Cuticular competing endogenous RNAs regulate insecticide penetration and resistance in a major agricultural pest

BMC Biology

Research Article

John Vontas¹  Meng-Ling Chen²  Wen-Jie Bai²  Yu Peng²  Zhen-Yu Li²  Li-Sha Zheng²  Li-Wei Meng³  Guo-Rui Yuan³  Jin-Jun Wang³  Wei Dou³ 

[1] Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, 70013, Heraklion, Greece;Pesticide Science Laboratory, Department of Crop Science, Agricultural University of Athens, 11855, Athens, Greece;Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, 400716, Chongqing, China;Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, 400716, Chongqing, China;Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Academy of Agricultural Sciences, Southwest University, 400715, Chongqing, China;

关键词: microRNA;    Cuticular protein;    Long noncoding RNA;    Insecticide resistance;    Insect integument;   

DOI  :  10.1186/s12915-023-01694-z

 received in 2023-03-18, accepted in 2023-08-29,  发布年份 2023

来源: Springer

【 摘 要 】

BackgroundThe continuously developing pesticide resistance is a great threat to agriculture and human health. Understanding the mechanisms of insecticide resistance is a key step in dealing with the phenomenon. Insect cuticle is recently documented to delay xenobiotic penetration which breaks the previous stereotype that cuticle is useless in insecticide resistance, while the underlying mechanism remains scarce.ResultsHere, we find the integument contributes over 40.0% to insecticide resistance via different insecticide delivery strategies in oriental fruit fly. A negative relationship exists between cuticle thickening and insecticide penetration in resistant/susceptible, also in field strains of oriental fruit fly which is a reason for integument-mediated resistance. Our investigations uncover a regulator of insecticide penetration that miR-994 mimic treatment causes cuticle thinning and increases susceptibility to malathion, whereas miR-994 inhibitor results in opposite phenotypes. The target of miR-994 is a most abundant cuticle protein (CPCFC) in resistant/susceptible integument expression profile, which possesses capability of chitin-binding and influences the cuticle thickness-mediated insecticide penetration. Our analyses find an upstream transcriptional regulatory signal of miR-994 cascade, long noncoding RNA (lnc19419), that indirectly upregulates CPCFC in cuticle of the resistant strain by sponging miR-994. Thus, we elucidate the mechanism of cuticular competing endogenous RNAs for regulating insecticide penetration and demonstrate it also exists in field strain of oriental fruit fly.ConclusionsWe unveil a regulatory axis of lnc19419 ~ miR-994 ~ CPCFC on the cuticle thickness that leads to insecticide penetration resistance. These findings indicate that competing endogenous RNAs regulate insecticide resistance by modulating the cuticle thickness and provide insight into the resistance mechanism in insects.

【 授权许可】

CC BY   
© BioMed Central Ltd., part of Springer Nature 2023

【 图 表 】

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