The Role of Low Molecular Weight Fungal Metabolites in Grapevine Trunk Disease Pathogenesis: Eutypa Dieback and Esca

Abstract

Eutypa dieback and Esca are serious grapevine trunk diseases (GTDs) caused by fungal consortia causing large economic losses in vineyards. Depending on the disease the species involved include Eutypa lata, Phaeoacremonium minimum, and Phaeomoniella chlamydospora. There is a need to understand the complex pathogenesis mechanisms used by these fungi to develop treatments for the diseases they cause. Low molecular weight metabolites (LMW) are known to be involved in non-enzymatic oxygen radical generation in fungal degradation of wood by some Basidiomycota species, and as part of our work to explore the basis for fungal consortia pathogenesis, LMW metabolite involvement by the causal GTD fungi was explored. The GTD fungal pathogens examined, E. lata, P. minimum and P. chlamydospora, were found to produce low molecular weight iron binding metabolites that preferentially reduced iron or redox cycled to produce hydrogen peroxide. Uniquely, different LMW metabolites isolated from the GTD fungi promoted distinct chemistries that are important in a type of non-enzymatic catalysis known as chelator-mediated Fenton (CMF) reactions. CMF chemistry promoted by LMW metabolites from these fungi allowed for the generation of highly reactive hydroxyl radicals under conditions promoted by the fungi. We hypothesize that this new reported mechanism may help to explain the necrosis of woody grapevine tissue as a causal mechanism important in pathogenesis in these two grapevine trunk diseases.

Microbial Biological Control of Fungi Associated with Grapevine Trunk Diseases: A Review of Strain Diversity, Modes of Action, and Advantages and Limits of Current Strategies

“…The enzymatic reduction of eutypine gives its corresponding alcohol, eutypinol, which is not toxic to grapevine, suggesting this as a detoxification pathway for eutypine [9]. In addition to eutypine, other phytotoxic compounds are thought to be involved in foliar symptoms [3,97,98]. For instance, Andolfi et al (2011) reported that E. lata produced related secondary metabolites, mainly acetylenic phenols, along with some low-molecular-weight metabolites involved in the chelator-mediated Fenton (CMF) reactions that generate highly damaging reactive hydroxyl radicals, likely inducing necrosis on grapevine wood tissue [3].…”

“…GTDs represent a group of vascular diseases caused by fungi affecting grapevine wood, mainly through pruning wounds, and inhabiting the xylem cells in the woody tissue [ 1 , 2 ]. The colonization of this tissue leads to a decline in the plant host because of a loss of the xylem function and subsequent decrease in hydraulic conductivity, causing significant necrosis and decay with time, which ultimately lead to foliar symptoms and grapevine death [ 3 , 4 , 5 ]. Esca, Botryosphaeria dieback, and Eutypa dieback are the most frequent on mature grapevines; they decrease vineyard longevity, thereby affecting wine quality and causing huge economic losses throughout the viticulture sector [ 6 , 7 ].…”