Soil microbiota influences clubroot disease by modulating Plasmodiophora brassicae and Brassica napus transcriptomes.
Identifieur interne : 000048 ( Main/Exploration ); précédent : 000047; suivant : 000049Soil microbiota influences clubroot disease by modulating Plasmodiophora brassicae and Brassica napus transcriptomes.
Auteurs : Stéphanie Daval [France] ; Kévin Gazengel [France] ; Arnaud Belcour [France] ; Juliette Linglin [France] ; Anne-Yvonne Guillerm-Erckelboudt [France] ; Alain Sarniguet [France] ; Maria J. Manzanares-Dauleux [France] ; Lionel Lebreton [France] ; Christophe Mougel [France]Source :
- Microbial biotechnology [ 1751-7915 ] ; 2020.
Abstract
The contribution of surrounding plant microbiota to disease development has led to the 'pathobiome' concept, which represents the interaction between the pathogen, the host plant and the associated biotic microbial community, resulting or not in plant disease. The aim herein is to understand how the soil microbial environment may influence the functions of a pathogen and its pathogenesis, and the molecular response of the plant to the infection, with a dual-RNAseq transcriptomics approach. We address this question using Brassica napus and Plasmodiophora brassicae, the pathogen responsible for clubroot. A time-course experiment was conducted to study interactions between P. brassicae, two B. napus genotypes and three soils harbouring high, medium or low microbiota diversities and levels of richness. The soil microbial diversity levels had an impact on disease development (symptom levels and pathogen quantity). The P. brassicae and B. napus transcriptional patterns were modulated by these microbial diversities, these modulations being dependent on the host genotype plant and the kinetic time. The functional analysis of gene expressions allowed the identification of pathogen and plant host functions potentially involved in the change of plant disease level, such as pathogenicity-related genes (NUDIX effector) in P. brassicae and plant defence-related genes (glucosinolate metabolism) in B. napus.
DOI: 10.1111/1751-7915.13634
PubMed: 32686326
PubMed Central: PMC7415369
Affiliations:
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Bretagne</region></placeName></affiliation></author><author><name sortKey="Sarniguet, Alain" sort="Sarniguet, Alain" uniqKey="Sarniguet A" first="Alain" last="Sarniguet">Alain Sarniguet</name><affiliation wicri:level="4"><nlm:affiliation>INRAE, Agrocampus Ouest, Université d'Angers, IRHS, Beaucouzé, F-49071, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, Agrocampus Ouest, Université d'Angers, IRHS, Beaucouzé, F-49071</wicri:regionArea><placeName><region type="region" nuts="2">Pays de la Loire</region></placeName><orgName type="university">Université d'Angers</orgName></affiliation></author><author><name sortKey="Manzanares Dauleux, Maria J" sort="Manzanares Dauleux, Maria J" uniqKey="Manzanares Dauleux M" first="Maria J" last="Manzanares-Dauleux">Maria J. Manzanares-Dauleux</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region></placeName></affiliation></author><author><name sortKey="Lebreton, Lionel" sort="Lebreton, Lionel" uniqKey="Lebreton L" first="Lionel" last="Lebreton">Lionel Lebreton</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region></placeName></affiliation></author><author><name sortKey="Mougel, Christophe" sort="Mougel, Christophe" uniqKey="Mougel C" first="Christophe" last="Mougel">Christophe Mougel</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region></placeName></affiliation></author></analytic><series><title level="j">Microbial biotechnology</title><idno type="eISSN">1751-7915</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">The contribution of surrounding plant microbiota to disease development has led to the 'pathobiome' concept, which represents the interaction between the pathogen, the host plant and the associated biotic microbial community, resulting or not in plant disease. The aim herein is to understand how the soil microbial environment may influence the functions of a pathogen and its pathogenesis, and the molecular response of the plant to the infection, with a dual-RNAseq transcriptomics approach. We address this question using Brassica napus and Plasmodiophora brassicae, the pathogen responsible for clubroot. A time-course experiment was conducted to study interactions between P. brassicae, two B. napus genotypes and three soils harbouring high, medium or low microbiota diversities and levels of richness. The soil microbial diversity levels had an impact on disease development (symptom levels and pathogen quantity). The P. brassicae and B. napus transcriptional patterns were modulated by these microbial diversities, these modulations being dependent on the host genotype plant and the kinetic time. The functional analysis of gene expressions allowed the identification of pathogen and plant host functions potentially involved in the change of plant disease level, such as pathogenicity-related genes (NUDIX effector) in P. brassicae and plant defence-related genes (glucosinolate metabolism) in B. napus.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32686326</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1751-7915</ISSN><JournalIssue CitedMedium="Internet"><Volume>13</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>09</Month></PubDate></JournalIssue><Title>Microbial biotechnology</Title><ISOAbbreviation>Microb Biotechnol</ISOAbbreviation></Journal><ArticleTitle>Soil microbiota influences clubroot disease by modulating Plasmodiophora brassicae and Brassica napus transcriptomes.