The NLR-Annotator Tool Enables Annotation of the Intracellular Immune Receptor Repertoire.
Identifieur interne : 000033 ( Main/Exploration ); précédent : 000032; suivant : 000034The NLR-Annotator Tool Enables Annotation of the Intracellular Immune Receptor Repertoire.
Auteurs : Burkhard Steuernagel [Royaume-Uni] ; Kamil Witek [Royaume-Uni] ; Simon G. Krattinger [Suisse] ; Ricardo H. Ramirez-Gonzalez [Royaume-Uni] ; Henk-Jan Schoonbeek [Royaume-Uni] ; Guotai Yu [Royaume-Uni] ; Erin Baggs [Royaume-Uni] ; Agnieszka I. Witek [Royaume-Uni] ; Inderjit Yadav [Inde] ; Ksenia V. Krasileva [Royaume-Uni] ; Jonathan D G. Jones [Royaume-Uni] ; Cristobal Uauy [Royaume-Uni] ; Beat Keller [Suisse] ; Christopher J. Ridout [Royaume-Uni] ; Brande B H. Wulff [Royaume-Uni]Source :
- Plant physiology [ 1532-2548 ] ; 2020.
Abstract
Disease resistance genes encoding nucleotide-binding and leucine-rich repeat (NLR) intracellular immune receptor proteins detect pathogens by the presence of pathogen effectors. Plant genomes typically contain hundreds of NLR-encoding genes. The availability of the hexaploid wheat (Triticum aestivum) cultivar Chinese Spring reference genome allows a detailed study of its NLR complement. However, low NLR expression and high intrafamily sequence homology hinder their accurate annotation. Here, we developed NLR-Annotator, a software tool for in silico NLR identification independent of transcript support. Although developed for wheat, we demonstrate the universal applicability of NLR-Annotator across diverse plant taxa. We applied our tool to wheat and combined it with a transcript-validated subset of genes from the reference gene annotation to characterize the structure, phylogeny, and expression profile of the NLR gene family. We detected 3,400 full-length NLR loci, of which 1,560 were confirmed as expressed genes with intact open reading frames. NLRs with integrated domains mostly group in specific subclades. Members of another subclade predominantly locate in close physical proximity to NLRs carrying integrated domains, suggesting a paired helper function. Most NLRs (88%) display low basal expression (in the lower 10 percentile of transcripts). In young leaves subjected to biotic stress, we found up-regulation of 266 of the NLRs To illustrate the utility of our tool for the positional cloning of resistance genes, we estimated the number of NLR genes within the intervals of mapped rust resistance genes. Our study will support the identification of functional resistance genes in wheat to accelerate the breeding and engineering of disease-resistant varieties.
DOI: 10.1104/pp.19.01273
PubMed: 32184345
PubMed Central: PMC7271791
Affiliations:
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Krattinger</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant and Microbial Biology, University of Zurich, 8008 Zurich, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Plant and Microbial Biology, University of Zurich, 8008 Zurich</wicri:regionArea><orgName type="university">Université de Zurich</orgName><placeName><settlement type="city">Zurich</settlement><region nuts="3" type="region">Canton de Zurich</region></placeName></affiliation><affiliation><nlm:affiliation>King Abdullah University of Science and Technology, Biological and Environmental Science and Engineering Division, Thuwal 23955-6900, Kingdom of Saudi Arabia.</nlm:affiliation><wicri:noCountry code="subField">Kingdom of Saudi Arabia</wicri:noCountry></affiliation></author><author><name sortKey="Ramirez Gonzalez, Ricardo H" sort="Ramirez Gonzalez, Ricardo H" uniqKey="Ramirez Gonzalez R" first="Ricardo H" last="Ramirez-Gonzalez">Ricardo H. Ramirez-Gonzalez</name><affiliation wicri:level="1"><nlm:affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Schoonbeek, Henk Jan" sort="Schoonbeek, Henk Jan" uniqKey="Schoonbeek H" first="Henk-Jan" last="Schoonbeek">Henk-Jan Schoonbeek</name><affiliation wicri:level="1"><nlm:affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Yu, Guotai" sort="Yu, Guotai" uniqKey="Yu G" first="Guotai" last="Yu">Guotai Yu</name><affiliation