, Volume 246, Issue 5, pp 803–816 | Cite as

Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering

  • Farhat Abbas
  • Yanguo Ke
  • Rangcai YuEmail author
  • Yuechong Yue
  • Sikandar Amanullah
  • Muhammad Muzammil Jahangir
  • Yanping FanEmail author


Main conclusion

Terpenoids play several physiological and ecological functions in plant life through direct and indirect plant defenses and also in human society because of their enormous applications in the pharmaceutical, food and cosmetics industries. Through the aid of genetic engineering its role can by magnified to broad spectrum by improving genetic ability of crop plants, enhancing the aroma quality of fruits and flowers and the production of pharmaceutical terpenoids contents in medicinal plants.

Terpenoids are structurally diverse and the most abundant plant secondary metabolites, playing an important role in plant life through direct and indirect plant defenses, by attracting pollinators and through different interactions between the plants and their environment. Terpenoids are also significant because of their enormous applications in the pharmaceutical, food and cosmetics industries. Due to their broad distribution and functional versatility, efforts are being made to decode the biosynthetic pathways and comprehend the regulatory mechanisms of terpenoids. This review summarizes the recent advances in biosynthetic pathways, including the spatiotemporal, transcriptional and post-transcriptional regulatory mechanisms. Moreover, we discuss the multiple functions of the terpene synthase genes (TPS), their interaction with the surrounding environment and the use of genetic engineering for terpenoid production in model plants. Here, we also provide an overview of the significance of terpenoid metabolic engineering in crop protection, plant reproduction and plant metabolic engineering approaches for pharmaceutical terpenoids production and future scenarios in agriculture, which call for sustainable production platforms by improving different plant traits.


Volatile terpenoids Multifunction Biosynthesis Plant defense Pollinator attractions Regulation Genetic engineering 



This work was supported in part by the National Natural Science Foundation of China to Yanping Fan (Grant nos. 30972026 and 31370694), a Specialized Research Fund for the Doctoral Program of Higher Education of China to Yanping Fan (Grant no. 20134404110016), and a Specialized Major Project of the Production-Study-Research Collaborative Innovation of Guangzhou Science and Information Bureau to Yanping Fan (Grant no. 156100058). We would like to say thank you to Mr. Yiwei Zhou (College of Forestry and Landscape Architecture), Dr. Umair Ashraf and Dr. Rashid Azad (College of Agriculture) for their help in generating figures.


  1. Abrol DP (2012) Biochemical basis of plant–pollination interaction. In: Pollination biology. Springer, pp 413–458. doi: 10.1007/978-94-007-1942-2_13
  2. Aharoni A, Giri AP, Verstappen FW, 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 16:3110–3131PubMedPubMedCentralCrossRefGoogle Scholar
  3. Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trend Plant Sci 10:594–602CrossRefGoogle Scholar
  4. Aharoni A, Jongsma MA, Kim TY, Ri MB, Giri AP, Verstappen FW, Schwab W, Bouwmeester HJ (2006) Metabolic engineering of terpenoid biosynthesis in plants. Phytochem Rev 5:49–58CrossRefGoogle Scholar
  5. Ali JG, Alborn HT, Campos-Herrera R, Kaplan F, Duncan LW, Rodriguez-Saona C, Koppenhöfer AM, Stelinski LL (2012) Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. PLoS One 7:e38146PubMedPubMedCentralCrossRefGoogle Scholar
