergande) in Murcia (south-east Spain). Pest Manag. Sci. 58: 967-971.
21. Feyereisen, R. 1999. Insect P450 enzymes. Annu. Rev. Entomol. 44: 507-533.
22. Gandhi, R., E. Varak, and M. L. Goldbergh. 1992. Molecular analysis of a cytochrome P450 gene of family 4 on the Drosophila X chromosome. DNA Cell Biol. 11: 397-404.
23. Grubor, V. D., and D. G. Heckel. 2007. Evaluation of the role of CYP6B cytochrome P450s in pyrethroid resistant Australian Helicoverpa armigera. Insect Mol. Biol. 16: 15-23.
24. Hardstone, M. C., C. Leichter, L. C. Harrington, S. Kasai, T. Tomita, and J. G. Scott. 2007. Cytochrome P450 monooxygenase-mediated permethrin resistance confers limited and larval specific cross-resistance in the southern house mosquito, Culex pipiens quinquefasciatus. Pestic. Biochem. Physiol. 89: 175-184.
25. Huang, S., D. Sun, and L. B. Brattsten. 2008. Novel cytochrome P450s, CYP6BB1 and CYP6P10, from the salt marsh mosquito Aedes sollicitans (Walker) (Diptera, Culicidae). Arch. Insect Biochem. Physiol. 67: 139-154.
26. Huber, D.P.W., M. L. Erickson, C. M. Leutenegger, J. Bohlmann, and S. J. Seybold. 2007. Isolation and extreme sex-specific expression of cytochrome P450 genes in the bark beetle, Ips paraconfusus, following feeding on the phloem of host ponderosa pine, Pinus ponderosa. Insect Mol. Biol. 16: 335-349.
27. Jensen, S. E. 2000. Insecticide resistance in the western flower thrips, Frankliniella occidentalis. Integrated Pest Manag. Rev. 5: 131-146.
28. Karunker, I., J. Benting, B. Lueke, T. Ponge, R. Nauen, E. Roditakis, J. Vontas, K. Gorman, I. Denholm, and S. Morin. 2008. Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochem. Mol. Biol. 38: 634-644.
29. Kimura, M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111-120.
30. Kranthi, K. R., D. Jadhav, R. Wanjari, S. Kranthi, and D. Russell. 2001. Pyrethroid resistance and mechanisms of resistance in field strains of Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 94: 253-263.
31. Li, H., H. Dai, and H. Wei. 2005. Molecular cloning and nucleotide sequence of CYP6BF1 from the diamondback moth, Plutella xylostella. J. Insect Sci. 5: 45.
32. Liu, N., and J. G. Scott. 1996. Genetic analysis of factors controlling elevated cytochrome P450, CYP6D1, cytochrome b5, P450 reductase and monooxygenase activities in LPR house flies, Musca domestica. Biochem. Genet. 34: 133-148.
33. Marcombe, S., R. Poupardin, F. Darriet, S. Reynaud, J. Bonnet, C. Strode, C. Brengues, A. Yébakima, H. Ranson, V. Corbel, and J. P. David. 2009. Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics 10: 494-508.
34. Martin, T., O. G. Ochou, M. Vaissayre, and D. Fournier. 2003. Oxidases responsible for resistance to pyrethroids sensitize Helicoverpa armigera (Hübner) to triazophos in West Africa. Insect Biochem. Mol. Biol. 33: 883-887.
35. Nauen, R., P. Bielza, I. Denholm, and K. Gorman. 2008. Age-specific expression of resistance to a neonicotinoid insecticide in the whitefly Bemisia tabaci. Pest Manag. Sci. 64: 1106-1110.
36. Nikou, D., H. Ranson, and J. Hemingway. 2003. An adult-specific CYP6 P450 gene is overexpressed in a pyrethroid-resistant strain of the malaria vector, Anopheles gambiae. Gene 318: 91-102.
