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. 2020 Feb 28;11(3):261.
doi: 10.3390/genes11030261.

Novel Aspects on The Interaction Between Grapevine and Plasmopara viticola: Dual-RNA-Seq Analysis Highlights Gene Expression Dynamics in The Pathogen and The Plant During The Battle For Infection

Silvia Laura Toffolatti  1 , Gabriella De Lorenzis  1 , Matteo Brilli  2 , Mirko Moser  3 , Vahid Shariati  4 , Elahe Tavakol  5 , Giuliana Maddalena  1 , Alessandro Passera  1 , Paola Casati  1 , Massimo Pindo  3 , Alessandro Cestaro  3 , David Maghradze  6   7 , Osvaldo Failla  1 , Piero Attilio Bianco  1 , Fabio Quaglino  1
Affiliations

Novel Aspects on The Interaction Between Grapevine and Plasmopara viticola: Dual-RNA-Seq Analysis Highlights Gene Expression Dynamics in The Pathogen and The Plant During The Battle For Infection

Silvia Laura Toffolatti et al. Genes (Basel). .

Abstract

Mgaloblishvili, a Vitis vinifera cultivar, exhibits unique resistance traits against Plasmopara viticola, the downy mildew agent. This offers the unique opportunity of exploring the molecular responses in compatible and incompatible plant-pathogen interaction. In this study, whole transcriptomes of Mgaloblishvili, Pinot noir (a V. vinifera susceptible cultivar), and Bianca (a resistant hybrid) leaves, inoculated and non-inoculated with the pathogen, were used to identify P. viticola effector-encoding genes and plant susceptibility/resistance genes. Multiple effector-encoding genes were identified in P. viticola transcriptome, with remarkable expression differences in relation to the inoculated grapevine cultivar. Intriguingly, five apoplastic effectors specifically associated with resistance in V. vinifera. Gene coexpression network analysis identified specific modules and metabolic changes occurring during infection in the three grapevine cultivars. Analysis of these data allowed, for the first time, the detection in V. vinifera of a putative P. viticola susceptibility gene, encoding a LOB domain-containing protein. Finally, the de novo assembly of Mgaloblishvili, Pinot noir, and Bianca transcriptomes and their comparison highlighted novel candidate genes that might be at the basis of the resistant phenotype. These results open the way to functional analysis studies and to new perspectives in molecular breeding of grapevine for resistance to P. viticola.

Keywords: RNA-seq; disease resistance and susceptibility; oomycete effectors; plant–pathogen interaction; resistance genes; susceptibility genes; transcriptome.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Venn diagram illustrating the comparison between genes differentially expressed (DEGs) by Plasmopara viticola (Pv) following inoculation on Mgaloblishvili (M) and Pinot noir (P) (PvM_vs_PvP), M and Bianca (B) (PvM_vs_PvB), and P and B (PvP_vs_PvB).
Figure 2
Figure 2
Heatmap of 35 genes encoding cytoplasmic (RXLR and YxSLK) and apoplastic effectors (trypsin, elicitin and NPP1) differentially expressed by Plasmopara viticola (Pv) following inoculation on Mgaloblishvili (M) and Pinot noir (P) (PvM_vs_PvP), M and Bianca (B) (PvM_vs_PvB), and P and B (PvP_vs_PvB).
Figure 3
Figure 3
Heatmap of 76 genes encoding effectors possessing a signal peptide for secretion differentially expressed by Plasmopara viticola (Pv) following inoculation on Mgaloblishvili (M) and Pinot noir (P) (PvM_vs_PvP), M and Bianca (B) (PvM_vs_PvB), and P and B (PvP_vs_PvB).
Figure 4
Figure 4
Identification of gene coexpression modules of all samples data (24 samples, 3000 genes) using average hierarchical linkage clustering; the y-axis denotes the coexpression distance and the x-axis corresponds to genes. Dynamic tree cutting was applied to identify modules by dividing the dendrogram at significant branch points. Modules are displayed with different colors in the horizontal bar.
See this image and copyright information in PMC

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