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Open Access Highly Accessed Research article

Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases

Frank-Jörg Vorhölter12*, Heinrich-Günter Wiggerich2, Heiko Scheidle1, Vishaldeep Kaur Sidhu13, Kalina Mrozek1, Helge Küster24, Alfred Pühler2 and Karsten Niehaus1

Author Affiliations

1 Department of Proteome and Metabolome Research, Faculty of Biology, Universität Bielefeld, Universitätsstr. 25, Bielefeld, 33615, Germany

2 CeBiTec, Universität Bielefeld, Universitätsstr. 27, Bielefeld, 33615, Germany

3 Laboratory of Molecular Signaling, 5625 Fishers Lane, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, MD, 20852, USA

4 Institut für Pflanzengenetik, Naturwissenschaftliche Fakultät, Leibniz Universität Hannover, Herrenhäuser Str. 2, Hannover, 30419, Germany

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BMC Microbiology 2012, 12:239  doi:10.1186/1471-2180-12-239

Published: 19 October 2012

Abstract

Background

Efficient 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.

Results

A 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.

Conclusions

To 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.

Keywords:
TonB system; Damage-associate molecular pattern; DAMP; Oligogalacturonide; Trans-envelope signaling; Molecular plant-microbe interaction; Pathogen; Xanthomonas campestris