Osmanthus fragrans is a well-known ornamental tree species for its pleasing floral fragrance. Linalool, as the characteristic aromatic component of O. fragrans, holds significant potential for applications in the flavor and fragrance industry. Although jasmonic acid (JA) is well documented to regulate the biosynthesis and accumulation of various plant secondary metabolites, its role in linalool biosynthesis remains largely unclear. Here, we discovered a positive correlation between the endogenous JA levels and linalool accumulation during the flowering stage of O. fragrans. Exogenous JA treatment was shown to enhance linalool biosynthesis by activating the linalool synthase gene OfTPS2. Dual-LUC and EMSA assays demonstrated that the key protein in the JA signaling pathway, OfJAZ3, interacted with OfMYB21 and subsequently suppressed the transcriptional activation of OfTPS2 mediated by OfMYB21. Functional validation further revealed that overexpression of OfJAZ3 significantly inhibited linalool biosynthesis in O. fragrans, A. thaliana, and N. tabacum plants. In contrast, JA promoted the degradation of OfJAZ3, thereby disrupting the formation of the OfJAZ3-OfMYB21 complex and relieving its inhibitory effect on OfTPS2. Split-LUC, BiFC, and pull-down assays confirmed that OfJAZ3 interacted with the F-box protein OfCOI1 (a key component of the E3 ubiquitin ligase SCFCOI1 complex), and JA treatment enhanced the strength of this interaction. Moreover, OfCOI1 was found to participate in OfTPS2 regulation by facilitating the ubiquitination and degradation of OfJAZ3. In conclusion, our findings elucidate the molecular mechanism by which OfJAZ3-OfMYB21 complex mediates JA signaling to regulate linalool biosynthesis in O. fragrans.

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