Alternative splicing of a potato disease resistance gene maintains homeostasis between development and immunity, and functions as a novel process for pathogen surveillance

Abstract

AbstractPlants possess a robust and sophisticated innate immune system against pathogens. The intracellularly localized receptors with nucleotide-binding, leucine-rich repeat (NLR) motifs recognize pathogen-derived effector proteins to trigger the immune response. To balance plant growth with rapid pathogen detection, NLR expression is precisely controlled in multifaceted ways. The role of post-transcriptional processing of NLRs, including alternative splicing (AS) of introns, in response to infection is an important area of research that requires further study. 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.RBmainly exists as intron-retained isoformRB_IRencoding a truncated lost-function RB protein to maintain plant normal growth without pathogen infection. Upon late blight infection, the causal pathogenPhytophthora infestansinduces intron splicing ofRB, increasing the abundance ofRB_CDS, which encodes a full-length, and active R protein. By deploying theRBsplicing isoforms fused withluciferasereporter system, we identified IPI-O1 (also known as Avrblb1), the RB cognate effector, as a facilitator ofRBAS. Importantly, IPI-O1 directly interacts with potato splicing factor StCWC15 to promoteRBsplicing for activation ofRB-mediated resistance. Thus, our study reveals that StCWC15 serves as a surveillance facilitator sensing the pathogen-secreted effector maintaining the trade-off betweenRB-mediated plant immunity and growth, expanding our understanding of molecular plant-microbe interactions.