Skip to main content
SpringerLink
Log in

Resistance Mechanisms of Helicoverpa armigera

  • Chapter
  • First Online:
Advances in Insect Control and Resistance Management

Abstract

The cotton bollworm, Helicoverpa armigera, is one of the major agricultural pest species in the Old World and recently also of the New World. This noctuid moth species is highly polyphagous and possesses a huge geographical distribution and the ability to quickly evolve resistance to insecticides from different chemical classes. There are different mechanisms known with which insects combat insecticides. They are ranging from behavioral over morphological to physiological adaptations. These resistance mechanisms can occur alone or in combination and may change in the field according to changing selection pressures. A reduced penetration through the cuticle of H. armigera larvae is known which reduces the concentration at the target site. Also mutations of the target of pyrethroid insecticides, organochlorines, and oxadiazines, voltage-dependent sodium channels, were described that lead to high or lower resistance levels. Furthermore, both carboxylesterases and cytochrome P450 monooxygenases were investigated to determine their role in insecticide resistance. So far, only few enzymes were identified in H. armigera which were proven to metabolize and thus detoxify insecticides. Most studies deal with the resistance against pyrethroids. One important resistance gene is the chimeric P450 CYP337B3 that is present in resistant and absent in susceptible individuals. The corresponding enzyme is capable of metabolizing fenvalerate and cypermethrin and thus confers resistance to H. armigera larvae. This new resistance mechanism by recombination seems to play an important role in H. armigera populations throughout the world.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahmad M (2007) Insecticide resistance mechanisms and their management in Helicoverpa armigera (Hübner)–a review. J Agric Res 45(4):319–335

    Google Scholar 

  • Ahmad M, McCaffery AR (1999) Penetration and metabolism of trans-cypermethrin in a susceptible and a pyrethroid-resistance strain of Helicoverpa armigera. Pestic Biochem Physiol 65:6–14

    Article  CAS  Google Scholar 

  • Ahmad M, Gladwell RT, McCaffery AR (1989) Decreased nerve sensitivity is a mechanism of resistance in a pyrethroid resistant strain of Heliothis armigera from Thailand. Pestic Biochem Physiol 35:165–171

    Article  CAS  Google Scholar 

  • Ahmad M, Arif MI, Attique MR (1997) Pyrethroid resistance of Helicoverpa armigera (Lepidoptera: Noctuidae) in Pakistan. Bull Entomol Res 87:343–347

    Article  CAS  Google Scholar 

  • Ahmad M, Denholm I, Bromilow RH (2006) Delayed cuticular penetration and enhanced metabolism of deltamethrin in pyrethroid-resistant strains of Helicoverpa armigera from China and Pakistan. Pest Manag Sci 62:805–810

    Article  CAS  PubMed  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 Manag Sci 66:900–909

    CAS  PubMed  Google Scholar 

  • Cen W (1992) Investigation on the resistance level of the cotton bollworm Heliothis armigera to four kinds of pyrethroid pesticides in China in 1991. Resistant Pest Manag Newsl 4:17–21

    Google Scholar 

  • Daborn PJ, Lumb C, Harrop TWR, Blasetti A, Pasricha S, Morin S, Mitchell SN, Donnelly MJ, Mülller P, Batterham P (2012) Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pests. Insect Biochem Mol Biol 42:918–924

    Article  CAS  PubMed  Google Scholar 

  • Dermauw W, Van Leeuwen T (2014) The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Biol 45:89–110

    Article  CAS  PubMed  Google Scholar 

  • Doichuanngam K, Thornhill RA (1992) Penetration, excretion and metabolism of 14C malathion in susceptible and resistant strains of Plutella xylostella. Comp Biochem Physiol 101C(3):583–588

    CAS  Google Scholar 

  • Dong K (2007) Insect sodium channels and insecticide resistance. Invert Neurosci 7:17–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14(1):3–8

    Article  CAS  PubMed  Google Scholar 

  • Feng H-Q, Wu K-M, Ni Y-X, Cheng D-F, Guo Y-Y (2005) Return migration of Helicoverpa armigera (Lepidoptera: Noctuidae) during autumn in northern China. Bull Entomol Res 95:361–370

    Article  PubMed  Google Scholar 

  • Feyereisen R (2006) Evolution of insect P450. Biochem Soc Trans 34(6):1252–1255

    Article  CAS  PubMed  Google Scholar 

  • Feyereisen R (2012) Insect CYP genes and P450 enzymes. In: Gilbert LI (ed) Insect molecular biology and biochemistry. Elsevier, London, pp 236–316

