Cuticle protein mediates the evolution of stress resistance by generating a decoy circular RNA in spider mite
Kaiyang Feng, Mingyu Zhao, Zhixin Jiang, Sihan Chen, Ya Yang, Qingying Chen, Xiang Wen, Lin Xu, Yuhan Yang, Zhifeng Xu, Jinzhi Niu, Wei Dou, Lin He
Abstract
Phytophagous mites, including Tetranychus cinnabarinus , are arthropods known for their wide infestation of host plants and pesticide resistance. We found that fenpropathrin-resistant female mites (YN-FeR, with target resistance: F1538I kdr mutation) exhibited significantly enhanced adaptability to various stress conditions, including exposure to different acaricides and high-temperature (34°C) and low-humidity environments (40% relative humidity). This evolution was attributed to cuticle thickening in resistant female mites. Cuticle protein CPR25 was identified as a critical gene mediating cuticle thickening. CPR25 regulated its own overexpression by producing a circular RNA, named circCPR25 , which acted as a decoy to selectively sequester and bind to the miR-34~317 cluster. This study revealed a distinctive mechanism underlying the evolution of stress resistance in spider mites. Specifically, a cuticle protein in spider mites regulates its own overexpression by producing a decoy circRNA, thereby promoting cuticle thickening and facilitating rapid adaptation to adverse conditions.