High-resolution QTL mapping in Tetranychus urticae reveals acaricide-specific responses and common target-site resistance after selection by different METI-I acaricides

Abstract

Arthropod herbivores cause dramatic crop losses, and frequent pesticide use has led to widespread resistance in numerous species. One such species, the two-spotted spider mite, Tetranychus urticae, is an extreme generalist herbivore and a major worldwide crop pest with a history of rapidly developing resistance to acaricides. Mitochondrial Electron Transport Inhibitors of complex I (METI-Is) have been used extensively in the last 25 years to control T. urticae around the globe, and widespread resistance to each has been documented. METI-I resistance mechanisms in T. urticae are likely complex, as increased metabolism by cytochrome P450 monooxygenases as well as a target-site mutation have been linked with resistance. To identify loci underlying resistance to the METI-I acaricides fenpyroximate, pyridaben and tebufenpyrad without prior hypotheses, we crossed a highly METI-I-resistant strain of T. urticae to a susceptible one, propagated many replicated populations over multiple generations with and without selection by each compound, and performed bulked segregant analysis genetic mapping. Our results showed that while the known H92R target-site mutation was associated with resistance to each compound, a genomic region that included cytochrome P450-reductase (CPR) was associated with resistance to pyridaben and tebufenpyrad. Within CPR, a single nonsynonymous variant distinguished the resistant strain from the sensitive one. Furthermore, a genomic region linked with tebufenpyrad resistance harbored a noncanonical member of the nuclear hormone receptor 96 (NHR96) gene family. This NHR96 gene does not encode a DNA-binding domain (DBD), an uncommon feature in arthropods, and belongs to an expanded family of 47 NHR96 proteins lacking DBDs in T. urticae. Our findings suggest that although cross-resistance to METI-Is involves known detoxification pathways, structural differences in METI-I acaricides have also resulted in resistance mechanisms that are compound-specific.

Identification and characterization of striking multiple‐insecticide resistance in a Tetranychus urticae field population from Greece

“…Target‐site mutations associated with acaricide resistance in T. urticae have been discovered in genes encoding: (a) acetylcholinesterase ( AChE ), which is associated with resistance to organophosphates and carbamates; 32 (b) voltage‐gated sodium channel ( vgsc ), which confers resistance to pyrethroids; 16,27,29 (c) glutamate‐gated chloride channels ( GluCl1/3 ), which are linked with resistance to abamectin; 30,31 (d) cytochrome b ( cytb ), which is associated with bifenazate and acequinocyl resistance; 26,40 (e) chitin synthase 1 ( chs1 ), which has been linked with high levels of resistance to the mite growth inhibitors (MGIs) etoxazole, clofentezine and hexythiazox; 22,41 (f) PSST subunit ( psst/NDUFS7 ) of mitochondrial respiratory complex I, which has been associated with resistance to pyridaben, tebufenpyrad and fenpyroximate; 9,42 and (g) succinate dehydrogenase subunits B and C ( SdhB and SdhC , respectively) conferring resistance to several complex II inhibitors 43 …”

Genetic analysis and screening of detoxification-related genes in an amitraz-resistant strain of Panonychus citri

“…Park et al found that ABCC transporters were involved in the resistance of S. exigua to Bt toxins through bulk segregant analysis (Park et al, 2014). To study non-monogenic resistant trait, Snoeck et al applied high-resolution QTL mapping to localize target genes related to the resistance of T. urticae to METI-I acaricides; a PSST homologue, cytochrome P450 reductase, and nuclear hormone receptor 96 were identified (Snoeck et al, 2019). In the future, whole genome resequencing for P. citri will be performed to localize resistant genes response to amitraz in mites.…”

High-resolution genetic mapping revealscis-regulatory and copy number variation in loci associated with cytochrome P450-mediated detoxification in a generalist arthropod pest

“…The haplodiploid spider mite Tetranychus urticae is a major global agricultural pest which rapidly develops resistance to pesticides of various modes of action [34]. As revealed by recent studies, T. urticae is highly amenable to BSA genetic mapping, with QTL, including for quantitative pesticide resistance, narrowed to small genomic intervals that have suggested specific candidate genes and causal alleles [29,33]. In some instances, known causal variants were recovered [35–38], confirming the validity of the narrow genomic intervals identified by BSA studies using large, highly replicated T. urticae experimental populations [25].…”