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Planta

, Volume 238, Issue 5, pp 983–989 | Cite as

Cloning of a sesquiterpene synthase from Lavandula x intermedia glandular trichomes

  • Lukman S. Sarker
  • Zerihun A. Demissie
  • Soheil S. Mahmoud
Short Communication

Abstract

The essential oil (EO) of Lavandula is dominated by monoterpenes, but can also contain small amounts of sesquiterpenes, depending on species and environmental conditions. For example, the sesquiterpene 9-epi-caryophyllene can make up to 8 % of the EO in a few species, including those commercially propagated for EO production. Here, we report the cloning and functional characterization of 9-epi-caryophyllene synthase (LiCPS) from the glandular trichomes of Lavandula x intermedia, cv. Grosso. The 1,617 bp open reading frame of LiCPS, which did not encode a transit peptide, was expressed in Escherichia coli and the recombinant protein purified by Ni–NTA agarose affinity chromatography. The ca. 60 kDa recombinant protein specifically converted farnesyl diphosphate to 9-epi-caryophyllene. LiCPS also produced a few monoterpenes when assayed with the monoterpene precursor geranyl diphosphate (GPP), but—unlike most monoterpene synthases—was not able to derive detectable amounts of any products from the cis isomer of GPP, neryl diphosphate. The LiCPS transcripts accumulated in developing L. x intermedia flowers and were highly enriched in glandular trichomes, but were not detected in leaves suggesting that the transcriptional expression of this gene is spatially and developmentally regulated.

Keywords

Isoprenoid Terpenoid Sesquiterpene Caryophyllene Essential oil Glandular trichome 

Notes

Acknowledgments

This work was supported through grants or in-kind contributions to Soheil Mahmoud by UBC Okanagan, Natural Sciences and Engineering Research Council of Canada, Canada Foundation for Innovation, Investment Agriculture Foundation of British Columbia, NRC Plant Biotechnology Institute through the NAPGEN program, and Genome British Columbia. We would also like to thank Lauren Erland for her help with manuscript editing.

