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 Cevik; Shuta  Asai; Eric Kemen; Neftaly  Cruz-Mireles; Ariane  Kemen; Khaoula  Belhaj; Sebastian Schornack; Sophien Kamoun; Eric  B Holub; Barbara Ann Halkier; Jonathan D G Jones

doi:10.1186/s12915-017-0360-z

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 Cevik, Shuta Asai, Eric Kemen, Neftaly Cruz-Mireles, Ariane Kemen, Khaoula Belhaj, Sebastian Schornack, Sophien Kamoun, Eric B Holub, Barbara Ann Halkier, Jonathan D G Jones

Molekylær Plantebiologi

8 Citationer (Scopus)

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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.

Originalsprog	Engelsk
Artikelnummer	20
Tidsskrift	B M C Biology
Vol/bind	15
Antal sider	22
ISSN	1741-7007
DOI	https://doi.org/10.1186/s12915-017-0360-z
Status	Udgivet - 20 mar. 2017

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10.1186/s12915-017-0360-z

Albugo-imposed changes to tryptophanderived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thalianaForlagets udgivne version, 6,9 MB

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Prince, D. C., Rallapalli, G., Xu, D., Schoonbeek, H-J., Cevik, V., Asai, S., Kemen, E., Cruz-Mireles, N., Kemen, A., Belhaj, K., Schornack, S., Kamoun, S., B Holub, E., Halkier, B. A., & Jones, J. D. G. (2017). Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana. B M C Biology, 15, [20]. https://doi.org/10.1186/s12915-017-0360-z

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 et al.

I: B M C Biology, Bind 15, 20, 20.03.2017.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

Prince, DC, Rallapalli, G, Xu, D, Schoonbeek, H-J, Cevik, V, Asai, S, Kemen, E, Cruz-Mireles, N, Kemen, A, Belhaj, K, Schornack, S, Kamoun, S, B Holub, E, 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', B M C Biology, bind 15, 20. https://doi.org/10.1186/s12915-017-0360-z

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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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author = "Prince, {David C.} and Ghanasyam Rallapalli and Deyang Xu and Henk-Jan Schoonbeek and Volkan Cevik and Shuta Asai and Eric Kemen and Neftaly Cruz-Mireles and Ariane Kemen and Khaoula Belhaj and Sebastian Schornack and Sophien Kamoun and {B Holub}, Eric and Halkier, {Barbara Ann} and Jones, {Jonathan D G}",

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doi = "10.1186/s12915-017-0360-z",

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TY - JOUR

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 - Cevik, Volkan

AU - Asai, Shuta

AU - Kemen, Eric

AU - Cruz-Mireles, Neftaly

AU - Kemen, Ariane

AU - Belhaj, Khaoula

AU - Schornack, Sebastian

AU - Kamoun, Sophien

AU - B Holub, Eric

AU - Halkier, Barbara Ann

AU - Jones, Jonathan D G

PY - 2017/3/20

Y1 - 2017/3/20

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.

AB - 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.

KW - Journal Article

U2 - 10.1186/s12915-017-0360-z

DO - 10.1186/s12915-017-0360-z

M3 - Journal article

C2 - 28320402

SN - 1741-7007

VL - 15

JO - B M C Biology

JF - B M C Biology

M1 - 20

ER -

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

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