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

Xiaoyue Chen; Graham A Hudson; Charlotte Mineo; Bashar Amer; Edward E K Baidoo; Samantha A Crowe; Yuzhong Liu; Jay D Keasling; Henrik V Scheller

doi:10.1038/s41467-023-42877-0

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

Nat Commun. 2023 Nov 4;14(1):7101. doi: 10.1038/s41467-023-42877-0.

Authors

Xiaoyue Chen^{1

2

3}, Graham A Hudson^{2

4}, Charlotte Mineo^{1

2}, Bashar Amer^{2

5}, Edward E K Baidoo^{2

5}, Samantha A Crowe^{2

4

6}, Yuzhong Liu^{2

4}, Jay D Keasling^{2

4

5

6

7

8

9}, Henrik V Scheller^{10

11

12}

Affiliations

¹ Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720, USA.
² Joint BioEnergy Institute, 5885 Hollis Street, Emeryville, CA, 94608, USA.
³ Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, CA, 94720, USA.
⁴ California Institute of Quantitative Biosciences (QB3), University of California, Berkeley, CA, 94720, USA.
⁵ Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, CA, 94720, USA.
⁶ Department of Chemical & Biomolecular Engineering, University of California, Berkeley, CA, 94720, USA.
⁷ Department of Bioengineering, University of California, Berkeley, CA, 94720, USA.
⁸ Technical University of Denmark, DK-2800, Kongens Lyngby, Denmark.
⁹ Center for Synthetic Biochemistry, Shenzhen Institutes for Advanced Technologies, Shenzhen, China.
¹⁰ Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720, USA. hscheller@lbl.gov.
¹¹ Joint BioEnergy Institute, 5885 Hollis Street, Emeryville, CA, 94608, USA. hscheller@lbl.gov.
¹² Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, CA, 94720, USA. hscheller@lbl.gov.

Abstract

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.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't

MeSH terms

Glucose
Plants / metabolism
Saponaria* / genetics
Saponaria* / metabolism
Saponins*
Sugars
Transcriptome
Triterpenes* / metabolism
Uridine Diphosphate
Vaccaria* / genetics

Substances

Triterpenes
methyl jasmonate
Saponins
Uridine Diphosphate
Glucose
Sugars