  6. Arimura G, Ozawa R, Kugimiya S, Takabayashi J, Bohlmann J (2004) Herbivore-induced defense response in a model legume: two-spotted spider mites Tetranychus urticae induce emission of (E)-beta-ocimene and transcript accumulation of (E)-beta-ocimene synthase in Lotus japonicus. Plant Physiol 135:1976–1983PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aros D, Gonzalez V, Allemann RK, Müller CT, Rosati C, Rogers HJ (2012) Volatile emissions of scented Alstroemeria genotypes are dominated by terpenes, and a myrcene synthase gene is highly expressed in scented Alstroemeria flowers. J Exp Bot 63(7):2739–2752PubMedPubMedCentralCrossRefGoogle Scholar
  8. Arpaia S, De Cristofaro A, Guerrieri E, Bossi S, Cellini F, Di Leo GM, Germinara GS, Iodice L, Maffei ME, Petrozza A (2011) Foraging activity of bumblebees (Bombus terrestris L.) on Bt-expressing eggplants. Arthropod Plant Interact 5:255–261CrossRefGoogle Scholar
  9. Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475PubMedCrossRefGoogle Scholar
  10. Baldwin IT, Halitschke R, Paschold A, Von Dahl CC, Preston CA (2006) Volatile signaling in plant–plant interactions: “talking trees” in the genomics era. Science 311:812–815PubMedCrossRefGoogle Scholar
  11. Benedito VA, Modolo LV (2014) Introduction to metabolic genetic engineering for the production of valuable secondary metabolites in in vivo and in vitro plant systems. Recent Patents Biotechnol 8:61–75CrossRefGoogle Scholar
  12. Bergougnoux V, Caissard JC, Jullien F, Magnard JL, Scalliet G, Cock JM, Hugueney P, Baudino S (2007) Both the adaxial and abaxial epidermal layers of the rose petal emit volatile scent compounds. Planta 226:853–866PubMedCrossRefGoogle Scholar
  13. Bertea C, Freije J, Van der Woude H, Verstappen F, Perk L, Marquez V, De Kraker JW, Posthumus M, Jansen B, De Groot A (2005) Identification of intermediates and enzymes involved in the early steps of artemisinin biosynthesis in Artemisia annua. Planta Med 71:40–47PubMedCrossRefGoogle Scholar
  14. Boatright J, Negre F, Chen X, Kish CM, Wood B, Peel G, Orlova I, Gang D, Rhodes D, Dudareva N (2004) Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol 135(4):1993–2011PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bohman B, Phillips RD, Menz MH, Berntsson BW, Flematti GR, Barrow RA, Dixon KW, Peakall R (2014) Discovery of pyrazines as pollinator sex pheromones and orchid semiochemicals: implications for the evolution of sexual deception. New Phytol 203:939–952PubMedCrossRefGoogle Scholar
  16. Brokl M, Fauconnier ML, Benini C, Lognay G, Jardin Pd, Focant JF (2013) Improvement of ylang–ylang essential oil characterization by GC × GC-TOFMS. Molecules 18:1783–1797PubMedCrossRefGoogle Scholar
  17. Buckingham J (2004) Dictionary of natural products web version 2004. Chapman and Hall, London.
  18. Capell T, Christou P (2004) Progress in plant metabolic engineering. Curr Opin Biotechnol 15:148–154PubMedCrossRefGoogle Scholar
  19. Caputi L, Aprea E (2011) Use of terpenoids as natural flavouring compounds in food industry. Recent Patent Food Nutr Agric 3:9–16CrossRefGoogle Scholar
  20. Chen F, Ro DK, Petri J, Gershenzon J, Bohlmann J, Pichersky E, Tholl D (2004) Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiol 135:1956–1966PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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 66:212–229PubMedCrossRefGoogle Scholar
  22. Colquhoun TA, Kim JY, Wedde AE, Levin LA, Schmitt KC, Schuurink RC, Clark DG (2010) PhMYB4 fine-tunes the floral volatile signature of Petunia × hybrida through PhC4H. J Exp Bot 62:1133–1143PubMedPubMedCentralCrossRefGoogle Scholar
  23. Colquhoun TA, Schwieterman ML, Wedde AE, Schimmel BC, Marciniak DM, Verdonk JC, Kim JY, Oh Y, Gális I, Baldwin IT (2011) EOBII controls flower opening by functioning as a general transcriptomic switch. Plant Physiol 156:974–984PubMedPubMedCentralCrossRefGoogle Scholar
  24. Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). Biochem Mol Biol Plants 24:1250–1319Google Scholar
  25. Das A, Lee SH, Hyun TK, Kim SW, Kim JY (2013) Plant volatiles as method of communication. Plant Biotechnol Rep 7:9–26CrossRefGoogle Scholar
  26. 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
