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Biochemistry, Cell and Molecular Biology

Transcriptome profile analysis reveals the emamectin benzoate-induced genes associated with olfaction and metabolic detoxification in Spodoptera exigua Hübner (Lepidoptera: noctuidae)

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Pages 340-357 | Received 06 May 2021, Accepted 08 Mar 2022, Published online: 24 Mar 2022

References

  • Abbas N, AliShad S, Ismail M. 2015. Resistance to conventional and new insecticides in house flies (Diptera: Muscidae) from poultry facilities in Punjab, Pakistan. J Econ Entomol. 108:826–833. doi:10.1093/jee/tou057.
  • Akter MS, Siddique SS, Momotaz R, Arifunnahar M, Mohiuddin SJ. 2019. Biological control of insect pests of agricultural crops through habitat management was discussed. J Agr Chem Environ. 8:1–13. doi:10.4236/jacen.2019.81001.
  • Argentine JA, Jansson RK, Halliday WR, Rugg D, Jany CS. 2002. Potency, spectrum and residual activity of four new insecticides under glass house conditions. Flo Entomol. 85:552–562. doi:10.1653/0015-4040(2002)085[0552:PSARAO]2.0.CO;2.
  • Bao YY, Li BL, Liu ZB, Xue J, Zhu ZR, Cheng JA, Zhang CX. 2010. Triazophos up-regulated gene expression in the female brown planthopper, Nilaparvata lugens. J Insect Physiol. 56:1087–1094. doi:10.1016/j.jinsphys.2010.03.004.
  • Buss DS, Callaghan A. 2008. Interaction of pesticides with p-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pestic Biochem Phy. 90(3):141153. doi:10.1016/j.pestbp.2007.12.001.
  • Che W, Huang J, Guan F, Wu Y, Yang Y. 2015. Cross-resistance and inheritance of resistance to Emamectin benzoate in Spodoptera exigua (Lepidoptera: Noctuidae). J Econ Entomol. 108:2015–2020. doi:10.1093/jee/tov168.
  • Chen S, Zhou Y, Chen Y, Gu J. 2018. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 34:884–890. doi:10.1101/274100.
  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 21:3674–3676. doi:10.1093/bioinformatics/bti610.
  • Dai HY. 2015. The adaptation mechanism of Spodoptera exigua to emamectin benzoate stress with different sublethal dose. [Master Thesis]. Nanjing Agricultural University.
  • Du LX, Liu Y, Zhang J, Gao XW, Wang B, Wang GR. 2018. Identification and characterization of chemosensory genes in the antennal T transcriptome of Spodoptera exigua. Comp Biochem Phys D. 27:54–65. doi:10.1016/j.cbd.2018.05.001.
  • ElSheikh ESA. 2015. Comparative toxicity and sublethal effects of emamectin benzoate, lufenuron and spinosad on Spodoptera littoralis Boisd. (Lepidoptera: Noctuidae). Crop Prot. 67:228–234. doi:10.1016/j.cropro.2014.10.022.
  • Epis S, Porretta D, Mastrantonio V, Urbanelli S, Sassera D, DeMarco L, Mereghetti V, Montagna M, Ricci I, Favia G. 2014. Temporal dynamics of the ABC transporter response to insecticide treatment: insights from the malaria vector Anopheles stephensi. Sci Rep-UK. 4:7435. doi:10.1038/srep07435.
  • Figueira-Mansur J, Ferreira-Pereira A, Mansur JF, Franco TA, Alvarenga ES, Sorgine MH, Neves BC, Melo AC, Leal WS, Masuda H. 2013. Silencing of P-glycoprotein increases mortality in temephos-treated Aedes aegypti larvae. Insect Mol Biol. 22:648–658. doi:10.1111/imb.12052.
  • Gott RC, Kunkel GR, Zobel ES, Lovett BR, Hawthorne DJ. 2017. Implicating ABC transporters in insecticide resistance: research strategies and a decision framework. J Econ Entom. 110(2):667–677. doi:10.1093/jee/tox041.
  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644–652. doi:10.1038/nbt.1883.
  • Hafeez M, Liu S, Yousaf HK, Jan S, Wang RL, Fernández-Grandon GM, Li X, Gulzar A, Ali B, Rehman M. 2020. RNA interference-mediated knockdown of a cytochrome P450 gene enhanced the toxicity of α-cypermethrin in xanthotoxin-fed larvae of Spodoptera exigua (Hübner). Pestic Biochem Phys. 162:6–14. doi:10.1016/j.pestbp.2019.07.003.
