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Information on EC 4.2.3.131 - miltiradiene synthase
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EC Tree
4.2.3.131 miltiradiene synthaseIUBMB Comments
Isolated from the plants Rosmarinus officinalis (rosemary) and Salvia miltiorrhiza. The enzyme from the plant Selaginella moellendorffii is mutifunctional and also catalyses EC 5.5.1.12, copalyl diphosphate synthase .
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Word Map
- 4.2.3.131
-
diterpenoids
- salvia
-
diterpene
- tanshinones
- miltiorrhiza
- synthases
-
copalyl
- triptolide
- wilfordii
-
tripterygium
-
hairy
- carnosol
-
glandular
-
ent-cpp
- lamiaceae
- jasmonate
-
labdane-related
- cyclases
- ferruginol
- benthamiana
- trichome
-
cosy
-
one-hybrid
- synthesis
The expected taxonomic range for this enzyme is: Bacteria, Eukaryota
Synonyms
miltiradiene synthase, smmds, sfksl, kaurene synthase-like 1, irtps4, twtps27v2, ent-kaurene synthase-like, 
more
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SYNONYM 
ORGANISM
UNIPROT
COMMENTARY 
LITERATURE
KSL
KSL1
SmiKSL
-
-
-
-
SmMDS
-
-
-
-
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REACTION
REACTION DIAGRAM
COMMENTARY
ORGANISM
UNIPROT
LITERATURE
(+)-copalyl diphosphate = miltiradiene + diphosphate
-
-
-
-
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PATHWAY SOURCE
PATHWAYS
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SYSTEMATIC NAME
IUBMB Comments
(+)-copaly-diphosphate diphosphate-lyase (cyclizing, miltiradiene-forming)
Isolated from the plants Rosmarinus officinalis (rosemary) and Salvia miltiorrhiza. The enzyme from the plant Selaginella moellendorffii is mutifunctional and also catalyses EC 5.5.1.12, copalyl diphosphate synthase [2].
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SUBSTRATE
PRODUCT
REACTION DIAGRAM
ORGANISM
UNIPROT
COMMENTARY
(Substrate)
(Substrate)
LITERATURE
(Substrate)
(Substrate)
COMMENTARY
(Product)
(Product)
LITERATURE
(Product)
(Product)
Reversibility
r=reversible
ir=irreversible
?=not specified
r=reversible
ir=irreversible
?=not specified
8-hydroxy-(+)-copalyl diphosphate
manoyl oxide + diphosphate
-
-
-
?
(+)-copalyl diphosphate
miltiradiene + diphosphate
-
-
-
?
(+)-copalyl diphosphate
miltiradiene + diphosphate
-
-
the enzyme is quite specific in its production of miltiradiene with more than 95% of the total product output
-
?
(+)-copalyl diphosphate
miltiradiene + diphosphate
-
products are abietatriene and miltiradiene, ratio of miltiradiene to abietatriene is 100:30. Miltiradiene spontaneously reacts to abietatriene
-
?
(+)-copalyl diphosphate
miltiradiene + diphosphate
-
-
-
?
additional information
?
-
synthesis of miltiradiene through the enzyme is confirmed by 1D and 2D NMR analyses, GC-MS analysis, overview
-
-
?
additional information
?
-
-
synthesis of miltiradiene through the enzyme is confirmed by 1D and 2D NMR analyses, GC-MS analysis, overview
-
-
?
additional information
?
-
-
MDS is a bifunctional miltiradiene synthase catalyzing the cyclization reaction of geranylgeranyl diphosphate via (+)-copalyl diphosphate to afford miltiradiene as a final product
-
-
?
additional information
?
-
substrate specificity analysis, rosemary RoKSL1/2 are functional enzymes able to convert either 8-OH-CDP or CDP into manoyl oxide or miltiradiene, respectively, and that they likely function in planta as miltiradiene synthases
-
-
?
additional information
?