  27. Degen T, Dillmann C, Marion-Poll F, Turlings TC (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135:1928–1938PubMedPubMedCentralCrossRefGoogle Scholar
  28. Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochem 70:1621–1637CrossRefGoogle Scholar
  29. Delory BM, Delaplace P, Fauconnier ML, Du Jardin P (2016) Root-emitted volatile organic compounds: can they mediate belowground plant–plant interactions? Plant Soil 402:1–26CrossRefGoogle Scholar
  30. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175PubMedCrossRefGoogle Scholar
  31. Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–634PubMedPubMedCentralCrossRefGoogle Scholar
  32. Dudareva N, Pichersky E (2008) Metabolic engineering of plant volatiles. Curr Opin Biotechnol 19:181–189PubMedCrossRefGoogle Scholar
  33. 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 102:933–938PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32PubMedCrossRefGoogle Scholar
  35. Fan YP, Yu RC, Huang Y, Chen YF (2003) Studies on the essential constituent of Hedychium flavum and H. coronarium. Acta Hortic Sin 30:475 (in Chinese) Google Scholar
  36. Fan YP, Wang X, Yu RC, Yang P (2007) Analysis on the aroma components in several species of Hedychium. Acta Hortic Sin 34:231–234 (in Chinese) Google Scholar
  37. Farré-Armengol G, Filella I, Llusia J, Peñuelas J (2013) Floral volatile organic compounds: between attraction and deterrence of visitors under global change. Persp Plant Ecol Evol Syst 15:56–67CrossRefGoogle Scholar
  38. Farré-Armengol G, Filella I, Llusia J, Peñuelas J (2015) Relationships among floral VOC emissions, floral rewards and visits of pollinators in five plant species of a Mediterranean shrubland. Plant Ecol Evol 148:90–99CrossRefGoogle Scholar
  39. Flügge UI, Gao W (2005) Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol 7:91–97PubMedCrossRefGoogle Scholar
  40. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414PubMedCrossRefGoogle Scholar
  41. Gershenzon J, McConkey ME, Croteau RB (2000) Regulation of monoterpene accumulation in leaves of peppermint. Plant Physiol 122:205–214PubMedPubMedCentralCrossRefGoogle Scholar
  42. Ginglinger JF, Boachon B, Höfer R, Paetz C, Köllner TG, Miesch L, Lugan R, Baltenweck R, Mutterer J, Ullmann P (2013) Gene coexpression analysis reveals complex metabolism of the monoterpene alcohol linalool in Arabidopsis flowers. Plant Cell 25:4640–4657PubMedPubMedCentralCrossRefGoogle Scholar
  43. Granero AM, Sanz JMG, Gonzalez FJE, Vidal JLM, Dornhaus A, Ghani J, Serrano AR, Chittka L (2005) Chemical compounds of the foraging recruitment pheromone in bumblebees. Naturwissenschaften 92:371–374PubMedCrossRefGoogle Scholar
  44. Green SA, Chen X, Nieuwenhuizen NJ, Matich AJ, Wang MY, Bunn BJ, Yauk YK, Atkinson RG (2011) Identification, functional characterization, and regulation of the enzyme responsible for floral (E)-nerolidol biosynthesis in kiwifruit (Actinidia chinensis). J Exp Bot 63:1951–1967PubMedPubMedCentralCrossRefGoogle Scholar
  45. Guirimand G, Guihur A, Phillips MA, Oudin A, Glévarec G, Melin C, Papon N, Clastre M, St-Pierre B, Rodríguez-Concepción M (2012) A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus. Plant Mol Biol 79:443–459PubMedCrossRefGoogle Scholar
  46. 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 3:93–101CrossRefGoogle Scholar
  47. Hampel D, Mosandl A, Wüst M (2005) Biosynthesis of mono- and sesquiterpenes in carrot roots and leaves (Daucus carota L.): metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways. Phytochemistry 66:305–311PubMedCrossRefGoogle Scholar
  48. Heil M, Bueno JCS (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472PubMedPubMedCentralCrossRefGoogle Scholar
  49. 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
  50. Hijaz F, Nehela Y, Killiny N (2016) Possible role of plant volatiles in tolerance against huanglongbing in citrus. Plant Signal Behav 11:e1138193PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hsieh MH, Chang CY, Hsu SJ, Chen JJ (2008) Chloroplast localization of methylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in ispD and ispE albino mutants in Arabidopsis. Plant Mol Biol 66:663–673PubMedCrossRefGoogle Scholar
