Biotransformation of monoterpenols upon pre‐treatment with oregano essential oil vapour alleviates downy mildew susceptibility in grapevine leaves

Grapevine downy mildew, caused by the oomycete Plasmopara viticola, is a destructive disease that causes major economic losses as most elite grapevine cultivars are susceptible to this pathogen. As most crop protection strategies rely on synthetic pesticides that pose a threat to the environment and public health, alternative disease control methods are sought after. One such method involves the use of plant-derived essential oils (EOs). Previous studies on pre-treatment of grapevine with oregano EO vapour reported promising results in downy mildew management. Nevertheless, it remains unclear whether and how specialized metabolism is involved in the observed alleviation of downy mildew susceptibility. Grapevine individuals of a susceptible cultivar were pre-treated with oregano EO vapour for 24 h, after which the plants were inoculated with P. viticola. The effect of this pre-treatment on P. viticola infection in grapevine leaves was analysed by untargeted chemical profiling using LC-MS. Metabolite extracts were prepared from leaves harvested after pre-treatment, and at early (12 h) and late (216 h) timepoints after inoculation with P. viticola. After pre-treatment, monoterpenol disaccharides putatively annotated as dihexosides of (hydroxylated) aromatic (e.g. carvacrol/thymol) and aliphatic (e.g. terpeneol isomers) monoterpenols were detected by LC-MS/MS. These monoterpene(di)ol glycosides positively correlated with reduced disease severity in grapevine leaves 216 h after inoculation. Aromatic monoterpenols are major constituents of oregano EO, and their putative detection as aglycons suggests that monoterpenols emitted from oregano EO are biotransformed and thereafter stored as glycosides in grapevine leaves, which may negatively affect P. viticola proliferation. Overall, our findings highlight the potential of oregano EO as a tool for crop protection in the management of downy mildew proliferation in the susceptible grapevine cultivar 'Müller-Thurgau'.