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

Giulia Chitarrini,Pietro Franceschi,Gabriele Magris,Antonella Vecchione,Michele Morgante,Urska Vrhovsek,Marco Stefanini,Serena Foria,Alessandro Cestaro,Gabriele Di Gaspero,Simone Larger,Massimo Pindo,Samantha Riccadonna,Luca Zulini

doi:10.1038/s41598-020-69051-6

Giulia Chitarrini, Pietro Franceschi + Show 12 more

Open Access

https://doi.org/10.1038/s41598-020-69051-6

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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.

Highlights

Plasmopara viticola is the causal agent of grapevine downy mildew (DM)
Using the same analytical and statistical methods and the same cut-off thresholds, we identified a higher number of metabolites (88 versus 53) that were significantly modulated over a 96 h period after the inoculation with the pathogen
We paid particular attention to the choice of an appropriate Rpv12-carrying genotype in order to minimise the confounding effects of the genetic background, we cannot exclude that part of the faster and stronger defence responses of the Rpv12-carrier compared to the Rpv3-carrier was due to more effective signal transduction components downstream of the R-gene in the genotype under study

Summary

Introduction

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 Rpv[3] and Rpv[12]. We recently performed metabolomic analyses after pathogen inoculation in the grape variety ‘Bianca’ that carries a major resistance haplotype called Rpv[], leading to the identification of 53 metabolites associated with the defence r esponse[20]. The resistance haplotype at the Rpv[12] locus was initially introgressed from the Asian species Vitis amurensis and confers higher levels of downy mildew resistance than Rpv[] when the resistance phenotype is quantitatively scored using the OIV452 descriptor[21], but both genes trigger a similar ETI-dependent response[12,21]. Eisenmann and coworkers[23] performed a transcriptomic analysis in ‘Regent’, a resistant variety that operates the same Rpv3mediated ETI response as does ‘Bianca’, showing that Rpv3-mediated changes in gene expression occur early after pathogen inoculation

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