Unveiling the molecular regulations of terpenoid biosynthesis in Sanqi flowers across two cultivation systems and flowering stages using multiomics approaches

The quality of Sanqi flowers is significantly influenced by the cultivation system of Sanqi. However, a comparison of the quality of Sanqi flowers during different flowering stages obtained from the Pinus armandii -Sanqi (PAS) and Pinus yunnanensis -Sanqi (PYS) agroforestry systems has hitherto not been conducted. Herein, a systematic analysis of the molecular mechanisms of terpenoid biosynthesis in the Sanqi flowers was performed using multiomics (GC-MS, LC-MS and transcriptomics) analyses. Totally, 41 and 42 types of volatile organic compounds (VOCs), predominantly classified as sesquiterpenoids, were present in Sanqi flowers from the PAS and PYS systems, respectively. Germacrene D was notably prominent in Sanqi flowers from the PAS system. Moreover, 154 metabolites of nonvolatile terpenoids were identified, which primarily included triterpenoid saponins (84.415 %) and triterpenoids (15.585 %). Cultivation system chiefly contributed to differences in the VOCs and non-VOCs of Sanqi flowers. A total of 45 and 49 differentially expressed metabolites were significantly upregulated in the early and full bloom stages, respectively, of Sanqi flowers from the PAS system. Furthermore, gypenoside XVII, gypenoside IX, notoginsenoside Fd, ginsenoside Rd, and chikusetsusaponin-FK1 were the major non-VOCs. Additionally, the SQLE and GERD genes directly regulated the biosynthesis of triterpenoids and sesquiterpenoids, respectively. The yeast one-hybrid system indicated that MYB61 transcription factor interacted with the GERD gene. Thus, Sanqi flowers of higher quality were obtained from the PAS system. Our results contribute to revealing the molecular mechanisms in terpenoid compounds in Sanqi flowers from the PAS systems, laying the foundation for the application of metabolites in the Sanqi flowers. • Cultivation systems chiefly contribute to differences in the VOCs and non-VOCs of Sanqi flowers. • Sesquiterpenoids and triterpenoid saponins are the primary VOCs and non-VOCs, respectively. • SQLE and GERD genes regulate terpenoid biosynthesis in Sanqi flowers. • MYB61 transcription factor interacted with the GERD gene. • High-quality of Sanqi flowers can be obtained with the Pinus armandii -Sanqi system.