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The Biochemistry and Molecular Biology of Volatile Messengers in Trees

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Biology, Controls and Models of Tree Volatile Organic Compound Emissions

Part of the book series: Tree Physiology ((TREE,volume 5))

Abstract

All tree species possess genes encoding terminal enzymes responsible for volatile isoprenoid synthesis. However, only in some species, these genes are expressed constitutively in leaves, while terpenoid emissions can be triggered by abiotic and biotic stress factor in essentially all species. This chapter analyses the biochemical diversity of volatile isoprenoid synthases and investigates the genomic modifications responsible for constitutive volatile production in trees. Plant terpenoids are up to three-domain proteins with either one active center in monofunctional synthases, or two active centers in bifunctional synthases. There is evidence of monophyletic origin of modern plant terpenoid synthases from a three-domain synthase in an ancient progenitor followed by extensive gene duplication and domain loss. The terpenoid synthase sequence similarity can be low among distant plant groups, but terpenoid tertiary structure is remarkably similar in different synthases, and this structural similarity is even conserved across domains of life. However, only minor changes in active center structure can lead to major changes in product profiles, indicating that presence of rich terpenoid genetic diversity constitutes an important means for rapid evolutionary adaptations to novel biotic interactions, and to new abiotic stresses in plant habitats.

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References

  • Aaron JA, Christianson DW (2010) Trinuclear metal clusters in catalysis by terpenoid synthases. Pure Appl Chem 82:1585–1597

    Article  CAS  PubMed  Google Scholar 

  • Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131

    Article  CAS  PubMed  Google Scholar 

  • Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602

    Article  CAS  PubMed  Google Scholar 

  • Al-Dous EK, George B, Al-Mahmoud ME, Al-Jaber MY, Wang H, Salameh YM, Al-Azwani EK, Chaluvadi S, Pontaroli AC, DeBarry J, Arondel V, Ohlrogge J, Saie IJ, Suliman-Elmeer KM, Bennetzen JL, Kruegger RR, Malek JA (2011) De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera). Nat Biotechnol 29:521–527

    Article  CAS  PubMed  Google Scholar 

  • Allona I, Quinn M, Shoop E, Swope K, St Cyr S, Carlis J, Riedl J, Retzel E, Campbell MM, Sederoff R, Whetten RW (1998) Analysis of xylem formation in pine by cDNA sequencing. Proc Natl Acad Sci USA 95:9693–9698

    Article  CAS  PubMed  Google Scholar 

  • Alonso WR, Croteau R (1993) Prenyltransferases and cyclases. In: Lea PJ (ed) Enzymes of secondary metabolism, vol 9, Methods in plant biochemistry. Academic, London/San Diego/ New York/Boston/Sydney/Tokyo/Toronto, pp 239–260

    Google Scholar 

  • Andreeva A, Howorth D, Chandonia J-M, Brenner SE, Hubbard TJP, Chothia C, Murzin AG (2008) Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res 36:D419–D425

    Article  CAS  PubMed  Google Scholar 

  • Arimura G-i, 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

    Article  CAS  PubMed  Google Scholar 

  • Arimura G-i, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa x deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (−)-germacrene D synthase, PtdTPS1. Plant J 37:603–616

    Article  CAS  PubMed  Google Scholar 

  • Ashworth K, Boissard C, Folberth G, Lathière J, Schurgers G (2013) Global modeling of volatile organic compound emissions. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Back KW, Chappell J (1996) Identifying functional domains within terpene cyclases using a domain-swapping strategy. Proc Natl Acad Sci USA 93:6841–6845

    Article  CAS  PubMed  Google Scholar 

  • Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hänsch R, Polle A, Bohlmann J, Schnitzler J-P (2007) Transgenic, non-isoprene emitting poplars don’t like it hot. Plant J 51:485–499

    Article  CAS  PubMed  Google Scholar 

  • Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242

    Article  CAS  PubMed  Google Scholar 

  • Besumbes Ó, Sauret-Güeto S, Phillips MA, Imperial S, Rodríguez-Concepción M, Boronat A (2004) Metabolic engineering of isoprenoid biosynthesis in Arabidopsis for the production of taxadiene, the first committed precursor of taxol. Biotechnol Bioeng 88:168–175

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J (2008) Insect-induced terpenoid defenses in spruce. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Berlin, pp 173–187

    Chapter  Google Scholar 

  • Bohlmann J, Croteau R (1999) Diversity and variability of terpenoid defences in conifers: molecular genetics, biochemistry and evolution of the terpene synthase gene family in grand fir (Abies grandis). Novartis Found Symp 223:132–149

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J, Steele CL, Croteau R (1997) Monoterpene synthases from grand fir (Abies grandis). cDNA isolation, characterization and functional expression of myrcene synthase, (−)-4S-limonene synthase and (−)-(1S,5S)-pinene synthase. J Biol Chem 272:21784–21792

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J, Crock J, Jetter R, Croteau R (1998a) Terpenoid-based defenses in conifers: cDNA cloning, characterization, and functional expression of wound-inducible (E)-α-bisabolene synthase from grand fir (Abies grandis). Proc Natl Acad Sci USA 95:6756–6761

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J, Meyer-Gauen G, Croteau R (1998b) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J, Phillips M, Ramachandiran V, Katoh S, Croteau R (1999) cDNA cloning, characterization, and functional expression of four new monoterpene synthase members of the Tpsd gene family from grand fir (Abies grandis). Arch Biochem Biophys 368:232–243

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J, Hall D, Robert J, Keeling C, Domanski D, Quesada AL, Jancsik S, Kuzyk M, Hamberger B, Borchers C (2011) Biomarkers and gene copy number variation for terpenoid traits associated with insect resistance in Sitka spruce: an integrated genomic, proteomic, and biochemical analysis of (+)-3-carene biosynthesis. BMC Proc 5:027

    Article  Google Scholar 

  • Braun EL, Dias AP, Matulnik TJ, Grotewold E (2001) Transcription factors and metabolic engineering: novel applications for ancient tools. In: Romeo JT, Saunders JA, Matthews BF (eds) Regulation of phytochemicals by molecular techniques. Elsevier Science, Beltsville, pp 79–109

    Chapter  Google Scholar 

  • Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, J-i M, Corcoran K (2000) Gene expression analysis by massively parrellel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18:630–634

    Article  CAS  PubMed  Google Scholar 

  • Byun McKay A, Hunter WL, Godard KA, Wang SX, Martin DM, Bohlmann J, Plant AL (2003) Insect attack and wounding induce traumatic resin duct development and gene expression of (−)-pinene synthase in Sitka spruce. Plant Physiol 133:368–378

