Volatile 2-Phenylethanol and β-Cyclocitral Trigger Defense-Related Transcriptional and Metabolic Changes in Grapevine Leaves Against Downy Mildew.

Volatile organic compounds (VOCs) are produced by grapevine leaves in response to phytopathogen infection. In particular, 2-phenylethanol and β-cyclocitral were triggered by Plasmopara viticola inoculation in downy mildew-resistant genotypes, but no information is available on their involvement in plant resistance induction. This study aimed to clarify transcriptional and metabolic changes associated with VOC-induced resistance activated by 2-phenylethanol and β-cyclocitral treatments against P. viticola. Both VOCs decreased downy mildew severity on grapevine leaf disks by complex reprogramming of the grapevine transcriptome at 1 and 6 days post inoculation. RNA-Seq analysis showed the modulation of transcripts related to defense (chitinases, defense-related proteins, and pathogenesis-related proteins), oxidative stress (glutathione S-transferases and peroxidases), secondary metabolism (nitrilases, stilbene synthases, and terpene synthases), signal transduction (e.g., kinases, receptor kinases, and calmodulins), and transcription (bHLH, ERF, MYB, NAC, and WRKY transcription factors) in leaf disks treated with 2-phenylethanol and β-cyclocitral. VOC treatments also caused changes in the leaf metabolome, and pathway analysis of metabolic features with significant changes in abundance in 2-phenylethanol- and β-cyclocitral-treated leaf disks revealed the reprogramming of amino acid, carbohydrate, flavonoid, phenylpropanoid, and terpenoid metabolism. In particular, compounds with increases in abundance belonged to putative carbohydrates, carboxylic acids, and phenylpropanoids in 2-phenylethanol-treated samples, or carboxylic acids and terpenoids in β-cyclocitral-treated samples, including molecules possibly associated with plant defense against pathogens, such as 3-dehydroquinic acid, 4-thujanol, aromadendrin, camphor, p-coumaryl alcohol, and perillaldehyde. Correlation analysis between transcriptomic and metabolomic data indicated that 2-phenylethanol and β-cyclocitral act as resistance inducers against downy mildew in grapevine.