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 the recent results with terpenoid engineering, showing 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 localization 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 behavior
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References
Adam, KP, and Zapp, J, 1998, Biosynthesis of the isoprene units of chamomile sesquiterpenes, Phytochemistry 48(6):953–959.
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(12):2866–2884.
Aharoni, A, Jongsma, MA, and Bouwmeester, HJ, 2005, Volatile science? Metabolic engineering of terpenoids in plants, Trends Plant Sci 10(12):594–602.
Aharoni, A, Jongsma, MA, Kim, TY, Ri, MB, Giri, AP, Verstappen, FWA, Schwab, W, and Bouwmeester, HJ, 2006, Metabolic engineering of terpenoid biosynthesis in plants, Phytochemistry Rev:In Press.
Baldwin, IT, 2001, An ecologically motivated analysis of plant-herbivore interactions in native tobacco, Plant Physiol 127(4):1449–1458.
Bertea, CM, Schalk, M, Karp, F, Maffei, M, and Croteau, R, 2001, Demonstration that menthofuran synthase of mint (Mentha) is a cytochrome P450 monooxygenase: Cloning, functional expression, and characterization of the responsible gene, Arch Biochem Biophys 390(2):279–286.
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.
Bewley, JD, 1997, Seed germination and dormancy, Plant Cell 9(7):1055–1066.
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, Arch Biochem Biophys 415(2):146–154.
Bosabalidis, AM, 1996, Ontogenesis, ultrastructure and morphometry of the petiole oil ducts of celery (Apium graveolens L), Flavour Frag J 11(5):269–274.
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(2):188–199.
Bouwmeester, HJ, Gershenzon, J, Konings, MCJM, and Croteau, R, 1998, Biosynthesis of the monoterpenes limonene and carvone in the fruit of carawayIDemonstration of enzyme activities and their changes with development, Plant Physiol 117(3):901–912.
Bouwmeester, HJ, Verstappen, FWA, Posthumus, MA, and Dicke, M, 1999, Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima beanThe first dedicated step in acyclic C11-homoterpene biosynthesis, Plant Physiol 121(1):173–180.
Bouwmeester, HJ, Kappers, IF, Verstappen, FW, Aharoni, A, Luckerhoff, LLP, Lücker, J, Jongsma, MA, and Dicke, M, 2003, Exploring multi-trophic plant-herbivore interactions for new crop protection methods, in The International Congress Crop Science and Technology, British Crop Protection Council, Alton, UK, Glasgow, 1123–1134.
Broun, P, 2004, Transcription factors as tools for metabolic engineering in plants, Curr Opin Plant Biol 7(2):202–209.
Capell, T, and Christou, P, 2004, Progress in plant metabolic engineering, Curr Opin Biotech 15(2):148–154.
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(4):1337–1343.
Chappell, J, 2002, The genetics and molecular genetics of terpene and sterol origami, Curr Opin Plant Biol 5(2):151–157.
Chappell, J, 2004, Valencene synthase – a biochemical magician and harbinger of transgenic aromas, Trends Plant Sci 9(6):266–269.
Chen, DH , Ye, HC, and Li, GF, 2000, Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua Ltransgenic plants via Agrobacterium tumefaciens-mediated transformation, Plant Sci 155(2):179–185.
Dicke, M, and van Loon, JJA, 2000, Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context, Entomol Exp Appl 97(3):237–249.
Diemer, F, Caissard Jean, C, Moja, S, Chalchat Jean, C, and Jullien, F, 2001, Altered monoterpene composition in transgenic mint following the introduction of 4S-limonene synthase, Plant Physiol Bioch 39(7–8):603–614.
Dudareva, N, Cseke, L, Blanc, VM, and Pichersky, E, 1996, Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the Cbreweri flower, Plant Cell 8(7):1137–1148.
Dudareva, N, Pichersky, E, and Gershenzon, J, 2004, Biochemistry of Plant Volatiles, Plant Physiol 135(4):1893–1902.
Dudareva, N, Andersson, S, Orlova, I, Gatto, N, Reichelt, M, Rhodes, D, Boland, W, and Gershenzon, J, 2005, The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers, P Natl Acad Sci USA 102(3):933–938.
El Tamer, MK, Smeets, M, Holthuysen, N, Lücker, J, Tang, A, Roozen, J, Bouwmeester, HJ, and Voragen, AGJ, 2003, The influence of monoterpene synthase transformation on the odour of tobacco, J Biotechnol 106(1):15–21.
Estevez, JM, Cantero, A, Reindl, A, Reichler, S, and Leon, P, 2001, 1-deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants, J Biol Chem 276(25):22901–22909.
Fahn, A, 1979, Secretory Tissues in Plants, Academic Press, London, pp 302.
Fray, RG, Wallace, A, Fraser, PD, Valero, D, Hedden, P, Bramley, PM, and Grierson, D, 1995, Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway, Plant J 8(5):693–701.
