Establishing the role of detoxifying enzymes in field‐evolved resistance to various insecticides in the brown planthopper (Nilaparvata lugens) in South India

The brown planthopper (BPH), Nilaparvata lugens (Stål), is one of the major pests of rice throughout Asia. Extensive use of insecticides for suppressing N. lugens has resulted in the development of insecticide resistance leading to frequent control failures in the field. The aim of the present study was to evaluate resistance in the field populations of N. lugens from major rice growing states of South India to various insecticides. We also determined the activity of detoxifying enzymes (esterases [ESTs], glutathione S‐transferases [GSTs], and mixed‐function oxidases [MFOs]). Moderate levels of resistance were detected in the field populations to acephate, thiamethoxam and buprofezin (resistance factors 1.05–20.92 fold, 4.52–14.99 fold, and 1.00–18.09 fold, respectively) as compared with susceptible strain while there were low levels of resistance to imidacloprid (resistance factor 1.23–6.70 fold) and complete sensitivity to etofenoprox (resistance factor 1.05–1.66 fold). EST activities in the field populations were 1.06 to 3.09 times higher than the susceptible strain while for GST and MFO the ratios varied from 1.29 to 3.41 and 1.03 to 1.76, respectively. The EST activity was found to be correlated to acephate resistance (r = 0.999, P ≥ 0.001). The high selection pressure of organophosphate, neonicotinoid, and insect growth regulator (IGR) in the field is likely to be contributing for resistance in BPH to multiple insecticides, leading to control failures. The results obtained will be beneficial to IPM recommendations for the use of effective insecticides against BPH.

[1]  D. Kwon,et al.  Insecticide resistance monitoring and correlation analysis to select appropriate insecticides against Nilaparvata lugens (Stål), a migratory pest in Korea , 2014 .

[2]  C. Walker.  The Development of Resistance , 2014 .

[3]  Z. Xiaolei,et al.  Field evolution of insecticide resistance in the brown planthopper (Nilaparvata lugens Stål) in China , 2014 .

[4]  S. Sanada-Morimura,et al.  Insecticide susceptibilities in populations of two rice planthoppers, Nilaparvata lugens and Sogatella furcifera, immigrating into Japan in the period 2005-2012. , 2014, Pest management science.

[5]  Xueqing Zhao,et al.  Status of Insecticide Resistance of the Whitebacked Planthopper, Sogatella furcifera (Hemiptera: Delphacidae) , 2013 .

[6]  D. Gowda,et al.  Susceptibility of Different Populations of Nilaparvata lugens from Major Rice Growing Areas of Karnataka, India to Different Groups of Insecticides , 2013 .

[7]  D. Kwon,et al.  Cloning of the acetylcholinesterase 1 gene and identification of point mutations putatively associated with carbofuran resistance in Nilaparvata lugens , 2012 .

[8]  Dale G. Bottrell,et al.  Resurrecting the ghost of green revolutions past: The brown planthopper as a recurring threat to high-yielding rice production in tropical Asia , 2012 .

[9]  Run-jie Zhang,et al.  Cross-Resistance of Bisultap Resistant Strain of Nilaparvata lugens and Its Biochemical Mechanism , 2011, Journal of economic entomology.

[10]  D. Gowda,et al.  Insect Pests of Rice and Their Management in Karnataka State of India – A Review , 2011 .

[11]  J. Oakeshott,et al.  Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. , 2011, Insect biochemistry and molecular biology.

[12]  M. Berenbaum,et al.  Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis , 2010, Insect molecular biology.

[13]  V. Lakshmi,et al.  Development of Insecticide Resistance in Rice Brown Planthopper and Whitebacked Planthopper in Godavari Delta of Andhra Pradesh , 2010 .

[14]  Akira Otuka,et al.  Current status of insecticide resistance in rice planthoppers in Asia , 2010 .

[15]  Zewen Liu,et al.  Imidacloprid resistance and its mechanisms in field populations of brown planthopper, Nilaparvata lugens Stål in China. , 2009 .

[16]  K. Zhu,et al.  Mechanisms of organophosphate resistance in a field population of oriental migratory locust, Locusta migratoria manilensis (Meyen). , 2009, Archives of insect biochemistry and physiology.

[17]  K. L. Heong,et al.  Planthopphers: new threats to the sustainability of intensive rice production systems in Asia , 2009 .

[18]  A. Che-Mendoza,et al.  Insecticide resistance and glutathione S-transferases in mosquitoes: A review , 2009 .

[19]  Yanhua Wang,et al.  Susceptibility to neonicotinoids and risk of resistance development in the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). , 2008, Pest management science.

[20]  S. Sanada-Morimura,et al.  Species-specific insecticide resistance to imidacloprid and fipronil in the rice planthoppers Nilaparvata lugens and Sogatella furcifera in East and South-east Asia. , 2008, Pest management science.