wicri:level="1"><nlm:affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Baggs, Erin" sort="Baggs, Erin" uniqKey="Baggs E" first="Erin" last="Baggs">Erin Baggs</name><affiliation wicri:level="1"><nlm:affiliation>Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ</wicri:regionArea><wicri:noRegion>NR4 7UZ</wicri:noRegion></affiliation></author><author><name sortKey="Witek, Agnieszka I" sort="Witek, Agnieszka I" uniqKey="Witek A" first="Agnieszka I" last="Witek">Agnieszka I. Witek</name><affiliation wicri:level="1"><nlm:affiliation>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Yadav, Inderjit" sort="Yadav, Inderjit" uniqKey="Yadav I" first="Inderjit" last="Yadav">Inderjit Yadav</name><affiliation wicri:level="1"><nlm:affiliation>School of Agricultural Biotechnology, Dr. G.S. Khush Laboratories, Punjab Agricultural University, Ludhiana-141 004, Punjab, India.</nlm:affiliation><country xml:lang="fr">Inde</country><wicri:regionArea>School of Agricultural Biotechnology, Dr. G.S. Khush Laboratories, Punjab Agricultural University, Ludhiana-141 004, Punjab</wicri:regionArea><wicri:noRegion>Punjab</wicri:noRegion></affiliation></author><author><name sortKey="Krasileva, Ksenia V" sort="Krasileva, Ksenia V" uniqKey="Krasileva K" first="Ksenia V" last="Krasileva">Ksenia V. Krasileva</name><affiliation wicri:level="1"><nlm:affiliation>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ</wicri:regionArea><wicri:noRegion>NR4 7UZ</wicri:noRegion></affiliation></author><author><name sortKey="Jones, Jonathan D G" sort="Jones, Jonathan D G" uniqKey="Jones J" first="Jonathan D G" last="Jones">Jonathan D G. Jones</name><affiliation wicri:level="1"><nlm:affiliation>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Uauy, Cristobal" sort="Uauy, Cristobal" uniqKey="Uauy C" first="Cristobal" last="Uauy">Cristobal Uauy</name><affiliation wicri:level="1"><nlm:affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Keller, Beat" sort="Keller, Beat" uniqKey="Keller B" first="Beat" last="Keller">Beat Keller</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant and Microbial Biology, University of Zurich, 8008 Zurich, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Plant and Microbial Biology, University of Zurich, 8008 Zurich</wicri:regionArea><orgName type="university">Université de Zurich</orgName><placeName><settlement type="city">Zurich</settlement><region nuts="3" type="region">Canton de Zurich</region></placeName></affiliation></author><author><name sortKey="Ridout, Christopher J" sort="Ridout, Christopher J" uniqKey="Ridout C" first="Christopher J" last="Ridout">Christopher J. Ridout</name><affiliation wicri:level="1"><nlm:affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Wulff, Brande B H" sort="Wulff, Brande B H" uniqKey="Wulff B" first="Brande B H" last="Wulff">Brande B H. Wulff</name><affiliation wicri:level="1"><nlm:affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom brande.wulff@jic.ac.uk.</nlm:affiliation><country wicri:rule="url">Royaume-Uni</country><wicri:regionArea>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author></analytic><series><title level="j">Plant physiology</title><idno type="eISSN">1532-2548</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Disease resistance genes encoding nucleotide-binding and leucine-rich repeat (NLR) intracellular immune receptor proteins detect pathogens by the presence of pathogen effectors. Plant genomes typically contain hundreds of NLR-encoding genes. The availability of the hexaploid wheat (<i>Triticum aestivum</i>) cultivar Chinese Spring reference genome allows a detailed study of its NLR complement. However, low <i>NLR</i> expression and high intrafamily sequence homology hinder their accurate annotation. Here, we developed NLR-Annotator, a software tool for in silico NLR identification independent of transcript support. Although developed for wheat, we demonstrate the universal applicability of NLR-Annotator across diverse plant taxa. We applied our tool to wheat and combined it with a transcript-validated subset of genes from the reference gene annotation to characterize the structure, phylogeny, and expression profile of the <i>NLR</i> gene family. We detected 