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Effects of dietary quercetin on performance and cytochrome P450 expression of the cotton bollworm, Helicoverpa armigera

Published online by Cambridge University Press:  06 October 2015

D. Liu
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China
Y. Yuan
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
M. Li
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
X. Qiu*
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China
*
*Author for correspondence Phone: 86 -10-64807231 Fax: +86-10-64807099 E-mail: [email protected]

Abstract

Quercetin is ubiquitous in terrestrial plants. The cotton bollworm Helicoverpa armigera as a highly polyphagous insect has caused severe crop losses. Until now, interactions between this pest and quercetin are poorly understood at the biochemical and molecular levels. In this study, we investigated the in vivo effects of quercetin on performance of cotton bollworm and on cytochrome P450 (P450) expression. Deleterious effects of quercetin on the performance of the cotton bollworm, including growth, survival, pupation and adult emergence were observed after oral administration of 3 and 10 mg g−1 quercetin to larvae since the third instar, whereas no significant toxic effect was found at 0.1 mg g−1 quercetin treatment. Piperonyl butoxide treatment enhanced the toxicity of quercetin. In vitro metabolism studies showed that quercetin was rapidly transformed by gut enzymes of fifth instar larvae of the cotton bollworm. qRT–PCR results revealed that the effect of quercetin on P450 expression was tissue- and dose-specific. Quercetin regulated P450 expression in a mild manner, and it could serve as P450 inducer (CYP337B1, CYP6B6) or repressor (CYP337B1, CYP6B7, CYP6B27, CYP9A14, CYP6AE11, and CYP4M7). These findings are important for advancing our understanding of the biochemical and molecular response of insects to plant toxins and have implications for a smart pest control.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2015 

