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Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana

BACKGROUND: Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused...

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Autores principales: Prince, David C., Rallapalli, Ghanasyam, Xu, Deyang, Schoonbeek, Henk-jan, Çevik, Volkan, Asai, Shuta, Kemen, Eric, Cruz-Mireles, Neftaly, Kemen, Ariane, Belhaj, Khaoula, Schornack, Sebastian, Kamoun, Sophien, Holub, Eric B., Halkier, Barbara A., Jones, Jonathan D. G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5358052/
https://www.ncbi.nlm.nih.gov/pubmed/28320402
http://dx.doi.org/10.1186/s12915-017-0360-z
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author Prince, David C.
Rallapalli, Ghanasyam
Xu, Deyang
Schoonbeek, Henk-jan
Çevik, Volkan
Asai, Shuta
Kemen, Eric
Cruz-Mireles, Neftaly
Kemen, Ariane
Belhaj, Khaoula
Schornack, Sebastian
Kamoun, Sophien
Holub, Eric B.
Halkier, Barbara A.
Jones, Jonathan D. G.
author_facet Prince, David C.
Rallapalli, Ghanasyam
Xu, Deyang
Schoonbeek, Henk-jan
Çevik, Volkan
Asai, Shuta
Kemen, Eric
Cruz-Mireles, Neftaly
Kemen, Ariane
Belhaj, Khaoula
Schornack, Sebastian
Kamoun, Sophien
Holub, Eric B.
Halkier, Barbara A.
Jones, Jonathan D. G.
author_sort Prince, David C.
collection PubMed
description BACKGROUND: Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused by Albugo species can overcome non-host resistance and enable secondary infection and reproduction of usually non-virulent pathogens, including the potato late blight pathogen Phytophthora infestans on Arabidopsis thaliana. However, the molecular basis of host defense suppression in this complex plant–microbe interaction is unclear. Here, we investigate specific defense mechanisms in Arabidopsis that are suppressed by Albugo infection. RESULTS: Gene expression profiling revealed that two species of Albugo upregulate genes associated with tryptophan-derived antimicrobial metabolites in Arabidopsis. Albugo laibachii-infected tissue has altered levels of these metabolites, with lower indol-3-yl methylglucosinolate and higher camalexin accumulation than uninfected tissue. We investigated the contribution of these Albugo-imposed phenotypes to suppression of non-host resistance to P. infestans. Absence of tryptophan-derived antimicrobial compounds enables P. infestans colonization of Arabidopsis, although to a lesser extent than Albugo-infected tissue. A. laibachii also suppresses a subset of genes regulated by salicylic acid; however, salicylic acid plays only a minor role in non-host resistance to P. infestans. CONCLUSIONS: Albugo sp. alter tryptophan-derived metabolites and suppress elements of the responses to salicylic acid in Arabidopsis. Albugo sp. imposed alterations in tryptophan-derived metabolites may play a role in Arabidopsis non-host resistance to P. infestans. Understanding the basis of non-host resistance to pathogens such as P. infestans could assist in development of strategies to elevate food security. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0360-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-53580522017-03-20 Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana Prince, David C. Rallapalli, Ghanasyam Xu, Deyang Schoonbeek, Henk-jan Çevik, Volkan Asai, Shuta Kemen, Eric Cruz-Mireles, Neftaly Kemen, Ariane Belhaj, Khaoula Schornack, Sebastian Kamoun, Sophien Holub, Eric B. Halkier, Barbara A. Jones, Jonathan D. G. BMC Biol Research Article BACKGROUND: Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused by Albugo species can overcome non-host resistance and enable secondary infection and reproduction of usually non-virulent pathogens, including the potato late blight pathogen Phytophthora infestans on Arabidopsis thaliana. However, the molecular basis of host defense suppression in this complex plant–microbe interaction is unclear. Here, we investigate specific defense mechanisms in Arabidopsis that are suppressed by Albugo infection. RESULTS: Gene expression profiling revealed that two species of Albugo upregulate genes associated with tryptophan-derived antimicrobial metabolites in Arabidopsis. Albugo laibachii-infected tissue has altered levels of these metabolites, with lower indol-3-yl methylglucosinolate and higher camalexin accumulation than uninfected tissue. We investigated the contribution of these Albugo-imposed phenotypes to suppression of non-host resistance to P. infestans. Absence of tryptophan-derived antimicrobial compounds enables P. infestans colonization of Arabidopsis, although to a lesser extent than Albugo-infected tissue. A. laibachii also suppresses a subset of genes regulated by salicylic acid; however, salicylic acid plays only a minor role in non-host resistance to P. infestans. CONCLUSIONS: Albugo sp. alter tryptophan-derived metabolites and suppress elements of the responses to salicylic acid in Arabidopsis. Albugo sp. imposed alterations in tryptophan-derived metabolites may play a role in Arabidopsis non-host resistance to P. infestans. Understanding the basis of non-host resistance to pathogens such as P. infestans could assist in development of strategies to elevate food security. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0360-z) contains supplementary material, which is available to authorized users. BioMed Central 2017-03-20 /pmc/articles/PMC5358052/ /pubmed/28320402 http://dx.doi.org/10.1186/s12915-017-0360-z Text en © Jones et al. 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Prince, David C.
Rallapalli, Ghanasyam
Xu, Deyang
Schoonbeek, Henk-jan
Çevik, Volkan
Asai, Shuta
Kemen, Eric
Cruz-Mireles, Neftaly
Kemen, Ariane
Belhaj, Khaoula
Schornack, Sebastian
Kamoun, Sophien
Holub, Eric B.
Halkier, Barbara A.
Jones, Jonathan D. G.
Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana
title Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana
title_full Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana
title_fullStr Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana
title_full_unstemmed Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana
title_short Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana
title_sort albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to phytophthora infestans in arabidopsis thaliana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5358052/
https://www.ncbi.nlm.nih.gov/pubmed/28320402
http://dx.doi.org/10.1186/s12915-017-0360-z
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