Abstract
Isoprenoids constitute one of the largest families of natural compounds. They play essential functions in plant growth and development and furnish compounds of high interest for humans. Here, we present the current knowledge on isoprenoid metabolism before describing the strategies that have been used for isoprenoid metabolic engineering. We discuss the advantages and drawbacks of using microorganisms and plants as cell platform for the production of isoprenoids of interest.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- ADS:
-
Amorpha 4,11-diene synthase
- CRY2:
-
Cryptochrome 2
- DET1:
-
De-etiolated 1
- DMAPP:
-
Dimethylallyl diphosphate
- DXP:
-
1-deoxy-d-xylulose 5-phosphate
- DXR:
-
1-deoxy-d-xylulose 5-phosphate
- FPP:
-
Farnesyl diphosphate
- FPS:
-
Farnesyl diphosphate synthase
- GGPP:
-
Geranyl geranyl diphosphate
- GGPS:
-
Geranyl geranyl diphosphate synthase
- GPP:
-
Geranyl diphosphate
- GPS:
-
Geranyl diphosphate synthase
- HMG:
-
3-hydroxyl-3-methylglutaryl
- HMGR:
-
3-hydroxyl-3-methylglutaryl reductase
- IDS:
-
Isoprenyl diphosphate synthase
- IPP:
-
Isopentenyl diphosphate
- IS:
-
Isoprene synthase
- MEP:
-
Methyl-d-erythritol 4-phosphate
- MGT:
-
Multigene transfer
- MVA:
-
Acetate/mevalonate
- NES1:
-
Nerolidol synthase
- NPP:
-
Neryl diphosphate
- PSY:
-
Phytoene synthase
- PTS:
-
Prenyltransferase
- SqS:
-
Squalene synthase
- TPS:
-
Terpene synthase
- VOCS:
-
Volatile organic compounds.
References
Thulasiram HV, Erickson HK, Poulter CD (2007) Chimeras of two isoprenoid synthases catalyze all four coupling reactions in isoprenoid biosynthesis. Science 316:73–76
Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291
Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–634
Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175
Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184
Finley JW, Kong A-N, Hintze KJ, Jeffery EH, Ji LL, Lei XG (2011) Antioxidants in foods: state of the science important to the food industry. J Agric Food Chem 59:6837–6846
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils – a review. Food Chem Toxicol 46:446–475
Liu B, Wang H, Du Z, Li G, Ye H (2011) Metabolic engineering of artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep 30:689–694
Greay S, Hammer K (2011) Recent developments in the bioactivity of mono- and diterpenes: anticancer and antimicrobial activity. Phytochem Rev: 1–6
Jennewein S, Rithner CD, Williams RM, Croteau RB (2001) Taxol biosynthesis: taxane 13 alpha-hydroxylase is a cytochrome P450-dependent monooxygenase. Proc Natl Acad Sci 98:13595–13600
Koepp AE, Hezari M, Zajicek J, Vogel BS, LaFever RE, Lewis NG, Croteau R (1995) Cyclization of geranylgeranyl diphosphate to taxa-4 (5), 11 (12) -diene is the committed step of taxol biosynthesis in pacific yew. J Biol Chem 270:8686–8690
Kirby J, Keasling JD (2009) Biosynthesis of plant isoprenoids: perspectives for microbial engineering. Annu Rev Plant Biol 60:335–355
Farmer WR, Liao JC (2000) Improving lycopene production in Escherichia coli by engineering metabolic control. Nat Biotechnol 18:533–537
Klein-Marcuschamer D, Ajikumar PK, Stephanopoulos G (2007) Engineering microbial cell factories for biosynthesis of isoprenoid molecules: beyond lycopene. Trends Biotechnol 25:417–424
Muntendam R, Melillo E, Ryden A, Kayser O (2009) Perspectives and limits of engineering the isoprenoid metabolism in heterologous hosts. Appl Microbiol Biotechnol 84:1003–1019
Hong K-K, Nielsen J (2012) Metabolic engineering of Saccharomyces cerevisiae: a key cell factory platform for future biorefineries. Cell Mol Life Sci: 1–20
Raja R, Hemaiswarya S, Rengasamy R (2007) Exploitation of Dunaliella for β-carotene production. Appl Microbiol Biotechnol 74:517–523
Wilson SA, Roberts SC (2012) Recent advances towards development and commercialization of plant cell culture processes for the synthesis of biomolecules. Plant Biotechnol J 10:249–268
Chandra S (2012) Natural plant genetic engineer Agrobacterium rhizogenes: role of T-DNA in plant secondary metabolism. Biotechnol Lett 34:407–415
Schörken U, Kempers P (2009) Lipid biotechnology: industrially relevant production processes. Eur J Lipid Sci Technol 111:627–645
Degenhardt J, Gershenzon J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14:169–176
Dudareva N, Pichersky E (2008) Metabolic engineering of plant volatiles. Curr Opin Biotechnol 19:181–189
Giuliano G, Tavazza R, Diretto G, Beyer P, Taylor MA (2008) Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol 26:139–145
Fraser PD, Enfissi EMA, Bramley PM (2009) Genetic engineering of carotenoid formation in tomato fruit and the potential application of systems and synthetic biology approaches. Arch Biochem Biophys 483:196–204
Van Herpen TWJM, Cankar K, Nogueira M, Bosch D, Bouwmeester HJ, Beekwilder J (2010) Nicotiana benthamiana as a production platform for artemisinin precursors. PLoS One 5:e14222
Yu F, Utsumi R (2009) Diversity, regulation, and genetic manipulation of plant mono- and sesquiterpenoid biosynthesis. Cell Mol Life Sci 66:3043–3052
Withers S, Keasling J (2007) Biosynthesis and engineering of isoprenoid small molecules. Appl Microbiol Biotechnol 73:980–990
