Genome-wide analysis of cuticle protein family genes in rice stem borer Chilo suppressalis: Insights into their role in environmental adaptation and insecticidal stress response

Abstract

Insect cuticle plays a key role in insect survival, adaptation and prosperity by serving as the exoskeleton and the first barrier against environmental stresses. As the major components of insect cuticle, the diverse structural cuticle proteins (CPs) contribute to variation in physical properties and functions of cuticle. However, the roles of CPs in cuticular versatility, especially in the stress response or adaption, remain incompletely understood. In this study, we performed a genome-wide analysis of CP superfamily in the rice-boring pest Chilosuppressalis. A total of 211 CP genes were identified and their encoding proteins were classified into eleven families and three subfamilies (RR1, RR2, and RR3). The comparative genomic analysis of CPs revealed that C. suppressalis had fewer CP genes compared to other lepidopteran species, which largely resulted from a less expansion of his-rich RR2 genes involved in cuticular sclerotization, suggesting long-term boring life of C. suppressalis inside rice hosts might evolutionarily prefer cuticular elasticity rather than cuticular sclerotization. We also investigated the response pattern of all CP genes under insecticidal stresses. >50 % CsCPs were upregulated at least 2-fold under insecticidal stresses. Notably, the majority of the highly upregulated CsCPs formed gene pairs or gene clusters on chromosomes, indicating the rapid response of adjacent CsCPs to insecticidal stress. Most high-response CsCPs encoded AAPA/V/L motifs that are related to cuticular elasticity and >50 % of the sclerotization-related his-rich RR2 genes were also upregulated. These results suggested the potential roles of CsCPs in balancing the elasticity and sclerotization of cuticles, which is essential for the survival and adaptation of plant borers including C. suppressalis. Our study provides valuable information for further developing cuticle-based strategies of both pest management and biomimetic applications.