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.

Automated summary

Filamentous fungal and oomycete plant pathogens that penetrate the leaf cell wall cause severe plant diseases. Plant preinvasive immunity, represented by the formation of papillae and encasements, is effective in preventing pathogen ingress. The SYP12 clade members, PEN1 and SYP122, are essential for the formation of papillae and encasements in Arabidopsis. Loss-of-function mutants show compromised preinvasive immunity against diverse filamentous pathogens. Complementation studies using SYP12s from Marchantia polymorpha confirm the evolutionary conservation of the SYP12 clade immunity function. These findings shed light on the ancient plant defense mechanism and its interaction with adapted pathogens.