Sawai S, Saito K (2011) Triterpenoid biosynthesis and engineering in plants. Front Plant Sci 2:25
Expósito O, Bonfill M, Moyano E, Onrubia M, Mirjalili M, Cusidó R, Palazón J (2009) Biotechnological production of taxol and related taxoids: current state and prospects. Anticancer Agents Med Chem 9:109–121
Rohmer M, Knani M, Pascale S, Sutter B, Sahm H (1993) Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J 295:517–524
Kovacs WJ, Olivier LM, Krisans SK (2002) Central role of peroxisomes in isoprenoid biosynthesis. Prog Lipid Res 41:369–391
Kovacs W, Tape K, Shackelford J, Duan X, Kasumov T, Kelleher J, Brunengraber H, Krisans S (2007) Localization of the pre-squalene segment of the isoprenoid biosynthetic pathway in mammalian peroxisomes. Histochem Cell Biol 127:273–290
Sapir-Mir M, Mett A, Belausov E, Tal-Meshulam S, Frydman A, Gidoni D, Eyal Y (2008) Peroxisomal localization of arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol 148:1219–1228
Kuzuyama T, Seto H (2003) Diversity of the biosynthesis of the isoprene units. Nat Prod Rep 20:171–183
Lichtenthaler HK, Schwender J, Disch A, Rohmer M (1997) Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett 400:271–274
Hemmerlin A, Harwood JL, Bach TJ (2012) A raison d'être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog Lipid Res 51:95–148
Towler M, Weathers P (2007) Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways. Plant Cell Rep 26:2129–2136
McCaskill D, Croteau R (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (mentha X piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta 197:49–56
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
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 149:499–514
Sallaud C, Rontein D, Onillon S, Jabès F, Duffé 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 Online 21:301–317
Kellogg BA, Poulter CD (1997) Chain elongation in the isoprenoid biosynthetic pathway. Curr Opin Chem Biol 1:570–578
Wang KC, Ohnuma S-I (2000) Isoprenyl diphosphate synthases. Biochim Biophys Acta (BBA) Mol Cell Biol Lipids 1529:33–48
Liang P-H, Ko T-P, Wang AHJ (2002) Structure, mechanism and function of prenyltransferases. Eur J Biochem 269:3339–3354
Fujihashi M, Zhang Y-W, Higuchi Y, Li X-Y, Koyama T, Miki K (2001) Crystal structure of cis-prenyl chain elongating enzyme, undecaprenyl diphosphate synthase. Proc Natl Acad Sci 98:4337–4342
Takahashi S, Koyama T (2006) Structure and function of cis-prenyl chain elongating enzymes. Chem Rec 6:194–205
Asawatreratanakul K, Zhang Y-W, Wititsuwannakul D, Wititsuwannakul R, Takahashi S, Rattanapittayaporn A, Koyama T (2003) Molecular cloning, expression and characterization of cDNA encoding cis-prenyltransferases from Hevea brasiliensis. Eur J Biochem 270:4671–4680
Post J, van Deenen N, Fricke J, Kowalski N, Wurbs D, Schaller H, Eisenreich W, Huber C, Twyman RM, Prüfer D, Gronover CS (2012) Laticifer-specific cis-prenyltransferase silencing affects the rubber, triterpene, and inulin content of Taraxacum brevicorniculatum. Plant Physiol 158:1406–1417
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
Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book 9:e0143
Tarshis LC, Proteau JP, Kellogg BA, Sacchettini JC, Poulter CD (1996) Regulation of product chain length by isoprenyl diphosphate synthases. Proc Natl Acad Sci 93:15018–15023
Ogura K, Koyama T (1998) Enzymatic aspects of isoprenoid chain elongation. Chem Rev 98:1263–1276
Liang P-H (2009) Reaction kinetics, catalytic mechanisms, conformational changes, and inhibitor design for prenyltransferases. Biochemistry 48:6562–6570
Oldfield E, Lin F-Y (2012) Terpene biosynthesis: modularity rules. Angew Chem Int Ed 51:1124–1137
Cervantes-Cervantes M, Gallagher CE, Zhu C, Wurtzel ET (2006) Maize cDNAs expressed in endosperm encode functional farnesyl diphosphate synthase with geranylgeranyl diphosphate synthase activity. Plant Physiol 141:220–231
Hsiao Y-Y, Jeng M-F, Tsai W-C, Chuang Y-C, Li C-Y, Wu T-S, Kuoh C-S, Chen W-H, Chen H-H (2008) A novel homodimeric geranyl diphosphate synthase from the orchid Phalaenopsis bellina lacking a DD(X)2–4D motif. Plant J 55:719–733
Schmidt A, Wächtler B, Temp U, Krekling T, Séguin A, Gershenzon J (2011) A bifunctional geranyl and geranylgeranyl diphosphate synthase is involved in terpene oleoresin formation in picea abies. Plant Physiol 152:639–655
Hsieh F-L, Chang T-H, Ko T-P, Wang AHJ (2011) Structure and mechanism of an Arabidopsis medium/long-chain-length prenyl pyrophosphate synthase. Plant Physiol 155:1079–1090
Ducluzeau A-L, Wamboldt Y, Elowsky CG, Mackenzie SA, Schuurink RC, Basset GJC (2012) Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis. Plant J 69:366–375
Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304
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
Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637
Martin DM, Fäldt J, Bohlmann J (2004) Functional characterization of nine Norway spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol 135:1908–1927