  53. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008PubMedCrossRefGoogle Scholar
  54. Islam A, Ali MA, Sayeed A, Salam S, Islam A, Rahman M, Khan G, Khatun S (2003) An antimicrobial terpenoid from Caesalpinia pulcherrima Swartz.: its characterization, antimicrobial and cytotoxic activities. Asian J Plant Sci 2:17–24Google Scholar
  55. Jabalpurwala FA, Smoot JM, Rouseff RL (2009) A comparison of citrus blossom volatiles. Phytochemistry 70:1428–1434PubMedCrossRefGoogle Scholar
  56. Jayaramaiah RH, Anand A, Beedkar SD, Dholakia BB, Punekar SA, Kalunke RM, Gade WN, Thulasiram HV, Giri AP (2016) Functional characterization and transient expression manipulation of a new sesquiterpene synthase involved in β-caryophyllene accumulation in Ocimum. Biochem Biophys Res Commun 473:265–271PubMedCrossRefGoogle Scholar
  57. Jin J, Kim MJ, Dhandapani S, Tjhang JG, Yin JL, Wong L, Sarojam R, Chua NH, Jang IC (2015) The floral transcriptome of ylang–ylang (Cananga odorata var. fruticosa) uncovers biosynthetic pathways for volatile organic compounds and a multifunctional and novel sesquiterpene synthase. J Exp Bot 66:3959–3975PubMedPubMedCentralCrossRefGoogle Scholar
  58. John AJ, Karunakaran VP, George V, Pradeep NS, Sethuraman MG (2007) Chemical composition and antibacterial activity of leaf oil of Neolitsea foliosa (Nees) Gamble var. caesia (Meisner) Gamble. J Essent Oil Res 19:498–500CrossRefGoogle Scholar
  59. Johnson D, Gilbert L (2015) Interplant signalling through hyphal networks. New Phytol 205:1448–1453PubMedCrossRefGoogle Scholar
  60. Kappers IF, Aharoni A, Van Herpen TW, Luckerhoff LL, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072PubMedCrossRefGoogle Scholar
  61. Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52PubMedCrossRefGoogle Scholar
  62. Kessler A (2010) Plant defences against herbivore attack. eLS. doi: 10.1002/9780470015902.a0001324.pub3
  63. Kessler D, Diezel C, Clark DG, Colquhoun TA, Baldwin IT (2013) Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecol Lett 16:299–306PubMedCrossRefGoogle Scholar
  64. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  65. Kolosova N, Gorenstein N, Kish CM, Dudareva N (2001) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13:2333–2347PubMedPubMedCentralCrossRefGoogle Scholar
  66. Krasnyanski S, May R, Loskutov A, Ball T, Sink K (1999) Transformation of the limonene synthase gene into peppermint (Mentha piperita L.) and preliminary studies on the essential oil profiles of single transgenic plants. Theor Appl Genet 99:676–682PubMedCrossRefGoogle Scholar
  67. Lan JB, Yu RC, Yu YY, Fan YP (2013) Molecular cloning and expression of Hedychium coronarium farnesyl pyrophosphate synthase gene and its possible involvement in the biosynthesis of floral and wounding/herbivory induced leaf volatile sesquiterpenoids. Gene 518:360–367PubMedCrossRefGoogle Scholar
  68. Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes—current status and future opportunities. Plant Biotechnol J 11:169–196PubMedCrossRefGoogle Scholar
  69. Lange BM, Wildung MR, Stauber EJ, Sanchez C, Pouchnik D, Croteau R (2000) Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc Natl Acad Sci USA 97:2934–2939PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Nam KH, Amar O, Lastochkin E, Larkov O, Ravid U (2001) Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol 127:1256–1265PubMedPubMedCentralCrossRefGoogle Scholar
  71. Li RH, Fan YP (2007) Changes in floral aroma constituents in Hedychium coronarium Koenig during different blooming stages. Plant Physiol Commun 43:176Google Scholar
  72. Li RH, Fan YP (2011) Molecular cloning and expression analysis of a terpene synthase gene, HcTPS2, in Hedychium coronarium. Plant Mol Biol Rep 29:35–42CrossRefGoogle Scholar
