Effects of phytocompound Precocene 1 on the expression and functionality of the P450 gene in λ-cyhalothrin-resistant Spodoptera litura (Fab.)

Spodoptera litura (Fabricius) is an agriculturally significant polyphagous insect pest that has evolved a high level of resistance to conventional insecticides. A dietary assay was used in this work to assess the resilience of field populations of S. litura to λ-cyhalothrin. Analysis of the function and expression of the cytochrome P450 gene was used to test the sensitivity of S. litura larvae to sub-lethal concentrations of the insecticidal plant chemical Precocene 1, both by itself and in combination with λ-cyhalothrin. The activity of esterase enzymes (α and β) was found to decrease 48 h post treatment with Precocene 1. The activity of GST enzyme and cytochrome P450 increased with Precocene 1 treatment post 48 h, however. Expression studies revealed the modulation by Precocene 1 of cytochrome P450 genes, CYP4M16, CYP4M15, CYP4S8V4, CYP4G31, and CYP4L10. While CYP4M16 expression was stimulated the most by the synergistic Precocene 1 + λ–cyhalothrin treatment, expression of CYP4G31 was the most down-regulated by Precocene 1 exposure. Hence, it is evident that λ–cyhalothrin-resistant pest populations are still sensitive to Precocene 1 at a sublethal concentration that is nevertheless capable of hindering their development. Precocene 1 can therefore be considered a potent candidate for the effective management of insecticide-resilient S. litura.

[1]  B. Buer,et al.  Phylogenomic and functional characterization of an evolutionary conserved cytochrome P450-based insecticide detoxification mechanism in bees , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Can Li,et al.  A review of physiological resistance to insecticide stress in Nilaparvata lugens , 2022, 3 Biotech.

[3]  W. Hunter,et al.  Efficacy of Precocene I from Desmosstachya bipinnata as an Effective Bioactive Molecules against the Spodoptera litura Fab. and Its Impact on Eisenia fetida Savigny , 2021, Molecules.

[4]  S. Senthil-Nathan,et al.  Bioefficacy of Epaltes divaricata (L.) n-Hexane Extracts and Their Major Metabolites against the Lepidopteran Pests Spodoptera litura (fab.) and Dengue Mosquito Aedes aegypti (Linn.) , 2021, Molecules.

[5]  S. Senthil-Nathan,et al.  Toxicity, behavioural and biochemical effect of Piper betle L. essential oil and its constituents against housefly, Musca domestica L. , 2021, Pesticide biochemistry and physiology.

[6]  R. Nauen,et al.  Insecticide resistance management and industry: the origins and evolution of the Insecticide Resistance Action Committee (IRAC) and the mode of action classification scheme , 2021, Pest management science.

[7]  K. Lu,et al.  The role of cytochrome P450-mediated detoxification in insect adaptation to xenobiotics. , 2020, Current opinion in insect science.

[8]  W. Hunter,et al.  Anti-herbivore activity of soluble silicon for crop protection in agriculture: a review , 2020, Environmental Science and Pollution Research.

[9]  S. Senthil-Nathan,et al.  Developmental response of Spodoptera litura Fab in response to plant extract of Desmostachya bipinnata (L.) and its effect on non-target organism, earthworm (Eisenia fetida) , 2020, Environmental Science and Pollution Research.

[10]  A. A. Abd El-Aty,et al.  An overview on the mechanisms and applications of enzyme inhibition-based methods for determination of organophosphate and carbamate pesticides. , 2020, Journal of agricultural and food chemistry.

[11]  Khalid Ali Khan,et al.  Expression and functional analysis of P450 gene induced tolerance/resistance to lambda-cyhalothrin in quercetin fed larvae of beet armyworm Spodoptera exigua (Hübner) , 2019, Saudi journal of biological sciences.

[12]  K. Lalitha,et al.  Effect of Manihot esculenta (Crantz) leaf extracts on antioxidant and immune system of Spodoptera litura (Lepidoptera: Noctuidae) , 2020 .