Keeling CI, Weisshaar S, Lin RPC, Bohlmann J (2008) Functional plasticity of paralogous diterpene synthases involved in conifer defense. Proc Natl Acad Sci 105:1085–1090
Aubourg SA, Lecharny AL, Bohlmann JB (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genet Genomics 267:730–745
Falara V, Akhtar TA, Nguyen TTH, Spyropoulou EA, Bleeker PM, Schauvinhold I, Matsuba Y, Bonini ME, Schilmiller AL, Last RL, Schuurink RC, Pichersky E (2011) The tomato terpene synthase gene family. Plant Physiol 157:770–789
Naoumkina MA, Modolo LV, Huhman DV, Urbanczyk-Wochniak E, Tang Y, Sumner LW, Dixon RA (2010) Genomic and coexpression analyses predict multiple genes involved in triterpene saponin biosynthesis in Medicago truncatula. Plant Cell Online 22:850–866
Keeling C, Weisshaar S, Ralph S, Jancsik S, Hamberger B, Dullat H, Bohlmann J (2011) Transcriptome mining, functional characterization, and phylogeny of a large terpene synthase gene family in spruce (Picea spp.). BMC Plant Biol 11:43
Hayashi K-i, Kawaide H, Notomi M, Sakigi Y, Matsuo A, Nozaki H (2006) Identification and functional analysis of bifunctional ent-kaurene synthase from the moss Physcomitrella patens. FEBS Lett 580:6175–6181
Sun TP, Kamiya Y (1994) The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell Online 6:1509–1518
Yamaguchi S, Sun T-p, Kawaide H, Kamiya Y (1998) The GA2 locus of arabidopsis thaliana encodes ent-kaurene synthase of gibberellin biosynthesis. Plant Physiol 116:1271–1278
Chen F, Tholl D, D'Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell Online 15:481–494
Chen F, Ro D-K, 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
Fäldt J, Arimura G-I, Gershenzon J, Takabayashi J, Bohlmann J (2003) Functional identification of AtTPS03 as (E)-beta-ocimene synthase: a monoterpene synthase catalyzing jasmonate- and wound-induced volatile formation in Arabidopsis thaliana. Planta 216:745–751
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
Herde M, Gärtner K, Köllner TG, Fode B, Boland W, Gershenzon J, Gatz C, Tholl D (2008) Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell Online 20:1152–1168
Bohlmann J, Martin D, Oldham NJ, Gershenzon J (2000) Terpenoid secondary metabolism in Arabidopsis thaliana: cDNA cloning, characterization, and functional expression of a myrcene/(E)-beta-ocimene synthase. Arch Biochem Biophys 375:261–269
Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell Online 16:3110–3131
Bleeker P, Spyropoulou E, Diergaarde P, Volpin H, De Both M, Zerbe P, Bohlmann J, Falara V, Matsuba Y, Pichersky E, Haring M, Schuurink R (2011) RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Mol Biol 77:323–336
Cankar K, Houwelingen AV, Bosch D, Sonke T, Bouwmeester H, Beekwilder J (2011) A chicory cytochrome P450 mono-oxygenase CYP71AV8 for the oxidation of (+)-valencene. FEBS Lett 585:178–182
Teoh KH, Polichuk DR, Reed DW, Nowak G, Covello PS (2006) Artemisia annua L (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett 580:1411–1416
Nelson D (2006) Plant cytochrome P450s from moss to poplar. Phytochem Rev 5:193–204
Bak S, Beisson F, Bishop G, Hamberger B, Höfer R, Paquette S, Werck-Reichhart D (2011) Cytochromes P450. The Arabidopsis Book 9:e0144
Mahmoud SS, Croteau RB (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 98:8915–8920
Lange BM, Mahmoud SS, Wildung MR, Turner GW, Davis EM, Lange I, Baker RC, Boydston RA, Croteau RB (2011) Improving peppermint essential oil yield and composition by metabolic engineering. Proc Natl Acad Sci 108:16944–16949
Ehlting J, Sauveplane V, Olry A, Ginglinger J-F, Provart N, Werck-Reichhart D (2008) An extensive (co-)expression analysis tool for the cytochrome P450 superfamily in Arabidopsis thaliana. BMC Plant Biol 8:47
Hassan AMM (2011) A review of secondary metabolites from plant materials for post harvest storage. Int J Pure Appl Sci Technol 6:94–102
Bouvier F, Suire C, D'Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J 24:241–252
Croteau R (1988) Catabolism of monoterpenes in essential oil plants. In: Lawrence BM, Mookherjee BD, Willis BJ (eds) Flavors and fragrances: a world perspective. Proceedings of the 10th international congress of essential oils, fragrances and flavors, Washington, DC, November, 1986. Elsevier Science, Amsterdam
Little DB, Croteau R (1999) Biochemistry of essential oil terpenes: a thirty year overview. In: Teranishi R, Wick EL, Hornstein I (eds) Flavor chemistry: thirty years of progress. Kluwer/Plenum, New York
Loza-Tavera H (1999) Monoterpenes in essential oils: biosynthesis and properties. Adv Exp Med Biol 464:49–62
Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens*. New Phytol 170:657–675
Kainulainen P, Satka H, Mustaniemi A, Holopainen JK, Oksanen J (1993) Conifer aphids in an air-polluted environment. II. Host plant quality. Environ Pollut 80:193–200
Turtola S, Manninen AM, Holopainen JK, Levula T, Raitio H, Kainulainen P (2002) Secondary metabolite concentrations and terpene emissions of scots pine xylem after long-term forest fertilization. J Environ Qual 31:1694–1701
Turtola S, Manninen A-M, Rikala R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in scots pine and Norway Spruce seedlings. J Chem Ecol 29:1981–1995
