Skip to main content

Biosynthesis and Biological Functions of Terpenoids in Plants

  • Chapter
  • First Online:
Biotechnology of Isoprenoids

Part of the book series: Advances in Biochemical Engineering/Biotechnology ((ABE,volume 148))

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. 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

    Google Scholar 

  2. Zhang FZ, Rodriguez S, Keasling JD (2011) Metabolic engineering of microbial pathways for advanced biofuels production. Curr Opin Biotechnol 22:775–783

    CAS  Google Scholar 

  3. Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes-current status and future opportunities. Plant Biotechnol J 11:169–196

    CAS  Google Scholar 

  4. 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

    CAS  Google Scholar 

  5. Hemmerlin A (2013) Post-translational events and modifications regulating plant enzymes involved in isoprenoid precursor biosynthesis. Plant Sci 203:41–54

    Google Scholar 

  6. 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

    Google Scholar 

  7. Vranova E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5:318–333

    CAS  Google Scholar 

  8. 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

    CAS  Google Scholar 

  9. 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

    Google Scholar 

  10. 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

    CAS  Google Scholar 

  11. Denbow CJ, Lang S, Cramer CL (1995) Targeting and membrane orientation of tomato 3-hydroxy-3-methylglutaryl coenzyme A reductases. Plant Physiol 108:144

    Google Scholar 

  12. 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

    CAS  Google Scholar 

  13. 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

    CAS  Google Scholar 

  14. 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

    CAS  Google Scholar 

  15. 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

    CAS  Google Scholar 

  16. 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

    CAS  Google Scholar 

  17. 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

    CAS  Google Scholar 

  18. 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

    CAS  Google Scholar 

  19. 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

    CAS  Google Scholar 

  20. 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

    CAS  Google Scholar 

  21. 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

    CAS  Google Scholar 

  22. Lichtenthaler HK (1998) The plant 1-deoxy-d-xylulose-5-phosphate pathway for biosynthesis of isoprenoids. Fett-Lipid 100:128–138

