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

Abstract 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.