Deciphering the Activity of <i>Gaultheria procumbens</i> Essential Oil on <i>Arabidopsis</i> Defense Responses Using Transcriptomic and Metabolomic Approaches

Gaultheria procumbens essential oil (GEO) is a natural source of defense inducers, as it is essentially composed of methyl salicylate (MeSA), a compound that can be converted in plant tissues into salicylic acid (SA), a central phytohormone regulating plant immunity. To gain insight into the response of plants to GEO treatment, we performed transcriptomic and metabolomic analyses of GEO-treated Arabidopsis thaliana plants. RNA-Seq analysis showed that fewer than 300 genes were differentially regulated, most of them belonging to functional categories related to receptors, signaling pathways, and transcription factors associated with plant defense or salicylic acid biosynthesis and signal transduction. Using the Arabidopsis SA biosynthesis–deficient sid2 line, we investigated MeSA metabolism in plant leaves following foliar GEO treatment. Quantification of MeSA, free SA, and total SA revealed that MeSA was mainly metabolized within 48 hours after treatment and that GEO treatment led to the accumulation of conjugated forms of SA. Next, an untargeted metabolomic study was performed on GEO-treated leaves and on plants treated with the SA analogue Acibenzolar-S-methyl (Bion®). This analysis revealed the accumulation of several benzoic acid derivatives upon GEO treatment but no accumulation of defense-related compounds such as indoles. By contrast, Bion® treatment induced several indolic derivatives, including indole-3-carboxylic acid. This suggests that Bion® directly triggered defense responses, whereas GEO treatment exerted a priming effect. Accordingly, metabolomic responses of A. thaliana leaves to Colletotrichum higginsianum infection showed a stronger accumulation of plant defense metabolites in GEO-treated leaves compared with untreated leaves.