37. Pedra, J. H., L. M. McIntyre, M. E. Scharf, and B. R. Pittendrigh. 2004. Genome-wide transcription profile of field and laboratory selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proc. Natl. Acad. Sci. U.S.A. 101: 7034-7039.
38. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: 2002-2007.
39. Pfaffl, M. W., G. W. Horgan, and L. Dempfle. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30: 9.1 e 36.
40. Pittendrigh, B., K. Aronstein, E. Zinkovsky, O. Andreev, B. Campbell, J. Daly, S. Trowell, and R. H. ffrench-Constant. 1997. Cytochrome P450 genes from Helicoverpa armigera, expression in a pyrethroid susceptible and resistant strain. Insect Biochem. Mol. Biol. 27: 507-512.
41. Poupardin, R., M. A. Riaz, J. Vontas, J. P. David, and S. Reynaud. 2010. Transcription profiling of eleven cytochrome P450s potentially involved in xenobiotic metabolism in the mosquito Aedes aegypti. Insect Mol. Biol. 19: 185-193.
42. Qiu, X. H., W. Li, and X. F. Leng. 2001. Cytochrome P450 monooxygenases in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae): in vivo effects of deltamethrin exposure. J. Agric. Urban Entomol. 18: 217-225.
43. Ranasinghe, C., and A. A. Hobbs. 1998. Isolation and characterization of two cytochrome P450 cDNA clones for CYP6B6 and CYP6B7 from Helicoverpa armigera (Hubner): possible involvement of CYP6B7 in pyrethroid resistance. Insect Biochem. Mol. Biol. 28: 571-580.
44. 5 mRNAs from Helicoverpa armigera (Hubner) by pyrethroid insecticides in organ culture. Insect Mol. Biol. 8: 443-447.
45. 5 in cytochrome P450 CYP6B7 activity towards pyrethroids. Insect Biochem. Mol. Biol. 29: 145-151.
46. Ranasinghe, C., M. Headlam, and A. A. Hobbs. 1997. Induction of the mRNA for CYP6B2, a pyrethroid inducible cytochrome P450, in Helicoverpa armigera (Hubner) by dietary monoterpenes. Arch. Insect Biochem. Physiol. 34: 99-109.
47. Rongnoparut, P., S. Boonsuepsakul, T. Chareonviriyaphap, and N. Thanomsing. 2003. Cloning of cytochrome P450, CYP6P5 and CYP6AA2 from Anopheles minimus resistant to deltamethrin. J. Vec. Ecol. 28: 150-158.
48. Rose, R. L., D. Goh, D. M. Thompson, K. D. Verma, D. G. Heckel, L. J. Gahan, R. M. Roe, and E. Hodgson. 1997. Cytochrome P450 (CYP) 9A1 in Heliothis virescens, the first member of a new CYP family. Insect Biochem. Mol. Biol. 27: 605-615.
49. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
50. Sasabe, M., Z. Wen, M. R. Berenbaum, and M. A. Schuler. 2004. Molecular analysis of CYP321A1, a novel cytochrome P450 involved in metabolism of plant allelochemicals (furanocoumarins) and insecticides (cypermethrin) in Helicoverpa zea. Gene 338: 163-175.
51. Sato, M. E., T. Tanaka, and T. Miyata. 2007. A cytochrome P450 gene involved in methidathion resistance in Amblyseius womersleyi Schicha (Acari, Phytoseiidae). Pestic. Biochem. Physiol. 88: 337-345.
52. Scharf, M. E., B. D. Siegfried, L. J. Meinke, R. J. Wright, and L. D. Chandler. 2000. Cytochrome P450-mediated N-demethylation activity and induction in insecticide-resistant and susceptible western corn rootworm populations. Pestic. Biochem. Physiol. 67: 137-143.
