Skip to main content
SpringerLink
Log in

Characterization of S-(+)-linalool synthase from several provenances of Cinnamomum osmophloeum

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Cinnamomum osmophloeum is a commercially important tree species in Taiwan, which has numerous chemotypes with various secondary metabolite profiles. The linalool chemotype is important because it generates pure S-(+)-linalool with high yield. In the present study, the linalool synthase (LIS) genes were isolated from different provenances of C. osmophloeum. The recombinant proteins of LIS were able to generate the S-(+)-linalool from GPP and (E)-nerolidol from FPP. Kinetic analysis showed differing enzyme activities of similar proteins from different provenances. Two point mutations enhanced enzyme activity up to sixfold. Phylogenetic analysis and leaf volatiles composition analysis clustered the genes into designated groups according to their chemotypes. Because the CoLIS-LL gene has a particularly abundant transcript, we suggest that the W-box, recognized by the WRKY transcription factor, might be responsible for high differential gene expression. A marker based on the W-box sequence can be used to distinguish linalool chemotype.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aharoni A, Giri A, Verstappen FWA, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aharoni A, Jongsma M, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602

    Article  CAS  PubMed  Google Scholar 

  • Aharoni A, Jongsma M, Kim TY, Ri MB, Giri AP, Verstappen FWA, Schwab W, Bouwmeester HJ (2006) Metabolic engineering of terpenoid biosynthesis in plants. Phytochem Rev 5:49–58

    Article  CAS  Google Scholar 

  • Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201

    Article  CAS  PubMed  Google Scholar 

  • Aubourg S, Lecharny A, Bohlmann J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Gen Genomics 267:730–745

    Article  CAS  Google Scholar 

  • Batista PA, de Paula Werner MF, Oliveira EC, Burgos L, Pereira P, da Silva Brum LF, Story GM, Santos ARS (2010) The antinociceptive effect of (–)-linalool in models of chronic inflammatory and neuropathic hypersensitivity in mice. J Pain 11:1222–1229

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci U S A 95:4126–4133

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Borg-Karlson AK, Unelius CR, Valterova I, Nilsson LA (1996) Floral fragrance chemistry in the early flowering shrub Daphne mezereum. Phytochemistry 41:1477–1483

    Article  CAS  Google Scholar 

  • Buckingham J (1993) Dictionary of natural products on DVD. Chapman and Hall/CRC, London

    Google Scholar 

  • Chang ST, Cheng SS (2002) Antitermitic activity of leaf essential oils and components from Cinnamomum osmophleum. J Agric Food Chem 50:1389–1392

    Article  CAS  PubMed  Google Scholar 

  • Chang ST, Chen PF, Chang SC (2001) Antibacterial activity of leaf essential oils and their constituents from Cinnamomum osmophloeum. J Ethnopharmacol 77:123–127

    Article  CAS  PubMed  Google Scholar 

  • Chappell J (1995) Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Annu Rev Plant Physiol Plant Mol Biol 46:521–547

    Article  CAS  Google Scholar 

  • Chen F, Tholl D, D’Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481–494

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng SS, Liu JY, Tsai KH, Chen WJ, Chang ST (2004) Chemical composition and mosquito larvicidal activity of essential oils from leaves of different Cinnamomum osmophloeum provenances. J Agric Food Chem 52:4395–4400

    Article  CAS  PubMed  Google Scholar 

  • Cheng BH, Lin CY, Yeh TF, Cheng SS, Chang ST (2012) Potential source of S-(+)-Linalool from Cinnamomum osmophloeum ct. linalool leaf: essential oil profile and enantiomeric purity. J Agric Food Chem 60:7623–7628

    Article  CAS  PubMed  Google Scholar 

  • Chu FH, Kuo PM, Chen YR, Wang SY (2009) Cloning and characterization of α-pinene synthase from Chamaecyparis formosensis Matsum. Holzforschung 63:69–74

