Advertisement

Cellular and Molecular Life Sciences

, Volume 66, Issue 18, pp 3043–3052 | Cite as

Diversity, regulation, and genetic manipulation of plant mono- and sesquiterpenoid biosynthesis

  • Fengnian Yu
  • Ryutaro Utsumi
Review
First Online:
Received:
Revised:
Accepted:

Abstract

Among plant secondary metabolites, terpenoids are the most abundant and structurally diverse group. In addition to their important roles in pollinator attraction and direct and indirect plant defense, terpenoids are also commercially valuable due to their broad applications in the cosmetic, food, and pharmaceutical industries. Because of their functional versatility and wide distribution, great efforts have been made to decipher terpenoid biosynthetic pathways, to investigate the molecular mechanism determining their structural diversity, and to understand their biosynthetic regulation. Recent progress on the manipulation of terpenoid production in transgenic plants not only holds considerable promise for improving various plant traits and crop protection but also increases our understanding of the significance of terpenoid metabolites in mediating plant-environment interactions.

Keywords

Plant terpenoid biosynthesis Structural diversity Regulation Genetic manipulation Transgenic plants 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We thank all the authors listed in the references for their valuable contribution in this field. This work was supported in part by the Research and Development Program for New Bio-industry Initiatives (2006–2010) from the Bio-oriented Technology Research Advancement Institution (BRAIN), by the “Academic Frontier” Project for Private Universities: matching fund subsidy from the Ministry of Education, Culture, Sports, Science and Technology (2004–2008) and by the Sasagawa Scientific Research Grant from the Japan Science Society.