    Article  CAS  Google Scholar 

  • Byun-McKay A, Godard KA, Toudefallah M, Martin DM, Alfaro R, King J, Bohlmann J, Plant AL (2006) Wound-induced terpene synthase gene expression in Sitka spruce that exhibit resistance or susceptibility to attack by the white pine weevil. Plant Physiol 140:1009–1021

    Article  CAS  PubMed  Google Scholar 

  • Cane DE, Ishida H (2012) Exploration and mining of the bacterial terpenome. Acc Chem Res 45:463–472

    Article  CAS  PubMed  Google Scholar 

  • Cane DE, Sohng J-K, Lamberson CR, Rudnicki SM, Wu Z, Lloyd MD, Oliver JS, Hubbard BR (1994) Pentalenene synthase. Purification, molecular cloning, sequencing, and high-level expression in Escherichia coli of a terpenoid cyclase from Streptomyces UC531g. Biochemistry 33:5846–5857

    Article  CAS  PubMed  Google Scholar 

  • Cao R, Zhang Y, Mann FM, Huang C, Mukkamala D, Hudock MP, Mead ME, Prisic S, Wang K, Lin F-Y, Chang T-K, Peters RJ, Odfield E (2010) Diterpene cyclases and the nature of the isoprene fold. Proteins Struct Funct Bioinform 78:2417–2432

    Article  CAS  Google Scholar 

  • Caruthers JM, Kang I, Rynkiewicz MJ, Cane DE, Christianson DW (2000) Crystal structure determination of aristolochene synthase from the blue cheese mold, Penicillium roqueforti. J Biol Chem 275:25533–25539

    Article  CAS  PubMed  Google Scholar 

  • Chang D, Duda TF Jr (2012) Extensive and continuous duplication facilitates rapid evolution and diversification of gene families. Mol Biol Evol 29:2019–2029

    Article  CAS  PubMed  Google Scholar 

  • Chappell J (1995) Biochemistry and molecular biology of the isoprenoid biosynthetic pathways in plants. Annu Rev Plant Physiol Plant Mol Biol 46:521–547

    Article  CAS  Google Scholar 

  • Chen F, Tholl D, D’Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:1–14

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Choudhary DK, Johri BN, Prakash A (2008) Volatiles as priming agents that initiate plant growth and defence responses. Curr Sci 94:595–604

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Christianson DW (2008) Unearthing the roots of the terpenome. Curr Opin Chem Biol 12:141–150

    Article  CAS  PubMed  Google Scholar 

  • Cinege G, Louis S, Hänsch R, Schnitzler J-P (2009) Regulation of isoprene synthase promoter by environmental and internal factors. Plant Mol Biol 69:593–604

    Article  CAS  PubMed  Google Scholar 

  • Copolovici L, Kännaste A, Remmel T, Vislap V, Niinemets Ü (2011) Volatile emissions from Alnus glutinosa induced by herbivory are quantitatively related to the extent of damage. J Chem Ecol 37:18–28

    Article  CAS  PubMed  Google Scholar 

  • Cori O, Rojas MC (1985) Carbocyclases from Citrus limonum. In: Law JH, Rilling HC, Kaplan NO (eds) Steroids and isoprenoids part A, vol 110, Methods in enzymology. Academic, Orlando/San Diego/New York/London/Toronto/Montreal/Sydney/Tokyo, pp 406–417

    Chapter  Google Scholar 

  • Crispin MC, Wurtele ES (2013) Use of metabolomics and transcriptomics to gain insights into the regulation and biosynthesis of medicinal compounds: Hypericum as a model. In: Chandra S, Lata H, Varma A (eds) Biotechnology for medicinal plants. Springer, Berlin, pp 395–411

    Chapter  Google Scholar 

  • Croteau R (1987) Biosynthesis and catabolism of monoterpenoids. Chem Rev 87:929–954

    Article  CAS  Google Scholar 

  • Croteau R, Karp F (1977) Biosynthesis of monoterpenes: partial purification and characterization of 1,8-cineole synthetase from Salvia officinalis. Arch Biochem Biophys 179:257–265

    Article  CAS  PubMed  Google Scholar 

  • Croteau R, Hooper CL, Felton M (1978) Biosynthesis of monoterpenes. Partial purification and characterization of a bicyclic monoterpenol dehydrogenase from sage (Salvia officinalis). Arch Biochem Biophys 188:182–193

    Article  CAS  PubMed  Google Scholar 

  • Crozier A, Clifford MN, Ashihara H (eds) (2006) Plant secondary metabolites, occurrence, structure and role in the human diet. Blackwell Publishing Ltd, Oxford

    Google Scholar 

  • Degenhardt J, Gershenzon J, Naldwin IT, Kessler A (2003) Attracting friends and feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14:169–176

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dehal SS, Croteau R (1988) Partial purification and characterization of two sesquiterpene cyclases from sage (Salvia officinalis) which catalyze the respective conversion of farnesyl pyrophosphate to humulene and caryophyllene. Arch Biochem Biophys 261:346–356

    Article  CAS  PubMed  Google Scholar 

  • Dewick PM (2002) The biosynthesis of C5-C25 terpenoid compounds. Nat Prod Rep 19:181–222

    Article  CAS  PubMed  Google Scholar 

  • Dicke M, Bruin J (2001) Chemical information transfer between plants: back to the future. Biochem Syst Ecol 29:981–994

    Article  CAS  Google Scholar 

  • Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324

    Article  CAS  PubMed  Google Scholar 

  • Dornelas MC, Mazzafera P (2007) A genomic approach to characterization of the Citrus terpene synthase gene family. Genet Mol Biol 30:832–840

    Article  CAS  Google Scholar 

  • Dudareva N, Pichersky E (2008) Metabolic engineering of plant volatiles. Curr Opin Biotechnol 19:181–189

    Article  CAS  PubMed  Google Scholar 

  • Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Faldt J, Miller B, Bohlmann J (2003) (E)-β-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell 15:1227–1241

    Article  CAS  PubMed  Google Scholar 

  • Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902

    Article  CAS  PubMed  Google Scholar 

  • Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  • Eisenreich W, Bacher A, Arigoni D, Rohdich F (2004) Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci 61:1401–1426

    Article  CAS  PubMed  Google Scholar 

  • El Tamer MK, Smeets M, Holthuysen N, Lücker J, Tang A, Roozen J, Bouwmeester HJ, Voragen AGJ (2003) The influence of monoterpene synthase transformation on the odour of tobacco. J Biotechnol 106:15–21

