Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua
The evolution of insect resistance to insecticides is frequently associated with overexpression of one or more cytochrome P450 enzyme genes. Although overexpression of CYP450 genes is a well-known mechanism of insecticide resistance, the underlying regulatory mechanisms are poorly understood. Here w...
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| Veröffentlicht in: | PLoS genetics 2021-03, Vol.17 (3), p.e1009403 |
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| creator | Hu, Bo Huang, He Hu, Songzhu Ren, Miaomiao Wei, Qi Tian, Xiangrui Esmail Abdalla Elzaki, Mohammed Bass, Chris Su, Jianya Reddy Palli, Subba |
| description | The evolution of insect resistance to insecticides is frequently associated with overexpression of one or more cytochrome P450 enzyme genes. Although overexpression of CYP450 genes is a well-known mechanism of insecticide resistance, the underlying regulatory mechanisms are poorly understood. Here we uncovered the mechanisms of overexpression of the P450 gene, CYP321A8 in a major pest insect, Spodoptera exigua that is resistant to multiple insecticides. CYP321A8 confers resistance to organophosphate (chlorpyrifos) and pyrethroid (cypermethrin and deltamethrin) insecticides in this insect. Constitutive upregulation of transcription factors CncC/Maf are partially responsible for upregulated expression of CYP321A8 in the resistant strain. Reporter gene assays and site-directed mutagenesis analyses demonstrated that CncC/Maf enhanced the expression of CYP321A8 by binding to specific sites in the promoter. Additional cis-regulatory elements resulting from a mutation in the CYP321A8 promoter in the resistant strain facilitates the binding of the orphan nuclear receptor, Knirps, and enhances the promoter activity. These results demonstrate that two independent mechanisms; overexpression of transcription factors and mutations in the promoter region resulting in a new cis-regulatory element that facilitates binding of the orphan nuclear receptor are involved in overexpression of CYP321A8 in insecticide-resistant S. exigua. |
| doi_str_mv | 10.1371/journal.pgen.1009403 |
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Although overexpression of CYP450 genes is a well-known mechanism of insecticide resistance, the underlying regulatory mechanisms are poorly understood. Here we uncovered the mechanisms of overexpression of the P450 gene, CYP321A8 in a major pest insect, Spodoptera exigua that is resistant to multiple insecticides. CYP321A8 confers resistance to organophosphate (chlorpyrifos) and pyrethroid (cypermethrin and deltamethrin) insecticides in this insect. Constitutive upregulation of transcription factors CncC/Maf are partially responsible for upregulated expression of CYP321A8 in the resistant strain. Reporter gene assays and site-directed mutagenesis analyses demonstrated that CncC/Maf enhanced the expression of CYP321A8 by binding to specific sites in the promoter. Additional cis-regulatory elements resulting from a mutation in the CYP321A8 promoter in the resistant strain facilitates the binding of the orphan nuclear receptor, Knirps, and enhances the promoter activity. These results demonstrate that two independent mechanisms; overexpression of transcription factors and mutations in the promoter region resulting in a new cis-regulatory element that facilitates binding of the orphan nuclear receptor are involved in overexpression of CYP321A8 in insecticide-resistant S. exigua.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1009403</identifier><identifier>PMID: 33690635</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Binding sites ; Bioassays ; Biology and Life Sciences ; Cytochrome ; DNA ; Enzymatic activity ; Enzymes ; Gene regulation ; Genes ; Genetic aspects ; Insecticide resistance ; Insecticides ; Insects ; Lepidoptera ; Metabolism ; Molecular modelling ; Mortality ; Mutation ; Natural history ; Pesticide resistance ; Physiological aspects ; Proteins ; Regulatory sequences ; Research and Analysis Methods ; Transcription factors</subject><ispartof>PLoS genetics, 2021-03, Vol.17 (3), p.e1009403</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Hu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Hu et al 2021 Hu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-10855c08a8c79055f7636b0c22b424d822a30f86d9cbf7990be45d463445b9373</citedby><cites>FETCH-LOGICAL-c726t-10855c08a8c79055f7636b0c22b424d822a30f86d9cbf7990be45d463445b9373</cites><orcidid>0000-0002-2590-1492 ; 0000-0001-9979-1356 ; 0000-0002-3749-3246 ; 0000-0002-0873-3247 ; 0000-0002-7290-635X ; 0000-0001-8363-038X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7978377/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7978377/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33690635$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ewer, John</contributor><creatorcontrib>Hu, Bo</creatorcontrib><creatorcontrib>Huang, He</creatorcontrib><creatorcontrib>Hu, Songzhu</creatorcontrib><creatorcontrib>Ren, Miaomiao</creatorcontrib><creatorcontrib>Wei, Qi</creatorcontrib><creatorcontrib>Tian, Xiangrui</creatorcontrib><creatorcontrib>Esmail