Compatible Interaction between Grapevine and Powdery Mildew (PM)

Powdery mildew (PM) is able to invade the epidermal cells of grapevine photosynthetic tissues. Upon entering the lumen of the plant cell, the fungus forms a specialized intracellular feeding structure, termed haustorium, which is accommodated by the invagination of the plant plasma membrane. The intimate nature of this pathogen-plant interaction suggests that E. necator is able to exploit the host’s cellular processes for its parasitic purpose. Evidence for this was generated by John Vogel and Shauna Somerville who identified recessive mutations in Arabidopsis thaliana which conferred resistance to the adapted powdery mildew fungus Erysiphe cichoracearum [PNAS 97:1897-1902, 2000]. One of the mutated genes (Pmr2) is an orthologue of the barley Mlo gene. Inactivation of the Mlo function also leads to PM resistance in barley [Jorgensen, 1992] and tomato [Bai et al., 2008].

The publication of the grapevine genome sequence [Jaillon et al., 2007] enabled us to identify all Mlo paralogues in grapevine, and measure their expression individually in various organs and in response to PM. We identified 17 grape Mlo genes, and demonstrated that fourteen of them were actively transcribed, and that several of these were up-regulated in response to PM infection [Winterhagen et al., 2008]. In general, high-level expressed Mlo genes are non-responsive to PM challenge.

Kovacs Graph 1

Figure 1: Expression of 14 Mlo genes in grapevine. Perpendicular axis (log10): relative transcript abundance in non-challenged leaf tissue; Left horizontal axis: fold-change of up-regulation triggered by E. necator; Right horizontal axis: grape Mlo paralogues. Relative transcript abundance of the lowest-level expressed Mlo gene was arbitrarily set to be 100.

To better understand grapevine’s susceptibility to PM, we also studied PM-induced changes at the level of the entire transcriptome in V. vinifera Cabernet Sauvignon. Despite the susceptible interaction, we detected a major defense-related restructuring of the transcriptome upon PM inoculation. These changes were associated with an increase with in SA levels, suggesting that the SA-mediated signal-transduction system was activated [Fung et al., 2008]. To determine if other signal transduction pathways also were activated, we performed comparative microarray studies in SA- and PM-treated grapevines. We found many genes that were up or down-regulated in response to PM, but not to SA treatment. The promoters of such genes will serve as molecular tools to probe signaling circuits activated by PM. This work is conducted in collaboration with researchers at Szent Istvan University, Hungary, and at the University of Missouri-Columbia.

Kovacs Graph 2

Figure 2: Genes that fall in clusters of similar expression patterns in PM-challenged tissues may be regulated by related signal transduction systems. Top panel: Clusters 3, 8, and 17 [Fig. S2, Fung et al., 2008] contain genes that are mostly responsive to SA and not to PM. Bottom panel: Clusters 4, 18, and 25 [Fig.S2, Fung et al., 2008] contain genes that are mostly responsive to PM and not to SA. The graphs on the right show expression ratios of genes that are significantly regulated by either SA or PM (p ≤ 0.001, Winterhagen, Su, and Kovacs, unpublished results) and that are from those whose expression pattern is clustered on the left.