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 Tetranychus urticae

Abstract

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 Tetranychus urticae, 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 T. urticae. 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 T. urticae, and these might synergize high levels of resistance.

Intraspecific diversity in the mechanisms underlying abamectin resistance in a cosmopolitan pest

“…Cases of target‐site insensitivity underlying resistance, as well as metabolic detoxification and transport of pesticides via enzyme families such as cytochrome P450 mono‐oxygenases (CYPs), glutathione S‐transferases (GSTs), carboxyl/cholinesterases (CCEs) and ATP‐binding cassette (ABC) transporters, have been reported across different taxa (Feyereisen et al, 2015 ; Van Leeuwen & Dermauw, 2016 ). In addition, enzymes of the uridine diphosphate (UDP)‐glycosyltransferases (UGTs) and transporters of the Major Facilitator Superfamily (MFS) have been associated with resistance (Ahn et al, 2012 , 2014 ; De Beer, Vandenhole, et al, 2022 ; Dermauw et al, 2012 ; Snoeck, Pavlidi, et al, 2019 ). Finally, horizontally transferred genes from bacteria and fungi (Wybouw et al, 2016 ), such as the intra‐diol ring cleavage dioxygenases (DOGs) from spider mites, can convey unexpected metabolic capacities that were previously overlooked in studying xenobiotic metabolism, such as aromatic ring cleavage (Njiru et al, 2022 ).…”

The Host Plant Strongly Modulates Acaricide Resistance Levels to Mitochondrial Complex Ii Inhibitors in a Multi-Resistant Field Population of Tetranychus Urticae

“…urticae (De Beer et al, 2022a, 2022bFotoukkiaii et al, 2021;Kurlovs et al, 2022;Lu et al, 2023). As such, whether infection occurred by chance or is related to the host plant shift, remains unclear and little is known on how these viruses interact with their hosts.…”

The complex II resistance mutation H258Y in succinate dehydrogenase subunit B causes fitness penalties associated with mitochondrial respiratory deficiency

“…The spider mite Tetranychus urticae is a major agricultural pest that quickly develops resistance to pesticides of varying modes of action. The resistance traits are often complex, involving a combination of multiple factors 21–26 . In most resistance cases, both metabolic detoxification genes and target‐site mutations have been identified in the resistant phenotypes 2,4,22,27 .…”

“…The resistance traits are often complex, involving a combination of multiple factors. [21][22][23][24][25][26] In most resistance cases, both metabolic detoxification genes and target-site mutations have been identified in the resistant phenotypes. 2,4,22,27 By carrying out repeated backcrossing, a number of target site mutations have been uncoupled from other mechanisms and their relative contribution to resistance assessed.…”