Molecular, metabolic, hormonal, and cell wall profiling of ripe grapes exhibiting esca disease

Abstract

Esca is a major grapevine trunk disease caused by a consortium of xylem-colonising and wood-degrading fungi, including Phaeomoniella chlamydospora, Phaeoacremonium minimum and Fomitiporia mediterranea and poses a growing threat to vineyard longevity. While its aetiology and effects on vegetative tissues have been extensively studied, the impact on grape berries remains poorly characterised. Previous findings from our research indicate a more pronounced metabolic shift in fruits compared to vegetative organs. In the present study, ripe grapes (EL38) of Vitis vinifera cv. Aragonez (syn. Tempranillo) from infected plants with and without Esca foliar symptoms were analysed using an integrative approach combining RNAsequencing, two complementary mass spectrometry-based metabolomics techniques — gas chromatography–time-of-flight mass spectrometry (GC-TOF-MS) and ultra-high-performance liquid chromatography coupled to high-resolution mass spectrometry (UHPLC-HRMS) — and Fourier-transform infrared spectroscopy with attenuated total reflectance (FTIR–ATR). Despite limited differential expression of genes, pathway enrichment analysis revealed a coordinated transcriptional reprogramming related to activation of oxidative stress and proteostasis pathways together with broad repression of translation, vesicle trafficking, cell wall organisation, and central metabolism in grapes from symptomatic plants. These transcriptional patterns were consistent with the metabolomic profile, which showed a tendency toward reduced levels of hexose sugars and several amino acids, together with increased accumulation of polyols and organic acids. Hormone profiling further revealed lower abscisic acid content in these grapes, consistent with altered hormonal signalling when Esca foliar symptoms are present. Cell wall analysis indicated increased contributions of pectic and hemicellulosic matrix glycans, higher O-acetylation, and enrichment of wall-associated phenolics in grapes from symptomatic vines, with differences largely confined to alkali-labile matrix polysaccharide decorations rather than to the cellulose scaffold. Collectively, these findings reveal a coordinated systemic response in grapes from plants displaying Esca symptomatology, characterised by the activation of stress-associated pathways, together with the repression of primary metabolism and the restructuring of cellular processes, despite the absence of direct pathogen colonisation. This response is consistent with a physiological shift in the whole plant associated with Esca-related vascular dysfunction, providing new insight into the impact of Esca disease on grape composition and structure, with possible implications in wine quality.