Skip to main content
SpringerLink
Log in

Metabolic-based insecticide resistance mechanism and ecofriendly approaches for controlling of beet armyworm Spodoptera exigua: a review

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The beet army worm, Spodoptera exigua, is a widely distributed polyphagous pest of economically important crops worldwide. The management of this pest insect continues to face many challenges. Despite synthetic chemicals posing a serious threat to the environment, these remain the conventional approach for controlling S. exigua in the field. An over-reliance on chemical control has not only led to selection for resistance to insecticides and to a reduction of natural enemies, but has also polluted various components of ecosystem. Given these increasing pressures on the ecosystem, there is a need to implement integrated pest management (IPM) approaches exploiting a wider range of tools (biotechnological approaches, microbial control, biological control, cultural control, and use of host plant resistance) for an alternative to chemical control. The IPM approach can not only reduce the hazard of chemical residues in the environment and associated health problems, but may also provide best strategies to control insect pests. This review synthesizes published information on insecticide resistance of S. exigua and explores alternative IPM approaches to control S. exigua.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Ahmad M, Arif IM (2010) Resistance of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) to endosulfan, organophosphorus and pyrethroid insecticides in Pakistan. Crop Prot 29:1428–1433. https://doi.org/10.1016/j.cropro.2010.07.025

    Article  CAS  Google Scholar 

  • Ahmad M, Farid A, Saeed M (2018) Resistance to new insecticides and their synergism in Spodoptera exigua (Lepidoptera: Noctuidae) from Pakistan. Crop Prot 107:79–86. https://doi.org/10.1016/j.cropro.2017.12.028

    Article  CAS  Google Scholar 

  • Ahmad M, Iqbal Arif M, Ahmad M (2007) Occurrence of insecticide resistance in field populations of Spodoptera litura (Lepidoptera: Noctuidae) in Pakistan. Crop Prot 26:809–817. https://doi.org/10.1016/j.cropro.2006.07.006

    Article  CAS  Google Scholar 

  • Aldosari SA, Watson TF, Sivasupramaniam S, Osman AA (1996) Susceptibility of field populations of beet armyworm (Lepidoptera: Noctuidae) to cyfluthrin, methomyl, and profenofos, and selection for resistance to cyfluthrin. J Econ Entomol 42:217–222. https://doi.org/10.1093/jee/89.6.1359

    Article  Google Scholar 

  • Amoabeng BW, Gurr GM, Gitau CW et al (2013) Tri-trophic insecticidal effects of African plants against cabbage pests. PLoS ONE 8:e78651. https://doi.org/10.1371/journal.pone.0078651

    Article  CAS  Google Scholar 

  • An R, Orellana D, Phelan LP et al (2016) Entomopathogenic nematodes induce systemic resistance in tomato against Spodoptera exigua, Bemisia tabaci and Pseudomonas syringae. Biol Control 93:24–29. https://doi.org/10.1016/j.biocontrol.2015.11.001

    Article  Google Scholar 

  • Ant T, Koukidou M, Rempoulakis P et al (2012) Control of the olive fruit fly using genetics-enhanced sterile insect technique. BMC Biol 19(10):51. https://doi.org/10.1186/1741-7007-10-51

    Article  Google Scholar 

  • Arain MS, Shakeel M, Elzaki ME, Abdalla FM et al (2018) Association of detoxification enzymes with butene-fipronil in larvae and adults of Drosophilia melanogaster. Environ Sci Pollut Res 25:10006–10013

    Article  CAS  Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300

    Article  CAS  Google Scholar 

  • Azidah AA, Sofian-Azirun M (2006) Life history of Spodoptera exigua (Lepidoptera: Noctuidae) on various host plants. Bull Entomol Res 96:613–618. https://doi.org/10.1017/BER2006461

    Article  CAS  Google Scholar 

  • Bassett AR, Tibbit C, Ponting CP, Liu J (2013) Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep 4:220–228

    Article  CAS  Google Scholar 

  • Boaventura D, Martin M, Pozzebon A et al (2020) Monitoring of target-site mutations conferring insecticide resistance in Spodoptera frugiperda. Insects 11:545. https://doi.org/10.3390/insects11080545

    Article  Google Scholar 

  • Brewer MJ, Trumble JT (1994) Beet Armyworm Resistance to Fenvalerate and Methomyl: Resistance Variation and Insecticide synergismI 56:442–448

    Google Scholar 

  • Calkins CO, Parker AG (2005) Sterile insect quality. In: Sterile insect technique: principles and practice in area-wide integrated pest management 269–296

  • Campbell PM, Newcomb RD, Russell RJ, Oakeshott JG (1998) Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol. 28: 139–150 https://doi.org/10.1016/S0965-1748(97)00109-4

  • Che W, Shi T, Wu Y, Yang Y (2013) Insecticide resistance status of field populations of Spodoptera exigua (Lepidoptera: Noctuidae) from China. J Econ Entomol 106(4):1855–1862. https://doi.org/10.1603/EC13128

    Article  CAS  Google Scholar 

  • Chen J, Tang B, Chen H et al (2010) Different functions of the insect soluble and membrane-bound trehalase genes in chitin biosynthesis revealed by rna interference. PLoS ONE 5(4):e10133. https://doi.org/10.1371/journal.pone.0010133

    Article  CAS  Google Scholar 

  • Chen Y (2005) Biodiversity and pest management in agroecosystems. J Environ Qual 30(8):e02201. https://doi.org/10.2134/jeq2005.0729

    Article  Google Scholar 

  • Claudianos C, Russell RJ, Oakeshott JG (1999) The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Biochem Mol Biol 29(8):675–686. https://doi.org/10.1016/S0965-1748(99)00035-1

    Article  CAS  Google Scholar 

  • Clement SL, Sharma HC, Muehlbauer FJ et al (2010) Resistance to beet armyworm in a chickpea recombinant inbred line population. J Appl Entomol 134:1–8

    Article  Google Scholar 

  • Commonwealth Agricultural Bureaux (CAB) (1972) Distribution maps of pests. Pest: Spodoptera exigua (Hübner). London. Series A, Map no. 302.

