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References
Kubeczka KH (2010) History and sources of essential oil research. In: Baser KHC, Buchbauer G (eds) Handbook of essential oils: science, technology, and applications. CRC Press/Taylor & Francis, Boca Raton, pp 3–38
Zhang FZ, Rodriguez S, Keasling JD (2011) Metabolic engineering of microbial pathways for advanced biofuels production. Curr Opin Biotechnol 22:775–783
Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes-current status and future opportunities. Plant Biotechnol J 11:169–196
Hemmerlin A, Harwood JL, Bach TJ (2012) A raison d’etre for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog Lip Res 51:95–148
Hemmerlin A (2013) Post-translational events and modifications regulating plant enzymes involved in isoprenoid precursor biosynthesis. Plant Sci 203:41–54
Vranova E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. In: Merchant SS (ed) Ann Rev Plant Biol, vol 64, pp 665–700
Vranova E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5:318–333
Caelles C, Ferrer A, Balcells L, Hegardt FG, Boronat A (1989) Isolation and structural characterization of a cDNA-encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Mol Biol 13:627–638
Enjuto M, Balcells L, Campos N, Caelles C, Arro M, Boronat A (1994) Arabidopsis thaliana contains 2 differentially expressed 3-hydroxy-3-methylglutaryl-CoA reductase genes, which encode microsomal forms of the enzyme. Proc Natl Acad Sci USA 91:927–931
Campos N, Boronat A (1995) Targeting and topology in the membrane of plant 3-hydroxy-3-methylglutaryl coenzyme a reductase. Plant Cell 7:2163–2174
Denbow CJ, Lang S, Cramer CL (1995) Targeting and membrane orientation of tomato 3-hydroxy-3-methylglutaryl coenzyme A reductases. Plant Physiol 108:144
Re EB, Brugger S, Learned M (1997) Genetic and biochemical analysis of the transmembrane domain of Arabidopsis 3-hydroxy-3-methylglutaryl coenzyme A reductase. J Cell Biochem 65:443–459
Vollack KU, Dittrich B, Ferrer A, Boronat A, Bach TJ (1994) Two radish genes for 3-hydroxy-3-methylglutaryl-CoA reductase isozymes complement mevalonate auxotrophy in a yeast mutant and yield membrane-bound active enzyme. J Plant Physiol 143:479–487
Re EB, Jones D, Learned RM (1995) Coexpression of native and introduced genes reveals cryptic regulation of HMG CoA reductase expression in Arabidopsis. Plant J 7:771–784
Holmberg N, Harker M, Wallace AD, Clayton JC, Gibbard CL, Safford R (2003) Co-expression of N-terminal truncated 3-hydroxy-3-methylglutaryl CoA reductase and C24-sterol methyltransferase type 1 in transgenic tobacco enhances carbon flux towards end-product sterols. Plant J 36:12–20
Ohyama K, Suzuki M, Masuda K, Yoshida S, Muranaka T (2007) Chemical phenotypes of the hmg1 and hmg2 mutants of Arabidopsis demonstrate the in-planta role of HMG-CoA reductase in triterpene biosynthesis. Chem Pharm Bull (Tokyo) 55:1518–1521
Suzuki M, Kamide Y, Nagata N, Seki H, Ohyama K, Kato H, Masuda K, Sato S, Kato T, Tabata S, Yoshida S, Muranaka T (2004) Loss of function of 3-hydroxy-3-methylglutaryl coenzyme A reductase 1 (HMG1) in Arabidopsis leads to dwarfing, early senescence and male sterility, and reduced sterol levels. Plant J 37:750–761
Manzano D, Fernandez-Busquets X, Schaller H, Gonzalez V, Boronat A, Arro M, Ferrer A (2004) The metabolic imbalance underlying lesion formation in Arabidopsis thaliana overexpressing farnesyl diphosphate synthase (isoform 1S) leads to oxidative stress and is triggered by the developmental decline of endogenous HMGR activity. Planta 219:982–992
Chappell J, Vonlanken C, Vogeli U (1991) Elicitor-inducible 3-hydroxy-3-methylglutaryl coenzyme A reductase activity is required for sesquiterpene accumulation in tobacco cell-suspension cultures. Plant Physiol 97:693–698
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
Choi D, Bostock RM, Avdiushko S, Hildebrand DF (1994) Lipid-derived signals that discriminate wound-responsive and pathogen-responsive isoprenoid pathways in plants—methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc Natl Acad Sci USA 91:2329–2333
Lichtenthaler HK (1998) The plant 1-deoxy-d-xylulose-5-phosphate pathway for biosynthesis of isoprenoids. Fett-Lipid 100:128–138
Rohmer M (1999) The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat Prod Rep 16:565–574
Boucher Y, Doolittle WF (2000) The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol Microbiol 37:703–716
Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci USA 97:13172–13177
Bouvier F, d’Harlingue A, Suire C, Backhaus RA, Camara B (1998) Dedicated roles of plastid transketolases during the early onset of isoprenoid biogenesis in pepper fruits. Plant Physiol 117:1423–1431
Lange BM, Wildung MR, McCaskill D, Croteau R (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc Natl Acad Sci USA 95:2100–2104
Chahed K, Oudin A, Guivarc’h N, Hamdi S, Chenieux JC, Rideau M, Clastre M (2000) l-Deoxy-d-xylulose 5-phosphate synthase from periwinkle: cDNA identification and induced gene expression in terpenoid indole alkaloid-producing cells. Plant Physiol Biochem 38:559–566
Lois LM, Rodriguez-Concepcion M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J 22:503–513
Walter MH, Fester T, Strack D (2000) Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the ‘yellow pigment’ and other apocarotenoids. Plant J 21:571–578
Estevez JM, Cantero A, Reindl A, Reichler S, Leon P (2001) 1-Deoxy-d-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276:22901–22909
Mandel MA, Feldmann KA, HerreraEstrella L, RochaSosa M, Leon P (1996) CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J 9:649–658
Estevez JM, Cantero A, Romero C, Kawaide H, Jimenez LF, Kuzuyama T, Seto H, Kamiya Y, Leon P (2000) Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-d-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol 124:95–103
Araki N, Kusumi K, Masamoto K, Niwa Y, Iba K (2000) Temperature-sensitive Arabidopsis mutant defective in 1-deoxy-d-xylulose 5-phosphate synthase within the plastid non-mevalonate pathway of isoprenoid biosynthesis. Physiol Plant 108:19–24
