• Please log in or register to access this feature.
You have free access to this content

Terpenoid Biosynthesis and Specialized Vascular Cells of Conifer Defense

  1. Katherine G. Zulak,
  2. Jörg Bohlmann*

Article first published online: 11 JAN 2010

DOI: 10.1111/j.1744-7909.2010.00910.x

Issue

Journal of Integrative Plant Biology

Journal of Integrative Plant Biology

Volume 52, Issue 1, pages 86–97, January 2010

Additional Information

How to Cite

Zulak, K. G. and Bohlmann, J. (2010), Terpenoid Biosynthesis and Specialized Vascular Cells of Conifer Defense. Journal of Integrative Plant Biology, 52: 86–97. doi: 10.1111/j.1744-7909.2010.00910.x

Author Information

  1. Michael Smith Laboratories, University of British Columbia, Vancouver BC V6T 1Z4, Canada

* *Corresponding author Tel: +1 604 822 0282; Fax: +1 604 822 2114; E-mail: bohlmann@msl.ubc.ca Available online on 6 January 2010 at http://www.jipb.net and http://www.interscience.wiley.com/journal/jipb

Publication History

  1. Issue published online: 11 JAN 2010
  2. Article first published online: 11 JAN 2010
  3. Received 17 Nov. 2009 Accepted 18 Nov. 2009

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (743K)

