ZmHPATR1 orchestrates phyllosphere organic acid flux to recruit Sphingomonas and enhance resistance of maize to Curvularia leaf spot

Leaf spots caused by Curvularia lunata infection pose a significant threat to global maize production. Although resistance gene breeding faces challenges due to pathogen evolution, the plant microbiome has emerged as a key modulator of disease resistance. However, the mechanisms via which plant genes regulate phyllosphere metabolites to recruit beneficial microbes remain poorly understood. Here, we combined gene mapping, metabolomics, microbiome analyses, cytological analysis, and in vitro and in vivo experiments to investigate the disease resistance mechanism of ZmHPATR1. We first identified that the loss-of-function mutation in ZmHPATR1 significantly increased the levels of fumaric acid, folic acid, and tetrahydrofolic acid in the leaves, leading to the enrichment of the genus Sphingomonas. We further demonstrated that the extracellular polysaccharide, welan gum, biosynthesized by Sphingomonas, effectively inhibited C. lunata growth and disrupted its cell structure. These results enable us to comprehensively understand the complicated mechanisms of plant resistance to disease through a four-level regulatory network that links plant genes, metabolites, microbes, and pathogens. Our findings provide new strategies for targeted microbiome-based disease-resistant breeding and the development of novel biopesticides for maize.