Schwender J, Muller C, Zeidler J, Lichlenthaler HK (1999) Cloning and heterologous expression of a cDNA encoding 1-deoxy-d-xylulose-5-phosphate reductoisomerase of Arabidopsis thaliana. FEBS Lett 455:140–144
Carretero-Paulet L, Ahumada I, Cunillera N, Rodriguez-Concepcion M, Ferrer A, Boronat A, 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
Kuzuyama T, Shimizu T, Takahashi S, Seto H (1998) Fosmidomycin, a specific inhibitor of 1-deoxy-d-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedron Lett 39:7913–7916
Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Turbachova I, Eberl M, Zeidler J, Lichtenthaler HK, Soldati D, Beck E (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285:1573–1576
Steinbacher S, Kaiser J, Eisenreich W, Huber R, Bacher A, Rohdich F (2003) Structural basis of fosmidomycin action revealed by the complex with 2-C-methyl-d-erythritol 4-phosphate synthase (IspC)—implications for the catalytic mechanism and anti-malaria drug development. J Biol Chem 278:18401–18407
Zeidler J, Schwender J, Muller C, Wiesner J, Weidemeyer C, Beck E, Jomaa H, Lichtenthaler HK (1998) Inhibition of the non-mevalonate 1-deoxy-d-xylulose-5-phosphate pathway of plant isoprenoid biosynthesis by fosmidomycin. Z fur Naturforsch C- J Biosci 53:980–986
Rodriguez-Concepcion M, Ahumada I, Diez-Juez E, Sauret-Gueto S, Lois LM, Gallego F, Carretero-Paulet L, Campos N, Boronat A (2001) 1-Deoxy-d-xylulose 5-phosphate reductoisomerase and plastid isoprenoid biosynthesis during tomato fruit ripening. Plant J 27:213–222
Huang MS, Abel C, Sohrabi R, Petri J, Haupt I, Cosimano J, Gershenzon J, Tholl D (2010) Variation of herbivore-induced volatile terpenes among Arabidopsis ecotypes depends on allelic differences and subcellular targeting of two terpene synthases, TPS02 and TPS03. Plant Physiol 153:1293–1310
Xing SF, Miao J, Li SA, Qin GJ, Tang S, Li HN, Gu HY, Qu LJ (2010) Disruption of the 1-deoxy-d-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis. Cell Res 20:688–700
Rohdich F, Wungsintaweekul J, Fellermeier M, Sagner S, Herz S, Kis K, Eisenreich W, Bacher A, Zenk MH (1999) Cytidine 5’-triphosphate-dependent biosynthesis of isoprenoids: YgbP protein of Escherichia coli catalyzes the formation of 4-diphosphocytidyl-2-C-methylerythritol. Proc Natl Acad Sci USA 96:11758–11763
Rohdich F, Wungsintaweekul J, Eisenreich W, Richter G, Schuhr CA, Hecht S, Zenk MH, Bacher A (2000) Biosynthesis of terpenoids: 4-Diphosphocytidyl-2C-methyl-d-erythritol synthase of Arabidopsis thaliana. Proc Natl Acad Sci USA 97:6451–6456
Lange BM, Croteau R (1999) Isopentenyl diphosphate biosynthesis via a mevalonate-independent pathway: Isopentenyl monophosphate kinase catalyzes the terminal enzymatic step. Proc Natl Acad Sci USA 96:13714–13719
Luttgen H, Rohdich F, Herz S, Wungsintaweekul J, Hecht S, Schuhr CA, Fellermeier M, Sagner S, Zenk MH, Bacher A, Eisenreich W (2000) Biosynthesis of terpenoids: YchB protein of Escherichia coli phosphorylates the 2-hydroxy group of 4-diphosphocytidyl-2C-methyl-d-erythritol. Proc Natl Acad Sci USA 97:1062–1067
Rohdich F, Wungsintaweekul J, Luttgen H, Fischer M, Eisenreich W, Schuhr CA, Fellermeier M, Schramek N, Zenk MH, Bacher A (2000) Biosynthesis of terpenoids: 4-diphosphocytidyl-2-C-methyl-d-erythritol kinase from tomato. Proc Natl Acad Sci USA 97:8251–8256
Rohdich F, Hecht S, Gärtner K, Adam P, Krieger C, Amslinger S, Arigoni D, Bacher A, Eisenreich W (2002) Studies on the nonmevalonate terpene biosynthetic pathway: metabolic role of IspH (LytB) protein. Proc Natl Acad Sci USA 99:1158–1163
Rohdich F, Zepeck F, Adam P, Hecht S, Kaiser J, Laupitz R, Grawert T, Amslinger S, Eisenreich W, Bacher A, Arigoni D (2003) The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proc Natl Acad Sci USA 100:1586–1591
Tritsch D, Hemmerlin A, Bach TJ, Rohmer M (2010) Plant isoprenoid biosynthesis via the MEP pathway: in vivo IPP/DMAPP ratio produced by (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase in tobacco BY-2 cell cultures. FEBS Lett 584:129–134
Hsieh MH, Goodman HM (2006) Functional evidence for the involvement of Arabidopsis IspF homolog in the nonmevalonate pathway of plastid isoprenoid biosynthesis. Planta 223:779–784
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
Gutierrez-Nava MDL, Gillmor CS, Jimenez LF, Guevara-Garcia A, Leon P (2004) Chloroplast biogenesis genes act cell and noncell autonomously in early chloroplast development. Plant Physiol 135:471–482
Hsieh MH, Goodman HM (2005) The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiol 138:641–653
Gil MJ, Coego A, Mauch-Mani B, Jorda L, Vera P (2005) The Arabidopsis csb3 mutant reveals a regulatory link between salicylic acid-mediated disease resistance and the methyl-erythritol 4-phosphate pathway. Plant J 44:155–166
Wang H, Nagegowda DA, Rawat R, Bouvier-Nave P, Guo DJ, Bach TJ, Chye ML (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
Alex D, Bach TJ, Chye ML (2000) Expression of Brassica juncea 3-hydroxy-3-methylglutaryl CoA synthase is developmentally regulated and stress-responsive. Plant J 22:415–426
Nagegowda DA, Ramalingam S, Hemmerlin A, Bach TJ, Chye ML (2005) Brassica juncea HMG-CoA synthase: localization of mRNA and protein. Planta 221:844–856
Ishiguro S, Nishimori Y, Yamada M, Saito H, Suzuki T, Nakagawa T, Miyake H, Okada K, Nakamura K (2010) The Arabidopsis FLAKY POLLEN1 gene encodes a 3-hydroxy-3-methylglutaryl-coenzyme A synthase required for development of tapetum-specific organelles and fertility of pollen grains. Plant Cell Physiol 51:896–911
Choi D, Ward BL, Bostock RM (1992) Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenezyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell 4:1333–1344
Rodriguez-Concepcion M, Gruissem W (1999) Arachidonic acid alters tomato HMG expression and fruit growth and induces 3-hydroxy-3-methylglutaryl coenzyme A reductase-independent lycopene accumulation. Plant Physiol 119:41–48
Suzuki H, Xia YJ, Cameron R, Shadle G, Blount J, Lamb C, Dixon RA (2004) Signals for local and systemic responses of plants to pathogen attack. J Exp Bot 55:169–179