  • Hafeez M, Ullah F, Khan MM, Li XW, Zhang ZJ, Shah S, Imran MA, Assiri MG, Mandela FG, Desneux N, et al. 2021. Metabolic-based insecticide resistance mechanism and ecofriendly approaches for controlling of beet armyworm Spodoptera exigua: a review. Environ Sci Pollut Res. 10:1–17. doi:10.1007/s11356-021-16974-w.
  • Hartman JB, Clair DAS. 1999. Combining ability for beet armyworm, Spodoptera exigua, resistance and horticultural traits of selected Lycopersicon pennellii-derived inbred backcross lines of tomato. Plant Breed. 118:523–530. doi:10.1046/j.1439-0523.1999.00437.x.
  • He C, Liang J, Liu S, Wang S, Wu Q, Xie W, Zhang Y. 2019. Changes in the expression of four ABC transporter genes in response to imidacloprid in Bemisia tabaci Q (Hemiptera: Aleyrodidae). Pestic Biochem Phys. 153:136–143. doi:10.1016/j.pestbp.2018.11.014.
  • Huang JM, Zhao YX, Sun H, Ni H, Liu C, Wang X, Gao CF, Wu SF. 2021. Monitoring and mechanisms of insecticide resistance in Spodoptera exigua (Lepidoptera: Noctuidae), with special reference to diamides. Pestic Biochem Phys. 174:104831. doi:10.1016/j.pestbp.2021.104831.
  • IRAC. 2019. IRAC mode of action classification scheme. Version 9.3. https://www.irac-online.org/modes-of-action; p. 1–26.
  • Ishaaya I, Kontsedalov S, Horowitz AR. 2002. Emamectin, a novel insecticide for controlling field crop pests. Pest Manag Sci. 58:1091–1095. doi:10.1002/ps.535.
  • Ishtiaq M, Razaq M, Saleem MA, Anjum F, Noorul AM, Raza AM, Wright DJ. 2014. Stability, cross-resistance and fitness costs of resistance to emamectin benzoate in a re-selected field population of the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae). Crop Prot. 65:227–231. doi:10.1016/j.cropro.2014.08.007.
  • Jin R, Liu NY, Liu Y, Dong SL. 2015. A larval specific OBP able to bind the major female sex pheromone component in Spodoptera exigua (Hübner). J Integr Agr. 14:1356–1366. doi:10.1016/S2095-3119(14)60849-2.
  • Jones P, Binns D, Chang HY, Fraser MW, Anulla M. 2014. Interproscan 5: genome-scale protein function classification. Bioinformatics. 30:1236–1240. doi:10.1093/bioinformatics/btu031.
  • Ketterman AJ, Saisawang C, Wongsantichon J. 2011. Insect glutathione transferases. Drug Metab Rev. 43:253–265. doi:10.3109/03602532.2011.552911.
  • Khan HA, Akram W, Khan T, Haider MS, Iqbal N, Zubair M. 2016. Risk assessment, cross-resistance potential, and biochemical mechanism of resistance to emamectin benzoate in a field strain of house fly (Musca domestica Linnaeus). Chemosphere. 151:133–137. doi:10.1016/j.chemosphere.2016.02.077.
  • Killcoyne S, Carter G, Smith J, Boyle J. 2009. Cytoscape: A community-based framework for network modeling. Methods Mol Biol (Clifton, N.J.). 563:219–239. doi:10.1007/978-1-60761-175-2_12.
  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. Tophat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36. doi:10.1186/gb-2013-14-4-r36.
  • Lai T, Li J, Su J. 2011. Monitoring of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) resistance to chlorantraniliprole in China. Pestic Biochem Phys. 101:198–205. doi:10.1016/j.pestbp.2011.09.006.
  • Langfelder P, Horvath S. 2008. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 9:559. doi:10.1186/1471-2105-9-559.
  • Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25.
  • Leal WS. 2013. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol. 58:373–391. doi:10.1146/annurev-ento-120811-153635.
  • Liburd OE, Funderburk JE, Olson SM. 2000. Effect of biological and chemical insecticides on Spodoptera species (Lep. Noctuidae) and marketable yields of tomatoes. J Appl Entomol. 124:19–25. doi:10.1046/j.1439-0418.2000.00418.x.