3,400 full-length NLR loci, of which 1,560 were confirmed as expressed genes with intact open reading frames. NLRs with integrated domains mostly group in specific subclades. Members of another subclade predominantly locate in close physical proximity to NLRs carrying integrated domains, suggesting a paired helper function. Most <i>NLRs</i> (88%) display low basal expression (in the lower 10 percentile of transcripts). In young leaves subjected to biotic stress, we found up-regulation of 266 of the <i>NLRs</i> To illustrate the utility of our tool for the positional cloning of resistance genes, we estimated the number of <i>NLR</i> genes within the intervals of mapped rust resistance genes. Our study will support the identification of functional resistance genes in wheat to accelerate the breeding and engineering of disease-resistant varieties.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32184345</PMID><DateRevised><Year>2020</Year><Month>07</Month><Day>16</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-2548</ISSN><JournalIssue CitedMedium="Internet"><Volume>183</Volume><Issue>2</Issue><PubDate><Year>2020</Year><Month>06</Month></PubDate></JournalIssue><Title>Plant physiology</Title><ISOAbbreviation>Plant Physiol</ISOAbbreviation></Journal><ArticleTitle>The NLR-Annotator Tool Enables Annotation of the Intracellular Immune Receptor Repertoire.</ArticleTitle><Pagination><MedlinePgn>468-482</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.19.01273</ELocationID><Abstract><AbstractText>Disease resistance genes encoding nucleotide-binding and leucine-rich repeat (NLR) intracellular immune receptor proteins detect pathogens by the presence of pathogen effectors. Plant genomes typically contain hundreds of NLR-encoding genes. The availability of the hexaploid wheat (<i>Triticum aestivum</i>) cultivar Chinese Spring reference genome allows a detailed study of its NLR complement. However, low <i>NLR</i> expression and high intrafamily sequence homology hinder their accurate annotation. Here, we developed NLR-Annotator, a software tool for in silico NLR identification independent of transcript support. Although developed for wheat, we demonstrate the universal applicability of NLR-Annotator across diverse plant taxa. We applied our tool to wheat and combined it with a transcript-validated subset of genes from the reference gene annotation to characterize the structure, phylogeny, and expression profile of the <i>NLR</i> gene family. We detected 3,400 full-length NLR loci, of which 1,560 were confirmed as expressed genes with intact open reading frames. NLRs with integrated domains mostly group in specific subclades. Members of another subclade predominantly locate in close physical proximity to NLRs carrying integrated domains, suggesting a paired helper function. Most <i>NLRs</i> (88%) display low basal expression (in the lower 10 percentile of transcripts). In young leaves subjected to biotic stress, we found up-regulation of 266 of the <i>NLRs</i> To illustrate the utility of our tool for the positional cloning of resistance genes, we estimated the number of <i>NLR</i> genes within the intervals of mapped rust resistance genes. Our study will support the identification of functional resistance genes in wheat to accelerate the breeding and engineering of disease-resistant varieties.</AbstractText><CopyrightInformation>© 2020 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Steuernagel</LastName><ForeName>Burkhard</ForeName><Initials>B</Initials><Identifier Source="ORCID">0000-0002-8284-7728</Identifier><AffiliationInfo><Affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Witek</LastName><ForeName>Kamil</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0003-0659-5562</Identifier><AffiliationInfo><Affiliation>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Krattinger</LastName><ForeName>Simon G</ForeName><Initials>SG</Initials><Identifier Source="ORCID">0000-0001-6912-7411</Identifier><AffiliationInfo><Affiliation>Department of Plant and Microbial Biology, University of Zurich, 8008 Zurich, Switzerland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>King