Suzuki M, Nakagawa S, Kamide Y, Kobayashi K, Ohyama K, Hashinokuchi H, Kiuchi R, Saito K, Muranaka T, Nagata N (2009) Complete blockage of the mevalonate pathway results in male gametophyte lethality. J Exp Biol 60:2055–2064
Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243–254
Paetzold H, Garms S, Bartram S, Wieczorek J, Uros-Gracia EM, Rodriguez-Concepcion 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
Brooker JD, Russell DW (1975) Properties of microsomal 3-hydroxy-3-methylglutaryl coenzyme A reductase from Pisum sativum seedlings. Arch Biochem Biophys 167:723–729
Soto G, Stritzler M, Lisi C, Alleva K, Pagano ME, Ardila F, Mozzicafreddo M, Cuccioloni M, Angeletti M, Ayub ND (2011) Acetoacetyl-CoA thiolase regulates the mevalonate pathway during abiotic stress adaptation. J Exp Bot 62:5699–5711
Schulte AE, van der Heijden R, Verpoorte R (2000) Purification and characterization of mevalonate kinase from suspension-cultured cells of Catharanthus roseus (L.) G. Don. Arch Biochem Biophys 378:287–298
Banerjee A, Wu Y, Banerjee R, Li Y, Yan HG, Sharkey TD (2013) Feedback inhibition of deoxy-d-xylulose-5-phosphate synthase regulates the methylerythritol 4-phosphate pathway. J Biol Chem 288:16926–16936
Ghirardo A, Wright LP, Bi Z, Rosenkranz M, Pulido P, Rodriguez-Concepcion M, Niinemets U, Brueggemann N, Gershenzon J, Schnitzler J-P (2014) Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene. Plant Physiol 165:37–51
Liao P, Wang H, Wang M, Hsiao A-S, Bach TJ, Chye M-L (2014) Transgenic tobacco overexpressing Brassica juncea HMG-CoA Synthase 1 shows increased plant growth, pod size, and seed yield. Plos One 9:e98264
Jin HN, Song ZH, Nikolau BJ (2012) Reverse genetic characterization of two paralogous acetoacetyl CoA thiolase genes in Arabidopsis reveals their importance in plant growth and development. Plant J 70:1015–1032
Holmberg N, Harker M, Gibbard CL, Wallace AD, Clayton JC, Rawlins S, Hellyer A, Safford R (2002) Sterol C-24 methyltransferase type 1 controls the flux of carbon into sterol biosynthesis in tobacco seed. Plant Physiol 130:303–311
Wentzinger LF, Bach TJ, Hartmann MA (2002) Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol 130:334–346
Ahn CS, Pai HS (2008) Physiological function of ispE, a plastid MEP pathway gene for isoprenoid biosynthesis, in organelle biogenesis and cell morphogenesis in Nicotiana benthamiana. Plant Mol Biol 66:503–517
Jung KH, Lee J, Dardick C, Seo YS, Cao P, Canlas P, Phetsom J, Xu X, Ouyang S, An K, Cho YJ, Lee GC, Lee Y, An G, Ronald PC (2008) Identification and functional analysis of light-responsive unique genes and gene family members in rice. PLoS Genet 4
Wille A, Zimmermann P, Vranova E, Furholz A, Laule O, Bleuler S, Hennig L, Prelic A, von Rohr P, Thiele L, Zitzler E, Gruissem W, Buhlmann P (2004) Sparse graphical Gaussian modeling of the isoprenoid gene network in Arabidopsis thaliana. Genome Biol 5
Ghassemian M, Lutes J, Tepperman JM, Chang HS, Zhu T, Wang X, Quail PH, Lange BM (2006) Integrative analysis of transcript and metabolite profiling data sets to evaluate the regulation of biochemical pathways during photomorphogenesis. Arch Biochem Biophys 448:45–59
Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET (2011) A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst Biol 5
Flores-Perez U, Perez-Gila J, Closa M, Wright LP, Botella-Pavia P, Phillips MA, Ferrer A, Gershenzon J, Rodriguez-Concepcion M (2010) PLEIOTROPIC REGULATORY LOCUS 1 (PRL1) integrates the regulation of sugar responses with isoprenoid metabolism in Arabidopsis. Mol Plant 3:101–112
Dale S, Arro M, Becerra B, Morrice NG, Boronat A, Hardie DG, Ferrer A (1995) Bacterial expression of the catalytic domain of 3-hydroxy-3-methylglutaryl-CoA reductase (isoform HMGR1) from Arabidopsis thaliana, and its inactivation by phosphorylation at Ser577 by Brassica oleracea 3-hydroxy-3-methylglutaryl-CoA reductase kinase. Eur J Biochem 233:506–513
Leivar P, Antolin-Llovera M, Ferrero S, Closa M, Arro M, Ferrer A, Boronat A, Camposa N (2011) Multilevel control of Arabidopsis 3-hydroxy-3-methylglutaryl coenzyme A reductase by protein phosphatase 2A. Plant Cell 23:1494–1511
Yoshioka H, Miyabe M, Hayakawa Y, Doke N (1996) Expression of genes for phenylalanine ammonia-lyase and 3-hydroxy-3-methylglutaryl CoA reductase in aged potato tubers infected with Phytophthora infestans. Plant Cell Physiol 37:81–90
Nieto B, Fores O, Arro M, Ferrer A (2009) Arabidopsis 3-hydroxy-3-methylglutaryl-CoA reductase is regulated at the post-translational level in response to alterations of the sphingolipid and the sterol biosynthetic pathways. Phytochemistry 70:53–59
Kang JH, McRoberts J, Shi F, Moreno JE, Jones AD, Howe GA (2014) The flavonoid biosynthetic enzyme chalcone isomerase modulates terpenoid production in glandular trichomes of tomato. Plant Physiol 164:1161–1174
Pourcel L, Irani NG, Koo AJK, Bohorquez-Restrepo A, Howe GA, Grotewold E (2013) A chemical complementation approach reveals genes and interactions of flavonoids with other pathways. Plant J 74:383–397
Sahu NK, Balbhadra SS, Choudhary J, Kohli DV (2012) Exploring pharmacological significance of chalcone scaffold: a review. Curr Med Chem 19:209–225
Saslowsky DE, Warek U, Winkel BSJ (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Biol Chem 280:23735–23740
Ben Zvi MM, 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
Cordoba E, Salmi M, Leon P (2009) Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J Exp Bot 60:2933–2943
Rodriguez-Concepcion M, Fores O, Martinez-Garcia JF, Gonzalez V, Phillips MA, Ferrer A, Boronat A (2004) Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 16:144–156
Toledo-Ortiz G, Huq E, Rodriguez-Concepcion M (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc Natl Acad Sci USA 107:11626–11631
Wiberley AE, Donohue AR, Westphal MM, Sharkey TD (2009) Regulation of isoprene emission from poplar leaves throughout a day. Plant Cell Environ 32:939–947
Mongelard G, Seemann M, Boisson AM, Rohmer M, Bligny R, Rivasseau C (2011) Measurement of carbon flux through the MEP pathway for isoprenoid synthesis by P-31-NMR spectroscopy after specific inhibition of 2-C-methyl-d-erythritol 2,4-cyclodiphosphate reductase. Effect of light and temperature. Plant Cell Environ 34:1241–1247
