Two-omics data revealed commonalities and differences between Rpv12- and Rpv3-mediated resistance in grapevine

Abstract

Plasmopara viticola is the causal agent of grapevine downy mildew (DM). DM resistant varieties deploy effector-triggered immunity (ETI) to inhibit pathogen growth, which is activated by major resistance loci, the most common of which are Rpv3 and Rpv12. We previously showed that a quick metabolome response lies behind the eti conferred by Rpv3 tiR-nB-LRR genes. Here we used a grape variety operating Rpv12-mediated eti, which is conferred by an independent locus containing cc-nB-LRR genes, to investigate the defence response using Gc/MS, UpLc, UHpLc and RnA-Seq analyses. Eighty-eight metabolites showed significantly different concentration and 432 genes showed differential expression between inoculated resistant leaves and controls. Most metabolite changes in sugars, fatty acids and phenols were similar in timing and direction to those observed in Rpv3-mediated eti but some of them were stronger or more persistent. Activators, elicitors and signal transducers for the formation of reactive oxygen species were early observed in samples undergoing Rpv12-mediated eti and were paralleled and followed by the upregulation of genes belonging to ontology categories associated with salicylic acid signalling, signal transduction, WRKY transcription factors and synthesis of PR-1, PR-2, PR-5 pathogenesis-related proteins. Downy mildew is one of the most destructive diseases of the grapevine, causing significant limitations on grape production in the absence of chemical protection of vineyards. Downy mildew is caused by the biotrophic oomycete Plasmopara viticola (Berk. And Curt) Berl. and Toni, which is native to North America and was introduced into Europe at the end of the nineteenth century. The European bunch grape (Vitis vinifera L.) does not normally activate the immune system in response to P. viticola with a few exceptions 1,2. The introgression of resistant genes from other grape species (i.e. V. rupestris, V. amurensis, V. cinerea, V. riparia and Muscadinia rotundifolia) into the crop germplasm can alleviate the dependence of viticulture on the use of fungicides 3. The pathogen can cause serious damage to any green organ of the grapevine. P. viticola deploys a specialized structure called haustorium to establish a close interaction with grapevines and to leak nutrients from viable host cells 4,5. P. viticola can feed on both susceptible and resistant grapevines and complete its life cycle on both hosts. Resistant grapevines are, however, able to detect the invading pathogen and operate defence responses. The initial phases of the infection are similar on both hosts, but mycelial growth is restricted in resistant hosts and sporangia are released at lower rates than in susceptible hosts. The similarity during early phases of infection suggests the presence of post-infection mechanisms of resistance, including callose deposition, cell wall-associated

The Durability of Quantitative Host Resistance and Variability in Pathogen Virulence in the Interaction Between European Grapevine Cultivars and Plasmopara viticola

“…There are some indications for the occurrence of a secondary defense mechanism. In V. riparia, a dramatic increase in JA was observed only at 48 hpi (Polesani et al, 2010) and in Rpv12 carriers, genes related to SA synthesis and signaling were only differentially expressed from 48 hpi (Chitarrini et al, 2020). Moreover, the first infection steps of Rpv3.1 + cultivars (Eisenmann et al, 2019) and Solaris (Busam et al, 1997;Boso and Kassemeyer, 2008) are essentially the same as in the susceptible V. vinifera, even though gene expression studies show that the defenses are induced at the first interaction between host cells and pathogen hyphae (Polesani et al, 2010;Eisenmann et al, 2019).…”

Fungal–Metal Interactions: A Review of Toxicity and Homeostasis

“…The most popular omics utilizes bioinformatics to analyze fungal–metal interactions at a nucleotide and protein level, which can reveal novel genes and mutations. In genomics, the entirety of a genome is assessed and compared to others for similarities and differences that can contribute to an organism’s characteristics [ 302 , 303 ]. Transcriptomics relies on RNA sequencing to survey gene expression through fold-changes in transcripts and proteomics assess fold-change in subsequent proteins.…”

Transcriptional profiling reveals multiple defense responses in downy mildew-resistant transgenic grapevine expressing a TIR-NBS-LRR gene located at the MrRUN1/MrRPV1 locus

“…For example, Wang et al 28 showed that stilbene synthase ( VvSTS ) was induced earlier in DM-resistant M. rotundifolia than in susceptible V. vinifera tissues following DM inoculation, while the resveratrol O -methyltransferase ( ROMT ) gene was upregulated in only the resistant genotype. More recent studies with V. vinifera hybrids containing either the Rpv3 or Rpv10 resistance locus have also strongly suggested a role for stilbenes in DM resistance mediated by these loci 23 , 24 , 29 . Similarly, in Rpv12 -mediated DM resistance, trans-resveratrol was proposed to act as a signaling molecule in ROS formation and initiation of programmed cell death (PCD) triggered by a CC-NB-LRR gene product 24 .…”

“…More recent studies with V. vinifera hybrids containing either the Rpv3 or Rpv10 resistance locus have also strongly suggested a role for stilbenes in DM resistance mediated by these loci 23 , 24 , 29 . Similarly, in Rpv12 -mediated DM resistance, trans-resveratrol was proposed to act as a signaling molecule in ROS formation and initiation of programmed cell death (PCD) triggered by a CC-NB-LRR gene product 24 .…”

“…For example, leaf hairs of some grape varieties can form a natural physical barrier to prevent the invasion of the DM pathogen 27 . Transcriptional analysis of V. riparia 20 , V. amurensis 21 , 22 , 24 , V. pseudoreticulata 26 , M. rotundifolia 28 , V. labrusca , and V. vinifera hybrids containing DM resistance loci 23 , 24 , 29 has revealed that the induction and regulation of many defense-related genes may contribute to DM resistance. However, one observation that is common across many of these studies is that there is more rapid or stronger upregulation of stilbene biosynthesis pathway genes in DM-resistant genotypes than in DM-susceptible genotypes.…”