Co-option of a default secretory pathway for plant immune responses
Cell-autonomous immunity is widespread in plant-fungus interactions and terminates fungal pathogenesis either at the cell surface or after pathogen entry. Although post-invasive resistance responses typically coincide with a self-contained cell death of plant cells undergoing attack by parasites, th...
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| Veröffentlicht in: | Nature 2008-02, Vol.451 (7180), p.835-840 |
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| creator | Kwon, Chian Neu, Christina Pajonk, Simone Yun, Hye Sup Lipka, Ulrike Humphry, Matt Bau, Stefan Straus, Marco Kwaaitaal, Mark Rampelt, Heike |
| description | Cell-autonomous immunity is widespread in plant-fungus interactions and terminates fungal pathogenesis either at the cell surface or after pathogen entry. Although post-invasive resistance responses typically coincide with a self-contained cell death of plant cells undergoing attack by parasites, these cells survive pre-invasive defence. Mutational analysis in Arabidopsis identified PEN1 syntaxin as one component of two pre-invasive resistance pathways against ascomycete powdery mildew fungi. Here we show that plasma-membrane-resident PEN1 promiscuously forms SDS-resistant soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) complexes together with the SNAP33 adaptor and a subset of vesicle-associated membrane proteins (VAMPs). PEN1-dependent disease resistance acts in vivo mainly through two functionally redundant VAMP72 subfamily members, VAMP721 and VAMP722. Unexpectedly, the same two VAMP proteins also operate redundantly in a default secretory pathway, suggesting dual functions in separate biological processes owing to evolutionary co-option of the default pathway for plant immunity. The disease resistance function of the secretory PEN1-SNAP33-VAMP721/722 complex and the pathogen-induced subcellular dynamics of its components are mechanistically reminiscent of immunological synapse formation in vertebrates, enabling execution of immune responses through focal secretion. |
| doi_str_mv | 10.1038/nature06545 |
| format | Article |
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Although post-invasive resistance responses typically coincide with a self-contained cell death of plant cells undergoing attack by parasites, these cells survive pre-invasive defence. Mutational analysis in Arabidopsis identified PEN1 syntaxin as one component of two pre-invasive resistance pathways against ascomycete powdery mildew fungi. Here we show that plasma-membrane-resident PEN1 promiscuously forms SDS-resistant soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) complexes together with the SNAP33 adaptor and a subset of vesicle-associated membrane proteins (VAMPs). PEN1-dependent disease resistance acts in vivo mainly through two functionally redundant VAMP72 subfamily members, VAMP721 and VAMP722. Unexpectedly, the same two VAMP proteins also operate redundantly in a default secretory pathway, suggesting dual functions in separate biological processes owing to evolutionary co-option of the default pathway for plant immunity. The disease resistance function of the secretory PEN1-SNAP33-VAMP721/722 complex and the pathogen-induced subcellular dynamics of its components are mechanistically reminiscent of immunological synapse formation in vertebrates, enabling execution of immune responses through focal secretion.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>EISSN: 1476-4679</identifier><identifier>DOI: 10.1038/nature06545</identifier><identifier>PMID: 18273019</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Airborne microorganisms ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - immunology ; Arabidopsis - microbiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Ascomycetes ; Ascomycota - physiology ; ATP-Binding Cassette Transporters - genetics ; ATP-Binding Cassette Transporters - metabolism ; Disease ; Disease resistance ; Erysiphe graminis ; Erysiphe pisi ; Fungi ; Humanities and Social Sciences ; Immunology ; letter ; membrane proteins ; Membranes ; multidisciplinary ; Mutation ; N-Glycosyl Hydrolases - genetics ; N-Glycosyl Hydrolases - metabolism ; Parasites ; Pathogens ; PEN1 protein ; Plant diseases ; Plant pathology ; plant proteins ; Plant resistance ; plasma membrane ; powdery mildew ; Proteins ; Qa-SNARE Proteins - genetics ; Qa-SNARE Proteins - metabolism ; Science ; Science (multidisciplinary) ; SNARE proteins ; SNARE Proteins - genetics ; SNARE Proteins - metabolism ; Vertebrates ; vesicle-associated membrane proteins</subject><ispartof>Nature, 2008-02, Vol.451 (7180), p.835-840</ispartof><rights>Springer Nature Limited 2008</rights><rights>COPYRIGHT 2008 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Feb 14, 2008</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c678t-dcf276f21012d98977365f2215190f54f102996becf6e98677edf9ae2590ce3a3</citedby><cites>FETCH-LOGICAL-c678t-dcf276f21012d98977365f2215190f54f102996becf6e98677edf9ae2590ce3a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature06545$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature06545$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27903,27904,41467,42536,51297</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18273019$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kwon, Chian</creatorcontrib><creatorcontrib>Neu, Christina</creatorcontrib><creatorcontrib>Pajonk, Simone</creatorcontrib><creatorcontrib>Yun, Hye Sup</creatorcontrib><creatorcontrib>Lipka, Ulrike</creatorcontrib><creatorcontrib>Humphry, Matt</creatorcontrib><creatorcontrib>Bau, Stefan</creatorcontrib><creatorcontrib>Straus, Marco</creatorcontrib><creatorcontrib>Kwaaitaal, Mark</creatorcontrib><creatorcontrib>Rampelt, Heike</creatorcontrib><title>Co-option