Transcription factor TaEPBM1 governs the humidity-responsive biosynthesis of cuticular wax and salicylic acid fine-tuning powdery mildew susceptibility1

• Functional characterization of the 3-ketoacyl-CoA reductase ( KCR ) genes in bread wheat revealed that TaKCR1 genes partially redundantly contribute to wheat cuticular wax biosynthesis. • Wheat transcription factor TaEPBM1 recruits TaADA2 to epigenetically activates transcription of TaKCR1 and TaICS2 genes and stimulates biosynthesis of cuticular wax and salicylic acid (SA). • High air humidity suppresses TaEPBM1 gene expression and dampens biosynthesis of cuticular wax and SA to affect wheat powdery mildew susceptibility. Powdery mildew disease caused by the host-adapted fungal pathogen Blumeria graminis f. sp. tritici ( Bgt ) threatens the yield and quality of bread wheat ( Triticum aestivum L.). Air humidity is a key environmental influence affecting the occurrence of plant diseases, but chemical mechanism underlying the response of compatible wheat- Bgt interaction to the air humidity changes remains largely unknown. This study reveals that transcription factor TaEPBM1 governs the humidity-responsive biosynthesis of wheat cuticular wax and salicylic acid (SA) to fine-tune the wheat susceptibility to Bgt. Partially redundant β-ketoacyl-Coenzyme A reductase TaKCR1s were demonstrated to catalyze the biosynthesis of wheat cuticular wax. Transcription factor TaEPBM1 directly targets TaKCR1s and the SA biosynthesis gene TaICS1 , and recruits TaADA2 to promote histone acetylation at TaKCR1s and TaICS1 promoters, thereby epigenetically activating cuticular wax and SA biosynthesis. In addition, we showed that high air humidity suppresses TaEPBM1 gene transcription and attenuates the epigenetic activation of cuticular wax and SA biosynthesis. Importantly, very-long-chain (VLC) aldehydes and SA were identified as the humidity-responsive chemical cues provided by the TaADA2-TaEPBM1-TaKCR1/TaICS1 circuit for fine-tuning the compatible wheat- Bgt interaction. These findings support that transcription factor TaEPBM1 governs the humidity-responsive biosynthesis of wheat cuticular wax and SA to fine-tune the wheat susceptibility to Bgt , providing valuable information for the wheat powdery mildew control.