Alternative splicing of a potato disease resistance gene maintains homeostasis between development and immunity

Plants possess a robust and sophisticated innate immune system against pathogens. The intracellular receptors with nucleotide-binding, leucine-rich repeat (NLR) motifs recognize pathogen-derived effector proteins to trigger the immune response. To balance plant growth and rapid pathogen detection, NLR expression is precisely controlled in multifaceted ways. The alternative splicing (AS) of introns in response to infection is recurrently observed but poorly understood. Here we report that the potato NLR geneRBundergoes AS of its intron, resulting in two transcriptional isoforms, which coordinately regulate plant immunity and growth homeostasis. During normal growth,RBpredominantly exists as intron-retained isoformRB_IR, encoding a truncated protein containing only the N-terminus of the NLR. Upon late blight infection, the pathogen induces intron splicing ofRB, increasing the abundance ofRB_CDS, which encodes a full-length and active R protein. By deploying theRBsplicing isoforms fused with aluciferasereporter system, we identified IPI-O1 (also known as Avrblb1), the RB cognate effector, as a facilitator ofRBAS. IPI-O1 directly interacts with potato splicing factor StCWC15, resulting in altered localization of StCWC15 from the nucleoplasm to the nucleolus and nuclear speckles. Mutations in IPI-O1 that eliminate StCWC15 binding also disrupt StCWC15 re-localization andRBintron splicing. Thus, our study reveals that StCWC15 serves as a surveillance facilitator sensing the pathogen-secreted effector, and regulates the trade-off betweenRB-mediated plant immunity and growth, expanding our understanding of molecular plant-microbe interactions.