References

  1. 1.
    Buckingham J (2004) Dictionary of natural products, web version 2004. Chapman & Hall, LondonGoogle Scholar
  2. 2.
    Chappell J (1995) The biochemistry and molecular biology of isoprenoid metabolism. Plant Physiol 107:1–6PubMedGoogle Scholar
  3. 3.
    Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902PubMedCrossRefGoogle Scholar
  4. 4.
    Facchini PJ, Chappell J (1992) Gene family for an elicitor-induced sesquiterpene cyclase in tobacco. Proc Natl Acad Sci USA 89:11088–11092PubMedCrossRefGoogle Scholar
  5. 5.
    Dobson HEM (1994) Floral volatiles in insect biology. In: Bernays EA (ed) Insect-plant interactions, vol 5. CRC Press, Boca Raton, pp 47–81Google Scholar
  6. 6.
    Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–633PubMedCrossRefGoogle Scholar
  7. 7.
    Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243PubMedCrossRefGoogle Scholar
  8. 8.
    Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280CrossRefGoogle Scholar
  9. 9.
    Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414PubMedCrossRefGoogle Scholar
  10. 10.
    Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331PubMedCrossRefGoogle Scholar
  11. 11.
    Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249CrossRefGoogle Scholar
  12. 12.
    Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  13. 13.
    Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean. Nature 406:512–515PubMedCrossRefGoogle Scholar
  14. 14.
    Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737PubMedCrossRefGoogle Scholar
  15. 15.
    Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42:757–771PubMedCrossRefGoogle Scholar
  16. 16.
    Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004) The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16:1115–1131PubMedCrossRefGoogle Scholar
  17. 17.
    Berry R, Wagner CJ, Moshonas MG (1967) Flavor studies of nootkatone in grapefruit juice. J Food Sci 32:75–78CrossRefGoogle Scholar
  18. 18.
    Klayman DL (1985) Qinghaosu (artemisinin): an antimalarial drug from China. Science 228:1049–1055PubMedCrossRefGoogle Scholar
  19. 19.
    Ozaki Y, Kawahara N, Harada M (1991) Anti-inflammatory effect of Zingiber cassumunar Roxb and its active principles. Chem Pharm Bull 39:2353–2356PubMedGoogle Scholar
  20. 20.
    Murakami A, Tanaka T, Lee JY, Surh YJ, Kim HW, Kawabata K, Nakamura Y, Jiwajinda S, Ohigashi H (2004) Zerumbone suppresses skin tumor initiation and promotion stages in mice: involvement of induction of anti-oxidative and phase II drug metabolizing enzymes and inhibition of NF-kB-mediated cyclooxygenase-2 expression. Int J Cancer 110:481–490PubMedCrossRefGoogle Scholar
  21. 21.
    Xian MJ, Ito K, Nakazato T, Shimizu T, Chen CK, Yamato K, Murakami A, Ohigashi H, Ikeda Y, Kizaki M (2007) Zerumbone, a bioactive sesquiterpene, induces G2/M cell cycle arrest and apoptosis in leukemia cells via a Fas- and mitochondria-mediated pathway. Cancer Sci 98:118–126PubMedCrossRefGoogle Scholar
  22. 22.
    Yu FN, Okamoto S, Nakasone K, Adachi K, Matsuda S, Harada H, Misawa N, Utsumi R (2008) Molecular cloning and functional characterization of α-humulene synthase, a possible key enzyme of zermbone biosynthesis in shampoo ginger (Zingiber zerumbet Smith). Planta 227:1291–1299PubMedCrossRefGoogle Scholar
  23. 23.
    McGarvey D, Croteau R (1995) Terpenoid metabolism. Plant Cell 7:1015–1026PubMedCrossRefGoogle Scholar
  24. 24.
    Sallaud C, Rontein D, Onillon S, Jabes F, Duffe P, Giacalone C, Thoraval S, Escoffier C, Herbette G, Leonhardt N, Causse M, Tissier A (2009) A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21:301–317PubMedCrossRefGoogle Scholar
  25. 25.
    Newman JD, Chappell J (1999) Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. Crit Rev Biochem Mol Biol 34:95–106PubMedCrossRefGoogle Scholar
  26. 26.
    Eisenreich W, Schwarz M, Cartayrade A, Arigoni D, Zenk MH, Bacher A (1998) The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem Biol 5:R221–R233PubMedCrossRefGoogle Scholar
  27. 27.
    Lichtenthaler HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65PubMedCrossRefGoogle Scholar
  28. 28.
    McCaskill D, Croteau R (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha × piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta 197:49–56CrossRefGoogle Scholar
  29. 29.
    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 278:26666–26676PubMedCrossRefGoogle Scholar
