TY - JOUR

T1 - Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens

AU - Rubiato, Hector M.

AU - Liu, Mengqi

AU - O'Connell, Richard J.

AU - Nielsen, Mads E.

PY - 2022

Y1 - 2022

N2 - 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.

AB - 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.

KW - M

KW - polymorpha

KW - B

KW - graminis hordei

KW - C

KW - destructivum

KW - P

KW - infestans

KW - innate immunity

KW - A

KW - thaliana

KW - Other

KW - NONHOST RESISTANCE

KW - POWDERY MILDEW

KW - PENETRATION RESISTANCE

KW - PHAKOPSORA-PACHYRHIZI

KW - CALLOSE DEPOSITION

KW - SNARE-PROTEIN

KW - PEN1 SYNTAXIN

KW - TIR DOMAINS

KW - CELL

KW - ARABIDOPSIS

U2 - 10.7554/eLife.73487

DO - 10.7554/eLife.73487

M3 - Journal article

C2 - 35119361

VL - 11

JO - eLife

JF - eLife

SN - 2050-084X

M1 - 73487

ER -