Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution
Abstract
The mint family (Lamiaceae) is well documented as a rich source of terpene natural products. More than 200 diterpene skeletons have been reported from mints, but biosynthetic pathways are known for just a few of these. We crossreferenced chemotaxonomic data with publicly available transcriptomes to select common selfheal (Prunella vulgaris) and its highly unusual vulgarisin diterpenoids as a case study for exploring the origins of diterpene skeletal diversity in Lamiaceae. Four terpene synthases (TPS) from the TPS-a subfamily, including two localised to the plastid, were cloned and functionally characterised. Previous examples of TPS-a enzymes from Lamiaceae were cytosolic and reported to act on the 15-carbon farnesyl diphosphate. Plastidial TPS-a enzymes using the 20-carbon geranylgeranyl diphosphate are known from other plant families, having apparently arisen independently in each family. All four new enzymes were found to be active on multiple prenyl-diphosphate substrates with different chain lengths and stereochemistries. One of the new enzymes catalysed the cyclisation of geranylgeranyl diphosphate into 11-hydroxy vulgarisane, the likely biosynthetic precursor of the vulgarisins. We uncovered the pathway to a rare diterpene skeleton. Our results support an emerging paradigm of substrate and compartment switching as important aspects of TPS evolution and diversification.
- Authors:
-
[1];
[2];
[1];
[1]
- Michigan State Univ., East Lansing, MI (United States). Dept. of of Biochemistry and Molecular Biology
- Michigan State Univ., East Lansing, MI (United States). Dept. of of Biochemistry and Molecular Biology and Dept. of Pharmacology and Toxicology
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1546989
- Grant/Contract Number:
- FC02-07ER64494; SC0018409; 1737898.
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 223; Journal Issue: 1; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Diterpenoid; Prunella vulgaris (common selfheal); terpene synthase; transcriptome; transit peptide; vulgarisane
Citation Formats
Johnson, Sean R., Bhat, Wajid Waheed, Sadre, Radin, Miller, Garret P., Garcia, Alekzander Sky, and Hamberger, Björn. Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution. United States: N. p., 2019.
Web. doi:10.1111/nph.15778.
Johnson, Sean R., Bhat, Wajid Waheed, Sadre, Radin, Miller, Garret P., Garcia, Alekzander Sky, & Hamberger, Björn. Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution. United States. https://doi.org/10.1111/nph.15778
Johnson, Sean R., Bhat, Wajid Waheed, Sadre, Radin, Miller, Garret P., Garcia, Alekzander Sky, and Hamberger, Björn. Mon .
"Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution". United States. https://doi.org/10.1111/nph.15778. https://www.osti.gov/servlets/purl/1546989.
@article{osti_1546989,
title = {Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution},
author = {Johnson, Sean R. and Bhat, Wajid Waheed and Sadre, Radin and Miller, Garret P. and Garcia, Alekzander Sky and Hamberger, Björn},
abstractNote = {The mint family (Lamiaceae) is well documented as a rich source of terpene natural products. More than 200 diterpene skeletons have been reported from mints, but biosynthetic pathways are known for just a few of these. We crossreferenced chemotaxonomic data with publicly available transcriptomes to select common selfheal (Prunella vulgaris) and its highly unusual vulgarisin diterpenoids as a case study for exploring the origins of diterpene skeletal diversity in Lamiaceae. Four terpene synthases (TPS) from the TPS-a subfamily, including two localised to the plastid, were cloned and functionally characterised. Previous examples of TPS-a enzymes from Lamiaceae were cytosolic and reported to act on the 15-carbon farnesyl diphosphate. Plastidial TPS-a enzymes using the 20-carbon geranylgeranyl diphosphate are known from other plant families, having apparently arisen independently in each family. All four new enzymes were found to be active on multiple prenyl-diphosphate substrates with different chain lengths and stereochemistries. One of the new enzymes catalysed the cyclisation of geranylgeranyl diphosphate into 11-hydroxy vulgarisane, the likely biosynthetic precursor of the vulgarisins. We uncovered the pathway to a rare diterpene skeleton. Our results support an emerging paradigm of substrate and compartment switching as important aspects of TPS evolution and diversification.},