  • Cordeiro EMG, Corrêa AS, Venzon M, Guedes RNC (2010) Insecticide survival and behavioral avoidance in the lacewings Chrysoperla externa and Ceraeochrysa cubana. Chemosphere 81(10):1352–1357. https://doi.org/10.1016/j.chemosphere.2010.08.021

    Article  CAS  Google Scholar 

  • Cordova D, Benner EA, Sacher MD et al (2006) Anthranilic diamides: a new class of insecticides with a novel mode of action, ryanodine receptor activation. Pestic Biochem Physiol 84:196–214. https://doi.org/10.1016/j.pestbp.2005.07.005

    Article  CAS  Google Scholar 

  • Dawkar V V., Chikate YR, Lomate PR, et al (2013) Molecular insights into resistance mechanisms of lepidopteran insect pests against toxicants. J. Proteome Res. 1–15

  • Diaz R, Knutson A, Bernal JS (2004) Effect of the red imported fire ant on cotton aphid population density and predation of bollworm and beet armyworm eggs. J Econ Entomol 97:222–229. https://doi.org/10.1093/jee/97.2.222

    Article  Google Scholar 

  • Diez MC, Gallardo F, Tortella G, et al (2012) Chlorophenol degradation in soil columns inoculated with Anthracophyllum discolor immobilized on wheat grains. J Environ Manage. S83-7 https://doi.org/10.1016/j.jenvman.2010.09.024

  • Ding Y, Li H, Chen L-L, Xie K (2016) Recent advances in genome editing using CRISPR/Cas9. Front Plant Sci 7:27252719. https://doi.org/10.3389/fpls.2016.00703

    Article  Google Scholar 

  • Divya K, Sankar M (2009) Entomopathogenic nematodes in pest management. Indian J Sci Technol. https://doi.org/10.17485/ijst/2009/v2i7/29499

  • Downes S, Parker TL, Mahon RJ (2009) Frequency of alleles conferring resistance to the Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in Australian populations of Helicoverpa punctigera (Lepidoptera: Noctuidae) from 2002 to 2006. J Econ Entomol 102(2):733–742. https://doi.org/10.1603/0022-0493(2007)100{[}1844:FOACRT]2.0.CO;2

    Article  CAS  Google Scholar 

  • Evans EW (2009) Lady beetles as predators of insects other than Hemiptera. Biol Control 46:590–596

    Google Scholar 

  • Farnham AW, Sawicki RM (1976) Development of resistance to pyrethroids in insects resistant to other insecticides. Pestic Sci 7:278–282. https://doi.org/10.1002/ps.2780070312

    Article  CAS  Google Scholar 

  • Feng HQ, Wu KM, Cheng DF, Guo YY (2003) Radar observations of the autumn migration of the beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) and other moths in northern China. Bull Entomol Res 93(2):115–124. https://doi.org/10.1079/BER2002221

    Article  Google Scholar 

  • Ferrer F (2001) Biological control of agricultural insect pest in Venezuela; advances, achievements, and future perspectives. 67–74

  • Feyereisen R (2011) Arthropod CYPomes illustrate the tempo and mode in P450 evolution. Biochim Biophys Acta - Proteins Proteomics 1814:19–28

    Article  CAS  Google Scholar 

  • Feyereisen R (2005) Insect cytochrome P450. In: Comprehensive molecular insect science. pp 1–77

  • Feyereisen R (2006) Evolution of insect P450. Biochem Soc Trans 1866:141–154. https://doi.org/10.1042/BST0341252

    Article  Google Scholar 

  • FIELD LM, (2000) Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). Biochem J 3:863–868. https://doi.org/10.1042/bj3490863

    Article  Google Scholar 

  • Lm F, Rl B, Tyler-Smith C, Al D (1999) Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). Biochem J 3:737–742. https://doi.org/10.1042/0264-6021:3390737

    Article  Google Scholar 

  • Field LM, Devonshire AL (1997) Structure and organization of amplicons containing the E4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer). Biochem J 3:867–871. https://doi.org/10.1042/bj3220867

    Article  Google Scholar 

  • Gao M, Mu W, Wang W et al (2014) Resistance mechanisms and risk assessment regarding indoxacarb in the beet armyworm, Spodoptera exigua. Phytoparasitica 42:585–594

    Article  CAS  Google Scholar 

  • Garzón A, Medina P, Amor F et al (2015) Toxicity and sublethal effects of six insecticides to last instar larvae and adults of the biocontrol agents Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Adalia bipunctata (L.) (Coleoptera: Coccinellidae). Chemosphere 132:87–93

    Article  Google Scholar 

  • Gay H (2012) Before and after Silent Spring : from chemical pesticides to biological control and integrated pest management — Britain, 1945–1980. Ambix. https://doi.org/10.1179/174582312X13345259995930

