Effects of phenanthrene on the essential oil composition and leaf metabolome in peppermint plants (Mentha piperita L.)

Polycyclic aromatic hydrocarbons (PAHs) are an important type of persistent organic pollutant that endangers soil ecosystems and human health. Cultivating aromatic plants in PAH-contaminated soils is considered a safe and sustainable phytoremediation strategy to mitigate PAH soil pollution. However, the impact of PAHs on plant essential oils and the metabolic responses within aromatic plants remain unclear. In this study, we investigated the effects of the model PAH phenanthrene (Phe) on the chemical composition of essential oils in the ubiquitous aromatic plant peppermint (Mentha piperita L.) using gas chromatography-mass spectrometry (GC-MS). A total of 56 essential oil components were identified in the plants, among which the ratios of 21 components were significantly altered by Phe exposure. However, the fundamental components of peppermint essential oils including menthol, menthone, menthofuran, and pulegone did not exhibit considerable changes in levels. Thus, Phe stress may have little effect on the primary characteristics of peppermint essential oils. We also evaluated the effects of Phe treatment on metabolome dynamics within peppermint leaves by detecting metabolites in leaves treated with Phe for 0, 1, 3, 5, and 7 days (d) using non-targeted metabolomics. Compared with their corresponding control groups, 26 key different metabolites in the Phe-treated groups were identified and annotated via enrichment analysis with the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. Enriched metabolites were primarily involved in the oxidation of unsaturated fatty acids (UFAs), phenylpropanoid metabolism, amino acids, and the formation of vitamin C and caffeine. Phe treatment significantly promoted the oxidation of UFAs, phenylpropanoid metabolism, and histidine production in the first three days of Phe treatment. After 3 d, Phe gradually suppressed the oxidation of UFAs and L-glutamic acid production, while promoting phenylpropanoid metabolism, in addition to the synthesis of vitamin C and caffeine. The dynamic changes in metabolic pathway functioning in Phe-treated peppermint leaves reveal adaptive defensive mechanisms to mitigate Phe stress. This study provides new insights into the responses of aromatic plants toward PAH stress, while also providing a reference for the application of aromatic plants in the phytoremediation of PAH-contaminated soils.