Integrated Transcriptome and MicroRNAome Analysis Reveals Dynamic Responses Underlying ZmWAK-Mediated Resistance to Head Smut in Maize

The maize wall-associated kinase gene ZmWAK confers partial resistance to head smut caused by Sporisorium reilianum, yet how it coordinates dynamic immune responses remains poorly understood. Here, we integrated transcriptome and microRNAome analyses of near-isogenic maize lines differing at the ZmWAK locus to dissect the regulatory landscape underlying ZmWAK-mediated resistance during mesocotyl infection. We found that ZmWAK was associated with a stage-specific defense trajectory characterized by dynamic shifts in phytohormone networks, intermediate cellular reprogramming, and late-stage cell wall remodeling. A conserved extracellular defense signature was maintained through sustained activation of apoplastic oxidoreductase-associated processes. Meanwhile, ZmWAK-associated miRNAs were preferentially reprogrammed during peak pathogen proliferation, and their predicted targets were enriched in phenylpropanoid metabolism, lignin biosynthesis, secondary metabolism, and apoplastic oxidoreductase activity. These patterns suggest that transcriptional and post-transcriptional responses converge on extracellular redox and cell wall-associated defense processes. Together, our findings define a dynamic, multilayered regulatory landscape associated with ZmWAK-mediated quantitative resistance and provide insights into how resistance loci coordinate temporal immune responses during pathogen infection.