Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella

Steinbach, Denise; Gutbrod, Oliver; Lümmen, Peter; Matthiesen, Svend; Schorn, Corinna; Nauen, Ralf

doi:10.1016/j.ibmb.2015.05.001

Cited by 130 publications

(165 citation statements)

References 39 publications

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“…Low but significant resistance levels against diflubenzuron and triflumuron were detected in a P. xylostella strain (Sudlon) recently sampled in a Philippine cabbage field. The strain was maintained under laboratory conditions since 2011 to investigate target-site mutations in ryanodine receptors conferring resistance to diamide insecticides (23,24). BPU insecticides have been used for diamondback moth control in Philippine cabbage in the past and were recently abandoned due to development of resistance.…”

Section: Resultsmentioning

confidence: 99%

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Resistance mutation conserved between insects and mites unravels the benzoylurea insecticide mode of action on chitin biosynthesis

Douris

Steinbach

Panteleri

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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167

166

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Despite the major role of chitin biosynthesis inhibitors such as benzoylureas (BPUs) in the control of pests in agricultural and public health for almost four decades, their molecular mode of action (MoA) has in most cases remained elusive. BPUs interfere with chitin biosynthesis and were thought to interact with sulfonylurea receptors that mediate chitin vesicle transport. Here, we uncover a mutation (I1042M) in the chitin synthase 1 (CHS1) gene of BPU-resistant Plutella xylostella at the same position as the I1017F mutation reported in spider mites that confers etoxazole resistance. Using a genome-editing CRISPR/Cas9 approach coupled with homology-directed repair (HDR) in Drosophila melanogaster, we introduced both substitutions (I1056M/F) in the corresponding fly CHS1 gene (kkv). Homozygous lines bearing either of these mutations were highly resistant to etoxazole and all tested BPUs, as well as buprofezin-an important hemipteran chitin biosynthesis inhibitor. This provides compelling evidence that BPUs, etoxazole, and buprofezin share in fact the same molecular MoA and directly interact with CHS. This finding has immediate effects on resistance management strategies of major agricultural pests but also on mosquito vectors of serious human diseases such as Dengue and Zika, as diflubenzuron, the standard BPU, is one of the few effective larvicides in use. The study elaborates on how genome editing can directly, rapidly, and convincingly elucidate the MoA of bioactive molecules, especially when target sites are complex and hard to reconstitute in vitro

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Section: Resultsmentioning

confidence: 99%

“…Procedures toward the investigation of insecticide MoA and resistance mechanisms typically involve in vitro screening systems (27), electrophysiology (28), direct ligand/receptor-insecticide interactions either in vivo (24) or in silico (29), functional expression of enzymes (30, 31), or genetic mapping linkage analysis (19, 32).…”

Section: Discussionmentioning

confidence: 99%

Resistance mutation conserved between insects and mites unravels the benzoylurea insecticide mode of action on chitin biosynthesis

Douris

Steinbach

Panteleri

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

167

166

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“…Whereas G4946 is highly conserved in all insect 503 species, methionine 4790 -described as a RyR mutation site in diamide resistant P. xylostella 504 -is wildtype in the RyR´s of several other insect species that are highly sensitive to 505 chlorantraniliprole, a fact prompting Steinbach et al, (2015) to speculate that this site 506 determines binding specificity and differences in selectivity profiles between anthranilic and 507 phthalic diamides rather than field-relevant resistance (reviewed in Nauen and Steinbach, 508 2016). Diamide resistance in T. absoluta strain IT-GELA-SD4 is autosomally inherited, and as 509 an incompletely recessive trait (heterozygotes display a near susceptible phenotype), a 510 finding corresponding to the inheritance of diamide resistance mediated by target-site 511 mutations in diamondback moth Steinbach et al, 2015). 512…”

Section: Cloning Sequencing and Characterisation Of The T Absoluta mentioning

confidence: 99%

Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae)

Roditakis¹,

Steinbach

Moritz

et al. 2017

Insect Biochemistry and Molecular Biology

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149

112

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36Insect ryanodine receptors (RyR) are the molecular target-site for the recently introduced 37 diamide insecticides. Diamides are particularly active on Lepidoptera pests, including tomato 38 leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). High levels of diamide resistance were 39 recently described in some European populations of T. absoluta, however, the mechanisms 40 of resistance remained unknown. In this study the molecular basis of diamide resistance was 41

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“…[5][6][7][8] The diamide resistance of P. xylostella has been shown to be incompletely or almost completely recessive. 7,9,10) The amino acid mutation (G4946E) in RyR has been shown to be a major factor related to target-insensitive diamide resistance in P. xylostella. 5,[9][10][11] A method to estimate the proportions of G4946E in P. xylostella populations has been developed using quantitative sequencing (QS).…”

Section: Introductionmentioning

confidence: 99%

“…7,9,10) The amino acid mutation (G4946E) in RyR has been shown to be a major factor related to target-insensitive diamide resistance in P. xylostella. 5,[9][10][11] A method to estimate the proportions of G4946E in P. xylostella populations has been developed using quantitative sequencing (QS). 12) Unlike conventional time-consuming bioassay methods, the QS-based method can estimate the proportion using insects collected in the field in a short time.…”

Section: Introductionmentioning

confidence: 99%

Seasonal proportion change of ryanodine receptor mutation (G4946E) in diamondback moth populations

Itagaki

Sonoda

2017

J. Pestic. Sci.

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This study examined the seasonal proportion change of ryanodine receptor mutation (G4946E) for Plutella xylostella populations using quantitative sequencing. Results showed that the proportions of G4946E generally increased from spring through summer, but then decreased in autumn. Furthermore, the proportions in late autumn were similar to those in early spring of the subsequent year. These results suggest that diamide effectiveness for P. xylostella control in the reference year can be evaluated based on a proportion survey in the prior year.

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Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella

Cited by 130 publications

References 39 publications

Resistance mutation conserved between insects and mites unravels the benzoylurea insecticide mode of action on chitin biosynthesis

Resistance mutation conserved between insects and mites unravels the benzoylurea insecticide mode of action on chitin biosynthesis

Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae)

Seasonal proportion change of ryanodine receptor mutation (G4946E) in diamondback moth populations

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