Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistance via azelaic acid and its precursor 9-oxo nonanoic acid.

Finni Wittek,Wilfried Schwab,Thomas Hoffmann,Marlies Bichlmeier,Basem Kanawati,Philippe Schmitt-Kopplin,Marion Wenig,A Corina Vlot,Claudia Knappe,Jane E Parker

doi:10.1093/jxb/eru331

Abstract

Systemic acquired resistance (SAR) is a form of inducible disease resistance that depends on salicylic acid and its upstream regulator ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1). Although local Arabidopsis thaliana defence responses activated by the Pseudomonas syringae effector protein AvrRpm1 are intact in eds1 mutant plants, SAR signal generation is abolished. Here, the SAR-specific phenotype of the eds1 mutant is utilized to identify metabolites that contribute to SAR. To this end, SAR bioassay-assisted fractionation of extracts from the wild type compared with eds1 mutant plants that conditionally express AvrRpm1 was performed. Using high-performance liquid chromatography followed by mass spectrometry, systemic immunity was associated with the accumulation of 60 metabolites, including the putative SAR signal azelaic acid (AzA) and its precursors 9-hydroperoxy octadecadienoic acid (9-HPOD) and 9-oxo nonanoic acid (ONA). Exogenous ONA induced SAR in systemic untreated leaves when applied at a 4-fold lower concentration than AzA. The data suggest that in planta oxidation of ONA to AzA might be partially responsible for this response and provide further evidence that AzA mobilizes Arabidopsis immunity in a concentration-dependent manner. The AzA fragmentation product pimelic acid did not induce SAR. The results link the C9 lipid peroxidation products ONA and AzA with systemic rather than local resistance and suggest that EDS1 directly or indirectly promotes the accumulation of ONA, AzA, or one or more of their common precursors possibly by activating one or more pathways that either result in the release of these compounds from galactolipids or promote lipid peroxidation.

Highlights

Plants protect themselves from pathogen invasion by innate immune mechanisms
Using high-performance liquid chromatography followed by mass spectrometry, systemic immunity was associated with the accumulation of 60 metabolites, including the putative Systemic acquired resistance (SAR) signal azelaic acid (AzA) and its precursors 9-hydroperoxy octadecadienoic acid (9-HPOD) and 9-oxo nonanoic acid (ONA)
It was tested whether ONA application elicits systemic resistance in the gly1-3 mutant, which is compromised for G3P accumulation and SAR (Chanda et al, 2011), or in azi1-2 mutant plants. Both mutants displayed normal susceptibility to Pseudomonas syringae pathovar tomato (Pst), but did not support SAR in response to the application of 250 μM ONA (Fig. 5B). These results suggest that the mechanisms leading to SAR downstream of ONA and AzA application are related since they are dependent on ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) and/or PAD4, salicylic acid (SA), AZI1, and G3P

Summary

Introduction

For example Arabidopsis thaliana, defence against biotrophic pathogens is dependent on the phytohormone salicylic acid (SA) and can be divided into local and systemic phases of immunity (Vlot et al, 2009; Spoel and Dong, 2012; Fu and Dong, 2013). Plants respond to pathogen-associated molecular patterns (PAMPs) with PAMP-triggered immunity (PTI; Jones and Dangl, 2006). The recognition of pathogen effectors leads to effector-triggered immunity (ETI), which augments PTI (Tsuda et al, 2009; Tsuda and Katagiri, 2010). PTI and ETI are associated with SA accumulation and a burst of reactive oxygen species (ROS; Jones and Dangl, 2006), and induce SA-dependent systemic acquired resistance (SAR) in systemic uninfected tissues (Cameron et al, 1994; Mishina and Zeier, 2007; Vlot et al, 2009; Liu et al, 2010; Fu and Dong, 2013; Breitenbach et al, 2014)

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