Abstract
In this study, the detoxification enzyme activity and the transcriptional profile changes in the second instar through RNA-sequencing technology due to emamectin benzoate (EB) were assessed. The cytochrome P450 monooxygenases (P450) enzyme activity was not altered by EB due to the change in concentration and exposure time in all treatments. The glutathione S-transferase (GST) enzyme was not considerably varying in all treatments, while exposure time significantly changed the enzyme activity. Results showed that the esterase (Ests) activity was elevated with the increasing concentrations and exposure time. Two libraries were generated, containing 107,767,542 and 108,142,289 clean reads for the samples treated with LC30 of EB and control. These reads were grouped into 218,070 transcripts and 38,097 unigenes. A total of 2257 differentially expressed genes (DEGs) were identified from these unigenes, of which 599 up-regulated and 1658 were down-regulated. The majority of these DEGs related to pesticides resistance were identified in numerous Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways, e.g., steroid hormone biosynthesis, glutathione metabolism, drug metabolism-other enzymes, chemical carcinogenesis, pathways of cancer, metabolism of xenobiotics by cytochrome P450, drug metabolism of cytochrome P450, linoleic acid metabolism, retinol metabolism, and insect hormone biosynthesis. These pathways also shared the same genes as cytochrome P450 monooxygenases (P450s), glutathione S-transferases (GSTs), Esterase (Ests), UDP-glucosyltransferases (UGTs), and ATP-binding cassettes (ABCs). A heatmap analysis also showed that regulation of genes in a pathway causes a series of gene expression regulation in subsequent pathways. Our quantitative reverse transcription-PCR (qRT-PCR) results were consistent with the DEG’s data of transcriptome analysis. The comprehensive transcriptome sequence resource attained through this study evidence that the EB induces significant modification in enzyme activity and transcriptome profile of Paederus fuscipes, which may enable more significant molecular underpinnings behind the insecticide-resistance mechanism for further investigations.
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Data availability
All the data is available in the manuscript.
Abbreviations
- LC10 :
-
Sublethal concentration on which 10% population mortality is expected.
- LC30 :
-
Sublethal concentration on which 30% population mortality is expected.
References
Abdu-Allah GAM, Pittendrigh BR (2018) Lethal and sub-lethal effects of select macrocyclic lactones insecticides on forager worker honey bees under laboratory experimental conditions. Ecotoxicology 27:81–88. https://doi.org/10.1007/s10646-017-1872-6
Alptekin S, Bass C, Nicholls C et al. (2016) Induced thiacloprid insensitivity in honeybees (Apis mellifera L.) is associated with up-regulation of detoxification genes. Insect Mol Biol 25:171–180. https://doi.org/10.1111/imb.12211
Antonova Y, Arik AJ, Moore W, et al (2012) 2 − Insulin-like peptides: structure, signaling, and function. Insect Endocrinol 63–92. https://doi.org/10.1016/B978-0-12-384749-2.10002-0
Araya JE, Araya M, Guerrero MA (2010) Effects of some insecticides applied in sublethal concentrations on the survival and longevity of aphidius ervi (haliday) (hymenoptera: aphidiidae) adults. Chil J Agric Res 70:221–227. https://doi.org/10.4067/S0718-58392010000200005
Azod F, Shahidi-Noghabi S, Mahdian K, Smagghe G (2016) Lethal and sublethal effects of spirotetramat and abamectin on predatory beetles (Menochilus sexmaculatus) via prey (Agonoscena pistaciae) exposure, important for integrated pest management in pistachio orchards. Belgian J Zool 146:113–122
Badisco L, Van Wielendaele P, Vanden Broeck J (2013) Eat to reproduce: a key role for the insulin signaling pathway in adult insects. 4:1–16. https://doi.org/10.3389/fphys.2013.00202
Bilal M, Freed S, Ashraf MZ et al. (2018) Activity of acetylcholinesterase and acid and alkaline phosphatases in different insecticide-treated Helicoverpa armigera (Hübner). Environ Sci Pollut Res 25:22903–22910. https://doi.org/10.1007/s11356-018-2394-3
