Verticillium longisporum Elicits Media-Dependent Secretome Responses With Capacity to Distinguish Between Plant-Related Environments.
Identifieur interne : 000245 ( Main/Exploration ); précédent : 000244; suivant : 000246Verticillium longisporum Elicits Media-Dependent Secretome Responses With Capacity to Distinguish Between Plant-Related Environments.
Auteurs : Miriam Leonard [Allemagne] ; Anika Kühn [Allemagne] ; Rebekka Harting [Allemagne] ; Isabel Maurus [Allemagne] ; Alexandra Nagel [Allemagne] ; Jessica Starke [Allemagne] ; Harald Kusch [Allemagne] ; Oliver Valerius [Allemagne] ; Kirstin Feussner [Allemagne] ; Ivo Feussner [Allemagne] ; Alexander Kaever [Allemagne] ; Manuel Landesfeind [Allemagne] ; Burkhard Morgenstern [Allemagne] ; Dörte Becher [Allemagne] ; Michael Hecker [Allemagne] ; Susanna A. Braus-Stromeyer [Allemagne] ; James W. Kronstad [Canada] ; Gerhard H. Braus [Allemagne]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2020.
Abstract
Verticillia cause a vascular wilt disease affecting a broad range of economically valuable crops. The fungus enters its host plants through the roots and colonizes the vascular system. It requires extracellular proteins for a successful plant colonization. The exoproteomes of the allodiploid Verticillium longisporum upon cultivation in different media or xylem sap extracted from its host plant Brassica napus were compared. Secreted fungal proteins were identified by label free liquid chromatography-tandem mass spectrometry screening. V. longisporum induced two main secretion patterns. One response pattern was elicited in various non-plant related environments. The second pattern includes the exoprotein responses to the plant-related media, pectin-rich simulated xylem medium and pure xylem sap, which exhibited similar but additional distinct features. These exoproteomes include a shared core set of 221 secreted and similarly enriched fungal proteins. The pectin-rich medium significantly induced the secretion of 143 proteins including a number of pectin degrading enzymes, whereas xylem sap triggered a smaller but unique fungal exoproteome pattern with 32 enriched proteins. The latter pattern included proteins with domains of known pathogenicity factors, metallopeptidases and carbohydrate-active enzymes. The most abundant proteins of these different groups are the necrosis and ethylene inducing-like proteins Nlp2 and Nlp3, the cerato-platanin proteins Cp1 and Cp2, the metallopeptidases Mep1 and Mep2 and the carbohydrate-active enzymes Gla1, Amy1 and Cbd1. Their pathogenicity contribution was analyzed in the haploid parental strain V. dahliae. Deletion of the majority of the corresponding genes caused no phenotypic changes during ex planta growth or invasion and colonization of tomato plants. However, we discovered that the MEP1, NLP2, and NLP3 deletion strains were compromised in plant infections. Overall, our exoproteome approach revealed that the fungus induces specific secretion responses in different environments. The fungus has a general response to non-plant related media whereas it is able to fine-tune its exoproteome in the presence of plant material. Importantly, the xylem sap-specific exoproteome pinpointed Nlp2 and Nlp3 as single effectors required for successful V. dahliae colonization.
