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Metabolic Engineering of Terpenoid Biosynthesis in Plants

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Metabolic Engineering of Terpenoid Biosynthesis in Plants Phytochemistry Reviews (2006) 5: 49–58 Ó Springer 2006 DOI 10.1007/s11101-005-3747-3 Metabolic engineering of terpenoid biosynthesis in plants Asaph Aharoni1,*, , Maarten A. Jongsma2, Tok-Yong Kim2,4, Man-Bok Ri2,4, Ashok P. Giri2,5, Francel W. A. Verstappen2, Wilfried Schwab3 & Harro J. Bouwmeester2 1Weizmann Institute of Science, 26 Rehovot 76100 Israel; 2Plant Research International, 16 6700 AA Wageningen The Netherlands; 3Biomolecular Food Technology, TU Mu¨nchen, Lise-Meitner-Str. 3485354 Freising, Mu¨nchen Germany; 4Research Institute of Agrobiology, Academy of Agricultural Sciences, Ryongsong Pyongyang, Democratic People’s Republic of Korea; 5Plant Molecular Biology Unit, Division of Biochemical Sciences, National Chemical Laboratory, Dr Homi Bhabha Road, Pune 411008 India; *Author for correspondence (Tel: +0972-(0)8-9343643; Fax: +0972-(0)8-9344181; E-mail: asaph.aharoni@ weizmann.ac.il) Key words: linalool, MEP pathway, mevalonate pathway, monoterpene, sesquiterpene 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 contri- bution 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 ses- quiterpenoids. 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 phyto- toxicity 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. Abbreviations: DMADP – dimethylallyl diphosphate; FDP – farnesyl diphosphate; GDP – geranyl diphosphate; GGDP – geranylgeranyl diphosphate; IDP – isopentenyl diphosphate; MEP – methylerythritol 4-phosphate; TPSs – terpene synthases. Introduction agents, pharmaceuticals, perfumes, insecticides and anti-microbial agents (Martin et al., 2003). In Terpenoids are the most structurally varied class nature, they play significant roles in plant–envi- of plant natural products. They are commercially ronment interactions, plant–plant communication important due to their wide application in a vast and plant–insect and plant–animal interactions number of industrial products such as flavouring (Pichersky and Gershenzon, 2002). Although A. Aharoni is an Incumbent of the Adolfo and Evelyn Blum Career Development chair. 50 many of them are associated with primary terpenoid structures (Lucker et al., 2001). Terpe- metabolism (e.g. the phytol side chain of chloro- noid biosynthesis occurs in the cytosol and the phyll, carotenoid pigments, and the plant hormone plastids (Figure 1). IDP and DMADP are synthe- gibberellin) others are typical plant secondary sized through the 2-methylerythritol 4-phosphate metabolites. pathway (MEP) via deoxy-D-xylulose 5-phosphate All terpenoids are synthesized through the in plastids. However, IDP is also synthesized in the condensation of isopentenyl diphosphate (IDP) cytosol via the mevalonate pathway (Bick and and its allylic isomer dimethyl allyl diphos- Lange, 2003). It is generally accepted that GDP phate (DMADP) (Carretero-Paulet et al., 2002). and GGDP in the plastids are used as substrate for The sequential head-to-tail addition of IDP units monoterpene and diterpene biosynthesis, respec- to DMADP yields the prenyl diphosphates geranyl tively whereas FDP in the cytosol is used for ses- diphosphate (GDP), farnesyl diphosphate quiterpene biosynthesis (Figure 1). (FDP) and geranylgeranyl diphosphate (GGDP) Why would we like to engineer terpenoid pro- (Figure 1). These three components serve as pre- duction in plants? Primarily, plants engineered for cursors for the monoterpenes, sesquiterpenes and their terpenoid profile could serve as a tool for diterpenes, respectively. Terpenoid synthases or improving a large number of traits in different cyclases catalyze the reactions in which the pri- crop species. Examples for such traits are mary terpene skeletons are formed from these enhanced disease resistance, weed control by pro- substrates. The parent skeletal type of mono-, ducing allelopathic compounds, improved pest sesqui- and diterpenes is normally further modified control, increased value of ornamentals and fruit by the activity of an array of different enzymes (fragrance and flavour) and improved pollination (e.g. hydroxylases, dehydrogenases, reductases