A functional EDS1 ortholog is differentially regulated in powdery mildew resistant and susceptible grapevines and complements an Arabidopsis eds1 mutant

Abstract

Vitis vinifera (grapevine) is the most economically important deciduous fruit crop, but cultivated grapevine varieties lack adequate innate immunity to a range of devastating diseases. To identify genetic resources for grapevine innate immunity and understand pathogen defense pathways in a woody perennial plant, we focus in this study on orthologs of the central Arabidopsis thaliana defense regulator ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1). The family of EDS1-like genes is expanded in grapevine, and members of this family were previously found to be constitutively upregulated in the resistant variety 'Norton' of the North American grapevine species Vitis aestivalis, while they were induced by Erysiphe necator, the causal agent of grapevine powdery mildew (PM), in the susceptible V. vinifera variety 'Cabernet Sauvignon'. Here, we determine the responsiveness of individual EDS1-like genes in grapevine to PM and salicylic acid, and find that EDS1-like paralogs are differentially regulated in 'Cabernet Sauvignon', while two are constitutively upregulated in 'Norton'. Sequencing of VvEDS1 and VaEDS1 cDNA and genomic clones revealed high conservation in the protein-encoding sequence and some divergence of the promoter sequence in the two grapevine varieties. Complementation of the Arabidopsis eds1-1 mutant showed that the EDS1-like gene with highest predicted amino acid sequence similarity to AtEDS1 from either grapevine varieties is a functional ortholog of AtEDS1. Together, our analyses show that differential susceptibility to PM is correlated with differences in EDS1 expression, not differences in EDS1 function, between resistant 'Norton' and susceptible 'Cabernet Sauvignon'.

Three transcripts of EDS1-like genes respond differently to Vitis flexuosa infection

“…Therefore, clustering EDLs in the phylogenic tree showed that EDS1 related proteins of Vitis are novel compared to other plant proteins. These results are consistent with those of a previous report that showed Vitis EDS1 proteins were grouped together in a phylogenetic tree and diverged from other plant proteins (Gao et al 2010). The predicted amino acid sequences from the three loci of the VfEDL gene showed a high level of similarity with protein sequences of other plant species in a homology study of VfEDL genes by BLAST searches of the NCBI database.…”

“…In the expression study, all three VfEDL genes were upregulated at 1 hpi against bacterial pathogen R. vitis and two genes, VfEDL2 and VfEDL3, also showed upregulation at 1 hpi against fungal pathogen E. ampelina, after which all of them showed reduction in their expressions. This expression pattern was similar to the previous reports about expression pattern of EDS1 genes (Oridi and Bouarab 2007;Gao et al 2010;Wang et al 2014). VfEDL1 showed down regulated expression at all time points against E. ampelina, but its expression was upregulated against R. vitis infection at early time points, suggesting that the VfEDL1 gene functions in diverse response processes against bacterial and fungal pathogens.…”

“…Interestingly, they showed that these two signaling molecules are required for the disease caused by B. cinerea by silencing these genes when the necrotic disease was significantly reduced on leaves in silenced plants compared to control plants, and that EDS1 and SGT1 transcript accumulation was reduced in silenced plants. Gao et al (2010) reported that there were no EDS1-like genes that were significantly upregulated by the grapevine powdery mildew pathogen Erysiphe necator in both resistant 'Norton' of V. aestivalis and susceptible 'Cabernet Sauvignon' of V. vinifera. Although transcript level was not significantly higher in treated samples than control samples, VaEDS1 complemented Arabidopsis eds1 mutants by reducing bacterial growth relative to eds1 mutant during inoculation of Pseudomonas syringae pv.…”

Vitis vinifera VvNPR1.1 is the functional ortholog of AtNPR1 and its overexpression in grapevine triggers constitutive activation of PR genes and enhanced resistance to powdery mildew

“…Low levels of polymorphism in the two VvNPR genes show that they experienced purifying selection and suggest that they are Complementation of the Arabidopsis npr1 mutation has been performed previously to characterize NPR1 from several crop plants, including rice (Yuan et al 2007), canola (Potlakayala et al 2007), soybean (Sandhu et al 2009), and cacao (Shi et al 2010). Recently, complementation of the Arabidopsis eds1 mutant with grapevine sequences also helped to characterize the function of Vitis EDS1, another central defense regulator acting upstream of SA in pathogen resistance (Gao et al 2010).…”

Enhanced Disease Susceptibility1 Mediates Pathogen Resistance and Virulence Function of a Bacterial Effector in Soybean

“…EDS1 and PAD4 interact with each other and also function in race-specific resistance derived from multiple R proteins from diverse plants (Parker et al, 1996;Aarts et al, 1998;Feys et al, 2001;Peart et al, 2002;Liu et al, 2002;Hu et al, 2005;Gao et al, 2010). We show that soybean contains two EDS1-like genes and one PAD4-like gene, which encode proteins with significant structural similarities to the Figure 8.…”