A novel mode of WRKY1 regulating PR1-mediated immune balance to defend against powdery mildew in apple.

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.