Skip to main content

Advertisement

SpringerLink
Log in

The effect of chlorantraniliprole on the transcriptomic profile of Spodoptera frugiperda: a typical case analysis for the response of a newly invaded pest to an old insecticide

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

Chlorantraniliprole is a diamide insecticide widely used in China over the last 15 years. The fall armyworm (FAW), Spodoptera frugiperda, newly invaded China in 2019. The response of FAW to chlorantraniliprole deserves more attention, in the context of many destructive lepidopteran species are resistant to diamide insecticides and the patent on core chemical of chlorantraniliprole in China expired in August 2022.

Methods and results

This study investigated the response profile in larvae under chlorantraniliprole-induced (LC50) stress using methods of bioassay, RNA-Seq and qPCR. We observed growth inhibition and lethal effects in FAW larvae, but at a relatively high LC50 value compared to other several pests. Additionally, under chlorantraniliprole-induced stress, 3309 unigenes were found to be differentially expressed genes. The impacted genes included 137 encoding for detoxification enzymes, 29 encoding for cuticle proteins, and 20 key enzymes involved in the chitin metabolism, which all associated with metabolic resistance. Finally, we obtained the single nucleotide polymorphisms (SNPs) of two RyR genes, which are the target proteins for chlorantraniliprole. We also investigated the causes of the high LC50 value in our FAW, which possibly related to the stabilized 4743 M on SNP frequency of RyR. These findings documented the genetic background of RyR of FAW and indicated that application of chlorantraniliprole has a high risk of controlling FAW in China.

Conclusion

In brief, our results provide a better understanding of the mechanisms of chlorantraniliprole toxicity and detoxification in FAW, and will aid in monitoring the development of resistant strains for a newly pest to an old insecticide.

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
Fig. 5

Similar content being viewed by others

Data availability

The six datasets generated and analyzed during the current study are available in the NCBI SRA database with the accession number of SRA: SRS15030502, SRS15030503, SRS15030520 (chlorantraniliprole-induced groups), and the accession number of SRA:SRS15030504, SRS15030505, SRS15030506 (control groups) (https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA877689).

References

  1. Wang R, Jiang C, Guo X, Chen D, You C, Zhang Y et al (2019) Potential distribution of Spodoptera frugiperda (J.E. Smith) in China and the major factors influencing distribution. Global Ecol Conserv 21:e00865. https://doi.org/10.1016/j.gecco.2021.e01994

    Article  Google Scholar 

  2. Sattelle DB, Cordova D, Cheek TR (2008) Insect ryanodine receptors: molecular targets for novel pest control chemicals. Invert Neurosci 8(3):107–119. https://doi.org/10.1007/s10158-008-0076-4

    Article  CAS  PubMed  Google Scholar 

  3. Richardson EB, Troczka BJ, Gutbrod O, Davies TGE, Nauen R (2020) Diamide resistance: 10 years of lessons from lepidopteran pests. J Pest Sci 93:911–928. https://doi.org/10.1007/s10340-020-01220-y

    Article  Google Scholar 

  4. Su JY, Lai T, Li J (2012) Susceptibility of field populations of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in China to chlorantraniliprole and the activities of detoxification enzymes. Crop Prot 42:217–222. https://doi.org/10.1016/j.cropro.2012.06.012

    Article  CAS  Google Scholar 

  5. Adams A, Gore J, Catchot A, Musser F, Cook D, Krishnan N (2016) Susceptibility of Helicoverpa zea (Lepidoptera: Noctuidae) neonates to Diamide Insecticides in the Midsouthern and Southeastern United States. J Econ Entomol 109(5):2205–2209. https://doi.org/10.1093/jee/tow175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ribeiro LM, Siqueira HA, Wanderley-Teixeira V, Ferreira HN, Silva V, Silva JE et al (2017) Field resistance of brazilian plutella xylostella to diamides is not metabolism-mediated. Crop Prot 93:82–88. https://doi.org/10.1016/j.cropro.2016.11.027

    Article  CAS  Google Scholar 

  7. Samurkas A, Yao L, Hadiatullah H, Ma R, Xie Y, Sundarraj R et al (2022) Ryanodine receptor as insecticide target. Curr Pharm Des 28(1):26–35. https://doi.org/10.2174/1381612827666210902150224

    Article  CAS  PubMed  Google Scholar 

  8. Boaventura D, Bolzan A, Padovez FE, Okuma DM, Omoto C, Nauen R (2020) Detection of a ryanodine receptor target-site mutation in diamide insecticide resistant fall armyworm, Spodoptera frugiperda. Pest Manage Sci 76(1):47–54. https://doi.org/10.1002/ps.5505

