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Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea

The grey mould fungus Botrytis cinerea causes losses of commercially important fruits, vegetables and ornamentals worldwide. Fungicide treatments are effective for disease control, but bear the risk of resistance development. The major resistance mechanism in fungi is target protein modification res...

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Autores principales: Kretschmer, Matthias, Leroch, Michaela, Mosbach, Andreas, Walker, Anne-Sophie, Fillinger, Sabine, Mernke, Dennis, Schoonbeek, Henk-Jan, Pradier, Jean-Marc, Leroux, Pierre, De Waard, Maarten A., Hahn, Matthias
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2785876/
https://www.ncbi.nlm.nih.gov/pubmed/20019793
http://dx.doi.org/10.1371/journal.ppat.1000696
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author Kretschmer, Matthias
Leroch, Michaela
Mosbach, Andreas
Walker, Anne-Sophie
Fillinger, Sabine
Mernke, Dennis
Schoonbeek, Henk-Jan
Pradier, Jean-Marc
Leroux, Pierre
De Waard, Maarten A.
Hahn, Matthias
author_facet Kretschmer, Matthias
Leroch, Michaela
Mosbach, Andreas
Walker, Anne-Sophie
Fillinger, Sabine
Mernke, Dennis
Schoonbeek, Henk-Jan
Pradier, Jean-Marc
Leroux, Pierre
De Waard, Maarten A.
Hahn, Matthias
author_sort Kretschmer, Matthias
collection PubMed
description The grey mould fungus Botrytis cinerea causes losses of commercially important fruits, vegetables and ornamentals worldwide. Fungicide treatments are effective for disease control, but bear the risk of resistance development. The major resistance mechanism in fungi is target protein modification resulting in reduced drug binding. Multiple drug resistance (MDR) caused by increased efflux activity is common in human pathogenic microbes, but rarely described for plant pathogens. Annual monitoring for fungicide resistance in field isolates from fungicide-treated vineyards in France and Germany revealed a rapidly increasing appearance of B. cinerea field populations with three distinct MDR phenotypes. All MDR strains showed increased fungicide efflux activity and overexpression of efflux transporter genes. Similar to clinical MDR isolates of Candida yeasts that are due to transcription factor mutations, all MDR1 strains were shown to harbor activating mutations in a transcription factor (Mrr1) that controls the gene encoding ABC transporter AtrB. MDR2 strains had undergone a unique rearrangement in the promoter region of the major facilitator superfamily transporter gene mfsM2, induced by insertion of a retrotransposon-derived sequence. MDR2 strains carrying the same rearranged mfsM2 allele have probably migrated from French to German wine-growing regions. The roles of atrB, mrr1 and mfsM2 were proven by the phenotypes of knock-out and overexpression mutants. As confirmed by sexual crosses, combinations of mrr1 and mfsM2 mutations lead to MDR3 strains with higher broad-spectrum resistance. An MDR3 strain was shown in field experiments to be selected against sensitive strains by fungicide treatments. Our data document for the first time the rising prevalence, spread and molecular basis of MDR populations in a major plant pathogen in agricultural environments. These populations will increase the risk of grey mould rot and hamper the effectiveness of current strategies for fungicide resistance management.
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spelling pubmed-27858762009-12-18 Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea Kretschmer, Matthias Leroch, Michaela Mosbach, Andreas Walker, Anne-Sophie Fillinger, Sabine Mernke, Dennis Schoonbeek, Henk-Jan Pradier, Jean-Marc Leroux, Pierre De Waard, Maarten A. Hahn, Matthias PLoS Pathog Research Article The grey mould fungus Botrytis cinerea causes losses of commercially important fruits, vegetables and ornamentals worldwide. Fungicide treatments are effective for disease control, but bear the risk of resistance development. The major resistance mechanism in fungi is target protein modification resulting in reduced drug binding. Multiple drug resistance (MDR) caused by increased efflux activity is common in human pathogenic microbes, but rarely described for plant pathogens. Annual monitoring for fungicide resistance in field isolates from fungicide-treated vineyards in France and Germany revealed a rapidly increasing appearance of B. cinerea field populations with three distinct MDR phenotypes. All MDR strains showed increased fungicide efflux activity and overexpression of efflux transporter genes. Similar to clinical MDR isolates of Candida yeasts that are due to transcription factor mutations, all MDR1 strains were shown to harbor activating mutations in a transcription factor (Mrr1) that controls the gene encoding ABC transporter AtrB. MDR2 strains had undergone a unique rearrangement in the promoter region of the major facilitator superfamily transporter gene mfsM2, induced by insertion of a retrotransposon-derived sequence. MDR2 strains carrying the same rearranged mfsM2 allele have probably migrated from French to German wine-growing regions. The roles of atrB, mrr1 and mfsM2 were proven by the phenotypes of knock-out and overexpression mutants. As confirmed by sexual crosses, combinations of mrr1 and mfsM2 mutations lead to MDR3 strains with higher broad-spectrum resistance. An MDR3 strain was shown in field experiments to be selected against sensitive strains by fungicide treatments. Our data document for the first time the rising prevalence, spread and molecular basis of MDR populations in a major plant pathogen in agricultural environments. These populations will increase the risk of grey mould rot and hamper the effectiveness of current strategies for fungicide resistance management. Public Library of Science 2009-12-18 /pmc/articles/PMC2785876/ /pubmed/20019793 http://dx.doi.org/10.1371/journal.ppat.1000696 Text en Kretschmer et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kretschmer, Matthias
Leroch, Michaela
Mosbach, Andreas
Walker, Anne-Sophie
Fillinger, Sabine
Mernke, Dennis
Schoonbeek, Henk-Jan
Pradier, Jean-Marc
Leroux, Pierre
De Waard, Maarten A.
Hahn, Matthias
Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea
title Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea
title_full Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea
title_fullStr Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea
title_full_unstemmed Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea
title_short Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea
title_sort fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus botrytis cinerea
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2785876/
https://www.ncbi.nlm.nih.gov/pubmed/20019793
http://dx.doi.org/10.1371/journal.ppat.1000696
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