Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria

• Published in: Nature communications Vol. 14; no. 1; p. 7101
• Main Authors: Chen, Xiaoyue, Hudson, Graham A., Mineo, Charlotte, Amer, Bashar, Baidoo, Edward E. K., Crowe, Samantha A., Liu, Yuzhong, Keasling, Jay D., Scheller, Henrik V.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 04.11.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 38/39; 38/91; 631/449/2667; 631/449/447; 631/61/191/2018; 82/16; 82/58; 82/80; Aglycones; Aldehydes; Anticancer properties; Biosynthesis; Cellulose; Cellulose synthase; Cytochrome P450; Cytochrome P450 monooxygenase; Cytochromes P450; Dehydration; Fucose; Gene expression; Gene sequencing; Glucose; Glycosylation; Herbal medicine; Humanities and Social Sciences; Methyl jasmonate; Microorganisms; multidisciplinary; Natural products; Nucleotides; Optimization; Oxidation; Reductases; Saponaria; Saponins; Science; Science (multidisciplinary); Sugar; Traditional Chinese medicine; Transcriptomes; Triterpenoids
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-42877-0

Methyl jasmonate (MeJA) is a known elicitor of plant specialized metabolism, including triterpenoid saponins. Saponaria vaccaria is an annual herb used in traditional Chinese medicine, containing large quantities of oleanane-type triterpenoid saponins with anticancer properties and structural similarities to the vaccine adjuvant QS-21. Leveraging the MeJA-elicited saponin biosynthesis, we identify multiple enzymes catalyzing the oxidation and glycosylation of triterpenoids in S. vaccaria . This exploration is aided by Pacbio full-length transcriptome sequencing and gene expression analysis. A cellulose synthase-like enzyme can not only glucuronidate triterpenoid aglycones but also alter the product profile of a cytochrome P450 monooxygenase via preference for the aldehyde intermediate. Furthermore, the discovery of a UDP-glucose 4,6-dehydratase and a UDP-4-keto-6-deoxy-glucose reductase reveals the biosynthetic pathway for the rare nucleotide sugar UDP- d -fucose, a likely sugar donor for fucosylation of plant natural products. Our work enables the production and optimization of high-value saponins in microorganisms and plants through synthetic biology approaches. Methyl jasmonate triggers saponin production in Saponaria vaccaria . Using transcriptome data and heterologous expression, the authors identify P450s and glycosyltransferases that modify triterpenoids. They also discover the pathway for UDP-D-fucose biosynthesis.