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Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis

The biotrophic fungus Ustilago maydis harbors a chitin deacetylase (CDA) family of six active genes as well as one pseudogene which are differentially expressed during colonization. This includes one secreted soluble CDA (Cda4) and five putatively glycosylphosphatidylinositol (GPI)-anchored CDAs, of...

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Autores principales: Rizzi, Yanina S., Happel, Petra, Lenz, Sandra, Urs, Mounashree J., Bonin, Martin, Cord-Landwehr, Stefan, Singh, Ratna, Moerschbacher, Bruno M., Kahmann, Regine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8092297/
https://www.ncbi.nlm.nih.gov/pubmed/33653886
http://dx.doi.org/10.1128/mBio.03419-20
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author Rizzi, Yanina S.
Happel, Petra
Lenz, Sandra
Urs, Mounashree J.
Bonin, Martin
Cord-Landwehr, Stefan
Singh, Ratna
Moerschbacher, Bruno M.
Kahmann, Regine
author_facet Rizzi, Yanina S.
Happel, Petra
Lenz, Sandra
Urs, Mounashree J.
Bonin, Martin
Cord-Landwehr, Stefan
Singh, Ratna
Moerschbacher, Bruno M.
Kahmann, Regine
author_sort Rizzi, Yanina S.
collection PubMed
description The biotrophic fungus Ustilago maydis harbors a chitin deacetylase (CDA) family of six active genes as well as one pseudogene which are differentially expressed during colonization. This includes one secreted soluble CDA (Cda4) and five putatively glycosylphosphatidylinositol (GPI)-anchored CDAs, of which Cda7 belongs to a new class of fungal CDAs. Here, we provide a comprehensive functional study of the entire family. While budding cells of U. maydis showed a discrete pattern of chitosan staining, biotrophic hyphae appeared surrounded by a chitosan layer. We purified all six active CDAs and show their activity on different chitin substrates. Single as well as multiple cda mutants were generated and revealed a virulence defect for mutants lacking cda7. We implicated cda4 in production of the chitosan layer surrounding biotrophic hyphae and demonstrated that the loss of this layer does not reduce virulence. By combining different cda mutations, we detected redundancy as well as specific functions for certain CDAs. Specifically, certain combinations of mutations significantly affected virulence concomitantly with reduced adherence, appressorium formation, penetration, and activation of plant defenses. Attempts to inactivate all seven cda genes simultaneously were unsuccessful, and induced depletion of cda2 in a background lacking the other six cda genes illustrated an essential role of chitosan for cell wall integrity.
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spelling pubmed-80922972021-05-04 Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis Rizzi, Yanina S. Happel, Petra Lenz, Sandra Urs, Mounashree J. Bonin, Martin Cord-Landwehr, Stefan Singh, Ratna Moerschbacher, Bruno M. Kahmann, Regine mBio Research Article The biotrophic fungus Ustilago maydis harbors a chitin deacetylase (CDA) family of six active genes as well as one pseudogene which are differentially expressed during colonization. This includes one secreted soluble CDA (Cda4) and five putatively glycosylphosphatidylinositol (GPI)-anchored CDAs, of which Cda7 belongs to a new class of fungal CDAs. Here, we provide a comprehensive functional study of the entire family. While budding cells of U. maydis showed a discrete pattern of chitosan staining, biotrophic hyphae appeared surrounded by a chitosan layer. We purified all six active CDAs and show their activity on different chitin substrates. Single as well as multiple cda mutants were generated and revealed a virulence defect for mutants lacking cda7. We implicated cda4 in production of the chitosan layer surrounding biotrophic hyphae and demonstrated that the loss of this layer does not reduce virulence. By combining different cda mutations, we detected redundancy as well as specific functions for certain CDAs. Specifically, certain combinations of mutations significantly affected virulence concomitantly with reduced adherence, appressorium formation, penetration, and activation of plant defenses. Attempts to inactivate all seven cda genes simultaneously were unsuccessful, and induced depletion of cda2 in a background lacking the other six cda genes illustrated an essential role of chitosan for cell wall integrity. American Society for Microbiology 2021-03-02 /pmc/articles/PMC8092297/ /pubmed/33653886 http://dx.doi.org/10.1128/mBio.03419-20 Text en Copyright © 2021 Rizzi et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Rizzi, Yanina S.
Happel, Petra
Lenz, Sandra
Urs, Mounashree J.
Bonin, Martin
Cord-Landwehr, Stefan
Singh, Ratna
Moerschbacher, Bruno M.
Kahmann, Regine
Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis
title Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis
title_full Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis
title_fullStr Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis
title_full_unstemmed Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis
title_short Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis
title_sort chitosan and chitin deacetylase activity are necessary for development and virulence of ustilago maydis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8092297/
https://www.ncbi.nlm.nih.gov/pubmed/33653886
http://dx.doi.org/10.1128/mBio.03419-20
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