Genome-wide identification and functional analysis of long non-coding RNAs in Chilo suppressalis reveal their potential roles in chlorantraniliprole resistance

Shuijin Huang; Dong Jing; Lu Xu; Guanghua Luo; Yanyue Hu; Ting Wu; Yao Hu; Fei Li; Kang He; Wenjing Qin; Yang Sun; Hui Liu

doi:10.3389/fphys.2022.1091232

Genome-wide identification and functional analysis of long non-coding RNAs in Chilo suppressalis reveal their potential roles in chlorantraniliprole resistance

Front Physiol. 2023 Jan 9:13:1091232. doi: 10.3389/fphys.2022.1091232. eCollection 2022.

Authors

Shuijin Huang¹, Dong Jing², Lu Xu³, Guanghua Luo³, Yanyue Hu¹, Ting Wu¹, Yao Hu⁴, Fei Li², Kang He², Wenjing Qin⁵, Yang Sun¹, Hui Liu⁶

Affiliations

¹ Institute of Plant Protection, Jiangxi Academy of Agricultural Sciences, Nanchang, China.
² Institute of Insect Sciences/Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.
³ Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Food and Safety-State Key Laboratory Cultivation Base of Ministry of Science and Technology, Nanjing, China.
⁴ Institute of Animal Husbandry and Veterinary Medicine, Jiangxi Academy of Agricultural Sciences, Nanchang City, China.
⁵ Institute of Soil Fertilizer and Environmental Resource, Jiangxi Academy of Agricultural Sciences, Nanchang, China.
⁶ Institute of Red Soil and Germplasm Resources in Jiangxi, Nanchang, China.

Abstract

Long non-coding RNAs, referred to as lncRNAs, perform essential functions in some biological processes, including reproduction, metamorphosis, and other critical life functions. Yet, lncRNAs are poorly understood in pesticide resistance, and no reports to date have characterized which lncRNAs are associated with chlorantraniliprole resistance in Chilo suppressalis. Here, RNA-seq was performed on two strains of C. suppressalis exposed to chlorantraniliprole: one is a susceptible strain (S), and the other is a resistant strain (R). In total, 3,470 lncRNAs were identified from 40,573 merged transcripts in six libraries, including 1,879 lincRNAs, 245 intronic lncRNAs, 853 sense lncRNAs, and 493 antisense lncRNAs. Moreover, differential expression analysis revealed 297 and 335 lncRNAs upregulated in S and R strains, respectively. Differentially expressed (DE) lncRNAs are usually assumed to be involved in the chlorantraniliprole resistance in C. suppressalis. As potential targets, adjacent protein-coding genes (within <1000 kb range upstream or downstream of DE lncRNAs), especially detoxification enzyme genes (cytochrome P450s, carboxyl/cholinesterases/esterases, and ATP-binding cassette transporter), were analyzed. Furthermore, the strand-specific RT-PCR was conducted to confirm the transcript orientation of randomly selected 20 DE lincRNAs, and qRT-PCR was carried out to verify the expression status of 8 out of them. MSTRG.25315.3, MSTRG.25315.6, and MSTRG.7482.1 were upregulated in the R strain. Lastly, RNA interference and bioassay analyses indicated overexpressed lincRNA MSTRG.7482.1 was involved in chlorantraniliprole resistance. In conclusion, we represent, for the first time, the genome-wide identification of chlorantraniliprole-resistance-related lncRNAs in C. suppressalis. It elaborates the views underlying the mechanism conferring chlorantraniliprole resistance in lncRNAs.

Keywords: Chilo suppressalis; adjacent protein-coding genes; chlorantraniliprole resistance; genome-wide identification; long non-coding RNAs.

Grants and funding

This study was financed by the National Natural Science Foundation of China (NSFC) (31860501 and 31972309) and the Natural Science Foundation of Zhejiang Province (LY22C140005), with additional finance provided by the Earmarked Fund for China Agriculture Research System (CARS-01-40) and the Jiangxi postdoctoral scientific research project (2019RC16 and 2020KY22).