    Article  Google Scholar 

  • Ghumare SS, Mukherjee SN, Sharma RN (1989) Effect of rutin on the neonate sensitivity, dietary utilization and mid-gut carboxylesterase activity of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Proc Anim Sci 98:399–404. https://doi.org/10.1007/BF03179652

    Article  CAS  Google Scholar 

  • Giolo FP, Medina P, Grützmacher AD, Viñuela E (2009) Effects of pesticides commonly used in peach orchards in Brazil on predatory lacewing Chrysoperla carnea under laboratory conditions. BioControl. 54, pages625–635 https://doi.org/10.1007/s10526-008-9197-2

  • Golikhajeh N, Naseri B, Razmjou J (2016) Effect of geographic population and host cultivar on demographic parameters of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). J Asia Pac Entomol 19:743–751. https://doi.org/10.1016/j.aspen.2016.07.002

    Article  Google Scholar 

  • Gong C, Yao X, Yang Q et al (2021) Fitness costs of chlorantraniliprole resistance related to the senpf overexpression in the spodoptera exigua (Lepidoptera: Noctuidae). Int J Mol Sci 22:5027. https://doi.org/10.3390/ijms22095027

    Article  CAS  Google Scholar 

  • Greenberg SM, Sappington TW, Liu T-X, et al (2006) Feeding and life history of Spodoptera exigua (Lepidoptera: Noctuidae) on different host plants. Ann Entomol Soc Am. 94: 566–575 https://doi.org/10.1603/0013-8746(2001)094[0566:falhos]2.0.co;2

  • Greenberg SM, Showler AT, Liu TX (2005) Effects of neem-based insecticides on beet armyworm (Lepidoptera: Noctuidae). Insect Sci 12:17–23. https://doi.org/10.1111/j.1672-9609.2005.00003.x

    Article  CAS  Google Scholar 

  • Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62. https://doi.org/10.1146/annurev-ento-010715-023646

    Article  CAS  Google Scholar 

  • Guo J, Wu S, Zhang F, et al (2020) Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review. BioControl pages 647–662

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    Article  CAS  Google Scholar 

  • Hafeez M, Liu S, Jan S et al (2019) Gossypol-induced fitness gain and increased resistance to deltamethrin in beet armyworm, Spodoptera exigua (Hübner). Pest Manag Sci 76:683–693. https://doi.org/10.1002/ps.5165

    Article  CAS  Google Scholar 

  • Hasan W (2010) Evaluation of some insecticides against spotted bollworm, Earias vittella (Fab.) on different okra cultivars. Trends Biosci. 3

  • Heckel DG (2012) Insecticide resistance after silent spring. Science 337:1612–1614

    Article  Google Scholar 

  • Heidari R, Devonshire AL, Campbell BE et al (2004) Hydrolysis of organophosphorus insecticides by in vitro modified carboxylesterase E3 from Lucilia cuprina. Insect Biochem Mol Biol 34:353–363. https://doi.org/10.1016/j.ibmb.2004.01.001

    Article  CAS  Google Scholar 

  • Hemingway J (2000) The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochem Mol Biol 30:1009–1015

    Article  CAS  Google Scholar 

  • Hemingway J, Ranson H, Magill A et al (2016) Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet 387:1785–1788. https://doi.org/10.1016/S0140-6736(15)00417-1

    Article  Google Scholar 

  • Hendrichs J, Robinson A (2009) Sterile insect technique. In: Encyclopedia of insects

  • Hong-Lun Bi, Jun Xu A-JT and Y-PH (2016b) CRISPR/Cas9-mediated targeted gene mutagenesis in Spodoptera litura. Insect Sci 23:469–477

  • Hu B, Zhang SH, Ren MM, et al (2017) The expression of Spodoptera exigua P450 and UGT genes: tissue specificity and response to insecticides. Insect Sci. 199–216.

  • Hurst GW (1964) Meteorological aspects of the migration to Britain of Laphygma exigua and certain other moths on specific occasions. Agric Meteorol 1:271–281

    Article  Google Scholar 

  • Hussain S, Sørensen SR, Devers-Lamrani M et al (2009) Characterization of an isoproturon mineralizing bacterial culture enriched from a French agricultural soil. Chemosphere 77:1052–1059. https://doi.org/10.1016/j.chemosphere.2009.09.020

    Article  CAS  Google Scholar 

  • Ishtiaq M, Saleem MA, Razaq M (2012) Monitoring of resistance in Spodoptera exigua (Lepidoptera: Noctuidae) from four districts of the Southern Punjab, Pakistan to four conventional and six new chemistry insecticides. Crop Prot 33:13–20

    Article  CAS  Google Scholar 

  • Ishtiaq MSM, RM, (2012) Monitoring of resistance in Spodoptera exigua (Lepidoptera: Noctuidae) from four districts of the Southern Punjab, Pakistan to four conventional and six new chemistry insecticides. Crop Prot 33:13–20

    Article  CAS  Google Scholar 

  • Jarvis DII, Padoch C, Cooper HDD (2013) Managing biodiversity in agricultural ecosystems. 512. https://doi.org/10.7312/jarv13648

  • Jiang XF, Luo LZ, Sappington TW (2010) Relationship of flight and reproduction in beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight syndrome. J Insect Physiol y 56:1631. https://doi.org/10.1016/j.jinsphys.2010.06.006