53. Scharf, M. E., S. Parimi, L. J. Meinke, L. D. Chandler, and B. D. Siegfried. 2001. Expression and induction of three family 4 cytochrome P450 (CYP4) genes identified from insecticide resistant and susceptible western corn rootworms, Diabrotica virgifera virgifera. Insect Mol. Biol. 10: 139-146.
54. Scott, J. G. 1999. Molecular basis of insecticide resistance: cytochromes P450. Insect Biochem. Mol. Biol. 29: 757-777.
55. Scott, J. G., and S. Kasai. 2004. Evolutionary plasticity of monooxygenase-mediated resistance. Pestic. Biochem. Physiol. 78: 171-178.
56. Snyder, M. J., J. L. Stevens, J. F. Andersen, and R. Feyereisen. 1995. Expression of cytochrome P450 genes of the CYP4 family in midgut and fat body of the tobacco hornworm, Manduca sexta. Arch Biochem. Biophys. 321: 13-20.
57. Strode, C., C. S. Wondji, J. P. David, N. J. Hawkes, N. Lumjuan, D. R. Nelson, D. R. Drane, S.H.P. Parakrama Karunaratne, J. Hemingway, W. C. Black, IV, and H. Ranson. 2008. Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 38: 113-123.
58. Strode, C., K. Steen, F. Ortelli, and H. Ranson. 2006. Differential expression of the detoxification genes in the different life stages of the malaria vector Anopheles gambiae. Insect Mol. Biol. 15: 523-530.
59. Sutherland, T. D., G. C. Unnithan, J. F. Andersen, P. H. Evans, M. B. Murataliev, L. Z. Szabo, E. A. Mash, W. S. Bowers, and R. Feyereisen. 1998. A cytochrome P450 terpenoid hydroxylase linked to the suppression of insect juvenile hormone synthesis. Proc. Natl. Acad. Sci. U.S.A. 95: 12884-12889.
60. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4, Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
61. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
62. Winter, J., G. Bilbe, H. Richener, B. Sehringer, and H. Kayser. 1999. Cloning of a cDNA encoding a novel cytochrome P450 from the insect Locusta migratoria, CYP6H1, a putative ecdysone 20-hydroxylase. Biochem. Biophys. Res. Commun. 259: 305-310.
63. Wu, J., P. J. Zhuang, and Z. H. Tang. 1999. CYP6B2 expression in insecticide resistant and susceptible strains of Helicoverpa armigera. Acta Biochem. Biophys. Sinica. 31: 101-103.
64. Xiao-Ping, W., and A. A. Hobbs. 1995. Isolation and sequence analysis of a cDNA clone for a pyrethroid inducible cytochrome P450 from Helicoverpa armigera. Insect Biochem. Mol. Biol. 25: 1001-1009.
65. Xu, Y. Q., J. J. Wang, H. B. Jiang, W. Dou, P. Tang, and F. M. An. 2009. Identification, characterization, and expression of P450 gene encoding CYP6BQ13v2 from the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Agric. Sci. China 8: 1210-1218.
66. Yang, Y., S. Chen, S. Wu, L. Yue, and Y. Wu. 2006. Constitutive overexpression of multiple cytochrome P450 genes associated with pyrethroid resistance in Helicoverpa armigera. J. Econ. Entomol. 99: 1784-1789.
67. Zhu, Y. C., and G. L. Snodgrass. 2003. Cytochrome P450 CYP6X1 cDNAs and mRNA expression levels in three strains of the tarnished plant bug Lygus lineolaris (Heteroptera, Miridae) having different susceptibilities to pyrethroid insecticide. Insect Mol. Biol. 12: 39-49.
68. Zhuang, H. M., K. F. Wang, L. Zheng, Z. J. Wu, T. Miyata, and G. Wu. 2011. Identification and characterization of a cytochrome P450 CYP6CX1 putatively associated with insecticide resistance in Bemisia tabaci. Insect Sci. 18: 484-494. (doi:10.1111/j.1744-7917.2010.01380.x).