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Silencing of CYP6AS160 in Solenopsis invicta Buren by RNA interference enhances worker susceptibility to fipronil

Published online by Cambridge University Press:  09 August 2021

Bai-Zhong Zhang Open the ORCID record for Bai-Zhong Zhang [Opens in a new window] ,
Gui-Lei Hu ,
Liu-Yang Lu ,
Xi-Ling Chen  and
Xi-Wu Gao
Bai-Zhong Zhang
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang453003, P.R. China Department of Entomology, China Agricultural University, Beijing100193, P.R. China
Gui-Lei Hu
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang453003, P.R. China
Liu-Yang Lu
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang453003, P.R. China
Xi-Ling Chen
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang453003, P.R. China
Xi-Wu Gao*
Affiliation:
Department of Entomology, China Agricultural University, Beijing100193, P.R. China
*
Author for correspondence: Xi-Wu Gao, Email: gaoxiwu@263.net.cn
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Abstract

Cytochrome P450 monooxygenases play a key role in pest resistance to insecticides by detoxification. Four new P450 genes, CYP6AS160, CYP6AS161, CYP4AB73 and CYP4G232 were identified from Solenopsis invicta. CYP6AS160 was highly expressed in the abdomen and its expression could be induced significantly with exposure to fipronil, whereas CYP4AB73 was not highly expressed in the abdomen and its expression could not be significantly induced following exposure to fipronil. Expression levels of CYP6AS160 and CYP4AB73 in workers were significantly higher than that in queens. RNA interference-mediated gene silencing by feeding on double-stranded RNA (dsRNA) found that the levels of this transcript decreased (by maximum to 64.6%) when they fed on CYP6AS160-specific dsRNA. Workers fed dsCYP6AS160 had significantly higher mortality after 24 h of exposure to fipronil compared to controls. Workers fed dsCYP6AS160 had reduced total P450 activity of microsomal preparations toward model substrates p-nitroanisole. However, the knockdown of a non-overexpressed P450 gene, CYP4AB73 did not lead to an increase of mortality or a decrease of total P450 activity. The knockdown effects of CYP6AS160 on worker susceptibility to fipronil, combined with our other findings, indicate that CYP6AS160 is responsible for detoxification of fipronil. Feeding insects dsRNA may be a general strategy to trigger RNA interference and may find applications in entomological research and in the control of insect pests in the field.

Keywords

FipronilP450RNAiSolenopsis invictatolerance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 2 , April 2022 , pp. 171 - 178
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Aravin, AA, Naumova, NM, Tulin, AV, Vagin, VV, Rozovsky, YM and Gvozdev, VA (2001) Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Current Biology 11, 1017–1027.CrossRefGoogle ScholarPubMed
Asokan, R, Chandra, GS, Manamohan, M, Kumar, NK and Sita, T (2014) Response of various target genes to diet-delivered dsRNA mediated RNA interference in the cotton bollworm, Helicoverpa armigera. Journal of Pest Science 87, 63–172.CrossRefGoogle Scholar
Badisco, L, Marchal, E, Van Wielendaele, P, Verlinden, H, Vleugels, R and Broeck, JV (2011) RNA interference of insulin-related peptide and neuroparsins affects vitellogenesis in the desert locust. Schistocerca gregaria. Peptides 32, 573–580.CrossRefGoogle ScholarPubMed
Baum, JA, Bogaert, T, Clinton, W, Heck, GR, Feldmann, P, Ilagan, O, Johnson, S, Plaetinck, G, Munyikwa, T, Pleau, M, Vaughn, T and Vaughn, T (2007) Control of coleopteran insect pests through RNA interference. Nature Biotechnology 25, 1322–1326.CrossRefGoogle ScholarPubMed
