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

文献类型： 外文期刊

作者： Fu, Buli 1 ; Liang, Jinjin 1 ; Hu, Jinyu 1 ; Du, Tianhua 1 ; Tan, Qimei 4 ; He, Chao 1 ; Wei, Xuegao 1 ; Gong, Peipan 1 ; Yang, Jing 1 ; Liu, Shaonan 1 ; Huang, Mingjiao 1 ; Gui, Lianyou 3 ; Liu, Kui 2 ; Zhou, Xuguo 1 ; Nauen, Ralf 7 ; Bass, Chris 8 ; Yang, Xin 1 ; Zhang, Youjun 1 ;

作者机构： 1.Chinese Acad Agr Sci, Inst Vegetables & Flowers, Dept Plant Protect, State Key Lab Vegetable Biobreeding, Beijing 100081, Peoples R China

2.Chinese Acad Trop Agr Sci, Environm & Plant Protect Inst, Key Lab Integrated Pest Management Trop Crops, Minist Agr & Rural Affairs, Haikou 571101, Peoples R China

3.Yangtze Univ, Coll Agr, Hubei Engn Technol Ctr Forewarning & Management Ag, Minist Agr & Rural Affairs Key Lab Sustainable Cro, Jingzhou 434025, Peoples R China

4.Hunan Acad Agr Sci, Inst Agr Biotechnol, Changsha 430125, Peoples R China

5.Hunan Agr Univ, Coll Plant Protect, Changsha 410125, Peoples R China

6.Univ Illinois, Coll Liberal Arts & Sci, Sch Integrat Biol, Dept Entomol, Urbana, IL 61801 USA

7.CropScience Div, Pest Control Biol, Bayer AG, D-40789 Monheim, Germany

8.Univ Exeter, Coll Life & Environm Sci, Penryn TR10 9FE, Cornwall, England

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 （ 影响因子：9.4； 五年影响因子：10.8 ）

ISSN： 0027-8424

年卷期： 2024 年 121 卷 28 期

页码：

收录情况： SCI

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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