Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2
Resistance in tomato against race 1 strains of the fungal vascular wilt pathogens Verticillium dahliae and V. albo-atrum is mediated by the Ve locus. This locus comprises two closely linked inversely oriented genes, Ve1 and Ve2, which encode cell surface receptors of the extracellular leucine-rich r...
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| description | Resistance in tomato against race 1 strains of the fungal vascular wilt pathogens Verticillium dahliae and V. albo-atrum is mediated by the Ve locus. This locus comprises two closely linked inversely oriented genes, Ve1 and Ve2, which encode cell surface receptors of the extracellular leucine-rich repeat receptor-like protein (eLRR-RLP) type. While Ve1 mediates Verticillium resistance through monitoring the presence of the recently identified V. dahliae Ave1 effector, no functionality for Ve2 has been demonstrated in tomato. Ve1 and Ve2 contain 37 eLRRs and share 84% amino acid identity, facilitating investigation of Ve protein functionality through domain swapping. In this study it is shown that Ve chimeras in which the first thirty eLRRs of Ve1 were replaced by those of Ve2 remain able to induce HR and activate Verticillium resistance, and that deletion of these thirty eLRRs from Ve1 resulted in loss of functionality. Also the region between eLRR30 and eLRR35 is required for Ve1-mediated resistance, and cannot be replaced by the region between eLRR30 and eLRR35 of Ve2. We furthermore show that the cytoplasmic tail of Ve1 is required for functionality, as truncation of this tail results in loss of functionality. Moreover, the C-terminus of Ve2 fails to activate immune signaling as chimeras containing the C-terminus of Ve2 do not provide Verticillium resistance. Furthermore, Ve1 was found to interact through its C-terminus with the eLRR-containing receptor-like kinase (eLRR-RLK) interactor SOBIR1 that was recently identified as an interactor of eLRR-RLP (immune) receptors. Intriguingly, also Ve2 was found to interact with SOBIR1. |
| doi_str_mv | 10.1371/journal.pone.0088208 |
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This locus comprises two closely linked inversely oriented genes, Ve1 and Ve2, which encode cell surface receptors of the extracellular leucine-rich repeat receptor-like protein (eLRR-RLP) type. While Ve1 mediates Verticillium resistance through monitoring the presence of the recently identified V. dahliae Ave1 effector, no functionality for Ve2 has been demonstrated in tomato. Ve1 and Ve2 contain 37 eLRRs and share 84% amino acid identity, facilitating investigation of Ve protein functionality through domain swapping. In this study it is shown that Ve chimeras in which the first thirty eLRRs of Ve1 were replaced by those of Ve2 remain able to induce HR and activate Verticillium resistance, and that deletion of these thirty eLRRs from Ve1 resulted in loss of functionality. Also the region between eLRR30 and eLRR35 is required for Ve1-mediated resistance, and cannot be replaced by the region between eLRR30 and eLRR35 of Ve2. We furthermore show that the cytoplasmic tail of Ve1 is required for functionality, as truncation of this tail results in loss of functionality. Moreover, the C-terminus of Ve2 fails to activate immune signaling as chimeras containing the C-terminus of Ve2 do not provide Verticillium resistance. Furthermore, Ve1 was found to interact through its C-terminus with the eLRR-containing receptor-like kinase (eLRR-RLK) interactor SOBIR1 that was recently identified as an interactor of eLRR-RLP (immune) receptors. Intriguingly, also Ve2 was found to interact with SOBIR1.