Rui Penghuan, Jia Zhaoxing, Fang Xinxin, Yu Tianqi, Mao Wenqi, Lin Jiajia, Zheng Hongying, Lu Yuwen, Yu Feng, Chen Jianping, Yan Fei, Wu Guanwei
College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, China.
State Key Laboratory for Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of MARA, Key Laboratory of Green Plant Protection of Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, China.
Plant Biotechnol J. 2025 Jul;23(7):2734-2751. doi: 10.1111/pbi.70099. Epub 2025 Apr 20.
The receptor-like kinase FERONIA (FER) is a prominent member of the Catharanthus roseus RLK1 (CrRLK1L) family, functioning as a modulator of immune receptor kinase complex formation in response to rapid alkalinization factors (RALFs). Typically, FER recognizes mature extracellular RALFs to combat bacterial and fungal infections. However, any role of the FER-RALF signalling cascade in plant viral infections remains unexplored. Here, we used turnip mosaic virus (TuMV), an important member of the genus Potyvirus, and the host Nicotiana benthamiana as a model system to explore the role of the FER-RALF cascade in plant-virus interactions. RALF1 from N. benthamiana (NbRALF1) positively regulated host resistance to inhibit TuMV infection. Co-expression studies showed that this process does not involve the conserved RRXL and YISY motifs typically associated with RALF function. Instead, NbRALF1 induced cell death and significantly inhibited TuMV infection in a manner that depends on the entire RALF1 sequence and also NbFER. These results suggest a novel mechanism where NbRALF1 may inhibit viral infection through intracellular interactions with NbFER, differing from the previously reported extracellular FER-RALF interactions that induce resistance to fungi and bacteria. Furthermore, we discovered that TuMV 6K2 interacts with NbRALF1 and promotes its degradation through the 26S proteasome pathway, thereby counteracting the host resistance induced by the NbFER-NbRALF1 cascade. Our findings imply the existence of an uncharacterized intracellular immunity signalling pathway mediated by the NbFER-NbRALF1 cascade and reveal a mechanism by which plant viruses counteract RALF1-FER module-mediated immunity.
类受体激酶FERONIA(FER)是长春花类受体激酶1(CrRLK1L)家族的重要成员,作为免疫受体激酶复合物形成的调节剂,响应快速碱化因子(RALFs)。通常,FER识别成熟的细胞外RALFs以对抗细菌和真菌感染。然而,FER-RALF信号级联在植物病毒感染中的任何作用仍未得到探索。在这里,我们使用芜菁花叶病毒(TuMV),马铃薯Y病毒属的重要成员,以及宿主本氏烟草作为模型系统,来探索FER-RALF级联在植物-病毒相互作用中的作用。来自本氏烟草的RALF1(NbRALF1)正向调节宿主抗性以抑制TuMV感染。共表达研究表明,这一过程不涉及通常与RALF功能相关的保守RRXL和YISY基序。相反,NbRALF1以依赖于整个RALF1序列以及NbFER的方式诱导细胞死亡并显著抑制TuMV感染。这些结果表明了一种新机制,其中NbRALF1可能通过与NbFER的细胞内相互作用来抑制病毒感染,这与先前报道的诱导对真菌和细菌抗性的细胞外FER-RALF相互作用不同。此外,我们发现TuMV 6K2与NbRALF1相互作用并通过26S蛋白酶体途径促进其降解,从而抵消由NbFER-NbRALF1级联诱导的宿主抗性。我们的研究结果暗示存在由NbFER-NbRALF1级联介导的未表征的细胞内免疫信号通路,并揭示了植物病毒对抗RALF1-FER模块介导的免疫的机制。