Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens
Abstract
Filamentous fungal and oomycete plant pathogens that invade by direct penetration through the leaf epidermal cell wall cause devastating plant diseases. Plant pre-invasive immunity towards non-adapted filamentous pathogens is highly effective and durable. Pre- and post-invasive 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 pre-invasive immunity towards a range of phylogenetically distant non-adapted 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 My of independent evolution. These results suggest that ancestral land plants evolved the SYP12 clade to provide a broad and durable pre-invasive 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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 3, 4, 5, 6 and 8.
Article and author information
Author details
Funding
the villum foundation (VKR023502)
- Mads Eggert Nielsen
independent research fund denmark, technical and production series (6111-00524B)
- Mads Eggert Nielsen
Novo Nordisk Fonden (NNF19OC0056457)
- Mads Eggert Nielsen
Agence Nationale de la Recherche (ANR-17-CAPS-0004-01)
- Richard J O'Connell
china scholarship council (No. 201906300075)
- Mengqi Liu
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2022, Molinelli et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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