Insecticide resistance reduces the profitability of insect-resistant rice cultivars

Rui Pang; Shihui Li; Weiwen Chen; Longyu Yuan; Hanxiang Xiao; Ke Xing; Yanfang Li; Zhenfei Zhang; Xionglei He; Wenqing Zhang

doi:10.1016/j.jare.2023.07.009

Insecticide resistance reduces the profitability of insect-resistant rice cultivars

J Adv Res. 2023 Jul 25:S2090-1232(23)00202-3. doi: 10.1016/j.jare.2023.07.009. Online ahead of print.

Authors

Rui Pang¹, Shihui Li², Weiwen Chen², Longyu Yuan³, Hanxiang Xiao⁴, Ke Xing², Yanfang Li⁴, Zhenfei Zhang⁴, Xionglei He², Wenqing Zhang⁵

Affiliations

¹ State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, Guangdong, China; National Key Laboratory of Green Pesticide, College of Plant Protection, South China Agricultural University, Guangzhou, Guangdong, China.
² State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, Guangdong, China.
³ State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, Guangdong, China; Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, Guangdong, China.
⁴ Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, Guangdong, China.
⁵ State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, Guangdong, China. Electronic address: lsszwq@mail.sysu.edu.cn.

PMID: 37499938
DOI: 10.1016/j.jare.2023.07.009

Abstract

Introduction: Preventing crop yield loss caused by pests is critical for global agricultural production. Agricultural pest control has largely relied on chemical pesticides. The interaction between insecticide resistance and the adaptation of herbivorous pests to host plants may represent an emerging threat to future food security.

Objectives: This study aims to unveil genetic evidence for the reduction in the profitability of resistant cultivars derived from insecticide resistance in target pest insects.

Methods: An experimental evolution system encompassing resistant rice and its major monophagous pest, the brown planthopper Nilaparvata lugens, was constructed. Whole genome resequencing and selective sweep analysis were utilized to identify the candidate gene loci related to the adaptation. RNA interference and induced expression assay were conducted to validate the function of the candidate loci.

Results: We found that the imidacloprid-resistant population of N. lugens rapidly adapted to resistant rice IR36. Gene loci related to imidacloprid resistance may contribute to this phenomenon. Multiple alleles in the nicotinic acetylcholine receptor (nAChR)-7-like and P450 CYP4C61 were significantly correlated with changes in virulence to IR36 rice and insecticide resistance of N. lugens. One avirulent/susceptible genotype and two virulent/resistant genotypes could be inferred from the corresponding alleles. Importantly, we found that the virulent/resistant genotypes already exist in the wild in China, exhibiting increasing frequencies along with insecticide usage. We validated the relevance of these genotypes and the virulence to three more resistant rice cultivars. Knockdown of the above two genes in N. lugens significantly decreased both the resistance to imidacloprid and the virulence towards resistant rice.

Conclusion: Our findings provide direct genetic evidence to the eco-evolutionary consequence of insecticide resistance, and suggest an urgent need for the implementation of predictably sustainable pest management.

Keywords: Evolution; Insect-resistant rice; Insecticide resistance; Interaction; Population genetic structure.