Metabolome and whole transcriptome analyses reveal the molecular mechanisms underlying terpenoids biosynthesis in Sapindus mukorossi fruits

Sapindus mukorossi fruit has been widely used as a source of daily necessities, cosmetics, biomedicine, and biodiesel due to its high terpenoids content. However, a systematic inventory of the regulatory mechanisms of terpenoids biosynthesis at different stages of fruit growth is still lacking. Here, we identified 50 terpenoid metabolites by terpenoid-targeted metabolomics and found that the most abundant kinds of terpenoids are triterpenoids and sesquiterpenoids. Mukurozioside and pyishiauoside of sesquiterpenoids were significantly upregulated in the mature fruit (S3) compared with the young fruit (S1) and mid-mature fruit (S2), indicating that they may be important factors leading to a high content of terpenoids. A total of 1669 differentially expressed (dif) lncRNAs, 13 dif-circRNAs, 219 dif-miRNAs, and 17,529 dif-mRNAs were identified by whole-transcriptome data. Enrichment analysis showed that these dif-RNAs were significantly enriched in phenylpropanoid biosynthesis, metabolic process, and plant hormone signal transduction. Co-expression and ceRNA network analysis showed that lncRNA:MSTRG.18127.1 was positively correlated with gma-miR156k, SmHSF14, and SmAXY4, regulating secondary metabolite biosynthesis. Correlation analysis between transcriptome and metabolite profiling showed that SmSE, Smβ-AS, SmCYP716A, SmUGT73, SmUGT94, SmTPS1, and SmTPS26 are key regulatory genes and that the upregulation of these genes may be beneficial to terpenoids biosynthesis. These findings can help elucidate the molecular mechanisms and regulatory networks of terpenoids biosynthesis in S. mukorossi and provide a biological basis for genomics-enabled improvements in molecular breeding.