Ustilaginoidea virens cortical patch protein is an essential virulence factor and activates plant immunity

Ustilaginoidea virens secretes numerous proteins during infection, the mechanisms regulating plant immunity and fungal virulence remain largely unknown. Herein, we identified a cortical patch protein, UvCPP1, from the U. virens secretome, as a cell death-inducing protein. UvCPP1 is secreted into rice florets via extracellular vesicles during U. virens infection. It activates plant basal immunity, as evidenced by reactive oxygen species (ROS) burst, callose deposition, and upregulation of defense-related genes. Notably, the UvCPP1^(1-136) is sufficient to elicit immune responses comparable to the full-length UvCPP1. UvCPP1-induced cell death in Nicotiana benthamiana depends on brassinosteroid-insensitive 1 (BRI1)-associated receptor kinase 1 (BAK1) but is independent of suppressor of BIR1-1 (SOBIR1) and nucleotide-binding leucine-rich repeat (NLR) co-receptors. The transcript level of UvCPP1 is significantly upregulated during infection. Both knockout and overexpression of UvCPP1 significantly attenuated fungal pathogenicity, demonstrating that UvCPP1 functions as a virulence factor to promote infection and is recognized by plants. Heterologous expression of UvCPP1 significantly enhances rice immunity without compromising agronomic traits, characterized by increased ROS accumulation, callose deposition, and mitogen-activated protein kinase (MAPK) phosphorylation. UvCPP1-overexpressing lines exhibit broad-spectrum resistance against multiple pathogens. RNA-seq analysis revealed that UvCPP1 expression activates defense-related genes, phytohormone signaling pathways, and diterpenoid biosynthesis. Although UvCPP1 is indispensable for the full virulence of U. virens, it simultaneously activates plant immune responses. The characteristics of UvCPP1 highlight its potential application as a molecular tool for breeding disease-resistant crops through immune priming, offering a sustainable strategy for false smut management.