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First published online December 31, 2008; 10.1104/pp.108.131805

Plant Physiology 149:1366-1386 (2009)
© 2009 American Society of Plant Biologists

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PLANTS INTERACTING WITH OTHER ORGANISMS

An Integrated Genomics Approach to Define Niche Establishment by Rhodococcus fascians1,[C],[W],[OA]

Stephen Depuydt, Sandra Trenkamp, Alisdair R. Fernie, Samira Elftieh, Jean-Pierre Renou, Marnik Vuylsteke, Marcelle Holsters* and Danny Vereecke

Department of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Ghent, Belgium (S.D., M.V., M.H., D.V.); Department of Plant Biotechnology and Genetics, Ghent University, 9052 Ghent, Belgium (S.D., M.V., M.H., D.V.); Max Planck Institute of Molecular Plant Physiology, University of Potsdam, 14476 Potsdam-Golm, Germany (S.T., A.R.F.); and Unité Mixte de Recherche en Génomique Végétale, Institut National de la Recherche Agronomique, 91057 Evry, France (S.E., J.-P.R.)

Rhodococcus fascians is a Gram-positive phytopathogen that induces shooty hyperplasia on its hosts through the secretion of cytokinins. Global transcriptomics using microarrays combined with profiling of primary metabolites on infected Arabidopsis (Arabidopsis thaliana) plants revealed that this actinomycete modulated pathways to convert its host into a niche. The transcript data demonstrated that R. fascians leaves a very characteristic mark on Arabidopsis with a pronounced cytokinin response illustrated by the activation of cytokinin perception, signal transduction, and homeostasis. The microarray data further suggested active suppression of an oxidative burst during the R. fascians pathology, and comparison with publicly available transcript data sets implied a central role for auxin in the prevention of plant defense activation. Gene Ontology categorization of the differentially expressed genes hinted at a significant impact of infection on the primary metabolism of the host, which was confirmed by subsequent metabolite profiling. The much higher levels of sugars and amino acids in infected plants are presumably accessed by the bacteria as carbon and nitrogen sources to support epiphytic and endophytic colonization. Hexoses, accumulating from a significantly increased invertase activity, possibly inhibited the expression of photosynthesis genes and photosynthetic activity in infected leaves. Altogether, these changes are indicative of sink development in symptomatic tissues. The metabolomics data furthermore point to the possible occurrence of secondary signaling during the interaction, which might contribute to symptom development. These data are placed in the context of regulation of bacterial virulence gene expression, suppression of defense, infection phenotype, and niche establishment.


1 This work was supported by the Bijzonder Onderzoeksfonds of Ghent University and the European Molecular Biology Organization (predoctoral and short-term fellowships, respectively, to S.D.).

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Danny Vereecke (danny.vereecke{at}psb.ugent.be).

[C] Some figures in this article are displayed in color online but in black and white in the print edition.

[W] The online version of this article contains Web-only data.

[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.131805

* Corresponding author; e-mail marcelle.holsters{at}psb.ugent.be.

Received October 28, 2008; accepted December 25, 2008; published December 31, 2008.


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