    Article  CAS  Google Scholar 

  • Kadous AA, Ghiasuddin SM, Matsumura F et al (1983) Difference in the picrotoxinin receptor between the cyclodiene-resistant and susceptible strains of the German cockroach. Pestic Biochem Physiol 19:157–166. https://doi.org/10.1016/0048-3575(83)90135-9

    Article  CAS  Google Scholar 

  • Kang S, Lee HJ, Kim YH et al (2012) Proteomics-based identification and characterization of biotype-specific carboxylesterase 2 putatively associated with insecticide resistance in Bemisia tabaci. J Asia Pac Entomol 15:389–396. https://doi.org/10.1016/j.aspen.2012.03.002

    Article  CAS  Google Scholar 

  • Kapoor D, Khan A, O’Donnell MJ, Kolosov D (2021) Novel mechanisms of epithelial ion transport: insights from the cryptonephridial system of lepidopteran larvae. Curr. Opin. Insect Sci. 53–61

  • Karimi-Malati A, Fathipour Y, Talebi AA, Bazoubandi M (2012) Comparative life table parameters of beet armyworm, Spodoptera exigua (Lep.: Noctuidae), on four commercial sugar beet cultivars. J Entomol Soc Iran 32:109–124

    Google Scholar 

  • Keïta M, Kané F, Thiero O et al (2020) Acetylcholinesterase (ace-1R) target site mutation G119S and resistance to carbamates in Anopheles gambiae (sensu lato) populations from Mali. Parasit Vectors 13:283. https://doi.org/10.1186/s13071-020-04150-x

    Article  CAS  Google Scholar 

  • Kerns DL PJ and TT (1998) Resistance of field strains of beet armyworm (Lepidoptera: Noctuidae) from Arizona and California to carbamate insecticides. J Econ Entomol 91:1038–1043

  • Khan Mz, Law Fcp (2005) Adverse effects of pesticides and related chemicals on enzyme and hormone systems of fish, amphibians and reptiles: a review. Law Proc Pakistan Acad Sci. 42(4)

  • Klatt BK, Rundlöf M, Smith HG (2016) Maintaining the restriction on neonicotinoids in the European Union—benefits and risks to bees and pollination services. Front Ecol Evol. https://doi.org/10.3389/fevo.2016.00004

    Article  Google Scholar 

  • Knox C, Moore SD, Luke GA, Hill MP (2015) Baculovirus-based strategies for the management of insect pests: a focus on development and application in South Africa. Biocontrol Sci Technol 25:1–20

    Article  Google Scholar 

  • Kumano N, Haraguchi D, Kohama T (2008) Effect of irradiation on mating performance and mating ability in the West Indian sweetpotato weevil. Euscepes Postfasciatus Entomol Exp Appl 127:229–236. https://doi.org/10.1111/j.1570-7458.2008.00706.x

    Article  Google Scholar 

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI et al (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41. https://doi.org/10.1016/j.jip.2015.07.009

    Article  CAS  Google Scholar 

  • Lai T, Li J, Su J (2011) Monitoring of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) resistance to chlorantraniliprole in China. Pestic Biochem Physiol 101:198–205. https://doi.org/10.1016/j.pestbp.2011.09.006

    Article  CAS  Google Scholar 

  • Lai T, Su J (2011) Assessment of resistance risk in Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Manag Sci 67:1468–1472. https://doi.org/10.1002/ps.2201

    Article  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. https://doi.org/10.1146/annurev.ento.51.110104.151104

    Article  CAS  Google Scholar 

  • Liu C, Liu Y, Walker WB et al (2013) Identification and functional characterization of sex pheromone receptors in beet armyworm Spodoptera exigua (Hübner). Insect Biochem Mol Biol 43:747–754

    Article  CAS  Google Scholar 

  • Liu YH, Chung YC, Xiong Y (2001) Purification and characterization of a dimethoate-degrading enzyme of Aspergillus niger ZHY256. Isolated from Sewage Appl Environ Microbiol 67:3746–3749. https://doi.org/10.1128/AEM.67.8.3746-3749.2001

    Article  CAS  Google Scholar 

  • Liu YJ, Shen JL, Jia B (2002) Occurrence and resistance status of the beet armyworm, Spodoptera exigua (Hubner). Cott Sci 14:305–309

    Google Scholar 

  • Malekmohammadi M, Galehdari H (2016) Target site insensitivity mutations in the AChE enzyme confer resistance to organophosphorous insecticides in Leptinotarsa decemlineata (Say). Pestic Biochem Physiol 126:85–91. https://doi.org/10.1016/j.pestbp.2015.08.002

    Article  CAS  Google Scholar 

  • MIKKOLA (1970) The interpretation of long-range migrations of Spodoptera exigua Hb. (Lepidoptera : Noctuidae). J Anim Ecol 39:593–598

    Article  Google Scholar 

  • Ming Li, Omar S. Akbari BJW (2017) Highly efficient site-specific mutagenesis in malaria mosquitoes using CRISPR. Genes|Genomes|Genetics 8: 653–658

  • Nelson DR (2011) Progress in tracing the evolutionary paths of cytochrome P450. Biochim Biophys Acta - Proteins Proteomics 14:14–18. https://doi.org/10.1016/j.bbapap.2010.08.008

    Article  CAS  Google Scholar 

  • Nicolas D, Axel D, Jean-Marie D (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

  • Oakeshott JG, Farnsworth CA, East PD, et al (2013) How many genetic options for evolving insecticide resistance in heliothine and spodopteran pests? Pest Manag. Sci. 889–96

  • Oliveira CM, Auad AM, Mendes SM, Frizzas MR (2014) Crop losses and the economic impact of insect pests on Brazilian agriculture. Crop Prot 56:50–54

    Article  Google Scholar 

  • Peng Z, Ming G, Wei M et al (2014) Resistant levels of Spodoptera exigua to eight various insecticides in Shandong. China J Pestic Sci 39:7–13

    Article  Google Scholar 

  • Peralta C, Palma L (2017) Is the insect world overcoming the efficacy of bacillus thuringiensis? Toxins (Basel).