    CAS  Google Scholar 

  23. 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

    CAS  Google Scholar 

  24. Boucher Y, Doolittle WF (2000) The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol Microbiol 37:703–716

    CAS  Google Scholar 

  25. 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

    CAS  Google Scholar 

  26. 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

    CAS  Google Scholar 

  27. 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

    CAS  Google Scholar 

  28. 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

    CAS  Google Scholar 

  29. 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

    CAS  Google Scholar 

  30. 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

    CAS  Google Scholar 

  31. 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

    CAS  Google Scholar 

  32. 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

    CAS  Google Scholar 

  33. 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

    CAS  Google Scholar 

  34. 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

    CAS  Google Scholar 

  35. 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

    CAS  Google Scholar 

  36. 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

    CAS  Google Scholar 

  37. 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

    CAS  Google Scholar 

  38. 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

    CAS  Google Scholar 

  39. 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

    CAS  Google Scholar 

  40. 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

    CAS  Google Scholar 

  41. 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

    CAS  Google Scholar 

  42. 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

    CAS  Google Scholar 

  43. 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

    CAS  Google Scholar 

  44. 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

    CAS  Google Scholar 

  45. 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

    CAS  Google Scholar 

  46. 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

    CAS  Google Scholar 

  47. 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

    Google Scholar 

  48. 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

    CAS  Google Scholar 

  49. 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

    CAS  Google Scholar 

  50. 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

    CAS  Google Scholar 

  51. 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

    CAS  Google Scholar 

  52. 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

    CAS  Google Scholar 

  53. 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

    CAS  Google Scholar 

  54. 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

    CAS  Google Scholar 

  55. Hsieh MH, Goodman HM (2005) The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiol 138:641–653

    CAS  Google Scholar 

  56. 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

    CAS  Google Scholar 

  57. 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

    Google Scholar 

  58. 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

    CAS  Google Scholar 

  59. 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

    CAS  Google Scholar 

  60. 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

    CAS  Google Scholar 

  61. 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

    CAS  Google Scholar 

  62. 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

    CAS  Google Scholar 

  63. 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

    CAS  Google Scholar 

  64. 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

    CAS  Google Scholar 

  65. 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

    CAS  Google Scholar 

  66. 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

    CAS  Google Scholar 

  67. 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

    CAS  Google Scholar 

  68. 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

    CAS  Google Scholar 

  69. 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

    CAS  Google Scholar 

  70. 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

    CAS  Google Scholar 

  71. 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

    CAS  Google Scholar 

  72. 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

    Google Scholar 

  73. 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

    CAS  Google Scholar 

  74. 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

    CAS  Google Scholar 

  75. 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

    CAS  Google Scholar 

  76. 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

    CAS  Google Scholar 

  77. 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

    Google Scholar 

  78. 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

    Google Scholar 

  79. 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

    CAS  Google Scholar 

  80. 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

    Google Scholar 

  81. 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

    CAS  Google Scholar 

  82. 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

    CAS  Google Scholar 

  83. 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

    CAS  Google Scholar 

  84. 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

    CAS  Google Scholar 

  85. 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

    CAS  Google Scholar 

  86. 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

    CAS  Google Scholar 

  87. 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

    CAS  Google Scholar 

  88. Sahu NK, Balbhadra SS, Choudhary J, Kohli DV (2012) Exploring pharmacological significance of chalcone scaffold: a review. Curr Med Chem 19:209–225

    CAS  Google Scholar 

  89. Saslowsky DE, Warek U, Winkel BSJ (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Biol Chem 280:23735–23740

    CAS  Google Scholar 

  90. 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

    CAS  Google Scholar 

  91. 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

    CAS  Google Scholar 

  92. 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

    CAS  Google Scholar 

  93. 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

    CAS  Google Scholar 

  94. 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

    CAS  Google Scholar 

  95. 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

    CAS  Google Scholar 

  96. 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

    CAS  Google Scholar 

  97. 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

    CAS  Google Scholar 

  98. 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

    CAS  Google Scholar 

  99. 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

    CAS  Google Scholar 

  100. 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

    CAS  Google Scholar 

  101. 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

    CAS  Google Scholar 

  102. 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

    CAS  Google Scholar 

  103. 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

    CAS  Google Scholar 

  104. 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

    CAS  Google Scholar 

  105. 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

    CAS  Google Scholar 

  106. 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

    CAS  Google Scholar 

  107. 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

    CAS  Google Scholar 

  108. 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

    CAS  Google Scholar 

  109. 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

    CAS  Google Scholar 

  110. 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

    CAS  Google Scholar 

  111. 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

    CAS  Google Scholar 

  112. 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

    CAS  Google Scholar 

  113. 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

    CAS  Google Scholar 

  114. 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

    CAS  Google Scholar 

  115. 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

    CAS  Google Scholar 

  116. 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

    CAS  Google Scholar 

  117. 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

    CAS  Google Scholar 

  118. 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

    CAS  Google Scholar 

  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

    CAS  Google Scholar 

  120. Flügge UI, Gao W (2005) Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol 7:91–97

    Google Scholar 

  121. 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

    CAS  Google Scholar 

  122. 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

    CAS  Google Scholar 

  123. 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

    CAS  Google Scholar 

  124. Wu S, Jiang Z, Kempinski C, Nybo SE, Husodo S, Williams R, Chappell J (2012) Engineering triterpene metabolism in tobacco. Planta 236:867–877

    CAS  Google Scholar 

  125. 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

    CAS  Google Scholar 

  126. 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

    CAS  Google Scholar 

  127. 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

    CAS  Google Scholar 

  128. 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

    CAS  Google Scholar 

  129. 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

    CAS  Google Scholar 

  130. 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

    CAS  Google Scholar 

  131. Kharel Y, Koyama T (2003) Molecular analysis of cis-prenyl chain elongating enzymes. Nat Prod Rep 20:111–118

    CAS  Google Scholar 

  132. 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

    CAS  Google Scholar 

  133. 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

    CAS  Google Scholar 

  134. 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

    CAS  Google Scholar 

  135. 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

    CAS  Google Scholar 

  136. 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

    CAS  Google Scholar 

  137. 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

    CAS  Google Scholar 

  138. 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

    CAS  Google Scholar 

  139. 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

    CAS  Google Scholar 

  140. 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

    CAS  Google Scholar 

  141. 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

    Google Scholar 

  142. 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

    CAS  Google Scholar 

  143. 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

    CAS  Google Scholar 

  144. 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

    CAS  Google Scholar 

  145. 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

    CAS  Google Scholar 

  146. 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

    CAS  Google Scholar 

  147. 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

    CAS  Google Scholar 

  148. 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

    CAS  Google Scholar 

  149. 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

    CAS  Google Scholar 

  150. 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

    CAS  Google Scholar 

  151. 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

    CAS  Google Scholar 

  152. 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

    CAS  Google Scholar 

  153. 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

    Google Scholar 

  154. 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

    CAS  Google Scholar 

  155. 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

    CAS  Google Scholar 

  156. Dai ZB, Liu Y, Huang LQ, Zhang XL (2012) Production of miltiradiene by metabolically engineered Saccharomyces cerevisiae. Biotechnol Bioeng 109:2845–2853