[13]  S. Senthil-Nathan A Review of Resistance Mechanisms of Synthetic Insecticides and Botanicals, Phytochemicals, and Essential Oils as Alternative Larvicidal Agents Against Mosquitoes , 2020, Frontiers in Physiology.

[14]  Aqeel Ahmad,et al.  Gossypol-induced fitness gain and increased resistance to deltamethrin in beet armyworm, Spodoptera exigua (Hübner). , 2018, Pest management science.

[15]  S. Senthil-Nathan Effect of methyl jasmonate (MeJA)-induced defenses in rice against the rice leaffolder Cnaphalocrocis medinalis (Guenèe) (Lepidoptera: Pyralidae). , 2018, Pest management science.

[16]  Xuegui Wang,et al.  Molecular identification of four novel cytochrome P450 genes related to the development of resistance of Spodoptera exigua (Lepidoptera: Noctuidae) to chlorantraniliprole. , 2018, Pest management science.

[17]  Z. Qin,et al.  Identification and Functional Analysis of a Novel Cytochrome P450 Gene CYP9A105 Associated with Pyrethroid Detoxification in Spodoptera exigua Hübner , 2018, International journal of molecular sciences.

[18]  N. Desneux,et al.  Uptake of quercetin reduces larval sensitivity to lambda-cyhalothrin in Helicoverpa armigera , 2018, Journal of Pest Science.

[19]  Yan Zhao,et al.  Functional Study of Cytochrome P450 Enzymes from the Brown Planthopper (Nilaparvata lugens Stål) to Analyze Its Adaptation to BPH-Resistant Rice , 2017, Front. Physiol..

[20]  H. Kishino,et al.  Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest , 2017, Nature Ecology & Evolution.

[21]  M. Shivakumar,et al.  Bioprospecting of Prosopis juliflora (Sw.) DC seed pod extract effect on antioxidant and immune system of Spodoptera litura (Lepidoptera: Noctuidae) , 2017 .

[22]  Ying Liu,et al.  Elevated carboxylesterase activity contributes to the lambda-cyhalothrin insensitivity in quercetin fed Helicoverpa armigera (Hübner) , 2017, PloS one.

[23]  W. Hunter,et al.  Toxicity and physiological effect of quercetin on generalist herbivore, Spodoptera litura Fab. and a non-target earthworm Eisenia fetida Savigny. , 2016, Chemosphere.

[24]  M. Zhang,et al.  Susceptibility and potential biochemical mechanism of Oedaleus asiaticus to beta-cypermethrin and deltamethrin in the Inner Mongolia, China. , 2016, Pesticide biochemistry and physiology.

[25]  Zhaojun Han,et al.  Constitutive overexpression of cytochrome P450 associated with imidacloprid resistance in Laodelphax striatellus (Fallén). , 2016, Pest management science.

[26]  S. Karthi,et al.  Time-of-day specific changes in pesticide detoxification ability of Spodoptera litura (Lepidoptera: Noctuidae) , 2016 .

[27]  S. R. Palli,et al.  A specialist herbivore pest adaptation to xenobiotics through up-regulation of multiple Cytochrome P450s , 2016, Scientific Reports.

[28]  S. Karthi,et al.  The protective effect of melatonin against cypermethrin-induced oxidative stress damage in Spodoptera litura (Lepidoptera: Noctuidae) , 2015 .

[29]  Guonian Zhu,et al.  Insecticide-Mediated Up-Regulation of Cytochrome P450 Genes in the Red Flour Beetle (Tribolium castaneum) , 2015, International journal of molecular sciences.

[30]  S. Senthil-Nathan A Review of Biopesticides and Their Mode of Action Against Insect Pests , 2015 .

[31]  S. Bak,et al.  How insects overcome two‐component plant chemical defence: plant β‐glucosidases as the main target for herbivore adaptation , 2014, Biological reviews of the Cambridge Philosophical Society.

