BdWRKY38 is required for the incompatible interaction of Brachypodium distachyon with the necrotrophic fungus Rhizoctonia solani.

Rhizoctonia solaniis a soil-borne necrotrophic fungus that causes sheath blight in grasses. The basal resistance of compatible interactions betweenR. solaniand rice is known to be modulated by some WRKY transcription factors (TFs). However, genes and defense responses involved in incompatible interaction withR. solaniremain unexplored, because no such interactions are known in any host plants. Recently, we demonstrated that Bd3-1, an accession of the model grassBrachypodium distachyon, is resistant toR. solaniand, upon inoculation with the fungus, undergoes rapid induction of genes responsive to the phytohormone salicylic acid (SA) that encode the WRKY TFs BdWRKY38 and BdWRKY44. Here, we show that endogenous SA and these WRKY TFs positively regulate this accession-specificR. solaniresistance. In contrast to a susceptible accession (Bd21), the infection process in the resistant accessions Bd3-1 and Tek-3 was suppressed at early stages before the development of fungal biomass and infection machinery. A comparative transcriptome analysis during pathogen infection revealed that putative WRKY-dependent defense genes were induced faster in the resistant accessions than in Bd21. A gene regulatory network (GRN) analysis based on the transcriptome dataset demonstrated thatBdWRKY38was a GRN hub connected to many target genes specifically in resistant accessions, whereasBdWRKY44was shared in the GRNs of all three accessions. Moreover, overexpression ofBdWRKY38increasedR. solaniresistance in Bd21. Our findings demonstrate that these resistant accessions can activate an incompatible host response toR. solani, and BdWRKY38 regulates this response by mediating SA signaling.