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First published online March 30, 2007; 10.1104/pp.106.094987

Plant Physiology 144:347-366 (2007)
© 2007 American Society of Plant Biologists

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PLANTS INTERACTING WITH OTHER ORGANISMS

Transcript Profiling of Poplar Leaves upon Infection with Compatible and Incompatible Strains of the Foliar Rust Melampsora larici-populina1,[W]

Cécile Rinaldi2, Annegret Kohler2, Pascal Frey, Frédéric Duchaussoy, Nathalie Ningre, Arnaud Couloux, Patrick Wincker, Didier Le Thiec, Silvia Fluch, Francis Martin and Sébastien Duplessis*

Unité Mixte de Recherche (UMR) 1136 Institut National de la Recherche Agronomique (INRA)/Nancy Université Interactions Arbres/Micro-organismes (C.R., A.K., P.F., F.D., F.M., S.D.), and UMR 1137 INRA/Nancy Université Ecophysiologie et Ecologie Forestières (N.N., D.L.T.), Centre INRA de Nancy, F–54280 Champenoux, France; Génoscope Centre National de la Recherche Scientifique UMR 8030, Centre National de Séquençage, F–91057 Evry cedex, France (A.C., P.W.); and Platform for Integrated Clone Management, Austrian Research Centers Seibersdorf Research Biogenetics, A–2444 Seibersdorf, Austria (S.F.)

To understand key processes governing defense mechanisms in poplar (Populus spp.) upon infection with the rust fungus Melampsora larici-populina, we used combined histological and molecular techniques to describe the infection of Populus trichocarpa x Populus deltoides ‘Beaupré’ leaves by compatible and incompatible fungal strains. Striking differences in host-tissue infection were observed after 48-h postinoculation (hpi) between compatible and incompatible interactions. No reactive oxygen species production could be detected at infection sites, while a strong accumulation of monolignols occurred in the incompatible interaction after 48 hpi, indicating a late plant response once the fungus already penetrated host cells to form haustorial infection structures. P. trichocarpa whole-genome expression oligoarrays and sequencing of cDNAs were used to determine changes in gene expression in both interactions at 48 hpi. Temporal expression profiling of infection-regulated transcripts was further compared by cDNA arrays and reverse transcription-quantitative polymerase chain reaction. Among 1,730 significantly differentially expressed transcripts in the incompatible interaction, 150 showed an increase in concentration ≥3-fold, whereas 62 were decreased by ≥3-fold. Regulated transcripts corresponded to known genes targeted by R genes in plant pathosystems, such as inositol-3-P synthase, glutathione S-transferases, and pathogenesis-related proteins. However, the transcript showing the highest rust-induced up-regulation encodes a putative secreted protein with no known function. In contrast, only a few transcripts showed an altered expression in the compatible interaction, suggesting a delay in defense response between incompatible and compatible interactions in poplar. This comprehensive analysis of early molecular responses of poplar to M. larici-populina infection identified key genes that likely contain the fungus proliferation in planta.

1 This work was supported by the Région Lorraine and Institut National de la Recherche Agronomique (INRA; doctoral scholarship to C.R., postdoctoral fellowship to A.K., and junior scientist support grant to S.D.; DNA sequencing and functional genomics facilities), by the Consortium National de Recherche en Génomique (Génoscope) within the framework of the ForEST project (sequencing of suppression subtractive hybridization cDNA clones), by INRA (Innovating Grant "Durabilité des resistances" and Action Incitative Programmée "Sequencing 2005–2006"), by the European project POPYOMICS (contract no. QLK5–CT–2002–00953), and by the Institut Fédérateur de Recherche 110 ("Génomique, Ecophysiologie et Ecologie Fonctionnelles"). The ESTs printed on the Platform for Integrated Clone Management arrays were produced by INRA-Nancy, INRA-Orléans, and University of Helsinki within the framework of the INRA LIGNOME and European ESTABLISH programs, respectively.

2 These authors contributed equally to the article.

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: Sébastien Duplessis (duplessi{at}nancy.inra.fr).

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

www.plantphysiol.org/cgi/doi/10.1104/pp.106.094987

* Corresponding author; e-mail duplessi{at}nancy.inra.fr; fax 33–383–39–40–69.

Received December 18, 2006; accepted March 20, 2007; published March 30, 2007.

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