    Chapter  Google Scholar 

  • Feyereisen R, Dermauw W, Van Leeuwen T (2015) Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pestic Biochem Physiol 121:61–77

    Article  CAS  PubMed  Google Scholar 

  • Firempong S, Zalucki MP (1989) Host plant preferences of populations of Helicoverpa-armigera (Hubner) (Lepidoptera, Noctuidae) from different geographic locations. Aust J Zool 37(6):665–673

    Article  Google Scholar 

  • Fitt GP (1989) The ecology of Heliothis species in relation to agroecosystems. Ann Rev Entomol 34:17–52

    Article  Google Scholar 

  • Forrester NW, Cahill M, Bird LJ, Layland JK (1993) Management of pyrethroid and endosulfan resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Bull Entomol Res Suppl 1:1–132

    Article  Google Scholar 

  • Grubor VD, Heckel DG (2007) Evaluation of the role of CYP6B cytochrome P450s in pyrethroid resistant Australian Helicoverpa armigera. Insect Mol Biol 16(1):15–23

    Article  CAS  PubMed  Google Scholar 

  • Gunning RV (1996) Bioassay for detecting pyrethroid nerve insensitivity in Australian Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol 89(4):816–819

    Article  Google Scholar 

  • Gunning RV, Easton CS, Greenup LR, Edge VE (1984) Pyrethroid resistance in Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) in Australia. J Econ Entomol 77(5):1283–1287

    Article  CAS  Google Scholar 

  • Gunning RV, Easton CS, Balfe ME, Ferris IG (1991) Pyrethroid resistance mechanisms in Australian Helicoverpa armigera. Pestic Sci 33:473–490

    Article  CAS  Google Scholar 

  • Gunning RV, Devonshire AL, Moores GD (1995) Metabolism of esfenvalerate by pyrethroid-susceptible and -resistant Australian Helicoverpa armigera (Lepidoptera: Noctuidae). Pestic Biochem Physiol 51:205–213

    Article  CAS  Google Scholar 

  • Gunning RV, Moores GD, Devonshire AL (1996) Esterase and esfenvalerate resistance in Australian Helicoverpa armigera (Hübner) Lepidoptera:Noctuidae. Pestic Biochem Physiol 54:12–23

    Article  CAS  Google Scholar 

  • Gunning RV, Moores GD, Jewess P, Boyes AL, Devonshire AL, Khambay BPS (2007) Use of pyrethroid analogues to identify key structural features for enhanced esterase resistance in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Pest Manag Sci 63:569–575

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Yu W, Zhang W, Yang Y, Walsh T, Oakeshott JG, Wu Y (2015) Variation in P450-mediated fenvalerate resistance levels is not correlated with CYP337B3 genotype in Chinese populations of Helicoverpa armigera. Pestic Biochem Physiol 121:129–135

    Article  CAS  PubMed  Google Scholar 

  • Head DJ, McCaffery AR, Callaghan A (1998) Novel mutations in the para-homologous sodium channel gene associated with phenotypic expression of nerve insensitivity resistance to pyrethroids in Heliothine lepidoptera. Insect Mol Biol 7(2):191–196

    Article  CAS  PubMed  Google Scholar 

  • Heckel DG, Gahan LJ, Daly JC, Trowell S (1998) A genomic approach to understanding Heliothis and Helicoverpa resistance to chemical and biological insecticides. Philos Trans R Soc Lond B Biol Sci 353:1713–1722

    Article  CAS  PubMed Central  Google Scholar 

  • Joußen N, Agnolet S, Lorenz S, Schöne SE, Ellinger R, Schneider B, Heckel DG (2012) Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3. Proc Natl Acad Sci U S A 109(38):15206–15211

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumari APP, Phokela A, Mehrotra KN (1995) Permeability of cuticle of Helicoverpa armigera (Hübner) larvae to deltamethrin. Curr Sci 69(5):464–466

    CAS  Google Scholar 

  • Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253

    Article  PubMed  Google Scholar 

  • Li Y, Farnsworth CA, Coppin CW, Teese MG, Liu J-W, Scott C, Zhang X, Russell RJ, Oakeshott JG (2013) Organophosphate and pyrethroid hydrolase activities of mutant esterases from the cotton bollworm Helicoverpa armigera. PLoS One 8(10), e77685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu N-N, Zhu F, Xu Q, Pridgeon JW, Gao X-W (2006) Behavioral change, physiological modification, and metabolic detoxification: mechanisms of insecticide resistance. Acta Entomol Sin 49(4):671–679