Kim YJ, Lee OR, Oh JY, Jang MG, Yang DC (2014) Functional analysis of 3-hydroxy-3-methylglutaryl coenzyme A reductase encoding genes in triterpene saponin-producing ginseng. Plant Physiol 165:373–387
Mannen K, Matsumoto T, Takahashi S, Yamaguchi Y, Tsukagoshi M, Sano R, Suzuki H, Sakurai N, Shibata D, Koyama T, Nakayama T (2014) Coordinated transcriptional regulation of isopentenyl diphosphate biosynthetic pathway enzymes in plastids by phytochrome-interacting factor 5. Biochem Biophys Res Commun 443:768–774
Flores-Perez U, Sauret-Gueto S, Gas E, Jarvis P, Rodriguez-Concepcion M (2008) A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20:1303–1315
Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, Sakakibara H, Mizuno T, Saito K (2009) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci USA 106:7251–7256
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
Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 101:7475–7480
Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100:370–375
Seemann M, Bui BTS, Wolff M, Miginlac-Maslow M, Rohmer M (2006) Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG. FEBS Lett 580:1547–1552
Vogeli U, Chappell J (1988) Induction of sesquiterpene cyclase and suppression of squalene synthase activities in plant cell cultures treated with fungal elicitor. Plant Physiol 88:1291–1296
Kim CY, Zhang SQ (2004) Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J 38:142–151
Jin HL, Liu YD, Yang KY, Kim CY, Baker B, Zhang SQ (2003) Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J 33:719–731
Kevei Z, Lougnon G, Mergaert P, Horvath GV, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss GB, Kondorosi A, Endre G, Kondorosi E, Ane JM (2007) 3-hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19:3974–3989
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
Simkin AJ, Guirimand G, Papon N, Courdavault V, Thabet I, Ginis O, Bouzid S, Giglioli-Guivarc’h N, Clastre M (2011) Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta. Planta 234:903–914
Guirimand G, Guihur A, Phillips MA, Oudin A, Glevarec G, Melin C, Papon N, Clastre M, St-Pierre B, Rodriguez-Concepcion M, Burlat V, Courdavault V (2012) A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus. Plant Mol Biol 79:443–459
Lichtenthaler HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65
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
Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange BM (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6866–6871
Bartram S, Jux A, Gleixner G, Boland W (2006) Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67:1661–1672
Chaurasiya ND, Sangwan NS, Sabir F, Misra L, Sangwan RS (2012) Withanolide biosynthesis recruits both mevalonate and DOXP pathways of isoprenogenesis in Ashwagandha Withania somnifera L. (Dunal). Plant Cell Rep 31:1889–1897
Woelwer-Rieck U, May B, Lankes C, Wuest M (2014) Methylerythritol and mevalonate pathway contributions to biosynthesis of mono-, sesqui-, and diterpenes in glandular trichomes and leaves of Stevia rebaudiana Bertoni. J Agric Food Chem 62:2428–2435
Zhao S, Wang L, Liu L, Liang Y, Sun Y, Wu J (2014) Both the mevalonate and the non-mevalonate pathways are involved in ginsenoside biosynthesis. Plant Cell Rep 33:393–400
Opitz S, Nes WD, Gershenzon J (2014) Both methylerythritol phosphate and mevalonate pathways contribute to biosynthesis of each of the major isoprenoid classes in young cotton seedlings. Phytochemistry 98:110–119
Bick JA, 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 415:146–154
Flügge UI, Gao W (2005) Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol 7:91–97
Gutensohn M, Orlova I, Nguyen TTH, Davidovich-Rikanati R, Ferruzzi MG, Sitrit Y, Lewinsohn E, Pichersky E, Dudareva N (2013) Cytosolic monoterpene biosynthesis is supported by plastid-generated geranyl diphosphate substrate in transgenic tomato fruits. Plant J 75:351–363
May B, Lange BM, Wuest M (2013) Biosynthesis of sesquiterpenes in grape berry exocarp of Vitis vinifera L.: evidence for a transport of farnesyl diphosphate precursors from plastids to the cytosol. Phytochemistry 95:135–144
Wu SQ, 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
Wu S, Jiang Z, Kempinski C, Nybo SE, Husodo S, Williams R, Chappell J (2012) Engineering triterpene metabolism in tobacco. Planta 236:867–877
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
Huchelmann A, Gastaldo C, Veinante M, Zeng Y, Heintz D, Tritsch D, Schaller H, Rohmer M, Bach TJ, Hemmerlin A (2014) S-Carvone suppresses cellulase-induced capsidiol production in Nicotiana tabacum by interfering with protein isoprenylation. Plant Physiol 164:935–950
Verbitskiy D, Zehrmann A, van der Merwe JA, Brennicke A, Takenaka M (2010) The PPR protein encoded by the Lovastatin Insensitive 1 gene is involved in RNA editing at three sites in mitochondria of Arabidopsis thaliana. Plant J 61:446–455
Tang JW, Kobayashi K, Suzuki M, Matsumoto S, Muranaka T (2010) The mitochondrial PPR protein LOVASTATIN INSENSITIVE 1 plays regulatory roles in cytosolic and plastidial isoprenoid biosynthesis through RNA editing. Plant J 61:456–466
Xiao YM, Savchenko T, Baidoo EEK, Chehab WE, Hayden DM, Tolstikov V, Corwin JA, Kliebenstein DJ, Keasling JD, Dehesh K (2012) Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149:1525–1535
Phillips MA, D’Auria JC, Gershenzon J, Pichersky E (2008) The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis. Plant Cell 20:677–696
Kharel Y, Koyama T (2003) Molecular analysis of cis-prenyl chain elongating enzymes. Nat Prod Rep 20:111–118
Burke C, Croteau R (2002) Interaction with the small subunit of geranyl diphosphate synthase modifies the chain length specificity of geranylgeranyl diphosphate synthase to produce geranyl diphosphate. J Biol Chem 277:3141–3149
Schmidt A, Gershenzon J (2008) Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 69:49–57
Chang TH, Hsieh FL, Ko TP, Teng KH, Liang PH, Wang AHJ (2010) Structure of a heterotetrameric geranyl pyrophosphate synthase from mint (Mentha piperita) reveals intersubunit regulation. Plant Cell 22:454–467
