The cross talk of sesquiterpenes and phenylpropanes mediated by the shikimic acid pathway affects essential oil content in Phoebe sheareri leaves

Plant essential oils contain abundant natural active compounds, mainly terpenes and phenylpropanes, with immense industrial and pharmaceutical applications. The opposite variations between sesquiterpenes and phenylpropanes are widespread, determining the application and value of essential oils. However, intricate regulatory mechanisms at the molecular level have not been uncovered. To this end, transcriptome, metabolome, high-performance gas chromatography, exogenous protocatechuic acid and ABA treatments were performed on P. sheareri leaves at different developmental stages. Results revealed that the content of essential oils in the young leaves (2.45 mg/g) was 70.14% higher than in mature ones (1.44 mg/g). Additionally, there were opposing variations in the accumulation of phenylpropanes and sesquiterpenes, which correlated with the differential expression genes (DEGs) enriched in the shikimate pathway, phenylpropanoid biosynthesis and related secondary metabolites pathways in P. sheareri leaves. Phenylpropanes and sesquiterpene profiles presented dynamic patterns that changed with leaf growth and were consistent with the pattern of key gene regulation in the corresponding paths. After the combined multi-omics analysis, structural genes (DHQS, TPS1, CYP707A2) and possible interacting TFs with the key genes (i.e., SHR, JA2L, WRKY12, WRKY76, and ERF113) could be responsible for the opposite relationship between phenylpropanes and sesquiterpenes. Different concentrations treatments of protocatechuic acid and ABA indicated shikimate pathway mediated biosynthesis and metabolism of phenylpropanes and sesquiterpenes in the P. sheareri leaves, in which the downregulated DHQS and CYP707A2, and upregulated TPS1 and SHR played the vital roles. Based on the identified differentially accumulated phenylpropanes, sesquiterpenes, and candidate hub DEGs, genetic and metabolic regulation mechanisms of secondary metabolites in the essential oils were further proposed, providing a new understanding of essential oils biosynthesis. Potential regulatory factors identified in this study will contribute to providing molecular traces for in-depth research on the relationship of phenylpropanes and sesquiterpenes biosynthesis, as well as product development for essential oils with higher value.