An enhancer-promoter-transcription factor module orchestrates plant immune homeostasis by constraining camalexin biosynthesis.

Abstract

Effective plant defense against pathogens relies on highly coordinated regulation of immune gene expression. Enhancers, as cis-regulatory elements, are indispensable determinants of dynamic gene regulation, but the molecular functions in plant immunity are not well understood. In this study, we identified a novel enhancer, CORE PATTERN-INDUCED ENHANCER 35 (CPIE35), which is rapidly activated upon pathogenic elicitation and negatively regulates antifungal resistance through modulating WRKY15 expression. During immune activation, CPIE35 activates the transcription of WRKY15 by forming chromatin loops with the promoter of WRKY15 in a WRKY18/40/60-, WRKY33-, and MYC2-dependent manner. WRKY15 directly binds to the promoters of PAD3 and GSTU4, suppressing their expression and leading to reduced camalexin synthesis and resistance. Interestingly, CPIE35 region is evolutionarily conserved among Brassicaceae plants, and the CPIE35-WRKY15 module exerts similar functions in Brassica napus to negatively regulate antifungal resistance. Our work reveals the "enhancer-promoter-transcription factor" regulatory mechanism in maintenance of immune homeostasis, highlighting the importance and conserved role of enhancers in fine-tuning immune gene expression in plants.