{"title":"A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple.","authors":"Liming Lan, Lifang Cao, Lulu Zhang, Weihong Fu, Changguo Luo, Chao Wu, Xianqi Zeng, Shenchun Qu, Xinyi Yu, Wenyi Deng, Xu Xu, Binhua Cai, Sanhong Wang","doi":"10.1186/s43897-024-00141-z","DOIUrl":null,"url":null,"abstract":"<p><p>Powdery mildew (PM), caused by the biotrophic fungus Podospharea leucotricha, poses a significant threat to apple production. Salicylic acid (SA) signaling plays a crucial role in enhancing resistance to biotrophic pathogens. While PR1, a defense protein induced by SA, is essential for plant immunity, its excessive accumulation can be detrimental. However, the mechanism of PR1-mediated immune balance remains unclear. This study identified a key transcription factor, WRKY1, which enhances the SA accumulation by modulating the SA biosynthesis gene EPS1, while simultaneously regulating the WRKY40-NPR3g module to prevent sustained PR1 expression caused by continuous SA accumulation. Specifically, the transcription factor WRKY40 upregulates NPR3g expression, and NPR3g interacts with NPR1 in an SA-dependent manner. Then, two TGA2c variants that interact with NPR1 to activate PR1 expression were identified: canonical TGA2c-1 and alternative splicing of TGA2c-2 with an exon deletion. SA does not influence the NPR1-TGA2c-1 interaction but is essential for the NPR1-TGA2c-2 interaction. Notably, NPR3g reduces PR1 levels by selectively disrupting the NPR1-TGA2c-2 complex through competition for the BTB-POZ domain of NPR1. In conclusion, this study identifies a novel mechanism by which WRKY1 modulates PR1-mediated immune balance to defend against PM.</p>","PeriodicalId":29970,"journal":{"name":"Molecular Horticulture","volume":"5 1","pages":"17"},"PeriodicalIF":10.6000,"publicationDate":"2025-03-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11881497/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Horticulture","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1186/s43897-024-00141-z","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"HORTICULTURE","Score":null,"Total":0}
引用次数: 0
Abstract
Powdery mildew (PM), caused by the biotrophic fungus Podospharea leucotricha, poses a significant threat to apple production. Salicylic acid (SA) signaling plays a crucial role in enhancing resistance to biotrophic pathogens. While PR1, a defense protein induced by SA, is essential for plant immunity, its excessive accumulation can be detrimental. However, the mechanism of PR1-mediated immune balance remains unclear. This study identified a key transcription factor, WRKY1, which enhances the SA accumulation by modulating the SA biosynthesis gene EPS1, while simultaneously regulating the WRKY40-NPR3g module to prevent sustained PR1 expression caused by continuous SA accumulation. Specifically, the transcription factor WRKY40 upregulates NPR3g expression, and NPR3g interacts with NPR1 in an SA-dependent manner. Then, two TGA2c variants that interact with NPR1 to activate PR1 expression were identified: canonical TGA2c-1 and alternative splicing of TGA2c-2 with an exon deletion. SA does not influence the NPR1-TGA2c-1 interaction but is essential for the NPR1-TGA2c-2 interaction. Notably, NPR3g reduces PR1 levels by selectively disrupting the NPR1-TGA2c-2 complex through competition for the BTB-POZ domain of NPR1. In conclusion, this study identifies a novel mechanism by which WRKY1 modulates PR1-mediated immune balance to defend against PM.
期刊介绍:
Aims
Molecular Horticulture aims to publish research and review articles that significantly advance our knowledge in understanding how the horticultural crops or their parts operate mechanistically. Articles should have profound impacts not only in terms of high citation number or the like, but more importantly on the direction of the horticultural research field.
Scope
Molecular Horticulture publishes original Research Articles, Letters, and Reviews on novel discoveries on the following, but not limited to, aspects of horticultural plants (including medicinal plants):
▪ Developmental and evolutionary biology
▪ Physiology, biochemistry and cell biology
▪ Plant-microbe and plant-environment interactions
▪ Genetics and epigenetics
▪ Molecular breeding and biotechnology
▪ Secondary metabolism and synthetic biology
▪ Multi-omics dealing with data sets of genome, transcriptome, proteome, metabolome, epigenome and/or microbiome.
The journal also welcomes research articles using model plants that reveal mechanisms and/or principles readily applicable to horticultural plants, translational research articles involving application of basic knowledge (including those of model plants) to the horticultural crops, novel Methods and Resources of broad interest.
In addition, the journal publishes Editorial, News and View, and Commentary and Perspective on current, significant events and topics in global horticultural fields with international interests.