Böhni R, Riesgo-Escovar J, Oldham S et al. (1999) Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97:865–875. https://doi.org/10.1016/S0092-8674(00)80799-0
Bozzolan F, Siaussat D, Maria A et al (2014) Antennal uridine diphosphate (UDP)-glycosyltransferases in a pest insect: Diversity and putative function in odorant and xenobiotics clearance. Insect Mol Biol 23:539–549
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Britton JS, Lockwood WK, Li L et al. (2002) Drosophila’s insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2:239–249. https://doi.org/10.1016/S1534-5807(02)00117-X
Brogiolo W, Stocker H, Ikeya T et al. (2001) An evolutionarily conserved function of the drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11:213–221. https://doi.org/10.1016/S0960-9822(01)00068-9
Buès R, Bouvier JC, Boudinhon L (2005) Insecticide resistance and mechanisms of resistance to selected strains of Helicoverpa armigera (Lepidoptera: Noctuidae) in the south of France. Crop Prot 24:814–820. https://doi.org/10.1016/j.cropro.2005.01.006
Çağatay NS, Menault P, Riga M et al. (2018) Identification and characterization of abamectin resistance in Tetranychus urticae Koch populations from greenhouses in Turkey. Crop Prot 112:112–117. https://doi.org/10.1016/j.cropro.2018.05.016
Cárcamo JG, Aguilar MN, Barrientos CA et al. (2014) Emamectin benzoate treatment alters the expression and activity of CYP1A, FMO and GST in different tissues of rainbow trout (Oncorhynchus mykiss). Aquaculture 434:188–200. https://doi.org/10.1016/j.aquaculture.2014.08.014
Chang X, Yuan Y, Zhang T et al. (2015) The toxicity and detoxifying mechanism of cycloxaprid and buprofezin in controlling Sogatella furcifera (Homoptera: delphacidae). J Insect Sci 15:2–6. https://doi.org/10.1093/jisesa/iev077
Chen C, Jack J, Garofalo RS (1996) The Drosophila insulin receptor is required for normal growth. Endocrinology 137:846–856. https://doi.org/10.1210/endo.137.3.8603594
Chen X, Zhang YL (2015) Identification and characterisation of multiple glutathione S-transferase genes from the diamondback moth, Plutella xylostella. Pest Manag Sci 71:592–600. https://doi.org/10.1002/ps.3884
Desneux N, Decourtye A, Delpuech J-M (2007) The Sublethal Effects of Pesticides on Beneficial Arthropods. Annu Rev Entomol. https://doi.org/10.1146/annurev.ento.52.110405.091440
Desneux N, Denoyelle R, Kaiser L (2006) A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere 65:1697–1706. https://doi.org/10.1016/j.chemosphere.2006.04.082
Elzen GW (2001) Lethal and sublethal effects of insecticide residues on orius insidiosus (hemiptera: anthocoridae) and geocoris punctipes (hemiptera: lygaeidae). J Econ Entomol 94:55–59. https://doi.org/10.1603/0022-0493(2001)094[0055:LASEOI]2.0.CO;2
Faber H, Vogel M, Karst U (2014) Electrochemistry/mass spectrometry as a tool in metabolism studies-A review. Anal Chim Acta 834:9–21. https://doi.org/10.1016/j.aca.2014.05.017
Frampton GK, van den Brink PJ (2007) Collembola and macroarthropod community responses to carbamate, organophosphate and synthetic pyrethroid insecticides: direct and indirect effects. Environ Pollut 147:14–25. https://doi.org/10.1016/j.envpol.2006.08.038
Galvan TL, Koch RL, Hutchison WD (2005) Effects of spinosad and indoxacarb on survival, development, and reproduction of the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Biol Control 34:108–114. https://doi.org/10.1016/j.biocontrol.2005.04.005
Gao X, Neufeld TP, Pan D (2000) Drosophila PTEN regulates cell growth and proliferation through PI3K- dependent and -independent pathways. Dev Biol 221:404–418. https://doi.org/10.1006/dbio.2000.9680
Genath A, Sharbati S, Buer B et al. (2020) Comparative transcriptomics indicates endogenous differences in detoxification capacity after formic acid treatment between honey bees and varroa mites. Sci Rep 10:21943. https://doi.org/10.1038/s41598-020-79057-9