    Article  CAS  PubMed  Google Scholar 

  • Engelhart GJ, Asa-Awuku A, Nenes A, Pandis SN (2008) CCN activity and droplet growth kinetics of fresh and aged monoterpene secondary organic aerosol. Atmos Chem Phys 8:3937–3949

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fares S, Loreto F, Kleist E, Wildt J (2008) Stomatal uptake and stomatal deposition of ozone in isoprene and monoterpene emitting plants. Plant Biol 10:44–54

    Article  CAS  PubMed  Google Scholar 

  • Fineschi S, Loreto F, Staudt M, Peñuelas J (2013) Diversification of volatile isoprenoid emissions from trees: evolutionary and ecological perspectives. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Fischbach RJ, Zimmer I, Steinbrecher R, Pfichner A, Schnitzler J-P (2000) Monoterpene synthase activities in leaves of Picea abies (L.) Karst. and Quercus ilex L. Phytochemistry 54:257–265

    Article  CAS  PubMed  Google Scholar 

  • Fischbach RJ, Zimmer W, Schnitzler J-P (2001) Isolation and functional analysis of a cDNA encoding a myrcene synthase from holm oak (Quercus ilex L.). Eur J Biochem 268:5633–5638

    Article  CAS  PubMed  Google Scholar 

  • Fischbach RJ, Staudt M, Zimmer I, Rambal S, Schnitzler J-P (2002) Seasonal pattern of monoterpene synthase activities in leaves of the evergreen tree Quercus ilex. Physiol Plant 114:354–360

    Article  CAS  PubMed  Google Scholar 

  • Fortunati A, Barta C, Brilli F, Centritto M, Zimmer I, Schnitzler J-P, Loreto F (2008) Isoprene emission is not temperature-dependent during and after severe drought-stress: a physiological and biochemical analysis. Plant J 55:687–697

    Article  CAS  PubMed  Google Scholar 

  • Fryxell KJ (1996) The coevolution of gene family trees. Trends Genet 12:364–369

    Article  CAS  PubMed  Google Scholar 

  • Gennadios HA, Gonzalez V, Di Costanzo L, Li A, Yu F, Miller DJ, Allemann RK, Christianson DW (2009) Crystal structure of (+)-δ-cadinene synthase from Gossypium arboreum and evolutionary divergence of metal binding motifs for catalysis. Biochemistry 48:6175–6183

    Article  CAS  PubMed  Google Scholar 

  • Gershenzon J, Croteau RB (1993) Terpenoid biosynthesis: the basic pathway and formation of monoterpenes, sesquiterpenes, and diterpenes. In: Moore TS (ed) Lipid metabolism in plants. CRC Press, Boca Raton/Ann Arbor/London/Tokyo, pp 339–388

    Google Scholar 

  • Godard K-A, Byun-McKay A, Levasseur C, Plant A, Séguin A, Bohlmann J (2007) Testing of a heterologous, wound- and insect-inducible promoter for functional genomics studies in conifer defense. Plant Cell Rep 26:2083–2090

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gough J, Karplus K, Hughey R, Chothia C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313:903–919

    Article  CAS  PubMed  Google Scholar 

  • Gowan E, Lewis BA, Turgeon R (1995) Phloem transport of antirrhinoside, an iridoid glycoside, in Asarina scandens (Scrophulariaceae). J Chem Ecol 21:1781–1788

    Article  CAS  Google Scholar 

  • Gray DW, Breneman SR, Topper LA, Sharkey TD (2011) Biochemical characterization and homology modeling of methylbutenol synthase and implications for understanding hemiterpene synthase evolution in plants. J Biol Chem 286:20582–20590

    Article  CAS  PubMed  Google Scholar 

  • Green S, Friel EN, Matich A, Beuning LL, Cooney JM, Rowan DD, MacRae E (2007) Unusual features of a recombinant apple α-farnesene synthase. Phytochemistry 68:176–188

    Article  CAS  PubMed  Google Scholar 

  • Grote R, Monson RK, Niinemets Ü (2013) Leaf-level models of constitutive and stress-driven volatile organic compound emissions. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Grotewold E (2008) Transcription factors for predictive plant metabolic engineering: are we there yet? Curr Opin Biotechnol 19:138–144

    Article  CAS  PubMed  Google Scholar 

  • Guenther A, Karl T, Harley P, Wiedinmyer C, Palmer PI, Geron C (2006) Estimates of global terrestrial isoprene emissions using MEGAN (model of emissions of gases and aerosols from nature). Atmos Chem Phys 6:3181–3210

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hamano Y, Kuzuyama T, Itoh N, Furihata K, Seto H, Dairi T (2002) Functional analysis of eubacterial diterpene cyclases responsible for biosynthesis of a diterpene antibiotic, terpentecin. J Biol Chem 277:37098–37104

    Article  CAS  PubMed  Google Scholar 

  • Hamberger B, Hall D, Yuen M, Oddy C, Hamberger B, Keeling CI, Ritland C, Ritland K, Bohlmann J (2009) Targeted isolation, sequence assembly and characterization of two white spruce (Picea glauca) BAC clones for terpenoid synthase and cytochrome P450 genes involved in conifer defence reveal insights into a conifer genome. BMC Plant Biol 9:106

    Article  PubMed  CAS  Google Scholar 

  • Harrison SP, Morfopoulos C, Dani KGS, Prentice IC, Arneth A, Atwell BJ, Barkley MP, Leishman MR, Loreto F, Medlyn BE, Niinemets Ü, Possell M, Peñuelas J, Wright IJ (2013) Volatile isoprenoid emissions from plastid to planet. New Phytol 197:49–57

    Article  CAS  PubMed  Google Scholar 

  • Haudenschild C, Schalk M, Karp F, Croteau R (2000) Functional expression of regiospecific cytochrome P450 limonene hydroxylases from mint (Mentha spp.) in Escherichia coli and Saccharomyces cerevisiae. Arch Biochem Biophys 379:127–136

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K-i, 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

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K-i, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, Hanada A, Nakashima T, Nakajima M, Mander LN, Yamane H, Hasebe M, Nozaki H (2010) Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol 153:1085–1097

    Article  CAS  PubMed  Google Scholar 

  • Heijari J, Nerg A-M, Kainulainen P, Vuorinen M, Holopainen JK (2008) Long-term effects of exogenous methyl jasmonate application on Scots pine (Pinus sylvestris) needle chemical defence and diprionid sawfly performance. Entomol Exp Appl 128:162–171

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hezari M, Lewis NG, Croteau R (1995) Purification and characterization of taxa-4(5),11(12)-diene synthase from Pacific yew (Taxus brevifolia) that catalyzes the first committed step of taxol biosynthesis. Arch Biochem Biophys 322:437–444