    Article  CAS  Google Scholar 

  • Chua MT, Tung YT, Chang ST (2008) Antioxidant activities of ethanolic extracts from the twigs of Cinnamomum osmophloeum. Bioresour Technol 99:1918–1925

    Article  CAS  PubMed  Google Scholar 

  • Cline M, Taylor JE, Flores J, Bracken S, McCall S, Ceremuga TE (2008) Investigation of the anxiolytic effects of linalool, a lavender extract, in the male Sprague-Dawley rat. AANA J 76:47–52

    PubMed  Google Scholar 

  • Connolly JD, Hill RAH (1991) Dictionary of terpenoids. Chapman and Hall/CRC, London

    Book  Google Scholar 

  • Crowell AL, Williams DC, Davis EM, Wildung MR, Croteau R (2002) Molecular cloning and characterization of a new linalool synthase. Arch Biochem Biophys 405:112–121

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) Chloro P, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  CAS  PubMed  Google Scholar 

  • Falara V, Akhtar TA, Nguyen TTH, Spyropoulou EA, Bleeker PM, Schauvinhold I, Matsuba Y, Bonini ME, Schilmiller AL, Last RL, Schuurink RC, Pichersky E (2011) The tomato terpene synthase gene family. Plant Physiol 157:770–789

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Höferl M, Krist S, Buchbauer G (2006) Chirality influences the effects of linalool on physiological parameters of stress. Planta Med 72:1188–1192

    Article  PubMed  Google Scholar 

  • Honda K, Omura H, Hayashi N (1998) Identification of floral volitiles from Ligustrum japonicum that stimulate flower-visiting by cabbage butterfly, Pieris rapae. J Chem Ecol 24:2167–2180

    Article  CAS  Google Scholar 

  • Hsu KH, Huang WK, Lin YL, Chang ST, Chu FH (2012) A genetic marker of 4-coumarate: coenzyme A ligase gene in the cinnamaldehyde-chemotype Cinnamomum osmophloeum. Holzforschung 66:897–904

    Article  CAS  Google Scholar 

  • Hu TW, Lin YT, Ho CK (1985) Natural variation of chemical components of the leaf oil of Cinnamomum osmophloeum Kaneh. Bull Taiwan For Res Inst Eng 78:296–313

    Google Scholar 

  • Hyatt DC, Youn B, Zhao Y, Santhamma B, Coates RM, Croteau RB, Kang C (2007) Structure of limonene synthase, a simple model for terpenoid cyclase catalysis. Proc Natl Acad Sci U S A 104:5360–5365

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jayaprakasha GK, Jagan Mohan Rao L, Sakariah KK (2003) Volatile constituents from Cinnamomum zeylanicum fruit stalks and their antioxidant activities. J Agric Food Chem 51:4344–4348

    Article  CAS  PubMed  Google Scholar 

  • Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675

    Article  CAS  PubMed  Google Scholar 

  • Kiefer F, Arnold K, Künzli M, Bordoli L, Schwede T (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res 37:D387–D392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Knudsen JT, Tollsten L, Bergström G (1993) Floral scents—a checklist of volatile compound by head-space techniques. Phytochemistry 33:253–280

    Article  CAS  Google Scholar 

  • Köksal M, Jin Y, Coates RM, Croteau R, Christianson DW (2011) Taxadiene synthase structure and evolution of modular architecture in terpene biosynthesis. Nature 469:116–120

    Article  PubMed Central  PubMed  Google Scholar 

  • Kumeta Y, Ito M (2010) Characterization of delta-guaiene synthases from cultured cells of Aquilaria, responsible for the formation of the sesquiterpenes in agarwood. Plant Physiol 154:1998–2007

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kuroda K, Inoue N, Ito Y, Kubota K, Sugimoto A, Kakuda T, Fushiki T (2005) Sedative effects of the jasmine tea odor and (R)-(–)-linalool, one of its major odor components, on autonomic nerve activity and mood states. Eur J Appl Physiol 95:107–114