    Article  CAS  Google Scholar 

  9. Li X, Guo L, Zhou X, Gao X, Liang P (2015) miRNAs regulated overexpression of ryanodine receptor is involved in chlorantraniliprole resistance in Plutella xylostella (L.). Sci Rep 5:14095. https://doi.org/10.1038/srep14095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009

    Article  CAS  PubMed  Google Scholar 

  11. Chao JT, Kong YZ, Wang Q, Sun YH, Gong DP, Lv J et al (2015) Mapgene2chrom, a tool to draw gene physical map based on perl and svg languages. Hereditas 37:91–97. https://doi.org/10.16288/j.yczz.2015.01.013

    Article  Google Scholar 

  12. He HL, Zhou AL, He L, Qiu L, Ding WB, Li YZ (2022) The frequency of cannibalism by Spodoptera frugiperda larvae determines their probability of surviving food deprivation. J Pest Sci 95:145–157. https://doi.org/10.1007/s10340-021-01371-6

    Article  CAS  Google Scholar 

  13. Wheelock CE, Shan G, Ottea J (2005) Overview of carboxylesterases and their role in the metabolism of insecticides. J Pest Sci 30:75–83. https://doi.org/10.1584/jpestics.30.75

    Article  CAS  Google Scholar 

  14. Xiao HM, Ye XH, Xu HX, Yang M, Yang Y, Chen X et al (2020) The genetic adaptations of fall armyworm Spodoptera frugiperda facilitated its rapid global dispersal and invasion. Mol Ecol Resour 20(4):1050–1068. https://doi.org/10.1111/1755-0998.13182

    Article  CAS  PubMed  Google Scholar 

  15. Steinbach D, Gutbrod O, Lümmen P, Matthiesen S, Schorn C, Nauen R (2015) Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella. Insect Biochem Mol Biol 63:14–22. https://doi.org/10.1016/j.ibmb.2015.05.001

    Article  CAS  PubMed  Google Scholar 

  16. Lutz AL, Bertolaccini I, Scotta RR, Curis MC, Favaro MA, Fernandez LN et al (2018) Lethal and sublethal effects of chlorantraniliprole on Spodoptera cosmioides (Lepidoptera: Noctuidae). Pest Manage Sci 74(12):2817–2821. https://doi.org/10.1002/ps.5070

    Article  CAS  Google Scholar 

  17. Lai T, Su JY (2011) Effects of chlorantraniliprole on development and reproduction of beet armyworm, Spodoptera exigua (Hübner). J Pest Sci 84:381–386. https://doi.org/10.1007/s10340-011-0366-1

    Article  Google Scholar 

  18. Huang L, Lu M, Han G, Du Y, Wang J (2016) Sublethal effects of chlorantraniliprole on development, reproduction and vitellogenin gene (CsVg) expression in the rice stem borer, Chilo suppressalis. Pest Manage Sci 72(12):2280–2286. https://doi.org/10.1002/ps.4271

    Article  CAS  Google Scholar 

  19. Gutiérrez-Moreno R, Mota-Sanchez D, Blanco CA, Whalon ME, Terán-Santofimio H, Rodriguez-Maciel JC et al (2019) Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to Synthetic Insecticides in Puerto Rico and Mexico. J Econ Entomol 112(2):792–802. https://doi.org/10.1093/jee/toy372

    Article  CAS  PubMed  Google Scholar 

  20. Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE 11(10):e0165632. https://doi.org/10.1371/journal.pone.0165632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Lv SL, Shi Y, Zhang JC, Liang P, Zhang L, Gao XW (2021) Detection of ryanodine receptor target-site mutations in diamide insecticide-resistant Spodoptera frugiperda in China. Insect Sci 28(3):639–648. https://doi.org/10.1111/1744-7917.12896

    Article  CAS  PubMed  Google Scholar 

  22. Li Q, Jin M, Yu S, Cheng Y, Shan Y, Wang P et al (2022) Knockout of the ABCB1 gene increases susceptibility to emamectin benzoate, beta-cypermethrin and chlorantraniliprole in Spodoptera frugiperda. Insects 13:137. https://doi.org/10.3390/insects13020137

    Article  PubMed  PubMed Central  Google Scholar 

  23. Li X, Li R, Zhu B, Gao X, Liang P (2018) Overexpression of cytochrome P450 CYP6BG1 may contribute to chlorantraniliprole resistance in Plutella xylostella (L.). Pest Manage Sci 74:1386–1393. https://doi.org/10.1002/ps.4816