-
substrate specificity analysis, rosemary RoKSL1/2 are functional enzymes able to convert either 8-OH-CDP or CDP into manoyl oxide or miltiradiene, respectively, and that they likely function in planta as miltiradiene synthases
-
-
?
additional information
?
-
miltiradiene spontaneously forms abietatriene
-
-
?
additional information
?
-
-
miltiradiene spontaneously forms abietatriene
-
-
?
additional information
?
-
GC-MS analysis of TwTPS27 assay product
-
-
?
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NATURAL SUBSTRATE
NATURAL PRODUCT
REACTION DIAGRAM
ORGANISM
UNIPROT
COMMENTARY
(Substrate)
(Substrate)
LITERATURE
(Substrate)
(Substrate)
COMMENTARY
(Product)
(Product)
LITERATURE
(Product)
(Product)
REVERSIBILITY
r=reversible
ir=irreversible
?=not specified
r=reversible
ir=irreversible
?=not specified
(+)-copalyl diphosphate
miltiradiene + diphosphate
-
-
-
?
(+)-copalyl diphosphate
miltiradiene + diphosphate
-
-
-
?
additional information
?
-
substrate specificity analysis, rosemary RoKSL1/2 are functional enzymes able to convert either 8-OH-CDP or CDP into manoyl oxide or miltiradiene, respectively, and that they likely function in planta as miltiradiene synthases
-
-
?
additional information
?
-
substrate specificity analysis, rosemary RoKSL1/2 are functional enzymes able to convert either 8-OH-CDP or CDP into manoyl oxide or miltiradiene, respectively, and that they likely function in planta as miltiradiene synthases
-
-
?
additional information
?
-
miltiradiene spontaneously forms abietatriene
-
-
?
additional information
?
-
-
miltiradiene spontaneously forms abietatriene
-
-
?
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METALS and IONS
ORGANISM
UNIPROT
COMMENTARY
LITERATURE
Mg2+
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pH OPTIMUM
ORGANISM
UNIPROT
COMMENTARY
LITERATURE
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TEMPERATURE OPTIMUM
ORGANISM
UNIPROT
COMMENTARY
LITERATURE
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ORGANISM
COMMENTARY
LITERATURE
UNIPROT
SEQUENCE DB
SOURCE
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SOURCE TISSUE
ORGANISM
UNIPROT
COMMENTARY
LITERATURE
SOURCE
low content of enzyme KSL3, moderate content of enzyme KSL1
brenda
high content of enzyme KSL1, moderate content of enzyme KSL3
brenda
additional information
high content of enzyme KSL3, moderate content of enzyme KSL1
brenda
young leaves show higher accumulation of SfKSL transcripts, when compared to the fully expanded leaves, consistent with the trichome and developmental regulation of carnosic acid build-up
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elevated expression in trichome of young leaf. Isoform KSL1 transcript level is less than 1% of expression of isoform KSL2
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periderm and cortex, high content of enzyme KSL1, low content of enzyme KSL3
brenda
additional information
expression patterns of isozymes KSL1 and KSL3, overview
brenda
additional information
real-time PCR analysis demonstrates higher expression level of SfKSL in isolated trichomes than in leaves without trichomes
brenda
additional information
-
real-time PCR analysis demonstrates higher expression level of SfKSL in isolated trichomes than in leaves without trichomes
brenda
additional information
quantitative RT-PCR expression analysis on whole leaves shows that RoKSL2 and RoKSL1 are preferentially expressed in young leaves, with RoKSL1 being much less expressed than RoKSL2. Direct comparison of the expression levels between RoKSL1 and RoKSL2 in isolated trichomes and in the remaining leaves indicates that RoKSL1 is not specific to the trichomes and significantly less expressed than RoKSL2 (RoKSL1 transcript level about 1% of expression of RoKSL2)
brenda
additional information
quantitative RT-PCR expression analysis on whole leaves shows that RoKSL2 and RoKSL1 are preferentially expressed in young leaves, with RoKSL1 being much less expressed than RoKSL2. Direct comparison of the expression levels between RoKSL1 and RoKSL2 in isolated trichomes and in the remaining leaves indicates that RoKSL1 is not specific to the trichomes and significantly less expressed than RoKSL2 (RoKSL1 transcript level about 1% of expression of RoKSL2)
brenda
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LOCALIZATION
ORGANISM
UNIPROT
COMMENTARY
GeneOntology No.
