AbstractMany filamentous fungal and oomycete plant pathogens invade by direct penetration through the leaf epidermal cell wall and cause devastating plant diseases. In response to attack, plants form evolutionarily conserved cell autonomous defense structures, named papillae and encasements, that are thought to block pathogen ingress. Previously, the syntaxin PEN1 in Arabidopsis, like its orthologue ROR2 in barley, was found to mediate pre-invasive immunity towards powdery mildew fungi, where it assures the timely formation of papilla defense structures. However, this powdery mildew-specific function of PEN1 in papilla timing, thought to take place at the trans-Golgi network, does not explain how plants generally ward off other filamentous pathogens. In the present study, we found that PEN1 has a second function, shared with its closest homologue SYP122, in the formation of papillae, as well as encasements. This second function provides pre-invasive immunity towards highly diverse non-adapted filamentous pathogens, underlining the versatility and efficacy of these defense structures. PEN1 and SYP122 belong to the broadly conserved land plant syntaxin clade SYP12, suggested to function in specialized forms of polarized secretion. In support of this, complementation studies using SYP12s from the basal plant, Marchantia polymorpha, showed that the SYP12 clade immunity function has survived 450 My of independent evolution. As saprophytic filamentous land fungi predate plant terrestrialization, we suggest ancestral land plants evolved the SYP12 clade to provide a durable immunity to facilitate their life on land.