Endogenous RALF peptide function is required for powdery mildew host colonization

Abstract The receptor kinase FERONIA (FER) is a susceptibility factor for biotrophic powdery mildew fungal pathogens in Arabidopsis thaliana , but the underlying molecular mechanisms remain largely unknown. FER is required for the perception of endogenous RAPID ALKALINIZATION FACTOR (RALF) peptides to control various aspects of plant growth, development and immunity. RALFs are perceived by FER-LORELEI-LIKE GPI-ANCHORED PROTEIN (LLG) heterocomplexes to induce cellular responses and bind to LEUCINE-RICH REPEAT EXTENSIN (LRX) proteins as structural components of the cell wall. Combining genetics, cell biology and biochemistry, we found that FER’s endogenous RALF ligands are necessary for full colonization success of the powdery mildew species Erysiphe cruciferarum . We reveal that LLGs and LRXs are also powdery mildew susceptibility factors. We show that cell wall remodeling and apoplastic pH homeostasis, hallmark features of RALF function, support powdery mildew reproductive success. Moreover, we provide data that RALF-dependent powdery mildew pathogenesis is partially independent of FER. Powdery mildew fungi likely do not produce RALF peptide mimics, suggesting their reliance on endogenous RALFs for successful host colonization. We propose that powdery mildew fungi require RALF-mediated modulation of apoplastic pH and pectin re-modelling for successful host colonization, highlighting a new susceptibility mechanism by obligate biotrophic fungi.