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, Stein C, Schroder R, Varama M, Mumm R (2005) Insect egg deposition induces defence responses in Pinus sylvestris: characterisation of the elicitor. J Exp Biol 208:1849–1854

    Article  PubMed  Google Scholar 

  • Hillwig ML, Xu M, Toyomasu T, Tiernan MS, Wei G, Cui G, Huang L, Peters RJ (2011) Domain loss has independently occurred multiple times in plant terpene synthase evolution. Plant J 68:1051–1060

    Article  CAS  PubMed  Google Scholar 

  • Hohn T (1999) Cloning and expression of terpene synthase genes. In: Cane DE (ed) Comprehensive natural products chemistry: isoprenoids including steroids and carotenoids, vol 2. Pergamon Press, Oxford, pp 155–200

    Google Scholar 

  • Holliday JA, Ralph SG, White R, Bohlmann J, Aitken SN (2008) Global monitoring of autumn gene expression within and among phenotypically divergent populations of Sitka spruce (Picea sitchensis). New Phytol 178:103–122

    Article  CAS  PubMed  Google Scholar 

  • Holopainen JK (2004) Multiple functions of inducible plant volatiles. Trends Plant Sci 9:529–533

    Article  CAS  PubMed  Google Scholar 

  • Holopainen JK, Nerg A-M, Blande JD (2013) Multitrophic signalling in polluted atmospheres. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Huang SH, Duke RK, Chebib M, Sasaki K, Wada K, Johnston GAR (2004) Ginkgolides, diterpene trilactones of Ginkgo biloba, as antagonists at recombinant α1γ2γ2L GABAA receptors. Eur J Pharmacol 494:131–138

    Article  CAS  PubMed  Google Scholar 

  • Huber DPW, Ralph S, Bohlmann J (2004) Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. J Chem Ecol 30:2399–2418

    Article  CAS  PubMed  Google Scholar 

  • Huff Hartz KE, Rosenørn T, Ferchak SR, Raymond TM, Bilde M, Donahue NM, Pandis SN (2005) Cloud condensation nuclei activation of monoterpene and sesquiterpene secondary organic aerosol. J Geophys Res Atmos 110:D14208. doi: 14210.11029/12004JD005754

    Article  CAS  Google Scholar 

  • Hyatt DC, Youn B, Zhao Y, Santhamma B, Coates RM, Croteau RB, Kang C (2007) Structure of limonene synthase, a simple model for terpenoid cyclase catalysis. Proc Natl Acad Sci USA 104:5360–5365

    Article  CAS  PubMed  Google Scholar 

  • Jin Q, Williams DC, Hezari M, Croteau R, Coates RM (2005) Stereochemistry of the macrocyclization and elimination steps in taxadiene biosynthesis through deuterium labeling. J Org Chem 70:4667–4675

    Article  CAS  PubMed  Google Scholar 

  • Jones CG, Keeling CI, Ghisalberti EL, Barbour EL, Plummer JA, Bohlmann J (2008) Isolation of cDNAs and functional characterisation of two multi-product terpene synthase enzymes from sandalwood, Santalum album L. Arch Biochem Biophys 477:121–130

    Article  CAS  PubMed  Google Scholar 

  • Jones CG, Moniodis J, Zulak KG, Scaffidi A, Plummer JA, Ghisalberti EL, Barbour EL, Bohlmann J (2011) Sandalwood fragrance biosynthesis involves sesquiterpene synthases of both the terpene synthase (Tps)-a and Tps-b subfamilies, including santalene synthases. J Biol Chem 286:17445–17454

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kane JF (1995) Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr Opin Biotechnol 6:494–500

    Article  CAS  PubMed  Google Scholar 

  • Kawaide H, Hayashi K-i, Kawanabe R, Sakigi Y, Matsuo A, Natsume M, Nozaki H (2011) Identification of the single amino acid involved in quenching the ent-kauranyl cation by a water molecule in ent-kaurene synthase of Physcomitrella patens. FEBS J 278:123–133

    Article  CAS  PubMed  Google Scholar 

  • Keeling CI, Bohlmann J (2006a) Diterpene resin acids in conifers. Phytochemistry 67:2415–2423

    Article  CAS  PubMed  Google Scholar 

  • Keeling CI, Bohlmann J (2006b) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Keeling CI, Dullat HK, Yuen M, Ralph SG, Jancsik S, Bohlmann J (2010) Identification and functional characterization of monofunctional ent-copalyl diphosphate and ent-kaurene synthases in white spruce reveal different patterns for diterpene synthase evolution for primary and secondary metabolism in gymnosperms. Plant Physiol 152:1197–1208

    Article  CAS  PubMed  Google Scholar 

  • Keeling CI, Weisshaar S, Ralph SG, Jancsik S, Hamberger B, Dullat HK, Bohlmann J (2011) Transcriptome mining, functional characterization, and phylogeny of a large terpene synthase gene family in spruce (Picea spp.). BMC Plant Biol 11:43

    Article  CAS  PubMed  Google Scholar 

  • Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371

    Article  CAS  PubMed  Google Scholar 

  • Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88

    Article  CAS  Google Scholar 

  • Köksal M, Zimmer I, Schnitzler J-P, Christianson DW (2010) Structure of isoprene synthase illuminates the chemical mechanism of teragram atmospheric carbon emission. J Mol Biol 402:363–373

    Article  PubMed  CAS  Google Scholar 

  • Köksal M, Hu H, Coates RM, Peters RJ, Christianson DW (2011a) Structure and mechanism of the diterpene cyclase ent-copalyl diphosphate synthase. Nat Chem Biol 7:431–433

    Article  PubMed  CAS  Google Scholar 

  • Köksal M, Jin Y, Coates RM, Croteau R, Christianson DW (2011b) Taxadiene synthase structure and evolution of modular architecture in terpene biosynthesis. Nature 469:116–120

    Article  PubMed  CAS  Google Scholar 

  • Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions. Phytochemistry 65:1895–1902

    Article  PubMed  CAS  Google Scholar 

  • Koyama T, Ogura K (1999) Isopentenyl diphosphate isomerase and prenyltransferases. In: Cane DE (ed) Comprehensive natural product chemistry: isoprenoids including carotenoids and steroids, vol 2. Pergamon Press, Oxford, pp 69–96

    Chapter  Google Scholar 

  • Kulmala M, Nieminen T, Chellapermal R, Makkonen R, Bäck J, Kerminen V-M (2013) Climate feedbacks linking the increasing atmospheric CO2 concentration, BVOC emissions, aerosols and clouds in forest ecosystems. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Laothawornkitkul J, Taylor JE, Paul ND, Hewitt CN (2009) Biogenic volatile organic compounds in the Earth system. New Phytol 183:27–51