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0088208</identifier><identifier>PMID: 24505431</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agriculture ; Amino Acid Sequence ; Amino acids ; Analysis ; arabidopsis-thaliana ; Biology ; C-Terminus ; Cell surface ; Chimeras ; cladosporium-fulvum ; Clonal deletion ; Cloning ; disease resistance protein ; Endoplasmic reticulum ; Functional analysis ; Gangrene ; Gene Deletion ; Gene Expression Regulation, Plant ; Genetic aspects ; Genomics ; Homology ; Host-Pathogen Interactions ; hypersensitive response ; innate immunity ; kinase bri1 ; Kinases ; Laboratories ; Leucine ; leucine-rich repeat ; Ligands ; Microbial drug resistance ; Molecular Sequence Data ; Peptides ; Plant Diseases - immunology ; Plant Diseases - microbiology ; Plant Proteins - chemistry ; Plant Proteins - genetics ; Plant Proteins - immunology ; plasma-membrane ; Protein Structure, Tertiary ; Proteins ; Receptors ; Receptors, Cell Surface - chemistry ; Receptors, Cell Surface - genetics ; Receptors, Cell Surface - immunology ; Receptors, Immunologic - chemistry ; Receptors, Immunologic - genetics ; Receptors, Immunologic - immunology ; Signal transduction ; Signaling ; Solanum lycopersicum - genetics ; Solanum lycopersicum - immunology ; Solanum lycopersicum - microbiology ; Swaps (Finance) ; Tobacco ; Tomatoes ; Verticillium - physiology ; Verticillium dahliae ; verticillium resistance ; Wilt</subject><ispartof>PloS one, 2014-02, Vol.9 (2), p.e88208</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Fradin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Fradin et al 2014 Fradin et al</rights><rights>Wageningen University & Research</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c743t-a9b6537e1b18677d068823eb56d73dd6b59054252a6bd6cca12b4e46acf7dd5d3</citedby><cites>FETCH-LOGICAL-c743t-a9b6537e1b18677d068823eb56d73dd6b59054252a6bd6cca12b4e46acf7dd5d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3914901/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3914901/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24505431$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Arnold, Dawn</contributor><creatorcontrib>Fradin, Emilie F</creatorcontrib><creatorcontrib>Zhang, Zhao</creatorcontrib><creatorcontrib>Rovenich, Hanna</creatorcontrib><creatorcontrib>Song, Yin</creatorcontrib><creatorcontrib>Liebrand, Thomas W H</creatorcontrib><creatorcontrib>Masini, Laura</creatorcontrib><creatorcontrib>van den Berg, Grardy C M</creatorcontrib><creatorcontrib>Joosten, Matthieu H A J</creatorcontrib><creatorcontrib>Thomma, Bart P H J</creatorcontrib><title>Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Resistance in tomato against race 1 strains of the fungal vascular wilt pathogens Verticillium dahliae and V. albo-atrum is mediated by the Ve locus. This locus comprises two closely linked inversely oriented genes, Ve1 and Ve2, which encode cell surface receptors of the extracellular leucine-rich repeat receptor-like protein (eLRR-RLP) type. While Ve1 mediates Verticillium resistance through monitoring the presence of the recently identified V. dahliae Ave1 effector, no functionality for Ve2 has been demonstrated in tomato. Ve1 and Ve2 contain 37 eLRRs and share 84% amino acid identity, facilitating investigation of Ve protein functionality through domain swapping. In this study it is shown that Ve chimeras in which the first thirty eLRRs of Ve1 were replaced by those of Ve2 remain able to induce HR and activate Verticillium resistance, and that deletion of these thirty eLRRs from Ve1 resulted in loss of functionality. Also the region between eLRR30 and eLRR35 is required for Ve1-mediated resistance, and cannot be replaced by the region between eLRR30 and eLRR35 of Ve2. We furthermore show that the cytoplasmic tail of Ve1 is required for functionality, as truncation of this tail results in loss of functionality. Moreover, the C-terminus of Ve2 fails to activate immune signaling as chimeras containing the C-terminus of Ve2 do not provide Verticillium resistance. Furthermore, Ve1 was found to interact through its C-terminus with the eLRR-containing receptor-like kinase (eLRR-RLK) interactor SOBIR1 that was recently identified as an interactor of eLRR-RLP (immune) receptors. Intriguingly, also Ve2 was found to interact with SOBIR1.