LITERATURE
SOURCE
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GENERAL INFORMATION
ORGANISM
UNIPROT
COMMENTARY
LITERATURE
evolution
malfunction
RNA interference targeting either both of the copalyl diphosphate synthases, TwTPS7v2 and TwTPS9v2, or the subsequently acting miltiradiene synthase, TwTPS27v2, leads to decreased production of triptolide
metabolism
physiological function
additional information
relationship of CPS and KSL genes and metabolic connection
evolution
the enzyme TwTPS27v2 belongs to the terpene synthases superfamily and the TPS-b subfamily
evolution
TwTPS27 belongs to the terpene synthase super family, subfamily TPS-b, additional diTPS detected in clade TPS-b detected in Tripterygium wilfordii roots by transcriptome analysis, overview
metabolism
Lamiaceae-specific clade genes (IrCPS1 and IrCPS2) synthesize the intermediate copalyl diphosphate (normal-CPP), while IrCPS4 and IrCPS5 synthesize the intermediate ent-copalyl diphosphate (ent-CPP). IrKSL2, IrKSL4, and IrKSL5 react with ent-CPP to produce an ent-isopimaradiene-like compound, ent-atiserene and ent-kaurene, respectively. Correspondingly, the Lamiaceae-specific clade genes IrKSL1 or IrKSL3 combined with normal-CPP lead to the formation of miltiradiene. Proposed diterpenoid biosynthesis in Isodon rubescens with two sequential diterpene synthases CPS1 and 2 and KSL1 and 3, overview. Miltiradiene is the precursor of abietatriene
metabolism
miltiradiene is the relevant precursor in the biosynthesis of tripolide. Triptolide production is induced by methyl jasmonate. ENzyme TwTPS7v2, TwTPS9v2 and TwTPS27v2 are involved in triptolide biosynthesis
metabolism
miltiradiene synthase TwTPS27 couples with copalyl diphosphate synthase TwTPS9 converting normal copalyl diphosphate to miltiradiene, GC-MS analysis of TwTPS9/CPS and TwTPS27 assay products. Detection of several simple abietane-type diterpenes and triptolide in the root, specific targeting of the transcriptome of the root for discovery of additional candidate TPSs with a characteristic DxDD motif and involved in the biosynthesis of diterpenoids in Tripterygium wilfordii, overview
metabolism
several stereoisomers of copalyl diphosphate (CDP) are found, among which the most common is ent-CDP, the precursor of gibberellins. Other isomers are syn-CDP and normal-CDP, the latter being utilized for the biosynthesis of diterpene resin acids in Gymnosperms and abietane-type tanshinones in Salvia miltiorrhiza. The second step of the cyclization is initiated through the formation of a carbocation upon ionization of the diphosphate linkage of CDP. This is catalyzed by class I terpene synthases which can transform CDP into a variety of polycyclic diterpenoids. By analogy to other labdane-type diterpenoids, the biosynthesis of the diterpene precursor of the carnosic acid pathway in rosemary proceeds in two sequential steps catalyzed by two distinct enzymes. The first is a class II TPS enzyme, CPS1, EC 5.5.1.12, that yields normal CDP, which then is converted by a KSL enzyme to yield an abietane diterpene, miltiradiene. Miltiradiene synthase appears in two isoforms, RoKSL1 and RoKSL2, in Rosmarinus officinalis. Hypothetical biosynthetic pathway of carnosic acid and carnosol produced in Rosmarinus officinalis, overview
physiological function
Nicotiana benthamiana transient expression of copalyl diphosphate synthase CPS1 with isoform KSL1 results in the production of miltiradiene plus about 25% abietatriene
physiological function
enzyme SfKSL is responsible for the formation of the carnosic acid precursor miltiradiene
physiological function
miltiradiene is the relevant precursor in the biosynthesis of tripolide. Triptolide and celastrol are the main active diterpenoid and triterpenoid ingredients, respectively, that exhibit impressive and effective anti-inflammatory, immunosuppressive and anti-tumor activities and make Tripterygium wilfordii a medicinal plant
physiological function
miltiradiene synthase TwTPS27 couples with copalyl diphosphate synthase TwTPS9 converting normal copalyl diphosphate to miltiradiene
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UNIPROT
ENTRY NAME
ORGANISM
NO. OF AA
NO. OF TRANSM. HELICES
MOLECULAR WEIGHT[Da]
SOURCE
SEQUENCE
LOCALIZATION PREDICTION
The reliability class of the localization prediction ranges from 1 (very reliable) to 5 (not reliable).