Galili, G, Galili, S, Lewinsohn, E, and Tadmor, Y, 2002, Genetic, molecular, and genomic approaches to improve the value of plant foods and feeds, Crit Rev Plant Sci 21(3):167–204.
Gershenzon, J, Maffei, M, and Croteau, R, 1989, Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata), Plant Physiol 89(4):1351–1357.
Gershenzon, J, and Croteau, RB, 1993, Terpenoid biosynthesis: the basic pathway and formation of monoterpenes, sesquiterpenes and diterpenes, in: Lipid metabolism in plants, Moore, TS, ed, CRC Press, Boca Raton, pp 340–388.
Gershenzon, J, McConkey, ME, and Croteau, RB, 2000, Regulation of monoterpene accumulation in leaves of peppermint, Plant Physiol 122(1):205–214.
Han, JL, Liu, BY, Ye, HC, Wang, H, Li, ZQ, and Li, GF, 2006, Effects of overexpression of the endogenous farnesyl diphosphate synthase on the artemisinin content in Artemisia annua L, Journal of Integrative Plant Biology 48(4):482–487.
Harker, M, Hellyer, A, Clayton, JC, Duvoix, A, Lanot, A, and Safford, R, 2003, Co-ordinate regulation of sterol biosynthesis enzyme activity during accumulation of sterols in developing rape and tobacco seed, Planta 216(4):707–715.
Haudenschild, C, and Croteau, R, 1998, Molecular engineering of monoterpene production, Genet Eng 20:267–280.
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(29):26666–26676.
Hohn, TM, and Ohlrogge, JB, 1991, Expression of a fungal sesquiterpene cyclase gene in transgenic tobacco, Plant Physiol 97(1):460–462.
Hori, M, 1998, Repellency of rosemary oil against Myzus persicae in a laboratory and in a screenhouse, J Chem Ecol 24(9):1425–1432.
Izumi, S, Takashima, O, and Hirata, T, 1999, Geraniol is a potent inducer of apoptosis-like cell death in the cultured shoot primordia of Matricaria chamomilla, Biochem Biophys Res Commun 259(3):519–522.
Jacobson, M, 1982, Plants, insects, and man – their interrelationships, Econ Bot 36(3):346–354.
Jongsma, MA, 2004, Novel genes for control and deterrence of sucking insect pests, in ISB News Report, November, 1–4 http://wwwisbvtedu/news/2004/Nov04pdf.
Kappers, IF, Aharoni, A, van Herpen, T, Luckerhoff, LLP, Dicke, M, and Bouwmeester, HJ, 2005, Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis, Science 309(5743):2070–2072.
Krasnyanski, S, May, RA, Loskutov, A, Ball, TM, and Sink, KC, 1999, Transformation of the limonene synthase gene into peppermint (Mentha x piperita L) and preliminary studies on the essential oil profiles of single transgenic plants, Theor Appl Genet 99(3–4):676–682.
Laule, O, Furholz, A, Chang, HS, Zhu, T, Wang, X, Heifetz, PB, Gruissem, W, and Lange, BM, 2003, Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana, P Natl Acad Sci USA 100(11):6866–6871.
Lavy, M, Zuker, A, Lewinsohn, E, Larkov, O, Ravid, U, Vainstein, A, and Weiss, D, 2002, Linalool and linalool oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene, Mol Breeding 9(2):103–111.
Lewinsohn, E, Schalechet, F, Wilkinson, J, Matsui, K, Tadmor, Y, Nam, KH, Amar, O, Lastochkin, E, Larkov, O, Ravid, U, Hiatt, W, Gepstein, S, and Pichersky, E, 2001, Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits, Plant Physiol 127(3):1256–1265.
Little, DB, and Croteau, RB, 1999, Biochemistry of essential oil terpenes – A thirty year overview, in: Flavor Chemistry: 30 Years of Progress, Teranishi, R, and Wick, EL, ed, Kluwer Academic/ Plenum Publishers, New York, pp 239–253.
Lücker, J, Bouwmeester, HJ, Schwab, W, Blaas, J, van der Plas, LHW, and 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(4):315–324.
Lücker, J, 2002, Metabolic Engineering of Monoterpene Biosynthesis in Plants, PhD Thesis, Wageningen University, pp 168.
Lücker, J, El Tamer, MK, Schwab, W, Verstappen, FWA, van der Plas, LHW, Bouwmeester, HJ, and Verhoeven, HA, 2002, Monoterpene biosynthesis in lemon (Citrus limon): cDNA isolation and functional analysis of four monoterpene synthases, Eur J Biochem 269(13):3160–3171.
Lücker, J, Schwab, W, van Hautum, B, Blaas, J, van der Plas, LHW, Bouwmeester, HJ, and Verhoeven, HA, 2004a, Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon, Plant Physiol 134(1):510–519.
Lücker, J, Schwab, W, Franssen, MCR, van der Plas, LHW, Bouwmeester, HJ, and Verhoeven, HA, 2004b, Metabolic engineering of monoterpene biosynthesis: Two-step production of (+)-trans-isopiperitenol by tobacco, Plant J 39(1):135–145.