    Article  CAS  PubMed  Google Scholar 

  • Laule O, Fürholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6866–6871

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Chappell J (2008) Biochemical and genomic characterization of terpene synthases in Magnolia grandiflora. Plant Physiol 147:1017–1033

    Article  CAS  PubMed  Google Scholar 

  • Lee A, Goldstein AH, Kroll JH, Ng NL, Varutbangkul V, Flagan RC, Seinfeld JH (2006) Gas-phase products and secondary aerosol yields from the photooxidation of 16 different terpenes. J Geophys Res Atmos 111:D17305

    Article  CAS  Google Scholar 

  • Lesburg CA, Zhai G, Cane DE, Christianson DW (1997) Crystal structure of pentalenene synthase: mechanistic insights on terpenoid cyclization reactions in biology. Science 277:1820–1824

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Sharkey T (2013a) Metabolic profiling of the methylerythritol phosphate pathway reveals the source of post-illumination isoprene burst from leaves. Plant Cell Environ 36:429–437

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Sharkey TD (2013b) Molecular and pathway controls on biogenic volatile organic compound emissions. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Li G, Köllner TG, Yin Y, Jiang Y, Chen H, Xu Y, Gershenzon J, Pichersky E, Chen F (2012) Nonseed plant Selaginella moellendorffii has both seed plant and microbial types of terpene synthases. Proc Natl Acad Sci USA 109:14711–14715

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Rohmer M, Schwender J (1997a) Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol Plant 101:643–652

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Schwender J, Disch A, Rohmer M (1997b) Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett 400:271–274

    Article  CAS  PubMed  Google Scholar 

  • Little DB, Croteau RB (2002) Alteration of product formation by directed mutagenesis and truncation of the multiple-product sesquiterpene synthases δ-selinene synthase and γ-humulene synthase. Arch Biochem Biophys 402:120–135

    Article  CAS  PubMed  Google Scholar 

  • Litvak ME, Monson RK (1998) Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory. Oecologia 114:531–540

    Article  Google Scholar 

  • Liu L, Li Y, Li S, Hu N, He Y, Pong R, Lin D, Lu L, Law M (2012) Comparison of next-generation sequencing systems. J Biomed Biotechnol 2012:251364

    PubMed  Google Scholar 

  • Loivamäki M, Gilmer F, Fischbach RJ, Sörgel C, Bachl A, Walter A, Schnitzler J-P (2007a) Arabidopsis, a model to study biological functions of isoprene emission? Plant Physiol 144:1066–1078

    Article  PubMed  CAS  Google Scholar 

  • Loivamäki M, Louis S, Cinege G, Zimmer I, Fischbach RJ, Schnitzler J-P (2007b) Circadian rhythms of isoprene biosynthesis in grey poplar leaves. Plant Physiol 143:540–551

    Article  PubMed  CAS  Google Scholar 

  • Loivamäki M, Mumm R, Dicke M, Schnitzler J-P (2008) Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc Natl Acad Sci USA 105:17430–17435

    Article  PubMed  Google Scholar 

  • Loreto F, Fischbach RJ, Schnitzler J-P, Ciccioli P, Brancaleoni E, Calfapietra C, Seufert G (2001a) Monoterpene emission and monoterpene synthase activities in the Mediterranean evergreen oak Quercus ilex L. grown at elevated CO2. Glob Change Biol 7:709–717

    Article  Google Scholar 

  • Loreto F, Mannozzi M, Maris C, Nascetti P, Ferranti F, Pasqualini S (2001b) Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiol 126:993–1000

    Article  CAS  PubMed  Google Scholar 

  • Lücker J, El Tamer MK, Schwab W, Verstappen FWA, van der Plas LHW, Bouwmeester HJ, Verhoeven HA (2002) Monoterpene biosynthesis in lemon (Citrus limon). cDNA isolation and functional analysis of four monoterpene synthases. Eur J Biochem 269:3160–3171

    Article  PubMed  CAS  Google Scholar 

  • Majdi M, Liu Q, Karimzadeh G, Malboobi MA, Beekwilder J, Cankar K, de Vos R, Todorovic S, Simonovic A, Bouwmeester H (2011) Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.). Phytochemistry 72:1739–1750

    Article  CAS  PubMed  Google Scholar 

  • Martin D, Bohlmann J (2005) Molecular biochemistry and genomics of terpenoid defenses in conifers. In: Romeo JT (ed) Recent advances in phytochemistry, vol 39. Elsevier, Amsterdam, pp 29–56

    Google Scholar 

  • Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129:1003–1018

    Article  CAS  PubMed  Google Scholar 

  • Martin D, Bohlmann J, Gershenzon J, Francke W, Seybold SJ (2003) A novel sex-specific and inducible monoterpene synthase activity associated with a pine bark beetle, the pine engraver, Ips pini. Naturwissenschaften 90:173–179

    CAS  PubMed  Google Scholar 

  • Martin DM, Faldt J, Bohlmann J (2004) Functional characterization of nine Norway spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol 135:1908–1927

    Article  CAS  PubMed  Google Scholar 

  • Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O, Lund ST, Bohlmann J (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10:226

    Article  PubMed  CAS  Google Scholar 

  • Mayrhofer S, Teuber M, Zimmer I, Louis S, Fischbach RJ, Schnitzler J-P (2005) Diurnal and seasonal variation of isoprene biosynthesis-related genes in grey poplar leaves. Plant Physiol 139:474–484

    Article  CAS  PubMed  Google Scholar 

  • McAndrew RP, Peralta-Yahya PP, DeGiovanni A, Pereira JH, Hadi MZ, Keasling JD, Adams PD (2011) Structure of a three-domain sesquiterpene synthase: a prospective target for advanced biofuels production. Structure 19:1876–1884

    Article  CAS  PubMed  Google Scholar 

  • Miller B, Oschinski C, Zimmer W (2001) First isolation of an isoprene synthase gene and successful expression of the gene from poplar in E. coli. Planta 213:483–487

    Article  CAS  PubMed  Google Scholar 

  • Miller B, Madilao LL, Ralph S, Bohlmann J (2005) Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol 137:369–382

    Article  CAS  PubMed  Google Scholar 

  • Ming R, Yu Q, Moore PH, Paull RE, Chen NJ, Wang M-L, Zhu YJ, Schuler MA, Jiang J, Paterson AH (2008) Genome of papaya, a fast growing tropical fruit tree. Tree Genet Genomes 8:445–462