Abdullah University of Science and Technology, Biological and Environmental Science and Engineering Division, Thuwal 23955-6900, Kingdom of Saudi Arabia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ramirez-Gonzalez</LastName><ForeName>Ricardo H</ForeName><Initials>RH</Initials><Identifier Source="ORCID">0000-0001-5745-7085</Identifier><AffiliationInfo><Affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schoonbeek</LastName><ForeName>Henk-Jan</ForeName><Initials>HJ</Initials><Identifier Source="ORCID">0000-0002-1087-2553</Identifier><AffiliationInfo><Affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yu</LastName><ForeName>Guotai</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baggs</LastName><ForeName>Erin</ForeName><Initials>E</Initials><Identifier Source="ORCID">0000-0003-3076-9489</Identifier><AffiliationInfo><Affiliation>Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Witek</LastName><ForeName>Agnieszka I</ForeName><Initials>AI</Initials><Identifier Source="ORCID">0000-0001-7395-687X</Identifier><AffiliationInfo><Affiliation>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yadav</LastName><ForeName>Inderjit</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>School of Agricultural Biotechnology, Dr. G.S. Khush Laboratories, Punjab Agricultural University, Ludhiana-141 004, Punjab, India.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Krasileva</LastName><ForeName>Ksenia V</ForeName><Initials>KV</Initials><Identifier Source="ORCID">0000-0002-1679-0700</Identifier><AffiliationInfo><Affiliation>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jones</LastName><ForeName>Jonathan D G</ForeName><Initials>JDG</Initials><Identifier Source="ORCID">0000-0002-4953-261X</Identifier><AffiliationInfo><Affiliation>Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Uauy</LastName><ForeName>Cristobal</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-9814-1770</Identifier><AffiliationInfo><Affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Keller</LastName><ForeName>Beat</ForeName><Initials>B</Initials><Identifier Source="ORCID">0000-0003-2379-9225</Identifier><AffiliationInfo><Affiliation>Department of Plant and Microbial Biology, University of Zurich, 8008 Zurich, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ridout</LastName><ForeName>Christopher J</ForeName><Initials>CJ</Initials><Identifier Source="ORCID">0000-0001-9287-938X</Identifier><AffiliationInfo><Affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wulff</LastName><ForeName>Brande B H</ForeName><Initials>BBH</Initials><Identifier Source="ORCID">0000-0003-4044-4346</Identifier><AffiliationInfo><Affiliation>John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom brande.wulff@jic.ac.uk.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>BB/L011794/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/G024960/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/M011216/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID> BB/P016855/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/P012574/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>03</Month><Day>17</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Plant Physiol</MedlineTA><NlmUniqueID>0401224</NlmUniqueID><ISSNLinking>0032-0889</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Plant Physiol. 2020 Jun;183(2):418-420</RefSource><PMID Version="1">32493798</PMID></CommentsCorrections></CommentsCorrectionsList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>10</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>03</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32184345</ArticleId><ArticleId IdType="pii">pp.19.01273</ArticleId><ArticleId IdType="doi">10.1104/pp.19.01273</ArticleId><ArticleId IdType="pmc">PMC7271791</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Genome Biol. 2015 Jan 31;16:26</Citation><ArticleIdList><ArticleId IdType="pubmed">25637298</ArticleId></ArticleIdList></Reference><Reference><Citation>Gene. 1995 Dec 29;167(1-2):GC1-10</Citation><ArticleIdList><ArticleId IdType="pubmed">8566757</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2017 Mar 15;543(7645):346-354</Citation><ArticleIdList><ArticleId IdType="pubmed">28300107</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2017 Jul 7;357(6346):93-97</Citation><ArticleIdList><ArticleId IdType="pubmed">28684525</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2012 May 30;485(7400):635-41</Citation><ArticleIdList><ArticleId IdType="pubmed">22660326</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant Microbe Interact. 