The reliability class of the localization prediction ranges from 1 (very reliable) to 5 (not reliable). ELS_MARVU
580
0
67098
Swiss-Prot
Chloroplast (Reliability: 4)
TPS4_SELML
867
0
99915
Swiss-Prot
Chloroplast (Reliability: 2)
KSL1_ISORU
626
0
72049
Swiss-Prot
Mitochondrion (Reliability: 4)
KSL1_SALMI
595
0
68370
Swiss-Prot
Chloroplast (Reliability: 3)
KSL2_ISOJA
597
0
68540
Swiss-Prot
Mitochondrion (Reliability: 5)
KSL3_ISORU
782
0
89155
Swiss-Prot
other Location (Reliability: 4)
A0A8F6T6Q0_9LAMI
597
0
68623
TrEMBL
Chloroplast (Reliability: 5)
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PDB
SCOP
CATH
UNIPROT
ORGANISM
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PROTEIN VARIANTS
ORGANISM
UNIPROT
COMMENTARY
LITERATURE
D391G/D392G
-
the mutant converts only (+)-copalyl diphosphate but not ent- or syn-copalyl diphosphate
D611G/D612G
-
the mutant converts geranylgeranyl diphosphate to ent-copalyl diphosphate
additional information
additional information
RNAi targeting of TwTPS27v2 is carried out reduces the transcript level of TwTPS27v2 to about 30%, with no reduction in the levels of the related TPS-b subfamily members TwTPS22v2, TwTPS23v2, TwTPS32 and TwTPS33, triptolide accumulation is decreased by about 40%
additional information
-
RNAi targeting of TwTPS27v2 is carried out reduces the transcript level of TwTPS27v2 to about 30%, with no reduction in the levels of the related TPS-b subfamily members TwTPS22v2, TwTPS23v2, TwTPS32 and TwTPS33, triptolide accumulation is decreased by about 40%
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PURIFICATION (Commentary)
ORGANISM
UNIPROT
LITERATURE
recombinant HA-His-tandem-tagged enzyme from Escherichia coli strain BL21-CodonPlus (DE3)-RIL by nickel affinity chromatography
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CLONED (Commentary)
ORGANISM
UNIPROT
LITERATURE
cDNA library screening and miltiradiene DNA and amino acid sequence determination and analysis, sequence comparisons and phylogenetic analysis
cloning of full-length cDNA, DNA and amino acid sequence determination and analysis, sequence comparisons and phylogenetic analysis, recombinant transient Agrobacterium tumefaciens-mediated coexpression of Isodon rubescens gene TPS4, encoding miltiradiene synthase, with Isodon rubescens gene TPS3, encoding (+)-copalyl diphosphate synthase in Nicotiana benthamiana results in production of miltiradiene, while coexpression with Isodon rubescens gene TPS2, encoding ent-copalyl diphosphate synthase, does not lead to product formation
gene KSL, DNA and amino acid sequence determination and analysis, phylogenetic analysis, real-time PCR enzyme expression analysis, recombinant expression of HA-His-tandem-tagged enzyme in Escherichia coli strain BL21-CodonPlus (DE3)-RIL, functional transient recombinant coexpression of Salvia fruticosa (+)-copalyl diphosphate sythase (SfCPS) and Salvia fruticosa ent-kaurene synthase-like (SfKSL) in Nicotiana benthamiana via transfection by Agrobacterium tumefaciens leading to production of miltiradiene in planta, NMR product analysis
