QTL mapping suggests that both cytochrome P450-mediated detoxification and target-site resistance are involved in fenbutatin oxide resistance in Tetranychus urticae

Beer, Berdien De; Villacis‐Perez, Ernesto; Khalighi, Mousaalreza; Saalwaechter, Corinna; Vandenhole, Marilou; Jonckheere, Wim; Ismaeil, Ibrahim; Geibel, Sven; Leeuwen, Thomas Van; Dermauw, Wannes

doi:10.1016/j.ibmb.2022.103757

Cited by 23 publications

(35 citation statements)

References 113 publications

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“…This was especially true for Na + channel modulators, GluCl allosteric modulators, inhibitors of mitochondrial ATP synthase, and METI-I compounds. Compared to MR-VPi, which is notably more resistant to METI-Is, MAR-ABi exhibited higher resistance to other classes, especially for inhibitors of mitochondrial ATP synthase (this study and De Beer et al [55]). In contrast to MR-VPi and MAR-ABi, JP-RRi showed intermediate resistance to most acaricide classes, with modestly higher resistance levels to METI-II compounds.…”

Section: Resultssupporting

confidence: 53%

“…Further, a recent BSA study that used two sets of fenbutatin oxide susceptible and resistant parental strains, including SOL- BEi and MAR-ABi, identified a candidate target site resistance mutation (V89A) for fenbutatin oxide in the gene encoding subunit c of mitochondrial ATP-synthase ( tetur06g03780 ) (present in resistant MAR- ABi, absent in susceptible SOL-BEi) [55]. We also found this mutation in ROS-ITi in addition to MAR- ABi; however, as noted by De Beer et al [55], this gene is duplicated and while the parental MAR-AB outbred strain was reported to have the mutations in both copies, only a single copy bears the mutation after inbreeding in both MAR-ABi and ROS-ITi. This probably explains the absence of resistance in ROS-ITi, and strongly suggests additional metabolic mechanisms of resistance in MAR-ABi.…”

Section: Resultsmentioning

confidence: 99%

“…The L915M mutation in the voltage gated sodium channel (VGSC, tetur34g00970) is associated with resistance to pyrethroids in Varroa destructor [58][59][60], and was present in all the strains highly resistant to bifenthrin (SOL-BEi, MAR-ABi, and MR-VPi). Further, a recent BSA study that used two sets of fenbutatin oxide susceptible and resistant parental strains, including SOL-BEi and MAR-ABi, identified a candidate target site resistance mutation (V89A) for fenbutatin oxide in the gene encoding subunit c of mitochondrial ATP-synthase (tetur06g03780) (present in resistant MAR-ABi, absent in susceptible SOL-BEi) [55]. We also found this mutation in ROS-ITi in addition to MAR-ABi; however, as noted by De Beer et al [55], this gene is duplicated and while the parental MAR-AB outbred strain was reported to have the mutations in both copies, only a single copy bears the mutation after inbreeding in both MAR-ABi and ROS-ITi.…”

Section: The Inbred Strains Have Diverse and Contrasting Resistance P...mentioning

confidence: 99%

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Abundant trans-driven variation in detoxification gene expression in the extreme generalist herbivore Tetranychus urticae

Kurlovs

Beer

et al. 2022

Preprint

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The extreme adaptation potential of the generalist herbivore Tetranychus urticae (the two-spotted spider mite) to pesticides as well as diverse host plants has been associated with clade-specific gene expansions in known detoxifying enzyme families, and with extensive and rapid transcriptional responses. However, how this broad transcriptional potential is regulated remains largely unknown. Using a parental/F1 design in which four inbred strains were crossed to a common inbred strain, we assessed the genetic basis and inheritance of gene expression variation in T. urticae. Mirroring known phenotypic variation in the progenitor strains of the inbreds, we confirmed that the inbred strains we created were genetically distinct, varied markedly in pesticide resistance, and also captured variation in host plant fitness commonly observed in this species. By examining differences in gene expression between parents and allele-specific expression in F1s, we found that variation in RNA abundance was more often explained in trans as compared to cis, with the former associated with dominance in inheritance. Strikingly, in a gene ontology analysis, detoxification genes of the cytochrome P450 monooxygenase (CYP) family, as well as dioxygenases (DOGs) acquired from horizontal gene transfer from fungi, were specifically enriched at the extremes of trans-driven up- and downregulation. In particular, a clade of CYPs with documented broad substrate-specificity including multiple pesticides, as well as DOGs that have recently been shown to have broad substrate specificity against plant specialized compounds, were exceptionally highly upregulated as a result of trans effects (or in some cases synergism of cis and trans) in the most multi-pesticide resistant strains. Collectively, our findings highlight the potential importance of trans-driven expression variation in genes associated with xenobiotic metabolism and host plant use for rapid adaptation in T. urticae, and also suggest modular control of these genes, a regulatory architecture that might ameliorate negative pleiotropic effects.