of a default secretory pathway for plant immune responses</title><title>Nature</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Cell-autonomous immunity is widespread in plant-fungus interactions and terminates fungal pathogenesis either at the cell surface or after pathogen entry. Although post-invasive resistance responses typically coincide with a self-contained cell death of plant cells undergoing attack by parasites, these cells survive pre-invasive defence. Mutational analysis in Arabidopsis identified PEN1 syntaxin as one component of two pre-invasive resistance pathways against ascomycete powdery mildew fungi. Here we show that plasma-membrane-resident PEN1 promiscuously forms SDS-resistant soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) complexes together with the SNAP33 adaptor and a subset of vesicle-associated membrane proteins (VAMPs). PEN1-dependent disease resistance acts in vivo mainly through two functionally redundant VAMP72 subfamily members, VAMP721 and VAMP722. Unexpectedly, the same two VAMP proteins also operate redundantly in a default secretory pathway, suggesting dual functions in separate biological processes owing to evolutionary co-option of the default pathway for plant immunity. The disease resistance function of the secretory PEN1-SNAP33-VAMP721/722 complex and the pathogen-induced subcellular dynamics of its components are mechanistically reminiscent of immunological synapse formation in vertebrates, enabling execution of immune responses through focal secretion.</description><subject>Airborne microorganisms</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - microbiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Ascomycetes</subject><subject>Ascomycota - physiology</subject><subject>ATP-Binding Cassette Transporters - genetics</subject><subject>ATP-Binding Cassette Transporters - metabolism</subject><subject>Disease</subject><subject>Disease resistance</subject><subject>Erysiphe graminis</subject><subject>Erysiphe pisi</subject><subject>Fungi</subject><subject>Humanities and Social Sciences</subject><subject>Immunology</subject><subject>letter</subject><subject>membrane proteins</subject><subject>Membranes</subject><subject>multidisciplinary</subject><subject>Mutation</subject><subject>N-Glycosyl Hydrolases - 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Although post-invasive resistance responses typically coincide with a self-contained cell death of plant cells undergoing attack by parasites, these cells survive pre-invasive defence. Mutational analysis in Arabidopsis identified PEN1 syntaxin as one component of two pre-invasive resistance pathways against ascomycete powdery mildew fungi. Here we show that plasma-membrane-resident PEN1 promiscuously forms SDS-resistant soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) complexes together with the SNAP33 adaptor and a subset of vesicle-associated membrane proteins (VAMPs). PEN1-dependent disease resistance acts in vivo mainly through two functionally redundant VAMP72 subfamily members, VAMP721 and VAMP722. Unexpectedly, the same two VAMP proteins also operate redundantly in a default secretory pathway, suggesting dual functions in separate biological processes owing to evolutionary co-option of the default pathway for plant immunity. The disease resistance function of the secretory PEN1-SNAP33-VAMP721/722 complex and the pathogen-induced subcellular dynamics of its components are mechanistically reminiscent of immunological synapse formation in vertebrates, enabling execution of immune responses through focal secretion.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>18273019</pmid><doi>10.1038/nature06545</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0028-0836 |
| ispartof | Nature, 2008-02, Vol.451 (7180), p.835-840 |
| issn | 0028-0836 1476-4687 1476-4679 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_864949678 |
| source | MEDLINE; SpringerLink Journals; Nature Journals Online |
| subjects | Airborne microorganisms Arabidopsis Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - microbiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Ascomycetes Ascomycota - physiology ATP-Binding Cassette Transporters - genetics ATP-Binding Cassette Transporters - metabolism Disease Disease resistance Erysiphe graminis Erysiphe pisi Fungi Humanities and Social Sciences Immunology letter membrane proteins Membranes multidisciplinary Mutation N-Glycosyl Hydrolases - genetics N-Glycosyl Hydrolases - metabolism Parasites Pathogens PEN1 protein Plant diseases Plant pathology plant proteins Plant resistance plasma membrane powdery mildew Proteins Qa-SNARE Proteins - genetics Qa-SNARE Proteins - metabolism Science Science (multidisciplinary) SNARE proteins SNARE Proteins - genetics SNARE Proteins - metabolism Vertebrates vesicle-associated membrane proteins |
| title | Co-option of a default secretory pathway for plant immune responses |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-25T07%3A46%3A28IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Co-option%20of%20a%20default%20secretory%20pathway%20for%20plant%20immune%20responses&rft.jtitle=Nature&rft.au=Kwon,%20Chian&rft.date=2008-02-14&rft.volume=451&rft.issue=7180&rft.spage=835&rft.epage=840&rft.pages=835-840&rft.issn=0028-0836&rft.eissn=1476-4687&rft.coden=NATUAS&rft_id=info:doi/10.1038/nature06545&rft_dat=%3Cgale_proqu%3EA189748318%3C/gale_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=204556101&rft_id=info:pmid/18273019&rft_galeid=A189748318&rfr_iscdi=true |