</ArticleTitle><Pagination><MedlinePgn>1648-1672</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/1751-7915.13634</ELocationID><Abstract><AbstractText>The contribution of surrounding plant microbiota to disease development has led to the 'pathobiome' concept, which represents the interaction between the pathogen, the host plant and the associated biotic microbial community, resulting or not in plant disease. The aim herein is to understand how the soil microbial environment may influence the functions of a pathogen and its pathogenesis, and the molecular response of the plant to the infection, with a dual-RNAseq transcriptomics approach. We address this question using Brassica napus and Plasmodiophora brassicae, the pathogen responsible for clubroot. A time-course experiment was conducted to study interactions between P. brassicae, two B. napus genotypes and three soils harbouring high, medium or low microbiota diversities and levels of richness. The soil microbial diversity levels had an impact on disease development (symptom levels and pathogen quantity). The P. brassicae and B. napus transcriptional patterns were modulated by these microbial diversities, these modulations being dependent on the host genotype plant and the kinetic time. The functional analysis of gene expressions allowed the identification of pathogen and plant host functions potentially involved in the change of plant disease level, such as pathogenicity-related genes (NUDIX effector) in P. brassicae and plant defence-related genes (glucosinolate metabolism) in B. napus.</AbstractText><CopyrightInformation>© 2020 The Authors. Microbial Biotechnology published by Society for Applied Microbiology and John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Daval</LastName><ForeName>Stéphanie</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0001-8848-4190</Identifier><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gazengel</LastName><ForeName>Kévin</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0001-9054-2281</Identifier><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Belcour</LastName><ForeName>Arnaud</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0003-1170-0785</Identifier><AffiliationInfo><Affiliation>INRIA, Université Rennes, CNRS, IRISA, Rennes, F-35000, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Linglin</LastName><ForeName>Juliette</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Ploudaniel, F-29260, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Guillerm-Erckelboudt</LastName><ForeName>Anne-Yvonne</ForeName><Initials>AY</Initials><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sarniguet</LastName><ForeName>Alain</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0001-6232-0200</Identifier><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université d'Angers, IRHS, Beaucouzé, F-49071, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Manzanares-Dauleux</LastName><ForeName>Maria J</ForeName><Initials>MJ</Initials><Identifier Source="ORCID">0000-0002-6452-0393</Identifier><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lebreton</LastName><ForeName>Lionel</ForeName><Initials>L</Initials><Identifier Source="ORCID">0000-0003-1759-5269</Identifier><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mougel</LastName><ForeName>Christophe</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0001-8675-3115</Identifier><AffiliationInfo><Affiliation>INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, Le Rheu, F-35650, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><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>07</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Microb Biotechnol</MedlineTA><NlmUniqueID>101316335</NlmUniqueID><ISSNLinking>1751-7915</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>13</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>07</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>07</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>7</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>7</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>7</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32686326</ArticleId><ArticleId IdType="doi">10.1111/1751-7915.13634</ArticleId><ArticleId IdType="pmc">PMC7415369</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Abramyan, J., and Stajich, J.E. 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Appl Soil Ecol 107: 324-333.</Citation></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>France</li></country><region><li>Pays de la Loire</li><li>Région Bretagne</li></region><orgName><li>Université d'Angers</li></orgName></list><tree><country name="France"><region name="Région Bretagne"><name sortKey="Daval, Stephanie" sort="Daval, Stephanie" uniqKey="Daval S" first="Stéphanie" last="Daval">Stéphanie Daval</name></region><name sortKey="Belcour, Arnaud" sort="Belcour, Arnaud" uniqKey="Belcour A" first="Arnaud" last="Belcour">Arnaud Belcour</name><name sortKey="Gazengel, Kevin" sort="Gazengel, Kevin" uniqKey="Gazengel K" first="Kévin" last="Gazengel">Kévin Gazengel</name><name sortKey="Guillerm Erckelboudt, Anne Yvonne" sort="Guillerm Erckelboudt, Anne Yvonne" uniqKey="Guillerm Erckelboudt A" first="Anne-Yvonne" last="Guillerm-Erckelboudt">Anne-Yvonne Guillerm-Erckelboudt</name><name sortKey="Lebreton, Lionel" sort="Lebreton, Lionel" uniqKey="Lebreton L" first="Lionel" last="Lebreton">Lionel Lebreton</name><name sortKey="Linglin, Juliette" sort="Linglin, Juliette" uniqKey="Linglin J" first="Juliette" last="Linglin">Juliette Linglin</name><name sortKey="Manzanares Dauleux, Maria J" sort="Manzanares Dauleux, Maria J" uniqKey="Manzanares Dauleux M" first="Maria J" last="Manzanares-Dauleux">Maria J. 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