DOI: 10.3389/fmicb.2020.01876
PubMed: 32849460
PubMed Central: PMC7423881
Affiliations:
- Allemagne, Canada
- Basse-Saxe, Colombie-Britannique
- Göttingen, Vancouver
- Université de la Colombie-Britannique
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sortKey="Kuhn, Anika" sort="Kuhn, Anika" uniqKey="Kuhn A" first="Anika" last="Kühn">Anika Kühn</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Harting, Rebekka" sort="Harting, Rebekka" uniqKey="Harting R" first="Rebekka" last="Harting">Rebekka Harting</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Maurus, Isabel" sort="Maurus, Isabel" uniqKey="Maurus I" first="Isabel" last="Maurus">Isabel Maurus</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen 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type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Starke, Jessica" sort="Starke, Jessica" uniqKey="Starke J" first="Jessica" last="Starke">Jessica Starke</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kusch, Harald" sort="Kusch, Harald" uniqKey="Kusch H" first="Harald" last="Kusch">Harald Kusch</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Valerius, Oliver" sort="Valerius, Oliver" uniqKey="Valerius O" first="Oliver" last="Valerius">Oliver Valerius</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Feussner, Kirstin" sort="Feussner, Kirstin" uniqKey="Feussner K" first="Kirstin" last="Feussner">Kirstin Feussner</name><affiliation wicri:level="3"><nlm:affiliation>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Feussner, Ivo" sort="Feussner, Ivo" uniqKey="Feussner I" first="Ivo" last="Feussner">Ivo Feussner</name><affiliation wicri:level="3"><nlm:affiliation>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kaever, Alexander" sort="Kaever, Alexander" 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Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Morgenstern, Burkhard" sort="Morgenstern, Burkhard" uniqKey="Morgenstern B" first="Burkhard" last="Morgenstern">Burkhard Morgenstern</name><affiliation wicri:level="3"><nlm:affiliation>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Becher, Dorte" sort="Becher, Dorte" uniqKey="Becher D" first="Dörte" last="Becher">Dörte Becher</name><affiliation wicri:level="1"><nlm:affiliation>Department Microbial Proteomics, Institute for Microbiology, University of Greifswald, Greifswald, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department Microbial Proteomics, Institute for Microbiology, University of Greifswald, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation></author><author><name sortKey="Hecker, Michael" sort="Hecker, Michael" uniqKey="Hecker M" first="Michael" last="Hecker">Michael Hecker</name><affiliation wicri:level="1"><nlm:affiliation>Department of Microbial Physiology, Institute for Microbiology, University of Greifswald, Greifswald, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Microbial Physiology, Institute for Microbiology, University of Greifswald, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation></author><author><name sortKey="Braus Stromeyer, Susanna A" sort="Braus Stromeyer, Susanna A" uniqKey="Braus Stromeyer S" first="Susanna A" last="Braus-Stromeyer">Susanna A. Braus-Stromeyer</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kronstad, James W" sort="Kronstad, James W" uniqKey="Kronstad J" first="James W" last="Kronstad">James W. Kronstad</name><affiliation wicri:level="4"><nlm:affiliation>Michael Smith Laboratories, Department of Microbiology and Immunology, The University of British Columbia, Vancouver, BC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Michael Smith Laboratories, Department of Microbiology and Immunology, The University of British Columbia, Vancouver, BC</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Braus, Gerhard H" sort="Braus, Gerhard H" uniqKey="Braus G" first="Gerhard H" last="Braus">Gerhard H. Braus</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32849460</idno><idno type="pmid">32849460</idno><idno type="doi">10.3389/fmicb.2020.01876</idno><idno type="pmc">PMC7423881</idno><idno type="wicri:Area/Main/Corpus">000127</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000127</idno><idno type="wicri:Area/Main/Curation">000127</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000127</idno><idno type="wicri:Area/Main/Exploration">000127</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en"><i>Verticillium longisporum</i> Elicits Media-Dependent Secretome Responses With Capacity to Distinguish Between Plant-Related Environments.