Abstract
Metabolic engineering of terpenoids in plants is a fascinating research topic from two main perspectives. On the one hand, the various biological activities of these compounds make their engineering a new tool for improving a considerable number of traits in crops. These include for example enhanced disease resistance, weed control by producing allelopathic compounds, better pest management, production of medicinal compounds, increased value of ornamentals and fruit and improved pollination. On the other hand, the same plants altered in the profile of terpenoids and their precursor pools make a most important contribution to fundamental studies on terpenoid biosynthesis and its regulation. In this review we describe our recent results with terpenoid engineering, focusing on two terpenoid classes the monoterpenoids and sesquiterpenoids. The emerging picture is that engineering of these compounds and their derivatives in plant cells is feasible, although with some requirements and limitations. For example, in terpenoid engineering experiments crucial factors are the subcellular localisation of both the precursor pool and the introduced enzymes, the activity of endogenous plant enzymes which modify the introduced terpenoid skeleton, the costs of engineering in terms of effects on other pathways sharing the same precursor pool and the phytotoxicity of the introduced terpenoids. Finally, we will show that transgenic plants altered in their terpenoid profile exert novel biological activities on their environment, for example influencing insect behaviour.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- DMADP:
-
dimethylallyl diphosphate
- FDP:
-
farnesyl diphosphate
- GDP:
-
geranyl diphosphate
- GGDP:
-
geranylgeranyl diphosphate
- IDP:
-
isopentenyl diphosphate
- MEP:
-
methylerythritol 4-phosphate
- TPSs:
-
terpene synthases
References
Aharoni A, Giri AP, Deuerlein S, Griepink F, de-Kogel W-J, Verstappen FWA, Verhoeven HA, Jongsma MA, Schwab W and Bouwmeester HJ (2003). Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15: 2866–2884
Aharoni A, Giri AP, Verstappen FW, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W and Bouwmeester HJ (2004). Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16: 3110–3131
Besumbes O, Sauret-Gueto S, Phillips MA, Imperial S, Rodriguez-Concepcion M and Boronat A (2004). Metabolic engineering of isoprenoid biosynthesis in Arabidopsis for the production of taxadiene, the first committed precursor of taxol. Biotechnol. Bioeng. 88(2): 168–175
Bick JA and Lange BM (2003). Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arc. Biochem. Biophys. 415: 146–154
Botella-Pavia P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A and Rodriguez-Concepcion M (2004). Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J. 40: 188–199
Bouwmeester HJ, Verstappen FWA, Posthumus MA and Dicke M (1999). Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean The first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiol. 121: 173–180
Carretero-Paulet L, Ahumada I, Cunillera N, Rodriguez-Concepcion M, Ferrer A, Boronat A and Campos N (2002). Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-d-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-c-methyl-d-erythritol 4-phosphate pathway. Plant Physiol. 129: 1581–1591
Chappell J, Wolf F, Proulx J, Cuellar R and 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
Chen F, Tholl D, D’Auria JC, Farooq A, Picherskey E and Gershenzon J (2003). Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15: 481–494
Crock J, Wildung M and Croteau R (1997). Isolation and bacterial expression of a sesquiterpene synthase cDNA clone from peppermint (Mentha × piperita L.) that produces the aphid alarm pheromone (E)- β - farnesene. Proc. Natl. Acad. Sci. USA 94: 12833–12838
D’Auria JC and Gershenzon J (2005). The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr. Opin. Plant Biol. 8: 308–316
Degenhardt J, Kollner T, Schnee C, Held M, Rasman S, Turlings TCJ & Gershenzon J. (2005). The role of maize sesquiterpene hydrocarbons as signals in multitrophic interaction. Book of Abstracts, Terpnet 2005 meeting, Wageningen, The Netherlands, p. 49