Tomlin ES, Antonejevic E, Alfaro RI, Borden JH (2000) Changes in volatile terpene and diterpene resin acid composition of resistant and susceptible white spruce leaders exposed to simulated white pine weevil damage. Tree Physiol 20:1087–1095
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
Raffa KF, Smalley EB (1995) Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia 102:285–295
Phillips MA, Croteau RB (1999) Resin-based defenses in conifers. Trends Plant Sci 4:184–190
Trapp S, Croteau R (2001) Defensive resin biosynthesis in conifers. Ann Rev Plant Physiol Plant Mol Biol 52:689–724
Franceschi VR, Krekling T, Christiansen E (2002) Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am J Bot 89:578–586
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 129:1003–1018
McKay SAB, Hunter WL, Godard K-A, 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 133:368–378
Rohloff J (2004) Essential oil drugs – terpene composition of aromatic herbs. In: Dris R, Jain SM (eds) Production practices and quality assessment of food crops, vol 3, Quality Handling and Evaluation. Kluwer, Dordrecht
Sangwan NK, Dhindsa KS, Malik OP, Sharma GD, Paroda RS (1982) Quantitative changes in levels of essential oil in C. martinii var motia during different growth stages and on ageing the harvested crop in field and Laboratory. In: Proceedings of the national seminar on medicinal and aromatic plants, India
Maeda E, Miyake H, Tomaru K (1999) Ultrastructure of mesophyll glands secreting the aromatic substances in Patchouli leaves. Crop Science Society of Japan, Tokyo
Lewinsohn E, Dudai N, Tadmor Y, Katzir I, Ravid UZI, Putievsky ELI, Joel DM (1998) Histochemical localization of citral accumulation in lemongrass leaves (Cymbopogon citratus(DC.) Stapf., Poaceae). Ann Bot 81:35–39
Dai X, Wang G, Yang DS, Tang Y, Broun P, Marks MD, Sumner LW, Dixon RA, Zhao PX (2010) TrichOME: a comparative omics database for plant trichomes. Plant Physiol 152:44–54
Gershenzon J, McConkey ME, Croteau RB (2000) Regulation of monoterpene accumulation in leaves of peppermint. Plant Physiol 122:205–214
McConkey ME, Gershenzon J, Croteau RB (2000) Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. Plant Physiol 122:215–224
Turner GW, Gershenzon J, Croteau RB (2000) Distribution of peltate glandular trichomes on developing leaves of peppermint. Plant Physiol 124:655–664
Gershenzon J, Maffei M, Croteau R (1989) Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). Plant Physiol 89:1351–1357
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 187:445–454
Tissier A (2012) Glandular trichomes: what comes after expressed sequence tags? Plant J 70:51–68
McDowell ET, Kapteyn J, Schmidt A, Li C, Kang J-H, Descour A, Shi F, Larson M, Schilmiller A, An L, Jones AD, Pichersky E, Soderlund CA, Gang DR (2011) Comparative functional genomic analysis of solanum glandular trichome Types. Plant Physiol 155:524–539
Mauseth JD (1988) Plant anatomy. Benjamin/Cummings, Menlo Park
van Beilen JB, Poirier Y (2007) Establishment of new crops for the production of natural rubber. Trends Biotechnol 25:522–529
Jayanthy T, Sankaranarayanan P (2005) Measurement of dry rubber content in latex using microwave technique. Meas Sci Rev 5:50–54
Cunningham F (2002) Regulation of carotenoid synthesis and accumulation in plants. Pure Appl Chem 74:1409–1417
Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29:435–445
Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell Online 7:1027–1038
Vishnevetsky M, Ovadis M, Vainstein A (1999) Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci 4:232–235
Deruère J, Römer S, d'Harlingue A, Backhaus RA, Kuntz M, Camara B (1994) Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell Online 6:119–133
Al-Babili S, Hartung W, Kleinig H, Beyer P (1999) CPTA modulates levels of carotenogenic proteins and their mRNAs and affects carotenoid and ABA content as well as chromoplast structure in Narcissus pseudonarcissus flowers. Plant Biol 1:607–612
Vranovà E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5:318–333
Croteau R (1977) Site of monoterpene biosynthesis in Majorana hortensis leaves. Plant Physiol 59:519–520
Croteau R, Felton M, Karp F, Kjonaas R (1981) Relationship of camphor biosynthesis to leaf development in sage (Salvia officinalis). Plant Physiol 67:820–824
Singh N, Luthra R, Sangwan RS (1989) Effect of leaf position and age on the essential oil quantity and quality in lemongrass (Cymbopogon flexuosus)1. Planta Med 55:254–256
Biswas K, Foster A, Aung T, Mahmoud S (2009) Essential oil production: relationship with abundance of glandular trichomes in aerial surface of plants. Acta Physiologiae Plantarum 31:13–19
Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Fäldt J, Miller B, Bohlmann J (2003) (E)-β-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 Online 15:1227–1241
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
Guitton Y, Nicolè F, Moja S, Valot N, Legrand S, Jullien F, Legendre L (2010) Differential accumulation of volatile terpene and terpene synthase mRNAs during lavender (Lavandula angustifolia and L. x intermedia) inflorescence development. Physiol Plant 138:150–163
