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

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

doi:10.1186/s12915-017-0360-z

Abstract

BackgroundPlants 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.ResultsGene 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.ConclusionsAlbugo 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.

Highlights

Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens
Two Albugo species compromise plant immunity and enables sporulation of Phytophthora infestans We recently reported that A. laibachii Nc14 (AlNc14) [47] suppresses Arabidopsis Non-host resistance (NHR) to P. infestans ([12], Fig. 1a, b, d and e)
As immunosuppression was demonstrated for the related species A. candida [10, 11], we investigated whether A. candida infection of Arabidopsis and Brassica juncea compromises NHR to P. infestans

Summary

Introduction

Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Plant defense responses are initiated by recognition of pathogen or pest attack via detection of pathogen molecules by plant cell surface receptors. Invariant and indispensable molecules known as microbe- or pathogen-associated molecular patterns, are recognized by transmembrane pattern recognition receptors at the plasma membrane. This leads to signaling responses that result in pattern-triggered immunity (PTI). PTI is sufficient to prevent colonization by most non-adapted pathogens or pests, but pathogens which are adapted to particular host plants have evolved effectors that suppress PTI. Plants evolved intracellular receptors that recognize the structure or action of effectors, resulting in effector-triggered immunity (ETI).

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