数字农科院2.0

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

文献类型： 外文期刊

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

作者机构：

关键词： adaptive evolution;fitness trade-offs;GPCR;MAPK;P450

期刊名称： Proceedings of the National Academy of Sciences of the United States of America

ISSN： 1091-6490

年卷期： 2024 年 121 卷 28 期

页码：

收录情况： SCIE（2024版）

摘要： 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 fundamental insights into the role of cis-trans regulatory networks incurred by GPCR-MAPK signaling pathways in evolutionary trade-offs and applied knowledge that can inform the development of strategies for the sustainable pest control.

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