Lücker, J, Verhoeven, HA, van der Plas, LHW, and Bouwmeester, HJ, 2006, Molecular engineering of floral scent, in: Biology of Floral Scent, Dudareva, N, and Pichersky, E, ed, CRC Press, Boca Raton, pp 321–337.
Mahmoud, SS, and Croteau, R, 2001, Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase, P Natl Acad Sci USA 98(15):8915–8920.
Mahmoud, SS, and Croteau, RB, 2002, Strategies for transgenic manipulation of monoterpene biosynthesis in plants, Trends Plant Sci 7(8):366–373.
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(5):547–554.
Masferrer, A, Arro, M, Manzano, D, Schaller, H, Fernandez-Busquets, X, Moncalean, P, Fernandez, B, Cunillera, N, Boronat, A, and Ferrer, A, 2002, Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels, Plant J 30(2):123–132.
McCaskill, D, and Croteau, R, 1998, Some caveats for bioengineering terpenoid metabolism in plants, Trends Biotechnol 16(8):349–355.
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(393):2635–2642.
Outchkourov, NS, Peters, J, de Jong, J, Rademakers, W, and Jongsma, MA, 2003, The promoter-terminator of chrysanthemum rbcS1 directs very high expression levels in plants, Planta 216(6):1003–1012.
Pichersky, E, and Gershenzon, J, 2002, The formation and function of plant volatiles: perfumes for pollinator attraction and defense, CurrOpinPlant Biol 5(3):237–243.
Rodriguez-Concepcion, M, and Boronat, A, 2002, Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastidsA metabolic milestone achieved through genomics, Plant Physiol 130(3):1079–1089.
Romagni, JG, Allen, SN, and Dayan, FE, 2000, Allelopathic effects of volatile cineoles on two weedy plant species, J Chem Ecol 26(1):303–313.
Sacchettini, JC, and Poulter, CD, 1997, Biochemistry – Creating isoprenoid diversity, Science 277(5333):1788–1789.
Sandmann, G, Romer, S, and Fraser, PD, 2006, Understanding carotenoid metabolism as a necessity for genetic engineering of crop plants, Metabol Eng 8(4):291–302.
Schaller, H, Grausem, B, Benveniste, P, Chye, ML, Tan, CT, Song, CT, and Chua, NH, 1995, Expression of the Hevea brasiliensis (HBK) MullArg 3-hydroxy-3-methylglutaryl-Coenzyme A reductase 1 in tobacco results in sterol overproduction, Plant Physiol 109(3):761–770.
Schnee, C, Kollner, TG, Held, M, Turlings, TCJ, Gershenzon, J, and Degenhardt, J, 2006, The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores, P Natl Acad Sci USA 103(4):1129–1134.
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, Phytochemistry Rev 2(1–2):3–16.
Suga, T, and Hirata, T, 1990, Biotransformation of exogenous substrates by plant cell cultures, Phytochemistry 29(8):2393–2406.
van Poecke, RMP, Posthumus, MA, and 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(10):1911–1928.
Vaughn, SF, and Spencer, GF, 1991, Volatile monoterpenes inhibit potato tuber sprouting, Am Potato J 68(12):821–831.
Vaughn, SF, and Spencer, GF, 1996, Synthesis and herbicidal activity of modified monoterpenes structurally similar to cimmethylin, Weed Sci 44(1):7–11.
Verlet, N, 1993, Commercial aspects, in: Volatile Oil Crops: their Biology, Biochemistry, and Production, Hay, RKM, and Waterman, PG, ed, Longman Scientific & Technical, Essex, UK, pp 137–174.
Wallaart, TE, 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(3):460–465.
Wang, E, Hall, JT, and Wagner, GJ, 2004, Transgenic Nicotiana tabacum L with enhanced trichome exudate cembratrieneols has reduced aphid infestation in the field, Mol Breeding 13(1):49–57.
Wang, EM, Wang, R, De Parasis, J, Loughrin, JH, Gan, SS, and Wagner, GJ, 2001, Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance, Nat Biotechnol 19(4):371–374.
Weidenhamer, JD, Macias, FA, Fischer, NH, and Williamson, GB, 1993, Just how insoluble are monoterpenes? J Chem Ecol 19(8):1799–1807.
Weissbecker, B, Schutz, S, Klein, A, and Hummel, HE, 1997, Analysis of volatiles emitted by potato plants by means of a Colorado beetle electroantennographic detector, Talanta 44(12):2217–2224.
Wolfertz, M, Sharkey, TD, Boland, W, and Kuhnemann, F, 2004, Rapid regulation of the methylerythritol 4-phosphate pathway during isoprene synthesis, Plant Physiol 135(4):1939–1945.
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Lücker, J., Bouwmeester, H.J., Aharoni, A. (2007). Metabolic Engineering of Terpenoid Biosynthesis in Plants. In: Verpoorte, R., Alfermann, A., Johnson, T. (eds) Applications of Plant Metabolic Engineering. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6031-1_9
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