Risk assessment, fitness cost, cross‐resistance, and mechanism of tetraniliprole resistance in the rice stem borer, Chilo suppressalis

• Published in: Insect science 2024-06, Vol.31 (3), p.835-846
• Main Authors: Sun, Hao, Wang, Shuai, Liu, Chong, Hu, Wen‐Kai, Liu, Jin‐Wei, Zheng, Ling‐Jun, Gao, Meng‐Yue, Guo, Fang‐Rui, Qiao, Song‐Tao, Liu, Jun‐Li, Sun, Bo, Gao, Cong‐Fen, Wu, Shun‐Fan
• Format: Article
• Language: English
• Subjects: Animals; Arthropods; Borers; Chilo suppressalis; CRISPR; cross‐resistance; diamide resistance; Fitness; fitness cost; Genetic Fitness; Heritability; High resistance; Insecticide Resistance - genetics; Insecticides; Insecticides - pharmacology; Larva - drug effects; Larva - genetics; Larva - growth & development; Moths - drug effects; Moths - genetics; Moths - growth & development; Mutation; ortho-Aminobenzoates - pharmacology; Pest control; Pest resistance; Pests; Populations; Reproductive fitness; Rice; Risk Assessment; Ryanodine receptors; RyR target‐site mutations
• ISSN: 1672-9609; 1744-7917; 1744-7917
• DOI: 10.1111/1744-7917.13282

The rice stem borer (RSB), Chilo suppressalis, a notorious rice pest in China, has evolved a high resistance level to commonly used insecticides. Tetraniliprole, a new anthranilic diamide insecticide, effectively controls multiple pests, including RSB. However, the potential resistance risk of RSB to tetraniliprole is still unknown. In this study, the tetraniliprole‐selection (Tet‐R) strain was obtained through 10 continuous generations of selection with tetraniliprole 30% lethal concentration (LC30). The realized heritability (h2) of the Tet‐R strain was 0.387, indicating that resistance of RSB to tetraniliprole developed rapidly under the continuous selection of tetraniliprole. The Tet‐R strain had a high fitness cost (relative fitness = 0.53). We established the susceptibility baseline of RSB to tetraniliprole (lethal concentration at LC50 = 0.727 mg/L) and investigated the resistance level of 6 field populations to tetraniliprole. All tested strains that had resistance to chlorantraniliprole exhibited moderate‐ to high‐level resistance to tetraniliprole (resistance ratio = 27.7−806.8). Detection of ryanodine receptor (RyR) mutations showed that the Y4667C, Y4667D, I4758M, and Y4891F mutations were present in tested RSB field populations. RyR mutations were responsible for the cross‐resistance between tetraniliprole and chlorantraniliprole. Further, the clustered regularly interspaced palindromic repeats (CRISPR) / CRISPR‐associated protein 9‐mediated genome‐modified flies were used to study the contribution of RyR mutations to tetraniliprole resistance. The order of contribution of a single RyR mutation to tetraniliprole resistance was Y4667D > G4915E > Y4667C ≈ I4758M > Y4891F. In addition, the I4758M and Y4667C double mutations conferred higher tetraniliprole resistance than single Y4667C mutations. These results can guide resistance management practices for diamides in RSB and other arthropods. Chilo suppressalis has a high resistance risk to tetraniliprole. Fitness costs of tetraniliprole resistance are present in the tetraniliprole‐selection strain. Tetraniliprole has a high cross‐resistance with chlorantraniliprole in C. suppressalis. RyR target‐site mutations are responsible for the cross‐resistance between tetraniliprole and chlorantraniliprole.