  • Pesticides Safety Directorate (2008) Assessment of the impact on crop protection in the UK of the ‘cut-off criteria’ and substitution provisions in the proposed Regulation of the European Parliament and of the Council concerning the placing of plant protection products in the market. Pestic Saf Dir UK, p 46

  • Pooggin MM (2017) RNAi-mediated resistance to viruses: a critical assessment of methodologies. Curr Opin Virol 26:28–35

    Article  CAS  Google Scholar 

  • Popp J, Hantos K (2013) The impact of crop protection on agricultural production. Stud Agric Econ. https://doi.org/10.7896/j.1003

    Article  Google Scholar 

  • Qiu L, Hou L, Zhang B, et al (2015) Cadherin is involved in the action of Bacillus thuringiensis toxins Cry1Ac and Cry2Aa in the beet armyworm, Spodoptera exigua. J Invertebr Pathol. 127:47-53 https://doi.org/10.1016/j.jip.2015.02.009

  • Rabelo MM, Paula-Moraes SV, Pereira EJG, Siegfried BD (2020) Contrasting susceptibility of lepidopteran pests to diamide and pyrethroid insecticides in a region of overwintering and migratory intersection. Pest Manag Sci 76:4240–4247. https://doi.org/10.1002/ps.5984

    Article  CAS  Google Scholar 

  • Ranson H, Edi CVA, Koudou BG, et al (2012) Multiple-insecticide resistance in anopheles gambiae mosquitoes, southern côte d’ivoire. Emerg Infect Dis. 18:1508–11 https://doi.org/10.3201/eid1809.120262

  • Reddy GV (2011) Comparative effect of integrated pest management and farmers’ standard pest control practice for managing insect pests on cabbage (Brassica spp.). Pest Manag Sci 67:980–985. https://doi.org/10.1002/ps.2142

    Article  CAS  Google Scholar 

  • Riga M, Bajda S, Themistokleous C et al (2017) The relative contribution of target-site mutations in complex acaricide resistant phenotypes as assessed by marker assisted backcrossing in Tetranychus urticae. Sci Rep 7:9202. https://doi.org/10.1038/s41598-017-09054-y

    Article  CAS  Google Scholar 

  • Rosell G, Quero C, Coll J, Guerrero A (2008) Biorational insecticides in pest management. J Pestic Sci 33:103–121. https://doi.org/10.1584/jpestics.r08-01

    Article  CAS  Google Scholar 

  • Saeed S, Sayyed AH, Ahmad I (2010) Effect of host plants on life-history traits of Spodoptera exigua (Lepidoptera: Noctuidae). J Pest Sci. 83: 165–172

  • Sappington TW, Miller NJ (2017) Editorial overview: Pests and resistance: shedding the albatross of resistance starts by embracing the ecological complexities of its evolution. Curr. Opin. Insect Sci. 21:v–viii

  • Sarfraz M, Keddie AB, Dosdall LM (2005) Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Sci Technol 15:763–789

    Article  Google Scholar 

  • Satpathy S, Shivalingaswamy TM, Kumar A et al (2010) Potentiality of Chinese cabbage (Brassica rapa subsp. pekinensis) as a trap crop for diamondback moth (Plutella xylostella) management in cabbage. Indian J Agric Sci 80:238–241

    Google Scholar 

  • Schuler MA (2011) P450s in plant-insect interactions. Biochim Biophys Acta - Proteins Proteomics 1814:36–45

    Article  CAS  Google Scholar 

  • Segal DJ, Meckler JF (2013) Genome engineering at the dawn of the golden age. Annu Rev Genomics Hum Genet 14:135–158. 

  • Sertkaya E, Bayram A, Kornosor S (2004) Egg and larval parasitoids of the beet armyworm spodoptera exigua on Maize in Turkey. Phytoparasitica 32(3):305–312

  • Shelton A, Perez C, Tang J, Vandenberg J (1997) Prospects for novel approaches towards management of the diamondback moth. In: The management of diamondback moth and other crucifer pests

  • SINGH SP, ZIMNIAK P, SAWICKI R, et al (2003) Cloning, expression and biochemical characterization of one Epsilon-class (GST-3) and ten Delta-class (GST-1) glutathione S-transferases from Drosophila melanogaster, and identification of additional nine members of the Epsilon class. Biochem J.370: 661–669 https://doi.org/10.1042/bj20021287

  • Slawik C, Rickmeyer C, Brehm M et al (2017) Glutathione adduct patterns of Michael-acceptor carbonyls. Environ Sci Technol 51:4018–4026. https://doi.org/10.1021/acs.est.6b04981

    Article  CAS  Google Scholar 

  • Smagghe G, Dhadialla TS, Derycke S, et al (1998) Action of the ecdysteroid agonist tebufenozide in susceptible and artificially selected beet armyworm. Pestic Sci.

