Long-term population studies uncover the genome structure and genetic basis of xenobiotic and host plant adaptation in the herbivoreTetranychus urticae

Abstract

Pesticide resistance arises rapidly in arthropod herbivores, as can host plant adaptation, and both are significant problems in agriculture. These traits have been challenging to study as both are often polygenic and many arthropods are genetically intractable. Here, we examined the genetic architecture of pesticide resistance and host plant adaptation in the two-spotted spider mite, Tetranychus urticae, a global agricultural pest. We show that the short generation time and high fecundity of T. urticae can be readily exploited in experimental evolution designs for high-resolution mapping of quantitative traits. As revealed by selection with spirodiclofen, an acetyl-CoA decarboxylase inhibitor, in populations from a cross between a spirodiclofen resistant and a susceptible strain, and which also differed in performance on tomato, we found that a limited number of loci could explain quantitative resistance to this compound. These were resolved to narrow genomic intervals, suggesting specific candidate genes, including acetyl-CoA decarboxylase itself, clustered and copy variable cytochrome P450 genes, and NADPH cytochrome P450 reductase, which encodes a redox partner for cytochrome P450s. For performance on tomato, candidate genomic regions for response to selection were distinct from those responding to the synthetic compound and were consistent with a more polygenic architecture. In accomplishing this work, we exploited the continuous nature of allele frequency changes across experimental populations to resolve the existing fragmented T.urticae draft genome to pseudochromosomes. This improved assembly was indispensable for our analyses, as it will be for future research with this model herbivore that is exceptionally amenable to genetic studies.

Overexpression of an alternative allele of carboxyl/choline esterase 4 (CCE04) of Tetranychus urticae is associated with high levels of resistance to the keto‐enol acaricide spirodiclofen

“…None of the QTLs was associated with the CCE04 locus (located on pseudochromosome 1 at 2.39 Mb), but contained other interesting candidate genes: ACCase -the target of keto-enol acaricides (on pseudochromosome 1 at 6.56 Mb), a region containing P450s (on pseudochromosome 1 at 24.13 Mb) belonging to the same P450 subfamily as CYP392E10, known to metabolize spirodiclofen 11 and cytochrome P450 reductase (CPR) (on pseudochromosome 2 at 5.69 Mb). 12 On the other hand, it is still possible that these genomic loci harbor regulators (e.g. transcription factors) that are associated with the potentially fixed CCE04 SR-VP allele.…”

Resistance risk assessment of the novel complex II inhibitor pyflubumide in the polyphagous pest Tetranychus urticae

“…The application of acaricides still remains the most frequently used method to keep T. urticae populations below economic thresholds for many crops. However, the fast development of resistance in the species, in part due to biological characteristics such as a short life cycle, high reproductive potential, arrhenotokous reproduction, together with a broad host plant range, reduces the efficacy of the application of acaricides (Dermauw et al 2013;Van Leeuwen et al 2010;Wybouw et al 2019). It is therefore important to continue to develop acaricides with new modes of action and limited cross-resistance to other commercially available compounds to secure proper resistance management in T. urticae (Nauen et al 2012;Van Leeuwen, Thomas et al 2015;Fotoukkiaii et al 2019).…”

Metabolic mechanisms of resistance to spirodiclofen and spiromesifen in Iranian populations of Panonychus ulmi

“…For spider mites, it has been shown that detoxification enzymes such as cytochrome P450 monooxygenases (P450s) are involved in spirodiclofen resistance, while carboxyl/choline esterases (CCEs) are much likely involved in sequestration of spirodiclofen (Demaeght et al, 2013;Kramer & Nauen, 2011;Wei et al, 2019, Bajda et al 2015. In a recent study, spirodiclofen resistance in T. urticae was also mapped to a number of genomic loci (Quantitative Trait Loci (QTL) mapping), with one of the QTLs containing the gene encoding ACCase, the target-site of spirodiclofen (Wybouw et al, 2019). In the ACCase gene of the resistant strain that was used for the mapping experiment, a non-synonymous mutation, A1079T, was also identified.…”

“…In the ACCase gene of the resistant strain that was used for the mapping experiment, a non-synonymous mutation, A1079T, was also identified. This mutation, however, was located outside the CTdomain of ACCase and awaits functional validation (Khajehali, 2010;Wybouw et al, 2019).…”