[32]  Ashok P Giri,et al.  Molecular insights into resistance mechanisms of lepidopteran insect pests against toxicants. , 2013, Journal of proteome research.

[33]  M. Berenbaum,et al.  Structure and Function of Cytochrome P450S in Insect Adaptation to Natural and Synthetic Toxins: Insights Gained from Molecular Modeling , 2013, Journal of Chemical Ecology.

[34]  Sambangi Pratyusha,et al.  Defensive role of Gossypium hirsutum L. anti-oxidative enzymes and phenolic acids in response to Spodoptera litura F. feeding , 2013 .

[35]  Xuetao Zhang,et al.  Molecular cloning and recombinant expression of cytochrome P450 CYP6B6 from Helicoverpa armigera in Escherichia coli , 2013, Molecular Biology Reports.

[36]  T. Chertemps,et al.  Cytochrome P450s and cytochrome P450 reductase in the olfactory organ of the cotton leafworm Spodoptera littoralis , 2012, Insect molecular biology.

[37]  Y. Shu,et al.  Response of the common cutworm Spodoptera litura to zinc stress: Zn accumulation, metallothionein and cell ultrastructure of the midgut. , 2012, The Science of the total environment.

[38]  Ying-Bo Mao,et al.  Gossypol‐enhanced P450 gene pool contributes to cotton bollworm tolerance to a pyrethroid insecticide , 2012, Molecular ecology.

[39]  M. Schuler Insect P450s: mounted for battle in their war against toxins , 2012, Molecular ecology.

[40]  Jianzhen Zhang,et al.  Identification of two new cytochrome P450 genes and RNA interference to evaluate their roles in detoxification of commonly used insecticides in Locusta migratoria. , 2012, Chemosphere.

[41]  Henry S. Pollock,et al.  Ecologically Appropriate Xenobiotics Induce Cytochrome P450s in Apis mellifera , 2012, PloS one.

[42]  R. Nauen,et al.  Overexpression of a cytochrome P450 monooxygenase, CYP6ER1, is associated with resistance to imidacloprid in the brown planthopper, Nilaparvata lugens , 2011, Insect molecular biology.

[43]  A. War,et al.  Herbivore- and Elicitor- Induced Resistance in Groundnut to Asian armyworm, Spodoptera litura (Fab.) (Lepidoptera: Noctuidae) , 2011, Plant signaling & behavior.

[44]  M. Berenbaum,et al.  A substrate-specific cytochrome P450 monooxygenase, CYP6AB11, from the polyphagous navel orangeworm (Amyelois transitella). , 2011, Insect biochemistry and molecular biology.

[45]  R. Feyereisen Arthropod CYPomes illustrate the tempo and mode in P450 evolution. , 2011, Biochimica et biophysica acta.

[46]  D. Nelson,et al.  Progress in tracing the evolutionary paths of cytochrome P450. , 2011, Biochimica et biophysica acta.

[47]  Ling Li,et al.  Protein profiles of the midgut of Spodoptera litura larvae at the sixth instar feeding stage by shotgun ESI-MS approach. , 2010, Journal of proteome research.

[48]  Mei Li,et al.  CYP9A12 and CYP9A17 in the cotton bollworm, Helicoverpa armigera: sequence similarity, expression profile and xenobiotic response. , 2010, Pest management science.

[49]  Q. Feng,et al.  Two epsilon glutathione S-transferase cDNAs from the common cutworm, Spodoptera litura: characterization and developmental and induced expression by insecticides. , 2009, Journal of insect physiology.

[50]  Toshiharu Tanaka,et al.  RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. , 2009, Insect biochemistry and molecular biology.

[51]  M. Rashid,et al.  Antimicrobial activity and toxicity of Quisqualis indica , 2008 .

[52]  M. Schuler,et al.  Helicoverpa zea CYP6B8 and CYP321A1: different molecular solutions to the problem of metabolizing plant toxins and insecticides. , 2007, Protein engineering, design & selection : PEDS.