Rai A, Smita SS, Singh AK, Shanker K, Nagegowda DA (2013) Heteromeric and homomeric geranyl diphosphate synthases from Catharanthus roseus and their role in monoterpene indole alkaloid biosynthesis. Mol Plant 6:1531–1549
Hsiao YY, Jeng MF, Tsai WC, Chuang YC, Li CY, Wu TS, Kuoh CS, Chen WH, Chen HH (2008) A novel homodimeric geranyl diphosphate synthase from the orchid Phalaenopsis bellina lacking a DD(X)(2-4)D motif. Plant J 55:719–733
Burke CC, Wildung MR, Croteau R (1999) Geranyl diphosphate synthase: cloning, expression, and characterization of this prenyltransferase as a heterodimer. Proc Natl Acad Sci USA 96:13062–13067
Tholl D, Kish CM, Orlova I, Sherman D, Gershenzon J, Pichersky E, Dudareva N (2004) Formation of monoterpenes in Antirrhinum majus and Clarkia breweri flowers involves heterodimeric geranyl diphosphate synthases. Plant Cell 16:977–992
Wang GD, Dixon RA (2009) Heterodimeric geranyl(geranyl)diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis. Proc Natl Acad Sci USA 106:9914–9919
Orlova I, Nagegowda DA, Kish CM, Gutensohn M, Maeda H, Varbanova M, Fridman E, Yamaguchi S, Hanada A, Kamiya Y, Krichevsky A, Citovsky V, Pichersky E, Dudareva N (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
van Schie CCN, Ament K, Schmidt A, Lange T, Haring MA, Schuurink RC (2007) Geranyl diphosphate synthase is required for biosynthesis of gibberellins. Plant J 52:752–762
Schmidt A, Wachtler B, Temp U, Krekling T, Seguin A, Gershenzon J (2010) A bifunctional geranyl and geranylgeranyl diphosphate synthase is involved in terpene oleoresin formation in Picea abies. Plant Physiol 152:639–655
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
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
Cunillera N, Arro M, Delourme D, Karst F, Boronat A, Ferrer A (1996) Arabidopsis thaliana contains two differentially expressed farnesyl-diphosphate synthase genes. J Biol Chem 271:7774–7780
Gaffe J, Bru JP, Causse M, Vidal A, Stamitti-Bert L, Carde JP, Gallusci P (2000) LEFPS1, a tomato farnesyl pyrophosphate gene highly expressed during early fruit development. Plant Physiol 123:1351–1362
Hemmerlin A, Rivera SB, Erickson HK, Poulter CD (2003) Enzymes encoded by the farnesyl diphosphate synthase gene family in the big sagebrush Artemisia tridentata ssp spiciformis. J Biol Chem 278:32132–32140
Cunillera N, Boronat A, Ferrer A (1997) The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J Biol Chem 272:15381–15388
Thabet I, Guirimand G, Courdavault V, Papon N, Godet S, Dutilleul C, Bouzid S, Giglioli-Guivarc’h N, Clastre M, Simkin AJ (2011) The subcellular localization of periwinkle farnesyl diphosphate synthase provides insight into the role of peroxisome in isoprenoid biosynthesis. J Plant Physiol 168:2110–2116
Ito J, Batth TS, Petzold CJ, Redding-Johanson AM, Mukhopadhyay A, Verboom R, Meyer EH, Millar AH, Heazlewood JL (2011) Analysis of the Arabidopsis cytosolic proteome highlights subcellular partitioning of central plant metabolism. J Proteome Res 10:1571–1582
Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber APM, Olsen LJ, Hu J (2009) In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 150:125–143
Closa M, Vranova E, Bortolotti C, Bigler L, Arro M, Ferrer A, Gruissem W (2010) The Arabidopsis thaliana FPP synthase isozymes have overlapping and specific functions in isoprenoid biosynthesis, and complete loss of FPP synthase activity causes early developmental arrest. Plant J 63:512–525
Keim V, Manzano D, Fernandez FJ, Closa M, Andrade P, Caudepon D, Bortolotti C, Vega MC, Arro M, Ferrer A (2012) Characterization of Arabidopsis FPS isozymes and FPS gene expression analysis provide insight into the biosynthesis of isoprenoid precursors in seeds. Plos One 7
Beck G, Coman D, Herren E, Ruiz-Sola M, Rodriguez-Concepcion M, Gruissem W, Vranova E (2013) Characterization of the GGPP synthase gene family in Arabidopsis thaliana. Plant Mol Biol 82:393–416
Ruppel NJ, Kropp KN, Davis PA, Martin AE, Luesse DR, Hangarter RP (2013) Mutations in geranylgeranyl diphosphate synthase 1 affect chloroplast development in Arabidopsis thaliana (Brassicaceae). Am J Bot 100:2074–2084
Dai ZB, Liu Y, Huang LQ, Zhang XL (2012) Production of miltiradiene by metabolically engineered Saccharomyces cerevisiae. Biotechnol Bioeng 109:2845–2853
Leonard E, Ajikumar PK, Thayer K, Xiao WH, 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 USA 107:13654–13659
Vandermoten S, Haubruge E, Cusson M (2009) New insights into short-chain prenyltransferases: structural features, evolutionary history and potential for selective inhibition. Cell Mol Life Sci 66:3685–3695
Tarshis LC, Yan MJ, Poulter CD, Sacchettini JC (1994) Crystal structure of recombinant farnesyl diphosphate synthase at 2.6 Angstrom resolution. Biochemistry 33:10871–10877
Koyama T, Gotoh Y, Nishino T (2000) Intersubunit location of the active site of farnesyl diphosphate synthase: reconstruction of active enzymes by hybrid-type heteromeric dimers of site-directed mutants. Biochemistry 39:463–469
Hosfield DJ, Zhang YM, Dougan DR, Broun A, Tari LW, Swanson RV, Finn J (2004) Structural basis for bisphosphonate-mediated inhibition of isoprenoid biosynthesis. J Biol Chem 279:8526–8529
Chang TH, Guo RT, Ko TP, Wang AHJ, Liang PH (2006) Crystal structure of type-III geranylgeranyl pyrophosphate synthase from Saccharomyces cerevisiae and the mechanism of product chain length determination. J Biol Chem 281:14991–15000
Gabelli SB, McLellan JS, Montalvetti A, Oldfield E, Docampo R, Amzel LM (2006) Structure and mechanism of the farnesyl diphosphate synthase from Trypanosoma cruza: implications for drug design. Proteins Struct Funct Bioinform 62:80–88
Kavanagh KL, Dunford JE, Bunkoczi G, Russell RGG, Oppermann U (2006) The crystal structure of human geranylgeranyl pyrophosphate synthase reveals a novel hexameric arrangement and inhibitory product binding. J Biol Chem 281:22004–22012
Kloer DP, Welsch R, Beyer P, Schulz GE (2006) Structure and reaction geometry of geranylgeranyl diphosphate synthase from Sinapis alba. Biochemistry 45:15197–15204