Bautista, MAM, Tanaka, T and Miyata, T (2007) Identification of permethrin-inducible cytochrome P450s from the diamondback moth, Plutella xylostella (L.) and the possibility of involvement in permethrin resistance. Pesticide Biochemistry and Physiology 87, 85–93.CrossRefGoogle Scholar
Bellés, X (2010) Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annual Review of Entomology 55, 111–128.CrossRefGoogle ScholarPubMed
Bloch, G, Wheeler, DE and Robinson, GE (2009) Endocrine influences on the organization of insect societies. Hormones 2, 1027–1068.Google Scholar
Bradford, MM (1976) A rapid sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle Scholar
Buczkowski, G, Wang, C and Bennett, G (2007) Immunomarking reveals food flow and feeding relationships in the eastern subterranean termite, Reticulitermes flavipes (Kollar). Environmental Entomology 36, 173–182.CrossRefGoogle Scholar
Cabrera, BJ and Rust, MK (1999) Caste differences in feeding and trophallaxis in the western drywood termite, Incisitermes minor (Hagen) (Isoptera, Kalotermitidae). Insectes Sociaux 46, 244–249.CrossRefGoogle Scholar
Cheng, D, Zhang, Z, He, X and Liang, GW (2013) Validation of reference genes in, Solenopsis invicta, in different developmental stages, castes and tissues. PLoS One 8, e57718.CrossRefGoogle ScholarPubMed
Cornette, R, Koshikawa, S, Hojo, M, Matsumoto, T and Miura, T (2006) Caste-specific cytochrome P450 in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae). Insect Molecular Biology 15, 235–244.CrossRefGoogle Scholar
Feyereisen, R (2005) Insect cytochrome P450. Comprehensive Molecular Insect Science 4, 1–77.Google Scholar
Ffrench-Constant, RH, Daborn, PJ and Goff, GL (2004) The genetics and genomics of insecticide resistance. Trends in Genetics 20, 163–170.CrossRefGoogle ScholarPubMed
Fire, A, Xu, S, Montgomery, MK, Kostas, SA, Driver, SE and Mello, CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.CrossRefGoogle ScholarPubMed
Gatehouse, JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytologist 156, 145–169.CrossRefGoogle ScholarPubMed
Gordon, KH and Waterhouse, PM (2007) RNAi for insect-proof plants. Nature Biotechnology 25, 1231–1232.CrossRefGoogle ScholarPubMed
Greenberg, L, Reierson, D and Rust, MK (2003) Fipronil trials in California against the red imported fire ant, Solenopsis invicta Buren, using sugar water consumption and mound counts as measures of ant abundance. Journal of Agricultural and Urban Entomology 20, 221–233.Google Scholar
Hamilton, WD (1972) Altruism and related phenomena, mainly in social insects. Annual Review of Ecology and Systematics 3, 193–232.CrossRefGoogle Scholar
Hoffmann, BD, Luque, GM, Bellard, C, Holmes, ND and Donlan, CJ (2016) Improving invasive ant eradication as a conservation tool: a review. Biological Conservation 198, 37–49.CrossRefGoogle Scholar
Hu, XP, Song, DL and Scherer, CW (2005) Transfer of indoxacarb among workers of Coptotermes formosanus (Isoptera: Rhinoter-mitidae): effects of dose, donor: recipient ratio and post-exposure time. Pest Management Science 61, 1209–1214.CrossRefGoogle Scholar
Huvenne, H and Smagghe, G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. Journal of Insect Physiology 56, 227–235.CrossRefGoogle ScholarPubMed
Johnson, RM, Wen, Z, Schuler, MA and Berenbaum, MR (2006) Mediation of pyrethroid insecticide toxicity to honey bees (Hymenoptera: Apidae) by cytochrome P450 monooxygenases. Journal of Economic Entomology 99, 1046–1050.CrossRefGoogle ScholarPubMed