</description><subject>Agriculture</subject><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Analysis</subject><subject>arabidopsis-thaliana</subject><subject>Biology</subject><subject>C-Terminus</subject><subject>Cell surface</subject><subject>Chimeras</subject><subject>cladosporium-fulvum</subject><subject>Clonal deletion</subject><subject>Cloning</subject><subject>disease resistance protein</subject><subject>Endoplasmic reticulum</subject><subject>Functional analysis</subject><subject>Gangrene</subject><subject>Gene Deletion</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetic aspects</subject><subject>Genomics</subject><subject>Homology</subject><subject>Host-Pathogen Interactions</subject><subject>hypersensitive response</subject><subject>innate immunity</subject><subject>kinase bri1</subject><subject>Kinases</subject><subject>Laboratories</subject><subject>Leucine</subject><subject>leucine-rich repeat</subject><subject>Ligands</subject><subject>Microbial drug resistance</subject><subject>Molecular Sequence Data</subject><subject>Peptides</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Proteins - chemistry</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - immunology</subject><subject>plasma-membrane</subject><subject>Protein Structure, Tertiary</subject><subject>Proteins</subject><subject>Receptors</subject><subject>Receptors, Cell Surface - chemistry</subject><subject>Receptors, Cell Surface - genetics</subject><subject>Receptors, Cell Surface - immunology</subject><subject>Receptors, Immunologic - chemistry</subject><subject>Receptors, Immunologic - genetics</subject><subject>Receptors, Immunologic - immunology</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>Solanum lycopersicum - genetics</subject><subject>Solanum lycopersicum - immunology</subject><subject>Solanum lycopersicum - microbiology</subject><subject>Swaps (Finance)</subject><subject>Tobacco</subject><subject>Tomatoes</subject><subject>Verticillium - physiology</subject><subject>Verticillium dahliae</subject><subject>verticillium resistance</subject><subject>Wilt</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk29r1TAUxosobk6_gWhBEH1xr0mTJq0vhDGcXhgM_LO3IU3SNpc26ZLU67696W43b2UvpJCE5Pc8PeckJ0leQrCGiMIPWzs6w7v1YI1aA1AUGSgeJcewRNmKZAA9PlgfJc-83wKQo4KQp8lRhnOQYwSPE3M-GhG0jU4pj8ON1z61dRpalQbb82BT3fejUalTQg3BuvRKwXjs7Ni0qYyINqnf8cGnOx3aVAefGmtW9V_f1va2s00UZs-TJzXvvHoxzyfJz_PPP86-ri4uv2zOTi9WgmIUVrysSI6oghUsCKUSkJgeUlVOJEVSkiovY_xZnnFSSSIEh1mFFSZc1FTKXKKT5PXed-isZ3OpPINlgXCW5QREYrMnpOVbNjjdc3fDLNfsdsO6hnEXtOgU41yWAlAi6kpiUKESKqQKBKAQROSwil4f91473iijTRyY4U5of2vY6cpN5rvRMdNN0zBWnmFKiwxG8ac51LHqlRTKBMe7RUTLE6Nb1thfLMaBSzAZvJsNnL0elQ-s116oruNG2TEmjcsSIoxKGtE3_6APl2amGh6z16a28b9iMmWnmMaboBTiSK0foOInVa9FfJS1jvsLwfuFIDJB_Q4NH71nm-_f_p-9vFqybw_YVvEutN524_T6_BLEe1A4671T9X2RIWBTT91Vg009xeaeirJXhxd0L7prIvQHM7YfCw</recordid><startdate>20140205</startdate><enddate>20140205</enddate><creator>Fradin, 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Cell Surface - immunology</topic><topic>Receptors, Immunologic - chemistry</topic><topic>Receptors, Immunologic - genetics</topic><topic>Receptors, Immunologic - immunology</topic><topic>Signal transduction</topic><topic>Signaling</topic><topic>Solanum lycopersicum - genetics</topic><topic>Solanum lycopersicum - immunology</topic><topic>Solanum lycopersicum - microbiology</topic><topic>Swaps (Finance)</topic><topic>Tobacco</topic><topic>Tomatoes</topic><topic>Verticillium - physiology</topic><topic>Verticillium dahliae</topic><topic>verticillium resistance</topic><topic>Wilt</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fradin, Emilie F</creatorcontrib><creatorcontrib>Zhang, Zhao</creatorcontrib><creatorcontrib>Rovenich, Hanna</creatorcontrib><creatorcontrib>Song, Yin</creatorcontrib><creatorcontrib>Liebrand, Thomas W H</creatorcontrib><creatorcontrib>Masini, Laura</creatorcontrib><creatorcontrib>van den Berg, Grardy C 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Emilie F</au><au>Zhang, Zhao</au><au>Rovenich, Hanna</au><au>Song, Yin</au><au>Liebrand, Thomas W H</au><au>Masini, Laura</au><au>van den Berg, Grardy C M</au><au>Joosten, Matthieu H A J</au><au>Thomma, Bart P H