gene SKL1, DNA and amino acid sequence determination and analysis, sequence comparisons, phylogenetic analysis and tree, RoKSL1 and RoKSL2 cluster into a discrete clade, together with other KSL proteins from the Lamiaceae and Solanaceae (NtABS, ShSBS and SlPHS). Functional recombinant expression in Saccharomyces cerevisiae strain AM113, and transient coexpression of RoSKL1 and RoSKL2 in Nicotiana benthamiana leaves
gene SKL2, DNA and amino acid sequence determination and analysis, sequence comparisons, phylogenetic analysis and tree, RoKSL1 and RoKSL2 cluster into a discrete clade, together with other KSL proteins from the Lamiaceae and Solanaceae (NtABS, ShSBS and SlPHS). Functional recombinant expression in Saccharomyces cerevisiae strain AM113, and transient coexpression of RoSKL1 and RoSKL2 in Nicotiana benthamiana leaves
gene TwTPS27, sequence comparisons and phylogenetic analysis
TwTPS27v2, phylogenetic analysis and tree, coexpression of TwTPS27v2 with either copalyl diphosphate synthases TwTPS7v2 or TwTPS9v2 in appropriately engineered Saccharomyces cerevisiae strain, or recombinant coexpression in Escherichia coli, the combination with TwTPS7v2 produces miltiradiene, recombinant expression oof GFP-tagged enzyme TwTPS27v2 in Nicotiana benthamiana chloroplasts, quantitative RT-PCR expression analysis
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APPLICATION
ORGANISM
UNIPROT
COMMENTARY
LITERATURE
synthesis
-
expression of copalyl diphosphate synthase and miltiradiene synthase in Saccharomyces cerevisiae, results in production of 4.2 mg/l miltiradiene. Miltiradiene production increases to 8.8 mg/l by improving supply of geranylgeranyl diphosphate by over-expression of a fusion gene of farnesyl diphosphate synthase ERG20 and endogenous geranylgeranyl diphosphate synthase BTS1 together with a heterologous geranylgeranyl diphosphate synthase from Sulfolobus acidocaldarius. Combinatorial overexpression of truncated 3-hydroxyl-3-methylglutaryl-CoA reductase with a mutated global regulatory factor upc2.1 and ERG20-BTS1-geranylgeranyl diphosphate synthase genes has synergetic effects on miltiradiene production, increasing titer to 61.8 mg/l. In fed-batch fermentation 488 mg/l miltiradiene can be produced
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REF.
AUTHORS
TITLE
JOURNAL
VOL.
PAGES
YEAR
ORGANISM (UNIPROT)
PUBMED ID
SOURCE
Zhou, Y.J.; Gao, W.; Rong, Q.; Jin, G.; Chu, H.; Liu, W.; Yang, W.; Zhu, Z.; Li, G.; Zhu, G.; Huang, L.; Zhao, Z.K.
Modular pathway engineering of diterpenoid synthases and the mevalonic acid pathway for miltiradiene production
J. Am. Chem. Soc.
134
3234-3241
2012
Salvia miltiorrhiza
brenda
Sugai, Y.; Ueno, Y.; Hayashi, K.; Oogami, S.; Toyomasu, T.; Matsumoto, S.; Natsume, M.; Nozaki, H.; Kawaide, H.
Enzymatic (13)C labeling and multidimensional NMR analysis of miltiradiene synthesized by bifunctional diterpene cyclase in Selaginella moellendorffii
J. Biol. Chem.
286
42840-42847
2011
Salvia miltiorrhiza
brenda
Gao, W.; Hillwig, M.; Huango, L.; Cui, G.; Wang, X.; Kong, J.; Yang, B.; Peters, R.