doi = {10.1111/nph.15778},
journal = {New Phytologist},
number = 1,
volume = 223,
place = {United States},
year = {Mon Apr 08 00:00:00 EDT 2019},
month = {Mon Apr 08 00:00:00 EDT 2019}
}
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Amphilectane Diterpenes from Salvia sclarea : Biosynthetic Considerations
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ent -Kaurane and Cembrane Diterpenoids from Isodon sculponeatus and Their Cytotoxicity
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New Antifeedant C 20 Terpenoids from Leucosceptrum canum
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Vulgarisin A, a New Diterpenoid with a Rare 5/6/4/5 Ring Skeleton from the Chinese Medicinal Plant Prunella vulgaris
journal, May 2014
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Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
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The I-TASSER Suite: protein structure and function prediction
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De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis
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Unusual Anti-allergic Diterpenoids from the Marine Sponge Hippospongia lachne
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ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data
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The Biochemical and Molecular Basis for the Divergent Patterns in the Biosynthesis of Terpenes and Phenylpropenes in the Peltate Glands of Three Cultivars of Basil
journal, October 2004
- Iijima, Yoko; Davidovich-Rikanati, Rachel; Fridman, Eyal
- Plant Physiology, Vol. 136, Issue 3
Characterization of the Monoterpene Synthase Gene tps26 , the Ortholog of a Gene Induced by Insect Herbivory in Maize
journal, January 2008
- Lin, Changfa; Shen, Binzhang; Xu, Zhennan
- Plant Physiology, Vol. 146, Issue 3
Gain and Loss of Fruit Flavor Compounds Produced by Wild and Cultivated Strawberry Species
journal, November 2004
- Aharoni, Asaph; Giri, Ashok P.; Verstappen, Francel W. A.
- The Plant Cell, Vol. 16, Issue 11
A Novel Pathway for Sesquiterpene Biosynthesis from Z,Z -Farnesyl Pyrophosphate in the Wild Tomato Solanum habrochaites
journal, January 2009
- Sallaud, Christophe; Rontein, Denis; Onillon, Sandrine
- The Plant Cell, Vol. 21, Issue 1
Formation of the Unusual Semivolatile Diterpene Rhizathalene by the Arabidopsis Class I Terpene Synthase TPS08 in the Root Stele Is Involved in Defense against Belowground Herbivory
journal, March 2013
- Vaughan, Martha M.; Wang, Qiang; Webster, Francis X.
- The Plant Cell, Vol. 25, Issue 3
Evolution of a Complex Locus for Terpene Biosynthesis in Solanum
journal, June 2013
- Matsuba, Y.; Nguyen, T. T. H.; Wiegert, K.
- The Plant Cell, Vol. 25, Issue 6
Production of Bioactive Diterpenoids in the Euphorbiaceae Depends on Evolutionarily Conserved Gene Clusters
journal, August 2014
- King, Andrew J.; Brown, Geoffrey D.; Gilday, Alison D.
- The Plant Cell, Vol. 26, Issue 8
pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants
journal, September 2009
- Sainsbury, Frank; Thuenemann, Eva C.; Lomonossoff, George P.
- Plant Biotechnology Journal, Vol. 7, Issue 7
The terpene synthase gene family in Tripterygium wilfordii harbors a labdane-type diterpene synthase among the monoterpene synthase TPS-b subfamily
journal, February 2017
- Hansen, Nikolaj L.; Heskes, Allison M.; Hamberger, Britta
- The Plant Journal, Vol. 89, Issue 3
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
text, January 2014
- Stamatakis, A.
- Karlsruhe
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Nerylneryl diphosphate is the precursor of serrulatane, viscidane and cembrane-type diterpenoids in Eremophila species
journal, February 2020
- Gericke, Oliver; Hansen, Nikolaj Lervad; Pedersen, Gustav Blichfeldt
- BMC Plant Biology, Vol. 20, Issue 1