  • Sparks TC, Nauen R (2015) IRAC: Mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128. https://doi.org/10.1016/j.pestbp.2014.11.014

    Article  CAS  Google Scholar 

  • Su J, Sun XX (2014) High level of metaflumizone resistance and multiple insecticide resistance in field populations of Spodoptera exigua (Lepidoptera: Noctuidae) in Guangdong Province. China Crop Prot 61:58–63. https://doi.org/10.1016/j.cropro.2014.03.013

    Article  CAS  Google Scholar 

  • Subramanian S, Muthulakshmi M (2016) Entomopathogenic nematodes. In: ecofriendly pest management for food security. 367–410

  • Sutherland TD, Weir KM, Lacey MJ et al (2002) Enrichment of a microbial culture capable of degrading endosulphate, the toxic metabolite of endosulfan. J Appl Microbiol 92:541–548. https://doi.org/10.1046/j.1365-2672.2002.01559.x

    Article  CAS  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594. https://doi.org/10.1146/annurev.ento.47.091201.145240

    Article  CAS  Google Scholar 

  • Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y (2008) Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 199–202

  • Tabashnik BE, Liesner LR, Ellsworth PC et al (2020) Transgenic cotton and sterile insect releases synergize eradication of pink bollworm a century after it invaded the United States. Proc Natl Acad Sci U S A 118(1):e2019115118. https://doi.org/10.1073/pnas.2019115118

    Article  CAS  Google Scholar 

  • Tang QL, Ma KS, Hou YM, Gao XW (2017) Monitoring insecticide resistance and diagnostics of resistance mechanisms in the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) in China. Pestic Biochem Physiol 143:39–47. https://doi.org/10.1016/j.pestbp.2017.09.013

    Article  CAS  Google Scholar 

  • Taylor JE, Riley DG (2008) Artificial infestations of beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), used to estimate an economic injury level in tomato. Crop Prot 27:268–274

    Article  Google Scholar 

  • Thailayil J, Magnusson K, Godfray HCJ et al (2011) Spermless males elicit large-scale female responses to mating in the malaria mosquito Anopheles gambiae. Proc Natl Acad Sci 108:13677–13681. https://doi.org/10.1073/pnas.1104738108

    Article  Google Scholar 

  • Tian H, Peng H, Yao Q et al (2009) Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS ONE 13:e6225. https://doi.org/10.1371/journal.pone.0006225

    Article  CAS  Google Scholar 

  • Tian X, Liu J, Guo Z et al (2018a) The characteristics of voltage-gated sodium channel and the association with lambda cyhalothrin resistance in Spodoptera exigua. J Asia Pac Entomol 21:1020–1027. https://doi.org/10.1016/j.aspen.2018.07.013

    Article  Google Scholar 

  • Tian X, Liu J, Guo Z et al (2018b) The characteristics of voltage-gated sodium channel and the association with lambda cyhalothrin resistance in Spodoptera exigua. J Asia Pac Entomol 21:1020–1027. https://doi.org/10.1016/j.aspen.2018.07.013

    Article  Google Scholar 

  • Tian X, Sun X, Su J (2014) Biochemical mechanisms for metaflumizone resistance in beet armyworm, Spodoptera exigua. Pestic Biochem Physiol 113:8–14. https://doi.org/10.1016/j.pestbp.2014.06.010

    Article  CAS  Google Scholar 

  • Tindall KV, Siebert MW, Leonard BR et al (2009) Efficacy of Cry1Ac:Cry1F proteins in cotton leaf tissue against fall armyworm, beet armyworm, and Soybean Looper (Lepidoptera: Noctuidae). J Econ Entomol 102:1497–1505. https://doi.org/10.1603/029.102.0414

    Article  CAS  Google Scholar 

  • Togola A, Boukar O, Belko N, et al (2017) Host plant resistance to insect pests of cowpea (Vigna unguiculata L. Walp.): achievements and future prospects. Euphytica 213:239

  • Tong F, Coats JR (2012) Quantitative structure-activity relationships of monoterpenoid binding activities to the housefly GABA receptor. Pest Manag Sci 68:1122–1129. https://doi.org/10.1002/ps.3280

    Article  CAS  Google Scholar 

  • Troczka BJ, Williamson MS, Field LM, Davies TGE (2017) Rapid selection for resistance to diamide insecticides in Plutella xylostella via specific amino acid polymorphisms in the ryanodine receptor. Neurotoxicology 60:224–233. https://doi.org/10.1016/j.neuro.2016.05.012

    Article  CAS  Google Scholar 

  • Ullah F, Gul H, Desneux N et al (2019) Clothianidin-induced sublethal effects and expression changes of vitellogenin and ecdysone receptors genes in the melon aphid, Aphis gossypii. Entomol Gen 39:137–149. https://doi.org/10.1127/entomologia/2019/0865

    Article  Google Scholar 

  • Umbanhowar J, Hastings A (2002) The impact of resource limitation and the phenology of parasitoid attack on the duration of insect herbivore outbreaks. Theor Popul Biol 62:259–269. https://doi.org/10.1006/tpbi.2002.1617

    Article  Google Scholar 

  • Van Laecke K, Smagghe G, Degheele D (1995) Detoxifying enzymes in greenhouse and laboratory strain of beet armyworm (Lepidoptera: Noctuidae). J Econ Entomol 88:777–781. https://doi.org/10.1093/jee/88.4.777

