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

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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.

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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.

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Hector Rubiato Molinelli

Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark

Competing interests
The authors declare that no competing interests exist.
Mengqi Liu

Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark

Competing interests
The authors declare that no competing interests exist.
Richard J O'Connell

INRAE, Université Paris-Saclay, Thiverval-Grignon, France

Competing interests
The authors declare that no competing interests exist.
Mads Eggert Nielsen

Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark

For correspondence
maen@plen.ku.dk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6170-8836

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

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.