  30. 30.
    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 100:6866–6871PubMedCrossRefGoogle Scholar
  31. 31.
    Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102:933–938PubMedCrossRefGoogle Scholar
  32. 32.
    Adam KP, Zapp J (1999) Biosynthesis of the isoprene units of chamomile sesquiterpenes. Phytochemistry 48:953–959CrossRefGoogle Scholar
  33. 33.
    Adam KP, Thiel R, Zapp J (1999) Incorporation of 1-[1–13C]deoxy-d-xylulose in chamomile sesquiterpenes. Arch Biochem Biophys 369:127–132PubMedCrossRefGoogle Scholar
  34. 34.
    Towler MJ, Weathers PJ (2007) Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways. Plant Cell Rep 26:2129–2136PubMedCrossRefGoogle Scholar
  35. 35.
    Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun ZK, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131PubMedCrossRefGoogle Scholar
  36. 36.
    Davidovich-Rikanati R, Lewinsohn E, Bar E, Iijima Y, Pichersky E, Sitrit Y (2008) Overexpression of the lemon basil α-zingiberene synthase gene increases both mono- and sesquiterpene contents in tomato fruit. Plant J 56:228–238PubMedCrossRefGoogle Scholar
  37. 37.
    Shen B, Zheng Z, Dooner HK (2000) A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. Proc Natl Acad Sci USA 97:14807–14812PubMedCrossRefGoogle Scholar
  38. 38.
    Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133PubMedCrossRefGoogle Scholar
  39. 39.
    Steele CL, Crock J, Bohlmann J, Croteau R (1998) Sesquiterpene synthases from grand fir (Abies grandis): comparison of constitutive and wound-induced activities, and cDNA isolation, characterization and bacterial expression of delta-selinene synthase and gamma-humulene synthase. J Biol Chem 273:2078–2089PubMedCrossRefGoogle Scholar
  40. 40.
    Trapp S, Croteau R (2001) Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 158:811–832PubMedGoogle Scholar
  41. 41.
    Starks CM, Back KW, Chappell J, Noel JP (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277:1815–1820PubMedCrossRefGoogle Scholar
  42. 42.
    Whittington DA, Wise ML, Urbansky M, Coates RM, Croteau R, Christianson DW (2002) Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase. Proc Natl Acad Sci USA 99:15375–15380PubMedCrossRefGoogle Scholar
  43. 43.
    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 USA 104:5360–5365PubMedCrossRefGoogle Scholar
  44. 44.
    Back KW, Chappell J (1996) Identifying functional domains within terpene cyclases using a domain-swapping strategy. Proc Natl Acad Sci USA 93:6841–6845PubMedCrossRefGoogle Scholar
  45. 45.
    Greenhagen BT, O’Maille PE, Noel JP, Chappell J (2006) Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases. Proc Natl Acad Sci USA 103:9826–9831PubMedCrossRefGoogle Scholar
  46. 46.
    Köllner T, O’Maille PE, Gatto N, Boland W, Gershenzon J, Degenhardt J (2006) Two pockets in the active site of maize sesquiterpene synthase TPS4 carry out sequential parts of the reaction scheme resulting in multiple products. Arch Biochem Biophys 448:83–92PubMedCrossRefGoogle Scholar
  47. 47.
    Besser K, Harper A, Welsby N, Schauvinhold I, Slocombe S, Li Y, Dixon RA, Broun P (2009) Divergent regulation of terpenoid metabolism in the trichomes of wild and cultivated tomato species. Plant Physiol 149:499–514PubMedCrossRefGoogle Scholar
  48. 48.
    van der Hoeven RS, Monforte AJ, Breeden D, Tanksley SD, Steffens JC (2000) Genetic control and evolution of sesquiterpene biosynthesis in Lycopersicon esculentum and L. hirsutum. Plant Cell 12:2283–2294CrossRefGoogle Scholar
  49. 49.
    Yoshikuni Y, Ferrin TE, Keasling JD (2006) Designed divergent evolution of enzyme function. Nature 440:1078–1082PubMedCrossRefGoogle Scholar
  50. 50.
    Croteau RB, Davis EM, Ringer KL, Wildung MR (2005) (-)-Menthol biosynthesis and molecular genetics. Naturwissenschaften 92:562–577PubMedCrossRefGoogle Scholar
  51. 51.
    Van Poecke RMP, Posthumus MA, Dicke M (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27:1911–1928PubMedCrossRefGoogle Scholar
  52. 52.
    Rodriguez-Saona C, Crafts-Brandner SJ, Cañas LA (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2539–2550PubMedCrossRefGoogle Scholar
  53. 53.
    Phillips MA, Croteau R (1999) Resin based defenses in conifers. Trends Plant Sci 4:184–190PubMedCrossRefGoogle Scholar
  54. 54.
    Staudt M, Bertin N (1998) Light and temperature dependence of the emission of cyclic and acyclic monoterpenes from holm oak (Quercus ilex L.) leaves. Plant Cell Environ 21:385–395CrossRefGoogle Scholar