    Article  Google Scholar 

  • Van Steenwyk RA, Toscano NC (2015) Relationship between lepidopterous larval density and damage in celery and celery plant growth analysis1. J Econ Entomol 20:709–726. https://doi.org/10.1093/jee/74.3.287

    Article  Google Scholar 

  • Varshney R, Poornesha B, Raghavendra A et al (2021) Biocontrol-based management of fall armyworm, Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae) on Indian maize. J Plant Dis Prot 128:87–95. https://doi.org/10.1007/s41348-020-00357-3

    Article  Google Scholar 

  • Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771

    Article  CAS  Google Scholar 

  • Vaughan A, Hawkes N, Hemingway J (1997) Co-amplification explains linkage disequilibrium of two mosquito esterase genes in insecticide-resistant Culex quinquefasciatus. Biochem J 325:359–365. https://doi.org/10.1042/bj3250359

    Article  CAS  Google Scholar 

  • Vontas JG, Small GJ, Hemingway J (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 357:65–72. https://doi.org/10.1042/bj3570065

    Article  CAS  Google Scholar 

  • Vontas JG, Small GJ, Nikou DC et al (2002) Purification, molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the rice brown planthopper. Nilaparvata Lugens Biochem J 362:329–337. https://doi.org/10.1042/0264-6021:3620329

  • Wang KY, Jiang XY, Yi MQCB, XX, (2002) Insecticide resistance of Spodoptera exigua. Acta Phytophylacica Sin 29:229–234

    CAS  Google Scholar 

  • Wang LL, Huang Y, Lu XP et al (2015) Overexpression of two α-esterase genes mediates metabolic resistance to malathion in the oriental fruit fly, Bactrocera dorsalis (Hendel). Insect Mol Biol 24:467–479. https://doi.org/10.1111/imb.12173

    Article  CAS  Google Scholar 

  • Wang P, Yang F, Wang Y et al (2021) Monitoring the resistance of the beet armyworm (Lepidoptera: Noctuidae) to four insecticides in Southern China from 2014 to 2018. J Econ Entomol 144:332–338. https://doi.org/10.1093/jee/toaa290

    Article  CAS  Google Scholar 

  • Wang RL, Liu SW, Baerson SR et al (2018a) Identification and functional analysis of a novel cytochrome P450 gene CYP9A105 associated with pyrethroid detoxification in spodoptera exigua hübner. Int J Mol Sci 19:737. https://doi.org/10.3390/ijms19030737

    Article  CAS  Google Scholar 

  • Wang X, Chen Y, Gong C et al (2018b) Molecular identification of four novel cytochrome P450 genes related to the development of resistance of Spodoptera exigua (Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Manag Sci 74:1938–1952

    Article  CAS  Google Scholar 

  • Wang X, Huang Q, Hao Q et al (2018c) Insecticide resistance and enhanced cytochrome P450 monooxygenase activity in field populations of Spodoptera litura from Sichuan, China. Crop Prot 106:110–116. https://doi.org/10.1016/j.cropro.2017.12.020

    Article  CAS  Google Scholar 

  • Wang X, Xiang X, Yu H et al (2018d) Monitoring and biochemical characterization of beta-cypermethrin resistance in Spodoptera exigua (Lepidoptera: Noctuidae) in Sichuan Province. China Pestic Biochem Physiol 146:71–79. https://doi.org/10.1016/j.pestbp.2018.02.008

    Article  CAS  Google Scholar 

  • Whyard S, Downe AER, Walker VK (1995) Characterization of a novel esterase conferring insecticide resistance in the mosquito Culex tarsalis. Arch Insect Biochem Physiol 29:329–342. https://doi.org/10.1002/arch.940290402

    Article  CAS  Google Scholar 

  • Whyard S, Erdelyan CNG, Partridge AL et al (2015) Silencing the buzz: a new approach to population suppression of mosquitoes by feeding larvae double-stranded RNAs. Parasit Vectors 12(8):96. https://doi.org/10.1186/s13071-015-0716-6

    Article  Google Scholar 

  • Wolfenbarger DA, Wolfenbarger DJ (2010) Beet armyworm (Lepidoptera: Noctuidae): selection for resistance to insecticides by a five strain cross. Trop Agric 87:175–181

    Google Scholar 

  • Xu C, Zhang Z, Cui K, et al (2017) Effects of sublethal concentrations of cyantraniliprole on the development, fecundity and nutritional physiology of the black cutworm (Lepidoptera: Noctuidae). PLoS One 11:11(6): e0156555. doi:https://doi.org/10.1371/journal.pone.0156555

  • Yates SR, Wang D, Papiernik SK, Gan J (2002) Predicting pesticide volatilization from soils. Environmetrics 13:569–578. https://doi.org/10.1002/env.542

    Article  CAS  Google Scholar 

  • Yayun Zuo, Hui Wang, Yanjun Xu, Jianlei Huang, Shuwen Wu, Yidong Wu YY (2017) CRISPR/Cas9 mediated G4946E substitution in the ryanodine receptor of Spodoptera exigua confers high levels of resistance to diamide insecticides. Insect Biochem Mol Biol 89:79–85

  • Yencho GC, Cohen MB, Byrne PF (2000) Applications of tagging and mapping insect resistance loci in plants. Annu Rev Entomol 45:393–422. https://doi.org/10.1146/annurev.ento.45.1.393