  73. Li XY, Zheng SY, Yu RC, Fan YP (2014) Promoters of HcTPS1 and HcTPS2 genes from Hedychium coronarium direct floral-specific, developmental-regulated and stress-inducible gene expression in transgenic tobacco. Plant Mol Biol Rep 32:864–880CrossRefGoogle Scholar
  74. Lluch MA, Masferrer A, Arró M, Boronat A, Ferrer A (2000) Molecular cloning and expression analysis of the mevalonate kinase gene from Arabidopsis thaliana. Plant Mol Biol 42:365–376PubMedCrossRefGoogle Scholar
  75. Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323CrossRefGoogle Scholar
  76. Lu S, Xu R, Jia JW, Pang J, Matsuda SP, Chen XY (2002) Cloning and functional characterization of a β-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiol 130:477–486PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lu X, Tang K, Li P (2016) Plant metabolic engineering strategies for the production of pharmaceutical terpenoids. Front Plant Sci 7:1647PubMedPubMedCentralGoogle Scholar
  78. 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
  79. Lücker J, Bowen P, Bohlmann J (2004) Vitis vinifera terpenoid cyclases: functional identification of two sesquiterpene synthase cDNAs encoding (+)-valencene synthase and (−)-germacrene D synthase and expression of mono- and sesquiterpene synthases in grapevine flowers and berries. Phytochemistry 65:2649–2659PubMedCrossRefGoogle Scholar
  80. Ma D, Li G, Zhu Y, Xie DY (2017) Overexpression and suppression of Artemisia annua 4-hydroxy-3-methylbut-2-enyl diphosphate reductase 1 gene (AaHDR1) differentially regulate Artemisinin and terpenoid biosynthesis. Front Plant Sci 8:77. doi: 10.3389/fpls.2017.00077
  81. Mahmoud SS, Croteau RB (2002) Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci 7:366–373PubMedCrossRefGoogle Scholar
  82. Mercke P, Kappers IF, Verstappen FW, Vorst O, Dicke M, Bouwmeester HJ (2004) Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiol 135:2012–2024PubMedPubMedCentralCrossRefGoogle Scholar
  83. 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 137:369–382PubMedPubMedCentralCrossRefGoogle Scholar
  84. Morse A, Kevan P, Shipp L, Khosla S, McGarvey B (2012) The impact of greenhouse tomato (Solanales: Solanaceae) floral volatiles on bumble bee (Hymenoptera: Apidae) pollination. Environ Entomol 41:855–864CrossRefGoogle Scholar
  85. Muhlemann JK, Waelti MO, Widmer A, Schiestl FP (2006) Postpollination changes in floral odor in Silene latifolia: adaptive mechanisms for seed-predator avoidance? J Chem Ecol 32:1855–1860PubMedCrossRefGoogle Scholar
  86. Muhlemann JK, Maeda H, Chang CY, San Miguel P, Baxter I, Cooper B, Perera MA, Nikolau BJ, Vitek O, Morgan JA (2012) Developmental changes in the metabolic network of snapdragon flowers. PLoS One 7:e40381PubMedPubMedCentralCrossRefGoogle Scholar
  87. Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant Cell Environ 37:1936–1949PubMedCrossRefGoogle Scholar
  88. Mumm R, Posthumus MA, Dicke M (2008) Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ 31:575–585PubMedCrossRefGoogle Scholar
  89. Nagegowda DA (2010) Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett 584:2965–2973PubMedCrossRefGoogle Scholar
  90. 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 55:224–239PubMedCrossRefGoogle Scholar
  91. Nagegowda DA, Rhodes D, Dudareva N (2010) Chapter 10. The role of the methyl-erythritol-phosphate (MEP) pathway in rhythmic emission of volatiles. In: Rebeiz CA et al (ed) The chloroplast. Advances in photosynthesis and respiration, vol 31. Springer, DordrechtGoogle Scholar
  92. Nieuwenhuizen NJ, Wang MY, Matich AJ, Green SA, Chen X, Yauk YK, Beuning LL, Nagegowda DA, Dudareva N, Atkinson RG (2009) Two terpene synthases are responsible for the major sesquiterpenes emitted from the flowers of kiwifruit (Actinidia deliciosa). J Exp Bot 60:3203–3219PubMedPubMedCentralCrossRefGoogle Scholar