Diemer F, Caissard J-C, Moja S, Chalchat J-C and Jullien F (2001). Altered monoterpene composition in transgenic mint following the introduction of 4S-limonene synthase. Plant Physiol. Biochem. 39: 603–614
Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W and Gershenson J (2005). The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc. Natl. Acad. Sci. USA 102: 933–938
Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Kagan IA, Grosdemange-Billiard C, Rohmer M and 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
Hohn TM and Ohlrogge JB (1991). Expression of a fungal sesquiterpene cyclase gene in transgenic tobacco. Plant Physiol. 97: 460–462
Kappers IF, Aharoni A, Luckerhoff LLP, Dicke M, Bouwmeester HJ and Herpen TWJM (2005). Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309: 2070–2072
Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W and Lange M (2003). Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100: 6866–6871
Lavy M, Zuker A, Lewinsohn E, Larkov O, Ravid U, Vainstein A and Weiss D (2002). Linalool and linallol oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene. Mol. Breeding 9: 103–111
Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Hee Nam K, Amar O, Lastochkin E, Larkov O, Ravid U, Hiatt W, Gepstein S and Picherskey E (2001). Enhanced levels of the aroma and flavor compound s-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol. 127: 1256–1265
Lucker J, Bouwmeester HJ, Schwab W, Blaas J, Verhoeven HA and Plas LHW (2001). Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-β-d-glycopyranoside. Plant J 27: 315–324
Lucker J, Schwab W, Franssen MCR, Bouwmeester HJ, Verhoeven HA and Plas LHW (2004a). Metabolic engineering of terpenoid biosynthesis in tobacco using monoterpene synthases and a cytochrome P450 hydroxylase. Plant J. 39: 135–145
Lucker J, Schwab W, Blaas J, Bouwmeester HJ and Verhoeven HA (2004b). Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon. Plant Physiol. 134: 510–519
Mahmoud SS and 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. USA 98: 8915–8920
Mahmoud SS, Williams M and Croteau R (2004). Cosuppression of limonene-3-hydroxylase in peppermint promotes accumulation of limonene in the essential oil. Phytochemistry 65: 547–554
Martin VJJ, Pitera DJ, Withers ST, Newman JD and Keasling JD (2003). Engineering the mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol. 21: 1–7
McCaskill D and Croteau R (1998). Some caveats for bioengineering terpenoid metabolism in plants. Trends Biotechnol. 16: 349–354
Ohara K, Ujihara T, Endo T, Sato F and Yazaki K (2003). Limonene production in tobacco with Perilla limonene synthase cDNA. J. Exp. Bot. 54: 2635–2642
Pichersky E and Gershenzon J (2002). The formation and function of plant volatiles: perfumes for polliator attraction and defense. Curr. Opin. Plant Biol. 5: 237–243
Schuhr CA, Radykewicz T, Sagner S, Latzel C, Zenk MH, Arigoni D, Bacher A, Rohdich F and Eisenreich W (2003). Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy. Phytochem. Rev. 2: 3–16
Steele CL, Crock J, Bohlmann J and Croteau R (1998). Sesquiterpene Synthases from Grand Fir (Abies grandis). J. Biol. Chem. 273: 2078–2089
Tholl D, Chen F, Petri J, Gershenzon J and Pichersky E (2005). Two sesquiterpene synthses are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J. 42: 757–771
Wallaart ET, Bouwmeester HJ, Hille J, Poppinga L and 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
Wang E, Wang R, DeParasis J, Loughrin JH, Gan S and Wagner GJ (2001). Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat. Biotechnol. 19: 71–374
Author information
Authors and Affiliations
Corresponding author
Additional information
A. Aharoni is an Incumbent of the Adolfo and Evelyn Blum Career Development chair
Rights and permissions
Open Access This is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License ( https://creativecommons.org/licenses/by-nc/2.0 ), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
About this article
Cite this article
Aharoni, A., Jongsma, M.A., Kim, TY. et al. Metabolic Engineering of Terpenoid Biosynthesis in Plants. Phytochem Rev 5, 49–58 (2006). https://doi.org/10.1007/s11101-005-3747-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-005-3747-3