Goberdhan DCI, Paricio N, Goodman EC et al. (1999) Drosophila tumor suppressor PTEN controls cell size and number by antagonizing the Chico/PI3-kinase signaling pathway. Genes Dev 13:3244–3258. https://doi.org/10.1101/gad.13.24.3244
Gong YJ, Wang ZH, Shi BC et al. (2013) Correlation between pesticide resistance and enzyme activity in the diamondback moth, plutella xylostella. J Insect Sci 13:135. https://doi.org/10.1673/031.013.13501
Grabherr MG, Haas BJ, Yassour M et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Grilo NM, Charneira C, Pereira SA et al. (2014) Bioactivation to an aldehyde metabolite-Possible role in the onset of toxicity induced by the anti-HIV drug abacavir. Toxicol Lett 224:416–423. https://doi.org/10.1016/j.toxlet.2013.10.036
Grosman DM, Upton WW (2006) Efficacy of systemic insecticides for protection of loblolly pine against southern pine engraver beetles (Coleoptera: Curculionidae: Scolytinae) and wood borers (Coleoptera: Cerambycidae). J Econ Entomol 99:94–101. 10.1603/0022-0493(2006)099[0094:EOSIFP]2.0.CO;2
Hafeez M, Liu S, Jan S, et al. (2019) Knock-down of gossypol-inducing cytochrome p450 genes reduced deltamethrin sensitivity in spodoptera exigua (hübner). Int J Mol Sci 20: https://doi.org/10.3390/ijms20092248
Han JB, Li GQ, Wan PJ et al. (2016) Identification of glutathione S-transferase genes in Leptinotarsa decemlineata and their expression patterns under stress of three insecticides. Pestic Biochem Physiol 133:26–34. https://doi.org/10.1016/j.pestbp.2016.03.008
He F, Sun S, Tan H et al. (2019) Compatibility of chlorantraniliprole with the generalist predator Coccinella septempunctata L. (Coleoptera: Coccinellidae) based toxicity, life-cycle development and population parameters in laboratory microcosms. Chemosphere 225:182–190. https://doi.org/10.1016/j.chemosphere.2019.03.025
Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis of insecticide resistance in mosquitoes. In: Insect Biochemistry and Molecular Biology. pp 653–665
Hoffmann K (2014) Insect molecular biology and ecology. CRC Press, Boca Raton
di Hu Z, Feng X, Lin QS et al. (2014) Biochemical mechanism of chlorantraniliprole resistance in the diamondback moth, Plutella xylostella Linnaeus. J Integr Agric 13:2452–2459. https://doi.org/10.1016/S2095-3119(14)60748-6
Huang H, Potter CJ, Tao W et al. (1999) PTEN affects cell size, cell proliferation and apoptosis during Drosophila eye development. Development 126:5365–5372. https://doi.org/10.5167/uzh-627
Iftikhar A, Hafeez F, Hafeez M et al. (2020) Sublethal effects of a juvenile hormone analog, Pyriproxyfen on demographic parameters of non-target predator, Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae). Ecotoxicology 29:1017–1028. https://doi.org/10.1007/s10646-020-02159-7
Jancova P, Anzenbacher P, Anzenbacherova E (2010) Phase II drug metabolizing enzymes. Biomed Pap 154:103–116. https://doi.org/10.5507/bp.2010.017
Jansson RK, Brown R, Cartwright B, et al (1997) Emamectin benzoate: a novel avermectin derivative for control of lepidopterous pests. In: 3rd International Workshop: the Management of Diamondback Moth and Other Crucifer Pests. pp 172–177
Kandil MA-H, Sammour EA, Abdel-Aziz NF, et al (2020) Comparative toxicity of new insecticides generations against tomato leafminer Tuta absoluta and their biochemical effects on tomato plants. Bull Natl Res Cent 44: https://doi.org/10.1186/s42269-020-00382-0
Kang Z-J, Shi B-C, Jin G-H et al. (2014) Correlation between pesticide resistance and enzyme activity in the diamondback moth, plutella xylostella. J Insect Sci 13:1–13. https://doi.org/10.1673/031.013.13501
Kellerová P, Matou P, Vok I et al. (2019) Veterinary parasitology Ivermectin-induced changes in the expression of cytochromes P450 and e ffl ux transporters in haemonchus contortus female and male adults. Vet Parasitol 273:24–31. https://doi.org/10.1016/j.vetpar.2019.07.006
Kenis M, Roy HE, Zindel R, Majerus MEN (2008) Current and potential management strategies against Harmonia axyridis. In: From Biological Control to Invasion: the Ladybird Harmonia Axyridis as a Model Species