2008 Dec;21(12):1635-42</Citation><ArticleIdList><ArticleId IdType="pubmed">18986259</ArticleId></ArticleIdList></Reference><Reference><Citation>Genome Biol. 2018 Feb 19;19(1):23</Citation><ArticleIdList><ArticleId IdType="pubmed">29458393</ArticleId></ArticleIdList></Reference><Reference><Citation>Bioinformatics. 1998;14(1):48-54</Citation><ArticleIdList><ArticleId IdType="pubmed">9520501</ArticleId></ArticleIdList></Reference><Reference><Citation>Genome Res. 2017 May;27(5):885-896</Citation><ArticleIdList><ArticleId IdType="pubmed">28420692</ArticleId></ArticleIdList></Reference><Reference><Citation>Genetics. 2009 Dec;183(4):1227-34</Citation><ArticleIdList><ArticleId IdType="pubmed">19797048</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 1999 Nov;20(3):317-32</Citation><ArticleIdList><ArticleId IdType="pubmed">10571892</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2013 Aug 16;341(6147):746-51</Citation><ArticleIdList><ArticleId IdType="pubmed">23950531</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Plants. 2017 Dec;3(12):946-955</Citation><ArticleIdList><ArticleId IdType="pubmed">29158546</ArticleId></ArticleIdList></Reference><Reference><Citation>Nucleic Acids Res. 2016 Jul 8;44(W1):W242-5</Citation><ArticleIdList><ArticleId IdType="pubmed">27095192</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2018 Feb;30(2):285-299</Citation><ArticleIdList><ArticleId IdType="pubmed">29382771</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Pathol J. 2017 Apr;33(2):103-108</Citation><ArticleIdList><ArticleId IdType="pubmed">28381956</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2015 Apr;206(2):606-13</Citation><ArticleIdList><ArticleId IdType="pubmed">25760815</ArticleId></ArticleIdList></Reference><Reference><Citation>BMC Genomics. 2012 Feb 15;13:75</Citation><ArticleIdList><ArticleId IdType="pubmed">22336098</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Syst Biol. 2011 Oct 11;7:539</Citation><ArticleIdList><ArticleId IdType="pubmed">21988835</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 1999 Nov;11(11):2099-112</Citation><ArticleIdList><ArticleId IdType="pubmed">10559437</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant Pathol. 2012 Apr;13(3):263-75</Citation><ArticleIdList><ArticleId IdType="pubmed">21933337</ArticleId></ArticleIdList></Reference><Reference><Citation>Genome Biol. 2016 Oct 31;17(1):221</Citation><ArticleIdList><ArticleId IdType="pubmed">27795210</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2017 Jun 22;546(7659):524-527</Citation><ArticleIdList><ArticleId IdType="pubmed">28605751</ArticleId></ArticleIdList></Reference><Reference><Citation>Microbes Infect. 2011 Dec;13(14-15):1168-76</Citation><ArticleIdList><ArticleId IdType="pubmed">21856436</ArticleId></ArticleIdList></Reference><Reference><Citation>Pest Manag Sci. 2014 Nov;70(11):1646-54</Citation><ArticleIdList><ArticleId IdType="pubmed">24753219</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Biotechnol. 2016 May;34(5):525-7</Citation><ArticleIdList><ArticleId IdType="pubmed">27043002</ArticleId></ArticleIdList></Reference><Reference><Citation>BMC Biol. 2016 Feb 19;14:8</Citation><ArticleIdList><ArticleId IdType="pubmed">26891798</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2003 Apr;15(4):809-34</Citation><ArticleIdList><ArticleId IdType="pubmed">12671079</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2014 Jul 18;345(6194):1249721</Citation><ArticleIdList><ArticleId IdType="pubmed">25035497</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2014 Jul 18;345(6194):1251788</Citation><ArticleIdList><ArticleId IdType="pubmed">25035500</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2009 