    Article  Google Scholar 

  • Modolo LV, Reichert AI, Dixon RA, Osbourn AE, Lanzotti V (2009) Introduction to the different classes of biosynthetic enzymes. In: Osbourn AE, Lanzotti V (eds) Plant-derived natural products synthesis, function, and application. Springer, New York, pp 143–163

    Chapter  Google Scholar 

  • Monson RK (2013) Metabolic and gene expression controls on the production of biogenic volatile organic compounds. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Monson RK, Jaeger CH, Adams WW III, Driggers EM, Silver GM, Fall R (1992) Relationships among isoprene emission rate, photosynthesis, and isoprene synthase activity as influenced by temperature. Plant Physiol 98:1175–1180

    Article  CAS  PubMed  Google Scholar 

  • Monson RK, Jones RT, Rosenstiel TN, Schnitzler J-P (2013) Why only some plants emit isoprene. Plant Cell Environ 33:503–516. doi:10.1111/pce.12015

    Article  CAS  Google Scholar 

  • Morrone D, Chambers J, Lowry L, Kim G, Anterola A, Bender K, Peters RJ (2009) Gibberellin biosynthesis in bacteria: separate ent-copalyl diphosphate and ent-kaurene synthases in Bradyrhizobium japonicum. FEBS Lett 583:475–480

    Article  CAS  PubMed  Google Scholar 

  • Murzin AG, Brenner SE, Hubbard T, Chothia C (2001) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536–540

    Google Scholar 

  • Myllykangas S, Buenrostro J, Ji HP (2012) Overview of sequencing technology platforms. In: Rodríguez-Ezpeleta N, Hackenberg M, Aransay AM (eds) Bioinformatics for high throughput sequencing. Springer, Berlin, pp 11–25

    Chapter  Google Scholar 

  • Nagegowda DA (2010) Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett 584:2965–2973

    Article  CAS  PubMed  Google Scholar 

  • Nagegowda DA, Gutensohn M, Wilkerson CG, Dudareva N (2008) Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers. Plant J 55:224–239

    Article  CAS  PubMed  Google Scholar 

  • Nakano C, Hoshino T (2009) Characterization of the Rv3377c gene product, a type-B diterpene cyclase, from the Mycobacterium tuberculosis H37 genome. Chembiochem 10:2060–2071

    Article  CAS  PubMed  Google Scholar 

  • Owen SM, Peñuelas J (2005) Opportunistic emissions of volatile isoprenoids. Trends Plant Sci 10:420–426

    Article  CAS  PubMed  Google Scholar 

  • Pechous SW, Whitaker BD (2004) Cloning and functional expression of an (E,E)-α-farnesene synthase cDNA from peel tissue of apple fruit. Planta 219:84–94

    Article  CAS  PubMed  Google Scholar 

  • Peralta-Yahya PP, Zhang F, del Cardayre SB, Keasling JD (2012) Microbial engineering for the production of advanced biofuels. Nature 488:320–328

    Article  CAS  PubMed  Google Scholar 

  • Peters RJ, Croteau RB (2002) Abietadiene synthase catalysis: conserved residues involved in protonation-initiated cyclization of geranylgeranyl diphosphate to (+)-copalyl diphosphate. Biochemistry 41:1836–1842

    Article  CAS  PubMed  Google Scholar 

  • Peters RJ, Ravn MM, Coates RM, Croteau RB (2001) Bifunctional abietadiene synthase: free diffusive transfer of the (+)-copalyl diphosphate intermediate between two distinct active sites. J Am Chem Soc 123:8974–8978

    Article  CAS  PubMed  Google Scholar 

  • Phillips MA, Wildung MR, Williams DC, Hyatt DC, Croteau R (2003) cDNA isolation, functional expression, and characterization of (+)-α-pinene synthase and (−)-α-pinene synthase from loblolly pine (Pinus taeda): stereocontrol in pinene biosynthesis. Arch Biochem Biophys 411:267–276

    Article  CAS  PubMed  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  CAS  PubMed  Google Scholar 

  • Pichersky E, Lewinsohn E, Croteau R (1995) Purification and characterization of S-linalool synthase, an enzyme involved in the production of floral scent in Clarkia breweri. Arch Biochem Biophys 316:803–807

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    Article  CAS  PubMed  Google Scholar 

  • Possell M, Loreto F (2013) The role of volatile organic compounds in plant resistance to abiotic stresses: responses and mechanisms. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Prlic A, Bliven S, Rose PW, Bluhm WF, Bizon C, Godzik A, Bourne PE (2010) Pre-calculated protein structure alignments at the RCSB PDB website. Bioinformatics 26:2983–2985

    Article  CAS  PubMed  Google Scholar 

  • Prosser I, Altug IG, Phillips AL, König WA, Bouwmeester HJ, Beale MH (2004) Enantiospecific (+)- and (−)-germacrene D synthases, cloned from goldenrod, reveal a functionally active variant of the universal isoprenoid-biosynthesis aspartate-rich motif. Arch Biochem Biophys 432:136–144

    Article  CAS  PubMed  Google Scholar 

  • Raffa KF, Aukema BH, Erbilgin N, Klepzig KD, Wallin KF (2005) Interactions among conifer terpenoids and bark beetles across multiple levels of scale: an attempt to understand links between population patterns and physiological processes. In: Romeo JT (ed) Chemical ecology and phytochemistry of forest ecosystems. Recent advances in phytochemistry, vol 39. Elsevier, Amsterdam, pp 79–118

    Chapter  Google Scholar 

  • Rasulov B, Copolovici L, Laisk A, Niinemets Ü (2009) Postillumination isoprene emission: in vivo measurements of dimethylallyldiphosphate pool size and isoprene synthase kinetics in aspen leaves. Plant Physiol 149:1609–1618

    Article  CAS  PubMed  Google Scholar 

  • Rasulov B, Hüve K, Laisk A, Niinemets Ü (2011) Induction of a longer-term component of isoprene release in darkened aspen leaves: origin and regulation under different environmental conditions. Plant Physiol 156:816–831

    Article  CAS  PubMed  Google Scholar 

  • Ro D-K, Bohlmann J (2006) Diterpene resin acid biosynthesis in loblolly pine (Pinus taeda): functional characterization of abietadiene/levopimaradiene synthase (PtTPS-LAS) cDNA and subcellular targeting of PtTPS-LAS and abietadienol/abietadienal oxidase (PtAO, CYP720B1). Phytochemistry 67:1572–1578