Abdalla Elzaki, Mohammed</creatorcontrib><creatorcontrib>Bass, Chris</creatorcontrib><creatorcontrib>Su, Jianya</creatorcontrib><creatorcontrib>Reddy Palli, Subba</creatorcontrib><title>Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The evolution of insect resistance to insecticides is frequently associated with overexpression of one or more cytochrome P450 enzyme genes. Although overexpression of CYP450 genes is a well-known mechanism of insecticide resistance, the underlying regulatory mechanisms are poorly understood. Here we uncovered the mechanisms of overexpression of the P450 gene, CYP321A8 in a major pest insect, Spodoptera exigua that is resistant to multiple insecticides. CYP321A8 confers resistance to organophosphate (chlorpyrifos) and pyrethroid (cypermethrin and deltamethrin) insecticides in this insect. Constitutive upregulation of transcription factors CncC/Maf are partially responsible for upregulated expression of CYP321A8 in the resistant strain. Reporter gene assays and site-directed mutagenesis analyses demonstrated that CncC/Maf enhanced the expression of CYP321A8 by binding to specific sites in the promoter. Additional cis-regulatory elements resulting from a mutation in the CYP321A8 promoter in the resistant strain facilitates the binding of the orphan nuclear receptor, Knirps, and enhances the promoter activity. These results demonstrate that two independent mechanisms; overexpression of transcription factors and mutations in the promoter region resulting in a new cis-regulatory element that facilitates binding of the orphan nuclear receptor are involved in overexpression of CYP321A8 in insecticide-resistant S. exigua.</description><subject>Binding sites</subject><subject>Bioassays</subject><subject>Biology and Life Sciences</subject><subject>Cytochrome</subject><subject>DNA</subject><subject>Enzymatic activity</subject><subject>Enzymes</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Insecticide resistance</subject><subject>Insecticides</subject><subject>Insects</subject><subject>Lepidoptera</subject><subject>Metabolism</subject><subject>Molecular modelling</subject><subject>Mortality</subject><subject>Mutation</subject><subject>Natural history</subject><subject>Pesticide resistance</subject><subject>Physiological 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John</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2021-03-09</date><risdate>2021</risdate><volume>17</volume><issue>3</issue><spage>e1009403</spage><pages>e1009403-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The evolution of insect resistance to insecticides is frequently associated with overexpression of one or more cytochrome P450 enzyme genes. Although overexpression of CYP450 genes is a well-known mechanism of insecticide resistance, the underlying regulatory mechanisms are poorly understood. Here we uncovered the mechanisms of overexpression of the P450 gene, CYP321A8 in a major pest insect, Spodoptera exigua that is resistant to multiple insecticides. CYP321A8 confers resistance to organophosphate (chlorpyrifos) and pyrethroid (cypermethrin and deltamethrin) insecticides in this insect. Constitutive upregulation of transcription factors CncC/Maf are partially responsible for upregulated expression of CYP321A8 in the resistant strain. Reporter gene assays and site-directed mutagenesis analyses demonstrated that CncC/Maf enhanced the expression of CYP321A8 by binding to specific sites in the promoter. Additional cis-regulatory elements resulting from a mutation in the CYP321A8 promoter in the resistant strain facilitates the binding of the orphan nuclear receptor, Knirps, and enhances the promoter activity. These results demonstrate that two independent mechanisms; overexpression of transcription factors and mutations in the promoter region resulting in a new cis-regulatory element that facilitates binding of the orphan nuclear receptor are involved in overexpression of CYP321A8 in insecticide-resistant S. exigua.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33690635</pmid><doi>10.1371/journal.pgen.1009403</doi><orcidid>https://orcid.org/0000-0002-2590-1492</orcidid><orcidid>https://orcid.org/0000-0001-9979-1356</orcidid><orcidid>https://orcid.org/0000-0002-3749-3246</orcidid><orcidid>https://orcid.org/0000-0002-0873-3247</orcidid><orcidid>https://orcid.org/0000-0002-7290-635X</orcidid><orcidid>https://orcid.org/0000-0001-8363-038X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Binding sites Bioassays Biology and Life Sciences Cytochrome DNA Enzymatic activity Enzymes Gene regulation Genes Genetic aspects Insecticide resistance Insecticides Insects Lepidoptera Metabolism Molecular modelling Mortality Mutation Natural history Pesticide resistance Physiological aspects Proteins Regulatory sequences Research and Analysis Methods Transcription factors |
| title | Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua |
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