and by altering scent profiles. In addition, large-scale glycosyl, methyl and acyl transferases) which to- production of terpenoids in plants, either for gether generate the many thousands of different medicinal uses or for other industries such as Figure 1. The mevalonate and MEP pathways producing different terpenoid classes in the cytosol and plastids, respectively. GA3P, D-glyceraldehyde-3-phosphate; TPSs, terpene synthases; IDP, isopentenyl diphosphate; DMADP, dimethylallyl diphosphate; FDP, farnesyl diphosphate; MEP, methylerythritol 4-phosphate; GDP, geranyl diphosphate; GGDP, geranylgeranyl diphosphate. Broken arrows represent multiple enzymatic steps. 51 cosmetics and food would be attractive. A second, The FaNES1 protein as a ‘sensor’ for both but not less important reason is that plants altered mono- and sesquiterpene precursors in the profile of terpenoids (and pool of precur- sors) make an important contribution to funda- We chose the strawberry FaNES1 (Fragaria anan- mental studies on their biosynthesis and assa Nerolidol Synthase 1) gene for performing regulation. For example, metabolic engineering metabolic engineering experiments in several plant experiments often reveal undiscovered branches to species (Aharoni et al., 2004). The recombinant an already known metabolic pathway or point to FaNES1 protein was previously shown to catalyze feedback loops within a pathway or between the conversion of GDP and FDP to (S)-linalool pathways. and (3S)-(E)-nerolidol, respectively with equal In recent years attempts to produce high levels efficiency. The ability of other recombinant terpene of monoterpenes in transgenic plants have been synthases to generate both sesquiterpenes and successful. Several different plant species were monoterpenes was already observed earlier (Crock engineered, mainly by overexpressing terpene et al., 1997; Steele et al., 1998). However, in these synthases under constitutive promoters. Petunia, cases the recombinant enzyme could generate the tomato, carnation, potato and Arabidopsis plants sesquiterpene with high efficiency while a combi- were generated that over-expressed genes encoding nation of monoterpenes would be formed from linalool synthases. Such plants produced and GDP but with low efficiency. FaNES1 could emitted the monoterpene linalool and its glycosy- therefore serve as an excellent ‘sensor’ for levels of lated or hydroxylated derivatives (Lewinson et al., both monoterpene and sesquiterpene precursors in 2001; Lucker et al., 2001; Lavy et al., 2002; the cell or even, as will be described later in this Aharoni et al., 2003). Mint and tobacco plants report, in a specific sub-cellular compartment. expressing limonene, c-terpinene and a-pinene synthases were also altered in their terpenoid Engineering monoterpenoids in Arabidopsis plants profile (Diemer et al., 2001; Lucker et al., 2004b). Levels of terpenoid precursors could also be ele- Recent research in Arabidopsis revealed that what vated by overexpressing genes encoding enzymes at first seemed a metabolically simple plant species from various steps of the MEP pathway (DXR and is in reality a reasonable producer of secondary HDR) (Mahmoud and Croteau, 2001; Botella- metabolites (D’Auria and Gershenzon, 2005). For Pavia et al., 2004). In addition, genes encoding example, nearly two dozen monoterpenes and ses- enzymes which modify monoterpene structures quiterpenes are emitted from its flowers (Aharoni have been successfully over-expressed or knocked et al., 2003; Chen et al., 2003; Tholl et al., 2005). down in tobacco and mint (Mahmoud and Leaves of Arabidopsis on the other hand emit only Croteau, 2001; Wang et al., 2001; Lucker et al., traces of one monoterpene, limonene. Transgenic 2004a; Mahmoud et al., 2004). In conclusion, in Arabidopsis plants were raised which expressed the many studies it was demonstrated that it is feasible FaNES1 gene driven by the CaMV 35S promoter. to engineer several steps of the monoterpenoid The FaNES1 protein was targeted to the plastids pathway. However, attempts to engineer sesquit- by fusing the wild strawberry FvNES1 (Fragaria erpenes in plants using terpene synthases resulted vesca Nerolidol Synthase 1) plastid
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