References

  • Alfaro R, Borden JH, King JN, Tomlin ES, Mcintosh RL, Bohlmann J (2002) Mechanisms of resistance in conifers against shoot infesting insects. In: WagnerMR, ClancyKM, LieutierF, PaineTD, eds. Mechanisms and Deployment of Resistance in Trees to Insects. Kluwer Academic Press, Dordrecht .
  • Bannan MW (1936) Vertical resin ducts in the secondary wood of the Abietineae. New Phytol. 35, 11–46.
    Direct Link:
  • Bohlmann J, Crock J, Jetter R, Croteau RB (1998a) Terpenoid-based defences 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.
  • Bohlmann J, Gershenzon J (2009) Old substrates for new enzymes of terpenoid biosynthesis. Proc. Natl. Acad. Sci. USA 106, 10402–10403.
  • Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J. 54, 656–669.
    Direct Link:
  • Bohlmann J, Meyer-Gauen G, Croteau RB (1998b) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc. Natl. Acad. Sci. USA 95, 4126–4133.
  • Bohlmann J, Phillips MA, Ramachandiran V, Katoh S, Croteau RB (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.
  • Bohlmann J, Steele C L, Croteau RB (1997) Monoterpene synthesis 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.
  • Bouvier F, Suire C, D’harlingue A, Backhause RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J. 24, 241–252.
    Direct Link:
  • Burke C, Croteau RB (2002a) Geranyl diphosphate synthase from Abies grandis: cDNA isolation, functional expression, and characterization. Arch. Biochem. Biophys. 405, 130–136.
  • Burke C, Croteau RB (2002b) Interaction with the small subunit of geranyldiphosphate synthase modifies the chain length specificity of geranylgeranyl diphosphate synthase to produced geranyl diphosphate. J. Biol. Chem. 277, 3141–3149.
  • Burke C, Klettke K, Croteau RB (2004) Heteromeric geranyl diphospahte synthase from mint: construction of a functional fusion protein and inhibition by bisphosphate substrate analogs. Arch. Biochem. Biophys. 422, 52–60.
  • 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.
  • 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.
  • Cane DE (1999) Sesquiterpene biosynthesis: cyclization mechanisms. In: CaneDE, ed. Comprehensive Natural Products Chemistry: Isoprenoids, Including Carotenoids and Steroids. Pergamon Press, Oxford .
  • Chappell J (1995) Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 46, 521–547.
  • Christiansen E, Franceschi VR, Nagy NE, Krekling T, Berryman AA, Krokene P, Solheim H (1999) Traumatic resin duct formation in Norway spruce (Picea abies (L.) Karst.) after wounding or infection with a bark beetle-associated blue-stain fungus (Ceratocystis polonica Siem.). In: LieutierF, MatsonWS, WagneMR, eds. Physiology and Genetics of Tree-pytophage Interactions. Les Colloques de l’INRA Editions, Versaille .
  • Christianson DW (2006) Structural biology and chemistry of the terpenoid cyclases. Chem. Rev. 106, 3412–3442.
  • Davis EM, Croteau RB (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. Top Curr. Chem. 209, 53–95.
  • Disch A, Hemmerlin A, Bach TJ, Rohmer M (1998) Mevalonate-derived ispentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl side chains in tobacco BY-2 cells. Biochem. J. 331, 615–621.
  • Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Fäldt 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.
  • Estevez JM, Cantero A, Reindl A, Reichler S, Leon P (2001) 1-deoxy-D-xylulose-5-phosphate synthase, a limiting step for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem. 276.
  • Fäldt J, Martin DM, Miller B, Rawat S, Bohlmann J (2003) Traumatic resin defense in Norway spruce (Picea abies): Methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Mol. Biol. 2003, 119–133.
  • Franceschi VR, Krekling T, Christiansen E (2002a) Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defence-related responses in the phloem and xylem. Am. J. Bot. 89, 578–586.
  • Franceschi VR, Krekling T, Christiansen E (2002b) Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am. J. Bot. 89, 578–586.
  • Franceschi VR, Kronkene P, Christiansen E, Krekling T (2005) Anatomical and chemical defense of conifer bark against bark beetles and other pests. New Phytol. 167, 353–376.
    Direct Link:
  • Gershenzon J, Kreis W (1999) Biochemistry of terpenoids: monoterpenes, sesquiterpenes, diterpenes, sterols, cardiac glycosides, and steroid saponins. In: WinkM, ed. Biochemistry of Plant Secondary Metabolism, Annual Plant Reviews. Sheffield Academic Press, Scheffield .
  • Hamberger B, Bohlmann J (2006) Cytochrome P450 monooxygenases in conifer genomes: Discovery of members of the terpenoid oxygenase superfamily in spruce and pine. Biochem. Soc. Trans. 34, 1209–1214.
