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The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings

BACKGROUND AND AIMS: Ramularia collo-cygni is an ascomycete fungus that colonizes barley primarily as a benign endophyte, although this interaction can become pathogenic, causing the disease Ramularia leaf spot (RLS). Factors, particularly reactive oxygen species, that resulted in the transition of...

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Autores principales: McGrann, Graham R D, Brown, James K M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5838821/
https://www.ncbi.nlm.nih.gov/pubmed/29309539
http://dx.doi.org/10.1093/aob/mcx170
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author McGrann, Graham R D
Brown, James K M
author_facet McGrann, Graham R D
Brown, James K M
author_sort McGrann, Graham R D
collection PubMed
description BACKGROUND AND AIMS: Ramularia collo-cygni is an ascomycete fungus that colonizes barley primarily as a benign endophyte, although this interaction can become pathogenic, causing the disease Ramularia leaf spot (RLS). Factors, particularly reactive oxygen species, that resulted in the transition of the fungus from endophyte to necrotrophic parasite and the development of disease symptoms were investigated. METHODS: Disease development in artificially inoculated seedlings of barley varieties varying in partial resistance to RLS was related to exposure to abiotic stress prior to inoculation. Histochemical and molecular analysis determined the effect of R. collo-cygni colonization on accumulation of reactive oxygen species and antioxidant gene expression. Development of RLS on barley lines defective in antioxidant enzymes and with altered redox status or non-functional chloroplasts was compared with the accumulation of fungal biomass to determine how these factors affect disease symptom expression. KEY RESULTS: Exposure to abiotic stress increased symptom development in all susceptible and most partially resistant barley varieties, in association with greater hydrogen peroxide (H(2)O(2)) levels in leaves. Decreased activity of the antioxidant enzymes superoxide dismutase and catalase in transgenic and mutant plants had no effect on the disease transition, whereas manipulation of H(2)O(2) levels during asymptomatic growth of the fungus increased disease symptoms in most susceptible varieties but not in partially resistant plants. Barley mutants that undergo rapid loss of green leaf area when infected by R. collo-cygni or albino mutants with non-functional chloroplasts showed reduced development of RLS symptoms. CONCLUSIONS: These results imply that in seedlings the pathogenic transition of the normally endophytic fungus R. collo-cygni does not result from senescence as such, but rather is promoted by factors that result in changes to host reactive oxygen species. Barley varieties vary in the extent to which these factors promote RLS disease.
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spelling pubmed-58388212018-03-28 The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings McGrann, Graham R D Brown, James K M Ann Bot Original Articles BACKGROUND AND AIMS: Ramularia collo-cygni is an ascomycete fungus that colonizes barley primarily as a benign endophyte, although this interaction can become pathogenic, causing the disease Ramularia leaf spot (RLS). Factors, particularly reactive oxygen species, that resulted in the transition of the fungus from endophyte to necrotrophic parasite and the development of disease symptoms were investigated. METHODS: Disease development in artificially inoculated seedlings of barley varieties varying in partial resistance to RLS was related to exposure to abiotic stress prior to inoculation. Histochemical and molecular analysis determined the effect of R. collo-cygni colonization on accumulation of reactive oxygen species and antioxidant gene expression. Development of RLS on barley lines defective in antioxidant enzymes and with altered redox status or non-functional chloroplasts was compared with the accumulation of fungal biomass to determine how these factors affect disease symptom expression. KEY RESULTS: Exposure to abiotic stress increased symptom development in all susceptible and most partially resistant barley varieties, in association with greater hydrogen peroxide (H(2)O(2)) levels in leaves. Decreased activity of the antioxidant enzymes superoxide dismutase and catalase in transgenic and mutant plants had no effect on the disease transition, whereas manipulation of H(2)O(2) levels during asymptomatic growth of the fungus increased disease symptoms in most susceptible varieties but not in partially resistant plants. Barley mutants that undergo rapid loss of green leaf area when infected by R. collo-cygni or albino mutants with non-functional chloroplasts showed reduced development of RLS symptoms. CONCLUSIONS: These results imply that in seedlings the pathogenic transition of the normally endophytic fungus R. collo-cygni does not result from senescence as such, but rather is promoted by factors that result in changes to host reactive oxygen species. Barley varieties vary in the extent to which these factors promote RLS disease. Oxford University Press 2018-03 2017-12-22 /pmc/articles/PMC5838821/ /pubmed/29309539 http://dx.doi.org/10.1093/aob/mcx170 Text en © The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. http://creativecommons.org/licenses/by/4.0/ 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
McGrann, Graham R D
Brown, James K M
The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings
title The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings
title_full The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings
title_fullStr The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings
title_full_unstemmed The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings
title_short The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings
title_sort role of reactive oxygen in the development of ramularia leaf spot disease in barley seedlings
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5838821/
https://www.ncbi.nlm.nih.gov/pubmed/29309539
http://dx.doi.org/10.1093/aob/mcx170
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