Abstract
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.
Similar content being viewed by others
References
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
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 16:3110–3131
Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trend Plant Sci 10:594–602
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 5:49–58
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:e38146
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 135:1976–1983
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):2739–2752
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 5:255–261
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475
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 311:812–815
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 8:61–75
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 226:853–866
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 71:40–47
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):1993–2011
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 203:939–952
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 18:1783–1797
Buckingham J (2004) Dictionary of natural products web version 2004. Chapman and Hall, London. http://www.chemnetbase.com
Capell T, Christou P (2004) Progress in plant metabolic engineering. Curr Opin Biotechnol 15:148–154
Caputi L, Aprea E (2011) Use of terpenoids as natural flavouring compounds in food industry. Recent Patent Food Nutr Agric 3:9–16
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 135:1956–1966
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 66:212–229
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 62:1133–1143
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 156:974–984
Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). Biochem Mol Biol Plants 24:1250–1319
Das A, Lee SH, Hyun TK, Kim SW, Kim JY (2013) Plant volatiles as method of communication. Plant Biotechnol Rep 7:9–26
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 56:228–238
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 135:1928–1938
Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochem 70:1621–1637
Delory BM, Delaplace P, Fauconnier ML, Du Jardin P (2016) Root-emitted volatile organic compounds: can they mediate belowground plant–plant interactions? Plant Soil 402:1–26
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175
Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–634
Dudareva N, Pichersky E (2008) Metabolic engineering of plant volatiles. Curr Opin Biotechnol 19:181–189
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 102:933–938
Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32
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)
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)
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 15:56–67
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 148:90–99
Flügge UI, Gao W (2005) Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol 7:91–97
Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414
Gershenzon J, McConkey ME, Croteau RB (2000) Regulation of monoterpene accumulation in leaves of peppermint. Plant Physiol 122:205–214
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 25:4640–4657
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 92:371–374
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 63:1951–1967
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 79:443–459
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 3:93–101
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 66:305–311
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 104:5467–5472
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 278:26666–26676
Hijaz F, Nehela Y, Killiny N (2016) Possible role of plant volatiles in tolerance against huanglongbing in citrus. Plant Signal Behav 11:e1138193
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 24:2635–2648
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 66:663–673
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 193:997–1008
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 2:17–24
Jabalpurwala FA, Smoot JM, Rouseff RL (2009) A comparison of citrus blossom volatiles. Phytochemistry 70:1428–1434
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 473:265–271
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 66:3959–3975
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 19:498–500
Johnson D, Gilbert L (2015) Interplant signalling through hyphal networks. New Phytol 205:1448–1453
Kappers IF, Aharoni A, Van Herpen TW, Luckerhoff LL, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072
Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52
Kessler A (2010) Plant defences against herbivore attack. eLS. doi:10.1002/9780470015902.a0001324.pub3
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 16:299–306
Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120
Kolosova N, Gorenstein N, Kish CM, Dudareva N (2001) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13:2333–2347
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 99:676–682
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 518:360–367
Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes—current status and future opportunities. Plant Biotechnol J 11:169–196
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 97:2934–2939
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 127:1256–1265
Li RH, Fan YP (2007) Changes in floral aroma constituents in Hedychium coronarium Koenig during different blooming stages. Plant Physiol Commun 43:176
Li RH, Fan YP (2011) Molecular cloning and expression analysis of a terpene synthase gene, HcTPS2, in Hedychium coronarium. Plant Mol Biol Rep 29:35–42
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 32:864–880
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 42:365–376
Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323
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 130:477–486
Lu X, Tang K, Li P (2016) Plant metabolic engineering strategies for the production of pharmaceutical terpenoids. Front Plant Sci 7:1647
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 27:315–324
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 65:2649–2659
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
Mahmoud SS, Croteau RB (2002) Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci 7:366–373
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 135:2012–2024
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 137:369–382
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 41:855–864
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 32:1855–1860
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:e40381
Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant Cell Environ 37:1936–1949
Mumm R, Posthumus MA, Dicke M (2008) Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ 31:575–585
Nagegowda DA (2010) Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett 584:2965–2973
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
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, Dordrecht
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 60:3203–3219
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 33:1065–1081
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 21:4002–4017
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 41:391–398
Paschold A, Halitschke R, Baldwin IT (2006) Using ‘mute’plants to translate volatile signals. Plant J 45:275–291
Peñuelas J, Asensio D, Tholl D, Wenke K, Rosenkranz M, Piechulla B, Schnitzler J (2014) Biogenic volatile emissions from the soil. Plant Cell Environ 37:1866–1891
Pichersky E, Dudareva N (2007) Scent engineering: toward the goal of controlling how flowers smell. Trends Biotechnol 25:105–110
Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811
Prabuseenivasan S, Jayakumar M, Ignacimuthu S (2006) In vitro antibacterial activity of some plant essential oils. BMC Complement Altern Med 6:39
Pulido P, Perello C, Rodriguez-Concepcion M (2012) New insights into plant isoprenoid metabolism. Mol Plant 5:964–967
Rasmann S, Kollner TG, Degenhardt J, Hiltpold I (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732
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 65:107–124
Rosenkranz M, Schnitzler JP (2016) Plant Volatiles. eLS. doi:10.1002/9780470015902.a0000910.pub3
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 106:10865–10870
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 103:1129–1134
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 5:143–178
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 168:987–995
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
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 220:696–707
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 39:3235–3243
Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65:225–257
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, Cham
Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book 9: e0143. doi:10.1199/tab.0143
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 42:757–771
Towler MJ, Weathers PJ (2007) Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways. Plant Cell Rep 26:2129–2136
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 138:516–528
Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485
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 27:1911–1928
Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:1612–1624
Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5:318–333
Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700
Waelti M, Muhlemann J, Widmer A, Schiestl F (2008) Floral odour and reproductive isolation in two species of Silene. J Evol Biol 21:111–121
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 10:173–183
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 23:841–851
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
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 13:227
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 63:4870–4878
Yu F, Utsumi R (2009) Diversity, regulation, and genetic manipulation of plant mono- and sesquiterpenoid biosynthesis. Cell Mol Life Sci 66:3043–3052
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 54:282–299
Yue Y, Yu RC, Fan YP (2014) Characterization of two monoterpene synthases involved in floral scent formation in Hedychium coronarium. Planta 240:745–762
Yue Y, Yu RC, Fan YP (2015) Transcriptome profiling provides new insights into the formation of floral scent in Hedychium coronarium. BMC Genom 16:470
Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integrative Plant Biol 52:86–97
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 195:335–345
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Abbas, F., Ke, Y., Yu, R. et al. Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering. Planta 246, 803–816 (2017). https://doi.org/10.1007/s00425-017-2749-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-017-2749-x