Ohnuma S, Hirooka K, Hemmi H, Ishida C, Ohto C, Nishino T (1996) Conversion of product specificity of archaebacterial geranylgeranyl- diphosphate synthase. Identification of essential amino acid residues for chain length determination of prenyltransferase reaction. J Biol Chem 271:18831–18837
Ohnuma SI, Nakazawa T, Hemmi H, Hallberg AM, Koyama T, Ogura K, Nishino T (1996) Conversion from farnesyl diphosphate synthase to geranylgeranyl diphosphate synthase by random chemical mutagenesis. J Biol Chem 271:10087–10095
Wallrapp FH, Pan J-J, Ramamoorthy G, Almonacid DE, Hillerich BS, Seidel R, Patskovsky Y, Babbitt PC, Almo SC, Jacobson MP, Poulter CD (2013) Prediction of function for the polyprenyl transferase subgroup in the isoprenoid synthase superfamily. Proc Natl Acad Sci USA 110:E1196–E1202
Coman D, Altenhoff A, Zoller S, Gruissem W, Vranova E (2014) Distinct evolutionary strategies in the GGPPS family from plants. Front Plant Sci 5
Takahashi S, Koyama T (2006) Structure and function of cis-prenyl chain elongating enzymes. Chem Rec 6:194–205
Surmacz L, Swiezewska E (2011) Polyisoprenoids—secondary metabolites or physiologically important superlipids? Biochem Biophys Res Commun 407:627–632
Schmidt T, Lenders M, Hillebrand A, van Deenen N, Munt O, Reichelt R, Eisenreich W, Fischer R, Prufer D, Gronover CS (2010) Characterization of rubber particles and rubber chain elongation in Taraxacum koksaghyz. BMC Biochem 11
Sallaud C, Rontein D, Onillon S, Jabes F, Duffe 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 21:301–317
Akhtar TA, Matsuba Y, Schauvinhold I, Yu G, Lees HA, Klein SE, Pichersky E (2013) The tomato cis-prenyltransferase gene family. Plant J 73:640–652
Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, Prins M, de Vos M, Haring MA, Schuurink RC (2012) Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc Natl Acad Sci USA 109:20124–20129
Gonzales-Vigil E, Hufnagel DE, Kim J, Last RL, Barry CS (2012) Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites. Plant J 71:921–935
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 USA 106:10865–10870
Gutensohn M, Nguyen TTH, McMahon RD III, Kaplan I, Pichersky E, Dudareva N (2014) Metabolic engineering of monoterpene biosynthesis in tomato fruits via introduction of the non-canonical substrate neryl diphosphate. Metab Eng 24:107–116
Demissie ZA, Erland LAE, Rheault MR, Mahmoud SS (2013) The biosynthetic origin of irregular monoterpenes in Lavandula: isolation and biochemical characterization of a novel cis-prenyl diphosphate synthase gene, lavendulyl diphosphate synthase. J Biol Chem 288:6333–6341
Surmacz L, Plochocka D, Kania M, Danikiewicz W, Swiezewska E (2014) cis-Prenyltransferase AtCPT6 produces a family of very short-chain polyisoprenoids in planta. Biochim Biophys Acta, Mol Cell Biol Lipids 1841:240–250
Kang J-H, Gonzales-Vigil E, Matsuba Y, Pichersky E, Barry CS (2014) Determination of residues responsible for substrate and product specificity of Solanum habrochaites short-chain cis-prenyltransferases. Plant Physiol 164:80–91
Kharel Y, Takahashi S, Yamashita S, Koyama T (2006) Manipulation of prenyl chain length determination mechanism of cis-prenyltransferases. FEBS J 273:647–657
Noike M, Katagiri T, Nakayama T, Koyama T, Nishino T, Hemmi H (2008) The product chain length determination mechanism of type II geranylgeranyl diphosphate synthase requires subunit interaction. FEBS J 275:3921–3933
Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54:656–669
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, Kollner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637
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
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
Kollner TG, Schnee C, Gershenzon J, Degenhardt J (2004) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 65:1895–1902
Xu MM, Wilderman PR, Peters RJ (2007) Following evolution’s lead to a single residue switch for diterpene synthase product outcome. Proc Natl Acad Sci USA 104:7397–7401
Keeling CI, Weisshaar S, Lin RPC, Bohlmann J (2008) Functional plasticity of paralogous diterpene synthases involved in conifer defense. Proc Natl Acad Sci USA 105:1085–1090
Greenhagen BT, O’Maille PE, Noel JP, Chappell J (2006) Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases. Proc Natl Acad Sci USA 103:9826–9831
Davis EM, Croteau R (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. In: Leeper FJ, Vederas JC (eds) Topics in current chemistry: biosynthesis-aromatic polyketides, isoprenoids, alkaloids. Springer, Heidelberg, pp 53–95
Zi J, Mafu S, Peters RJ (2014) To gibberellins and beyond! Surveying the evolution of (di)terpenoid metabolism. Annu Rev Plant Biol 65:259–286
Hayashi K, 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
Anterola A, Shanle E, Mansouri K, Schuette S, Renzaglia K (2009) Gibberellin precursor is involved in spore germination in the moss Physcomitrella patens. Planta 229:1003–1007
Peters RJ, Carter OA, Zhang Y, Matthews BW, Croteau RB (2003) Bifunctional abietadiene synthase: mutual structural dependence of the active sites for protonation-initiated and ionization-initiated cyclizations. Biochemistry 42:2700–2707
Li GL, Kollner TG, Yin YB, Jiang YF, Chen H, Xu Y, Gershenzon J, Pichersky E, Chen F (2012) Nonseed plant Selaginella moellendorfii has both seed plant and microbial types of terpene synthases. Proc Natl Acad Sci USA 109:14711–14715
Geu-Flores F, Sherden NH, Courdavault V, Burlat V, Glenn WS, Wu C, Nims E, Cui Y, O’Connor SE (2012) An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis. Nature 492:138–142
Tundis R, Loizzo MR, Menichini F, Statti GA, Menichini F (2008) Biological and pharmacological activities of iridoids: recent developments. Mini-Rev Med Chem 8:399–420
Dewhirst SY, Pickett JA, Hardie J (2010) Aphid pheromones. In: Litwack G (ed) Vitamins and hormones: pheromones, pp 551–574
Koksal M, Zimmer I, Schnitzler JP, Christianson DW (2010) Structure of isoprene synthase illuminates the chemical mechanism of teragram atmospheric carbon emission. J Mol Biol 402:363–373