    CAS  Google Scholar 

  157. 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

    CAS  Google Scholar 

  158. 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

    CAS  Google Scholar 

  159. 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

    CAS  Google Scholar 

  160. 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

    CAS  Google Scholar 

  161. 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

    CAS  Google Scholar 

  162. 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

    CAS  Google Scholar 

  163. 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

    CAS  Google Scholar 

  164. 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

    CAS  Google Scholar 

  165. Kloer DP, Welsch R, Beyer P, Schulz GE (2006) Structure and reaction geometry of geranylgeranyl diphosphate synthase from Sinapis alba. Biochemistry 45:15197–15204

    CAS  Google Scholar 

  166. 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

    CAS  Google Scholar 

  167. 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

    CAS  Google Scholar 

  168. 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

    CAS  Google Scholar 

  169. Coman D, Altenhoff A, Zoller S, Gruissem W, Vranova E (2014) Distinct evolutionary strategies in the GGPPS family from plants. Front Plant Sci 5

    Google Scholar 

  170. Takahashi S, Koyama T (2006) Structure and function of cis-prenyl chain elongating enzymes. Chem Rec 6:194–205

    CAS  Google Scholar 

  171. Surmacz L, Swiezewska E (2011) Polyisoprenoids—secondary metabolites or physiologically important superlipids? Biochem Biophys Res Commun 407:627–632

    CAS  Google Scholar 

  172. 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

    Google Scholar 

  173. 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

    CAS  Google Scholar 

  174. 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

    CAS  Google Scholar 

  175. 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

    CAS  Google Scholar 

  176. 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

    CAS  Google Scholar 

  177. 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

    CAS  Google Scholar 

  178. 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

    CAS  Google Scholar 

  179. 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

    CAS  Google Scholar 

  180. 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

    CAS  Google Scholar 

  181. 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

    CAS  Google Scholar 

  182. Kharel Y, Takahashi S, Yamashita S, Koyama T (2006) Manipulation of prenyl chain length determination mechanism of cis-prenyltransferases. FEBS J 273:647–657

    CAS  Google Scholar 

  183. 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

    CAS  Google Scholar 

  184. Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54:656–669

    CAS  Google Scholar 

  185. 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

    CAS  Google Scholar 

  186. Degenhardt J, Kollner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637

    CAS  Google Scholar 

  187. 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

    CAS  Google Scholar 

  188. 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

    CAS  Google Scholar 

  189. 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

    CAS  Google Scholar 

  190. 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

    CAS  Google Scholar 

  191. 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

    CAS  Google Scholar 

  192. 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

    CAS  Google Scholar 

  193. 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

    Google Scholar 

  194. 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

    CAS  Google Scholar 

  195. 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

    CAS  Google Scholar 

  196. 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

    CAS  Google Scholar 

  197. 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

    CAS  Google Scholar 

  198. 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

    CAS  Google Scholar 

  199. 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

    CAS  Google Scholar 

  200. 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

    CAS  Google Scholar 

  201. Dewhirst SY, Pickett JA, Hardie J (2010) Aphid pheromones. In: Litwack G (ed) Vitamins and hormones: pheromones, pp 551–574

    Google Scholar 

  202. 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

    Google Scholar 

  203. 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

    Google Scholar 

  204. 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

    CAS  Google Scholar 

  205. 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

    CAS  Google Scholar 

  206. 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

    CAS  Google Scholar 

  207. 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

    CAS  Google Scholar 

  208. 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

    CAS  Google Scholar 

  209. 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

    Google Scholar 

  210. 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

    CAS  Google Scholar 

  211. 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

    CAS  Google Scholar 

  212. 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

    CAS  Google Scholar 

  213. 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

    Google Scholar 

  214. Gao Y, Honzatko RB, Peters RJ (2012) Terpenoid synthase structures: a so far incomplete view of complex catalysis. Nat Prod Rep 29:1153–1175