[53]  L. Després,et al.  The evolutionary ecology of insect resistance to plant chemicals. , 2007, Trends in ecology & evolution.

[54]  May R Berenbaum,et al.  Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. , 2007, Annual review of entomology.

[55]  Zhaojun Han,et al.  Mechanisms for multiple resistances in field populations of common cutworm, Spodoptera litura (Fabricius) in China , 2007 .

[56]  M. Berenbaum,et al.  Allelochemical Induction of Cytochrome P450 Monooxygenases and Amelioration of Xenobiotic Toxicity in Helicoverpa zea , 2007, Journal of Chemical Ecology.

[57]  K. Kalaivani,et al.  Combined effects of azadirachtin and nucleopolyhedrovirus (SpltNPV) on Spodoptera litura Fabricius (Lepidoptera: Noctuidae) larvae , 2006 .

[58]  M. Berenbaum,et al.  Remarkable substrate‐specificity of CYP6AB3 in Depressaria pastinacella, a highly specialized caterpillar , 2006, Insect molecular biology.

[59]  Xueyan Shi,et al.  Induction of the cytochrome P450 activity by plant allelochemicals in the cotton bollworm, Helicoverpa armigera (Hübner) , 2006 .

[60]  K. Kalaivani,et al.  Efficacy of nucleopolyhedrovirus and azadirachtin on Spodoptera litura Fabricius (Lepidoptera: Noctuidae) , 2005 .

[61]  J. Takabayashi,et al.  Variation in composition of predator-attracting allelochemicals emitted by herbivore-infested plants: Relative influence of plant and herbivore , 1991, CHEMOECOLOGY.

[62]  M. Agosin Insect cytochrome P-450 , 1976, Molecular and Cellular Biochemistry.

[63]  R. Feyereisen,et al.  4.1 – Insect Cytochrome P450 , 2005 .

[64]  M. Berenbaum,et al.  Characterization and evolution of furanocoumarin‐inducible cytochrome P450s in the parsnip webworm, Depressaria pastinacella , 2004, Insect molecular biology.

[65]  M. Berenbaum,et al.  Molecular analysis of CYP321A1, a novel cytochrome P450 involved in metabolism of plant allelochemicals (furanocoumarins) and insecticides (cypermethrin) in Helicoverpa zea. , 2004, Gene.

[66]  Sason Shaik,et al.  Mechanism of oxidation reactions catalyzed by cytochrome p450 enzymes. , 2004, Chemical reviews.

[67]  M. Berenbaum,et al.  Structural and functional divergence of insect CYP6B proteins: From specialist to generalist cytochrome P450. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[68]  S. Mukherjee Influence of plant allelochemicals on growth rate, nutritional physiology and mid-gut esterase activity in fifth instar larvae of Spodoptera litura (F.) (Lepidoptera: Noctuidae) , 2003 .

[69]  D. Russell,et al.  Insecticide resistance in five major insect pests of cotton in India , 2002 .

[70]  Z. Wen,et al.  Cytochromes P450 of insects: the tip of the iceberg. , 2001, Pest management science.

[71]  Sharda P. Singh,et al.  Catalytic function of Drosophila melanogaster glutathione S-transferase DmGSTS1-1 (GST-2) in conjugation of lipid peroxidation end products. , 2001, European journal of biochemistry.

[72]  M. Berenbaum,et al.  Cross-Resistance to α-Cypermethrin After Xanthotoxin Ingestion in Helicoverpa zea (Lepidoptera: Noctuidae) , 2000, Journal of economic entomology.

[73]  Mushtaq Ahmad,et al.  Penetration and Metabolism of trans-Cypermethrin in a Susceptible and a Pyrethroid-Resistant Strain of Helicoverpa armigera , 1999 .

[74]  J. Vulule,et al.  Heme peroxidase activity measured in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. , 1997, Journal of the American Mosquito Control Association.

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

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