  55. 55.
    Llusià J, Peñuelas J (2000) Seasonal patterns of terpene content and emission from seven Mediterranean woody species in field conditions. Am J Bot 87:133–140PubMedCrossRefGoogle Scholar
  56. 56.
    Gouinguene SP, Turlings TC (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307PubMedCrossRefGoogle Scholar
  57. 57.
    Hakola H, Tarvainen V, Bäck J, Ranta H, Bonn B, Rinne J, Kulmala M (2006) Seasonal variation of mono- and sesquiterpene emission rates of Scots pine. Biogeosciences 2:1697–1717Google Scholar
  58. 58.
    Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Fäldt J, Miller B, Bohlmann J (2003) (E)-beta-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell 15:1227–1241PubMedCrossRefGoogle Scholar
  59. 59.
    Roeder S, Hartmann AM, Effmert U, Piechulla B (2007) Regulation of simultaneous synthesis of floral scent terpenoids by the 1,8-cineole synthase of Nicotiana suaveolens. Plant Mol Biol 65:107–124PubMedCrossRefGoogle Scholar
  60. 60.
    Loughrin JH, Hamilton-Kemp TR, Andersen RA, Hildebrand DF (1990) Volatiles from flowers of Nicotiana sylvestris, N. otophora and Malus × domestica: headspace components and day/night changes in their relative concentrations. Phytochemistry 29:2473–2477CrossRefGoogle Scholar
  61. 61.
    Heath RR, Landolt PJ, Dueben B, Lenczewski B (1992) Identification of floral compounds of night-blooming jessamine attractive to cabbage looper moths. Environ Entomol 21:854–859Google Scholar
  62. 62.
    Gershenzon J, Maffei M, Croteau R (1989) Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). Plant Physiol 89:1351–1357PubMedCrossRefGoogle Scholar
  63. 63.
    McCaskill D, Gershenzon J, Croteau R (1992) Morphology and monoterpene biosynthetic capabilities of secretory cell clusters isolated from glandular trichomes of peppermint (Mentha piperita L.). Planta 187:445–454CrossRefGoogle Scholar
  64. 64.
    Banan MW (1936) Vertical resin ducts in the secondary wood of the abietineae. New Phytol 35:11–46CrossRefGoogle Scholar
  65. 65.
    Nagy NE, Franceschi VR, Solheim H, Krekling T, Christiansen E (2000) Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. Am J Bot 87:302–313PubMedCrossRefGoogle Scholar
  66. 66.
    McKay SA, Hunter WL, Godard KA, Wang SX, Martin DM, Bohlmann J, Plant AL (2003) Insect attack and wounding induce traumatic resin duct development and gene expression of (-)-pinene synthase in Sitka spruce. Plant Physiol 133:368–378PubMedCrossRefGoogle Scholar
  67. 67.
    Degenhardt DC, Lincoln DE (2006) Volatile emissions from an odorous plant in response to herbivory and methyl jasmonate exposure. J Chem Ecol 32:1573–1561CrossRefGoogle Scholar
  68. 68.
    Loughrin JH, Manukian A, Heath RR, Turlings TC, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plant. Proc Natl Acad Sci USA 91:11836–11840PubMedCrossRefGoogle Scholar
  69. 69.
    Gershenzon J, McConkey ME, Croteau R (2000) Regulation of monoterpene accumulation in leaves of peppermint. Plant Physiol 122:205–214PubMedCrossRefGoogle Scholar
  70. 70.
    Sharon-Asa L, Shalit M, Frydman A, Bar E, Holland D, Or E, Lavi U, Lewinsohn E, Eyal Y (2003) Citrus fruit flavor and aroma biosynthesis: isolation, functional characterization, and developmental regulation of Cstps1, a key gene in the production of the sesquiterpene aroma compound valencene. Plant J 36:664–674PubMedCrossRefGoogle Scholar
  71. 71.
    Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129:1003–1018PubMedCrossRefGoogle Scholar
  72. 72.
    Schnee C, Köllner TG, Gershenzon J, Degenhardt J (2002) The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-β-farnesene, (E)-nerolidol, and (E, E)-farnesol after herbivore damage. Plant Physiol 130:2049–2060PubMedCrossRefGoogle Scholar
  73. 73.
    Arimura G, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa × deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (−)-germacrene D synthase, PtdTPS1. Plant J 37:603–616PubMedCrossRefGoogle Scholar
  74. 74.
    Miller B, Madilao LL, Ralph S, Bohlmann J (2005) Insect-induced conifer defense: white pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol 137:369–382PubMedCrossRefGoogle Scholar
  75. 75.
    Cheng AX, Xiang CY, Li JX, Yang CQ, Hu WL, Wang LJ, Lou YG, Chen XY (2007) The rice (E)-b-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry 68:1632–1641PubMedCrossRefGoogle Scholar