    Article  CAS  Google Scholar 

  24. Mallott M, Hamm S, Troczka BJ, Randall E, Pym A, Grant G et al (2019) A flavin-dependent monooxgenase confers resistance to chlorantraniliprole in the diamondback moth, Plutella xylostella. Insect Biochem Mol Biol 115:103247. https://doi.org/10.1016/j.ibmb.2019.103247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Zhang BZ, Su X, Zhen CA, Lu LY, Li YS, Ge X et al (2020) Silencing of cytochrome P450 in Spodoptera frugiperda (Lepidoptera: Noctuidae) by RNA interference enhances susceptibility to chlorantraniliprole. J Insect Sci 20:1–7. https://doi.org/10.1093/jisesa/ieaa047

    Article  CAS  Google Scholar 

  26. Tan QM, Chen WW, Li HH, Liao SC, Yi GQ, Mei Y et al (2022) Adipokinetic hormone signaling regulates cytochrome P450-mediated chlorantraniliprole sensitivity in Spodoptera frugiperda (Lepidoptera: Noctuidae). Pest Manage Sci 78(6):2618–2628. https://doi.org/10.1002/ps.6896

    Article  CAS  Google Scholar 

  27. Zhang MY, Zhang P, Su X, Guo TX, Zhou JL, Zhang BZ et al (2022) MicroRNA-190-5p confers chlorantraniliprole resistance by regulating CYP6K2 in Spodoptera frugiperda (Smith). Pestic Biochem Physiol 184:105133. https://doi.org/10.1016/j.pestbp.2022.105133

    Article  CAS  PubMed  Google Scholar 

  28. Tang B, Yang M, Shen Q, Xu Y, Wang H, Wang S (2017) Suppressing the activity of trehalase with validamycin disrupts the trehalose and chitin biosynthesis pathways in the rice brown planthopper, Nilaparvata lugens. Pestic Biochem Physiol 137:81–90. https://doi.org/10.1016/j.pestbp.2016.10.003

    Article  CAS  PubMed  Google Scholar 

  29. Tao Y, Gutteridge S, Benner EA, Wu l, Rhoades DF, Sacher MD et al (2013) Identification of a critical region in the Drosophila ryanodine receptor that confers sensitivity to diamide insecticides. Insect Biochem Mol Biol 43(9):820–828. https://doi.org/10.1016/j.ibmb.2013.06.006

    Article  CAS  PubMed  Google Scholar 

  30. Roditakis E, Steinbach D, Moritz G, Vasakis E, Stavrakaki M, Ilias A et al (2017) Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Insect Biochem Mol Biol 80:11–20. https://doi.org/10.1002/ps.4439

    Article  CAS  PubMed  Google Scholar 

  31. Yao R, Zhao DD, Zhang S, Zhou LQ, Wang X, Gao CF et al (2017) Monitoring and mechanisms of insecticide resistance in Chilo suppressalis (Lepidoptera: Crambidae), with special reference to diamides. Pest Manage Sci 73:1169–1178. https://doi.org/10.1002/ps.4439

    Article  CAS  Google Scholar 

  32. Wei Y, Yan R, Zhou Q, Qiao L, Zhu G, Chen M (2019) Monitoring and mechanisms of Chlorantraniliprole Resistance in Chilo suppressalis (Lepidoptera: Crambidae) in China. J Econ Entomol 112(3):1348–1353. https://doi.org/10.1093/jee/toz001

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by the key research and development program of Hunan Province (China) (2020NK2034), Science and Technology Program of Changsha (kq2202226). The authors would like to thank Yi Zhou, Qiyao Liang, and Laili Deng for their help in S. frugiperda breeding and insecticide treatments to larvae.

Author information

Authors and Affiliations

  1. Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, College of Plant Protection, Hunan Agricultural University, Changsha, 410128, China

    Hualiang He, Haijuan Shu, Lin Qiu, Wenbing Ding, Qiao Gao, Jin Xue & Youzhi Li

  2. Agriculture and Rural Department of Hunan Province, Plant Protection and Inspection Station, Changsha, 410005, China

    Yi Li, Yufeng Lin & Zhengbing Zhang

  3. National Research Center of Engineering & Technology for Utilization of Botanical Functional Ingredients, Hunan Agricultural University, Changsha, 410128, China

    Youzhi Li

Authors
  1. Hualiang He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haijuan Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yufeng Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhengbing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lin Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wenbing Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qiao Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jin Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Youzhi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HH, YL, YL and conceived and designed research. YL, ZZ, LQ, and WD helped with the laboratory and field efficacy trial. HS, QG, JX helped with the data analysis. HH and YL wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Youzhi Li.

Ethics declarations

Conflict of interest

The author declares that they have no conflict of interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher’s Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1021.9 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, H., Li, Y., Shu, H. et al. The effect of chlorantraniliprole on the transcriptomic profile of Spodoptera frugiperda: a typical case analysis for the response of a newly invaded pest to an old insecticide. Mol Biol Rep 50, 2399–2410 (2023). https://doi.org/10.1007/s11033-022-08229-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-022-08229-9

Keywords

Search

Navigation