Transcriptome dynamic of Arabidopsis roots infected with Phytophthora parasitica identifies VQ29, a gene induced during the penetration and involved in the restriction of infection

Little is known about the responses of plant roots to filamentous pathogens, particularly to oomycetes. To assess the molecular dialog established between the host and the pathogen during early stages of infection, we investigated the overall changes in gene expression in A. thaliana roots challenged with P. parasitica. We analyzed various infection stages, from penetration and establishment of the interaction to the switch from biotrophy to necrotrophy. We identified 3390 genes for which expression was modulated during the infection. The A. thaliana transcriptome displays a dynamic response to P. parasitica infection, from penetration onwards. Some genes were specifically coregulated during penetration and biotrophic growth of the pathogen. Many of these genes have functions relating to primary metabolism, plant growth, and defense responses. In addition, many genes encoding VQ motif-containing proteins were found to be upregulated in plant roots, early in infection. Inactivation of VQ29 gene significantly increased susceptibility to P. parasitica during the late stages of infection. This finding suggests that the gene contributes to restricting oomycete development within plant tissues. Furthermore, the vq29 mutant phenotype was not associated with an impairment of plant defenses involving SA-, JA-, and ET-dependent signaling pathways, camalexin biosynthesis, or PTI signaling. Collectively, the data presented here thus show that infection triggers a specific genetic program in roots, beginning as soon as the pathogen penetrates the first cells.