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Open Access Highly Accessed Research article

Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica

Agnès Attard1, Edouard Evangelisti2, Naïma Kebdani-Minet1, Franck Panabières1, Emeline Deleury1, Cindy Maggio1, Michel Ponchet1 and Mathieu Gourgues1*

Author Affiliations

1 Université de Nice Sophia-Antipolis, UMR Institut Sophia Agrobiotech, INRA1355-CNRS7254-UNSA, 400 route des chappes, F-06903 Sophia Antipolis, France

2 Sainsbury Laboratory (SLCU), University of Cambridge, Bateman Street, Cambridge CB2 1LR, UK

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BMC Genomics 2014, 15:538  doi:10.1186/1471-2164-15-538

Published: 29 June 2014

Abstract

Background

Oomycetes are a group of filamentous microorganisms that includes both animal and plant pathogens and causes major agricultural losses. Phytophthora species can infect most crops and plants from natural ecosystems. Despite their tremendous economic and ecologic importance, few effective methods exist for limiting the damage caused by these species. New solutions are required, and their development will require improvements in our understanding of the molecular events governing infection by these pathogens. In this study, we characterized the genetic program activated during penetration of the plant by the soil-borne pathogen Phytophthora parasitica.

Results

Using all the P. parasitica sequences available in public databases, we generated a custom oligo-array and performed a transcriptomic analysis of the early events of Arabidopsis thaliana infection. We characterized biological stages, ranging from the appressorium-mediated penetration of the pathogen into the roots to the occurrence of first dead cells in the plant. We identified a series of sequences that were transiently modulated during host penetration. Surprisingly, we observed an overall down regulation of genes encoding proteins involved in lipid and sugar metabolism, and an upregulation of functions controlling the transport of amino acids. We also showed that different groups of genes were expressed by P. parasitica during host penetration and the subsequent necrotrophic phase. Differential expression patterns were particularly marked for cell wall-degrading enzymes and other proteins involved in pathogenicity, including RXLR effectors. By transforming P. parasitica with a transcriptional fusion with GFP, we showed that an RXLR-ecoding gene was expressed in the appressorium and infectious hyphae during infection of the first plant cell.

Conclusion

We have characterized the genetic program activated during the initial invasion of plant cells by P. parasitica. We showed that a specific set of proteins, including effectors, was mobilized for penetration and to facilitate infection. Our detection of the expression of an RXLR encoding gene by the appressorium and infection hyphae highlights a role of this structure in the manipulation of the host cells.

Keywords:
Phytophthora; Arabidopsis thaliana; Appressorium; Transcriptome; Root infection