Oct;60(2):218-26</Citation><ArticleIdList><ArticleId IdType="pubmed">19519800</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2008 Apr 24;452(7190):991-6</Citation><ArticleIdList><ArticleId IdType="pubmed">18432245</ArticleId></ArticleIdList></Reference><Reference><Citation>BMC Biol. 2016 Oct 3;14(1):84</Citation><ArticleIdList><ArticleId IdType="pubmed">27716181</ArticleId></ArticleIdList></Reference><Reference><Citation>BMC Plant Biol. 2014 May 05;14:120</Citation><ArticleIdList><ArticleId IdType="pubmed">24885638</ArticleId></ArticleIdList></Reference><Reference><Citation>Comput Biol Med. 2016 Nov 1;78:42-48</Citation><ArticleIdList><ArticleId IdType="pubmed">27658260</ArticleId></ArticleIdList></Reference><Reference><Citation>Front Plant Sci. 2016 Aug 10;7:1205</Citation><ArticleIdList><ArticleId IdType="pubmed">27559340</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Biotechnol. 2017 Aug;35(8):793-796</Citation><ArticleIdList><ArticleId IdType="pubmed">28504667</ArticleId></ArticleIdList></Reference><Reference><Citation>Front Plant Sci. 2014 Nov 25;5:606</Citation><ArticleIdList><ArticleId IdType="pubmed">25506347</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2014 Sep 5;345(6201):1181-4</Citation><ArticleIdList><ArticleId IdType="pubmed">25190796</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Genet. 2019 May;51(5):885-895</Citation><ArticleIdList><ArticleId IdType="pubmed">30962619</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2009 Dec;60(6):1043-54</Citation><ArticleIdList><ArticleId IdType="pubmed">19769576</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Biotechnol. 2016 Jun;34(6):652-5</Citation><ArticleIdList><ArticleId IdType="pubmed">27111722</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS Comput Biol. 2011 Oct;7(10):e1002195</Citation><ArticleIdList><ArticleId IdType="pubmed">22039361</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Genet Genomics. 2010 May;283(5):427-38</Citation><ArticleIdList><ArticleId IdType="pubmed">20217430</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2018 Aug 17;361(6403):</Citation><ArticleIdList><ArticleId IdType="pubmed">30115783</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Genet. 2018 Feb;50(2):285-296</Citation><ArticleIdList><ArticleId IdType="pubmed">29358651</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Opin Plant Biol. 2017 Aug;38:59-67</Citation><ArticleIdList><ArticleId IdType="pubmed">28494248</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2004 Nov;16(11):2870-94</Citation><ArticleIdList><ArticleId IdType="pubmed">15494555</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Dis. 2000 Feb;84(2):203</Citation><ArticleIdList><ArticleId IdType="pubmed">30841334</ArticleId></ArticleIdList></Reference><Reference><Citation>Phytopathology. 2015 Jul;105(7):917-28</Citation><ArticleIdList><ArticleId IdType="pubmed">25775107</ArticleId></ArticleIdList></Reference><Reference><Citation>Gigascience. 2017 Nov 1;6(11):1-7</Citation><ArticleIdList><ArticleId IdType="pubmed">29069494</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS One. 2010 Mar 10;5(3):e9490</Citation><ArticleIdList><ArticleId IdType="pubmed">20224823</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2017 Nov 23;551(7681):498-502</Citation><ArticleIdList><ArticleId IdType="pubmed">29143815</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2001 Apr;26(1):101-12</Citation><ArticleIdList><ArticleId IdType="pubmed">11359614</ArticleId></ArticleIdList></Reference><Reference><Citation>J Comput Biol. 2000 Feb-Apr;7(1-2):203-14</Citation><ArticleIdList><ArticleId IdType="pubmed">10890397</ArticleId></ArticleIdList></Reference><Reference><Citation>Bioinformatics. 2015 May 15;31(10):1665-7</Citation><ArticleIdList><ArticleId IdType="pubmed">25586514</ArticleId></ArticleIdList></Reference><Reference><Citation>Evol Bioinform Online. 