  • Liu Q, Liu W, Zeng B, Wang G, Hao D, Huang Y. 2017. Deletion of the Bombyx mori odorant receptor co-receptor (BmOrco) impairs olfactory sensitivity in silkworms. Insect Biochem Molec. 86:58–67. doi:10.1016/j.ibmb.2017.05.007.
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 25:402–408. doi:10.1006/meth.2001.1262.0.
  • López JD, Latheef MA, Hoffmann WC. 2010. Effect of emamectin benzoate on mortality, proboscis extension, gustation and reproduction of the corn earworm, Helicoverpa zea. J Insect Sci. 10:1–16. doi:10.1673/031.010.8901.
  • Mastrantonio V, Ferrari M, Epis S, Negri A, Scuccimarra G, Montagna M, Favia G, Porretta D, Urbanelli S, Bandi C. 2017. Gene expression modulation of ABC transporter genes in response to permethrin in adults of the mosquito malaria vector Anopheles stephensi. Acta Trop. 171:37–43. doi:10.1016/j.actatropica.2017.03.012.
  • Mokbel ES, Huesien A. 2020. Sublethal effects of emamectin benzoate on life table parameters of the cotton leafworm, Spodoptera littoralis (Boisd.). Bull Nat Res Cen. 44(1):1–8. doi:10.1186/s42269-020-00412-x.
  • Moulton JK, Pepper DA, Jansson RK, Dennehy TJ. 2002. Pro-active management of beet armyworm (Lepidoptera: Noctuidae) resistance to tebufenozide and methoxyfenozide: baseline monitoring, risk assessment, and isolation of resistance. J Econ Entomol. 95:414–424. doi:10.1603/0022-0493-95.2.414.
  • Moustafa MAM, Kákai Á, Awad M, Fónagy A. 2016. Sublethal effects of spinosad and emamectin benzoate on larval development and reproductive activities of the cabbage moth, Mamestra brassicae L. (Lepidoptera: Noctuidae). Crop Prot. 90:197–204. doi:10.1016/j.cropro.2016.09.004.
  • Muhammad M K, Muhammad N, Hua H X, Cai W L, Zhao J. 2018. Lethal and sublethal effects of emamectin benzoate on the rove beetle, Paederus fuscipes, a non-target predator of rice brown planthopper. Nilaparvata lugens. Ecotoxicology and Environmental Safety. 165:19–24. doi:10.1016/j.ecoenv.2018.08.047.
  • Mushtaq M, Syintsakos LR, Krieter PA, Colletti A, Wislocki PG. 1996. Absorption, tissue distribution, excretion, and metabolism of 3H- and 14C-labeled emamectin benzoate in rats. J Agr Food Chem. 44:3342–3349. doi:10.1021/jf960034j.
  • Pelosi P, Iovinella I, Zhu J, Wang G, Dani FR. 2018. Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biol Rev. 93:184–200. doi:10.1111/brv.12339.
  • Pignatelli P, Ingham VA, Balabanidou V, Vontas J, Lycett G, Ranson H. 2018. The Anopheles gambiae ATP-binding cassette transporter family: phylogenetic analysis and tissue localization provide clues on function and role in insecticide resistance. Insect Mol Biol. 27:110–122. doi:10.1111/imb.12351.
  • Ren XL, Wang YY, Ma YJ, Jiang WL, Ma XY, Hu HY, Wang D, Ma Y. 2020. Midgut de novo transcriptome analysis and gene expression profiling of Spodoptera exigua larvae exposed with sublethal concentrations of Cry1Ca protein. 3 Biotech. 10(3):138. doi:10.1007/s13205-020-2129-2.
  • Roberts A, Pimentel H, Trapnell C, Pachter L. 2011. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics. 27:2325–2329. doi:10.1093/bioinformatics/btr355.
  • Sato K, Touhara K. 2009. Insect olfaction: receptors, signal transduction, and behavior. Results Prob Cell Differ. 47:121–138. doi:10.1007/400_2008_10.
  • Scanlan JL, Gledhill-Smith RS, Battlay P, Robin C. 2020. Genomic and transcriptomic analyses in Drosophila suggest that the ecdysteroid kinase-like (EcKL) gene family encodes the ‘detoxification-by-phosphorylation’ enzymes of insects. Insect Biochem Molec. 123:103429. doi:10.1016/j.ibmb.2020.103429.