    CAS  Google Scholar 

  • Lockwood JA, Byford RL, Story RN, Sparks TC, Quisenberry SS (1985) Behavioral resistance to the pyrethroids in the horn fly, Haematobia irritans (Diptera: Muscidae). Environ Entomol 14(6):873–880

    Article  CAS  Google Scholar 

  • Martin T, Chandre F, Ochou OG, Vaissayre M, Fournier D (2002) Pyrethroid resistance mechanisms in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) from West Africa. Pestic Biochem Physiol 74:17–26

    Article  Google Scholar 

  • McCaffery AR, Head DJ, Jianguo T, Dubbeldam AA, Subramaniam VR, Callaghan A (1997) Nerve insensitivity resistance to pyrethroids in Heliothine lepidoptera. Pestic Sci 51:315–320

    Article  CAS  Google Scholar 

  • Murúa MG, Scalora FS, Navarro FR, Cazado LE, Casmuz A, Villagrán ME, Lobos E, Gastaminza G (2014) First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Fla Entomol 97(2):854–856

    Article  Google Scholar 

  • Pittendrigh B, Aronstein K, Zinkovsky E, Andreev O, Campbell B, Daly J, Trowell S, ffrench-Constant RH (1997) Cytochrome P450 genes from Helicoverpa armigera: expression in a pyrethroid-susceptible and -resistant strain. Insect Biochem Mol Biol 27(6)

    Google Scholar 

  • Ranasinghe C, Hobbs AA (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

    Article  CAS  PubMed  Google Scholar 

  • Ranasinghe C, Campbell B, Hobbs AA (1998) Over-expression of cytochrome P450 CYP6B7 mRNA and pyrethroid resistance in Australian populations of Helicoverpa armigera (Hübner). Pestic Sci 54:195–202

    Article  CAS  Google Scholar 

  • Rasool A, Joußen N, Lorenz S, Ellinger R, Schneider B, Khan SA, Ashfaq M, Heckel DG (2014) An independent occurrence of the chimeric P450 enzyme CYP337B3 of Helicoverpa armigera confers cypermethrin resistance in Pakistan. Insect Biochem Mol Biol 53:54–65

    Article  CAS  PubMed  Google Scholar 

  • Ru L, Wei C, Zhao J-Z, Liu A (1998) Differences in resistance to fenvalerate and cyhalothrin and inheritance of knockdown resistance to fenvalerate in Helicoverpa armigera. Pest Biochem Physiol 61:79–85

    Article  CAS  Google Scholar 

  • Shono T, Ohsawa K, Casida JE (1979) Mechanism of trans- and cis-permethrin, trans- and cis-cypermethrin, and decamethrin by microsomal enzymes. J Agric Food Chem 27(2):316–325

    Article  CAS  PubMed  Google Scholar 

  • Silverman J, Bieman DN (1993) Glucose aversion in the German cockroach, Blattella germanica. J Insect Physiol 39(11):925–933

    Article  CAS  Google Scholar 

  • Sparks TC, Nauen R (2015) IRAC: mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128

    Article  CAS  PubMed  Google Scholar 

  • Srinivas R, Udikeri SS, Jayalakshmi SK, Sreeramulu K (2004) Identification of factors responsible for insecticide resistance in Helicoverpa armigera. Comp Biochem Physiol 137C:261–269

    CAS  Google Scholar 

  • Strycharz JP, Lao A, Li H, Qiu X, Lee SH, Sun W, Yoon KS, Doherty JJ, Pittendrigh BR, Clark JM (2013) Resistance in the highly DDT-resistant 91-R strain of Drosophila melanogaster involves decreased penetration, increased metabolism, and direct excretion. Pestic Biochem Physiol 107:207–217

    Article  CAS  Google Scholar 

  • Tang T, Zhao C, Feng X, Liu X, Qiu L (2012) Knockdown of several components of cytochrome P450 enzyme systems by RNA interference enhances the susceptibility of Helicoverpa armigera to fenvalerate. Pest Manag Sci 68:1501–1511

    Article  CAS  PubMed  Google Scholar 

  • Tay WT, Soria MF, Walsh T, Thomazoni D, Silvie P, Behere GT, Anderson C, Downes S (2013) A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS One 8(11), e80134

    Article  PubMed  PubMed Central  Google Scholar 

  • Teese MG, Campbell PM, Scott C, Gordon KHJ, Southon A, Hovan D, Robin C, Russell RJ, Oakeshott JG (2010) Gene identification and proteomic analysis of the esterases of the cotton bollworm, Helicoverpa armigera. Insect Biochem Mol Biol 40:1–16

