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Investigating mechanisms associated with emamectin benzoate resistance in the tomato borer Tuta absoluta

Abstract

The tomato borer Tuta absoluta is a major pest of tomato mainly controlled by chemical insecticides. However, development of resistance to specific chemical classes has made control of the pest extremely difficult. Emamectin benzoate belongs to the avermectin mode of action and to date, low or no resistance levels against this insecticide have been documented. Recently, reduced efficacy of emamectin benzoate was documented, in a field population from Crete (ninefold resistant ratio (RR)). Subsequent laboratory selections with emamectin benzoate for eight sequential generations resulted in an increase of the RR to 60-fold, the highest resistance level reported to the particular insecticide. Hereby, we are presenting the characterization of emamectin benzoate resistance in T. absoluta. Sequencing of the GluCl and GABA receptor (rdl) genes, the molecular targets of emamectin benzoate indicted absence of non-synonymous SNPs. The use of known enzyme inhibitors (PBO, DEF and DEM) revealed that P450s partially synergized emamectin benzoate resistance, suggesting potential implication of metabolic resistance. RNAseq approach was used to identify differentially expressed genes, from emamectin benzoate resistant and susceptible T. absoluta populations. Twelve libraries were sequenced using the Illumina platform, which generated 81 Gbp, thus substantially increasing the number of publicly available genomic resources for this species. The de novo transcriptome assembly consisted of 549,601 contigs, grouped in 233,453 unigenes. Differential expression analysis and qPCR validation revealed over-expression of one unigene similar to cytochrome P450 (Clan 4) potentially implicated in emamectin benzoate resistance, supporting further the involvement of P450s in the observed resistance phenotype.

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Data availability

The datasets used or analysed during the current study are available from the corresponding author upon justified request. The sequencing reads are available from the Sequence Read Archive (SRA) under the bioproject accession PRJNA749726. https://dataview.ncbi.nlm.nih.gov/object/PRJNA749726?reviewer=qnecd1etje9f0bbpfddb4s9vue

References

  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267. https://doi.org/10.1093/jee/18.2.265a

    CAS  Article  Google Scholar 

  2. Afzal MBS, Shad SA (2016) Characterization of Phenacoccus solenopsis (Tinsley)(Homoptera: Pseudococcidae) resistance to emamectin benzoate: cross-resistance patterns and fitness cost analysis. Neotrop Entomol 45:310–319. https://doi.org/10.1007/s13744-016-0370-5

    CAS  Article  PubMed  Google Scholar 

  3. Ahmad M, Mehmood R (2015) Monitoring of resistance to new chemistry insecticides in Spodoptera litura (Lepidoptera: Noctuidae) in Pakistan. J Econ Entomol 108:1279–1288. https://doi.org/10.1093/jee/tov085

    CAS  Article  PubMed  Google Scholar 

  4. Aigbedion-Atalor PO, Hill MP, Zalucki MP, Obala F, Idriss GE, Midingoyi S-K, Chidege M, Ekesi S, Mohamed SA (2019) The South America tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), spreads its wings in Eastern Africa: distribution and socioeconomic impacts. J Econ Entomol 112:2797–2807. https://doi.org/10.1093/jee/toz220

    Article  PubMed  Google Scholar 

  5. Arena JP, Liu KK, Paress PS, Frazier EG, Cully DF, Mrozik H, Schaeffer JM (1995) The mechanism of action of avermectins in Caenorhabditis elegans: correlation between activation of glutamate-sensitive chloride current, membrane binding, and biological activity. J parasitol: 286–294 https://doi.org/10.2307/3283936

  6. Baek JH, Clark JM, Lee SH (2010) Cross-strain comparison of cypermethrin-induced cytochrome P450 transcription under different induction conditions in diamondback moth. Pestic Biochem Physiol 96:43–50. https://doi.org/10.1016/j.pestbp.2009.08.014

    CAS  Article  Google Scholar 

  7. Biondi A, Guedes RNC, Wan F-H, Desneux N (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63:239–258. https://doi.org/10.1146/annurev-ento-031616-034933

