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Two novel cytochrome P450 genes CYP6CS1 and CYP6CW1 from Nilaparvata lugens (Hemiptera: Delphacidae): cDNA cloning and induction by host resistant rice

Published online by Cambridge University Press:  08 July 2010

Z. Yang ,
Y. Zhang ,
X. Liu  and
X. Wang
Z. Yang*
Affiliation:
College of Life Sciences, Hubei University, Wuhan 430062, China
Y. Zhang
Affiliation:
College of Life Sciences, Hubei University, Wuhan 430062, China
X. Liu
Affiliation:
College of Life Sciences, Hubei University, Wuhan 430062, China
X. Wang
Affiliation:
College of Life Sciences, Hubei University, Wuhan 430062, China
*
*Author for correspondence Fax: +86-27-87214327 E-mail: [email protected]
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Abstract

Two novel full-length P450 cDNAs, CYP6CS1 and CYP6CW1, were cloned from the fourth instar nymphs of brown planthopper Nilaparvata lugens Stål (Hemiptera: Delphacidae) reared on its susceptible rice variety Taichung Native 1 (TN1) plants. The deduced proteins are typical microsomal P450s sharing conserved structural and functional domains with other insect CYP6 members. Temporal expression analysis by northern blot hybridization indicated pre-exposure to N. lugens moderately resistant rice Minghui 63 (MH63) seedlings caused a time course-dependent induction of CYP6CS1 which peaked after 24 h of treatment; in contrast, CYP6CW1 was induced and remained at a constant time course from 0–72 h. CYP6CS1 and CYP6CW1 are dramatically induced in gut tissues and, slightly upregulated in carcass and fat bodies as revealed in spatial gene expression analysis. Whole mount in situ hybridizaion revealed that the two genes are expressed at a basal level in gut tissue and Malpighian tubules in nymphs fed with TN1 rice. After exposure to MH63, the expression of CYP6CW1 was found to be high in the whole gut, including Malpighian tubules. Expression of CYP6CS1 was significantly increased in midgut, and slightly increased in foregut, hindgut and Malpighian tubules. These data suggest a potential role of the two P450s in determining patterns of N. lugens-rice relationships through allelochemical detoxification.

Keywords

brown planthopperNilaparvata lugens (Hemiptera: Delphacidae)cytochrome P450 monooxygenasehost rice resistanceallelochemical detoxification
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 1 , February 2011 , pp. 73 - 80
Copyright
Copyright © Cambridge University Press 2010

