Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins.
Identifieur interne : 000110 ( Main/Exploration ); précédent : 000109; suivant : 000111Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins.
Auteurs : Nick C. Snelders [Pays-Bas] ; Hanna Rovenich [Pays-Bas] ; Gabriella C. Petti [Pays-Bas, Suisse] ; Mercedes Rocafort [Pays-Bas, Nouvelle-Zélande] ; Grardy C M. Van Den Berg [Pays-Bas] ; Julia A. Vorholt [Suisse] ; Jeroen R. Mesters [Allemagne] ; Michael F. Seidl [Pays-Bas] ; Reindert Nijland [Pays-Bas] ; Bart P H J. Thomma [Pays-Bas, Allemagne]Source :
- Nature plants [ 2055-0278 ] ; 2020.
Abstract
During colonization of their hosts, pathogens secrete effector proteins to promote disease development through various mechanisms. Increasing evidence shows that the host microbiome plays a crucial role in health, and that hosts actively shape their microbiomes to suppress disease. We proposed that pathogens evolved to manipulate host microbiomes to their advantage in turn. Here, we show that the previously identified virulence effector VdAve1, secreted by the fungal plant pathogen Verticillium dahliae, displays antimicrobial activity and facilitates colonization of tomato and cotton through the manipulation of their microbiomes by suppressing antagonistic bacteria. Moreover, we show that VdAve1, and also the newly identified antimicrobial effector VdAMP2, are exploited for microbiome manipulation in the soil environment, where the fungus resides in absence of a host. In conclusion, we demonstrate that a fungal plant pathogen uses effector proteins to modulate microbiome compositions inside and outside the host, and propose that pathogen effector catalogues represent an untapped resource for new antibiotics.
DOI: 10.1038/s41477-020-00799-5
PubMed: 33139860
Affiliations:
- Allemagne, Nouvelle-Zélande, Pays-Bas, Suisse
- Canton de Zurich, Utrecht (province)
- Utrecht, Zurich
- Université d'Utrecht
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Snelders</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation></author><author><name sortKey="Rovenich, Hanna" sort="Rovenich, Hanna" uniqKey="Rovenich H" first="Hanna" last="Rovenich">Hanna Rovenich</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation></author><author><name sortKey="Petti, Gabriella C" sort="Petti, Gabriella C" uniqKey="Petti G" first="Gabriella C" last="Petti">Gabriella C. Petti</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute of Microbiology, ETH Zürich, Zürich, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Institute of Microbiology, ETH Zürich, Zürich</wicri:regionArea><placeName><settlement type="city">Zurich</settlement><region nuts="3" type="region">Canton de Zurich</region></placeName></affiliation></author><author><name sortKey="Rocafort, Mercedes" sort="Rocafort, Mercedes" uniqKey="Rocafort M" first="Mercedes" last="Rocafort">Mercedes Rocafort</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Agriculture and Environment, Massey University, Palmerston North, New Zealand.</nlm:affiliation><country xml:lang="fr">Nouvelle-Zélande</country><wicri:regionArea>School of Agriculture and Environment, Massey University, Palmerston North</wicri:regionArea><wicri:noRegion>Palmerston North</wicri:noRegion></affiliation></author><author><name sortKey="Van Den Berg, Grardy C M" sort="Van Den Berg, Grardy C M" uniqKey="Van Den Berg G" first="Grardy C M" last="Van Den Berg">Grardy C M. Van Den Berg</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation></author><author><name sortKey="Vorholt, Julia A" sort="Vorholt, Julia A" uniqKey="Vorholt J" first="Julia A" last="Vorholt">Julia A. Vorholt</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Microbiology, ETH Zürich, Zürich, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Institute of Microbiology, ETH Zürich, Zürich</wicri:regionArea><placeName><settlement type="city">Zurich</settlement><region nuts="3" type="region">Canton de Zurich</region></placeName></affiliation></author><author><name sortKey="Mesters, Jeroen R" sort="Mesters, Jeroen R" uniqKey="Mesters J" first="Jeroen R" last="Mesters">Jeroen R. Mesters</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Biochemistry, University of Lübeck, Center for Structural and Cell Biology in Medicine, Lübeck, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Biochemistry, University of Lübeck, Center for Structural and Cell Biology in Medicine, Lübeck</wicri:regionArea><wicri:noRegion>Lübeck</wicri:noRegion><wicri:noRegion>Lübeck</wicri:noRegion><wicri:noRegion>Lübeck</wicri:noRegion></affiliation></author><author><name sortKey="Seidl, Michael F" sort="Seidl, Michael F" uniqKey="Seidl M" first="Michael F" last="Seidl">Michael F. Seidl</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:affiliation>Theoretical Biology & Bioinformatics Group, Department of Biology, Utrecht University, Utrecht, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Theoretical Biology & Bioinformatics Group, Department of Biology, Utrecht University, Utrecht</wicri:regionArea><placeName><settlement type="city">Utrecht</settlement><region