Wheat DNA Methyltransferase TaMET1 Negatively Regulates Salicylic Acid Biosynthesis to Facilitate Powdery Mildew Susceptibility

Powdery mildew disease caused by the obligate biotrophic fungus Blumeria graminis forma specialis tritici (B.g. tritici) severely affects grain yields and end-use quality of bread wheat (Triticum aestivum L.). Uncovering the mechanism underlying the wheat susceptibility to B.g. tritici pathogen could contribute to the wheat breeding against powdery mildew disease. Herein, we revealed that the wheat DNA methyltransferase TaMET1 negatively regulates biosynthesis of defense hormone salicylic acid (SA) to promote powdery mildew susceptibility. Overexpression of TaMET1 compromised wheat resistance against B.g. tritici pathogen, while silencing of TaMET1 led to the SA overaccumulation and enhanced powdery mildew resistance. TaMET1 directly targets the SA biosynthesis activator gene TaSARD1. Decreased DNA methylation, increased histone acetylation, and reduced nucleosome occupancy at TaSARD1 promoter regions were observed in the TaMET1-silenced wheat plants, which is associated with activated TaSARD1 gene transcription. Silencing of the TaSARD1 and TaICS1 genes resulted in attenuated SA biosynthesis and dampened powdery mildew resistance in the TaMET1-silenced wheat plants. These results implied that DNA methyltransferase TaMET1 epigenetically suppresses the SA biosynthesis activator gene TaSARD1 by modulating DNA methylation, histone acetylation and nucleosome occupancy, thereby negatively regulating SA biosynthesis and facilitating the powdery mildew susceptibility.