Khan MM, Huang Q, Wagan TA et al. (2020a) Behavioral response of Nilaparvata lugens (Stål), Cyrtorhinus lividipennis Reuter and Paederus fuscipes Curtis to three synthetic volatile chemical compounds. J Asia Pac Entomol 23:269–276. https://doi.org/10.1016/j.aspen.2019.12.015
Khan MM, Kaleem-Ullah RM, Siddiqui JA, Ali S (2020b) Insecticide resistance and detoxification enzymes activity in Nilaparvata lugens Stål against neonicotinoids. J Agric Sci 12:24. https://doi.org/10.5539/jas.v12n5p24
Khan MM, Nawaz M, Hua H et al. (2018) Lethal and sublethal effects of emamectin benzoate on the rove beetle, Paederus fuscipes, a non-target predator of rice brown planthopper, Nilaparvata lugens. Ecotoxicol Environ Saf 165:19–24. https://doi.org/10.1016/j.ecoenv.2018.08.047
Kramer JM, Davidge JT, Lockyer JM, Staveley BE (2003) Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol 3:1–4. https://doi.org/10.1186/1471-213X-3-5
Kwon DH, Seong GM, Kang TJ, Lee SH (2010) Multiple resistance mechanisms to abamectin in the two-spotted spider mite. J Asia Pac Entomol 13:229–232. https://doi.org/10.1016/j.aspen.2010.02.002
Laine JE, Auriola S, Pasanen M, Juvonen RO (2009) Acetaminophen bioactivation by human cytochrome P450 enzymes and animal microsomes. Xenobiotica 39:11–21. https://doi.org/10.1080/00498250802512830
Le Gall VL, Klafke GM, Torres TT (2018) Detoxification mechanisms involved in ivermectin resistance in the cattle tick, Rhipicephalus (Boophilus) microplus. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-30907-7
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
Lin T, Cai Z, Wu H (2015) Transcriptome analysis of the Japanese pine sawyer beetle, Monochamus alternatus (Coleoptera: Cerambycidae) by high-throughput Illumina sequencing. J Asia Pac Entomol 18:439–445. https://doi.org/10.1016/j.aspen.2015.04.011
Lin X, Smagghe G (2019) Roles of the insulin signaling pathway in insect development and organ growth. Peptides 122:169923. https://doi.org/10.1016/j.peptides.2018.02.001
Liu Z, Wu J, Zhang Y, et al (2015) Mechanisms of rice planthopper resistance to insecticides. In: Rice Planthoppers: Ecology, Management, Socio Economics and Policy. pp 117–141
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. https://doi.org/10.1006/meth.2001.1262
López JD, Latheef MA, Hoffmann WC (2010) Effect of emamectin benzoate on mortality, proboscis extension, gustation and reproduction of the corn earworm, helicoverpa zea. Source J Insect Sci Publ By Univ Wisconsin Libr J Insect Sci J Insect Sci 10:1–16. https://doi.org/10.1673/031.010.8901
Lu Y, Wu K, Jiang Y et al. (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365. https://doi.org/10.1038/nature11153
Manley GV (1977) A predator of rice in west Malaysia. Entomophaga 22:47–59
Mao T, Li F, Fang Y et al. (2019) Effects of chlorantraniliprole exposure on detoxification enzyme activities and detoxification-related gene expression in the fat body of the silkworm, Bombyx mori. Ecotoxicol Environ Saf 176:58–63. https://doi.org/10.1016/j.ecoenv.2019.03.074
Meng J, Mabubu JI, Han Y et al. (2016) No impact of transgenic cry1C rice on the rove beetle Paederus fuscipes, a generalist predator of brown planthopper Nilaparvata lugens. Sci Rep 6:1–9. https://doi.org/10.1038/srep30303
Nasir S, Akram W, Ahmed F (2012) The population dynamics, ecological and seasonal activity of Paederus fuscipes Curtis (Staphylinidae; Coleoptera) in the Punjab, Pakistan. APCBEE Procedia 4:36–41. https://doi.org/10.1016/j.apcbee.2012.11.007
Nawaz M (2018) Potential effects of chlorantraniliprole and sulfoxaflor on non-specific predator Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Huazhong Agricultural University
Nawaz M, Hafeez M, Mabubu JI et al. (2018) Transcriptomic analysis of differentially expressed genes and related pathways in Harmonia axyridis after sulfoxaflor exposure. Int J Biol Macromol 119:157–165. https://doi.org/10.1016/j.ijbiomac.2018.07.032
Ostrowski S, Dierick HA, Bejsovec A (2002) Genetic control of cuticle formation during embryonic development of Drosophila melanogaster. Genetics 161:171–182
