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

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