    CAS  Article  PubMed  Google Scholar 

  8. Bray NL, Pimentel H, Melsted P, Pachter L (2016) Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol 34:525–527. https://doi.org/10.1038/nbt.3519

    CAS  Article  Google Scholar 

  9. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:1–9. https://doi.org/10.1186/1471-2105-10-421

    Article  Google Scholar 

  10. Campos MR, Silva TBM, Silva WM, Silva JE, Siqueira HAA (2014) Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci 88:405–412. https://doi.org/10.1007/s10340-014-0618-y

    Article  Google Scholar 

  11. Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N (2017) From the Western palaearctic region to beyond: Tuta absoluta 10 years after invading Europe. J Pest Sci 90:787–796. https://doi.org/10.1007/s10340-017-0867-7

    Article  Google Scholar 

  12. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973. https://doi.org/10.1093/bioinformatics/btp348

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 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. https://doi.org/10.1093/jee/tov168

    CAS  Article  PubMed  Google Scholar 

  14. Clark JM, Scott JG, Campos F, Bloomquist JR (1995) Resistance to avermectins: extent, mechanisms, and management implications. Annu Rev Entomol 40:1–30. https://doi.org/10.1146/annurev.en.40.010195.000245

    CAS  Article  PubMed  Google Scholar 

  15. Dermauw W, Ilias A, Riga M, Tsagkarakou A, Grbić M, Tirry L, Van Leeuwen T, Vontas J (2012) The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: implications for acaricide toxicology and a novel mutation associated with abamectin resistance. Insect Biochem Mol Biol 42:455–465. https://doi.org/10.1016/j.ibmb.2012.03.002

    CAS  Article  PubMed  Google Scholar 

  16. Dermauw W, Van Leeuwen T, Feyereisen R (2020) Diversity and evolution of the P450 family in arthropods. Insect biochem mol biol. 127:103490. https://doi.org/10.1016/j.ibmb.2020.103490

    CAS  Article  Google Scholar 

  17. Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Ruescas DC, Tabone E, Frandon J (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215. https://doi.org/10.1007/s10340-010-0321-6

    Article  Google Scholar 

  18. Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408. https://doi.org/10.1007/s10340-011-0398-6

    Article  Google Scholar 

  19. Elzaki MEA, Zhang W, Han Z (2015) Cytochrome P450 CYP4DE1 and CYP6CW3v2 contribute to ethiprole resistance in Laodelphax striatellus (Fallén). Insect Mol Biol 24:368–376. https://doi.org/10.1111/imb.12164

    CAS  Article  PubMed  Google Scholar 

  20. Feyereisen R (2015) Insect P450 inhibitors and insecticides: challenges and opportunities. Pest Manag Sci 71:793–800. https://doi.org/10.1002/ps.3895

    CAS  Article  PubMed  Google Scholar 

  21. 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. https://doi.org/10.1016/j.pestbp.2015.01.004

    CAS  Article  PubMed  Google Scholar 

  22. Finney DJ (1964) A statistical treatment of the sigmoid response curve. Probit analysis 25

  23. Fisher MH, Mrozik H (1992) The chemistry and pharmacology of avermectins. Ann Rev Pharmacol Toxicol (USA) 32:537–553. https://doi.org/10.1146/annurev.pa.32.040192.002541

    CAS  Article  Google Scholar 

  24. 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. https://doi.org/10.1038/nbt.1883

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Grant C, Jacobson R, Ilias A, Berger M, Vasakis E, Bielza P, Zimmer CT, Williamson MS, ffrench-Constant RH, Vontas J, Roditakis E, Bass C (2019) The evolution of multiple-insecticide resistance in UK populations of tomato leafminer, Tuta absoluta. Pest Manag Sci 75:2079–2085. https://doi.org/10.1002/ps.5381

    CAS  PubMed  Google Scholar 

  26. Guedes RNC, Roditakis E, Campos MR, Haddi K, Bielza P, Siqueira HAA, Tsagkarakou A, Vontas J, Nauen R (2019) Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. J Pest Sci. 1–14, https://doi.org/10.1007/s10340-019-01086-9

