A mutation in the PSST homologue of complex I (NADH:ubiquinone oxidoreductase) from Tetranychus urticae is associated with resistance to METI acaricides

Bajda, Sabina; Dermauw, Wannes; Panteleri, Rafaela; Sugimoto, Naoya; Douris, Vassilis; Tirry, Luc; Osakabe, Masahiro; Vontas, John; Leeuwen, Thomas Van

doi:10.1016/j.ibmb.2016.11.010

Cited by 96 publications

(149 citation statements)

References 88 publications

Supporting

Mentioning

140

Contrasting

Order By: Relevance

“…S3A) (35). This localization was corroborated by a recent genetic study (48), which demonstrated that a mutation (H92R) in the PSST homolog in phytophagous mite (Tetranychus urticae), corresponding to His-61 in bovine PSST, is associated with significant resistance to fenpyroximate. The labeled area faces a part of the "top" of the channel, whereas the presumed location of fenpyroximate is not inside the channel.…”

Section: Physiological Relevance Of the Quinone/inhibitor-access Chansupporting

confidence: 57%

Exploring the quinone/inhibitor-binding pocket in mitochondrial respiratory complex I by chemical biology approaches

Uno¹,

Kimura²,

Murai

et al. 2019

Journal of Biological Chemistry

View full text Add to dashboard Cite

Edited by Ruma Banerjee NADH-quinone oxidoreductase (respiratory complex I) couples NADH-to-quinone electron transfer to the translocation of protons across the membrane. Even though the architecture of the quinone-access channel in the enzyme has been modeled by X-ray crystallography and cryo-EM, conflicting findings raise the question whether the models fully reflect physiologically relevant states present throughout the catalytic cycle. To gain further insights into the structural features of the binding pocket for quinone/inhibitor, we performed chemical biology experiments using bovine heart sub-mitochondrial particles. We synthesized ubiquinones that are oversized (SF-UQs) or lipid-like (PC-UQs) and are highly unlikely to enter and transit the predicted narrow channel. We found that SF-UQs and PC-UQs can be catalytically reduced by complex I, albeit only at moderate or low rates. Moreover, quinone-site inhibitors completely blocked the catalytic reduction and the membrane potential formation coupled to this reduction. Photoaffinity-labeling experiments revealed that amiloride-type inhibitors bind to the interfacial domain of multiple core subunits (49 kDa, ND1, and PSST) and the 39-kDa supernumerary subunit, although the latter does not make up the channel cavity in the current models. The binding of amilorides to the multiple target subunits was remarkably suppressed by other quinone-site inhibitors and SF-UQs. Taken together, the present results are difficult to reconcile with the current channel models. On the basis of comprehensive interpretations of the present results and of previous findings, we discuss the physiological relevance of these models. Figure 2. Structures of photoreactive amilorides synthesized in this study. PRA1 and PRA2 used in our previous work (17) are also shown. A photolabile azido group attached to each compound is indicated by a gray circle. The concentration in parentheses is the average IC 50 value, which is the molar concentration (nanomolar) needed to reduce the control NADH oxidase activity in bovine heart SMPs (30 g of proteins/ml) by 50%. As a reference, the IC 50 value of bullatacin was 1.1 (Ϯ 0.09) nM under the same experimental conditions. Quinone/inhibitor-binding pocket in respiratory complex I

show abstract

Section: Physiological Relevance Of the Quinone/inhibitor-access Chansupporting

confidence: 57%

Exploring the quinone/inhibitor-binding pocket in mitochondrial respiratory complex I by chemical biology approaches

Uno¹,

Kimura²,

Murai

et al. 2019

Journal of Biological Chemistry

View full text Add to dashboard Cite

show abstract

“…The near‐isogenic lines were generated in a previous study using a marker‐assisted backcrossing technique (Bajda et al., 2017; Riga et al., 2017). Briefly, these were lines that carry introgressed nucleus‐encoded nonsynonymous mutations in CHS1 gene (CHS1_R1‐R3), VGSC gene (VGSC_R2 and R3), GluCl genes (GluCl1+3_R1‐3) and their congenic susceptible controls (CHS1_C, VGSC_C1 and GluCl1+3_C, respectively) as well as lines carrying an introgressed mitochondrial‐encoded mutation in cytb gene (cytb_R1‐R3).…”

Section: Methodsmentioning

confidence: 99%

“…An elegant solution to overcome this experimental limitation is to backcross the target‐site mutation of interest into a susceptible genomic background over multiple generations, hereby generating near‐isogenic lines. This procedure maximizes the chance that the observed difference in population growth is caused by the target‐site mutation under investigation (Bajda et al., 2017; Brito et al., 2013; Riga et al., 2017). Unfortunately, the biological characteristics of many insect and mite pests render the generation of near‐isogenic lines extremely difficult and time‐consuming.…”