  • Shad SA, Sayyed AH, Saleem MA. 2010. Cross-resistance, mode of inheritance and stability of resistance to emamectin in Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag Sci. 66:839–846. doi:10.1002/ps.1950.
  • Su HH, Yang Y, Zou JC, Cheng YQ, Yang Y, Wu JJ, Pollak P, Yang YZ. 2020. Transcriptome analysis of the ovary of beet armyworm Spodoptera exigua under different exposures of cadmium stress. Chemophere. 251:126372. doi:10.1016/j.chemosphere.2020.126372.
  • Sun H, Liu F, Ye Z, Baker A, Zwiebel LJ. 2020. Mutagenesis of the orco odorant receptor co-receptor impairs olfactory function in the malaria vector Anopheles coluzzii. Insect Biochem Molec. 127:103497. doi:10.1016/j.ibmb.2020.103497.
  • Sun Y, Sheng Y, Bai L, Zhang Y, Xiao Y, Xiao L, Tan Y, Shen Y. 2014. Characterizing heat shock protein 90 gene of Apolygus lucorum (Meyer-Dür) and its expression in response to different temperature and pesticide stresses. Cell Stress Chaperon. 19:725–739. doi:10.1007/s12192-014-0500-0.
  • Sun Y, Zhao J, Sheng Y, Xiao YF, Zhang YJ, Bai LX, Tan Y, Xiao LB, Xu GC. 2016. Identification of heat shock cognate protein 70 gene (Alhsc70) of Apolygus lucorum and its expression in response to different temperature and pesticide stresses. Insect Sci. 23:37–49. doi:10.1111/1744-7917.12193.
  • Tang XK, Zhou XM, Wu J, Li JB, Bai LY. 2014. A novel function of sanshools: the alleviation of injury from metolachlor in rice seedlings. Pestic Biochem Phys. 110:44–49. doi:10.1016/j.pestbp.2014.02.006.
  • Tian X, Liu J, Guo Z, Hu B, Kibe MD, Wang S, Wei Q, Su J. 2018. The characteristics of voltage-gated sodium channel and the association with lambda cyhalothrin resistance in Spodoptera exigua. J Asia-Pac Entomol. 21:1020–1027. doi:10.1016/j.aspen.2018.07.013.
  • Trapnell C, Pachter L, Salzberg SL. 2009. Tophat: discovering splice junctions with RNA-Seq. Bioinformatics. 25:1105–1111. doi:10.1093/bioinformatics/btp120.
  • Wang W, Wang J, Wei Q, Wei Q, Li B, Zhong X, Hu T, Hu H, Bao C. 2019a. Transcriptome-wide identification and characterization of circular RNAs in leaves of Chinese cabbage (Brassica rapa L. ssp. pekinensis) in response to calcium deficiency-induced tip-burn. Sci rep. 9(1):1–9. doi:10.1038/s41598-019-51190-0.
  • Wang X, Huang Q, Hao Q, Ran S, Wu Y, Cui P, Yang J, Jiang C, Yang Q. 2018. Insecticide resistance and enhanced cytochrome P450 monooxygenase activity in field populations of Spodoptera litura from Sichuan, China. Crop Prot. 106:110–116. doi:10.1016/j.cropro.2017.12.020.
  • Wang X, Lou L, Su J. 2019b. Prevalence and stability of insecticide resistances in field population of Spodoptera litura (Lepidoptera: Noctuidae) from Huizhou, Guangdong province, China. J Asia-Pac Entomol. 22:728–732. doi:10.1016/j.aspen.2019.05.009.
  • Wu H, Liu Y, Shi X, Zhang X, Ye C, Zhu KY, Zhu F, Zhang J, Ma E. 2020. Transcriptome analysis of antennal cytochrome P450s and their transcriptional responses to plant and locust volatiles in Locusta migratoria. Int J Biol Macromol. 149:741–753. doi:10.1016/j.ijbiomac.2020.01.309.
  • Xiong W, Gao S, Lu Y, Wei L, Mao J, Xie J, Cao Q, Liu J, Bi J, Song X. 2019. Latrophilin participates in insecticide susceptibility through positively regulating CSP10 and partially compensated by OBPC01 in Tribolium castaneum. Pestic Biochem Phys. 159:107–117. doi:10.1016/j.pestbp.2019.06.005.