    Article  CAS  PubMed  Google Scholar 

  • Ro DK, Arimura GL, Lau SYW, Piers E, Bohlmann J (2005) Loblolly pine abietadienol/abietadienal oxidase PtAO (CYP720B1) is a multifunctional, multisubstrate cytochrome P450 monooxygenase. Proc Natl Acad Sci USA 102:8060–8065

    Article  CAS  PubMed  Google Scholar 

  • Rohmer M, Knani M, Simonin P, Sutter B, Sahm H (1993) Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J 295:517–524

    CAS  PubMed  Google Scholar 

  • Rosenkranz M, Schnitzler J-P (2013) Genetic engineering of BVOC emissions from trees. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Rynkiewicz MJ, Cane DE, Christianson DW (2001) Structure of trichodiene synthase from Fusarium sporotrichioides provides mechanistic inferences on the terpene cyclization cascade. Proc Natl Acad Sci USA 98:13543–13548

    Article  CAS  PubMed  Google Scholar 

  • Sallaud C, Rontein D, Onillon S, Jabès F, Duffé 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

    Article  CAS  PubMed  Google Scholar 

  • Saranitzky E, White CM, Baker EL, Baker WL, Coleman CI (2009) Feverfew for migraine prophylaxis: a systematic review. J Dietary Suppl 6:91–103

    Article  Google Scholar 

  • Sasaki K, Ohara K, Yazaki K (2005) Gene expression and characterization of isoprene synthase from Populus alba. FEBS Lett 579:2514–2518

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Saito T, Lämsä M, Oksman-Caldentey K-M, Suzuki M, Ohyama K, Muranaka T, Ohara K, Yazaki K (2007) Plants utilize isoprene emission as a thermotolerance mechanism. Plant Cell Physiol 48:1254–1262

    Article  CAS  PubMed  Google Scholar 

  • Schepmann HG, Pang J, Matsuda SPT (2001) Cloning and characterization of Ginkgo biloba levopimaradiene synthase, which catalyzes the first committed step in ginkgolide biosynthesis. Arch Biochem Biophys 392:263–269

    Article  CAS  PubMed  Google Scholar 

  • Schnitzler J-P, Zimmer I, Bachl A, Arend M, Fromm J, Fischbach R (2005) Biochemical properties of isoprene synthase in poplar (Populus x canescens). Planta 222:777–786

    Article  CAS  PubMed  Google Scholar 

  • Seemann M, Rohmer M (2007) Isoprenoid biosynthesis via the methylerythritol phosphate pathway: GcpE and LytB, two novel iron-sulphur proteins. Comptes Rendus Chimie 10:748–755

    Article  CAS  Google Scholar 

  • Seemann M, Bui BTS, Wolff M, Miginiac-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

    Article  CAS  PubMed  Google Scholar 

  • Seigler DS (1998) Plant secondary metabolism. Springer, New York

    Book  Google Scholar 

  • Sharkey TD, Singsaas EL (1995) Why plants emit isoprene. Nature 374:769

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Yeh S, Wiberley AE, Falbel TG, Gong D, Fernandez DE (2005) Evolution of the isoprene biosynthetic pathway in kudzu. Plant Physiol 137:700–712

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot 101:5–18

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Gray DW, Pell HK, Breneman SR, Topper L (2013) Isoprene synthase genes form a monophyletic clade of acyclic terpene synthases in the Tps-b terpene synthase family. Evolution 67:1026–1040. doi:10.1111/evo.12013

    Google Scholar 

  • Sharp PM, Li W-H (1987) The codon adaptation index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295

    Article  CAS  PubMed  Google Scholar 

  • Shiraki T, Kondo S, Katayama S, Waki K, Kasukawa T, Kawaji H, Kodzius R, Watahiki A, Nakamura M, Arakawa T, Fukuda S, Sasaki D, Podhajska A, Harbers M, Kawai J, Carninci P, Hayashizaki Y (2003) Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage. Proc Natl Acad Sci USA 100:15776–15781

    Article  CAS  PubMed  Google Scholar 

  • Siedenburg G, Jendrossek D (2011) Squalene-hopene cyclases. Appl Environ Microbiol 77:3905–3915

    Article  CAS  PubMed  Google Scholar 

  • Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiol 115:1413–1420

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Staudt M, Joffre R, Rambal S (2003) How growth conditions affect the capacity of Quercus ilex leaves to emit monoterpenes. New Phytol 158:61–73

    CAS  Google Scholar 

  • Steele CL, Katoh S, Bohlmann J, Croteau R (1998) Regulation of oleoresins in grand fir (Abies grandis). Differential transcriptional control of monoterpene, sesquiterpene, and diterpene synthase genes in response to wounding. Plant Physiol 116:1497–1504

    Article  CAS  PubMed  Google Scholar 

  • Stofer Vogel B, Wildung MR, Vogel G, Croteau R (1996) Abietadiene synthase from grand fir (Abies grandis). cDNA isolation, characterization, and bacterial expression of a bifunctional diterpene cyclase involved in resin acid biosynthesis. J Biol Chem 271:23262–23268

    Article  Google Scholar 

  • Sun Z, Niinemets Ü, Hüve K, Noe SM, Rasulov B, Copolovici L, Vislap V (2012) Enhanced isoprene emission capacity and altered light responsiveness in aspen grown under elevated atmospheric CO2 concentration. Glob Change Biol 18:3423–3440

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Thaler JS (2002) Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J Anim Ecol 71:141–150

    Article  Google Scholar 

  • Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304

    Article  CAS  PubMed  Google Scholar 

  • Tissier A (2012) Interactions among conifer terpenoids and bark beetles across multiple levels of scale: an attempt to understand links between population patterns and physiological processes. In: Çiftçi YO (ed) Transgenic plants – advances and limitations. InTech, Rijeka, pp 353–378

    Google Scholar 

  • Trapp SC, Croteau RB (2001) Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 158:811–832

    CAS  PubMed  Google Scholar 

  • Trowbridge AM, Stoy PC (2013) BVOC-mediated plant-herbivore interactions. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –

    Google Scholar 

  • Trusheva B, Todorov I, Ninova M, Najdenski H, Daneshmand A, Bankova V (2010) Antibacterial mono- and sesquiterpene esters of benzoic acids from Iranian propolis. Chem Cent J 4:8

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen G-L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé J-C, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C-J, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Ujino-Ihara T, Yoshimura K, Ugawa Y, Yoshimaru H, Nagasaka K, Tsumura Y (2000) Expression analysis of ESTs derived from the inner bark of Cryptomeria japonica. Plant Mol Biol 43:451–457