J</au><au>Arnold, Dawn</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-02-05</date><risdate>2014</risdate><volume>9</volume><issue>2</issue><spage>e88208</spage><pages>e88208-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Resistance in tomato against race 1 strains of the fungal vascular wilt pathogens Verticillium dahliae and V. albo-atrum is mediated by the Ve locus. This locus comprises two closely linked inversely oriented genes, Ve1 and Ve2, which encode cell surface receptors of the extracellular leucine-rich repeat receptor-like protein (eLRR-RLP) type. While Ve1 mediates Verticillium resistance through monitoring the presence of the recently identified V. dahliae Ave1 effector, no functionality for Ve2 has been demonstrated in tomato. Ve1 and Ve2 contain 37 eLRRs and share 84% amino acid identity, facilitating investigation of Ve protein functionality through domain swapping. In this study it is shown that Ve chimeras in which the first thirty eLRRs of Ve1 were replaced by those of Ve2 remain able to induce HR and activate Verticillium resistance, and that deletion of these thirty eLRRs from Ve1 resulted in loss of functionality. Also the region between eLRR30 and eLRR35 is required for Ve1-mediated resistance, and cannot be replaced by the region between eLRR30 and eLRR35 of Ve2. We furthermore show that the cytoplasmic tail of Ve1 is required for functionality, as truncation of this tail results in loss of functionality. Moreover, the C-terminus of Ve2 fails to activate immune signaling as chimeras containing the C-terminus of Ve2 do not provide Verticillium resistance. Furthermore, Ve1 was found to interact through its C-terminus with the eLRR-containing receptor-like kinase (eLRR-RLK) interactor SOBIR1 that was recently identified as an interactor of eLRR-RLP (immune) receptors. Intriguingly, also Ve2 was found to interact with SOBIR1.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24505431</pmid><doi>10.1371/journal.pone.0088208</doi><tpages>e88208</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2014-02, Vol.9 (2), p.e88208 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1983422560 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Agriculture Amino Acid Sequence Amino acids Analysis arabidopsis-thaliana Biology C-Terminus Cell surface Chimeras cladosporium-fulvum Clonal deletion Cloning disease resistance protein Endoplasmic reticulum Functional analysis Gangrene Gene Deletion Gene Expression Regulation, Plant Genetic aspects Genomics Homology Host-Pathogen Interactions hypersensitive response innate immunity kinase bri1 Kinases Laboratories Leucine leucine-rich repeat Ligands Microbial drug resistance Molecular Sequence Data Peptides Plant Diseases - immunology Plant Diseases - microbiology Plant Proteins - chemistry Plant Proteins - genetics Plant Proteins - immunology plasma-membrane Protein Structure, Tertiary Proteins Receptors Receptors, Cell Surface - chemistry Receptors, Cell Surface - genetics Receptors, Cell Surface - immunology Receptors, Immunologic - chemistry Receptors, Immunologic - genetics Receptors, Immunologic - immunology Signal transduction Signaling Solanum lycopersicum - genetics Solanum lycopersicum - immunology Solanum lycopersicum - microbiology Swaps (Finance) Tobacco Tomatoes Verticillium - physiology Verticillium dahliae verticillium resistance Wilt |
| title | Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2 |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-19T19%3A03%3A43IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Functional%20analysis%20of%20the%20tomato%20immune%20receptor%20Ve1%20through%20domain%20swaps%20with%20its%20non-functional%20homolog%20Ve2&rft.jtitle=PloS%20one&rft.au=Fradin,%20Emilie%20F&rft.date=2014-02-05&rft.volume=9&rft.issue=2&rft.spage=e88208&rft.pages=e88208-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0088208&rft_dat=%3Cgale_plos_%3EA478827714%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1983422560&rft_id=info:pmid/24505431&rft_galeid=A478827714&rft_doaj_id=oai_doaj_org_article_aad9c076cfbd40b391e3e8301cc6c51b&rfr_iscdi=true |