Wheat SWI3B Subunit of SWI/SNF Chromatin Remodeling Complex Governs Powdery Mildew Susceptibility by Suppressing Salicylic Acid Biosynthesis

The fungal pathogen <i>Blumeria graminis forma specialis tritici</i> (<i>B.g. tritici</i>) infects bread wheat (<i>Triticum aestivum</i> L.) to cause wheat powdery mildew disease. Elucidating the molecular mechanism underlying wheat susceptibility to the pathogenic fungus <i>B.g. tritici</i> could facilitate wheat genetic improvement. In this study, we identified the wheat <i>TaSWI3B</i> gene as a novel <i>Susceptibility</i> gene positively regulating wheat susceptibility to <i>B.g. tritici.</i> The <i>TaSWI3B</i> gene encodes the SWI3B subunit of the SWI/SNF chromatin remodeling complex. The overexpression of the <i>TaSWI3B</i> gene enhances wheat powdery mildew susceptibility, whereas <i>TaSWI3B</i> silencing results in attenuated wheat powdery mildew susceptibility. Importantly, we found that TaSWI3B could be enriched at the promoter regions of the salicylic acid (SA) biosynthesis activator gene <i>TaSARD1</i>, facilitating nucleosome occupancy and thereby suppressing <i>TaSARD1</i> transcription and inhibiting SA biosynthesis. Silencing of <i>TaSARD1</i> and <i>TaICS1</i> encoding a key enzyme in SA biosynthesis could attenuate the SA biosynthesis and powdery mildew resistance potentiated by knockdown of <i>TaSWI3B</i> expression. Collectively, these results suggest that the SWI3B subunit of the wheat SWI/SNF chromatin remodeling complex negatively regulates SA biosynthesis by suppressing <i>TaSARD1</i> transcription at the epigenetic level and thus facilitates wheat powdery mildew susceptibility.