    Article  CAS  PubMed  Google Scholar 

  • van Schie CCN, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64:251–263

    Article  CAS  PubMed  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487

    Article  CAS  PubMed  Google Scholar 

  • Velikova V, Várkonyi Z, Szabó M, Maslenkova L, Nogues I, Kovács L, Peeva V, Busheva M, Garab G, Sharkey TD, Loreto F (2011) Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques. Plant Physiol 157:905–916

    Article  CAS  PubMed  Google Scholar 

  • Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009a) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291

    Article  CAS  PubMed  Google Scholar 

  • Vickers CE, Possell M, Cojocariu CI, Velikova VB, Laothawornkitkul J, Ryan A, Mullineaux PM, Hewitt CN (2009b) Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant Cell Environ 32:520–531

    Article  CAS  PubMed  Google Scholar 

  • Vickers CE, Possell M, Hewitt CN, Mullineaux PM (2010) Genetic structure and regulation of isoprene synthase in poplar (Populus spp.). Plant Mol Biol 73:547–558

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vogel BS, Wildung MR, Vogel G, Croteau R (1996) Abietadiene synthase from grand fir (Abies grandis). cDNA isolation, characterization, and bacterial expression of a bifunctional diterpene cyclase involved in resin acid biosynthesis. J Biol Chem 271:23262–23268

    Article  CAS  PubMed  Google Scholar 

  • Vu TT, Vohradsky J (2007) Nonlinear differential equation model for quantification of transcriptional regulation applied to microarray data of Saccharomyces cerevisiae. Nucleic Acids Res 35:279–287

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  PubMed  Google Scholar 

  • Wanke M, Skorupinska-Tudek K, Swiezewska E (2001) Isoprenoid biosynthesis via 1-deoxy-D-xylulose 5-phosphate/2-C-methyl-D-erythritol 4-phosphate (DOXP/MEP) pathway. Acta Biochim Pol 48:663–672

    CAS  PubMed  Google Scholar 

  • Wendt KU, Poralla K, Schulz GE (1997) Structure and function of a squalene cyclase. Science 277:1811–1815

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wiberley AE, Donohue AR, Meier ME, Westphal MM, Sharkey TD (2008) Regulation of isoprene emission in Populus trichocarpa leaves subjected to changing growth temperature. Plant Cell Environ 31:258–267

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wildermuth MC, Fall R (1996) Light-dependent isoprene emission. Characterization of a thylakoid-bound isoprene synthase in Salix discolor chloroplasts. Plant Physiol 112:171–182

    CAS  PubMed  Google Scholar 

  • Wildermuth MC, Fall R (1998) Biochemical characterization of stromal and thylakoid-bound isoforms of isoprene synthase in willow leaves. Plant Physiol 116:1111–1123

    Article  CAS  PubMed  Google Scholar 

  • Wildung MR, Croteau R (1996) A cDNA clone for taxadiene synthase, the diterpene cyclase that catalyzes the committed step of taxol biosynthesis. J Biol Chem 271:9201–9204

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson MJ, Monson RK, Trahan N, Lee S, Brown E, Jackson RB, Polley HW, Fay PA, Fall R (2009) Leaf isoprene emission rate as a function of atmospheric CO2 concentration. Glob Change Biol 15:1189–1200

    Article  Google Scholar 

  • Williams DC, Wildung MR, Jin AQ, Dalal D, Oliver JS, Coates RM, Croteau R (2000) Heterologous expression and characterization of a “pseudomature” form of taxadiene synthase involved in paclitaxel (taxol) biosynthesis and evaluation of a potential intermediate and inhibitors of the multistep diterpene cyclization reaction. Arch Biochem Biophys 379:137–146

    Article  CAS  PubMed  Google Scholar 

  • Wilson D, Pethica R, Zhou Y, Talbot C, Vogel C, Madera M, Chothia C, Gough J (2009) SUPERFAMILY – sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res 37:D380–D386

    Article  CAS  PubMed  Google Scholar 

  • Wu S, 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

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Wu J, Deng C, Gou C, Zhou W, Yin H, Qin G, Sha Y, Tao Y, Chen H, Yang Y, Song Y, Zhan D, Wang J, Li L, Dai M, Gu C, Wang Y, Shi D, Wang X, Zhang H, Zeng L, Zheng D, Wang C, Chen M, Wang G, Xie L, Sovero V, Sha S, Huang W, Zhang S, Zhang M, Sun J, Xu L, Li Y, Liu X, Li Q, Shen J, Wang J, Paull RE, Bennetzen JL, Wang J, Zhang S (2013) The genome of pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408. doi:10.1101/gr.144311.144112

    Article  CAS  PubMed  Google Scholar 

  • Xie X, Kirby J, Keasling JD (2012) Functional characterization of four sesquiterpene synthases from Ricinus communis (castor bean). Phytochemistry 78:20–28

    Article  CAS  PubMed  Google Scholar 

  • Yin SH, Mei L, Newman J, Back K, Chappell J (1997) Regulation of sesquiterpene cyclase gene expression – characterization of an elicitor- and pathogen-inducible promoter. Plant Physiol 115:437–451

    Article  CAS  PubMed  Google Scholar 

  • Zerbe P, Chiang A, Bohlmann J (2012a) Mutational analysis of white spruce (Picea glauca) ent-kaurene synthase (PgKS) reveals common and distinct mechanisms of conifer diterpene synthases of general and specialized metabolism. Phytochemistry 74:30–39

    Article  CAS  PubMed  Google Scholar 

  • Zerbe P, Chiang A, Yuen M, Hamberger B, Hamberger B, Draper JA, Britton R, Bohlmann J (2012b) Bifunctional cis-abienol synthase from Abies balsamea discovered by transcriptome sequencing and its implications for diterpenoid fragrance production. J Biol Chem 287:12121–12131

    Article  CAS  PubMed  Google Scholar 

  • Zhou K, Peters RJ (2009) Investigating the conservation pattern of a putative second terpene synthase divalent metal binding motif in plants. Phytochemistry 70:366–369

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Authors’ work on plant volatiles is funded by the Estonian Ministry of Science and Education (institutional grant IUT-8-3), the European Science Foundation (Eurocores project A-BIO-VOC), the European Commission through European Regional Fund (the Center of Excellence in Environmental Adaptation) and the European Research Council (advanced grant 322603, SIP-VOL+). We thank Dr. Maaria Rosenkranz for insightful comments on the manuscript.

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Memari, H.R., Pazouki, L., Niinemets, Ü. (2013). The Biochemistry and Molecular Biology of Volatile Messengers in Trees. In: Niinemets, Ü., Monson, R. (eds) Biology, Controls and Models of Tree Volatile Organic Compound Emissions. Tree Physiology, vol 5. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6606-8_3

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