Cuticle protein mediates the evolution of stress resistance by generating a decoy circular RNA in spider mite

Phytophagous mites, including <i>Tetranychus cinnabarinus</i>, 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 <i>kdr</i> 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 <i>CPR25</i> was identified as a critical gene mediating cuticle thickening. <i>CPR25</i> regulated its own overexpression by producing a circular RNA, named <i>circCPR25</i>, 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.