GPCR–MAPK signaling pathways underpin fitness trade-offs in whitefly

作者：Buli Fu, Jinjin Liang, Jinyu Hu, Tianhua Du, Qimei Tan, Chao He, Xuegao Wei, Peipan Gong, Jing Yang, Shaonan Liu, Mingjiao Huang, Lianyou Gui, Kui Liu, Xuguo Zhou, Ralf Nauen, Chris Bass, Xin Yang, Youjun Zhang · 发表于：Proceedings of the National Academy of Sciences · 年份：2024 · DOI：10.1073/pnas.2402407121 · 被引用次数：45 · 研究领域：Insect-Plant Interactions and Control、Insect Resistance and Genetics、Insect behavior and control techniques

Trade-offs between evolutionary gain and loss are prevalent in nature, yet their genetic basis is not well resolved. The evolution of insect resistance to insecticide is often associated with strong fitness costs; however, how the fitness trade-offs operates remains poorly understood. Here, we show that the mitogen-activated protein kinase (MAPK) pathway and its upstream and downstream actors underlie the fitness trade-offs associated with insecticide resistance in the whitefly Bemisia tabaci . Specifically, we find a key cytochrome P450 gene CYP6CM1 , that confers neonicotinoids resistance to in B. tabaci , is regulated by the MAPKs p38 and ERK through their activation of the transcription factor cAMP-response element binding protein. However, phosphorylation of p38 and ERK also leads to the activation of the transcription repressor Cap “n” collar isoform C (CncC) that negatively regulates exuperantia (Ex), vasa (Va), and benign gonial cell neoplasm (Bg ), key genes involved in oogenesis, leading to abnormal ovary growth and a reduction in female fecundity. We further demonstrate that the transmembrane G protein-coupled receptor (GPCR) neuropeptide FF receptor 2 (NPFF2) triggers the p38 and ERK pathways via phosphorylation. Additionally, a positive feedback loop between p38 and NPFF2 leads to the continuous activation of the MAPK pathways, thereby constitutively promoting neonicotinoids resistance but with a significant reproductive cost. Collectively, these findings provide...