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References

Berenbaum, M.R. (1999) Animal-plant warfare: molecular basis for cytochrome P450-mediated natural adaptation. pp. 553–571 in Puga, A. & Wallace, K.B. (Eds) Molecular Biology of the Toxic Response. Philadelphia, PA, Taylor & Francis Press.Google Scholar
Berenbaum, M.R., Cohen, M.B. & Schuler, M.A. (1992) Diversity among Insects. pp. 114–124 in Mullin, C.J. & Scott, J.G. (Eds) Molecular Basis of Insecticide Resistance. American Chemical Society Symposium Series 505, Washington, DC., ACS.Google Scholar
Chung, H., Sztal, T., Pasricha, S., Sridhar, M., Batterham, P. & Daborn, P.J. (2009) Characterization of Drosophila melanogaster cytochrome P450 genes. Proceedings of the National Academy of Sciences, USA 106, 5731–5736.Google Scholar
Cornette, R., Koshikawa, S., Hojo, M., Matsumoto, T. & Miura, T. (2006) Caste-specific cytochrome P450 in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae). Insect Molecular Biology 15(2), 235–244.CrossRefGoogle ScholarPubMed
Danielson, P.B., Macintyre, R.J. & Fogleman, J.C. (1997) Molecular cloning of a family of xenobiotic-inducible drosophilid cytochrome P450s: evidence for involvement in host-plant allelochemical resistance. Proceedings of the National Academy of Sciences, USA 94, 10797–10802.Google Scholar
Danielson, P.B., Foster, J.L.M., McMahill, M.M., Smith, M.K. & Fogleman, J.C. (1998) Induction by alkaloids and phenobarbital of Family 4 Cytochrome P450s in Drosophila: evidence for involvement in host plant utilization. Molecular and General Genetics 259, 54–59.Google Scholar
David, J.P., Boyera, S., Mesneaub, A., Ballc, A., Ransonc, H. & Dauphin-Villemant, C. (2006) Involvement of cytochrome P450 monooxygenases in the response of mosquito larvae to dietary plant xenobiotics. Insect Biochemistry and Molecular Biology 36, 410–420.CrossRefGoogle ScholarPubMed
Dow, J.A. & Davies, S.A. (2006) The Malpighian tubule: rapid insights from post-genomic biology. Journal of Insect Physiology 52, 365–378.CrossRefGoogle ScholarPubMed
Feyereisen, R. (2005) Insect cytochrome P450. pp. 1–77 in Gilbert, L.I., Iatrou, K. & Gill, S. (Eds) Comprehensive Insect Physiology, Biochemistry, Pharmacology and Molecular Biology. Amsterdam, Elsevier.Google Scholar
Fogleman, J.C., Danielson, P.B. & MacIntyre, R.J. (1998) The molecular basis of adaptation in Drosophila – The role of cytochrome P450s. Evolutionary Biology 30, 15–77.Google Scholar
Gong, M.Q., Gu, Y., Hu, X.B., Sun, Y., Ma, L., Li, X.L., Sun, L.X., Sun, J., Qian, J. & Zhu, C.L. (2005) Cloning and overexpression of CYP6F1, a cytochrome P450 gene, from deltamethrin-resistant Culex pipiens pallens. Acta Biochimica et Biophysica Sinica 37(5), 317–326.Google Scholar
Huang, C.H., Chang, W.L. & Chang, T.T. (1972) Ponlai varieties and Taichung Native 1. pp. 31–46 in Rice Breeding. Los Baños, Philippines, International Rice Research Institute.Google Scholar
Huang, S.M., Sun, D.B. & Brattsten, L.B. (2008) Novel cytochrome P450s, CYP6BB1 and CYP6P10, from the salt marsh mosquito Aedes sollicitans (Walker) (Diptera: Culicidae). Archives of Insect Biochemistry and Physiology 67, 139–154.Google Scholar
Kasai, S., Weerashinghe, I.S., Shono, T. & Yamakawa, M. (2000) Molecular cloning, nucleotide sequence and gene expression of a cytochrome P450 (CYP6F1) from the pyrethroid-resistant mosquito, Culex quinquefasciatus Say. Insect Biochemistry and Molecular Biology 30, 163–171.Google Scholar
Li, B., Bisgaard, H.C. & Forbes, V.E. (2004a) Identification and expression of two novel cytochrome P450 genes, belonging to CYP4 and a new CYP331 family, in the polychaete Capitella capitata sp.I. Biochemical and Biophysical Research Communications 325, 510–517.Google Scholar
Li, X., Baudry, J., Berenbaum, M.R. & Schuler, M.A. (2004b) Structural and functional evolution of insect CYP6B proteins: from specialist to generalist P450. Proceedings of the National Academy of Sciences, USA 101, 2939–2944.Google Scholar
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231–253.Google Scholar
Niu, G., Wen, Z., Rupasinghe, S.G., Zeng, R.S., Berenbaum, M.R. & Schuler, M.A. (2008) Aflatoxin B1 detoxification by CYP321A1 in Helicoverpa zea. Archives of Insect Biochemistry and Physiology 69, 32–45.Google Scholar
Ren, X., Weng, Q.M., Zhu, L.L. & He, G.C. (2004) Dynamic mapping of quantitative trait loci for resistance to brown planthopper in rice. Cereal Research Communications 32, 31–38.CrossRefGoogle Scholar
Rubia-Sanchez, E., Suzuki, Y., Miyamoto, K. & Watanabe, T. (1999) The potential for compensation of the effects of the brown planthopper Nilaparvata lugens Stål. (Homoptera: Delphacidae) feeding on rice. Crop Protection 18, 39–45.CrossRefGoogle Scholar
Sasabe, M., Wen, Z., Berenbaum, M.R. & Schuler, M.A. (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.Google Scholar
Scott, J.G. & Wen, Z. (2001) Cytochrome P450 of insects: the tip of the iceberg. Pest Management Science 57, 958–967.Google Scholar
Senger, K., Harris, K. & Levine, M. (2006) GATA factors participate in tissue-specific immune responses in Drosophila larvae. Proceedings of the National Academy of Sciences, USA 103, 15957–15962.CrossRefGoogle ScholarPubMed
Snyder, M.J., Stevens, J.L., Andersen, J.F. & Feyereisen, R. (1995) Expression of cytochrome P450 genes of the CYP4 family in midgut and fat body of the tobacco hornworm Manduca sexta. Archives of Biochemistry and Biophysics 321, 13–20.Google Scholar
Stevens, J.L., Snyder, M.J., Koener, J.F. & Feyereisen, R. (2000) Inducible P450s of the CYP9 family from larval Manduca sexta midgut. Insect Biochemistry and Molecular Biology 30, 559–568.Google Scholar
Terra, W.R. & Ferreira, C. (2005) pp. 171–244. in Gilbert, L.I.Iatrou, K. & Gill, S. (Eds) Comprehensive Molecular Insect Science. Amsterdam, Elsevier.CrossRefGoogle Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.Google Scholar
Tzou, P., Ohresser, S., Ferrandon, D., Capovilla, M., Reichhart, J.M., Lemaitre, B., Hoffmann, J.A. & Imler, J.L. (2000) Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13, 737–748.CrossRefGoogle ScholarPubMed
Wigglesworth, V.B. (1972) The Principles of Insect Physiology, 7th edn. London, Chapman & Hall.Google Scholar
Yang, Z.F., Yang, H.Y. & He, G.C. (2007) Cloning and characterization of two cytochrome P450 CYP6AX1 and CYP6AY1 cDNAs from Nilaparvata lugens Stål (Homoptera: Delphacidae). Archives of Insect Biochemistry and Physiology 64, 88–99.Google Scholar
Zhou, X.J., Ma, C.X., Li, M., Sheng, C.F., Liu, H.X. & Qiu, X.H. (2010) CYP9A12 and CYP9A17 in the cotton bollworm, Helicoverpa armigera: sequence similarity, expression profile and xenobiotic response. Pest Management Science 66, 65–73.Google Scholar