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 63:2739–2752
Sangwan NS, Farooqi AHA, Shabih F, Sangwan RS (2001) Regulation of essential oil production in plants. J Plant Growth Regul 34:3–21
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
Müller-Schwarze D, Thoss V (2008) Defense on the rocks: low monoterpenoid levels in plants on pillars without mammalian herbivores. J Chem Ecol 34:1377–1381
Opitz S, Kunert G, Gershenzon J (2008) Increased terpenoid accumulation in cotton (Gossypium hirsutum) foliage is a general wound response. J Chem Ecol 34:508–522
Kappers IF, Aharoni A, van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072
Demmig-Adams B, Adams Iii WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26
Bramley PM (2002) Regulation of carotenoid formation during tomato fruit ripening and development. J Exp Bot 53:2107–2113
Li L, Van Eck J (2007) Metabolic engineering of carotenoid accumulation by creating a metabolic sink. Transgenic Res 16:581–585
Li L, Paolillo DJ, Parthasarathy MV, DiMuzio EM, Garvin DF (2001) A novel gene mutation that confers abnormal patterns of β-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J 26:59–67
Lu S, Van Eck J, Zhou X, Lopez AB, O'Halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J, Kochian LV, Küpper H, Earle ED, Cao J, Li L (2006) The cauliflower or gene encodes a DNAj cysteine-rich domain-containing protein that mediates high levels of ß-carotene accumulation. Plant Cell Online 18:3594–3605
Lopez AB, Van Eck J, Conlin BJ, Paolillo DJ, O'Neill J, Li L (2008) Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Exp Bot 59:213–223
Stephanopoulos G (1999) Metabolic fluxes and metabolic engineering. Metab Eng 1:1–11
Naqvi S, Farré G, Sanahuja G, Capell T, Zhu C, Christou P (2010) When more is better: multigene engineering in plants. Trends Plant Sci 15:48–56
Kacser H, Burns JA (1973) The control of flux. Symp Soc Exp Biol 27:65–104
Wiechert W, Möllney M, Petersen S, de Graaf AA (2001) A universal framework for 13C metabolic flux analysis. Metab Eng 3:265–283
Zhu C, Naqvi S, Breitenbach J, Sandmann G, Christou P, Capell T (2008) Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize. Proc Natl Acad Sci 105:18232–18237
Farhi M, Marhevka E, Ben-Ari J, Algamas-Dimantov A, Liang Z, Zeevi V, Edelbaum O, Spitzer-Rimon B, Abeliovich H, Schwartz B, Tzfira T, Vainstein A (2011) Generation of the potent anti-malarial drug artemisinin in tobacco. Nat Biotechnol 29:1072–1074
Daviet L, Schalk M (2010) Biotechnology in plant essential oil production: progress and perspective in metabolic engineering of the terpene pathway. Flavour Frag J 25:123–127
Vranová E, Hirsch-Hoffmann M, Gruissem W (2011) AtIPD: a curated database of arabidopsis isoprenoid pathway models and genes for isoprenoid network analysis. Plant Physiol 156:1655–1660
Ajikumar PK, Xiao W-H, Tyo KEJ, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G (2010) Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330:70–74
Tugizimana F, Steenkamp PA, Piater LA, Dubery IA (2012) Ergosterol-induced sesquiterpenoid synthesis in tobacco cells. Molecules 17:1698–1715
Lange BM, Mahmoud SS, Wildung MR, Turner GW, Davis EM, Lange I, Baker RC, Boydston RA, Croteau RB (2010) Improving peppermint essential oil yield and composition by metabolic engineering. Proc Natl Acad Sci 108:16944–16949
Misawa N (2011) Pathway engineering for functional isoprenoids. Curr Opin Biotechnol 22:627–633
Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602
Nafis T, Akmal M, Ram M, Alam P, Ahlawat S, Mohd A, Abdin M (2011) Enhancement of artemisinin content by constitutive expression of the HMG-CoA reductase gene in high-yielding strain of Artemisia annua L. Plant Biotechnol Rep 5:53–60
Ajikumar PK, Tyo K, Carlsen S, Mucha O, Phon TH, Stephanopoulos G (2008) Terpenoids: opportunities for biosynthesis of natural product drugs using engineered microorganisms. Mol Pharm 5:167–190
Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson BØ (2009) Reconstruction of biochemical networks in microorganisms. Nat Rev Micro 7:129–143
Martin VJJ, Yoshikuni Y, Keasling JD (2001) The in vivo synthesis of plant sesquiterpenes by Escherichia coli. Biotechnol Bioeng 75:497–503
Rodríguez-Villalón A, Pérez-Gil J, Rodríguez-Concepción M (2008) Carotenoid accumulation in bacteria with enhanced supply of isoprenoid precursors by upregulation of exogenous or endogenous pathways. J Biotechnol 135:78–84
Pitera DJ, Paddon CJ, Newman JD, Keasling JD (2007) Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli. Metab Eng 9:193–207
Kim S-W, Keasling JD (2001) Metabolic engineering of the nonmevalonate isopentenyl diphosphate synthesis pathway in Escherichia coli enhances lycopene production. Biotechnol Bioeng 72:408–415
Leonard E, Ajikumar PK, Thayer K, Xiao W-H, Mo JD, Tidor B, Stephanopoulos G, Prather KLJ (2010) Combining metabolic and protein engineering of a terpenoid biosynthetic pathway for overproduction and selectivity control. Proc Natl Acad Sci 107:13654–13659