  • 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.
  • Hefner J, Ketchum RE, Croteau RB (1998) Cloning and functional expression of of a cDNA encoding geranylgeranyl diphosphate synthase from Taxus canadiensis and assessments of the role of this prenyltransferase in cells induced for taxol production. Arch. Biochem. Biophys. 260, 62–74.
  • Huber DPW, Philippe RN, Godard KA, Bohlmann J (2005) Characterization of four monoterpene synthase cDNAs from methyl jasmonate-induced Douglas fir (Pseudotsuga menziesii). Phytochemistry 66, 1427–1439.
  • Hudgens JW, Christiansen E, Franceschi VR (2003) Methyl jasmonate induces changes mimicking anatomical defenses in diverse members of the Pinaceae. Tree Physiol. 23, 361–371.
  • Hudgins JW, Christiansen E, Franceschi VR (2003) Methyl jasmonate induces changes mimicking anatomical defenses in diverse members of the Pinaceae. Tree Physiol. 23, 361–371.
  • Hudgins JW, Franceschi VR (2004) Methyl jasmonate-induced ethylene production is responsible for conifer phloem defense responses and reprogramming of stem cambial zone for traumatic resin duct formation. Plant Physiol. 135, 2314–2149.
  • Hudgins JW, Ralph S, Franceschi VR, Bohlmann J (2006) Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in resin duct and phenolic parenchyma cells. Planta 224, 865–877.
  • Kaukinen KH, Tranbarger TJ, Misra S (1996) Post germination induced and hormonally dependent expression of low molecular weight heat shock protein genes in Douglas fir. Plant Mol. Biol. 30, 1115–1128.
  • Keeling CI, Bohlmann J (2006a) Diterpene resin acids in conifers. Phytochemistry 67.
  • 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.
    Direct Link:
  • 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.
  • Ketchum RE, Gibson DM, Croteau RB, Shuler ML (1999) The kinetics of taxoid accumulation in cell suspension cultures of Taxus following elicitation with methyl jasmonate. Biotechnol. Bioeng. 62, 97–105.
    Direct Link:
  • Kim YB, Kim SM, Kang MK, Kuzuyama T, Lee JK, Park SC, Shin SC, Kim SU (2009) Regulation of resin acid synthesis in Pinus densifolora by differential transcription of genes encoding multiple 1-deoxy-D-xylulose 5-phosphate synthase and 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase genes. Tree Physiol. 29, 737–749.
  • Kozlowski G, Buchala A, Metraux JP (1999) Methyl jasmonate protects Norway spruce [Picea abies (L.) Karst.] seedlings against Pythium ultimum Trow. Physiol. Mol. Plant Pathol. 55, 53–58.
  • Krekling T, Franceschi VR, Kronkene P, Solheim H (2004) Differential anatomical response of Norway spruce stem tissues to sterile and fungus infected inoculations. Trees 18, 1–9.
  • Lange BM, Ghassemian M (2003) Genome organization in Arabidopsis thaliana: A survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol. Biol. 58, 925–948.
  • Lange BM, Wildung MR, Mccaskill D, Croteau RB (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc. Natl. Acad. Sci. USA 95, 2100–2104.
  • Lapointe G, Luckevich MD, Seguin A (2001) Investigation on the induction of 14–3-3 in white spruce. Plant Cell Rep. 20, 79–84.
  • Lippert D, Chowrira S, Ralph SG, Zhuang J, Aeschliman D, Ritland C, Ritland K, Bohlmann J (2007) Conifer defense against insects: Proteome analysis of Sitka spruce (Picea sitchensis) bark induced by mechanical wounding or feeding by white pine weevils (Pissodes strobi). Proteomics 7, 248–270.
    Direct Link:
  • Lois LM, Campos N, Putra SR, Danielsen K, Rohmer M, Boronat A (1998) Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of C-1-deoxy-D-xylulose 5-phosphate, a common precursor for isoprenoid, thiamine, and pyridoxol biosynthesis. Proc. Natl. Acad. Sci. USA 95, 2105–2110.
  • Lois LM, Rodríguez-Concepción 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.
    Direct Link:
  • Martin DM, Fäldt 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.
  • Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol. 132, 1586–1599.
  • Martin DM, 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.
  • Mcgarvey DJ, Croteau RB (1995) Terpenoid metabolism. Plant Cell 7, 1015–1026.
  • 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.
  • Nagy NE, Franceschi, VR, Solheim H, Krekling T, Christiansen E (2000) Wound induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. Am. J. Bot. 87, 302–313.
  • Phillips MA, Walter MH, Ralph SG, Dabrowska P, Luck K, Urós EM, Boland W, Strack D, Rodríguez-Concepción M, Bohlmann J, Gershenzon J (2007) Functional identification and differential expression of 1-deoxy-D-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol. Biol. 65, 243–257.