  • Yang H, Dong J, Sun Y, Hu Z, Lv Q, Li D. 2020. Antennal transcriptome analysis and expression profiles of putative chemosensory soluble proteins in Histia rhodope Cramer (Lepidoptera: Zygaenidae). CBPD. 33:100654. doi:10.1016/j.cbd.2020.100654.
  • Yang X, Xie W, Wang SL, Wu QJ, Pan HP, Li RM, Yang NN, Liu BM, Xu BY, Zhou X. 2013. Two cytochrome P450 genes are involved in imidacloprid resistance in field populations of the whitefly, Bemisia tabaci, in China. Pestic Bioche Phys. 107:343–350. doi:10.1016/j.pestbp.2013.10.002.
  • Yu H, He L, Li ZQ, Li N, Yang YYO, Huang GH. 2019. Altering of host larval (Spodoptera exigua) calcineurin activity in response to ascovirus infection. Pest Manag Sci. 76:1048–1059. doi:10.1002/ps.5615.
  • Yu H, Li ZQ, He L, Yang YYO, Li N, Huang GH. 2018. Response analysis of host Spodoptera exigua larvae to infection by Heliothis virescens ascovirus 3h (HvAV-3h) via transcriptome. Sci. Rep. 8:5367. doi:10.1038/s41598-018-23715-6.
  • Zaka SM, Abbas N, Shad SA, Shah RM. 2014. Effect of emamectin benzoate on life history traits and relative fitness of Spodoptera litura (Lepidoptera: Noctuidae). Phytoparasitica. 42:493–501. doi:10.1007/s12600-014-0386-5.
  • 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). Agr Sci China. 10:1232–1240. doi:10.1016/S1671-2927(11)60114-4.
  • Zhang XQ, Yan Q, Li LL, Xu JW, Mang D, Wang XL, Hoh HH, Ye J, Ju Q, Ma Y. 2020a. Different binding properties of two general-odorant binding proteins in Athetis lepigone with sex pheromones, host plant volatiles and insecticides. Pestic Biochem Phys. 164:173–182. doi:10.1016/j.pestbp.2020.01.012.
  • Zhang Y, Dong X, Liu J, Hu M, Zhong G, Geng P, Yi X. 2012. Molecular cloning, expression and molecular Modeling of chemosensory protein from Spodoptera litura and its binding properties with Rhodojaponin III. PloS one. 7:e47611. doi:10.1371/journal.pone.0047611.
  • Zhang YN, Xu JW, Zhang XC, Zhang XQ, Li LL, Yuan VX, Mang DZ, Zhu XY, Zhang F, Dewer Y. 2020b. Organophosphorus insecticide interacts with the pheromone-binding proteins of Athetis lepigone: implication for olfactory dysfunction. J Hazard Mater. 397:122777. doi:10.1016/j.jhazmat.2020.122777.
  • Zhao J, Sun Y, Xiao LB, Tan YA, Jiang YP, Bai LX. 2018. Vitellogenin and vitellogenin receptor gene expression profiles in Spodoptera exigua are related to host plant suitability. Pest Manag Sci. 74:950–958. doi:10.1002/ps.4794.
  • Zheng XL, Cong XP, Wang XP, Lei CL. 2011. A review of geographic distribution, overwintering and migration in Spodoptera exigua Hubner (Lepidoptera: Noctuidae). J Entomol Res Soc. 13:39–48.
  • Zhou C, Liu Y, Yu W, Deng Z, Gao M, Liu F, Mu W. 2011. Resistance of Spodoptera exigua to ten insecticides in Shandong, China. Phytoparasitica. 39:315. doi:10.1007/s12600-011-0157-5.
  • Zhu J, Ban LP, Song LM, Liu Y, Pelosi P, Wang GR. 2016. General odorant-binding 765 proteins and sex pheromone guide larvae of Plutella xylostella to better food. Insect Biochem Mol Biol. 72:10–19. doi:10.1016/j.ibmb.2016.03.005.
  • Zuo YY, Huang JL, Wang J, Feng Y, Han TT, Wu YD, Yang YH. 2018. Knockout of a P-glycoprotein gene increases susceptibility to abamectin and emamectin benzoate in Spodoptera exigua. Insect Mol Biol. 27:36–45. doi:10.1111/imb.12338.