Abstract
BackgroundEuropean grapevine cultivars (Vitis vinifera spp.) are highly susceptible to the downy mildew pathogen Plasmopara viticola. Breeding of resistant V. vinifera cultivars is a promising strategy to reduce the impact of disease management. Most cultivars that have been bred for resistance to downy mildew, rely on resistance mediated by the Rpv3 (Resistance toP.viticola) locus. However, despite the extensive use of this locus, little is known about the mechanism of Rpv3-mediated resistance.ResultsIn this study, Rpv3-mediated defense responses were investigated in Rpv3+ and Rpv3ˉ grapevine cultivars following inoculation with two distinct P. viticola isolates avrRpv3+ and avrRpv3ˉ, with the latter being able to overcome Rpv3 resistance. Based on comparative microscopic, metabolomic and transcriptomic analyses, our results show that the Rpv3–1-mediated resistance is associated with a defense mechanism that triggers synthesis of fungi-toxic stilbenes and programmed cell death (PCD), resulting in reduced but not suppressed pathogen growth and development. Functional annotation of the encoded protein sequence of genes significantly upregulated during the Rpv3–1-mediated defense response revealed putative roles in pathogen recognition, signal transduction and defense responses.ConclusionThis study used histochemical, transcriptomic and metabolomic analyses of Rpv3+ and susceptible cultivars inoculated with avirulent and virulent P. viticola isolates to investigate mechanism underlying the Rpv3–1-mediated resistance response. We demonstrated a strong correlation between the expressions of stilbene biosynthesis related genes, the accumulation of fungi-toxic stilbenes, pathogen growth inhibition and PCD.
Highlights
European grapevine cultivars (Vitis vinifera spp.) are highly susceptible to the downy mildew pathogen Plasmopara viticola
After inoculation with the avrRpv3+ isolate, the number of sporangia produced on Rpv3+ cultivars was significantly lower (94–98% reduction) than that observed on the susceptible (Rpv3ˉ) cultivar (Fig. 1a-d, i)
In contrast to the susceptible cultivar, necrotic areas were observed on the leaf discs of the Rpv3+ genotypes inoculated with the avrRpv3+ isolate (Fig. 1a-d)
Summary
European grapevine cultivars (Vitis vinifera spp.) are highly susceptible to the downy mildew pathogen Plasmopara viticola. Successful pathogen recognition leads to activation of signal transduction pathways involving MAP kinases and WRKY transcription factors, which in turn trigger primary immune responses such as accumulation of pathogenesis related (PR) proteins, reactive oxygen species (ROS) or phytoalexins, resulting in a hypersensitive response (HR) that prevents pathogen growth and development [27] It has been demonstrated for different model organisms that a localized HR at the infection site is a common defense mechanisms observed during ETI [28, 29]. Correlations between resistance against P. viticola and high levels of ε-viniferin and trans-pterostilbene were demonstrated for Muscadinia rotundifolia genotypes and an Rpv10-locus containing cultivar [46, 47] Despite these previous publications implicating a role for stilbene biosynthesis in R-loci mediated resistance, not much is known about their role in Rpv3–1-mediated defense. Our unique approach provides evidence that the Rpv3-mediated defense response involves the induction of the biosynthesis of fungitoxic stilbenes, resulting in reduced, but not completely suppressed, pathogen growth and development
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