Abstract

BackgroundEfficient perception of attacking pathogens is essential for plants. Plant defense is evoked by molecules termed elicitors. Endogenous elicitors or damage-associated molecular patterns (DAMPs) originate from plant materials upon injury or pathogen activity. While there are comparably well-characterized examples for DAMPs, often oligogalacturonides (OGAs), generated by the activity of fungal pathogens, endogenous elicitors evoked by bacterial pathogens have been rarely described. In particular, the signal perception and transduction processes involved in DAMP generation are poorly characterized.ResultsA mutant strain of the phytopathogenic bacterium Xanthomonas campestris pv. campestris deficient in exbD2, which encodes a component of its unusual elaborate TonB system, had impaired pectate lyase activity and caused no visible symptoms for defense on the non-host plant pepper (Capsicum annuum). A co-incubation of X. campestris pv. campestris with isolated cell wall material from C. annuum led to the release of compounds which induced an oxidative burst in cell suspension cultures of the non-host plant. Lipopolysaccharides and proteins were ruled out as elicitors by polymyxin B and heat treatment, respectively. After hydrolysis with trifluoroacetic acid and subsequent HPAE chromatography, the elicitor preparation contained galacturonic acid, the monosaccharide constituent of pectate. OGAs were isolated from this crude elicitor preparation by HPAEC and tested for their biological activity. While small OGAs were unable to induce an oxidative burst, the elicitor activity in cell suspension cultures of the non-host plants tobacco and pepper increased with the degree of polymerization (DP). Maximal elicitor activity was observed for DPs exceeding 8. In contrast to the X. campestris pv. campestris wild type B100, the exbD2 mutant was unable to generate elicitor activity from plant cell wall material or from pectin.ConclusionsTo our knowledge, this is the second report on a DAMP generated by bacterial features. The generation of the OGA elicitor is embedded in a complex exchange of signals within the framework of the plant-microbe interaction of C. annuum and X. campestris pv. campestris. The bacterial TonB-system is essential for the substrate-induced generation of extracellular pectate lyase activity. This is the first demonstration that a TonB-system is involved in bacterial trans-envelope signaling in the context of a pathogenic interaction with a plant.

Highlights

  • Efficient perception of attacking pathogens is essential for plants

  • While the presence of different TonB-dependent receptors has been attributed to their distinct binding specificities, where different molecules are bound at the outer cell surface to be either transported inside or to signal their presence to the cell interior, so far it has been assumed that only one set of tonB-exbB-exbD genes is required to build a TonB protein complex that interacts with all the different TonB-dependent receptors

  • As far as we know, we report here for the first time on a Damageassociated Molecular Pattern (DAMP) that is produced by Xanthomonas exoenzymes from non-host plant cell walls

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Summary

Introduction

Plant defense is evoked by molecules termed elicitors. While there are comparably well-characterized examples for DAMPs, often oligogalacturonides (OGAs), generated by the activity of fungal pathogens, endogenous elicitors evoked by bacterial pathogens have been rarely described. There are only a few detailed model systems that describe MAMP, PRR, and perception-induced signaling [2]. An example for such a well-characterized PTI is the recognition of bacterial flagellin in Arabidopsis thaliana [3]. Molecules which evoke defense-related plant reactions and which are assumed to be involved in the recognition process of non-host plants were termed elicitors [2]. Examples for MAMPs are the harpin proteins from Erwinia [5,6], Xanthomonas [7,8], or Pseudomonas [9], syringolides from Pseudomonas syringae [10] or lipopolysaccharides (LPSs), characteristic glycoconjugate cell envelope constituents of Gram-negative bacteria [11]

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