2016 Jan 14;12:9-21</Citation><ArticleIdList><ArticleId IdType="pubmed">26792976</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2017 Feb 2;542(7640):145-146</Citation><ArticleIdList><ArticleId IdType="pubmed">28179687</ArticleId></ArticleIdList></Reference><Reference><Citation>Genome Res. 2005 Apr;15(4):526-36</Citation><ArticleIdList><ArticleId IdType="pubmed">15805493</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2006 Nov 16;444(7117):323-9</Citation><ArticleIdList><ArticleId IdType="pubmed">17108957</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2012 Nov 29;491(7426):705-10</Citation><ArticleIdList><ArticleId IdType="pubmed">23192148</ArticleId></ArticleIdList></Reference><Reference><Citation>Genome Biol. 2013 Aug 30;14(8):R93</Citation><ArticleIdList><ArticleId IdType="pubmed">24000942</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Plants. 2015 Nov 30;1:15186</Citation><ArticleIdList><ArticleId IdType="pubmed">27251721</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2011 Jul 10;475(7355):189-95</Citation><ArticleIdList><ArticleId IdType="pubmed">21743474</ArticleId></ArticleIdList></Reference><Reference><Citation>Theor Appl Genet. 2015 May;128(5):985-98</Citation><ArticleIdList><ArticleId IdType="pubmed">25805314</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Dis. 2016 Feb;100(2):483-489</Citation><ArticleIdList><ArticleId IdType="pubmed">30694133</ArticleId></ArticleIdList></Reference><Reference><Citation>Nucleic Acids Res. 2015 Jan;43(Database issue):D257-60</Citation><ArticleIdList><ArticleId IdType="pubmed">25300481</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2018 Aug 17;361(6403):</Citation><ArticleIdList><ArticleId IdType="pubmed">30115782</ArticleId></ArticleIdList></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>Inde</li><li>Royaume-Uni</li><li>Suisse</li></country><region><li>Canton de Zurich</li></region><settlement><li>Zurich</li></settlement><orgName><li>Université de Zurich</li></orgName></list><tree><country name="Royaume-Uni"><noRegion><name sortKey="Steuernagel, Burkhard" sort="Steuernagel, Burkhard" uniqKey="Steuernagel B" first="Burkhard" last="Steuernagel">Burkhard Steuernagel</name></noRegion><name sortKey="Baggs, Erin" sort="Baggs, Erin" uniqKey="Baggs E" first="Erin" last="Baggs">Erin Baggs</name><name sortKey="Jones, Jonathan D G" sort="Jones, Jonathan D G" uniqKey="Jones J" first="Jonathan D G" last="Jones">Jonathan D G. Jones</name><name sortKey="Krasileva, Ksenia V" sort="Krasileva, Ksenia V" uniqKey="Krasileva K" first="Ksenia V" last="Krasileva">Ksenia V. Krasileva</name><name sortKey="Krasileva, Ksenia V" sort="Krasileva, Ksenia V" uniqKey="Krasileva K" first="Ksenia V" last="Krasileva">Ksenia V. Krasileva</name><name sortKey="Ramirez Gonzalez, Ricardo H" sort="Ramirez Gonzalez, Ricardo H" uniqKey="Ramirez Gonzalez R" first="Ricardo H" last="Ramirez-Gonzalez">Ricardo H. Ramirez-Gonzalez</name><name sortKey="Ridout, Christopher J" sort="Ridout, Christopher J" uniqKey="Ridout C" first="Christopher J" last="Ridout">Christopher J. Ridout</name><name sortKey="Schoonbeek, Henk Jan" sort="Schoonbeek, Henk Jan" uniqKey="Schoonbeek H" first="Henk-Jan" last="Schoonbeek">Henk-Jan Schoonbeek</name><name sortKey="Uauy, Cristobal" sort="Uauy, Cristobal" uniqKey="Uauy C" first="Cristobal" last="Uauy">Cristobal Uauy</name><name sortKey="Witek, Agnieszka I" sort="Witek, Agnieszka I" uniqKey="Witek A" first="Agnieszka I" last="Witek">Agnieszka I. Witek</name><name sortKey="Witek, Kamil" sort="Witek, Kamil" uniqKey="Witek K" first="Kamil" last="Witek">Kamil Witek</name><name sortKey="Wulff, Brande B H" sort="Wulff, Brande B H" uniqKey="Wulff B" first="Brande B H" last="Wulff">Brande B H. Wulff</name><name sortKey="Yu, Guotai" sort="Yu, Guotai" uniqKey="Yu G" first="Guotai" last="Yu">Guotai Yu</name></country><country name="Suisse"><region name="Canton de Zurich"><name sortKey="Krattinger, Simon G" sort="Krattinger, Simon G" uniqKey="Krattinger S" first="Simon G" last="Krattinger">Simon G. Krattinger</name></region><name sortKey="Keller, Beat" sort="Keller, Beat" uniqKey="Keller B" first="Beat" last="Keller">Beat Keller</name></country><country name="Inde"><noRegion><name sortKey="Yadav, Inderjit" sort="Yadav, Inderjit" uniqKey="Yadav I" first="Inderjit" last="Yadav">Inderjit Yadav</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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