nuts="2" type="province">Utrecht (province)</region></placeName><orgName type="university">Université d'Utrecht</orgName></affiliation></author><author><name sortKey="Nijland, Reindert" sort="Nijland, Reindert" uniqKey="Nijland R" first="Reindert" last="Nijland">Reindert Nijland</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Marine Animal Ecology Group, Wageningen University and Research, Wageningen, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Marine Animal Ecology Group, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation></author><author><name sortKey="Thomma, Bart P H J" sort="Thomma, Bart P H J" uniqKey="Thomma B" first="Bart P H J" last="Thomma">Bart P H J. Thomma</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands. bthomma@uni-koeln.de.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, Wageningen</wicri:regionArea><wicri:noRegion>Wageningen</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Botanical Institute, Cologne, Germany. bthomma@uni-koeln.de.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Botanical Institute, Cologne</wicri:regionArea><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion></affiliation></author></analytic><series><title level="j">Nature plants</title><idno type="eISSN">2055-0278</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">During colonization of their hosts, pathogens secrete effector proteins to promote disease development through various mechanisms. Increasing evidence shows that the host microbiome plays a crucial role in health, and that hosts actively shape their microbiomes to suppress disease. We proposed that pathogens evolved to manipulate host microbiomes to their advantage in turn. Here, we show that the previously identified virulence effector VdAve1, secreted by the fungal plant pathogen Verticillium dahliae, displays antimicrobial activity and facilitates colonization of tomato and cotton through the manipulation of their microbiomes by suppressing antagonistic bacteria. Moreover, we show that VdAve1, and also the newly identified antimicrobial effector VdAMP2, are exploited for microbiome manipulation in the soil environment, where the fungus resides in absence of a host. In conclusion, we demonstrate that a fungal plant pathogen uses effector proteins to modulate microbiome compositions inside and outside the host, and propose that pathogen effector catalogues represent an untapped resource for new antibiotics.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">33139860</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>10</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">2055-0278</ISSN><JournalIssue CitedMedium="Internet"><Volume>6</Volume><Issue>11</Issue><PubDate><Year>2020</Year><Month>Nov</Month></PubDate></JournalIssue><Title>Nature plants</Title><ISOAbbreviation>Nat Plants</ISOAbbreviation></Journal><ArticleTitle>Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins.</ArticleTitle><Pagination><MedlinePgn>1365-1374</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41477-020-00799-5</ELocationID><Abstract><AbstractText>During colonization of their hosts, pathogens secrete effector proteins to promote disease development through various mechanisms. Increasing evidence shows that the host microbiome plays a crucial role in health, and that hosts actively shape their microbiomes to suppress disease. We proposed that pathogens evolved to manipulate host microbiomes to their advantage in turn. Here, we show that the previously identified virulence effector VdAve1, secreted by the fungal plant pathogen Verticillium dahliae, displays antimicrobial activity and facilitates colonization of tomato and cotton through the manipulation of their microbiomes by suppressing antagonistic bacteria. Moreover, we show that VdAve1, and also the newly identified antimicrobial effector VdAMP2, are exploited for microbiome manipulation in the soil environment, where the fungus resides in absence of a host. In conclusion, we demonstrate that a fungal plant pathogen uses effector proteins to modulate microbiome compositions inside and outside the host, and propose that pathogen effector catalogues represent an untapped resource for new antibiotics.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Snelders</LastName><ForeName>Nick C</ForeName><Initials>NC</Initials><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rovenich</LastName><ForeName>Hanna</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Petti</LastName><ForeName>Gabriella C</ForeName><Initials>GC</Initials><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Microbiology, ETH Zürich, Zürich, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rocafort</LastName><ForeName>Mercedes</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-7192-695X</Identifier><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Agriculture and Environment, Massey University, Palmerston North, New Zealand.