A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple
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 plan...
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| Format: | Article |
| Language: | English |
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BMC
2025-03-01
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| Series: | Molecular Horticulture |
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| Online Access: | https://doi.org/10.1186/s43897-024-00141-z |
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| author | 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 |
| author_facet | 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 |
| author_sort | Liming Lan |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-7a65c30539b347fdb123281e8109993e |
| institution | DOAJ |
| issn | 2730-9401 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Molecular Horticulture |
| spelling | doaj-art-7a65c30539b347fdb123281e8109993e2025-08-20T03:05:44ZengBMCMolecular Horticulture2730-94012025-03-015112110.1186/s43897-024-00141-zA novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in appleLiming Lan0Lifang Cao1Lulu Zhang2Weihong Fu3Changguo Luo4Chao Wu5Xianqi Zeng6Shenchun Qu7Xinyi Yu8Wenyi Deng9Xu Xu10Binhua Cai11Sanhong Wang12College of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityInstitute of Pomology, Guizhou Academy of Agricultural SciencesCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityAbstract 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.https://doi.org/10.1186/s43897-024-00141-zApple powdery mildewSalicylic acidPR1Plant immunityImmune balanceWRKY40-NPR3g module |
| spellingShingle | 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 A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple Molecular Horticulture Apple powdery mildew Salicylic acid PR1 Plant immunity Immune balance WRKY40-NPR3g module |
| title | A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple |
| title_full | A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple |
| title_fullStr | A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple |
| title_full_unstemmed | A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple |
| title_short | A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple |
| title_sort | novel mode of wrky1 regulating pr1 mediated immune balance to defend against powdery mildew in apple |
| topic | Apple powdery mildew Salicylic acid PR1 Plant immunity Immune balance WRKY40-NPR3g module |
| url | https://doi.org/10.1186/s43897-024-00141-z |
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