  • Phillips MA, Wildung MR, Williams DC, Hyatt DC, Croteau RB (2003) cDNA isolation, functional expression, and characterization of (+)-α-pinene synthase from loblolly pine (Pinus taeda): Stereocontrol in pinene biosynthesis. Arch. Biochem. Biophys. 411, 267–276.
  • Ralph SG, Chun HJ, Kolosova N, Cooper D, Oddy C, Ritland CE et al. (2008) A conifer genomics resource of 200 000 spruce (Picea spp.) ESTs and 6 464 high-quality, sequence-finished full-length cDNAs for Sitka spruce (Picea sitchensis). BMC Genomics 9, 484.
  • Ralph SG, Hudgins JW, Jancsik S, Franceschi VR, Bohlmann J (2007) Aminocyclopropane carboxylate synthase is a regulated step in ethylene-dependent induced conifer defense. Full-length cDNA cloning of a multigene family, differential constitutive and wound- and insect-induced expression, and cellular and subcellular localization in spruce and Douglas fir. Plant Physiol. 143.
  • Ralph SG, Yueh H, Friedmann M, Aeschliman D, Zeznik JA, Nelson CC, Butterfield YS, Kirkpatrick R, Liu J, Jones SJ, Marra MA, Douglas CJ, Ritland K, Bohlmann J (2006) Conifer defence against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworms (Choristoneura occidentalis) or white pine weevils (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant Cell Environ. 29, 1545–1570.
    Direct Link:
  • Regvar M, Gogala N, Znidarsic N (1997) Jasmonic acid effects mycorrhization of spruce seedlings with Laccaria laccata. Trees 11, 511–514.
  • Ro DK, Arimura G, Lau SY, 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.
  • Ro DK, 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.
  • Rodríguez-Concepción M (2006) Early steps in isoprenoid biosynthesis: Multilevel regulation of the supply of common precursors in plant cells. Phytochem. Rev. 5, 1–15.
  • Rodríguez-Concepción M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130, 1079–1089.
  • Sallaud C, Rontein D, Onillon S, Jabés 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-farnesy pyropyosphate in the wild tomato Solanum habrochaites. Plant Cell 21, 301–317.
  • 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. doi: 10.1073/pnas.0904113106.
  • Schmidt A, Gershenzon J (2007) Cloning and characterization of isoprenyl diphosphate synthases with farnesyl diphosphate and geranylgeranyl diphosphate synthase activity from Norway spruce (Picea abies) and their relation to induced oleoresin formation. Phytochemistry 68, 2649–2649.
  • 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.
  • Schuler MA, Werck-Reichhart D (2003) Functional genomics of P450s. Annu. Rev. Plant Biol. 54, 629–667.
  • Sprenger GA, Schorken U, Weiegert T, Grolle S, Graff A, Taylor SV (1997) Identification of a thiamine-dependent synthase in Escherichia coli required for the formation of the 1-deoxyxylulose 5-phosphate precursor to isoprenoids, thiamine and pyridoxol. Proc. Natl. Acad. Sci. USA 94.
  • 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.
  • Steele CL, Crock J, Bohlmann J, Croteau RB (1998) Sesquiterpene synthases from grand fir (Abies grandis): comparison of constitutive and wound-induced activities, and cDNA isolation, characterization and bacterial expression of δ-selinene synthase and γ-humulene synthase. J. Biol. Chem. 273, 2078–2089.
  • Tholl D, Croteau RB, Gershenzon J (2001) Partial purification and characterization of the short-chain prenyltransferases, geranyl diphosphate synthase, and farnesyl diphosphate synthase, from Abies grandis (grand fir). Arch. Biochem. Biophys. 386, 233–242.
  • 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 heterdimeric geranyl diphosphate synthases. Plant Cell 16, 977–992.
  • 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.
    Direct Link:
  • Wise ML, Croteau RB (1999) Monoterpene biosynthesis. In: CaneDE, ed. Comprehensive Natural Products Chemistry: Isoprenoids, Including Carotenoids and Steroids. Pergmon Press, Oxford .
  • Wu H, Hu Z (1997) Comparative anatomy of resin ducts of the Pinaceae. Trees 11, 135–143.
  • Yukimune Y, Tabata H, Higashi Y, Hara Y (1996) Methyl-jasmonate induced overproduction of paclitaxel and baccatin III in Taxus cell suspension cultures. Nat. Biotech. 14.
  • Zulak KG, Lippert DN, Kuzyk MA, Domanski D, Chou T, Borchers CH, Bohlmann J (2009) Targeted proteomics using selected reaction monitoring reveals the induction of specific terpene synthases in a multi-level study of methyl jasmonate-treated Norway spruce (Picea abies). Plant J. doi: 10.1111/j.1365-313X.2009.04020.x.
    Direct Link:
View Full Article (HTML) Get PDF (743K)