  27. Guedes RNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bulletin 42:211–216. https://doi.org/10.1111/epp.2557

    Article  Google Scholar 

  28. Haddi K, Berger M, Bielza P, Rapisarda C, Williamson MS, Moores G, Bass C (2017) Mutation in the ace-1 gene of the tomato leaf miner (Tuta absoluta) associated with organophosphates resistance. J Appl Entomol 141:612–619. https://doi.org/10.1111/jen.12386

    CAS  Article  Google Scholar 

  29. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, pp. 95–98. [London]: Information Retrieval Ltd., c1979-c2000

  30. He Z, Zhang H, Gao S, Lercher MJ, Chen W-H, Hu S (2016) Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees. Nucleic Acids Res 44:W236–W241. https://doi.org/10.1093/nar/gkw370

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Huang S, Qin W, Chen Q (2010) Cloning and mRNA expression levels of cytochrome P450 genes CYP4M14 and CYP4S9 in the common cutworm Spodoptera litura (Fabricius). Scientia Agricultura Sinica 43:3115–3124

    CAS  Google Scholar 

  32. IRAC (2021) IRAC MoA Classiication Scheme (Version 10.1). http://www.irac-online.org: (Accessed, May, 2021)

  33. Ishtiaq M, Razaq M, Saleem MA, Anjum F, ul Ane MN, 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. https://doi.org/10.1016/j.cropro.2014.08.007

    CAS  Article  Google Scholar 

  34. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. https://doi.org/10.1093/bioinformatics/btu031

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Kandil MA, Fouad EA, El Hefny DE, Abdel-Mobdy YE (2020) Toxicity of fipronil and emamectin benzoate and their mixtures against cotton leafworm, Spodoptera littoralis (Lepidoptera: Noctuidae) with relation to GABA content. J Econ Entomol 113:385–389. https://doi.org/10.1093/jee/toz232

    CAS  PubMed  Google Scholar 

  36. Kaplanoglu E, Chapman P, Scott IM, Donly C (2017) Overexpression of a cytochrome P450 and a UDP-glycosyltransferase is associated with imidacloprid resistance in the Colorado potato beetle, Leptinotarsa decemlineata. Sci Rep 7:1–10. https://doi.org/10.1038/s41598-017-01961-4

    CAS  Article  Google Scholar 

  37. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Killiny N, Hajeri S, Tiwari S, Gowda S, Stelinski LL (2014) Double-stranded RNA uptake through topical application, mediates silencing of five CYP4 genes and suppresses insecticide resistance in Diaphorina citri. PloS one 9:e110536. https://doi.org/10.1371/journal.pone.0110536

    Article  Google Scholar 

  39. Kim D, Langmead B, Salzberg SL (2015) HISAT: A fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, Miller CA, Mardis ER, Ding L, Wilson RK (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22:568–576. https://doi.org/10.1101/gr.129684.111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Kwon DH, Yoon KS, Clark JM, Lee SH (2010) A point mutation in a glutamate-gated chloride channel confers abamectin resistance in the two-spotted spider mite, Tetranychus urticae Koch. Insect Mol Biol 19:583–591. https://doi.org/10.1111/j.1365-2583.2010.01017.x

    CAS  Article  Google Scholar 

  42. Lasota JA, Dybas RA (1991) Avermectins, a novel class of compounds: implications for use in arthropod pest control. Annu Rev Entomol 36:91–117. https://doi.org/10.1146/annurev.en.36.010191.000515

    CAS  Article  PubMed  Google Scholar 

  43. Lasota JA, Shelton AM, Bolognese JA, Dybas RA (1996) Toxicity of avermectins to diamondback moth (Lepidoptera: Plutellidae) populations: implications for susceptibility monitoring. J Econ Entomol 89:33–38. https://doi.org/10.1093/jee/89.1.33

    CAS  Article  Google Scholar 

  44. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-9. https://doi.org/10.1093/bioinformatics/btp352

  45. Lietti MMM, Botto E, Alzogaray RA (2005) Insecticide resistance in argentine populations of Tuta absoluta (Meyrick)(Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119. https://doi.org/10.1590/S1519-566X2005000100016

