Single-cell transcriptomic profiling of maize cell heterogeneity and systemic immune responses against Puccinia polysora Underw

Southern corn rust (SCR), caused by Puccinia polysora Underw (P. polysora), is a catastrophic disease affecting maize, leading to significant global yield losses. The disease manifests primarily as pustules on the upper surface of corn leaves, obscuring our understanding of its cellular heterogeneity, the maize's response to its infection and the underlying gene expression regulatory mechanisms. In this study, we dissected the heterogeneity of maize's response to P. polysora infection using single-cell RNA sequencing. We delineated cell-type-specific gene expression alterations in six leaf cell types, creating the inaugural single-cell atlas of a maize leaf under fungal assault. Crucially, by reconstructing cellular trajectories in susceptible line N110 and resistant line R99 during infection, we identified diverse regulatory programs that fortify R99's resistance across different leaf cell types. This research uncovers an immune-like state in R99 leaves, characterized by the expression of various fungi-induced genes in the absence of fungal infection, particularly in guard and epidermal cells. Our findings also highlight the role of the fungi-induced glycoside hydrolase family 18 chitinase 7 protein (ZmChit7) in conferring resistance to P. polysora. Collectively, our results shed light on the mechanisms of maize resistance to fungal pathogens through comparative single-cell transcriptomics, offering a valuable resource for pinpointing novel genes that bolster resistance to P. polysora.