</title><author><name sortKey="Leonard, Miriam" sort="Leonard, Miriam" uniqKey="Leonard M" first="Miriam" last="Leonard">Miriam Leonard</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kuhn, Anika" sort="Kuhn, Anika" uniqKey="Kuhn A" first="Anika" last="Kühn">Anika Kühn</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Harting, Rebekka" sort="Harting, Rebekka" uniqKey="Harting R" first="Rebekka" last="Harting">Rebekka Harting</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Maurus, Isabel" sort="Maurus, Isabel" uniqKey="Maurus I" first="Isabel" last="Maurus">Isabel Maurus</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Nagel, Alexandra" sort="Nagel, Alexandra" uniqKey="Nagel A" first="Alexandra" last="Nagel">Alexandra Nagel</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Starke, Jessica" sort="Starke, Jessica" uniqKey="Starke J" first="Jessica" last="Starke">Jessica Starke</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kusch, Harald" sort="Kusch, Harald" uniqKey="Kusch H" first="Harald" last="Kusch">Harald Kusch</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Valerius, Oliver" sort="Valerius, Oliver" uniqKey="Valerius O" first="Oliver" last="Valerius">Oliver Valerius</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Feussner, Kirstin" sort="Feussner, Kirstin" uniqKey="Feussner K" first="Kirstin" last="Feussner">Kirstin Feussner</name><affiliation wicri:level="3"><nlm:affiliation>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Feussner, Ivo" sort="Feussner, Ivo" uniqKey="Feussner I" first="Ivo" last="Feussner">Ivo Feussner</name><affiliation wicri:level="3"><nlm:affiliation>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kaever, Alexander" sort="Kaever, Alexander" uniqKey="Kaever A" first="Alexander" last="Kaever">Alexander Kaever</name><affiliation wicri:level="3"><nlm:affiliation>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Landesfeind, Manuel" sort="Landesfeind, Manuel" uniqKey="Landesfeind M" first="Manuel" last="Landesfeind">Manuel Landesfeind</name><affiliation wicri:level="3"><nlm:affiliation>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Morgenstern, Burkhard" sort="Morgenstern, Burkhard" uniqKey="Morgenstern B" first="Burkhard" last="Morgenstern">Burkhard Morgenstern</name><affiliation wicri:level="3"><nlm:affiliation>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Becher, Dorte" sort="Becher, Dorte" uniqKey="Becher D" first="Dörte" last="Becher">Dörte Becher</name><affiliation wicri:level="1"><nlm:affiliation>Department Microbial Proteomics, Institute for Microbiology, University of Greifswald, Greifswald, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department Microbial Proteomics, Institute for Microbiology, University of Greifswald, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation></author><author><name sortKey="Hecker, Michael" sort="Hecker, Michael" uniqKey="Hecker M" first="Michael" last="Hecker">Michael Hecker</name><affiliation wicri:level="1"><nlm:affiliation>Department of Microbial Physiology, Institute for Microbiology, University of Greifswald, Greifswald, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Microbial Physiology, Institute for Microbiology, University of Greifswald, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation></author><author><name sortKey="Braus Stromeyer, Susanna A" sort="Braus Stromeyer, Susanna A" uniqKey="Braus Stromeyer S" first="Susanna A" last="Braus-Stromeyer">Susanna A. Braus-Stromeyer</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kronstad, James W" sort="Kronstad, James W" uniqKey="Kronstad J" first="James W" last="Kronstad">James W. Kronstad</name><affiliation wicri:level="4"><nlm:affiliation>Michael Smith Laboratories, Department of Microbiology and Immunology, The University of British Columbia, Vancouver, BC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Michael Smith Laboratories, Department of Microbiology and Immunology, The University of British Columbia, Vancouver, BC</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Braus, Gerhard H" sort="Braus, Gerhard H" uniqKey="Braus G" first="Gerhard H" last="Braus">Gerhard H. Braus</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</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">Verticillia cause a vascular wilt disease affecting a broad range of economically valuable crops. The fungus enters its host plants through the roots and colonizes the vascular system. It requires extracellular proteins for a successful plant colonization. The exoproteomes of the allodiploid <i>Verticillium longisporum</i> upon cultivation in different media or xylem sap extracted from its host plant <i>Brassica napus</i> were compared. Secreted fungal proteins were identified by label free liquid chromatography-tandem mass spectrometry screening. <i>V. longisporum</i> induced two main secretion patterns. One response pattern was elicited in various non-plant related environments. The second pattern includes the exoprotein responses to the plant-related media, pectin-rich simulated xylem medium and pure xylem sap, which exhibited similar but additional distinct features. These exoproteomes include a shared core set of 221 secreted and similarly enriched fungal proteins. The pectin-rich medium significantly induced the secretion of 143 proteins