Regulatory and Functional Aspects of Indolic Metabolism in Plant Systemic Acquired Resistance

Elia Stahl,Patricia Bellwon,Stefan Huber,Klaus Schlaeppi,Friederike Bernsdorff,Armelle Vallat-Michel,Felix Mauch,Jürgen Zeier

doi:10.1016/j.molp.2016.01.005

Elia Stahl, Patricia Bellwon + Show 6 more

Open Access

https://doi.org/10.1016/j.molp.2016.01.005

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Abstract

Tryptophan-derived, indolic metabolites possess diverse functions in Arabidopsis innate immunity to microbial pathogen infection. Here, we investigate the functional role and regulatory characteristics of indolic metabolism in Arabidopsis systemic acquired resistance (SAR) triggered by the bacterial pathogen Pseudomonas syringae. Indolic metabolism is broadly activated in both P. syringae-inoculated and distant, non-inoculated leaves. At inoculation sites, camalexin, indol-3-ylmethylamine (I3A), and indole-3-carboxylic acid (ICA) are the major accumulating compounds. Camalexin accumulation is positively affected by MYB122, and the cytochrome P450 genes CYP81F1 and CYP81F2. Local I3A production, by contrast, occurs via indole glucosinolate breakdown by PEN2- dependent and independent pathways. Moreover, exogenous application of the defense hormone salicylic acid stimulates I3A generation at the expense of its precursor indol-3-ylmethylglucosinolate (I3M), and the SAR regulator pipecolic acid primes plants for enhanced P. syringae-induced activation of distinct branches of indolic metabolism. In uninfected systemic tissue, the metabolic response is more specific and associated with enhanced levels of the indolics I3A, ICA, and indole-3-carbaldehyde (ICC). Systemic indole accumulation fully depends on functional CYP79B2/3, PEN2, and MYB34/51/122, and requires functional SAR signaling. Genetic analyses suggest that systemically elevated indoles are dispensable for SAR and associated systemic increases of salicylic acid. However, soil-grown but not hydroponically -cultivated cyp79b2/3 and pen2 plants, both defective in indolic secondary metabolism, exhibit pre-induced immunity, which abrogates their intrinsic ability to induce SAR.

Highlights

The immune system of plants is based on a multi-layered arsenal of constitutive and inducible defense strategies (ThordalChristensen, 2003)
Two days after inoculation of lower (1) leaves with the compatible P. syringae pv. maculicola ES4326 (Psm) strain, systemic acquired resistance (SAR) fully develops in nontreated upper (2) leaves. This is associated with significant accumulation of the two SAR-regulatory metabolites salicylic acid (SA) and pipecolic acid (Pip), and with a massive transcriptional reprogramming in 2 leaves (Navarovaet al., 2012; Gruner et al, 2013; Bernsdorff et al, 2016)
A cyp79b2 cyp79b3 double knockout mutant is blocked in the production of Trp-derived metabolites such as indole glucosinolates and camalexin (Glawischnig et al, 2004; Bednarek et al, 2009; Bottcher et al, 2009)

Summary

Introduction

The immune system of plants is based on a multi-layered arsenal of constitutive and inducible defense strategies (ThordalChristensen, 2003). These involve the action of low molecular weight plant metabolites at different functional levels. 662 Molecular Plant 9, 662–681, May 2016 a The Author 2016. Such as avenacin protect oat plants against root infection by varieties of the fungal pathogen Gaeumannomyces graminis that lack saponin-deglycosylating enzymes (Papadopoulou et al, 1999). Phytoalexins, by contrast, are antimicrobial low molecular weight secondary metabolites only produced in the course of a plant–pathogen interaction.

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