The molecular mechanism by which plants defend against plant root-knot nematodes (RKNs) is largely unknown. The plant receptor kinase FERONIA and its peptide ligands, rapid alkalinization factors (RALFs), regulate plant immune responses and cell expansion, which are two important factors for successful RKN parasitism. In this study, we found that mutation of FERONIA in Arabidopsis thaliana resulted in plants showing low susceptibility to the RKN Meloidogyne incognita. To identify the underlying mechanisms associated with this phenomenon, we identified 18 novel RALF-likes from multiple species of RKNs and showed that two RALF-likes (i.e., MiRALF1 and MiRALF3) from M. incognita were expressed in the esophageal gland with high expression during the parasitic stages of nematode development. These nematode RALF-likes also possess the typical activities of plant RALFs and can directly bind to the extracellular domain of FERONIA to modulate specific steps of nematode parasitism-related immune responses and cell expansion. Genetically, both MiRALF1/3 and FERONIA are required for RKN parasitism in Arabidopsis and rice. Collectively, our study suggests that nematode-encoded RALFs facilitate parasitism via plant-encoded FERONIA and provides a novel paradigm for studying host–pathogen interactions.

植物抵御植物根结线虫（RKNs）的分子机制尚不清楚。植物受体激酶FERONIA及其肽配体，快速碱化因子（RALF）调节植物免疫反应和细胞扩增，这是成功实现RKN寄生的两个重要因素。在这项研究中，我们发现拟南芥中FERONIA的突变导致植物对RKN Meloidogyne incognita的敏感性较低。为了确定与此现象相关的潜在机制，我们从多个RKNs物种中鉴定出18种新颖的RALF样，并发现了隐孢分枝杆菌的两个RALF样（即，MiRALF1和MiRALF3）。在线虫发育的寄生阶段在食管腺中高表达。这些线虫的RALF样也具有植物RALF的典型活性，并且可以直接与FERONIA的胞外域结合，从而调节线虫寄生虫相关免疫应答和细胞扩增的特定步骤。从基因上讲，拟南芥和水稻中RKN寄生需要同时使用MiRALF1 / 3和FERONIA。总体而言，我们的研究表明，线虫编码的RALF通过植物编码的FERONIA促进了寄生，并为研究宿主与病原体的相互作用提供了新的范例。