Uncovering the Molecular Response of Oregano (Origanum vulgare L.) to 12C6+ Heavy-Ion Irradiation Through Transcriptomic and Metabolomic Analyses

<i>Origanum vulgare</i> L., a medicinal herb rich in bioactive phenols and terpenes, is recognized for its anti-inflammatory and antimicrobial properties. Heavy-ion beam mutagenesis, a sophisticated breeding technique, can induce significant variations in plants, thereby affecting their secondary metabolite production. This study utilized metabolomic and transcriptomic approaches to investigate the effects of ¹²C⁶⁺ heavy-ion irradiation on oregano. Our results indicated substantial changes in mutant lines, including marked alterations in plant height, leaf morphology, and biomass accumulation. Metabolomic analysis indicated that the differentially accumulated volatile compounds were primarily terpenoids. Furthermore, transcriptomic analysis indicated a predominant enrichment of differentially expressed genes in terpenoid biosynthesis. Integrated analyses identified key transcriptional changes in genes encoding terpenoid backbone enzymes, such as <i>GPPS</i>, <i>GGPPS</i>, <i>DXS</i>, and <i>HMGR</i>, and pinpointed candidate genes, including <i>TPS3</i>, <i>TPS6A</i>, <i>TPS6C</i>, <i>CYP71D178</i>, <i>CYP71D181</i>, and <i>CYP71D10B</i>, whose expression patterns were closely associated with the differential accumulation of carvacrol and thymol. This comprehensive study elucidates the molecular mechanisms underlying metabolic reprogramming induced by heavy-ion irradiation in oregano and offers valuable genetic resources for future metabolic engineering and precision breeding initiatives aimed at enhancing the production of valuable bioactive compounds.