Whittington DA, Wise ML, Croteau R, Christianson DW (2002) Insights into monoterpene cyclization reactions in biology: crystal structure of (+)-bornyl diphosphate synthase. Biochemistry 41:8973
Whittington DA, Wise ML, Urbansky M, Coates RM, Croteau RB, Christianson DW (2002) Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase. Proc Natl Acad Sci USA 99:15375–15380
Hyatt DC, Youn BY, Zhao YX, Santhamma B, Coates RM, Croteau RB, Kang CH (2007) Structure of limonene synthase, a simple model for terpenoid cyclase catalysis. Proc Natl Acad Sci USA 104:5360–5365
Kampranis SC, Ioannidis D, Purvis A, Mahrez W, Ninga E, Katerelos NA, Anssour S, Dunwell JM, Degenhardt J, Makris AM, Goodenough PW, Johnson CB (2007) Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. Plant Cell 19:1994–2005
Starks CM, Back KW, Chappell J, Noel JP (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277:1815–1820
Gennadios HA, Gonzalez V, Di Costanzo L, Li AA, Yu FL, Miller DJ, Allemann RK, Christianson DW (2009) Crystal structure of (+)-delta-cadinene synthase from Gossypium arboreum and evolutionary divergence of metal binding motifs for catalysis. Biochemistry 48:6175–6183
Koksal M, Jin YH, Coates RM, Croteau R, Christianson DW (2011) Taxadiene synthase structure and evolution of modular architecture in terpene biosynthesis. Nature 469:116–120
Koksal M, Potter K, Peters RJ, Christianson DW (2014) 1.55 angstrom-resolution structure of ent-copalyl diphosphate synthase and exploration of general acid function by site-directed mutagenesis. Biochim Biophys Acta, Gen Sub 1840:184–190
Koeksal M, Hu H, Coates RM, Peters RJ, Christianson DW (2011) Structure and mechanism of the diterpene cyclase ent-copalyl diphosphate synthase. Nat Chem Biol 7:431–433
Zhou K, Gao Y, Hoy JA, Mann FM, Honzatko RB, Peters RJ (2012) Insights into diterpene cyclization from structure of bifunctional abietadiene synthase from Abies grandis. J Biol Chem 287:6840–6850
Cao R, Zhang YH, Mann FM, Huang CC, Mukkamala D, Hudock MP, Mead ME, Prisic S, Wang K, Lin FY, Chang TK, Peters RJ, Odfield E (2010) Diterpene cyclases and the nature of the isoprene fold. Proteins: Struct Funct Bioinform 78:2417–2432
Gao Y, Honzatko RB, Peters RJ (2012) Terpenoid synthase structures: a so far incomplete view of complex catalysis. Nat Prod Rep 29:1153–1175
Christianson DW (2006) Structural biology and chemistry of the terpenoid cyclases. Chem Rev 106:3412–3442
Aubourg S, Lecharny A, Bohlmann J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genet Genomics 267:730–745
Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book 9:e0143
Field B, Osbourn AE (2008) Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320:543–547
Field B, Fiston-Lavier AS, Kemen A, Geisler K, Quesneville H, Osbourn AE (2011) Formation of plant metabolic gene clusters within dynamic chromosomal regions. Proc Natl Acad Sci USA 108:16116–16121
Mugford ST, Louveau T, Melton R, Qi XQ, Bakht S, Hill L, Tsurushima T, Honkanen S, Rosser SJ, Lomonossoff GP, Osbourn A (2013) Modularity of plant metabolic gene clusters: a trio of linked genes that are collectively required for acylation of triterpenes in oat. Plant Cell 25:1078–1092
Wilderman PR, Xu MM, Jin YH, Coates RM, Peters RJ (2004) Identification of syn-pimara-7,15-diene synthase reveals functional clustering of terpene synthases involved in rice phytoalexin/allelochemical biosynthesis. Plant Physiol 135:2098–2105
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
Segura MJR, Jackson BE, Matsuda SPT (2003) Mutagenesis approaches to deduce structure-function relationships in terpene synthases. Nat Prod Rep 20:304–317
Phillips DR, Rasbery JM, Bartel B, Matsuda SPT (2006) Biosynthetic diversity in plant triterpene cyclization. Curr Opin Plant Biol 9:305–314
Wegel E, Koumproglou R, Shaw P, Osbourn A (2009) Cell type-specific chromatin decondensation of a metabolic gene cluster in oats. Plant Cell 21:3926–3936
Mylona P, Owatworakit A, Papadopoulou K, Jenner H, Qin B, Findlay K, Hill L, Qi X, Bakht S, Melton R, Osbourn A (2008) Sad3 and Sad4 are required for saponin biosynthesis and root development in oat. Plant Cell 20:201–212
Yamane H (2013) Biosynthesis of phytoalexins and regulatory mechanisms of it in rice. Biosci Biotech Biochem 77:1141–1148
Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiol 135:507–515
Lu X, Zhang L, Zhang FY, Jiang WM, Shen Q, Zhang LD, Lv ZY, Wang GF, Tang KX (2013) AaORA, a trichome-specific AP2/ERF transcription factor of Artemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to Botrytis cinerea. New Phytol 198:1191–1202
Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, Chetelat A, Haupt I, Kennerley BJ, Hodgens C, Farmer EE, Nagpal P, Reed JW (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8
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
Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245
Yadav V, Mallappa C, Gangappa SN, Bhatia S, Chattopadhyay S (2005) A basic helix-loop-helix transcription factor in Arabidopsis, MYC2, acts as a repressor of blue light-mediated photomorphogenic growth. Plant Cell 17:1953–1966
Vaughan MM, Wang Q, Webster FX, Kiemle D, Hong YJ, Tantillo DJ, Coates RM, Wray AT, Askew W, O’Donnell C, Tokuhisa JG, Tholl D (2013) Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. Plant Cell 25:1108–1125
Ro DK, Ehlting J, Keeling CI, Lin R, Mattheus N, Bohlmann J (2006) Microarray expression profiling and functional characterization of AtTPS genes: duplicated Arabidopsis thaliana sesquiterpene synthase genes At4g13280 and At4g13300 encode root-specific and wound-inducible (Z)-γ-bisabolene synthases. Arch Biochem Biophys 448:104–116
Loreto F, Dicke M, Schnitzler JP, Turlings TCJ (2014) Plant volatiles and the environment. Plant Cell Environ 37:1905–1908
Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hasch R, Polle A, Bohlmann J, Schnitzler JP (2007) Transgenic, non-isoprene emitting poplars don’t like it hot. Plant J 51:485–499
Sharkey TD, Yeh SS (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52:407–436
Velikova V, Ghirardo A, Vanzo E, Merl J, Hauck SM, Schnitzler J-P (2014) Genetic manipulation of isoprene emissions in poplar plants remodels the chloroplast proteome. J Proteome Res 13:2005–2018
