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Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice

BACKGROUND: Induced resistance is a state of enhanced defensive capacity developed by a plant reacting to specific biotic or chemical stimuli. Over the years, several forms of induced resistance have been characterized, including systemic acquired resistance, which is induced upon localized infectio...

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Autores principales: De Vleesschauwer, David, Chernin, Leonid, Höfte, Monica M
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2650696/
https://www.ncbi.nlm.nih.gov/pubmed/19161601
http://dx.doi.org/10.1186/1471-2229-9-9
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author De Vleesschauwer, David
Chernin, Leonid
Höfte, Monica M
author_facet De Vleesschauwer, David
Chernin, Leonid
Höfte, Monica M
author_sort De Vleesschauwer, David
collection PubMed
description BACKGROUND: Induced resistance is a state of enhanced defensive capacity developed by a plant reacting to specific biotic or chemical stimuli. Over the years, several forms of induced resistance have been characterized, including systemic acquired resistance, which is induced upon localized infection by an avirulent necrotizing pathogen, and induced systemic resistance (ISR), which is elicited by selected strains of nonpathogenic rhizobacteria. However, contrary to the relative wealth of information on inducible defense responses in dicotyledoneous plants, our understanding of the molecular mechanisms underlying induced resistance phenomena in cereal crops is still in its infancy. Using a combined cytomolecular and pharmacological approach, we analyzed the host defense mechanisms associated with the establishment of ISR in rice by the rhizobacterium Serratia plymuthica IC1270. RESULTS: In a standardized soil-based assay, root treatment with IC1270 rendered foliar tissues more resistant to the hemibiotrophic pathogen Magnaporthe oryzae, causal agent of the devastating rice blast disease. Analysis of the cytological and biochemical alterations associated with restriction of fungal growth in IC1270-induced plants revealed that IC1270 primes rice for enhanced attacker-induced accumulation of reactive oxygen species (ROS) and autofluorescent phenolic compounds in and near epidermal cells displaying dense cytoplasmic granulation. Similar, yet more abundant, phenotypes of hypersensitively dying cells in the vicinity of fungal hyphae were evident in a gene-for-gene interaction with an avirulent M. oryzae strain, suggesting that IC1270-inducible ISR and R protein conditioned effector-triggered immunity (ETI) target similar defense mechanisms. Yet, this IC1270-inducible ISR response seems to act as a double-edged sword within the rice defense network as induced plants displayed an increased vulnerability to the necrotrophic pathogens Rhizoctonia solani and Cochliobolus miyabeanus. Artificial enhancement of ROS levels in inoculated leaves faithfully mimicked the opposite effects of IC1270 bacteria on aforementioned pathogens, suggesting a central role for oxidative events in the IC1270-induced resistance mechanism. CONCLUSION: Besides identifying ROS as modulators of antagonistic defense mechanisms in rice, this work reveals the mechanistic similarities between S. plymuthica-mediated ISR and R protein-dictated ETI and underscores the importance of using appropriate innate defense mechanisms when breeding for broad-spectrum rice disease resistance.
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spelling pubmed-26506962009-03-04 Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice De Vleesschauwer, David Chernin, Leonid Höfte, Monica M BMC Plant Biol Research Article BACKGROUND: Induced resistance is a state of enhanced defensive capacity developed by a plant reacting to specific biotic or chemical stimuli. Over the years, several forms of induced resistance have been characterized, including systemic acquired resistance, which is induced upon localized infection by an avirulent necrotizing pathogen, and induced systemic resistance (ISR), which is elicited by selected strains of nonpathogenic rhizobacteria. However, contrary to the relative wealth of information on inducible defense responses in dicotyledoneous plants, our understanding of the molecular mechanisms underlying induced resistance phenomena in cereal crops is still in its infancy. Using a combined cytomolecular and pharmacological approach, we analyzed the host defense mechanisms associated with the establishment of ISR in rice by the rhizobacterium Serratia plymuthica IC1270. RESULTS: In a standardized soil-based assay, root treatment with IC1270 rendered foliar tissues more resistant to the hemibiotrophic pathogen Magnaporthe oryzae, causal agent of the devastating rice blast disease. Analysis of the cytological and biochemical alterations associated with restriction of fungal growth in IC1270-induced plants revealed that IC1270 primes rice for enhanced attacker-induced accumulation of reactive oxygen species (ROS) and autofluorescent phenolic compounds in and near epidermal cells displaying dense cytoplasmic granulation. Similar, yet more abundant, phenotypes of hypersensitively dying cells in the vicinity of fungal hyphae were evident in a gene-for-gene interaction with an avirulent M. oryzae strain, suggesting that IC1270-inducible ISR and R protein conditioned effector-triggered immunity (ETI) target similar defense mechanisms. Yet, this IC1270-inducible ISR response seems to act as a double-edged sword within the rice defense network as induced plants displayed an increased vulnerability to the necrotrophic pathogens Rhizoctonia solani and Cochliobolus miyabeanus. Artificial enhancement of ROS levels in inoculated leaves faithfully mimicked the opposite effects of IC1270 bacteria on aforementioned pathogens, suggesting a central role for oxidative events in the IC1270-induced resistance mechanism. CONCLUSION: Besides identifying ROS as modulators of antagonistic defense mechanisms in rice, this work reveals the mechanistic similarities between S. plymuthica-mediated ISR and R protein-dictated ETI and underscores the importance of using appropriate innate defense mechanisms when breeding for broad-spectrum rice disease resistance. BioMed Central 2009-01-22 /pmc/articles/PMC2650696/ /pubmed/19161601 http://dx.doi.org/10.1186/1471-2229-9-9 Text en Copyright © 2009 De Vleesschauwer et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
De Vleesschauwer, David
Chernin, Leonid
Höfte, Monica M
Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
title Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
title_full Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
title_fullStr Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
title_full_unstemmed Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
title_short Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
title_sort differential effectiveness of serratia plymuthica ic1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2650696/
https://www.ncbi.nlm.nih.gov/pubmed/19161601
http://dx.doi.org/10.1186/1471-2229-9-9
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