Section: Introductionmentioning

confidence: 99%

Fitness costs of key point mutations that underlie acaricide target‐site resistance in the two‐spotted spider miteTetranychus urticae

Bajda

Riga

Wybouw

et al. 2018

Evolutionary Applications

Self Cite

View full text Add to dashboard Cite

The frequency of insecticide/acaricide target‐site resistance is increasing in arthropod pest populations and is typically underpinned by single point mutations that affect the binding strength between the insecticide/acaricide and its target‐site. Theory predicts that although resistance mutations clearly have advantageous effects under the selection pressure of the insecticide/acaricide, they might convey negative pleiotropic effects on other aspects of fitness. If such fitness costs are in place, target‐site resistance is thus likely to disappear in the absence of insecticide/acaricide treatment, a process that would counteract the spread of resistance in agricultural crops. Hence, there is a great need to reliably quantify the various potential pleiotropic effects of target‐site resistance point mutations on arthropod fitness. Here, we used near‐isogenic lines of the spider mite pest Tetranychus urticae that carry well‐characterized acaricide target‐site resistance mutations to quantify potential fitness costs. Specifically, we analyzed P262T in the mitochondrial cytochrome b, the combined G314D and G326E substitutions in the glutamate‐gated chloride channels, L1024V in the voltage‐gated sodium channel, and I1017F in chitin synthase 1. Five fertility life table parameters and nine single‐generation life‐history traits were quantified and compared across a total of 15 mite lines. In addition, we monitored the temporal resistance level dynamics of populations with different starting frequency levels of the chitin synthase resistant allele to further support our findings. Three target‐site resistance mutations, I1017F and the co‐occurring G314D and G326E mutations, were shown to significantly and consistently alter certain fitness parameters in T. urticae. The other two mutations (P262T and L1024V) did not result in any consistent change in a fitness parameter analyzed in our study. Our findings are discussed in the context of the global spread of T. urticae pesticide resistance and integrated pest management.

show abstract

“…Progeny of a single female with the G132A (iso-FS1) and G126S + A133T (iso-FS8) mutations were used to create the isofemale lines. Introgressed lines were established using the backcrossing methods described by Bajda et al 40,41 Briefly, JP-R and iso-FS8 virgin females were crossed with susceptible Wasatch males. A virgin F1 female was backcrossed to Wasatch males, and the backcrossing was repeated seven times.…”

Section: Generation Of Isofemale and Introgressed Linesmentioning

confidence: 99%

Identification and characterization of new mutations in mitochondrial cytochrome b that confer resistance to bifenazate and acequinocyl in the spider miteTetranychus urticae

Fotoukkiaii

Tan

Xue

et al. 2019

Pest Management Science

Self Cite

View full text Add to dashboard Cite

BACKGROUND In spider mites, mutations in the mitochondrial cytochrome b Qo pocket have been reported to confer resistance to the Qo inhibitors bifenazate and acequinocyl. In this study, we surveyed populations of the two‐spotted spider mite Tetranychus urticae for mutations in cytochrome b, linked newly discovered mutations with resistance and assessed potential pleiotropic fitness costs. RESULTS We identified two novel mutations in the Qo site: G132A (equivalent to G143A in fungi resistant to strobilurins) and G126S + A133T (previously reported to cause bifenazate and acequinocyl resistance in Panonychus citri). Two T. urticae strains carrying G132A were highly resistant to bifenazate but not acequinocyl, whereas a strain with G126S + A133T displayed high levels of acequinocyl resistance, but only moderate levels of bifenazate resistance. Bifenazate and acequinocyl resistance were inherited maternally, providing strong evidence for the involvement of these mutations in the resistance phenotype. Near isogenic lines carrying G132A revealed several fitness penalties in T. urticae; a lower net reproductive rate (R0), intrinsic rate of increase (rm) and finite rate of increase (LM); a higher doubling time (DT); and a more male‐biased sex ratio. CONCLUSIONS Several lines of evidence were provided to support the causal role of newly discovered cytochrome b mutations in bifenazate and acequinocyl resistance. Because of the fitness costs associated with the G132A mutation, resistant T. urticae populations might be less competitive in a bifenazate‐free environment, offering opportunities for resistance management. © 2019 Society of Chemical Industry

show abstract

A mutation in the PSST homologue of complex I (NADH:ubiquinone oxidoreductase) from Tetranychus urticae is associated with resistance to METI acaricides

Cited by 96 publications

References 88 publications

Exploring the quinone/inhibitor-binding pocket in mitochondrial respiratory complex I by chemical biology approaches

Exploring the quinone/inhibitor-binding pocket in mitochondrial respiratory complex I by chemical biology approaches

Fitness costs of key point mutations that underlie acaricide target‐site resistance in the two‐spotted spider miteTetranychus urticae

Identification and characterization of new mutations in mitochondrial cytochrome b that confer resistance to bifenazate and acequinocyl in the spider miteTetranychus urticae

Contact Info

Product

Resources

About