  76. 76.
    Opitz S, Kunert G, Gershenzon J (2008) Increased terpenoid accumulation in cotton (Gossypium hirsutum) foliage is a general wound response. J Chem Ecol 34:508–522PubMedCrossRefGoogle Scholar
  77. 77.
    Threlfall DR, Whitehead IM (1988) Coordinated inhibition of squalene synthetase and induction of enzymes of sesquiterpenoid phytoalexin biosynthesis in cultures of Nicotiana tabacum. Phytochemistry 27:2567–2580CrossRefGoogle Scholar
  78. 78.
    Vögeli U, Chappell J (1988) Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol 88:1291–1296PubMedCrossRefGoogle Scholar
  79. 79.
    Brindle PA, Kuhn P, Tbxelfall DR (1988) Biosynthesis and metabolism of sesquiterpenoid phytoalexins and triterpenoids in potato cell suspension cultures. Phytochemistry 27:133–150CrossRefGoogle Scholar
  80. 80.
    Tjamos EC, Kuc JA (1982) Inhibition of steroid glyoalkaloid accumulation by eicosapentaenoic and arachidonic acid in potato. Science 217:542–544PubMedCrossRefGoogle Scholar
  81. 81.
    Mahmoud SS, Croteau R (2002) Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci 7:366–373PubMedCrossRefGoogle Scholar
  82. 82.
    Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602PubMedCrossRefGoogle Scholar
  83. 83.
    Aharoni A, Jongsma MA, Kim TY, Ri MB, Giri AP, Verstappen FWA, Schwab W, Bouwmeester HJ (2006) Metabolic engineering of terpenoid biosynthesis in plants. Phytochem Rev 5:49–58CrossRefGoogle Scholar
  84. 84.
    Pichersky E, Dudareva N (2007) Scent engineering: toward the goal of controlling how flowers smell. Trends Biotechnol 25:105–110PubMedCrossRefGoogle Scholar
  85. 85.
    Dudareva N, Pichersky E (2008) Metabolic engineering of plant volatiles. Curr Opin Biotechnol 19:181–189PubMedCrossRefGoogle Scholar
  86. 86.
    Mahmoud SS, Croteau R (2001) Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc Natl Acad Sci USA 98:8915–8920PubMedCrossRefGoogle Scholar
  87. 87.
    Chen D, Ye H, Li G (2000) Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci 155:179–185PubMedCrossRefGoogle Scholar
  88. 88.
    Mahmoud SS, Williams M, Croteau R (2004) Cosuppression of limonene-3-hydroxylase in peppermint promotes accumulation of limonene in the essential oil. Phytochemistry 65:547–554PubMedCrossRefGoogle Scholar
  89. 89.
    Lücker J, Schwab W, Franssen MC, Van Der Plas LH, Bouwmeester HJ, Verhoeven HA (2004) Metabolic engineering of monoterpene biosynthesis: two-step production of (+)-trans-isopiperitenol by tobacco. Plant J 39:135–145PubMedCrossRefGoogle Scholar
  90. 90.
    Lücker J, Schwab W, Hautum BV, van der Plas LHW, Bouwmeester HJ, Verhoeven HA (2004) Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon. Plant Physiol 134:510–519PubMedCrossRefGoogle Scholar
  91. 91.
    Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor K, Nam KH, Amar O, Lastochkin E, Larkov O, Ravid U, Hiatt W, Gepstein S, Pichersky E (2001) Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol 127:1256–1265PubMedCrossRefGoogle Scholar
  92. 92.
    Davidovich-Rikanati R, Sitrit Y, Tadmor Y, Iijima Y, Bilenko N, Bar E, Carmona B, Fallik E, Dudai N, Simon JE, Pichersky E, Lewinsohn E (2007) Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway. Nat Biotechnol 25:899–901PubMedCrossRefGoogle Scholar
  93. 93.
    Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FWA, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884PubMedCrossRefGoogle Scholar
  94. 94.
    Schnee C, Kollner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J (2006) The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 103:1129–1134PubMedCrossRefGoogle Scholar
  95. 95.
    Kappers IF, Aharoni A, Van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072PubMedCrossRefGoogle Scholar
  96. 96.
    Wu SQ, 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 24:1441–1447PubMedCrossRefGoogle Scholar
  97. 97.
    Lücker J, Bouwmeester HJ, Schwab W, Blaas J, van der Plas LH, 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 27:315–324PubMedCrossRefGoogle Scholar
  98. 98.
    Lavy M, Zuker A, Lewinsohn E, Larkov O, Ravid U, Vainstein A, Weiss D (2002) Linalool and linalool oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene. Mol Breed 9:103–111CrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  1. 1.Department of Bioscience, Graduate School of AgricultureKinki UniversityNakamachiJapan

Personalised recommendations

Cite article

Buy options