Chromatin Remodeler TaSWI3D Controls Wheat Susceptibility to Pathogenic Fungus Blumeria graminis forma specialis tritici

Pathogenic fungus <i>Blumeria graminis</i><i>forma specialis</i><i>tritici</i> (<i>B.g. tritici</i>) is the causal agent of the devastating wheat powdery mildew disease. Identifying the key regulators governing wheat susceptibility to the <i>B.g. tritici</i> pathogen is essential for developing wheat varieties with improved powdery mildew resistance. In this study, we demonstrated that the wheat chromatin remodeler TaSWI3D positively regulates wheat susceptibility to <i>B.g. tritici</i>. Overexpression of <i>TaSWI3D</i> gene attenuates wheat resistance against <i>B.g. tritici</i>, while silencing of <i>TaSWI3D</i> gene potentiates wheat powdery mildew resistance. TaSWI3D protein was found to be enriched at the promoter regions of the <i>TaSARD1</i> gene encoding the salicylic acid (SA) biosynthesis activator, and silencing of <i>TaSWI3D</i> resulted in decreased nucleosome occupancy at the <i>TaSARD1</i> promoter regions. Activated <i>TaSARD1</i> transcription and increased SA accumulation were observed in the <i>TaSWI3D</i>-silenced wheat plants. Silencing of <i>TaSARD1</i> and the SA biosynthesis gene <i>TaICS1</i> resulted in attenuated SA biosynthesis and decreased powdery mildew resistance in the <i>TaSWI3D</i>-silenced wheat plants. These findings support that the chromatin remodeler TaSWI3D maintains epigenetic suppression of the SA biosynthesis activator gene <i>TaSARD1</i> and negatively regulates SA biosynthesis, thereby positively contributing to wheat powdery mildew susceptibility.