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Title: The terpene synthase gene family in Tripterygium wilfordii harbors a labdane-type diterpene synthase among the monoterpene synthase TPS-b subfamily

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.13410· OSTI ID:1427678
 [1];  [1];  [1];  [2];  [3];  [1]; ORCiD logo [1]
  1. Univ. of Copenhagen (Denmark). Plant Biochemistry Laboratory, Department of Plant and Environmental Sciences; Center for Synthetic Biology 'bioSYNergy' and Copenhagen Plant Sciences Centre, Copenhagen (Denmark)
  2. Univ. of Copenhagen (Denmark). Plant Biochemistry Laboratory, Department of Plant and Environmental Sciences
  3. Royal Institute of Technology, Stockholm (Sweden). Science for Life Laboratory, Kungliga Tekniska Högskolan

We present Tripterygium wilfordii (Celastraceae) is a medicinal plant with anti-inflammatory and immunosuppressive properties. Identification of a vast array of unusual sesquiterpenoids, diterpenoids and triterpenoids in T. wilfordii has spurred investigations of their pharmacological properties. The tri-epoxide lactone triptolide was the first of many diterpenoids identified, attracting interest due to the spectrum of bioactivities. To probe the genetic underpinning of diterpenoid diversity, an expansion of the class II diterpene synthase (diTPS) family was recently identified in a leaf transcriptome. Following detection of triptolide and simple diterpene scaffolds in the root, we sequenced and mined the root transcriptome. This allowed identification of the root-specific complement of TPSs and an expansion in the class I diTPS family. Functional characterization of the class II diTPSs established their activities in the formation of four C-20 diphosphate intermediates, precursors of both generalized and specialized metabolism and a novel scaffold for Celastraceae. Functional pairs of the class I and II enzymes resulted in formation of three scaffolds, accounting for some of the terpenoid diversity found in T. wilfordii. The absence of activity-forming abietane-type diterpenes encouraged further testing of TPSs outside the canonical class I diTPS family. TwTPS27, close relative of mono-TPSs, was found to couple with TwTPS9, converting normal-copalyl diphosphate to miltiradiene. The phylogenetic distance to established diTPSs indicates neo-functionalization of TwTPS27 into a diTPS, a function not previously observed in the TPS-b subfamily. Finally, this example of evolutionary convergence expands the functionality of TPSs in the TPS-b family and may contribute miltiradiene to the diterpenoids of T. wilfordii.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
FC02-07ER64494
OSTI ID:
1427678
Journal Information:
The Plant Journal, Vol. 89, Issue 3; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 58 works
Citation information provided by
Web of Science

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Cited By (12)

Trends in herbgenomics journal August 2018
Annotation of the Corymbia terpene synthase gene family shows broad conservation but dynamic evolution of physical clusters relative to Eucalyptus journal March 2018
Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution journal April 2019
Friedelane‐type triterpene cyclase in celastrol biosynthesis from Tripterygium wilfordii and its application for triterpenes biosynthesis in yeast journal April 2019
The expression of TwDXS in the MEP pathway specifically affects the accumulation of triptolide journal December 2019
Identification and functional characterization of diterpene synthases for triptolide biosynthesis from Tripterygium wilfordii journal December 2017
Nerylneryl diphosphate is the precursor of serrulatane, viscidane and cembrane-type diterpenoids in Eremophila species journal February 2020
Integrating pathway elucidation with yeast engineering to produce polpunonic acid the precursor of the anti-obesity agent celastrol journal January 2020
Probing the Single Key Amino Acid Responsible for the Novel Catalytic Function of ent-Kaurene Oxidase Supported by NADPH-Cytochrome P450 Reductases in Tripterygium wilfordii journal October 2017
Genome of Tripterygium wilfordii and identification of cytochrome P450 involved in triptolide biosynthesis journal February 2020
Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity journal October 2019
Production of Putative Diterpene Carboxylic Acid Intermediates of Triptolide in Yeast journal June 2017

Figures / Tables (19)