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Oxygen Radical-Generating Metabolites Secreted by Eutypa and Esca Fungal Consortia: Understanding the Mechanisms Behind Grapevine Wood Deterioration and Pathogenesis

ABSTRACT: Eutypa dieback and Esca complex are fungal diseases of grape that cause large economic losses in vineyards. These diseases require, or are enhanced by, fungal consortia growth which leads to the deterioration of the wood tissue in the grapevine trunk; however, pathogenesis and the underlying mechanisms involved in the woody tissue degradation are not understood. We examined the role that the consortia fungal metabolome have in generating oxygen radicals that could potentially play a role in trunk decay and pathogenesis. Unique metabolites were isolated from the consortia fungi with some metabolites preferentially reducing iron whereas others were involved in redox cycling to generate hydrogen peroxide. Metabolite suites with different functions were produced when fungi were grown separately vs. when grown in consortia. Chelator-mediated Fenton (CMF) chemistry promoted by metabolites from these fungi allowed for the generation of highly reactive hydroxyl radicals. We hypothesize that this mechanism may be involved in pathogenicity in grapevine tissue as a causal mechanism associated with trunk wood deterioration/necrosis in these two diseases of grape.

SUBMITTER: Perez-Gonzalez G

PROVIDER: S-EPMC9327790 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Leaf samples were obtained from Vitis vinifera 'Malvasia Fina' plants with well-characterized esca complex disease symptoms (n = 18) and from healthy uninfected plants (n = 6). Leaves from diseased plants were divided into three groups: asymptomatic (ASY), chlorotic (SY1), and scorched leaves (SY2). The metabolic profile of these leaves was then examined using an ultrahigh performance liquid chromatography system coupled to a Q-Exactive Hybrid Quadrupole-Orbitrap high resolution/accurate mass spectrometer interfaced with a heated electrospray ionization source. The number of small molecules measured in a sample was increased by varying the reconstitution solvent, chromatographic column, and ionization source. Data on accurate masses, peak areas, and relative levels of several metabolites were documented for each leaf sample, using the abovementioned approach. In this paper, data on 235 metabolites of known structural identity are reported, along with the biochemical pathways to which the metabolites belong. The remaining data related to lipid species and with a different focus of the research question are reported elsewhere. The broad coverage of metabolites reported here resulted in a greater coverage of the biochemical pathways involved in grapevine metabolism, which could provide a better understanding of the biochemical changes occurring during the onset and progression of foliar symptoms after invasion of woods by esca-associated pathogens. To determine which metabolites varied according to the study design, the detected ion features were processed using different statistical methods, including mean and median values, fold changes, Welch's two-sample t-test, false discovery rate, and quartiles represented by box and whisker plots. The goal of this statistical evaluation was to assess the responses of healthy, asymptomatic, and symptomatic leaf groups using a pairwise comparison, thus providing an opportunity for detecting statistically significant compounds and uncovering the dynamic metabolic models underlying disease latency and symptom expression.

Project description:BackgroundWhole genome transcriptomics analysis is a very powerful approach because it gives an overview of the activity of genes in certain cells or tissue types. However, biological interpretation of such results can be rather tedious. MapMan is a software tool that displays large datasets (e.g. gene expression data) onto diagrams of metabolic pathways or other processes and thus enables easier interpretation of results. The grapevine (Vitis vinifera) genome sequence has recently become available bringing a new dimension into associated research. Two microarray platforms were designed based on the TIGR Gene Index database and used in several physiological studies.ResultsTo enable easy and effective visualization of those and further experiments, annotation of Vitis vinifera Gene Index (VvGI version 5) to MapMan ontology was set up. Due to specificities of grape physiology, we have created new pictorial representations focusing on three selected pathways: carotenoid pathway, terpenoid pathway and phenylpropanoid pathway, the products of these pathways being important for wine aroma, flavour and colour, as well as plant defence against pathogens. This new tool was validated on Affymetrix microarrays data obtained during berry ripening and it allowed the discovery of new aspects in process regulation. We here also present results on transcriptional profiling of grape plantlets after exposal to the fungal pathogen Eutypa lata using Operon microarrays including visualization of results with MapMan. The data show that the genes induced in infected plants, encode pathogenesis related proteins and enzymes of the flavonoid metabolism, which are well known as being responsive to fungal infection.ConclusionThe extension of MapMan ontology to grapevine together with the newly constructed pictorial representations for carotenoid, terpenoid and phenylpropanoid metabolism provide an alternative approach to the analysis of grapevine gene expression experiments performed with Affymetrix or Operon microarrays. MapMan was first validated on an already published dataset and later used to obtain an overview of transcriptional changes in a susceptible grapevine - Eutypa lata interaction at the time of symptoms development, where we showed that the responsive genes belong to families known to be involved in the plant defence towards fungal infection (PR-proteins, enzymes of the phenylpropanoid pathway).

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Oxygen Radical-Generating Metabolites Secreted by Eutypa and Esca Fungal Consortia: Understanding the Mechanisms Behind Grapevine Wood Deterioration and Pathogenesis

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