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...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-02-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/73487 |
| _version_ | 1811201580039405568 |
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| author | Hector M Rubiato Mengqi Liu Richard J O'Connell Mads E Nielsen |
| author_facet | Hector M Rubiato Mengqi Liu Richard J O'Connell Mads E Nielsen |
| author_sort | Hector M Rubiato |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T02:24:02Z |
| format | Article |
| id | doaj.art-1922543209fa495f80b4ad0e1b2f3e59 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:24:02Z |
| publishDate | 2022-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-1922543209fa495f80b4ad0e1b2f3e592022-12-22T03:52:02ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.73487Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogensHector M Rubiato0Mengqi Liu1Richard J O'Connell2Mads E Nielsen3https://orcid.org/0000-0001-6170-8836University of Copenhagen, Faculty of Science, CPSC, Department of Plant and Environmental Sciences, Copenhagen, DenmarkUniversity of Copenhagen, Faculty of Science, CPSC, Department of Plant and Environmental Sciences, Copenhagen, DenmarkUniversity of Paris-Saclay, INRAE, UR BIOGER, Thiverval-Grignon, FranceUniversity of Copenhagen, Faculty of Science, CPSC, Department of Plant and Environmental Sciences, Copenhagen, DenmarkFilamentous 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.https://elifesciences.org/articles/73487M. polymorphaB. graminis hordeiC. destructivumP. infestansinnate immunity |
| spellingShingle | Hector M Rubiato Mengqi Liu Richard J O'Connell Mads E Nielsen Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens eLife M. polymorpha B. graminis hordei C. destructivum P. infestans innate immunity |
| title | Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens |
| title_full | Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens |
| title_fullStr | Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens |
| title_full_unstemmed | Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens |
| title_short | Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens |
| title_sort | plant syp12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens |
| topic | M. polymorpha B. graminis hordei C. destructivum P. infestans innate immunity |
| url | https://elifesciences.org/articles/73487 |
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