    Article  Google Scholar 

  46. Liu F, Shi X, Liang Y, Wu Q, Xu B, Xie W, Wang S, Zhang Y, Liu N (2014) A 36-bp deletion in the alpha subunit of glutamate-gated chloride channel contributes to abamectin resistance in Plutella xylostella. Entomol Exp Appl 153:85–92. https://doi.org/10.1111/eea.12232

    CAS  Article  Google Scholar 

  47. Ludmerer SW, Warren VA, Williams BS, Zheng Y, Hunt DC, Ayer MB, Wallace MA, Chaudhary AG, Egan MA, Meinke PT (2002) Ivermectin and nodulisporic acid receptors in Drosophila melanogaster contain both γ-aminobutyric acid-gated Rdl and glutamate-gated GluClα chloride channel subunits. Biochemistry 41:6548–6560. https://doi.org/10.1021/bi015920o

    CAS  Article  Google Scholar 

  48. McCarthy DJ, Chen Y, Smyth GK (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40:4288–4297. https://doi.org/10.1093/nar/gks042

    CAS  Article  Google Scholar 

  49. Muraro DS, de Oliveira Abbade Neto D, Kanno RH, Kaiser IS, Bernardi O, Omoto C (2021) Inheritance patterns, cross‐resistance and synergism in Spodoptera frugiperda (Lepidoptera: Noctuidae) resistant to emamectin benzoate. Pest Management Science. https://doi.org/10.1002/ps.6545

  50. Nelson DR (1999) Cytochrome P450 and the individuality of species. Arch Biochem Biophys 369:1–10. https://doi.org/10.1006/abbi.1999.1352

    CAS  Article  Google Scholar 

  51. Pearce SL, Clarke DF, East PD, Elfekih S, Gordon KHJ, Jermiin LS, McGaughran A, Oakeshott JG, Papanikolaou A, Perera OP (2017) Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol 15:1–30. https://doi.org/10.1186/s12915-017-0402-6

    Article  Google Scholar 

  52. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45. https://doi.org/10.1093/nar/29.9.e45

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36–e36. https://doi.org/10.1093/nar/30.9.e36

    Article  PubMed  PubMed Central  Google Scholar 

  54. Prichard R, Ménez C, Lespine A (2012) Moxidectin and the avermectins: consanguinity but not identity. Int J Parasitol Drugs Drug Resist 2:134–153. https://doi.org/10.1016/j.ijpddr.2012.04.001

    Article  Google Scholar 

  55. Pu X, Yang Y, Wu S, Wu Y (2010) Characterisation of abamectin resistance in a field-evolved multiresistant population of Plutella xylostella. Pest Manag Sci: Formerly Pesticide Sci 66:371–378. https://doi.org/10.1002/ps.1885

    CAS  Article  Google Scholar 

  56. Reimand J, Arak T, Adler P, Kolberg L, Reisberg S, Peterson H, Vilo J (2016) g: Profiler—a web server for functional interpretation of gene lists (2016 update). Nucleic Acids Res 44:W83–W89. https://doi.org/10.1093/nar/gkw199

    CAS  Article  Google Scholar 

  57. Riga M, Tsakireli D, Ilias A, Morou E, Myridakis A, Stephanou EG, Nauen R, Dermauw W, Van Leeuwen T, Paine M (2014) Abamectin is metabolized by CYP392A16, a cytochrome P450 associated with high levels of acaricide resistance in Tetranychus urticae. Insect Biochem Mol Biol 46:43–53. https://doi.org/10.1016/j.ibmb.2014.01.006

    CAS  Article  Google Scholar 

  58. Riley D, Smith H, Bennett J, Torrance P, Huffman E, Sparks A Jr, Gruver C, Dunn T, Champagne D (2020) Regional survey of diamondback moth (Lepidoptera: Plutellidae) response to maximum dosages of insecticides in Georgia and Florida. J Econ Entomol 113:2458–2464. https://doi.org/10.1093/jee/toaa125

