Neofunctionalization of Duplicated P450 Genes Drives the Evolution of Insecticide Resistance in the Brown Planthopper

A - Papers appearing in refereed journals

Zimmer, C. T., Garrood, W. T., Singh, K. S., Randall, E., Lueke, B., Gutbrod, O., Matthiesen, S., Kohler, M., Nauen, R., Davies, T. G. E. and Bass, C. 2018. Neofunctionalization of Duplicated P450 Genes Drives the Evolution of Insecticide Resistance in the Brown Planthopper. Current Biology. 28 (2), pp. 268-274.

AuthorsZimmer, C. T., Garrood, W. T., Singh, K. S., Randall, E., Lueke, B., Gutbrod, O., Matthiesen, S., Kohler, M., Nauen, R., Davies, T. G. E. and Bass, C.
Abstract

Gene duplication is a major source of genetic variation that has been shown to underpin the evolution of a wide range of adaptive traits. For example, duplication or amplification of genes encoding detoxification enzymes has been shown to play an important role in the evolution of insecticide resistance. In this context, gene duplication performs an adaptive function as a result of its effects on gene dosage and not as a source of functional novelty. Here, we show that duplication and neofunctionalization of a cytochrome P450, CYP6ER1, led to the evolution of insecticide resistance in the brown planthopper. Considerable genetic variation was observed in the coding sequence of CYP6ER1 in populations of brown planthopper collected from across Asia, but just two sequence variants are highly overexpressed in resistant strains and metabolize imidacloprid. Both variants are characterized by profound amino-acid alterations in substrate recognition sites, and the introduction of these mutations into a susceptible P450 sequence is sufficient to confer resistance. CYP6ER1 is duplicated in resistant strains with individuals carrying paralogs with and without the gain-of-function mutations. Despite numerical parity in the genome, the susceptible and mutant copies exhibit marked asymmetry in their expression with the resistant paralogs overexpressed. In the primary resistance-conferring CYP6ER1 variant, this results from an extended region of novel sequence upstream of the gene that provides enhanced expression. Our findings illustrate the versatility of gene duplication in providing opportunities for functional and regulatory innovation during the evolution of an adaptive trait.

Year of Publication2018
JournalCurrent Biology
Journal citation28 (2), pp. 268-274
Digital Object Identifier (DOI)doi:10.1016/j.cub.2017.11.060
PubMed ID29337073
Open accessPublished as ‘gold’ (paid) open access
FunderEuropean Research Council
Biotechnology and Biological Sciences Research Council
Bayer Crop Science
Funder project or codeEuropean Union’s Horizon 2020 research and innovation programme
A genomic approach to understanding insecticide resistance in crop pests
Bayer Crop Science studentship S2088
Publisher's version
Copyright license
CC BY
Output statusPublished
Publication dates
Online22 Jan 2018
Publication process dates
Accepted23 Nov 2017
PublisherCell Press
ISSN0960-9822

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