Mobility of the syntaxin PEN1 in Arabidopsis reflects functional specialization of the conserved SYP12 clade.

Plant innate immunity toward cell-wall penetrating filamentous pathogens relies on the conserved SYP12 clade of secretory syntaxins. In Arabidopsis, the two closely related SYP12 clade members, PEN1 and SYP122, play an overlapping role in this general immunity, which can be complemented by two SYP12 clade members from Marchantia (MpSYP12A and MpSYP12B). However, in addition to the conserved SYP12 clade function, PEN1 alone mediates pre-invasive immunity toward powdery mildew fungi, which likely reflects a specialization of its functionality. Here, we show that the PEN1-specific specialization in immunity correlates with a continuous BFA-sensitive recycling and the ability to accumulate strongly at the growing cell plate. This contrasts with the behavior of SYP122, MpSYP12A, and MpSYP12B, all being more stable at the plasma membrane. We suggest that the highly mobile SYP12 specialization observed for PEN1 is required for a fast pre-invasive immune response to resist attack from powdery mildew fungi.

Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens.

Filamentous fungal and oomycete plant pathogens that invade by direct penetration through the leaf epidermal cell wall cause devastating plant diseases. Plant preinvasive immunity toward nonadapted filamentous pathogens is highly effective and durable. Pre- and postinvasive immunity correlates with the formation of evolutionarily conserved and cell-autonomous cell wall structures, named papillae and encasements, respectively. Yet, it is still unresolved how papillae/encasements are formed and whether these defense structures prevent pathogen ingress. Here, we show that in Arabidopsis the two closely related members of the SYP12 clade of syntaxins (PEN1 and SYP122) are indispensable for the formation of papillae and encasements. Moreover, loss-of-function mutants were hampered in preinvasive immunity toward a range of phylogenetically distant nonadapted filamentous pathogens, underlining the versatility and efficacy of this defense. Complementation studies using SYP12s from the early diverging land plant, Marchantia polymorpha, showed that the SYP12 clade immunity function has survived 470 million years of independent evolution. These results suggest that ancestral land plants evolved the SYP12 clade to provide a broad and durable preinvasive immunity to facilitate their life on land and pave the way to a better understanding of how adapted pathogens overcome this ubiquitous plant defense strategy.