Behnke K, Kleist E, Uerlings R, Wildt J, Rennenberg H, Schnitzler JP (2009) RNAi-mediated suppression of isoprene biosynthesis in hybrid poplar impacts ozone tolerance. Tree Physiol 29:725–736
Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166
Vickers CE, Possell M, Laothawornkitkul J, Ryan AC, Hewitt CN, Mullineaux PM (2011) Isoprene synthesis in plants: lessons from a transgenic tobacco model. Plant Cell Environ 34:1043–1053
Schnitzler JP, Louis S, Behnke K, Loivamaki M (2010) Poplar volatiles—biosynthesis, regulation and (eco)physiology of isoprene and stress-induced isoprenoids. Plant Biol 12:302–316
Byers K, Bradshaw HD, Riffell JA (2014) Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J Exp Biol 217:614–623
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
Junker RR, Loewel C, Gross R, Dötterl S, Keller A, Blüthgen N (2011) Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol 13:918–924
Wang H, Guo WF, Zhang PJ, Wu ZY, Liu SS (2008) Experience-induced habituation and preference towards non-host plant odors in ovipositing females of a moth. J Chem Ecol 34:330–338
Laothawornkitkul J, Paul ND, Vickers CE, Possell M, Taylor JE, Mullineaux PM, Hewitt CN (2008) Isoprene emissions influence herbivore feeding decisions. Plant Cell Environ 31:1410–1415
Bleeker PM, Diergaarde PJ, Ament K, Schutz S, Johne B, Dijkink J, Hiemstra H, de Gelder R, de Both MTJ, Sabelis MW, Haring MA, Schuurink RC (2011) Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies. Phytochemistry 72:68–73
Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97
Hall DE, Robert JA, Keeling CI, Domanski D, Quesada AL, Jancsik S, Kuzyk MA, Hamberger B, Borchers CH, Bohlmann J (2011) An integrated genomic, proteomic and biochemical analysis of (+)-3-carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes that are resistant or susceptible to white pine weevil. Plant J 65:936–948
Gols R (2014) Direct and indirect chemical defences against insects in a multitrophic framework. Plant Cell Environ 37:1741–1752
Pierik R, Ballare CL, Dicke M (2014) Ecology of plant volatiles: taking a plant community perspective. Plant Cell Environ 37:1845–1853
Schnee C, Kollner 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
Fontana A, Held M, Fantaye CA, Turlings TC, Degenhardt J, Gershenzon J (2011) Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp Cotesia marginiventris (Cresson). J Chem Ecol 37:582–591
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
McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310
Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357
Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379–1397
Buchel K, Malskies S, Mayer M, Fenning TM, Gershenzon J, Hilker M, Meiners T (2011) How plants give early herbivore alert: volatile terpenoids attract parasitoids to egg-infested elms. Basic Appl Ecol 12:403–412
Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515
Frost CJ, Appel M, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498
Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144
Heil M (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol. doi:10.1111/nph.12977
Himanen SJ, Blande JD, Klemola T, Pulkkinen J, Heijari J, Holopainen JK (2010) Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants—a mechanism for associational herbivore resistance? New Phytol 186:722–732
Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967
Jassbi AR, Zamanizadehnajari S, Baldwin IT (2010) 17-Hydroxygeranyllinalool glycosides are major resistance traits of Nicotiana obtusifolia against attack from tobacco hornworm larvae. Phytochemistry 71:1115–1121
Schmelz EA, Kaplan F, Huffaker A, Dafoe NJ, Vaughan MM, Ni XZ, Rocca JR, Alborn HT, Teal PE (2011) Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc Natl Acad Sci USA 108:5455–5460
Huffaker A, Kaplan F, Vaughan MM, Dafoe NJ, Ni XZ, Rocca JR, Alborn HT, Teal PEA, Schmelz EA (2011) Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol 156:2082–2097
Kuzina V, Ekstrom CT, Andersen SB, Nielsen JK, Olsen CE, Bak S (2009) Identification of defense compounds in Barbarea vulgaris against the herbivore Phyllotreta nemorum by an ecometabolomic approach. Plant Physiol 151:1977–1990
Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737
Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:47–56
Degenhardt J, Hiltpold I, Kollner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106:13213–13218
Robert CAM, Erb M, Hiltpold I, Hibbard BE, Gaillard MDP, Bilat J, Degenhardt J, Cambet-Petit-Jean X, Turlings TCJ, Zwahlen C (2013) Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol J 11:628–639
Xu MM, Galhano R, Wiemann P, Bueno E, Tiernan M, Wu W, Chung IM, Gershenzon J, Tudzynski B, Sesma A, Peters RJ (2012) Genetic evidence for natural product-mediated plant–plant allelopathy in rice (Oryza sativa). New Phytol 193:570–575
Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65:225–257
Kemen AC, Honkanen S, Melton RE, Findlay KC, Mugford ST, Hayashi K, Haralampidis K, Rosser SJ, Osbourn A (2014) Investigation of triterpene synthesis and regulation in oats reveals a role for beta-amyrin in determining root epidermal cell patterning. Proc Natl Acad Sci USA 111:8679–8684
Chaturvedi R, Venables B, Petros RA, Nalam V, Li MY, Wang XM, Takemoto LJ, Shah J (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J 71:161–172
Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–U122
Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211–221
Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28
Rodriguez S, Kirby J, Denby CM, Keasling JD (2014) Production and quantification of sesquiterpenes in Saccharomyces cerevisiae, including extraction, detection and quantification of terpene products and key related metabolites. Nat Protoc 9:1980–1996
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This work was supported by the National Science Foundation MCB grant 0950865.
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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. https://doi.org/10.1007/10_2014_295
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