    Article  CAS  PubMed  Google Scholar 

  • Teese MG, Farnsworth CA, Li Y, Coppin CW, Devonshire AL, Scott C, East P, Russell RJ, Oakeshott JG (2013) Heterologous expression and biochemical characterisation of fourteen esterases from Helicoverpa armigera. PLoS One 8(6), e65951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinson BS, Law PK (1971) Cuticular composition and DDT resistance in the tobacco budworm. J Econ Entomol 64:1387–1390

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Cheng J-A, Liu Z-M, Wu S-G, Zhao X-P, Wu C-X (2005) Influences of insecticides on toxicity and cuticular penetration of abamectin in Helicoverpa armigera. Insect Sci 12:109–119

    Article  Google Scholar 

  • Wee CW, Lee SF, Robin C, Heckel DG (2008) Identification of candidate genes for fenvalerate resistance in Helicoverpa armigera using cDNA-AFLP. Insect Mol Biol 17(4):351–360

    Article  CAS  PubMed  Google Scholar 

  • Wheelock CE, Shan G, Ottea J (2005) Overview of carboxylesterases and their role in the metabolism of insecticides. J Pestic Sci 30(2):75–83

    Article  CAS  Google Scholar 

  • Wu S, Yang Y, Yuan G, Campbell PM, Teese MG, Russell RJ, Oakeshott JG, Wu Y (2011) Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. Insect Biochem Mol Biol 41:14–21

    Article  CAS  PubMed  Google Scholar 

  • Xiao-Ping W, Hobbs AA (1995) Isolation and sequence analysis of a cDNA clone for a pyrethroid inducible cytochrome P450 from Helicoverpa armigera. Insect Biochem Mol Biol 25(9):1001–1009

    Article  CAS  Google Scholar 

  • Yang Y, Wu Y, Chen S, Devine GJ, Denholm I, Jewess P, Moores GD (2004) The involvement of microsomal oxidases in pyrethroid resistance in Helicoverpa armigera from Asia. Insect Biochem Mol Biol 34:763–773

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Yue L, Chen S, Wu Y (2008) Functional expression of Helicoverpa armigera CYP9A12 and CYP9A14 in Saccharomyces cerevisiae. Pestic Biochem Physiol 92:101–105

    Article  CAS  Google Scholar 

  • Zalucki MP, Daglish G, Firempong S, Twine P (1986) The biology and ecology of Heliothis armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what do we know? Aust J Zool 34:779–814

    Article  Google Scholar 

  • Zhang S (2008) Functional expression and pyrethroid metabolism of P450 genes CYP9A12 and CYP9A17 of Helicoverpa armigera (Hübner). Master’s thesis, Nanjing Agricultural College

    Google Scholar 

  • Zhang S, Yang Y-H, Wu S-W, Wu Y-D (2008) Metabolism of pyrethroids by Helicoverpa armigera cytochrome P450 gene CYP9A12 heterologously expressed in Saccharomyces cerevisiae. Acta Entomol Sin 51(12):1255–1259

    CAS  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 (Hübner) from China. J Appl Entomol 134:754–761

    Article  CAS  Google Scholar 

  • Zhang X, Yuan D, Ding L, Li P, Liu X (2013) Expression of cytochrome P450 CYP6B6 in the different developmental stages of the insect Helicoverpa armigera (Lepidoptera: Noctuidae). Eur J Entomol 110(1):39–45

    Article  CAS  Google Scholar 

  • Zuber R, Anzenbacherová E, Anzenbacer P (2002) Cytochrome P450 and experimental models of drug metabolism. J Cell Mol Med 6(2):189–198

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745, Jena, Germany

    Nicole Joußen & David G. Heckel

Authors
  1. Nicole Joußen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David G. Heckel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicole Joußen .

Editor information

Editors and Affiliations

  1. Department of Entomology, Agricultural Research Organization, Gilat Research Center, Negev, Israel

    A. Rami Horowitz

  2. Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel

    Isaac Ishaaya

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Joußen, N., Heckel, D.G. (2016). Resistance Mechanisms of Helicoverpa armigera . In: Horowitz, A., Ishaaya, I. (eds) Advances in Insect Control and Resistance Management. Springer, Cham. https://doi.org/10.1007/978-3-319-31800-4_13

Download citation

Publish with us

Policies and ethics

Search

Navigation