Cell-type-specific immune programs orchestrate spatial defense in the Arabidopsis leaf epidermis

Sessile plants rely on individual cells to perceive pathogens and coordinate defense. Guard cells (GCs), best known for regulating stomatal aperture, have poorly understood intrinsic immune roles. Here, we integrate single-cell and spatial analyses of Arabidopsis thaliana leaves infected with diverse phytopathogens, combining live and fixed imaging of transgenic immune reporters with single cell transcriptomic data. Powdery mildew infection triggers strong salicylic acid (SA) biosynthesis and transport in pavement cells, spreading to neighboring uninfected cells. In contrast, GCs fail to activate SA biosynthesis or SA-responsive genes. These cell-type-specific immune programs distinguishing GC and pavement cells are conserved across infections by the hemibiotrophic fungus Colletotrichum higginsianum and the bacterial pathogen Pseudomonas syringae. Despite impaired SA signaling and response, GCs display rapid calcium influx and pronounced reactive oxygen species bursts, transmitting immune signals to adjacent pavement cells via the apoplast. Notably, GCs are incompatible with adapted fungal pathogens and underwent hypersensitive cell death. Together, these findings uncover distinct immune programs among epidermal cell types, highlight GC-autonomous defense mechanisms, and provide a framework for understanding spatial immune coordination in plants.