Volatile linalool activates grapevine resistance against downy mildew with changes in the leaf metabolome

Abstract

Volatile organic compounds (VOCs) are produced by plants in response to biotic and abiotic stimuli. In grapevine, volatile terpenoids are triggered by downy mildew infection (caused by Plasmopara viticola), suggesting their involvement in plant defense responses. In particular, linalool was detected in leaves of downy mildew-resistant genotypes, but no information is available on its involvement in the defense mechanisms against P. viticola. The aim of this study was to investigate the defense mechanisms activated by linalool in grapevine leaves against P. viticola and to identify metabolic changes associated with linalool-induced resistance. Linalool treatment reduced downy mildew severity on leaf disks of susceptible grapevines (cultivar Pinot noir) and stimulated callose deposition at the sites of P. viticola infection. Moreover, the upregulation of defense-related genes was found in linalool-treated leaf disks, indicating the activation of grapevine defense mechanisms of salicylic acid and jasmonic acid pathways. Linalool treatment caused changes in the leaf metabolome of mock-inoculated and P. viticola-inoculated samples at one and six days post inoculation, as revealed by ultra-high pressure liquid chromatography-electrospray ionization-high-resolution quadrupole time of flight-mass spectrometry. Pathway analysis of annotated features with significant increases and decreases in abundance revealed the reprogramming of amino acid, phenylpropanoid, and terpenoid metabolisms in response to linalool treatment and P. viticola inoculation. In particular, features with significant increases in abundance in linalool-treated samples mainly belonged to putative phenylpropanoids, putative terpenoids, putative lipids, and lipid-like compounds, including molecules possibly associated with plant defense against pathogens, such as 2-phenylethanol, 2,4-heptadienal, α-terpineol, citral, and geraniol. These results demonstrated that linalool induces grapevine resistance against downy mildew, acting as a signaling molecule for plant resistance induction.

Keywords

• Volatile organic compounds
• Induced systemic resistance
• Vitis vinifera
• Downy mildew
• Untargeted metabolomics analysis
• Gene expression