Vadali RV, Fu Y, Bennett GN, San K-Y (2005) Enhanced lycopene productivity by manipulation of carbon flow to isopentenyl diphosphate in Escherichia coli. Biotechnol Prog 21:1558–1561
Paradise EM, Kirby J, Chan R, Keasling JD (2008) Redirection of flux through the FPP branch-point in Saccharomyces cerevisiae by down-regulating squalene synthase. Biotechnol Bioeng 100:371–378
Alper H, Miyaoku K, Stephanopoulos G (2005) Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat Biotechnol 23:612–616
Huang Q, Roessner CA, Croteau R, Scott AI (2001) Engineering Escherichia coli for the synthesis of taxadiene, a key intermediate in the biosynthesis of taxol. Bioorg Med Chem 9:2237–2242
Misawa N, Nodate M, Otomatsu T, Shimizu K, Kaido C, Kikuta M, Ideno A, Ikenaga H, Ogawa J, Shimizu S, Shindo K (2011) Bioconversion of substituted naphthalenes and β-eudesmol with the cytochrome P450 BM3 variant F87V. Appl Microbiol Biotechnol 90:147–157
Guo F, Zhou W, Zhang J, Xu Q, Deng X (2012) Effect of the citrus lycopene β-cyclase transgene on carotenoid metabolism in transgenic tomato fruits. PLoS One 7:e32221
Rosati C, Aquilani R, Dharmapuri S, Pallara P, Marusic C, Tavazza R, Bouvier F, Camara B, Giuliano G (2000) Metabolic engineering of beta-carotene and lycopene content in tomato fruit. Plant J 24:413–420
D'Ambrosio C, Giorio G, Marino I, Merendino A, Petrozza A, Salfi L, Stigliani AL, Cellini F (2004) Virtually complete conversion of lycopene into β-carotene in fruits of tomato plants transformed with the tomato lycopene β-cyclase (tlcy-b) cDNA. Plant Sci 166:207–214
Fray RG, Wallace A, Fraser PD, Valero D, Hedden P, Bramley PM, Grierson D (1995) Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway. Blackwell, Oxford, Royaume-UNI
Zhang J, Tao N, Xu Q, Zhou W, Cao H, Xu J, Deng X (2009) Functional characterization of Citrus PSY gene in Hongkong kumquat (Fortunella hindsii Swingle). Plant Cell Rep 28:1737–1746
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
Ohara K, Matsunaga E, Nanto K, Yamamoto K, Sasaki K, Ebinuma H, Yazaki K (2010) Monoterpene engineering in a woody plant Eucalyptus camaldulensis using a limonene synthase cDNA. Plant Biotechnol J 8:28–37
Lücker J, Schwab W, van Hautum B, Blaas J, 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 134:510–519
Muñoz-Bertomeu J, Ros R, Arrillaga I, Segura J (2008) Expression of spearmint limonene synthase in transgenic spike lavender results in an altered monoterpene composition in developing leaves. Metab Eng 10:166–177
Schnee C, Köllner 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 103:1129–1134
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 9:103–111
Ohara K, Ujihara T, Endo T, Sato F, Yazaki K (2003) Limonene production in tobacco with Perilla limonene synthase cDNA. J Exp Bot 54:2635–2642
Hohn TM, Ohlrogge JB (1991) Expression of a fungal sesquiterpene cyclase gene in transgenic tobacco. Plant Physiol 97:460–462
Wallaart TE, Bouwmeester HJ, Hille J, Poppinga L, Maijers NCA (2001) Amorpha-4,11-diene synthase: cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin. Planta 212:460–465
Yu X, Jones H, Ma Y, Wang G, Xu Z, Zhang B, Zhang Y, Ren G, Pickett J, Xia L (2012) (E)-β-Farnesene synthase genes affect aphid (Myzus persicae) infestation in tobacco (Nicotiana tabacum). Funct Integr Genomics 12:207–213
Banerjee S, Zehra M, Gupta MM, Kumar S (1997) Agrobacterium rhizogenes-mediated transformation of Artemisia annua: production of transgenic plants. Thieme, Stuttgart/Allemagne
Han J-L, Liu B-Y, Ye H-C, Wang H, Li Z-Q, Li G-F (2006) Effects of overexpression of the endogenous farnesyl diphosphate synthase on the artemisinin content in Artemisia annua L. J Integr Plant Biol 48:482–487
Ma D, Pu G, Lei C, Ma L, Wang H, Guo Y, Chen J, Du Z, Wang H, Li G, Ye H, Liu B (2009) Isolation and characterization of AaWRKY1, an Artemisia annua transcription factor that regulates the amorpha-4,11-diene synthase gene, a key gene of artemisinin biosynthesis. Plant Cell Physiol 50:2146–2161
Chen D-H, Ye H-C, Li G-F (2000) Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci 155:179–185
Chen D-H, Liu C-J, Ye H-C, Li G-F, Liu B-Y, Meng Y-L, Chen X-Y (1999) Ri-mediated transformation of Artemisia annua with a recombinant farnesyl diphosphate synthase gene for artemisinin production. Plant Cell Tissue Organ Cult 57:157–162
Aquil S, Husaini AM, Abdin MZ, Rather GM (2009) Overexpression of the HMG-CoA reductase gene leads to enhanced artemisinin biosynthesis in transgenic Artemisia annua plants. Planta Med 75:1453–1458
Schramek N, Wang H, Römisch-Margl W, Keil B, Radykewicz T, Winzenhörlein B, Beerhues L, Bacher A, Rohdich F, Gershenzon J, Liu B, Eisenreich W (2010) Artemisinin biosynthesis in growing plants of Artemisia annua. A 13CO2 study. Phytochemistry 71:179–187
Alam P, Abdin M (2011) Over-expression of HMG-CoA reductase and amorpha-4,11-diene synthase genes in Artemisia annua L. and its influence on artemisinin content. Plant Cell Rep 30:1919–1928
Wang H, Nagegowda DA, Rawat R, Bouvier-Navé P, Guo D, Bach TJ, Chye M-L (2012) Overexpression of Brassica juncea wild-type and mutant HMG-CoA synthase 1 in Arabidopsis up-regulates genes in sterol biosynthesis and enhances sterol production and stress tolerance. Plant Biotechnol J 10:31–42