  93. Okamoto T, Kawakita A, Kato M (2007) Interspecific variation of floral scent composition in Glochidion and its association with host-specific pollinating seed parasite (Epicephala). J Chem Ecol 33:1065–1081PubMedCrossRefGoogle Scholar
  94. Orlova I, Nagegowda DA, Kish CM, Gutensohn M, Maeda H, Varbanova M, Fridman E, Yamaguchi S, Hanada A, Kamiya Y (2009) The small subunit of snapdragon geranyl diphosphate synthase modifies the chain length specificity of tobacco geranylgeranyl diphosphate synthase in planta. Plant Cell 21:4002–4017PubMedPubMedCentralCrossRefGoogle Scholar
  95. Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T (2000) Involvement of jasmonate and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 41:391–398PubMedCrossRefGoogle Scholar
  96. Paschold A, Halitschke R, Baldwin IT (2006) Using ‘mute’plants to translate volatile signals. Plant J 45:275–291PubMedCrossRefGoogle Scholar
  97. Peñuelas J, Asensio D, Tholl D, Wenke K, Rosenkranz M, Piechulla B, Schnitzler J (2014) Biogenic volatile emissions from the soil. Plant Cell Environ 37:1866–1891PubMedCrossRefGoogle Scholar
  98. Pichersky E, Dudareva N (2007) Scent engineering: toward the goal of controlling how flowers smell. Trends Biotechnol 25:105–110PubMedCrossRefGoogle Scholar
  99. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811PubMedPubMedCentralCrossRefGoogle Scholar
  100. Prabuseenivasan S, Jayakumar M, Ignacimuthu S (2006) In vitro antibacterial activity of some plant essential oils. BMC Complement Altern Med 6:39PubMedPubMedCentralCrossRefGoogle Scholar
  101. Pulido P, Perello C, Rodriguez-Concepcion M (2012) New insights into plant isoprenoid metabolism. Mol Plant 5:964–967PubMedCrossRefGoogle Scholar
  102. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732PubMedCrossRefGoogle Scholar
  103. 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
  104. Rosenkranz M, Schnitzler JP (2016) Plant Volatiles. eLS. doi: 10.1002/9780470015902.a0000910.pub3
  105. Schilmiller AL, Schauvinhold I, Larson M, Xu R, Charbonneau AL, Schmidt A, Wilkerson C, Last RL, Pichersky E (2009) Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proc Natl Acad Sci 106:10865–10870PubMedPubMedCentralCrossRefGoogle Scholar
  106. Schnee C, Köllner TG, Held M, Turlings TC, 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 103:1129–1134PubMedPubMedCentralCrossRefGoogle Scholar
  107. Seybold SJ, Huber DP, Lee JC, Graves AD, Bohlmann J (2006) Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication. Phytochem Rev 5:143–178CrossRefGoogle Scholar
  108. Shimada T, Endo T, Fujii H, Hara M, Omura M (2005) Isolation and characterization of (E)-β-ocimene and 1,8 cineole synthases in Citrus unshiu Marc. Plant Sci 168:987–995CrossRefGoogle Scholar
  109. Singh B, Sharma RA (2015) Plant terpenes: defense responses, phylogenetic analysis, regulation and clinical applications. 3 Biotech 5(2):129–151. doi: 10.1007/s13205-014-0220-2 PubMedCrossRefGoogle Scholar
  110. Suzuki H, Reddy MS, Naoumkina M, Aziz N, May GD, Huhman DV, Sumner LW, Blount JW, Mendes P, Dixon RA (2005) Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta 220:696–707PubMedCrossRefGoogle Scholar
  111. Thabet I, Guirimand G, Guihur A, Lanoue A, Courdavault V, Papon N, Bouzid S, Giglioli-Guivarc’h N, Simkin AJ, Clastre M (2012) Characterization and subcellular localization of geranylgeranyl diphosphate synthase from Catharanthus roseus. Mol Biol Rep 39:3235–3243PubMedCrossRefGoogle Scholar
  112. Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65:225–257PubMedCrossRefGoogle Scholar
  113. Tholl D (2015) Biosynthesis and biological functions of terpenoids in plants. In: Schrader J, Bohlmann J (eds) Biotechnology of isoprenoids. Advances in biochemical engineering/biotechnology, vol 148. Springer, ChamGoogle Scholar
  114. Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book 9: e0143. doi: 10.1199/tab.0143
  115. 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
  116. 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
