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Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola

BACKGROUND: Glutathione transferases (GSTs) represent an extended family of multifunctional proteins involved in detoxification processes and tolerance to oxidative stress. We thus anticipated that some GSTs could play an essential role in the protection of fungal necrotrophs against plant-derived t...

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Autores principales: Calmes, Benoit, Morel-Rouhier, Mélanie, Bataillé-Simoneau, Nelly, Gelhaye, Eric, Guillemette, Thomas, Simoneau, Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470081/
https://www.ncbi.nlm.nih.gov/pubmed/26081847
http://dx.doi.org/10.1186/s12866-015-0462-0
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author Calmes, Benoit
Morel-Rouhier, Mélanie
Bataillé-Simoneau, Nelly
Gelhaye, Eric
Guillemette, Thomas
Simoneau, Philippe
author_facet Calmes, Benoit
Morel-Rouhier, Mélanie
Bataillé-Simoneau, Nelly
Gelhaye, Eric
Guillemette, Thomas
Simoneau, Philippe
author_sort Calmes, Benoit
collection PubMed
description BACKGROUND: Glutathione transferases (GSTs) represent an extended family of multifunctional proteins involved in detoxification processes and tolerance to oxidative stress. We thus anticipated that some GSTs could play an essential role in the protection of fungal necrotrophs against plant-derived toxic metabolites and reactive oxygen species that accumulate at the host-pathogen interface during infection. RESULTS: Mining the genome of the necrotrophic Brassica pathogen Alternaria brassicicola for glutathione transferase revealed 23 sequences, 17 of which could be clustered into the main classes previously defined for fungal GSTs and six were ‘orphans’. Five isothiocyanate-inducible GSTs from five different classes were more thoroughly investigated. Analysis of their catalytic properties revealed that two GSTs, belonging to the GSTFuA and GTT1 classes, exhibited GSH transferase activity with isothiocyanates (ITC) and peroxidase activity with cumene hydroperoxide, respectively. Mutant deficient for these two GSTs were however neither more susceptible to ITC nor less aggressive than the wild-type parental strain. By contrast mutants deficient for two other GSTs, belonging to the Ure2pB and GSTO classes, were distinguished by their hyper-susceptibility to ITC and low aggressiveness against Brassica oleracea. In particular AbGSTO1 could participate in cell tolerance to ITC due to its glutathione-dependent thioltransferase activity. The fifth ITC-inducible GST belonged to the MAPEG class and although it was not possible to produce the soluble active form of this protein in a bacterial expression system, the corresponding deficient mutant failed to develop normal symptoms on host plant tissues. CONCLUSIONS: Among the five ITC-inducible GSTs analyzed in this study, three were found essential for full aggressiveness of A. brassicicola on host plant. This, to our knowledge is the first evidence that GSTs might be essential virulence factors for fungal necrotrophs. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-015-0462-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-44700812015-06-18 Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola Calmes, Benoit Morel-Rouhier, Mélanie Bataillé-Simoneau, Nelly Gelhaye, Eric Guillemette, Thomas Simoneau, Philippe BMC Microbiol Research Article BACKGROUND: Glutathione transferases (GSTs) represent an extended family of multifunctional proteins involved in detoxification processes and tolerance to oxidative stress. We thus anticipated that some GSTs could play an essential role in the protection of fungal necrotrophs against plant-derived toxic metabolites and reactive oxygen species that accumulate at the host-pathogen interface during infection. RESULTS: Mining the genome of the necrotrophic Brassica pathogen Alternaria brassicicola for glutathione transferase revealed 23 sequences, 17 of which could be clustered into the main classes previously defined for fungal GSTs and six were ‘orphans’. Five isothiocyanate-inducible GSTs from five different classes were more thoroughly investigated. Analysis of their catalytic properties revealed that two GSTs, belonging to the GSTFuA and GTT1 classes, exhibited GSH transferase activity with isothiocyanates (ITC) and peroxidase activity with cumene hydroperoxide, respectively. Mutant deficient for these two GSTs were however neither more susceptible to ITC nor less aggressive than the wild-type parental strain. By contrast mutants deficient for two other GSTs, belonging to the Ure2pB and GSTO classes, were distinguished by their hyper-susceptibility to ITC and low aggressiveness against Brassica oleracea. In particular AbGSTO1 could participate in cell tolerance to ITC due to its glutathione-dependent thioltransferase activity. The fifth ITC-inducible GST belonged to the MAPEG class and although it was not possible to produce the soluble active form of this protein in a bacterial expression system, the corresponding deficient mutant failed to develop normal symptoms on host plant tissues. CONCLUSIONS: Among the five ITC-inducible GSTs analyzed in this study, three were found essential for full aggressiveness of A. brassicicola on host plant. This, to our knowledge is the first evidence that GSTs might be essential virulence factors for fungal necrotrophs. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-015-0462-0) contains supplementary material, which is available to authorized users. BioMed Central 2015-06-18 /pmc/articles/PMC4470081/ /pubmed/26081847 http://dx.doi.org/10.1186/s12866-015-0462-0 Text en © Calmes et al. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Calmes, Benoit
Morel-Rouhier, Mélanie
Bataillé-Simoneau, Nelly
Gelhaye, Eric
Guillemette, Thomas
Simoneau, Philippe
Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola
title Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola
title_full Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola
title_fullStr Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola
title_full_unstemmed Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola
title_short Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola
title_sort characterization of glutathione transferases involved in the pathogenicity of alternaria brassicicola
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470081/
https://www.ncbi.nlm.nih.gov/pubmed/26081847
http://dx.doi.org/10.1186/s12866-015-0462-0
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