References

  1. Adam K, Thiel R, Zapp J (1999) Incorporation of 1-[1-C-13]deoxy-d-xylulose in chamomile sesquiterpenes. Arch Biochem Biophys 369(1):127–132PubMedCrossRefGoogle Scholar
  2. Arigoni D, Sagner S, Latzel C, Eisenreich W, Bacher A, Zenk M (1997) Terpenoid biosynthesis from 1-deoxy-d-xylulose in higher plants by intramolecular skeletal rearrangement. Proc Natl Acad Sci USA 94(20):10600–10605PubMedCrossRefGoogle Scholar
  3. Bick JA, Lange BM (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415(2):146–154PubMedCrossRefGoogle Scholar
  4. Cai Y, Jia JW, Crock J, Lin ZX, Chen XY, Croteau R (2002) A cDNA clone for beta-caryophyllene synthase from Artemisia annua. Phytochemistry 61(5):523–529PubMedCrossRefGoogle Scholar
  5. Chappell J, Wolf F, Proulx J, Cuellar R, Saunders C (1995) Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme-a reductase a rate-limiting step for isoprenoid biosynthesis in plants? Plant Physiol 109(4):1337–1343PubMedGoogle Scholar
  6. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66(1):212–229PubMedCrossRefGoogle Scholar
  7. Cheng A, Lou Y, Mao Y, Lu S, Wang L, Chen X (2007) Plant terpenoids: biosynthesis and ecological functions. J Integr Plant Biol 49(2):179–186CrossRefGoogle Scholar
  8. Demissie ZA, Sarker LS, Mahmoud SS (2011) Cloning and functional characterization of β-phellandrene synthase from Lavandula angustifolia. Planta 233(4):685–696PubMedCrossRefGoogle Scholar
  9. Demissie ZA, Cella MA, Sarker LS, Thompson TJ, Rheault MR, Mahmoud SS (2012) Cloning, functional characterization and genomic organization of 1,8-cineole synthases from Lavandula. Plant Mol Biol 79(4–5):393–411PubMedCrossRefGoogle Scholar
  10. Demissie ZA, Erland LA, Rheault MR, Mahmoud SS (2013) The biosynthetic origin of irregular monoterpenes in Lavandula: isolation and biochemical characterization of a novel cis-prenyl diphosphate synthase gene, lavandulyl diphosphate synthase. J Biol Chem 288(9):6333–6341PubMedCrossRefGoogle Scholar
  11. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J, Guindon S, Lefort V, Lescot M, Claverie J, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469PubMedCrossRefGoogle Scholar
  12. Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Kagan IA, Grosdemange-Billiard C, Rohmer M, Bach TJ (2003) Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in Tobacco Bright Yellow-2 cells. J Biol Chem 278(29):26666–726676PubMedCrossRefGoogle Scholar
  13. Iijima Y, Davidovich-Rikanati R, Fridman E, Gang DR, Bar E, Lewinsohn E, Pichersky E (2004a) 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. Plant Physiol 136(3):3724–3736PubMedCrossRefGoogle Scholar
  14. Iijima Y, Gang DR, Fridman E, Lewinsohn E, Pichersky E (2004b) Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiol 134(1):370–379PubMedCrossRefGoogle Scholar
  15. Koellner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J (2008) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20(2):482–494CrossRefGoogle Scholar
  16. Kollner TG, Schnee C, Gershenzon J, Degenhardt J (2004) The variability of sesquiterpenes cultivars is controlled by allelic emitted from two Zea mays variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16(5):1115–1131PubMedCrossRefGoogle Scholar
  17. Kubo I, Chaudhuri S, Kubo Y, Sanchez Y, Ogura T, Saito T, Ishikawa H, Haraguchi H (1996) Cytotoxic and antioxidative sesquiterpenoids from Heterotheca inuloides. Planta Med 62(5):427–430PubMedCrossRefGoogle Scholar
  18. Landmann C, Fink B, Festner M, Dregus M, Engel K, Schwab W (2007) Cloning and functional characterization of three terpene synthases from lavender (Lavandula angustifolia). Arch Biochem Biophys 465(2):417–429PubMedCrossRefGoogle Scholar
  19. Lane A, Boecklemann A, Woronuk GN, Sarker L, Mahmoud SS (2010) A genomics resource for investigating regulation of essential oil production in Lavandula angustifolia. Planta 231(4):835–845PubMedCrossRefGoogle Scholar
  20. Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange BM (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100(11):6866–6871PubMedCrossRefGoogle Scholar
  21. Lis-Balchin M (2002) Chemical composition of essential oils from different species, hybrids and cultivars of Lavandula. In: Lis-Balchin M (ed) Lavender: the genus Lavandula. Taylor & Francis, London, pp 251–262Google Scholar
  22. Li-Weber M, Giaisi M, Treiber M, Krammer P (2002) The anti-inflammatory sesquiterpene lactone parthenolide suppresses IL-4 gene expression in peripheral blood T cells. Eur J Immunol 32(12):3587–3597PubMedCrossRefGoogle Scholar
  23. Mahmoud SS, Croteau RB (2002) Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci 7(8):366–373PubMedCrossRefGoogle Scholar
  24. Mahmoud S, Croteau R (2003) Menthofuran regulates essential oil biosynthesis in peppermint by controlling a downstream monoterpene reductase. Proc Natl Acad Sci USA 100(24):14481–14486PubMedCrossRefGoogle Scholar
  25. Majdi M, Liu Q, Karimzadeh G, Malboobi MA, Beekwilder J, Cankar K, de Vos R, Todorovic S, Simonovic A, Bouwmeester H (2011) Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.). Phytochemistry 72(14–15):1739–1750PubMedCrossRefGoogle Scholar
  26. McGarvey D, Croteau R (1995) Terpenoid metabolism. Plant Cell 7:1015–1026PubMedGoogle Scholar
  27. Okada K (2011) The biosynthesis of isoprenoids and the mechanisms regulating it in plants. Biosci Biotechnol Biochem 75(7):1219–1225PubMedCrossRefGoogle Scholar
  28. Phillips MA, Leon P, Boronat A, Rodriguez-Concepcion M (2008) The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci 13(12):619–623PubMedCrossRefGoogle Scholar
  29. Sarker LS (2013) Cloning of Lavandula essential oil biosynthetic genes. Dissertation or thesis, University of British ColumbiaGoogle Scholar
  30. Trusheva B, Todorov I, Ninova M, Najdenski H, Daneshmand A, Bankova V (2010) Antibacterial mono- and sesquiterpene esters of benzoic acids from Iranian propolis. Chem Cent J. doi: 10.1186/1752-153X-4-8 PubMedGoogle Scholar
  31. Ulubelen A, Topcu G, Eris C, Sonmez U, Kartal M, Kurucu S, Bozokjohansson C (1994) Terpenoids from Salvia sclarea. Phytochemistry 36(4):971–974PubMedCrossRefGoogle Scholar
  32. Upson T, Andrews S, Harriott G, King C, Langhorne J (2004) The genus Lavandula. Timber Press, Portland, pp 78–85Google Scholar
  33. Zheng G, Kenney P, Lam L (1992) Sesquiterpenes from clove (Eugenia caryophyllata) as potential anticarcinogenic agents. J Nat Prod 55(7):999–1003PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Lukman S. Sarker
    • 1
  • Zerihun A. Demissie
    • 1
  • Soheil S. Mahmoud
    • 1
  1. 1.University of British ColumbiaKelownaCanada

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