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

Abstract Plants 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 gene RB undergoes AS of its intron, resulting in two transcriptional isoforms, which coordinately regulate plant immunity and growth homeostasis. RB mainly exists as intron-retained isoform RB_IR encoding a truncated lost-function RB protein to maintain plant normal growth without pathogen infection. Upon late blight infection, the causal pathogen Phytophthora infestans induces intron splicing of RB , increasing the abundance of RB_CDS , which encodes a full-length, and active R protein. By deploying the RB splicing isoforms fused with luciferase reporter system, we identified IPI-O1 (also known as Avrblb1), the RB cognate effector, as a facilitator of RB AS. Importantly, IPI-O1 directly interacts with potato splicing factor StCWC15 to promote RB splicing for activation of RB -mediated resistance. Thus, our study reveals that StCWC15 serves as a surveillance facilitator sensing the pathogen-secreted effector maintaining the trade-off between RB -mediated plant immunity and growth, expanding our understanding of molecular plant-microbe interactions.