P450 gene duplication and divergence led to the evolution of dual novel functions and insecticide cross-resistance in the brown planthopper Nilaparvata lugens

A - Papers appearing in refereed journals

Duarte, A., Pym, A., Garrood, W. T., Troczka, B. J., Zimmer, C. T., Davies, T. G. E., Nauen, R., O'Reilly, O. A. and Bass, C. G. 2022. P450 gene duplication and divergence led to the evolution of dual novel functions and insecticide cross-resistance in the brown planthopper Nilaparvata lugens. PLOS Genetics. 18 (6), p. e1010279. https://doi.org/10.1371/journal.pgen.1010279

AuthorsDuarte, A., Pym, A., Garrood, W. T., Troczka, B. J., Zimmer, C. T., Davies, T. G. E., Nauen, R., O'Reilly, O. A. and Bass, C. G.
Abstract

The sustainable control of many highly damaging insect crop pests and disease vectors is threatened by the evolution of insecticide resistance. As a consequence, strategies have been developed that aim to prevent or delay resistance development by rotating or mixing insecticides with different modes of action (MoA). However, these approaches can be compromised by the emergence of mechanisms that confer cross-resistance to insecticides with different MoA. Despite the applied importance of cross-resistance, its evolutionary underpinnings remain poorly understood. Here we reveal how a single gene evolved the capacity to detoxify two structurally unrelated insecticides with different MoA. Using transgenic approaches we demonstrate that a specific variant of the cytochrome P450 CYP6ER1, previously shown to confer resistance to the neonicotinoid imidacloprid in the brown planthopper, N. lugens, also confers cross-resistance to the phenylpyrazole ethiprole. CYP6ER1 is duplicated in resistant strains, and we show that while the acquisition of mutations in two encoded substrate recognition sites (SRS) of one of the parologs led to resistance to imidacloprid, a different set of mutations, outside of known SRS, are primarily responsible for resistance to ethiprole. Epistatic interactions between these mutations and their genetic background suggest that the evolution of dual resistance from the same gene copy involved functional trade-offs in respect to CYP6ER1 catalytic activity for ethiprole versus imidacloprid. Surprisingly, the mutations leading to ethiprole and imidacloprid resistance do not confer the ability to detoxify the insecticide fipronil, another phenylpyrazole with close structural similarity to ethiprole. Taken together, these findings reveal how gene duplication and divergence can lead to the evolution of multiple novel functions from a single gene. From an applied perspective they also demonstrate how cross-resistance to structurally unrelated insecticides can evolve, and illustrate the difficulty in predicting cross-resistance profiles mediated by metabolic mechanisms.

Year of Publication2022
JournalPLOS Genetics
Journal citation18 (6), p. e1010279
Digital Object Identifier (DOI)https://doi.org/10.1371/journal.pgen.1010279
PubMed ID35727851
PubMed Central ID9249207
Web address (URL)https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1010279
Open accessPublished as ‘gold’ (paid) open access
FunderEuropean Research Council
Funder project or codeEuropean Union’s Horizon 2020 research and innovation programme
Publisher's version
Copyright license
CC BY 4.0
Output statusPublished
Publication dates
Online21 Jun 2022
Publication process dates
Accepted01 Jun 2022
PublisherPublic Library of Science (PLOS)
ISSN1553-7404

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