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

生物 RNA剪接 免疫 植物抗病性 选择性拼接 平衡 细胞生物学 疾病 遗传学 基因 植物免疫 抗性(生态学) 免疫系统 核糖核酸 生态学 拟南芥 外显子 内科学 医学 突变体
作者
Biying Sun,Jie Huang,Liang Kong,Chuyun Gao,Fei Zhao,Jiayong Shen,Tianruo Wang,Kangping Li,Luyao Wang,Yuanchao Wang,Dennis Halterman,Suomeng Dong
出处
期刊:The Plant Cell [Oxford University Press]
卷期号:36 (9): 3729-3750 被引量:5
标识
DOI:10.1093/plcell/koae189
摘要

Abstract Plants possess a robust and sophisticated innate immune system against pathogens and must balance growth with rapid pathogen detection and defense. The intracellular receptors with nucleotide-binding leucine-rich repeat (NLR) motifs recognize pathogen-derived effector proteins and thereby trigger the immune response. The expression of genes encoding NLR receptors 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 (Solanum tuberosum) NLR gene RB undergoes AS of its intron, resulting in 2 transcriptional isoforms, which coordinately regulate plant immunity and growth homeostasis. During normal growth, RB predominantly exists as an intron-retained isoform RB_IR, encoding a truncated protein containing only the N-terminus of the NLR. Upon late blight infection, the pathogen 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 a luciferase reporter system, we identified IPI-O1 (also known as Avrblb1), the RB cognate effector, as a facilitator of RB AS. 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 and RB intron splicing. Thus, our study reveals that StCWC15 serves as a surveillance facilitator that senses the pathogen-secreted effector and regulates the trade-off between RB-mediated plant immunity and growth, expanding our understanding of molecular plant–microbe interactions.
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