    CAS  Article  Google Scholar 

  59. Robertson JL, Jones MM, Olguin E, Alberts B (2017) Bioassays with arthropods. CRC Press. https://doi.org/10.1201/9781315373775

    Book  Google Scholar 

  60. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26. https://doi.org/10.1038/nbt.1754

    CAS  Article  Google Scholar 

  61. Roditakis E, Skarmoutsou C, Staurakaki M (2013) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840. https://doi.org/10.1002/ps.3442

    CAS  Article  PubMed  Google Scholar 

  62. Roditakis E, Vasakis E, Grispou M, Stavrakaki M, Nauen R, Gravouil M, Bassi A (2015) First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88:9–16. https://doi.org/10.1007/s10340-015-0643-5

    Article  Google Scholar 

  63. Roditakis E, Mavridis K, Riga M, Vasakis E, Morou E, Rison JL, Vontas J (2017) Identification and detection of indoxacarb resistance mutations in the para sodium channel of the tomato leafminer, Tuta absoluta. Pest Manag Sci 73:1679–1688. https://doi.org/10.1002/ps.4513

    CAS  Article  PubMed  Google Scholar 

  64. Roditakis E, Vasakis E, Garcia-Vidal L, del Rosario M-A, Rison JL, Haxaire-Lutun MO, Nauen R, Tsagkarakou A, Bielza P (2018) A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region. J Pest Sci 91:421–435. https://doi.org/10.1007/s10340-017-0900-x

    Article  Google Scholar 

  65. Rugg D, Buckingham SD, Sattelle DB, Jansson RK (2005) The insecticidal macrocyclic lactones. https://doi.org/10.1016/B0-44-451924-6/00065-X

  66. Sakuma M (1998) Probit analysis of preference data. Appl Entomol Zool 33:339–347. https://doi.org/10.1303/aez.33.339

    Article  Google Scholar 

  67. Santana PA, Kumar L, Da Silva RS, Picanço MC (2019) Global geographic distribution of Tuta absoluta as affected by climate change. J Pest Sci 92:1373–1385. https://doi.org/10.1007/s10340-018-1057-y

    Article  Google Scholar 

  68. Silva GA, Picanço MC, Bacci L, Crespo ALB, Rosado JF, Guedes RNC (2011) Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci 67:913–920. https://doi.org/10.1002/ps.2131

    CAS  Article  PubMed  Google Scholar 

  69. Silva WM, Berger M, Bass C, Balbino VQ, Amaral MHP, Campos MR, Siqueira HAA (2015) Status of pyrethroid resistance and mechanisms in Brazilian populations of Tuta absoluta. Pestic Biochem Physiol 122:8–14. https://doi.org/10.1016/j.pestbp.2015.01.011

    CAS  Article  PubMed  Google Scholar 

  70. Silva JE, Assis CPO, Ribeiro LMS, Siqueira HAA (2016a) Field-evolved resistance and cross-resistance of Brazilian Tuta absoluta (Lepidoptera: Gelechiidae) populations to diamide insecticides. J Econ Entomol 109:2190–2195. https://doi.org/10.1093/jee/tow161

    CAS  Article  PubMed  Google Scholar 

  71. Silva WM, Berger M, Bass C, Williamson M, Moura DMN, Ribeiro LMS, Siqueira HAA (2016b) Mutation (G275E) of the nicotinic acetylcholine receptor α6 subunit is associated with high levels of resistance to spinosyns in Tuta absoluta (Meyrick)(Lepidoptera: Gelechiidae). Pestic Biochem Physiol 131:1–8. https://doi.org/10.1016/j.pestbp.2016.02.006

    CAS  Article  PubMed  Google Scholar 

  72. Siqueira HAA, Guedes RNC, Picanco MC (2000a) Cartap resistance and synergism in populations of Tuta absoluta (Lep., Gelechiidae). J Appl Entomol 124:233–238. https://doi.org/10.1046/j.1439-0418.2000.00470.x

    CAS  Article  Google Scholar 

  73. Siqueira HÁA, Guedes RNC, Picanço MC (2000b) Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agric for Entomol 2:147–153. https://doi.org/10.1046/j.1461-9563.2000.00062.x