including a number of pectin degrading enzymes, whereas xylem sap triggered a smaller but unique fungal exoproteome pattern with 32 enriched proteins. The latter pattern included proteins with domains of known pathogenicity factors, metallopeptidases and carbohydrate-active enzymes. The most abundant proteins of these different groups are the necrosis and ethylene inducing-like proteins Nlp2 and Nlp3, the cerato-platanin proteins Cp1 and Cp2, the metallopeptidases Mep1 and Mep2 and the carbohydrate-active enzymes Gla1, Amy1 and Cbd1. Their pathogenicity contribution was analyzed in the haploid parental strain <i>V. dahliae</i>. Deletion of the majority of the corresponding genes caused no phenotypic changes during <i>ex planta</i> growth or invasion and colonization of tomato plants. However, we discovered that the <i>MEP1</i>, <i>NLP2</i>, and <i>NLP3</i> deletion strains were compromised in plant infections. Overall, our exoproteome approach revealed that the fungus induces specific secretion responses in different environments. The fungus has a general response to non-plant related media whereas it is able to fine-tune its exoproteome in the presence of plant material. Importantly, the xylem sap-specific exoproteome pinpointed Nlp2 and Nlp3 as single effectors required for successful <i>V. dahliae</i> colonization.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32849460</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle><i>Verticillium longisporum</i> Elicits Media-Dependent Secretome Responses With Capacity to Distinguish Between Plant-Related Environments.</ArticleTitle><Pagination><MedlinePgn>1876</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2020.01876</ELocationID><Abstract><AbstractText>Verticillia cause a vascular wilt disease affecting a broad range of economically valuable crops. The fungus enters its host plants through the roots and colonizes the vascular system. It requires extracellular proteins for a successful plant colonization. The exoproteomes of the allodiploid <i>Verticillium longisporum</i> upon cultivation in different media or xylem sap extracted from its host plant <i>Brassica napus</i> were compared. Secreted fungal proteins were identified by label free liquid chromatography-tandem mass spectrometry screening. <i>V. longisporum</i> induced two main secretion patterns. One response pattern was elicited in various non-plant related environments. The second pattern includes the exoprotein responses to the plant-related media, pectin-rich simulated xylem medium and pure xylem sap, which exhibited similar but additional distinct features. These exoproteomes include a shared core set of 221 secreted and similarly enriched fungal proteins. The pectin-rich medium significantly induced the secretion of 143 proteins including a number of pectin degrading enzymes, whereas xylem sap triggered a smaller but unique fungal exoproteome pattern with 32 enriched proteins. The latter pattern included proteins with domains of known pathogenicity factors, metallopeptidases and carbohydrate-active enzymes. The most abundant proteins of these different groups are the necrosis and ethylene inducing-like proteins Nlp2 and Nlp3, the cerato-platanin proteins Cp1 and Cp2, the metallopeptidases Mep1 and Mep2 and the carbohydrate-active enzymes Gla1, Amy1 and Cbd1. Their pathogenicity contribution was analyzed in the haploid parental strain <i>V. dahliae</i>. Deletion of the majority of the corresponding genes caused no phenotypic changes during <i>ex planta</i> growth or invasion and colonization of tomato plants. However, we discovered that the <i>MEP1</i>, <i>NLP2</i>, and <i>NLP3</i> deletion strains were compromised in plant infections. Overall, our exoproteome approach revealed that the fungus induces specific secretion responses in different environments. The fungus has a general response to non-plant related media whereas it is able to fine-tune its exoproteome in the presence of plant material. Importantly, the xylem sap-specific exoproteome pinpointed Nlp2 and Nlp3 as single effectors required for successful <i>V. dahliae</i> colonization.</AbstractText><CopyrightInformation>Copyright © 2020 Leonard, Kühn, Harting, Maurus, Nagel, Starke, Kusch, Valerius, Feussner, Feussner, Kaever, Landesfeind, Morgenstern, Becher, Hecker, Braus-Stromeyer, Kronstad and Braus.