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van den Berg</LastName><ForeName>Grardy C M</ForeName><Initials>GCM</Initials><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vorholt</LastName><ForeName>Julia A</ForeName><Initials>JA</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-6011-4910</Identifier><AffiliationInfo><Affiliation>Institute of Microbiology, ETH Zürich, Zürich, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mesters</LastName><ForeName>Jeroen R</ForeName><Initials>JR</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-8532-6699</Identifier><AffiliationInfo><Affiliation>Institute of Biochemistry, University of Lübeck, Center for Structural and Cell Biology in Medicine, Lübeck, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Seidl</LastName><ForeName>Michael F</ForeName><Initials>MF</Initials><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Theoretical Biology & Bioinformatics Group, Department of Biology, Utrecht University, Utrecht, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nijland</LastName><ForeName>Reindert</ForeName><Initials>R</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-0049-3768</Identifier><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Marine Animal Ecology Group, Wageningen University and Research, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thomma</LastName><ForeName>Bart P H J</ForeName><Initials>BPHJ</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-4125-4181</Identifier><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands. bthomma@uni-koeln.de.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Botanical Institute, Cologne, Germany. bthomma@uni-koeln.de.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>EXC 2048/1 - Project ID: 390686111</GrantID><Agency>Deutsche Forschungsgemeinschaft (German Research Foundation)</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>11</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Nat Plants</MedlineTA><NlmUniqueID>101651677</NlmUniqueID><ISSNLinking>2055-0278</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>02</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>09</Month><Day>29</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>11</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>11</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>11</Month><Day>3</Day><Hour>5</Hour><Minute>44</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33139860</ArticleId><ArticleId IdType="doi">10.1038/s41477-020-00799-5</ArticleId><ArticleId IdType="pii">10.1038/s41477-020-00799-5</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Allemagne</li><li>Nouvelle-Zélande</li><li>Pays-Bas</li><li>Suisse</li></country><region><li>Canton de Zurich</li><li>Utrecht (province)</li></region><settlement><li>Utrecht</li><li>Zurich</li></settlement><orgName><li>Université d'Utrecht</li></orgName></list><tree><country name="Pays-Bas"><noRegion><name sortKey="Snelders, Nick C" sort="Snelders, Nick C" uniqKey="Snelders N" first="Nick C" last="Snelders">Nick C. Snelders</name></noRegion><name sortKey="Nijland, Reindert" sort="Nijland, Reindert" uniqKey="Nijland R" first="Reindert" last="Nijland">Reindert Nijland</name><name sortKey="Nijland, Reindert" sort="Nijland, Reindert" uniqKey="Nijland R" first="Reindert" last="Nijland">Reindert Nijland</name><name sortKey="Petti, Gabriella C" sort="Petti, Gabriella C" uniqKey="Petti G" first="Gabriella C" last="Petti">Gabriella C. Petti</name><name sortKey="Rocafort, Mercedes" sort="Rocafort, Mercedes" uniqKey="Rocafort M" first="Mercedes" last="Rocafort">Mercedes Rocafort</name><name sortKey="Rovenich, Hanna" sort="Rovenich, Hanna" uniqKey="Rovenich H" first="Hanna" last="Rovenich">Hanna Rovenich</name><name sortKey="Seidl, Michael F" sort="Seidl, Michael F" uniqKey="Seidl M" first="Michael F" last="Seidl">Michael F. Seidl</name><name sortKey="Seidl, Michael F" sort="Seidl, Michael F" uniqKey="Seidl M" first="Michael F" last="Seidl">Michael F. Seidl</name><name sortKey="Thomma, Bart P H J" sort="Thomma, Bart P H J" uniqKey="Thomma B" first="Bart P H J" last="Thomma">Bart P H J. Thomma</name><name sortKey="Van Den Berg, Grardy C M" sort="Van Den Berg, Grardy C M" uniqKey="Van Den Berg G" first="Grardy C M" last="Van Den Berg">Grardy C M. Van Den Berg</name></country><country name="Suisse"><region name="Canton de Zurich"><name sortKey="Petti, Gabriella C" sort="Petti, Gabriella C" uniqKey="Petti G" first="Gabriella C" last="Petti">Gabriella C. Petti</name></region><name sortKey="Vorholt, Julia A" sort="Vorholt, Julia A" uniqKey="Vorholt J" first="Julia A" last="Vorholt">Julia A. Vorholt</name></country><country name="Nouvelle-Zélande"><noRegion><name sortKey="Rocafort, Mercedes" sort="Rocafort, Mercedes" uniqKey="Rocafort M" first="Mercedes" last="Rocafort">Mercedes Rocafort</name></noRegion></country><country name="Allemagne"><noRegion><name sortKey="Mesters, Jeroen R" sort="Mesters, Jeroen R" uniqKey="Mesters J" first="Jeroen R" last="Mesters">Jeroen R. Mesters</name></noRegion><name sortKey="Thomma, Bart P H J" sort="Thomma, Bart P H J" uniqKey="Thomma B" first="Bart P H J" last="Thomma">Bart P H J. Thomma</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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