A Lipidomic Analysis of Leaves of Esca-Affected Grapevine Suggests a Role for Galactolipids in the Defense Response and Appearance of Foliar Symptoms

Both qualitative and quantitative changes occur in the lipid composition of Vitis vinifera L. tissues, which may compromise the defense response against Esca complex disease, a widespread and damaging trunk disease. In this study, a lipidomic analysis of grapevine leaves is conducted to assess how lipid membrane remodeling relates to the emergence and progression of Esca foliar symptoms. In total, 208 molecular species (including lipids, four hormones, and some other compounds of the metabolism of lipids) were detected. Lipid species were readily assigned to the classes fatty acyls, glycerolipids, glycerophospholipids, sphingolipids, sterols, and prenol lipids. Using different clustering analyses, distinct metabolic pathways stimulated at different stages of disease development were characterized. These analyses revealed consistent changes in the abundance of 13 galactolipids and two diacylglycerolipids. Overall, the observations indicated an increment in the levels of these lipid species in leaves of asymptomatic vines and a progressive drop with increasing foliar symptom severity in symptomatic vines. Five fatty acids also appear to exert a central role in the etiopathogenesis of Esca complex disease because of their accumulation in leaves of asymptomatic vines, namely, heptadecanoic, linoleic, γ-linolenic, arachidonic, and stearic acids. Symptomatic leaves were characterized by high levels of all lipid classes, except for galactolipids, lyso-galactolipids, and compounds relevant to the biosynthesis of chlorophylls and carotenoids, that exhibited decreased levels. The data also suggested a jasmonic acid-associated signaling mechanism activation upon the invasion of woods by Esca-associated fungi, compared with abscisic and salicylic acids. Further research is required for validation of these results with additional molecular analyses using more vine cultivars.