Allelic Variation in Maize Malate Dehydrogenase 7 Shapes Promoter Methylation and Banded Leaf and Sheath Blight Resistance

In this study maize chloroplastic malate dehydrogenase7 (ZmMDH7), is identified as a Rhizoctonia solani resistance gene in maize. ZmMDH7 is regulated by transcription factor ZmWRKY44 via pathogens challenge to elevate mitochondrial ROS and SA signaling pathway. A transposable element insertion in promotor of ZmRRS1 dampens ZmWRKY44‐mediated expression of ZmMDH7, that suppress maize resistance to R. solani. Abstract Rhizoctonia solani, a globally distributed phytopathogen, causes banded leaf and sheath blight (BLSB) in maize and sheath blight in rice, severely threatening crop productivity. Here, this work identifies ZmRRS1 (Resistance to Rhizoctonia solani 1), which encodes maize malate dehydrogenase, as a key positive regulator of BLSB resistance in the field through a genome‐wide association study. ZmRRS1 knockout lines exhibit increased susceptibility to BLSB, whereas overexpression of ZmRRS1 and its homologs confer enhanced resistance to R. solani in both maize and rice. Using heterozygote inbred families (HIF), this work uncovers that the presence and absence of a 831‐bp transposable element (TE) element is the causal polymorphism that determines the differential expression pattern of the two ZmRRS1 alleles in response to R. solani. Furthermore, the absence of the TE increases the binding of the ZmWRKY44 transcription factor to the W‐box motif in the promoter of ZmRRS1, thereby enhancing BLSB resistance. Transcriptomic analysis reveals that ZmRRS1 potentiates reactive oxygen species (ROS)‐mediated immunity against BLSB. Notably, the overexpression of ZmRRS1 does not incur agronomic penalties under normal growth conditions. Collectively, this work identifies ZmRRS1 as a positive regulator of BLSB resistance, offering valuable genetic resources for breeding BLSB‐resistant maize and rice varieties. In this study maize chloroplastic malate dehydrogenase7 ( ZmMDH7 ), is identified as a Rhizoctonia solani resistance gene in maize. ZmMDH7 is regulated by transcription factor ZmWRKY44 via pathogens challenge to elevate mitochondrial ROS and SA signaling pathway. A transposable element insertion in promotor of ZmRRS1 dampens ZmWRKY44-mediated expression of ZmMDH7, that suppress maize resistance to R. solani. Abstract Rhizoctonia solani, a globally distributed phytopathogen, causes banded leaf and sheath blight (BLSB) in maize and sheath blight in rice, severely threatening crop productivity. Here, this work identifies ZmRRS1 (Resistance to Rhizoctonia solani 1), which encodes maize malate dehydrogenase, as a key positive regulator of BLSB resistance in the field through a genome-wide association study. ZmRRS1 knockout lines exhibit increased susceptibility to BLSB, whereas overexpression of ZmRRS1 and its homologs confer enhanced resistance to R. solani in both maize and rice. Using heterozygote inbred families (HIF), this work uncovers that the presence and absence of a 831-bp transposable element (TE) element is the causal polymorphism that determines the differential expression pattern of the two ZmRRS1 alleles in response to R. solani. Furthermore, the absence of the TE increases the binding of the ZmWRKY44 transcription factor to the W-box motif in the promoter of ZmRRS1, thereby enhancing BLSB resistance. Transcriptomic analysis reveals that ZmRRS1 potentiates reactive oxygen species (ROS)-mediated immunity against BLSB. Notably, the overexpression of ZmRRS1 does not incur agronomic penalties under normal growth conditions. Collectively, this work identifies ZmRRS1 as a positive regulator of BLSB resistance, offering valuable genetic resources for breeding BLSB-resistant maize and rice varieties. Advanced Science, EarlyView.