[21]  Zewen Liu,et al.  Neonicotinoid resistance in rice brown planthopper, Nilaparvata lugens. , 2008, Pest management science.

[22]  Yanhua Wang,et al.  Buprofezin susceptibility survey, resistance selection and preliminary determination of the resistance mechanism in Nilaparvata lugens (Homoptera: Delphacidae). , 2008, Pest management science.

[23]  Xiwu Gao,et al.  Differential mRNA expression levels and gene sequences of carboxylesterase in both deltamethrin resistant and susceptible strains of the cotton aphid, Aphis gossypii , 2008 .

[24]  R. Nauen,et al.  Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). , 2008, Insect biochemistry and molecular biology.

[25]  Jianzhen Zhang,et al.  Increased activity and reduced sensitivity of acetylcholinesterase associated with malathion resistance in a field population of the oriental migratory locust, Locusta migratoria manilensis (Meyen) , 2008 .

[26]  K. Hoffmann,et al.  Recent advances in hormones in insect pest control , 1998, Phytoparasitica.

[27]  Zewen Liu,et al.  A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[28]  L. Chengjun,et al.  Selection for imidacloprid resistance in Nilaparvata lugens: cross-resistance patterns and possible mechanisms. , 2003, Pest management science.

[29]  D. M. Soderlund,et al.  The molecular biology of knockdown resistance to pyrethroid insecticides. , 2003, Insect biochemistry and molecular biology.

[30]  D. Sujatha,et al.  Development of Resistance to Carbofuran, Phosphamidon and Neem oil in Rice BPH, Nilaparvata lugens Populations in Tamii Nadu, India , 2003 .

[31]  K. Kumar,et al.  Development of Resistance in Rice Brown Planthopper Nilaparvata lugens (Stai) and Green Leafhopper Nephotettix virescens (Dist) to Neem Formulation , 2002 .

[32]  J Hemingway,et al.  Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. , 2001, The Biochemical journal.

[33]  S. Endo,et al.  Insecticide Susceptibility of the Brown Planthopper and the White-backed Planthopper Collected from Southeast Asia , 2001 .

[34]  J. Hemingway,et al.  Molecular characterization of the amplified carboxylesterase gene associated with organophosphorus insecticide resistance in the brown planthopper, Nilaparvata lugens , 2000, Insect molecular biology.

[35]  J. Hemingway.  The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. , 2000, Insect biochemistry and molecular biology.

[36]  Shen Jin-liang,et al.  A method for monitoring of resistance to buprofezin in brown planthopper. , 2000 .

[37]  J. G. Scott,et al.  Cytochromes P450 and insecticide resistance. , 1999, Insect biochemistry and molecular biology.

[38]  R. ffrench-Constant.  Target site mediated insecticide resistance: what questions remain? , 1999 .

[39]  Young-Joon Kim,et al.  Toxicity of Tebufenpyrad to Tetranychus urticae (Acari: Tetranychidae) and Amblyseius womersleyi (Acari: Phytoseiidae) Under Laboratory and Field Conditions , 1999 .

[40]  K. Zhu,et al.  Increased activity associated with reduced sensitivity of acetylcholinesterase in organophosphate‐resistant greenbug, schizaphis graminum (homoptera: aphididae) , 1999 .

[41]  C. Tyler-Smith,et al.  Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). , 1999, The Biochemical journal.

[42]  N. Krishnaiah,et al.  Assessment of Insecticide Resistance in Field Population of Rice Brown Planthopper, Nilaparvata lugens (Stal) in Godavari Delta, (A.P.), India. , 1998 .

[43]  R. Feyereisen,et al.  Molecular biology of insecticide resistance. , 1995, Toxicology letters.

[44]  A. Mutero,et al.  Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. B. Green,et al.  Pest Management in Rice , 1990, Springer Netherlands.

[46]  C. Hung,et al.  Parathion and Methyl Parathion Resistance in Diamondback Moth (Lepidoptera: Plutellidae) Larvae , 1989 .

[47]  S. Lee,et al.  Microsomal cytochrome P450 monooxygenases in the house fly (Musca domestica L.): Biochemical changes associated with pyrethroid resistance and phenobarbital induction , 1989 .

[48]  A. Devonshire,et al.  A carboxylesterase with broad substrate specificity causes organophosphorus, carbamate and pyrethroid resistance in peach-potato aphids (Myzus persicae) , 1982 .

[49]  E. Heinrichs,et al.  Selection of Biotype Populations 2 and 3 of Nilaparvata lugens by Exposure to Resistant Rice Varieties , 1982 .

[50]  K. Kiritani.  PEST MANAGEMENT IN RICE , 1979 .

[51]  T. Nagata,et al.  Resistance in the Brown Planthopper, Nilaparvata lugens STÅL, to Lindane , 1974 .

[52]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.