    Article  Google Scholar 

  74. Siqueira HAA, Guedes RNC, Fragoso DdB, Magalhaes LC (2001) Abamectin resistance and synergism in Brazilian populations of Tuta absoluta (Meyrick)(Lepidoptera: Gelechiidae). Int J Pest Manag 47:247–251. https://doi.org/10.1080/09670870110044634

    Article  Google Scholar 

  75. Snoeck S, Greenhalgh R, Tirry L, Clark RM, Van Leeuwen T, Dermauw W (2017) The effect of insecticide synergist treatment on genome-wide gene expression in a polyphagous pest. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-13397-x

    Article  Google Scholar 

  76. 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

    CAS  Article  PubMed  Google Scholar 

  77. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  78. Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11:1–9. https://doi.org/10.1186/1471-2105-11-7

    Article  Google Scholar 

  79. Suzek BE, Wang Y, Huang H, McGarvey PB, Wu CH, UniProt C (2015) UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics 31:926–932. https://doi.org/10.1093/bioinformatics/btu739

    CAS  Article  PubMed  Google Scholar 

  80. Turner MJ, Schaeffer JM (1989) Mode of action of ivermectin. In Ivermectin and abamectin, pp. 73–88. Springer. https://doi.org/10.1007/978-1-4612-3626-9_5

  81. Urbaneja A, Vercher R, Navarro V, Porcuna JL, Garcia- Marí F (2007) La polilla del tomate, Tuta absoluta. Phytoma España 194:16–24

    Google Scholar 

  82. Wang R, Wu Y (2014) Dominant fitness costs of abamectin resistance in Plutella xylostella. Pest Manag Sci 70:1872–1876. https://doi.org/10.1002/ps.3741

    CAS  Article  PubMed  Google Scholar 

  83. Wang X, Wang R, Yang Y, Wu S, O’Reilly AO, Wu Y (2016a) A point mutation in the glutamate-gated chloride channel of Plutella xylostella is associated with resistance to abamectin. Insect Mol Biol 25:116–125. https://doi.org/10.1111/imb.12204

    CAS  Article  PubMed  Google Scholar 

  84. Wang XG, Gao XW, Liang P, Shi XY, Song DL (2016b) Induction of cytochrome P450 activity by the interaction of chlorantraniliprole and sinigrin in the Spodoptera exigua (Lepidoptera: Noctuidae). Environ Entomol 45:500–507. https://doi.org/10.1093/ee/nvw007

    CAS  Article  PubMed  Google Scholar 

  85. Wang X-G, Ruan Y-W, Gong C-W, Xiang X, Xu X, Zhang Y-M, Shen L-T (2019) Transcriptome analysis of Sogatella furcifera (Homoptera: Delphacidae) in response to Sulfoxaflor and functional verification of resistance-related P450 Genes. Int J Mol Sci 20:4573. https://doi.org/10.3390/ijms20184573

    CAS  Article  PubMed Central  Google Scholar 

  86. Waterhouse RM, Seppey M, Simão FA, Manni M, Ioannidis P, Klioutchnikov G, Kriventseva EV, Zdobnov EM (2018) BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol 35:543–548. https://doi.org/10.1093/molbev/msx319

    CAS  Article  PubMed  Google Scholar 

  87. Wolstenholme AJ, Rogers AT (2005) Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131:S85. https://doi.org/10.1017/S0031182005008218

    CAS  Article  PubMed  Google Scholar 

  88. Wu L, Zhang ZF, Yu Z, Yu R, Ma E, Fan YL, Liu TX, Feyereisen R, Zhu KY, Zhang J (2020) Both LmCYP4G genes function in decreasing cuticular penetration of insecticides in Locusta migratoria. Pest Manag Sci 76:3541–3550. https://doi.org/10.1002/ps.5914

    CAS  Article  PubMed  Google Scholar 

  89. Xiao Q, Deng L, Elzaki MEA, Zhu L, Xu Y, Han X, Wang C, Han Z, Wu M (2020) The Inducible CYP4C71 Can Metabolize Imidacloprid in Laodelphax striatellus (Hemiptera: Delphacidae). J Econ Entomol 113:399–406. https://doi.org/10.1093/jee/toz292

