An Apple Susceptibility-Related LRR Receptor-Like Kinase MdRLKT21 Activates Plant Immunity by Hijacking a Trans-Kingdom Fungal microRNA-Like RNA

Fungal small RNAs (sRNAs) represent a novel class of effector molecules in plant-pathogen interactions. However, understanding of how plants counteract fungal sRNAs-mediated trans-kingdom RNA interference (RNAi) in plant immunity remains limited. In previous study, a milRNA (Vm-milR1) from Valsa mali can be found to transboundary inhibit the expression of disease-resistance genes MdRLKT1 and MdRLKT2 in apple. In this study, a leucine-rich repeat receptor-like kinase MdRLKT21 is isolated and characterized, and is confirmed to play a negative regulatory role in the basal immune response. Importantly, MdRLKT21 could hijack Vm-milR1 to rescue the suppression of MdRLKT1 and MdRLKT2, and a similar phenomenon is also observed in the interaction between V. mali and pear trees. Meanwhile, it is demonstrated that MdRLKT21 can interact with and phosphorylate a C3HC4-type RING finger protein MdRFP1, which positively regulates the apple resistance to V. mali infection. What's more, it is found that MdRLKT21 could inhibit the MdRFP1-mediated immune response, probably by promoting the 26S proteasome-mediated degradation of MdRFP1 in a kinase activity-dependent manner. Taken together, it is proposed that an apple susceptibility-related LRR-RLK competitively binds to fungal sRNA effector and subsequently activates defenses by salvaging the expression of MdRLKT1 and MdRLKT2 and thereby releasing the resistance protein MdRFP1.