Key role of the ryanodine receptor I4790K mutation in mediating diamide resistance in Plutella xylostella

A - Papers appearing in refereed journals

Jiang, D., Yu, Z., He, Y., Wang, F., Gu, Y., Davies, T. G. E., Fan, Z., Wang, X. and Wu, Y. 2024. Key role of the ryanodine receptor I4790K mutation in mediating diamide resistance in Plutella xylostella. Insect Biochemistry and Molecular Biology. 168 (May), p. 104107. https://doi.org/10.1016/j.ibmb.2024.104107

AuthorsJiang, D., Yu, Z., He, Y., Wang, F., Gu, Y., Davies, T. G. E., Fan, Z., Wang, X. and Wu, Y.
Abstract

The diamondback moth Plutella xylostella, a global insect pest of cruciferous vegetables, has evolved resistance to many classes of insecticides including diamides. Three point mutations (I4790M, I4790K, and G4946E) in the ryanodine receptor of P. xylostella (PxRyR) have been identified to associate with varying levels of resistance. In this study, we generated a knockin strain (I4790K-KI) of P. xylostella, using CRISPR/Cas9 to introduce the I4790K mutation into PxRyR of the susceptible IPP-S strain. Compared to IPP-S, the edited I4790K-KI strain exhibited high levels of resistance to both anthranilic diamides (chlorantraniliprole 1857-fold, cyantraniliprole 1433-fold) and the phthalic acid diamide flubendiamide (>2272-fold). Resistance to chlorantraniliprole in the I4790K-KI strain was inherited in an autosomal and recessive mode, and genetically linked with the I4790K knockin mutation. Computational modelling suggests the I4790K mutation reduces the binding of diamides to PxRyR by disrupting key hydrogen bonding interactions within the binding cavity. The approximate frequencies of the 4790M, 4790K, and 4946E alleles were assessed in ten geographical field populations of P. xylostella collected in China in 2021. The levels of chlorantraniliprole resistance (2.3- to 1444-fold) in these populations were significantly correlated with the frequencies (0.017 to 0.917) of the 4790K allele, but not with either 4790M (0 to 0.183) or 4946E (0.017 to 0.450) alleles. This demonstrates that the PxRyR I4790K mutation is currently the major contributing factor to chlorantraniliprole resistance in P. xylostella field populations within China. Our findings provide in vivo functional evidence for the causality of the I4790K mutation in PxRyR with high levels of diamide resistance in P. xylostella, and suggest that tracking the frequency of the I4790K allele is crucial for optimizing the monitoring and management of diamide resistance in this crop pest.

KeywordsDiamondback moth; Diamides; CRISPR/Cas9; Ryanodine receptor; I4790K
Year of Publication2024
JournalInsect Biochemistry and Molecular Biology
Journal citation168 (May), p. 104107
Digital Object Identifier (DOI)https://doi.org/10.1016/j.ibmb.2024.104107
Web address (URL)https://www.sciencedirect.com/science/article/abs/pii/S0965174824000389
Open accessPublished as non-open access
FunderNational Key Research and Development Program of China
Biotechnology and Biological Sciences Research Council
Funder project or codeGrowing Health (WP1) - bio-inspired solutions for healthier agroecosystems: Understanding biointeractions
Output statusPublished
Publication dates
Online14 Mar 2024
Publication process dates
Accepted13 Mar 2024
PublisherElsevier
ISSN0965-1748

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