    CAS  Article  PubMed  Google Scholar 

  90. Xu L, Luo G, Sun Y, Huang S, Xu D, Xu G, Han Z, Gu Z, Zhang Y (2020) Multiple down-regulated cytochrome P450 monooxygenase genes contributed to synergistic interaction between chlorpyrifos and imidacloprid against Nilaparvata lugens. J Asia-Pacific Entomol 23:44–50. https://doi.org/10.1016/j.aspen.2019.10.017

    Article  Google Scholar 

  91. Xue W, Snoeck S, Njiru C, Inak E, Dermauw W, Van Leeuwen T (2020) Geographical distribution and molecular insights into abamectin and milbemectin cross-resistance in European field populations of Tetranychus urticae. Pest Manag Sci 76:2569–2581. https://doi.org/10.1002/ps.5831

    CAS  Article  PubMed  Google Scholar 

  92. Yalcin M, Mermer S, Kozaci LD, Turgut C (2015) Insecticide resistance in two populations of Tuta absoluta (Meyrick, 1917)(Lepidoptera: Gelechiidae) from Turkey. Türkiye Entomoloji Dergisi 39:137–145. https://doi.org/10.16970/ted.63047

    Google Scholar 

  93. 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. https://doi.org/10.1007/s12600-014-0386-5

    CAS  Article  Google Scholar 

  94. Zhang Y, Yang Y, Sun H, Liu Z (2016) Metabolic imidacloprid resistance in the brown planthopper, Nilaparvata lugens, relies on multiple P450 enzymes. Insect Biochem Mol Biol 79:50–56. https://doi.org/10.1016/j.ibmb.2016.10.009

    CAS  Article  PubMed  Google Scholar 

  95. Zhao JZ, Collins HL, Li YX, Mau RFL, Thompson GD, Hertlein M, Andaloro JT, Boykin R, Shelton AM (2006) Monitoring of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad, indoxacarb, and emamectin benzoate. J Econ Entomol 99:176–181. https://doi.org/10.1093/jee/99.1.176

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This research is co-financed by Greece and the European Union (European Social Fund—ESF) through the Operational Programme “Human Resources Development, Education and Lifelong Learning” in the context of the project “Strengthening Human Resources Research Potential via Doctorate Research” (MIS-5000432), implemented by the State Scholarships Foundation (ΙΚΥ) (M.S.). This research has been co-financed by Greek national funds through the Public Investments Project (PIP) of General Secretariat for Research & Technology (GSRT), under the Emblematic Action “Research in the Agri-Food Sector of Crete", which is part of Subproject 2, “Pilot application of new standards of agricultural production" of the project sector of agri-food” (project code 2018 ΣΕ01300000). The research has been co-financed by the project Smart Diagnostic tools and database to support precision plant protection in horticultural crops in Crete' 'SmartPP' funded by the Crete Operational Program 2014-2020 and co-funded by the European Regional Development Fund (ERDF), under the Priority Axis “Enhancing the Competitiveness, Innovation, and Entrepreneurship of Crete", Action 1.b.1: Demonstration—Experimental Development Projects, Promoting Research and Innovation in RIS3Crete. Also, this study is co-financed by Greece and the European Union (European Social Fund- ESF) through the Operational Programme «Human Resources Development, Education and Lifelong Learning» in the context of the project “Reinforcement of Postdoctoral Researchers—2nd Cycle” (MIS-5033021), implemented by the State Scholarships Foundation (ΙΚΥ) (A.I.).

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Stavrakaki, M., Ilias, A., Ioannidis, P. et al. Investigating mechanisms associated with emamectin benzoate resistance in the tomato borer Tuta absoluta. J Pest Sci (2021). https://doi.org/10.1007/s10340-021-01448-2

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Keywords

  • Tuta absoluta
  • Resistance
  • Avermectins
  • Emamectin benzoate
  • Abamectin
  • Tomato
  • Borer
  • P450s
  • Greece