    CAS  Google Scholar 

  215. Christianson DW (2006) Structural biology and chemistry of the terpenoid cyclases. Chem Rev 106:3412–3442

    CAS  Google Scholar 

  216. 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

    CAS  Google Scholar 

  217. Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book 9:e0143

    Google Scholar 

  218. Field B, Osbourn AE (2008) Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320:543–547

    CAS  Google Scholar 

  219. 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

    CAS  Google Scholar 

  220. 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

    CAS  Google Scholar 

  221. 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

    CAS  Google Scholar 

  222. 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

    CAS  Google Scholar 

  223. Segura MJR, Jackson BE, Matsuda SPT (2003) Mutagenesis approaches to deduce structure-function relationships in terpene synthases. Nat Prod Rep 20:304–317

    CAS  Google Scholar 

  224. Phillips DR, Rasbery JM, Bartel B, Matsuda SPT (2006) Biosynthetic diversity in plant triterpene cyclization. Curr Opin Plant Biol 9:305–314

    CAS  Google Scholar 

  225. 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

    CAS  Google Scholar 

  226. 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

    CAS  Google Scholar 

  227. Yamane H (2013) Biosynthesis of phytoalexins and regulatory mechanisms of it in rice. Biosci Biotech Biochem 77:1141–1148

    CAS  Google Scholar 

  228. 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

    CAS  Google Scholar 

  229. 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

    CAS  Google Scholar 

  230. 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

    Google Scholar 

  231. 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

    CAS  Google Scholar 

  232. 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

    CAS  Google Scholar 

  233. 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

    CAS  Google Scholar 

  234. 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

    CAS  Google Scholar 

  235. 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

    CAS  Google Scholar 

  236. Loreto F, Dicke M, Schnitzler JP, Turlings TCJ (2014) Plant volatiles and the environment. Plant Cell Environ 37:1905–1908

    Google Scholar 

  237. 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

    CAS  Google Scholar 

  238. Sharkey TD, Yeh SS (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52:407–436

    CAS  Google Scholar 

  239. 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

    CAS  Google Scholar 

  240. 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

    CAS  Google Scholar 

  241. Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166

    CAS  Google Scholar 

  242. 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

    CAS  Google Scholar 

  243. 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

    CAS  Google Scholar 

  244. Byers K, Bradshaw HD, Riffell JA (2014) Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J Exp Biol 217:614–623

    Google Scholar 

  245. 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

    CAS  Google Scholar 

  246. 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

    CAS  Google Scholar 

  247. 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

    Google Scholar 

  248. 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

    CAS  Google Scholar 

  249. 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

    CAS  Google Scholar 

  250. Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97

    CAS  Google Scholar 

  251. 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

    CAS  Google Scholar 

  252. Gols R (2014) Direct and indirect chemical defences against insects in a multitrophic framework. Plant Cell Environ 37:1741–1752

    Google Scholar 

  253. Pierik R, Ballare CL, Dicke M (2014) Ecology of plant volatiles: taking a plant community perspective. Plant Cell Environ 37:1845–1853

    Google Scholar 

  254. 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

    CAS  Google Scholar 

  255. 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

    CAS  Google Scholar 

  256. 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

    CAS  Google Scholar 

  257. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310

    Google Scholar 

  258. Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357

    Google Scholar 

  259. Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379–1397

    CAS  Google Scholar 

  260. 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

    Google Scholar 

  261. 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

    CAS  Google Scholar 

  262. 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

    Google Scholar 

  263. Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144

    Google Scholar 

  264. Heil M (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol. doi:10.1111/nph.12977

    Google Scholar 

  265. 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

    CAS  Google Scholar 

  266. Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967

    CAS  Google Scholar 

  267. 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

    CAS  Google Scholar 

  268. 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

    CAS  Google Scholar 

  269. 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

    CAS  Google Scholar 

  270. 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

    CAS  Google Scholar 

  271. 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

    CAS  Google Scholar 

  272. Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:47–56

    Google Scholar 

  273. 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

    CAS  Google Scholar 

  274. 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

    CAS  Google Scholar 

  275. 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

    CAS  Google Scholar 

  276. Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65:225–257

    CAS  Google Scholar 

  277. 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

    CAS  Google Scholar 

  278. 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

    CAS  Google Scholar 

  279. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622

    CAS  Google Scholar 

  280. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    CAS  Google Scholar 

  281. 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

    CAS  Google Scholar 

  282. 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

    Google Scholar 

  283. Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211–221

    CAS  Google Scholar 

  284. Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28

    CAS  Google Scholar 

  285. 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

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation MCB grant 0950865.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dorothea Tholl .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

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

Download citation

Publish with us

Policies and ethics