Johnson, RM, Pollock, HS and Berenbaum, MR (2009) Synergistic interactions between in-hive miticides in Apis mellifera. Journal of Economic Entomology 102, 474–479.CrossRefGoogle ScholarPubMed
Kuriachan, I and Vinson, SB (2000) A queen's worker attractiveness influences her movement in polygynous colonies of the red imported fire ant (Hymenoptera: Formicidae) in response to adverse temperatures. Environmental Entomology 29, 943–949.CrossRefGoogle Scholar
Liu, N and Scott, JG (1998) Increased transcription of CYP6D1 causes cytochrome P450-mediated insecticide resistance in house fly. Insect Biochemistry and Molecular Biology 28, 531–535.CrossRefGoogle ScholarPubMed
Liu, N and Zhang, L (2004) CYP4AB1, CYP4AB2, and Gp-9 gene overexpression associated with workers of the red imported fire ant, Solenopsis invicta Buren. Gene 327, 81–87.CrossRefGoogle ScholarPubMed
Liu, N, Li, M, Gong, Y, Liu, F and Li, T (2015) Cytochrome p450s – their expression, regulation, and role in insecticide resistance. Pesticide Biochemistry & Physiology 120, 77–81.CrossRefGoogle ScholarPubMed
Loftin, K, Hopkins, J, Gavin, J and Shanklin, D (2003) Evaluation of broadcast applications of various contact insecticides against red imported fire ants, Solenopsis invicta Buren. Journal of Agricultural and Urban Entomology 20, 151–156.Google Scholar
Mao, YB, Cai, WJ, Wang, JW, Hong, GJ, Tao, XY, Wang, LJ, Huang, YP and Chen, XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnology 25, 1307–1313.CrossRefGoogle ScholarPubMed
Mao, W, Rupasinghe, SG, Johnson, RM, Zangerl, AR, Schuler, MA and Berenbaum, MR (2009) Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 154, 427–434.CrossRefGoogle Scholar
Mao, W, Schuler, MA and Berenbaum, MR (2011) CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proceedings of the National Academy of Sciences 108, 12657–12662.CrossRefGoogle Scholar
Marr, R, O'Dowd, D and Green, P (2003) Assessment of non-target impacts on Presto 01 ant bait on litter invertebrates in Christmas Island National Park, Indian Ocean, School of Biological Sciences. Report to Parks Australia North. Monash University, Melbourne.Google Scholar
Mazumdar-Leighton, S and Broadway, RM (2001) Identification of six chymotrypsin cDNAs from larval midguts of Helicoverpa zea and Agrotis ipsilon feeding on the soybean (Kunitz) trypsin inhibitor. Insect Biochemistry and Molecular Biology 31, 633–644.CrossRefGoogle ScholarPubMed
Niu, QW, Lin, SS, Reyes, JL, Chen, KC, Wu, HW, Yeh, SD and Chua, NH (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nature Biotechnology 24, 1420–1428.CrossRefGoogle ScholarPubMed
Ott, SR, Verlinden, H, Rogers, SM, Brighton, CH, Quah, PS, Vleugels, RK, Verdonck, R and Broeck, JV (2012) Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust. Proceedings of the National Academy of Sciences 109, E381–E387.CrossRefGoogle ScholarPubMed
Passera, L, Aron, S, Vargo, EL and Keller, L (2001) Queen control of sex ratio in fire ants. Science (New York, N.Y.) 293, 1308–1310.CrossRefGoogle ScholarPubMed
Pennisi, E (2001) Queens, not workers, rule the ant nest. Science (New York, N.Y.) 293, 1239–1241.CrossRefGoogle Scholar
Pfaffl, MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45–e45.CrossRefGoogle ScholarPubMed
Pilling, ED, Bromleychallenor, KAC, Walker, CH and Jepson, PC (1995) Mechanism of synergism between the pyrethroid insecticide λ-cyhalothrin and the imidazole fungicide prochloraz, in the honeybee (Apis mellifera L). Pesticide Biochemistry and Physiology 51, 1–11.CrossRefGoogle Scholar