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Leonard</LastName><ForeName>Miriam</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kühn</LastName><ForeName>Anika</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Harting</LastName><ForeName>Rebekka</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maurus</LastName><ForeName>Isabel</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nagel</LastName><ForeName>Alexandra</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Starke</LastName><ForeName>Jessica</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kusch</LastName><ForeName>Harald</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Valerius</LastName><ForeName>Oliver</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feussner</LastName><ForeName>Kirstin</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feussner</LastName><ForeName>Ivo</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>Department for Plant Biochemistry, Göttingen Center for Molecular Biosciences, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kaever</LastName><ForeName>Alexander</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Landesfeind</LastName><ForeName>Manuel</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Morgenstern</LastName><ForeName>Burkhard</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Department of Bioinformatics, Göttingen Center for Molecular Biosciences, Institute for Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Becher</LastName><ForeName>Dörte</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department Microbial Proteomics, Institute for Microbiology, University of Greifswald, Greifswald, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hecker</LastName><ForeName>Michael</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Microbial Physiology, Institute for Microbiology, University of Greifswald, Greifswald, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Braus-Stromeyer</LastName><ForeName>Susanna A</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kronstad</LastName><ForeName>James W</ForeName><Initials>JW</Initials><AffiliationInfo><Affiliation>Michael Smith Laboratories, Department of Microbiology and Immunology, The University of British Columbia, Vancouver, BC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Braus</LastName><ForeName>Gerhard H</ForeName><Initials>GH</Initials><AffiliationInfo><Affiliation>Department of Molecular Microbiology and Genetics, Göttingen Center for Molecular Biosciences, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>08</Month><Day>06</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Nep1-like proteins</Keyword><Keyword MajorTopicYN="N">Verticillium dahliae</Keyword><Keyword MajorTopicYN="N">Verticillium longisporum</Keyword><Keyword MajorTopicYN="N">effectors</Keyword><Keyword MajorTopicYN="N">plant pathogen</Keyword><Keyword MajorTopicYN="N">plant- and media-dependent exoproteomes</Keyword><Keyword MajorTopicYN="N">xylem</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>04</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>07</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>8</Month><Day>28</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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last="Becher">Dörte Becher</name><name sortKey="Braus Stromeyer, Susanna A" sort="Braus Stromeyer, Susanna A" uniqKey="Braus Stromeyer S" first="Susanna A" last="Braus-Stromeyer">Susanna A. Braus-Stromeyer</name><name sortKey="Braus, Gerhard H" sort="Braus, Gerhard H" uniqKey="Braus G" first="Gerhard H" last="Braus">Gerhard H. Braus</name><name sortKey="Feussner, Ivo" sort="Feussner, Ivo" uniqKey="Feussner I" first="Ivo" last="Feussner">Ivo Feussner</name><name sortKey="Feussner, Kirstin" sort="Feussner, Kirstin" uniqKey="Feussner K" first="Kirstin" last="Feussner">Kirstin Feussner</name><name sortKey="Harting, Rebekka" sort="Harting, Rebekka" uniqKey="Harting R" first="Rebekka" last="Harting">Rebekka Harting</name><name sortKey="Hecker, Michael" sort="Hecker, Michael" uniqKey="Hecker M" first="Michael" last="Hecker">Michael Hecker</name><name sortKey="Kaever, Alexander" sort="Kaever, Alexander" uniqKey="Kaever A" first="Alexander" last="Kaever">Alexander Kaever</name><name sortKey="Kuhn, Anika" sort="Kuhn, Anika" uniqKey="Kuhn A" first="Anika" last="Kühn">Anika Kühn</name><name sortKey="Kusch, Harald" sort="Kusch, Harald" uniqKey="Kusch H" first="Harald" last="Kusch">Harald Kusch</name><name sortKey="Landesfeind, Manuel" sort="Landesfeind, Manuel" uniqKey="Landesfeind M" first="Manuel" last="Landesfeind">Manuel Landesfeind</name><name sortKey="Maurus, Isabel" sort="Maurus, Isabel" uniqKey="Maurus I" first="Isabel" last="Maurus">Isabel Maurus</name><name sortKey="Morgenstern, Burkhard" sort="Morgenstern, Burkhard" uniqKey="Morgenstern B" first="Burkhard" last="Morgenstern">Burkhard Morgenstern</name><name sortKey="Nagel, Alexandra" sort="Nagel, Alexandra" uniqKey="Nagel A" first="Alexandra" last="Nagel">Alexandra Nagel</name><name sortKey="Starke, Jessica" sort="Starke, Jessica" uniqKey="Starke J" first="Jessica" last="Starke">Jessica Starke</name><name sortKey="Valerius, Oliver" sort="Valerius, Oliver" uniqKey="Valerius O" first="Oliver" last="Valerius">Oliver Valerius</name></country><country name="Canada"><region name="Colombie-Britannique "><name sortKey="Kronstad, James W" sort="Kronstad, James W" uniqKey="Kronstad J" first="James W" last="Kronstad">James W. 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