    Article  CAS  Google Scholar 

  • Yousafi Q, Sarfaraz A, Saad Khan M et al (2021) In silico annotation of unreviewed acetylcholinesterase (AChE) in some lepidopteran insect pest species reveals the causes of insecticide resistance. Saudi J Biol Sci 28:2197–2209. https://doi.org/10.1016/j.sjbs.2021.01.007

    Article  CAS  Google Scholar 

  • Zeng R Sen, Wen Z, Niu G, et al (2007) Allelochemical induction of cytochrome P450 monooxygenases and amelioration of xenobiotic toxicity in Helicoverpa zea. J Chem Ecol. 33: 449-61 https://doi.org/10.1007/s10886-006-9238-1

  • Zhang B, Liu H, Helen HS, Wang JJ (2011) Effect of host plants on development, fecundity and enzyme activity of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Agric Sci China 10:1232–1240. https://doi.org/10.1016/S1671-2927(11)60114-4

    Article  CAS  Google Scholar 

  • Zhang J, Khan SA, Heckel DG, Bock R (2017) Next-generation insect-resistant plants: RNAi-mediated crop protection. Trends Biotechnol 35:871–882

    Article  CAS  Google Scholar 

  • Zhang J, Pelletier Y, Goyer C (2008) Identification of potential detoxification enzyme genes in Leptinotarsa decemlineata (Say) and study of their expression in insects reared on different plants. J Plant Sci 107:360–368. https://doi.org/10.4141/CJPS07001

    Article  Google Scholar 

  • Zheng XL, Cong XP, Wang XP, Lei CL (2011) A review of geographic distribution, overwintering and migration in spodoptera exigua H??bner (Lepidoptera: Noctuidae). J Entomol Res Soc 13:39–48

    Google Scholar 

  • Zhu F, Moural TW, Nelson DR et al (2016) A specialist herbivore pest adaptation to xenobiotics through up-regulation of multiple cytochrome P450s. Sci Rep. https://doi.org/10.1038/srep20421

    Article  Google Scholar 

  • Zhu KY, Palli SR (2020) Mechanisms, applications, and challenges of insect RNA interference. Annu. Rev. Entomol. 293–311

  • Zuo YY, Ma HH, Lu WJ et al (2020) Identification of the ryanodine receptor mutation I4743M and its contribution to diamide insecticide resistance in Spodoptera exigua (Lepidoptera: Noctuidae). Insect Sci 24:791–800. https://doi.org/10.1111/1744-7917.12695

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Key R&D Program of China (2017YFD0200400), the Key R&D Program of Zhejiang Province (2018C02032), and the National Natural Science Foundation of China (31570387; 31901885). M. Imran extended their appreciation to the Deanship of Scientific Research at King Khalid University for funding through general research grant number GRP. 203/42 and project funded by China Postdoctoral Science Foundation (233952).

Author information

Authors and Affiliations

  1. State Key Laboratory for Managing Biotic and Chemical Threats To the Quality and Safety of Agro-Products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, People’s Republic of China

    Muhammad Hafeez, Xiaowei Li, Zhijun Zhang & Yaobin Lu

  2. Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, 100193, China

    Farman Ullah

  3. Key Laboratory of Bio-Pesticide Innovation and Application, Guangdong Province, South China Agricultural University, Guangzhou, 510642, China

    Muhammad Musa Khan

  4. Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, 430070, Hubei, People’s Republic of China

    Sakhawat Shah

  5. Department of Chemistry, Faculty of Science, King Khalid University, P.O. Box 9004, Abha, 61413, Saudi Arabia

    Muhammad Imran & Mohammed A. Assiri

  6. Natural Resources Institute, University of Greenwich, Chatham Maritime, Kent, ME4 4TB, UK

    G. Mandela Fernández-Grandon

  7. UMR ISA, Université Côte d’Azur, INRAE, CNRS, 06000, Nice, France

    Nicolas Desneux

  8. School of Agriculture, Yunnan University, Kunming, 650504, Yunnan, China

    Muzammal Rehman

  9. Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, College of Tropical Crops, Hainan University, Haikou, 570228, Hainan, China

    Shah Fahad

  10. Department of Agronomy, University of Haripur, Khyber Pakhtunkhwa, 22620, Pakistan

    Shah Fahad

Authors
  1. Muhammad Hafeez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farman Ullah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Musa Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaowei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhijun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sakhawat Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Muhammad Imran
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mohammed A. Assiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. G. Mandela Fernández-Grandon
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nicolas Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Muzammal Rehman
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Shah Fahad
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Yaobin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MH, XL, and YL conceived the idea and designed the study. MH performed all bioassays. ZZ, JZ, FU, SS, JH, MAA, ND, and MMH made a significant contribution to molecular and application assays of dsRNAs. MH, MMK, XYR, and SZ conducted statistical analyses and wrote the manuscript. SF, MR, MH, YL, MFG, and MI reviewed and approved the manuscript.

Corresponding authors

Correspondence to Shah Fahad or Yaobin Lu.

Ethics declarations

Ethics approval and consent to participate

We all declare this manuscript reports studies that do not involve any human participants, human data, or human tissue. So, ethics approval and consent to participate are not applicable.

Consent for publication

Our manuscript does not contain data from any individual person, so consent for publication is not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hafeez, M., Ullah, F., Khan, M.M. et al. Metabolic-based insecticide resistance mechanism and ecofriendly approaches for controlling of beet armyworm Spodoptera exigua: a review. Environ Sci Pollut Res 29, 1746–1762 (2022). https://doi.org/10.1007/s11356-021-16974-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-16974-w

Keywords

Search

Navigation