Parsaeyan E, Ali S, Saber M (2018) Effects of emamectin benzoate and cypermethrin on the demography of Trichogramma brassicae Bezdenko. Crop Prot 110:269–274. https://doi.org/10.1016/j.cropro.2017.03.026
Polak M, Starmer WT (1998) Parasite-induced risk of mortality elevates reproductive effort in male Drosophila. Proceeding R Soc London 2197–2202
Puig O, Marr MT, Ruhf ML, Tjian R (2003) Control of cell number by Drosophila FOXO: Downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17:2006–2020. https://doi.org/10.1101/gad.1098703
Saber M (2011) Acute and population level toxicity of imidacloprid and fenpyroximate on an important egg parasitoid, Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). Ecotoxicology 20:1476–1484. https://doi.org/10.1007/s10646-011-0704-3
Shi L, Wei P, Wang X et al. (2016) Functional analysis of esterase TCE2 gene from tetranychus cinnabarinus (boisduval) involved in acaricide resistance. Sci Rep 6:1–12. https://doi.org/10.1038/srep18646
Song Y, Wang H, Chen Y et al. (2017) Cross-resistance and Biochemical Resistance Mechanisms of Emamectin Benzoate Resistant Population of Mythimna separate. Chinese J Pestic Sci 2017: https://doi.org/10.16801/j.issn.1008-7303.2017.0001-en
Stara J, Ourednickova J, Kocourek F (2011) Laboratory evaluation of the side effects of insecticides on Aphidius colemani (Hymenoptera: Aphidiidae), Aphidoletes aphidimyza (Diptera: Cecidomyiidae), and Neoseiulus cucumeris (Acari: Phytoseidae). J Pest Sci (2004) 84:25–31. https://doi.org/10.1007/s10340-010-0322-5
Schmitt A, Nebreda AR(2002) Signalling pathways in oocyte meiotic maturation. J Cell Sci 115:2457–2459
Steuer Costa W, Van der Auwera P, Glock C, et al (2019) A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics. Nat Commun 10: https://doi.org/10.1038/s41467-019-12098-5
Tamò M, Srinivasan R, Dannon E, et al (2012) Biological control: a major component for the long- term cowpea pest management strategy. In: Proceedings of the Fifth World Cowpea Conference. pp 249–259
Tang B, Liu XJ, Shi ZK et al. (2017) Transcriptome analysis and identification of induced genes in the response of Harmonia axyridis to cold hardiness. Comp Biochem Physiol Part D Genomics Proteomics 22:78–89. https://doi.org/10.1016/j.cbd.2017.01.004
de Tang L, Wang XM, Jin FL et al. (2014) De novo sequencing-based transcriptome and digital gene expression analysis reveals insecticide resistance-relevant genes in Propylaea japonica (Thunberg) (Coleoptea: Coccinellidae). PLoS One 9:1–10. https://doi.org/10.1371/journal.pone.0100946
Trapnell C, Williams BA, Pertea G et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621
Tu MP, Yin CM, Tatar M (2002) Impaired ovarian ecdysone synthesis of Drosophila melanogaster insulin receptor mutants. Aging Cell 1:158–160. https://doi.org/10.1046/j.1474-9728.2002.00016.x
Tucca F, Díaz-Jaramillo M, Cruz G et al. (2014) Toxic effects of antiparasitic pesticides used by the salmon industry in the marine amphipod Monocorophium insidiosum. Arch Environ Contam Toxicol 67:139–148. https://doi.org/10.1007/s00244-014-0008-8
Udomsinprasert R, Pongjaroenkit S, Wongsantichon J et al. (2005) Identification, characterization and structure of a new Delta class glutathione transferase isoenzyme. Biochem J 388:763–771. https://doi.org/10.1042/BJ20042015
Ugale TB, Barkhade UP, Moharil MP, Ghule S (2011) Influence of different hosts on induction of midgut carboxylesterase and cytochrome p-450 in Helicoverpa armigera (Hubner) and the effect on insecticide metabolism. Int J Plant Prot 4:7–13
van Asperen K (1962) A study of housefly esterases by means of a sensitive colorimetric method. J Insect Physiol 8: https://doi.org/10.1016/0022-1910(62)90074-4
Verdu J, Buratovicht MA, Wilder EL, Birnbaum MJ (1999) Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat Cell Biol 1:500–506. https://doi.org/10.1038/70293
Waddy SL, Merritt VA, Hamilton-Gibson MN et al. (2007) Relationship between dose of emamectin benzoate and molting response of ovigerous American lobsters (Homarus americanus). Ecotoxicol Environ Saf 67:95–99. https://doi.org/10.1016/j.ecoenv.2006.05.002
