Peroxiredoxin alleviates the fitness costs of imidacloprid resistance in an insect pest of rice

Rui Pang,Xiangzhao Yue,Wenqing Zhang,Xianchun Li,Longyu Yuan,Ke Xing,Meng Chen,Xionglei He,Yan Ling,Zhikun Liang,Yi Dong,Nora J Besansky

doi:10.1371/journal.pbio.3001190

Abstract

Chemical insecticides have been heavily employed as the most effective measure for control of agricultural and medical pests, but evolution of resistance by pests threatens the sustainability of this approach. Resistance-conferring mutations sometimes impose fitness costs, which may drive subsequent evolution of compensatory modifier mutations alleviating the costs of resistance. However, how modifier mutations evolve and function to overcome the fitness cost of resistance still remains unknown. Here we show that overexpression of P450s not only confers imidacloprid resistance in the brown planthopper, Nilaparvata lugens, the most voracious pest of rice, but also leads to elevated production of reactive oxygen species (ROS) through metabolism of imidacloprid and host plant compounds. The inevitable production of ROS incurs a fitness cost to the pest, which drives the increase or fixation of the compensatory modifier allele T65549 within the promoter region of N. lugens peroxiredoxin (NlPrx) in the pest populations. T65549 allele in turn upregulates the expression of NlPrx and thus increases resistant individuals’ ability to clear the cost-incurring ROS of any source. The frequent involvement of P450s in insecticide resistance and their capacity to produce ROS while metabolizing their substrates suggest that peroxiredoxin or other ROS-scavenging genes may be among the common modifier genes for alleviating the fitness cost of insecticide resistance.

Highlights

Arthropod pests pose a serious threat to both agriculture and human health through ingestion of agricultural produce and transmission of plant, livestock, and human pathogens
The dead nymphs of both batches were considered the GX-P-LR individuals, but the 2 replicates of 30 each used for subsequent genome resequencing were randomly selected from the nymphs that died on day 2 and 3 after exposure to imidacloprid (S2 Table)
Further analyses of Tajima’s D statistics and of Gene Ontology (GO) functional categories (S5 Table) of the 69 candidate genes between GX-P-HR and GX-P-LR identified N. lugens peroxiredoxin (NlPrx) as the most likely fitness modifier gene candidate of imidacloprid resistance in N. lugens. This agrees with the function of peroxiredoxins to scavenge reactive oxygen species (ROS), which can be elicited by exposure to many insecticides and plant defense allelochemicals [61,54,55,56,66,67,68] and can reduce the fitness of insects [57,58]

Summary

Introduction

Arthropod pests pose a serious threat to both agriculture and human health through ingestion of agricultural produce and transmission of plant, livestock, and human pathogens. These deadly pests cause approximately 20% of crop yield loss annually despite the current crop protection practice [1], and are responsible for more than 17% of infectious diseases

Methods

Results

Conclusion