Nematode-Encoded RALF Peptide Mimics Facilitate Parasitism of Plants through the FERONIA Receptor Kinase

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. Eighteen novel RALF-likes were identified from multiple species of root-knot nematodes (RKNs). Both nematode RALF-likes and the plant receptor kinase FERONIA were found to be required for RKN parasitism in Arabidopsis and rice. Nematode RALF-likes are expressed in the esophageal gland and serve as ligands of FERONIA to modulate the immune response and facilitate parasitism, providing a novel paradigm for studying host–pathogen interactions.