Morris WL, Ducreux LJM, Shepherd T, Lewinsohn E, Davidovich-Rikanati R, Sitrit Y, Taylor MA (2011) Utilisation of the MVA pathway to produce elevated levels of the sesquiterpene α-copaene in potato tubers. Phytochemistry 72:2288–2293
Enfissi EMA, Fraser PD, Lois L-M, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3:17–27
Carretero-Paulet L, Cairó A, Botella-Pavía P, Besumbes O, Campos N, Boronat A, Rodríguez-Concepción M (2006) Enhanced flux through the methylerythritol 4-phosphate pathway in Arabidopsis plants overexpressing deoxyxylulose 5-phosphate reductoisomerase. Plant Mol Biol 62:683–695
Kovacs K, Zhang L, Linforth R, Whittaker B, Hayes C, Fray R (2007) Redirection of carotenoid metabolism for the efficient production of taxadiene [taxa-4(5),11(12)-diene] in transgenic tomato fruit. Transgenic Res 16:121–126
Yang T, Stoopen G, Yalpani N, Vervoort J, de Vos R, Voster A, Verstappen FWA, Bouwmeester HJ, Jongsma MA (2011) Metabolic engineering of geranic acid in maize to achieve fungal resistance is compromised by novel glycosylation patterns. Metab Eng 13:414–425
Farhi M, Marhevka E, Masci T, Marcos E, Eyal Y, Ovadis M, Abeliovich H, Vainstein A (2011) Harnessing yeast subcellular compartments for the production of plant terpenoids. Metab Eng 13:474–481
Zhang Y, Teoh KH, Reed DW, Maes L, Goossens A, Olson DJH, Ross ARS, Covello PS (2008) The molecular cloning of artemisinic aldehyde Δ11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J Biol Chem 283:21501–21508
Zhang Y, Nowak G, Reed DW, Covello PS (2011) The production of artemisinin precursors in tobacco. Plant Biotechnol J 9:445–454
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 109:1337–1343
Wu S, Schalk M, Clark A, Miles RB, Coates R, Chappell J (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat Biotechnol 24:1441–1447
Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-Carotene) biosynthetic pathway into (Carotenoid-Free) rice endosperm. Science 287:303–305
Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, Drake R (2005) Improving the nutritional value of golden rice through increased pro-vitamin A content. Nat Biotechnol 23:482–487
Fujisawa M, Takita E, Harada H, Sakurai N, Suzuki H, Ohyama K, Shibata D, Misawa N (2009) Pathway engineering of Brassica napus seeds using multiple key enzyme genes involved in ketocarotenoid formation. J Exp Bot 60:1319–1332
Diretto G, Al-Babili S, Tavazza R, Papacchioli V, Beyer P, Giuliano G (2007) Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoS One 2:e350
Yang T, Stoopen G, Yalpani N, Vervoort J, de Vos R, Voster A, Verstappen FWA, Bouwmeester HJ, Jongsma MA (2005) Metabolic engineering of geranic acid in maize to achieve fungal resistance is compromised by novel glycosylation patterns. Metab Eng 13:414–425
Zeevi V, Liang Z, Arieli U, Tzfira T (2012) Zinc finger nuclease and homing endonuclease-mediated assembly of multigene plant transformation vectors. Plant Physiol 158:132–144
Wani SH, Haider N, Kumar H, Singh N (2010) Plant plastid engineering. Current Genomics 11:500–512
Apel W, Bock R (2009) Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol 151:59–66
Hasunuma T, Takeno S, Hayashi S, Sendai M, Bamba T, Yoshimura S, Tomizawa K-I, Fukusaki E, Miyake C (2008) Overexpression of 1-Deoxy-d-xylulose-5-phosphate reductoisomerase gene in chloroplast contributes to increment of isoprenoid production. J Biosci Bioeng 105:518–526
Kumar S, Hahn FM, Baidoo E, Kahlon TS, Wood DF, McMahan CM, Cornish K, Keasling JD, Daniell H, Whalen MC (2012) Remodeling the isoprenoid pathway in tobacco by expressing the cytoplasmic mevalonate pathway in chloroplasts. Metab Eng 14:19–28
Fraser PD, Romer S, Shipton CA, Mills PB, Kiano JW, Misawa N, Drake RG, Schuch W, Bramley PM (2002) Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci 99:1092–1097
Diretto G, Al-Babili S, Tavazza R, Scossa F, Papacchioli V, Migliore M, Beyer P, Giuliano G (2010) Transcriptional-metabolic networks in β-carotene-enriched potato tubers: the long and winding road to the golden phenotype. Plant Physiol 154:899–912
Stålberg K, Lindgren O, Ek B, Höglund A-S (2003) Synthesis of ketocarotenoids in the seed of Arabidopsis thaliana. Plant J 36:771–779
Memelink J, Gantet P (2007) Transcription factors involved in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Phytochem Rev 6:353–362
Toledo-Ortiz G, Huq E, Rodríguez-Concepción M (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc Natl Acad Sci 107:11626–11631
Jones MO, Piron-Prunier F, Marcel F, Piednoir-Barbeau E, Alsadon AA, Wahb-Allah MA, Al-Doss AA, Bowler C, Bramley PM, Fraser PD, Bendahmane A (2012) Characterisation of alleles of tomato light signalling genes generated by TILLING. Phytochemistry 79:78–86
Feng S, Jacobsen SE (2011) Epigenetic modifications in plants: an evolutionary perspective. Curr Opin Plant Biol 14:179–186
Cazzonelli CI, Yin K, Pogson BJ (2009) Potential implications for epigenetic regulation of carotenoid biosynthesis during root and shoot development. Plant Signal Behav 4:339–341
