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Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum

BACKGROUND: Fusarium Head Blight (FHB) caused primarily by Fusarium graminearum (Fg) is one of the major diseases of small-grain cereals including bread wheat. This disease both reduces yields and causes quality losses due to the production of deoxynivalenol (DON), the major type B trichothecene myc...

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Autores principales: Pasquet, Jean-Claude, Chaouch, Séjir, Macadré, Catherine, Balzergue, Sandrine, Huguet, Stéphanie, Martin-Magniette, Marie-Laure, Bellvert, Floriant, Deguercy, Xavier, Thareau, Vincent, Heintz, Dimitri, Saindrenan, Patrick, Dufresne, Marie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4124148/
https://www.ncbi.nlm.nih.gov/pubmed/25063396
http://dx.doi.org/10.1186/1471-2164-15-629
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author Pasquet, Jean-Claude
Chaouch, Séjir
Macadré, Catherine
Balzergue, Sandrine
Huguet, Stéphanie
Martin-Magniette, Marie-Laure
Bellvert, Floriant
Deguercy, Xavier
Thareau, Vincent
Heintz, Dimitri
Saindrenan, Patrick
Dufresne, Marie
author_facet Pasquet, Jean-Claude
Chaouch, Séjir
Macadré, Catherine
Balzergue, Sandrine
Huguet, Stéphanie
Martin-Magniette, Marie-Laure
Bellvert, Floriant
Deguercy, Xavier
Thareau, Vincent
Heintz, Dimitri
Saindrenan, Patrick
Dufresne, Marie
author_sort Pasquet, Jean-Claude
collection PubMed
description BACKGROUND: Fusarium Head Blight (FHB) caused primarily by Fusarium graminearum (Fg) is one of the major diseases of small-grain cereals including bread wheat. This disease both reduces yields and causes quality losses due to the production of deoxynivalenol (DON), the major type B trichothecene mycotoxin. DON has been described as a virulence factor enabling efficient colonization of spikes by the fungus in wheat, but its precise role during the infection process is still elusive. Brachypodium distachyon (Bd) is a model cereal species which has been shown to be susceptible to FHB. Here, a functional genomics approach was performed in order to characterize the responses of Bd to Fg infection using a global transcriptional and metabolomic profiling of B. distachyon plants infected by two strains of F. graminearum: a wild-type strain producing DON (Fgdon(+)) and a mutant strain impaired in the production of the mycotoxin (Fgdon(-)). RESULTS: Histological analysis of the interaction of the Bd21 ecotype with both Fg strains showed extensive fungal tissue colonization with the Fgdon(+) strain while the florets infected with the Fgdon(-) strain exhibited a reduced hyphal extension and cell death on palea and lemma tissues. Fungal biomass was reduced in spikes inoculated with the Fgdon(-) strain as compared with the wild-type strain. The transcriptional analysis showed that jasmonate and ethylene-signalling pathways are induced upon infection, together with genes encoding putative detoxification and transport proteins, antioxidant functions as well as secondary metabolite pathways. In particular, our metabolite profiling analysis showed that tryptophan-derived metabolites, tryptamine, serotonin, coumaroyl-serotonin and feruloyl-serotonin, are more induced upon infection by the Fgdon(+) strain than by the Fgdon(-) strain. Serotonin was shown to exhibit a slight direct antimicrobial effect against Fg. CONCLUSION: Our results show that Bd exhibits defense hallmarks similar to those already identified in cereal crops. While the fungus uses DON as a virulence factor, the host plant preferentially induces detoxification and the phenylpropanoid and phenolamide pathways as resistance mechanisms. Together with its amenability in laboratory conditions, this makes Bd a very good model to study cereal resistance mechanisms towards the major disease FHB. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-629) contains supplementary material, which is available to authorized users.
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spelling pubmed-41241482014-08-12 Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum Pasquet, Jean-Claude Chaouch, Séjir Macadré, Catherine Balzergue, Sandrine Huguet, Stéphanie Martin-Magniette, Marie-Laure Bellvert, Floriant Deguercy, Xavier Thareau, Vincent Heintz, Dimitri Saindrenan, Patrick Dufresne, Marie BMC Genomics Research Article BACKGROUND: Fusarium Head Blight (FHB) caused primarily by Fusarium graminearum (Fg) is one of the major diseases of small-grain cereals including bread wheat. This disease both reduces yields and causes quality losses due to the production of deoxynivalenol (DON), the major type B trichothecene mycotoxin. DON has been described as a virulence factor enabling efficient colonization of spikes by the fungus in wheat, but its precise role during the infection process is still elusive. Brachypodium distachyon (Bd) is a model cereal species which has been shown to be susceptible to FHB. Here, a functional genomics approach was performed in order to characterize the responses of Bd to Fg infection using a global transcriptional and metabolomic profiling of B. distachyon plants infected by two strains of F. graminearum: a wild-type strain producing DON (Fgdon(+)) and a mutant strain impaired in the production of the mycotoxin (Fgdon(-)). RESULTS: Histological analysis of the interaction of the Bd21 ecotype with both Fg strains showed extensive fungal tissue colonization with the Fgdon(+) strain while the florets infected with the Fgdon(-) strain exhibited a reduced hyphal extension and cell death on palea and lemma tissues. Fungal biomass was reduced in spikes inoculated with the Fgdon(-) strain as compared with the wild-type strain. The transcriptional analysis showed that jasmonate and ethylene-signalling pathways are induced upon infection, together with genes encoding putative detoxification and transport proteins, antioxidant functions as well as secondary metabolite pathways. In particular, our metabolite profiling analysis showed that tryptophan-derived metabolites, tryptamine, serotonin, coumaroyl-serotonin and feruloyl-serotonin, are more induced upon infection by the Fgdon(+) strain than by the Fgdon(-) strain. Serotonin was shown to exhibit a slight direct antimicrobial effect against Fg. CONCLUSION: Our results show that Bd exhibits defense hallmarks similar to those already identified in cereal crops. While the fungus uses DON as a virulence factor, the host plant preferentially induces detoxification and the phenylpropanoid and phenolamide pathways as resistance mechanisms. Together with its amenability in laboratory conditions, this makes Bd a very good model to study cereal resistance mechanisms towards the major disease FHB. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-629) contains supplementary material, which is available to authorized users. BioMed Central 2014-07-25 /pmc/articles/PMC4124148/ /pubmed/25063396 http://dx.doi.org/10.1186/1471-2164-15-629 Text en © Pasquet et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. 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
Pasquet, Jean-Claude
Chaouch, Séjir
Macadré, Catherine
Balzergue, Sandrine
Huguet, Stéphanie
Martin-Magniette, Marie-Laure
Bellvert, Floriant
Deguercy, Xavier
Thareau, Vincent
Heintz, Dimitri
Saindrenan, Patrick
Dufresne, Marie
Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum
title Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum
title_full Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum
title_fullStr Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum
title_full_unstemmed Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum
title_short Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum
title_sort differential gene expression and metabolomic analyses of brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of fusarium graminearum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4124148/
https://www.ncbi.nlm.nih.gov/pubmed/25063396
http://dx.doi.org/10.1186/1471-2164-15-629
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