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References

Aboshi, T., Ishida, M., Matsushita, K., Hirano, Y., Nishida, R. & Mori, N. (2014) Stage-specific quercetin sulfation in the gut of Mythimna separata larvae (Lepidoptera: Noctuidae). Bioscience, Biotechnology and Biochemistry 78(1), 3840.Google Scholar
Bai, L., Sun, H., Sun, Y. & Su, C. (1997) Studies on the host plant species and their fitness to cotton bollworm. Acta Phytophylacica Sinica 24(1), 16.Google Scholar
Biesaga, M. & Pyrzynska, K. (2009) Analytical procedures for determination of quercetin and its glycosides in plant material. Critical Reviews in Analytical Chemistry 39(2), 95107.Google Scholar
Brun-Barale, A., Héma, O., Martin, T., Suraporn, S., Audant, P., Sezutsu, H. & Feyereisen, R. (2010) Multiple P450 genes overexpressed in deltamethrin-resistant strains of Helicoverpa armigera . Pest Management Science 66, 900909.Google Scholar
Chen, F.J., Zhang, C.Z. & Gao, X.W. (2007) In vitro inhibition of glutathione S-transferases by several insecticides and allelochemicals in cotton bollworm, Helicoverpa armigera Hubner. Journal of Entomological Science 42(2), 296305.CrossRefGoogle Scholar
Elliger, C.A., Chan, B.C. & Waiss, A.C. (1980) Flavonoids as larval growth inhibitors. Naturwissenschaften 67(7), 358360.Google Scholar
Ferreres, F., Fernandes, F., Pereira, D.M., Pereira, J.A., Valentao, P. & Andrade, P.B. (2009) Phenolics metabolism in insects: Pieris brassicae-Brassica oleracea var. costata Ecological Duo. Journal of Agricultural and Food Chemistry 57(19), 90359043.Google Scholar
Feyereisen, R. (2012) Insect CYP genes and P450 enzymes. pp. 236316 in Gilbert, L.I. (Ed.) Insect Molecular Biology and Biochemistry. Elsevier Science Publishers, San Diego.Google Scholar
Giraudo, M., Hilliou, F., Fricaux, T., Audant, P., Feyereisen, R. & Goff, G.L. (2014) Cytochrome P450s from the fall armyworm (Spodoptera frugiperda): responses to plant allelochemicals and pesticides. Insect Molecular Biology. DOI: 10.1111/imb.12140.Google ScholarPubMed
Hirayama, C., Ono, H., Tamura, Y., Konno, K. & Nakamura, K. (2008) Regioselective formation of quercetin 5-O-glucoside from orally administered quercetin in the silkworm, Bombyx mori . Phytochemistry 69, 11411149.Google Scholar
Johnson, R.M., Mao, W., Pollock, H.S., Niu, G., Schuler, M.A. & Berenbaum, M.R. (2012) Ecologically Appropriate Xenobiotics Induce Cytochrome P450s in Apis mellifera . PLoS ONE 7(2), e31051.Google Scholar
Li, B., Zhang, H., Ni, M., Wang, B.B., Li, F.C., Xu, K.Z., Shen, W.D., Xia, Q.Y. & Zhao, P. (2014) Identification and characterization of six cytochrome P450 genes belonging to CYP4 and CYP6 gene families in the silkworm, Bombyx mori . Molecular Biology Reports 41(8), 51355146.Google Scholar
Li, X.C., Baudry, J., Berenbaum, M.R. & Schuler, M.A. (2004) Structural and functional divergence of insect CYP6B proteins: from specialist to generalist cytochrome P450. Proceedings of the National Academy of Sciences of the United States of America 101(9), 29392944.Google Scholar
Lin, F., Wu, D., Lu, Y., Zhang, Y., Qang, M. & Wu, K. (2011) The relationship between the main secondary metabolites and the resistance of cotton to Apolygus lucorum . Acta Ohytophylacia Sinica 38(3), 202208.Google Scholar
Lindroth, R.L. & Peterson, S.S. (1988) Effects of plant phenols on performance of southern armyworm larvae. Oecologia 75(2), 185189.CrossRefGoogle ScholarPubMed
Liu, D., Zhou, X., Li, M., Zhu, S. & Qiu, X. (2014) Characterization of NADPH-cytochrome P450 reductase gene from the cotton bollworm, Helicoverpa armigera . Gene 545(2), 262270.Google Scholar
Liu, X.N., Liang, P., Gao, X.W. & Shi, X.Y. (2006) Induction of the cytochrome P450 activity by plant allelochemicals in the cotton bollworm, Helicoverpa armigera (Hubner). Pesticide Biochemistry and Physiology 84(2), 127134.Google Scholar
Mao, W., Rupasinghe, S.G., Johnson, R.M., Zangerl, A.R., Schuler, M.A. & Berenbaum, M.R. (2009) Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comparative Biochemistry and Physiology, Part B: Biochemistry and Molecular Biology 154(4), 427434.Google Scholar
Mao, W., Schuler, M.A. & Berenbaum, M.R. (2011) CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America 108(31), 1265712662.Google Scholar
Mitchell, M.J., Keogh, D.P., Crooks, J.R. & Smith, S.L. (1993) Effects of plant flavonoids and other allelochemicals on insect cytochrome P-450 dependent steroid hydroxylase activity. Insect Biochemistry and Molecular Biology 23(1), 6571.Google Scholar
Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real-time PCR data by the comparative Ct method. Nature Protocols 3(6), 11011108.CrossRefGoogle Scholar
Schuler, M.A. (2011) P450s in plant-insect interactions. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1814(1), 3645.Google Scholar
Sharma, R. & Sohal, S. (2013) Bioefficacy of quercetin against melon fruit fly. Bulletin of Insectology 66(1), 7983.Google Scholar
Simmonds, M.S.J. (2001) Importance of flavonoids in insect–plant interactions: feeding and oviposition. Phytochemistry 56(3), 245252.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(7), 559568.Google Scholar
Tao, X.Y., Xue, X.Y., Huang, Y.P., Chen, X.Y. & Mao, Y.B. (2012) Gossypol-enhanced P450 gene pool contributes to cotton bollworm tolerance to a pyrethroid insecticide. Molecular Ecology 21(17), 43714385.Google Scholar
U.S. Department of Agriculture, Agricultural Research Service (2011) USDA Database for the Flavonoid Content of Selected Foods, Release 3.0. Available online at http://www.ars.usda.gov/nutrientdata/flav Google Scholar
Vandock, K.P., Mitchell, M.J. & Fioravanti, C. (2012) Effects of plant flavonoids on Manduca sexta (tobacco hornworm) fifth larval instar midgut and fat body mitochondrial transhydrogenase. Archives of Insect Biochemistry and Physiology 80(1), 1525.Google Scholar
War, A.R., Paulraj, M.G., Hussain, B., Buhroo, A.A., Savarimuthu, I. & Sharma, H.C. (2013) Effect of plant secondary metabolites on legume pod borer, Helicoverpa armigera . Journal of Pest Science 86(3), 399408.CrossRefGoogle Scholar
Wu, K. & Gong, P. (1997) A new and practical artificial diet for the cotton bollworm. Entomologia Sinica 4(3), 277282.Google Scholar
Wu, K.M. & Guo, Y.Y. (2005) The evolution of cotton pest management practices in China. Annual Review Entomology 50, 3152.Google Scholar
Yu, S.J. (1983) Induction of detoxifying enzymes by allelochemicals and host plants in the fall armyworm. Pesticide Biochemistry Physiology 19, 330336.Google Scholar
Zhang, H., Tang, T., Cheng, Y., Shui, R., Zhang, W. & Qiu, L. (2010) Cloning and expression of cytochrome P450 CYP6B7 in fenvalerate-resistant and susceptible Helicoverpa armigera (Hubner) from China. Journal of Applied Entomology 134, 754761.Google Scholar
Zhang, Y.E., Ma, H.J., Feng, D.D., Lai, X.F., Chen, Z.M., Xu, M.Y., Yu, Q.Y. & Zhang, Z. (2012) Induction of detoxification enzymes by quercetin in the silkworm. Journal of Economic Entomology 105(3), 10341042.Google Scholar
Zhou, X., Ma, C., Sheng, C., Liu, H., Gong, P. & Qiu, X. (2010 a) CYP9A12 and CYP9A17 in the cotton bollworm, Helicoverpa armigera: sequence similarity, expression profile and xenobiotic response. Pest Management Science 66, 6573.Google Scholar
Zhou, X., Sheng, C., Li, M., Wan, H., Liu, D. & Qiu, X. (2010 b) Expression responses of nine cytochrome P450 genes to xenobiotics in the cotton bollworm Helicoverpa armigera . Pesticide Biochemistry and Physiology 97(3), 209213.Google Scholar
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