    Article  CAS  PubMed  Google Scholar 

  • Landmann C, Fink B, Festner M, Dregus M, Engel K-H, Schwab W (2007) Cloning and functional characterization of three terpene synthases from lavender (Lavandula angustifolia). Arch Biochem Biophys 465:417–429

    Article  CAS  PubMed  Google Scholar 

  • Lee MJ, Rao YK, Chen K, Lee YC, Tzeng YM (2009) Effect of flavonol glycosides from Cinnamomum osmophloeum leaves on adiponectin secretion and phosphorylation of insulin receptor-β in 3T3-L1 adipocytes. J Ethnopharmacol 126:79–85

    Article  CAS  PubMed  Google Scholar 

  • Liu YC, Lu FY, Ou CH (1998) Trees of Taiwan. College of Agriculture, National Chung-Hsing University, Taichung, Taiwan

  • Lu FY, Ou CH, Chen YC, Chi YS, Lu KC (2000) Tree of Taiwan I. National Chung-Hsing University Press, Taichung

    Google Scholar 

  • Lücker J, Bouwmeester HJ, Schwab W, Blaas J, van der Plas LHW, Verhoeven HA (2001) Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-β-d-glucopyranoside. Plant J 27:315–324

    Article  PubMed  Google Scholar 

  • Ma D, Pu G, Lei C, Ma L, Wang H, Guo Y, Chen J, Du Z, Wang H, Li G, Ye H, Liu B (2009) Isolation and characterization of AaWRKY1, an Artemisia annua transcription factor that regulates the amorpha-4,11-diene synthase gene, a key gene of artemisinin biosynthesis. Plant Cell Physiol 50:2146–2161

    Article  CAS  PubMed  Google Scholar 

  • Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–1653

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O, Lund ST, Bohlmann J (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10:226

    Article  PubMed Central  PubMed  Google Scholar 

  • Nagegowda DA, Gutensohn M, Wilkerson CG, Dudareva N (2008) Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers. Plant J 55:224–239

    Article  CAS  PubMed  Google Scholar 

  • Nakamura A, Fujiwara S, Matsumoto I, Abe K (2009) Stress repression in restrained rats by (R)-(–)-linalool inhalation and gene expression profiling of their whole blood cells. J Agric Food Chem 57:5480–5485

    Article  CAS  PubMed  Google Scholar 

  • Oldfield E, Lin FY (2012) Terpene biosynthesis: modularity rules. Angew Chem Int Ed 51:1124–1137

    Article  CAS  Google Scholar 

  • Olesen JM, Knudsent JT (1994) Scent profiles of flower colour morphs of Corydak cava (Fumariaceae) in relation to foraging behaviour of bumblebee queens (Bombus terrestris). Biochem Syst Ecol 22:231–237

    Article  CAS  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    Article  CAS  PubMed  Google Scholar 

  • Pham-Delegue M, Etievant P, Guichard E, Marilleau R, Douault PH, Chauffaille J, Masson C (1990) Chemicals involved in honeybee–sunflower relationship. J Chem Ecol 16:3053–3065

    Article  CAS  PubMed  Google Scholar 

  • Schwab W (2001) Mechanism of monoterpene cyclization: stereochemical aspects of the transformation of noncyclizable substrate analogs by recombinant (−)-limonene synthase, (+)-bornyl diphosphate synthase, and (−)-pinene synthase. Arch Biochem Biophys 392:123–136

    Article  CAS  PubMed  Google Scholar 

  • Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590

    Article  CAS  PubMed  Google Scholar 

  • Starks CM, Back K, Chappell J, Noel JP (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277:1815–1820

    Article  CAS  PubMed  Google Scholar 

  • Sugawara Y, Hara C, Aoki T, Sugimoto N, Masujima T (2000) Odor distinctiveness between enantiomers of linalool: difference in perception and responses elicited by sensory test and forehead surface potential wave measurement. Chem Senses 25:77–84

