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

David C. Prince, Ghanasyam Rallapalli, Deyang Xu, Henk jan Schoonbeek, Volkan Çevik, Shuta Asai, Eric Kemen, Neftaly Cruz-Mireles, Ariane Kemen, Khaoula Belhaj, Sebastian Schornack, Sophien Kamoun, Eric B. Holub, Barbara A. Halkier, Jonathan D G Jones

Research output: Contribution to journalArticle

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Abstract

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.

LanguageEnglish
Article number20
JournalBMC Biology
Volume15
Issue number1
DOIs
StatusPublished - 20 Mar 2017

Fingerprint

Albugo
Phytophthora infestans
Biosynthesis
Pathogens
Metabolites
Arabidopsis
Tryptophan
tryptophan
metabolite
Arabidopsis thaliana
pathogen
anti-infective agents
biosynthesis
metabolites
salicylic acid
Salicylic Acid
pathogens
Tissue
colonization
Genes

Keywords

  • Albugo
  • Arabidopsis thaliana
  • Camalexin
  • Glucosinolates
  • Non-host resistance
  • Phytophthora infestans
  • Salicylic acid

Cite this

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.

In: BMC Biology, Vol. 15, No. 1, 20, 20.03.2017.

Research output: Contribution to journalArticle

Prince, DC, Rallapalli, G, Xu, D, Schoonbeek, HJ, Çevik, V, Asai, S, Kemen, E, Cruz-Mireles, N, Kemen, A, Belhaj, K, Schornack, S, Kamoun, S, Holub, EB, Halkier, BA & Jones, JDG 2017, 'Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana', BMC Biology, vol. 15, no. 1, 20. https://doi.org/10.1186/s12915-017-0360-z
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. In: BMC Biology. 2017 ; Vol. 15, No. 1.
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abstract = "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.",
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T1 - Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana

AU - Prince, David C.

AU - Rallapalli, Ghanasyam

AU - Xu, Deyang

AU - Schoonbeek, Henk jan

AU - Çevik, Volkan

AU - Asai, Shuta

AU - Kemen, Eric

AU - Cruz-Mireles, Neftaly

AU - Kemen, Ariane

AU - Belhaj, Khaoula

AU - Schornack, Sebastian

AU - Kamoun, Sophien

AU - Holub, Eric B.

AU - Halkier, Barbara A.

AU - Jones, Jonathan D G

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N2 - 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.

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KW - Albugo

KW - Arabidopsis thaliana

KW - Camalexin

KW - Glucosinolates

KW - Non-host resistance

KW - Phytophthora infestans

KW - Salicylic acid

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