A functional genomics approach to tanshinone biosynthesis provides stereochemical insights
Org. Lett.
11
5170-5173
2009
Salvia miltiorrhiza
brenda
Dai, Z.; Liu, Y.; Huang, L.; Zhang, X.
Production of miltiradiene by metabolically engineered Saccharomyces cerevisiae
Biotechnol. Bioeng.
109
2845-2853
2012
Salvia miltiorrhiza
brenda
Brueckner, K.; Bozic, D.; Manzano, D.; Papaefthimiou, D.; Pateraki, I.; Scheler, U.; Ferrer, A.; de Vos, R.C.; Kanellis, A.K.; Tissier, A.
Characterization of two genes for the biosynthesis of abietane-type diterpenes in rosemary (Rosmarinus officinalis) glandular trichomes
Phytochemistry
101
52-64
2014
Salvia rosmarinus (W8QEG7), Salvia rosmarinus (W8QMF8)
brenda
Brueckner, K.; Bozic, D.; Manzano, D.; Papaefthimiou, D.; Pateraki, I.; Scheler, U.; Ferrer, A.; de Vos, R.C.; Kanellis, A.K.; Tissier, A.
Characterization of two genes for the biosynthesis of abietane-type diterpenes in rosemary (Rosmarinus officinalis) glandular trichomes
Phytochemistry
101
52-64
2014
Salvia rosmarinus (W8QEG7), Salvia rosmarinus (W8QMF8)
brenda
Jin, B.; Cui, G.; Guo, J.; Tang, J.; Duan, L.; Lin, H.; Shen, Y.; Chen, T.; Zhang, H.; Huang, L.
Functional diversification of kaurene synthase-like genes in Isodon rubescens
Plant Physiol.
174
943-955
2017
Isodon rubescens (A0A1W6QDI7)
brenda
Pelot, K.A.; Hagelthorn, D.M.; Addison, J.B.; Zerbe, P.
Biosynthesis of the oxygenated diterpene nezukol in the medicinal plant Isodon rubescens is catalyzed by a pair of diterpene synthases
PLoS ONE
12
e0176507
2017
Isodon rubescens (A0A1W6QDI7), Isodon rubescens
brenda
Hansen, N.L.; Heskes, A.M.; Hamberger, B.; Olsen, C.E.; Hallstroem, B.M.; Andersen-Ranberg, J.; Hamberger, B.
The terpene synthase gene family in Tripterygium wilfordii harbors a labdane-type diterpene synthase among the monoterpene synthase TPS-b subfamily
Plant J.
89
429-441
2017
Tripterygium wilfordii (A0A1C7AAM8)
brenda
Su, P.; Guan, H.; Zhao, Y.; Tong, Y.; Xu, M.; Zhang, Y.; Hu, T.; Yang, J.; Cheng, Q.; Gao, L.; Liu, Y.; Zhou, J.; Peters, R.J.; Huang, L.; Gao, W.
Identification and functional characterization of diterpene synthases for triptolide biosynthesis from Tripterygium wilfordii
Plant J.
93
50-65
2018
Tripterygium wilfordii (A0A1C7AAM8), Tripterygium wilfordii
brenda
Bozic, D.; Papaefthimiou, D.; Brueckner, K.; de Vos, R.C.; Tsoleridis, C.A.; Katsarou, D.; Papanikolaou, A.; Pateraki, I.; Chatzopoulou, F.M.; Dimitriadou, E.; Kostas, S.; Manzano, D.; Scheler, U.; Ferrer, A.; Tissier, A.; Makris, A.M.; Kampranis, S.C.; Kanellis, A.K.
Towards elucidating carnosic acid biosynthesis in Lamiaceae Functional characterization of the three first steps of the pathway in Salvia fruticosa and Rosmarinus officinalis
PLoS ONE
10
e0124106
2015
Salvia fruticosa (A0A0C5QH30), Salvia fruticosa
brenda
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