Robinson, GE (2002) Genomics and integrative analyses of division of labor in honeybee colonies. The American Naturalist 160, 160–171.CrossRefGoogle ScholarPubMed
Rose, RL, Barbhaiya, L, Roe, RM, Rock, GC and Hodgson, E (1995) Cytochrome P450-associated insecticide resistance and the development of biochemical diagnostic assays in Heliothis virescens. Pesticide Biochemistry and Physiology 51, 178–191.CrossRefGoogle Scholar
Scott, JG, Liu, N and Wen, Z (1998) Insect cytochromes P450: diversity, insecticide resistance and tolerance to plant toxins. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 121, 147–155.Google ScholarPubMed
Shukla, JN, Kalsi, M, Sethi, A, Narva, KE, Fishilevich, E, Singh, S, Mogilicherla, K and Palli, SR (2016) Reduced stability and intracellular transport of dsRNA contribute to poor RNAi response in lepidopteran insects. RNA Biology 13, 656–669.CrossRefGoogle ScholarPubMed
Tabara, H, Sarkissian, M, Kelly, WG, Fleenor, J, Grishok, A, Timmons, L, Fire, A and Mello, CC (1999) The rde-1 Gene, RNA interference, and transposon silencing in C. elegans. Cell 99, 123–132.CrossRefGoogle ScholarPubMed
Tarver, MR, Coy, MR and Scharf, ME (2012) Cyp15F1: a novel cytochrome p450 gene linked to juvenile hormone-dependent caste differention in the termite Reticulitermes flavipes. Archives of Insect Biochemistry and Physiology 80, 92–108.CrossRefGoogle ScholarPubMed
Tenllado, F and Dıaz-Ruız, JR (2001) Double-stranded RNA-mediated interference with plant virus infection. Journal of Virology 75, 12288–12297.CrossRefGoogle ScholarPubMed
Turner, CT, Davy, MW, MacDiarmid, RM, Plummer, KM, Birch, NP and Newcomb, RD (2006) RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Molecular Biology 15(3), 383–391.CrossRefGoogle ScholarPubMed
Van Wielendaele, P, Dillen, S, Marchal, E, Badisco, L and Broeck, JV (2012) CRF-like diuretic hormone negatively affects both feeding and reproduction in the desert locust, Schistocerca gregaria. PLoS One 7, e31425.CrossRefGoogle ScholarPubMed
Vinson, SB (1997) Invasion of the red imported fire ant (Hymenoptera: Formicidae) spread, biology and impact. American Entomologist 43, 23–39.CrossRefGoogle Scholar
Wang, L, Lu, YY, Xu, YJ and Zeng, L (2013) The current status of research on Solenopsis invicta Buren (Hymenoptera: Formicidae) in Mainland China. Asian Myrmecology 5, 125–137.Google Scholar
Wesley, SV, Helliwell, CA, Smith, NA, Wang, M, Rouse, DT, Liu, Q, Gooding, PS, Singh, SP, Abbott, D, Stoutjesdijk, PA, Robinson, SP, Gleave, AP, Green, AG, Waterhouse, PM and Robinson, SP (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. The Plant Journal 27, 581–590.CrossRefGoogle ScholarPubMed
Wittstock, U, Agerbirk, N, Stauber, EJ, Olsen, CE, Hippler, M, Mitchell-Olds, T, Gershenzon, J and Vogel, H (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proceedings of the National Academy of Sciences of the United States of America 101, 4859–4864.CrossRefGoogle ScholarPubMed
Zhang, B, Kong, F, Wang, H, Gao, X, Zeng, X and Shi, X (2016) Insecticide induction of o-demethylase activity and expression of cytochrome P450 genes in the red imported fire ant (Solenopsis invicta Buren). Journal of Integrative Agriculture 15, 135–144.CrossRefGoogle Scholar
Zhang, B, Su, X, Xie, L, Zhen, C, Hu, G, Jiang, K, Huang, ZY, Liu, R, Gao, Y, Chen, X and Gao, X (2020) Multiple detoxification genes confer imidacloprid resistance to Sitobion avenae Fabricius. Crop Protection 128, 105014.CrossRefGoogle Scholar
Zhou, X, Wheeler, MM, Oi, FM and Scharf, ME (2008) RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochemistry and Molecular Biology 38, 805–815.CrossRefGoogle ScholarPubMed