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Section: Resultssupporting

confidence: 53%

Section: Resultsmentioning

confidence: 99%

Section: The Inbred Strains Have Diverse and Contrasting Resistance P...mentioning

confidence: 99%

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Abundant trans-driven variation in detoxification gene expression in the extreme generalist herbivore Tetranychus urticae

Kurlovs

Beer

et al. 2022

Preprint

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“…This indicates the importance of the residue in functioning of the protein, but does not allow to validate its role in resistance. However, resistance in T. urticae may often have a polygenic basis, as was further supported by recent studies, including genetic mapping experiments 34, 46, 47 . The involvement of both mechanisms of decreased exposure and decreased sensitivity may result in synergism 48 .…”

Section: Discussionmentioning

confidence: 78%

“…However, resistance in T. urticae may often have a polygenic basis, as was further supported by recent studies, including genetic mapping experiments. 34,46,47 The involvement of both mechanisms of decreased exposure and decreased sensitivity may result in synergism. 48 This has also been documented for METI-I resistance, where the role of P450-mediated detoxification is indeed very well supported.…”

Section: Discussionmentioning

confidence: 99%

The H92R substitution in PSST is a reliable diagnostic biomarker for predicting resistance to mitochondrial electron transport inhibitors of complex I in European populations of Tetranychus urticae

Xue

Mavridis³

et al. 2022

Pest Management Science

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BACKGROUND: Mitochondrial Electron Transport Inhibitors of complex I (METI-I), such as tebufenpyrad and fenpyroximate, are acaricides that have been used extensively to control Tetranychus urticae Koch (Acari: Tetranychidae) for more than 20 years. Because of the ability of this spider mite to rapidly develop acaricide resistance, field (cross-) resistance monitoring and elucidation of resistance mechanisms are extremely important for resistance management (RM). In the present study, 42 European T. urticae field populations were screened for tebufenpyrad and fenpyroximate resistance, and the correlation between resistance and the H92R substitution in PSST was investigated.RESULTS: According to the calculated lethal concentration values that kill 90% of the population (LC 90 ), tebufenpyrad and fenpyroximate would fail to control many of the collected populations at recommended field rates. Six populations exhibited high to very high resistance levels (200-to over 1950-fold) to both METI-Is. Analysis based on the LC 50 values displayed a clear correlation between tebufenpyrad and fenpyroximate resistance, further supporting cross-resistance, which is of great operational importance in acaricide RM. The previously uncovered METI-I target-site mutation H92R in the PSST homologue of complex I (NADH:ubiquinone oxidoreductase) was found with high allele frequencies in populations resistant to tebufenpyrad and fenpyroximate. Synergist assays showed this mutation is not the only factor involved in METI-I resistance and additive or synergistic effects of multiple mechanisms most likely determine the phenotypic strength.CONCLUSIONS: The predictive value of resistance by H92R is very high in European populations and offers great potential to be used as a molecular diagnostic marker for METI-I resistance.

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

Njiru

Saalwaechter

Mavridis

et al. 2023

Pest Management Science

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BACKGROUNDThe acaricides cyflumetofen, cyenopyrafen and pyflubumide inhibit the mitochondrial electron transport chain at complex II [succinate dehydrogenase (SDH) complex]. A target site mutation H258Y was recently discovered in a resistant strain of the spider mite pest Tetranychus urticae. H258Y causes strong cross‐resistance between cyenopyrafen and pyflubumide, but not cyflumetofen. In fungal pests, fitness costs associated with substitutions at the corresponding H258 position that confer resistance to fungicidal SDH inhibitors have not been uncovered. Here, we used H258 and Y258 near‐isogenic lines of T. urticae to quantify potential pleiotropic fitness effects on mite physiology.RESULTSThe H258Y mutation was not associated with consistent significant changes of single generation life history traits and fertility life table parameters. In contrast, proportional Sanger sequencing and droplet digital polymerase chain reaction showed that the frequency of the resistant Y258 allele decreased when replicated 50:50 Y258:H258 experimentally evolving populations were maintained in an acaricide‐free environment for approximately 12 generations. Using in vitro assays with mitochondrial extracts from resistant (Y258) and susceptible (H258) lines, we identified a significantly reduced SDH activity (48% lower activity) and a slightly enhanced combined complex I and III activity (18% higher activity) in the Y258 lines.CONCLUSIONOur findings suggest that the H258Y mutation is associated with a high fitness cost in the spider mite T. urticae. Importantly, while it is the most common approach, it is clear that only comparing life history traits and life table fecundity does not allow to reliably estimate fitness costs of target site mutations in natural pest populations. © 2023 Society of Chemical Industry.

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QTL mapping suggests that both cytochrome P450-mediated detoxification and target-site resistance are involved in fenbutatin oxide resistance in Tetranychus urticae

Cited by 23 publications

References 113 publications

Abundant trans-driven variation in detoxification gene expression in the extreme generalist herbivore Tetranychus urticae

Abundant trans-driven variation in detoxification gene expression in the extreme generalist herbivore Tetranychus urticae

The H92R substitution in PSST is a reliable diagnostic biomarker for predicting resistance to mitochondrial electron transport inhibitors of complex I in European populations of Tetranychus urticae

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

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