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Maize (Zea mays) is one of the most important crops in the world, but its yield and quality are seriously affected by diverse diseases. Identifying broad-spectrum resistance genes is crucial for developing effective strategies to control the disease in maize. In a genome-wide study in maize, we identified a G-type lectin receptor kinase ZmLecRK1, as a new resistance protein against Pythium aphanidermatum , one of the causal pathogens of stalk rot in maize. Genetic analysis showed that the specific ZmLecRK1 allele can confer resistance to multiple pathogens in maize. The cell death and disease resistance phenotype mediated by the resistant variant of ZmLecRK1 requires the co-receptor ZmBAK1. A naturally occurring A404S variant in the extracellular domain of ZmLecRK1 determines the ZmLecRK1-ZmBAK1 interaction and the formation of ZmLecRK1-related protein complexes. Interestingly, the ZmLecRK1 susceptible variant was found to possess the amino acid S404 that is present in the ancestral variants of ZmLecRK1 and conserved among the majority of grass species, while the resistance variant of ZmLecRK1 with A404 is only present in a few maize inbred lines. Substitution of S by A at position 404 in ZmLecRK1-like proteins of sorghum and rice greatly enhances their ability to induce cell death. Further transcriptomic analysis reveals that ZmLecRK1 likely regulates gene expression related to the pathways in cell wall organization or biogenesis in response to pathogen infection. Taken together, these results suggest that the ZmLecRK1 resistance variant enhances its binding affinity to the co-receptor ZmBAK1, thereby enhancing the formation of active complexes for defense in maize. Our work highlights the biotechnological potential for generating disease-resistant crops by precisely modulating the activity of ZmLecRK1 and its homologs through targeted base editing. The G-type lectin receptor kinase ZmLecRK1 confers multiple disease resistance in maize. A naturally occurring A404S variant in ZmLecRK1 determines the ZmLecRK1-ZmBAK1 interaction for defense. The susceptible variant of ZmLecRK1 with S404 that is conserved among the majority of grass species constitutes the ancestral variants of ZmLecRK1, while the resistance variant with A404 is only present in a few maize inbred lines. [ABSTRACT FROM AUTHOR]

Summary: Maize is one of the most important crops for food, cattle feed and energy production. However, maize is frequently attacked by various pathogens and pests, which pose a significant threat to maize yield and quality. Identification of quantitative trait loci and genes for resistance to pests will provide the basis for resistance breeding in maize. Here, a β‐glucosidase ZmBGLU17 was identified as a resistance gene against Pythium aphanidermatum, one of the causal agents of corn stalk rot, by genome‐wide association analysis. Genetic analysis showed that both structural variations at the promoter and a single nucleotide polymorphism at the fifth intron distinguish the two ZmBGLU17 alleles. The causative polymorphism near the GT‐AG splice site activates cryptic alternative splicing and intron retention of ZmBGLU17 mRNA, leading to the downregulation of functional ZmBGLU17 transcripts. ZmBGLU17 localizes in both the extracellular matrix and vacuole and contribute to the accumulation of two defence metabolites lignin and DIMBOA. Silencing of ZmBGLU17 reduces maize resistance against P. aphanidermatum, while overexpression significantly enhances resistance of maize against both the oomycete pathogen P. aphanidermatum and the Asian corn borer Ostrinia furnacalis. Notably, ZmBGLU17 overexpression lines exhibited normal growth and yield phenotype in the field. Taken together, our findings reveal that the apoplastic and vacuolar localized ZmBGLU17 confers resistance to both pathogens and insect pests in maize without a yield penalty, by fine‐tuning the accumulation of lignin and DIMBOA. [ABSTRACT FROM AUTHOR]