Wang W, Gao C, Ren L, Luo Y (2019) The effect of longwave ultraviolet light radiation on Dendrolimus tabulaeformis antioxidant and detoxifying enzymes. Insects 11:1–11. https://doi.org/10.3390/insects11010001
Wang X, Khakame SK, Ye C et al. (2013) Characterisation of field-evolved resistance to chlorantraniliprole in the diamondback moth, Plutella xylostella, from China. Pest Manag Sci 69:661–665. https://doi.org/10.1002/ps.3422
Wang XW, Luan JB, Li JM et al. (2010) De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 11:. https://doi.org/10.1186/1471-2164-11-400
Wei DD, Chen EH, Ding TB et al. (2013) De novo assembly, gene annotation, and marker discovery in stored-product pest Liposcelis entomophila (enderlein) using transcriptome sequences. PLoS One 8:e80046. https://doi.org/10.1371/journal.pone.0080046
Wei S, Zhang H, Li B et al. (2019) Insecticidal effect of aconitine on the rice brown planthoppers. PLoS One 14:1–11. https://doi.org/10.1371/journal.pone.0221090
Weinkove D, Neufeld TP, Twardzik T et al. (1999) Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor. Curr Biol 9:1019–1029. https://doi.org/10.1016/S0960-9822(99)80450-3
Weisburger JH (1999) Carcinogenicity and mutagenicity testing, then and now. Mutat Res - Rev Mutat Res 437:105–112. https://doi.org/10.1016/S1383-5742(99)00077-0
Wu S, Yang Y, Yuan G et al. (2011) Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. Insect Biochem Mol Biol 41:14–21. https://doi.org/10.1016/j.ibmb.2010.09.007
Yorulmaz S, Ay R (2009) Multiple resistance, detoxifying enzyme activity, and inheritance of abamectin resistance in Tetranychus urticae Koch (Acarina: Tetranychidae). Turkish J Agric For 33:393–402. https://doi.org/10.3906/tar-0809-15
Yu C, Lin R, Fu M et al. (2014) Impact of imidacloprid on life-cycle development of Coccinella septempunctata in laboratory microcosms. Ecotoxicol Environ Saf 110:168–173. https://doi.org/10.1016/j.ecoenv.2014.08.022
Yuan J, Wang X, Gu Z et al. (2015) Activity and transcriptional responses of hepatopancreatic biotransformation and antioxidant enzymes in the oriental river prawn Macrobrachium nipponense exposed to microcystin-LR. Toxins (Basel) 7:4006–4022. https://doi.org/10.3390/toxins7104006
Zanger UM, Schwab M (2013) Cytochrome P450 enzymes in drug metabolism: Regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol Ther 138:103–141. https://doi.org/10.1016/j.pharmthera.2012.12.007
Zhang BZ, Su X, Zhen CA 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
Zhang Y, Jiang R, Wu H et al. (2012) Next-generation sequencing-based transcriptome analysis of Cryptolaemus montrouzieri under insecticide stress reveals resistance-relevant genes in ladybirds. Genomics 100:35–41. https://doi.org/10.1016/j.ygeno.2012.05.002
Zhu J, He Y, Gao M et al. (2011) Photodegradation of emamectin benzoate and its influence on efficacy against the rice stem borer, Chilo suppressalis. Crop Prot 30:1356–1362. https://doi.org/10.1016/j.cropro.2011.06.006
Acknowledgements
We want to thank Prof. Dr. Hua Hongxia, Huazhong Agricultural University, and Wuhan China to fund this project. We thank Dr. Yueping He (Huazhong Agricultural University, Wuhan, China) for his valuable guidance and statistical assistance during this study.
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This work was financially supported by the State Key Special Program (2017YFD0301400).
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MMK: Conceptualization, Formal analysis, Investigation, Methodology, Writing—original draft. AHK: Formal analysis, MWA: Methodology, MH: Formal analysis, DC: Resources, FZ: Resources, SA: Software: MS: Writing—review & editing.
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Khan, M.M., Khan, A.H., Ali, M.W. et al. Emamectin benzoate induced enzymatic and transcriptional alternation in detoxification mechanism of predatory beetle Paederus fuscipes (Coleoptera: Staphylinidae) at the sublethal concentration. Ecotoxicology 30, 1227–1241 (2021). https://doi.org/10.1007/s10646-021-02426-1
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DOI: https://doi.org/10.1007/s10646-021-02426-1