  117. Townsend BJ, Poole A, Blake CJ, Llewellyn DJ (2005) Antisense suppression of a (+)-δ-cadinene synthase gene in cotton prevents the induction of this defense response gene during bacterial blight infection but not its constitutive expression. Plant Physiol 138:516–528PubMedPubMedCentralCrossRefGoogle Scholar
  118. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485PubMedCrossRefGoogle Scholar
  119. Van Poecke RM, 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
  120. Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:1612–1624PubMedPubMedCentralCrossRefGoogle Scholar
  121. Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5:318–333PubMedCrossRefGoogle Scholar
  122. Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700PubMedCrossRefGoogle Scholar
  123. Waelti M, Muhlemann J, Widmer A, Schiestl F (2008) Floral odour and reproductive isolation in two species of Silene. J Evol Biol 21:111–121PubMedGoogle Scholar
  124. Weathers PJ, Arsenault PR, Covello PS, McMickle A, Teoh KH, Reed DW (2011) Artemisinin production in Artemisia annua: studies in planta and results of a novel delivery method for treating malaria and other neglected diseases. Phytochem Rev 10:173–183PubMedPubMedCentralCrossRefGoogle Scholar
  125. Wright GA, Schiestl FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol 23:841–851CrossRefGoogle Scholar
  126. 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 24:1441PubMedCrossRefGoogle Scholar
  127. Xi Z, Bradley RK, Wurdack KJ, Wong K, Sugumaran M, Bomblies K, Rest JS, Davis CC (2012) Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genom 13:227CrossRefGoogle Scholar
  128. Yahyaa M, Tholl D, Cormier G, Jensen R, Simon PW, Ibdah M (2015) Identification and characterization of terpene synthases potentially involved in the formation of volatile terpenes in carrot (Daucus carota L.) roots. J Agric Food Chem 63:4870–4878PubMedCrossRefGoogle Scholar
  129. Yu F, Utsumi R (2009) Diversity, regulation, and genetic manipulation of plant mono- and sesquiterpenoid biosynthesis. Cell Mol Life Sci 66:3043–3052PubMedCrossRefGoogle Scholar
  130. Yu XD, Pickett J, Ma YZ, Bruce T, Napier J, Jones HD, Xia LQ (2012) Metabolic engineering of plant-derived (E)-β-farnesene synthase genes for a novel type of aphid-resistant genetically modified crop plants. J Integrative Plant Biol 54:282–299CrossRefGoogle Scholar
  131. Yue Y, Yu RC, Fan YP (2014) Characterization of two monoterpene synthases involved in floral scent formation in Hedychium coronarium. Planta 240:745–762PubMedCrossRefGoogle Scholar
  132. Yue Y, Yu RC, Fan YP (2015) Transcriptome profiling provides new insights into the formation of floral scent in Hedychium coronarium. BMC Genom 16:470CrossRefGoogle Scholar
  133. Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integrative Plant Biol 52:86–97CrossRefGoogle Scholar
  134. Zvi MMB, Shklarman E, Masci T, Kalev H, Debener T, Shafir S, Ovadis M, Vainstein A (2012) PAP1 transcription factor enhances production of phenylpropanoid and terpenoid scent compounds in rose flowers. New Phytol 195:335–345PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Farhat Abbas
    • 1
  • Yanguo Ke
    • 1
  • Rangcai Yu
    • 2
    Email author
  • Yuechong Yue
    • 1
  • Sikandar Amanullah
    • 3
  • Muhammad Muzammil Jahangir
    • 4
  • Yanping Fan
    • 1
    • 5
    Email author
  1. 1.The Research Center for Ornamental Plants, College of Forestry and Landscape ArchitectureSouth China Agricultural UniversityGuangzhouChina
  2. 2.College of Life SciencesSouth China Agricultural UniversityGuangzhouChina
  3. 3.College of Horticulture and Landscape ArchitectureNortheast Agricultural UniversityHarbinChina
  4. 4.Institute of Horticultural SciencesUniversity of AgricultureFaisalabadPakistan
  5. 5.Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant GermplasmSouth China Agricultural UniversityGuangzhouChina

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