Enfissi EMA, Barneche F, Ahmed I, Lichtlé C, Gerrish C, McQuinn RP, Giovannoni JJ, Lopez-Juez E, Bowler C, Bramley PM, Fraser PD (2010) Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell Online 22:1190–1215
Davuluri GR, van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Bramley PM, Pennings HMJ, Bowler C (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23:890–895
Benvenuto G, Formiggini F, Laflamme P, Malakhov M, Bowler C (2002) The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Curr Biol 12:1529–1534
Liu Y, Koornneef M, Soppe WJJ (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell Online 19:433–444
Chinnusamy V, Gong Z, Zhu J-K (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195
Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952
Giliberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, Bramley PM, Fiore A, Tavazza M, Giuliano G (2005) Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol 137:199–208
Davuluri GR, van Tuinen A, Mustilli AC, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Pennings HMJ, Bowler C (2004) Manipulation of DET1 expression in tomato results in photomorphogenic phenotypes caused by post-transcriptional gene silencing. Plant J 40:344–354
Wei S, Li X, Gruber MY, Li R, Zhou R, Zebarjadi A, Hannoufa A (2009) RNAi-mediated suppression of DET1 alters the levels of carotenoids and sinapate esters in seeds of Brassica napus. J Agric Food Chem 57:5326–5333
Wei S, Yu B, Gruber MY, Khachatourians GG, Hegedus DD, Hannoufa A (2010) Enhanced seed carotenoid levels and branching in transgenic Brassica napus expressing the Arabidopsis miR156b gene. J Agric Food Chem 58:9572–9578
Wang E, Wagner G (2003) Elucidation of the functions of genes central to diterpene metabolism in tobacco trichomes using posttranscriptional gene silencing. Planta 216:686–691
Ennajdaoui H, Vachon G, Giacalone C, Besse I, Sallaud C, Herzog M, Tissier A (2010) Trichome specific expression of the tobacco (Nicotiana sylvestris) cembratrien-ol synthase genes is controlled by both activating and repressing cis-regions. Plant Mol Biol 73:673–685
Gutiérrez-Alcalá G, Calo L, Gros F, Caissard J-C, Gotor C, Romero LC (2005) A versatile promoter for the expression of proteins in glandular and non-glandular trichomes from a variety of plants. J Exp Bot 56:2487–2494
Nagel J, Culley LK, Lu Y, Liu E, Matthews PD, Stevens JF, Page JE (2008) EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell Online 20:186–200
Chow K-S, Wan K-L, Isa MNM, Bahari A, Tan S-H, Harikrishna K, Yeang H-Y (2007) Insights into rubber biosynthesis from transcriptome analysis of Hevea brasiliensis latex. J Exp Bot 58:2429–2440
Ponciano G, McMahan CM, Xie W, Lazo GR, Coffelt TA, Collins-Silva J, Nural-Taban A, Gollery M, Shintani DK, Whalen MC (2012) Transcriptome and gene expression analysis in cold-acclimated guayule (Parthenium argentatum) rubber-producing tissue. Phytochemistry 79:57–66
Nieuwenhuizen NJ, Green S, Atkinson RG (2010) Floral sesquiterpenes and their synthesis in dioecious kiwifruit. Plant Signal Behav 5:61–63
Shiba Y, Paradise EM, Kirby J, Ro D-K, Keasling JD (2007) Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab Eng 9:160–168
Ro D-K, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MCY, Withers ST, Shiba Y, Sarpong R, Keasling JD (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:940–943
Takahashi S, Yeo Y, Greenhagen BT, McMullin T, Song L, Maurina-Brunker J, Rosson R, Noel JP, Chappell J (2007) Metabolic engineering of sesquiterpene metabolism in yeast. Biotechnol Bioeng 97:170–181
Télef N, Stammitti-Bert L, Mortain-Bertrand A, Maucourt M, Carde J, Rolin D, Gallusci P (2006) Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs. Plant Mol Biol 62:453–469
Flores-Pérez Ú, Pérez-Gil J, Closa M, Wright LP, Botella-Pavía P, Phillips MA, Ferrer A, Gershenzon J, Rodríguez-Concepción M (2010) PLEIOTROPIC REGULATORY LOCUS 1 (PRL1) integrates the regulation of sugar responses with isoprenoid metabolism in Arabidopsis. Mol Plant 3:101–112
Paetzold H, Garms S, Bartram S, Wieczorek J, Urós-Gracia E-M, Rodríguez-Concepción M, Boland W, Strack D, Hause B, Walter MH (2010) The isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 controls isoprenoid profiles, precursor pathway allocation, and density of tomato trichomes. Mol Plant 3:904–916
Acknowledgments
We wish to thank Dr Sophie Colombié for critical reading of this manuscript. Dr Anne Pribat was in receipt of a grant from the French National Research Agency (ANR) in the frame of the “Polyterp” project.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this entry
Cite this entry
Pribat, A. et al. (2013). Metabolic Engineering of Isoprenoid Biosynthesis. In: Ramawat, K., Mérillon, JM. (eds) Natural Products. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22144-6_126
Download citation
DOI: https://doi.org/10.1007/978-3-642-22144-6_126
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-22143-9
Online ISBN: 978-3-642-22144-6
eBook Packages: Chemistry and Materials ScienceReference Module Physical and Materials ScienceReference Module Chemistry, Materials and Physics