High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i>
Pyrethroids are widely applied insecticides in agriculture, but their frequent use has provoked many cases of resistance, in which mutations in the voltage-gated sodium channel (VGSC), the pyrethroid target-site, were shown to play a major role. However, for the spider mite <i>Tetranychus urti...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-11-01
|
| Series: | Biology |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2079-7737/11/11/1630 |
| _version_ | 1797469080373952512 |
|---|---|
| author | Berdien De Beer Marilou Vandenhole Christine Njiru Pieter Spanoghe Wannes Dermauw Thomas Van Leeuwen |
| author_facet | Berdien De Beer Marilou Vandenhole Christine Njiru Pieter Spanoghe Wannes Dermauw Thomas Van Leeuwen |
| author_sort | Berdien De Beer |
| collection | DOAJ |
| description | Pyrethroids are widely applied insecticides in agriculture, but their frequent use has provoked many cases of resistance, in which mutations in the voltage-gated sodium channel (VGSC), the pyrethroid target-site, were shown to play a major role. However, for the spider mite <i>Tetranychus urticae</i>, it has also been shown that increased detoxification contributes to resistance against the pyrethroid bifenthrin. Here, we performed QTL-mapping to identify the genomic loci underlying bifenthrin resistance in <i>T. urticae</i>. Two loci on chromosome 1 were identified, with the VGSC gene being located near the second QTL and harboring the well-known L1024V mutation. In addition, the presence of an L925M mutation in the VGSC of a highly bifenthrin-resistant strain and its loss in its derived, susceptible, inbred line indicated the importance of target-site mutations in bifenthrin resistance. Further, RNAseq experiments revealed that genes encoding detoxification enzymes, including carboxyl/choline esterases (CCEs), cytochrome P450 monooxygenases and UDP-glycosyl transferases (UGTs), were overexpressed in resistant strains. Toxicity bioassays with bifenthrin (ester pyrethroid) and etofenprox (non-ester pyrethroid) also indicated a possible role for CCEs in bifenthrin resistance. A selection of CCEs and UGTs were therefore functionally expressed, and CCEinc18 was shown to metabolize bifenthrin, while teturUGT10 could glycosylate bifenthrin-alcohol. To conclude, our findings suggest that both target-site and metabolic mechanisms underlie bifenthrin resistance in <i>T. urticae</i>, and these might synergize high levels of resistance. |
| first_indexed | 2024-03-09T19:15:23Z |
| format | Article |
| id | doaj.art-a662fec1a92d4969adfbd86ea7c216d1 |
| institution | Directory Open Access Journal |
| issn | 2079-7737 |
| language | English |
| last_indexed | 2024-03-09T19:15:23Z |
| publishDate | 2022-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Biology |
| spelling | doaj.art-a662fec1a92d4969adfbd86ea7c216d12023-11-24T03:48:34ZengMDPI AGBiology2079-77372022-11-011111163010.3390/biology11111630High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i>Berdien De Beer0Marilou Vandenhole1Christine Njiru2Pieter Spanoghe3Wannes Dermauw4Thomas Van Leeuwen5Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumPyrethroids are widely applied insecticides in agriculture, but their frequent use has provoked many cases of resistance, in which mutations in the voltage-gated sodium channel (VGSC), the pyrethroid target-site, were shown to play a major role. However, for the spider mite <i>Tetranychus urticae</i>, it has also been shown that increased detoxification contributes to resistance against the pyrethroid bifenthrin. Here, we performed QTL-mapping to identify the genomic loci underlying bifenthrin resistance in <i>T. urticae</i>. Two loci on chromosome 1 were identified, with the VGSC gene being located near the second QTL and harboring the well-known L1024V mutation. In addition, the presence of an L925M mutation in the VGSC of a highly bifenthrin-resistant strain and its loss in its derived, susceptible, inbred line indicated the importance of target-site mutations in bifenthrin resistance. Further, RNAseq experiments revealed that genes encoding detoxification enzymes, including carboxyl/choline esterases (CCEs), cytochrome P450 monooxygenases and UDP-glycosyl transferases (UGTs), were overexpressed in resistant strains. Toxicity bioassays with bifenthrin (ester pyrethroid) and etofenprox (non-ester pyrethroid) also indicated a possible role for CCEs in bifenthrin resistance. A selection of CCEs and UGTs were therefore functionally expressed, and CCEinc18 was shown to metabolize bifenthrin, while teturUGT10 could glycosylate bifenthrin-alcohol. To conclude, our findings suggest that both target-site and metabolic mechanisms underlie bifenthrin resistance in <i>T. urticae</i>, and these might synergize high levels of resistance.https://www.mdpi.com/2079-7737/11/11/1630bifenthrinpyrethroidstarget-site resistancemetabolic resistance<i>Tetranychus urticae</i>carboxyl/choline esterases |
| spellingShingle | Berdien De Beer Marilou Vandenhole Christine Njiru Pieter Spanoghe Wannes Dermauw Thomas Van Leeuwen High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i> Biology bifenthrin pyrethroids target-site resistance metabolic resistance <i>Tetranychus urticae</i> carboxyl/choline esterases |
| title | High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i> |
| title_full | High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i> |
| title_fullStr | High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i> |
| title_full_unstemmed | High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i> |
| title_short | High-Resolution Genetic Mapping Combined with Transcriptome Profiling Reveals That Both Target-Site Resistance and Increased Detoxification Confer Resistance to the Pyrethroid Bifenthrin in the Spider Mite <i>Tetranychus urticae</i> |
| title_sort | high resolution genetic mapping combined with transcriptome profiling reveals that both target site resistance and increased detoxification confer resistance to the pyrethroid bifenthrin in the spider mite i tetranychus urticae i |
| topic | bifenthrin pyrethroids target-site resistance metabolic resistance <i>Tetranychus urticae</i> carboxyl/choline esterases |
| url | https://www.mdpi.com/2079-7737/11/11/1630 |
| work_keys_str_mv | AT berdiendebeer highresolutiongeneticmappingcombinedwithtranscriptomeprofilingrevealsthatbothtargetsiteresistanceandincreaseddetoxificationconferresistancetothepyrethroidbifenthrininthespidermiteitetranychusurticaei AT marilouvandenhole highresolutiongeneticmappingcombinedwithtranscriptomeprofilingrevealsthatbothtargetsiteresistanceandincreaseddetoxificationconferresistancetothepyrethroidbifenthrininthespidermiteitetranychusurticaei AT christinenjiru highresolutiongeneticmappingcombinedwithtranscriptomeprofilingrevealsthatbothtargetsiteresistanceandincreaseddetoxificationconferresistancetothepyrethroidbifenthrininthespidermiteitetranychusurticaei AT pieterspanoghe highresolutiongeneticmappingcombinedwithtranscriptomeprofilingrevealsthatbothtargetsiteresistanceandincreaseddetoxificationconferresistancetothepyrethroidbifenthrininthespidermiteitetranychusurticaei AT wannesdermauw highresolutiongeneticmappingcombinedwithtranscriptomeprofilingrevealsthatbothtargetsiteresistanceandincreaseddetoxificationconferresistancetothepyrethroidbifenthrininthespidermiteitetranychusurticaei AT thomasvanleeuwen highresolutiongeneticmappingcombinedwithtranscriptomeprofilingrevealsthatbothtargetsiteresistanceandincreaseddetoxificationconferresistancetothepyrethroidbifenthrininthespidermiteitetranychusurticaei |