    Article  CAS  PubMed  Google Scholar 

  • Suttipanta N, Pattanaik S, Kulshrestha M, Patra B, Singh SK, Yuan L (2011) The transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol 157:2081–2093

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Thien LB, Bernhardt P, Gibbs GW, Pellmyr O, Bergström G, Groth I, McPherson G (1985) The pollination of Zygogynum (winteraceae) by a moth, Sabatinca (micropterigidae): an ancient association? Science 227:540–543

    Article  CAS  PubMed  Google Scholar 

  • Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304

    Article  CAS  PubMed  Google Scholar 

  • Toh HC, Wang SY, Chang ST, Chu FH (2013) Molecular cloning and characterization of flavonol synthase in Acacia confusa. Tree Genet Genomes 9:85–92

    Article  Google Scholar 

  • Tung YT, Chua MT, Wang SY, Chang ST (2008) Anti-inflammation activities of essential oil and its constituents from indigenous cinnamon (Cinnamomum osmophloeum) twigs. Bioresour Technol 99:3908–3913

    Article  CAS  PubMed  Google Scholar 

  • van Schie CCN, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64:251–263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang SY, Chen PF, Chang ST (2005) Antifungal activities of essential oils and their constituents from indigenous cinnamon (Cinnamomum osmophloeum) leaves against wood decay fungi. Bioresour Technol 96:813–818

    Article  CAS  PubMed  Google Scholar 

  • Wang SY, Yang CW, Liao JW, Zhen WW, Chu FH, Chang ST (2008) Essential oil from leaves of Cinnamomum osmophloeum acts as a xanthine oxidase inhibitor and reduces the serum uric acid levels in oxonate-induced mice. Phytomedicine 15:940–945

    Article  CAS  PubMed  Google Scholar 

  • Whittington DA, Wise ML, Urbansky M, Coates RM, Croteau RB, Christianson DW (2002) Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase. Proc Natl Acad Sci U S A 99:15375–15380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu S, Schalk M, Clark A, Miles RB, Coates R, Chappell J (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat Biotechnol 24:1441–1447

    Article  CAS  PubMed  Google Scholar 

  • Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-δ-cadinene synthase-A. Plant Physiol 135:507–515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yin S, Mei L, Newman J, Back K, Chappel J (1997) Regulation of sesquiterpene cyclase gene expression. Plant Physiol 115:437–451

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yuan JS, Köllner TG, Wiggins G, Grant J, Degenhardt J, Chen F (2008) Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J 55:491–503

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Council of Agriculture Executive Yuan of Taiwan for financial support.

Author information

Authors and Affiliations

  1. School of Forestry and Resource Conservation, National Taiwan University, No.1, Sec. 4, Roosevelt Rd., Da’an Dist, Taipei City, 106, Taiwan

    Yan-Liang Lin, Yi-Ru Lee, Wen-Ke Huang, Shang-Tzen Chang & Fang-Hua Chu

Authors
  1. Yan-Liang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yi-Ru Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wen-Ke Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shang-Tzen Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fang-Hua Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fang-Hua Chu.

Additional information

Communicated by D. Neale

Data archiving statement

The sequences of CoLIS-B1 (GenBank accession number: JX133145), CoLIS-D4 (JX028230), CoLIS-E1 (JX133146), CoLIS-HS (JX028231), CoLIS-L (JX133147), CoLIS-LL (JX028232), CoLIS-M21 (JX133148), CoLIS-S1 (JX133149), and CoLIS-T1 (JX028233) have submitted to NCBI GenBank database.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 40 kb)

Figure S1

(JPEG 393 kb)

Figure S2

(JPEG 119 kb)

Figure S3

(JPEG 285 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, YL., Lee, YR., Huang, WK. et al. Characterization of S-(+)-linalool synthase from several provenances of Cinnamomum osmophloeum . Tree Genetics & Genomes 10, 75–86 (2014). https://doi.org/10.1007/s11295-013-0665-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-013-0665-1

Keywords

Search

Navigation