Phytochemistry Reviews

, 5:179 | Cite as

Molecular Regulation of Induced Terpenoid Biosynthesis in Conifers

  • Michael A. PhillipsEmail author
  • Jörg Bohlmann
  • Jonathan Gershenzon


Conifers have evolved elaborate inducible, terpenoid-based defense mechanisms to deter attacks from bark beetles and other herbivore species. Herbivore damage triggers the production of oleoresin containing monoterpene, sesquiterpene and diterpene components that serve as toxins and physical barriers to herbivore invasion. Induced terpene formation appears to be regulated by specific enzymes of terpene metabolism whose activity increases on herbivore damage. Among the best studied of these are terpene synthases, enzymes which convert acyclic prenyl diphosphates to the parent terpene skeletons. Terpene synthase activity in turn is regulated by the transcription of terpene synthase genes. Induced terpene biosynthesis is also often accompanied by extensive cellular differentiation, including the formation of new resin ducts. The signal transduction cascades that initiate these shifts in conifer metabolism and cell differentiation are poorly understood due to the lack of well-developed model systems and appropriate genetic mutants. However, there are strong indications that octadecanoid pathway metabolites and ethylene have roles in this signaling, as they do in defense signaling in angiosperms. There are still large gaps in our knowledge of the signal transduction networks leading to herbivore-induced terpenoid accumulation in conifers. However, the development of new genomic, proteomic and metabolomic tools, as well as the establishment of convenient in vitro systems should facilitate more rapid advances in this field in the near future. The results will have important implications for understanding the evolution of conifer defense mechanisms as well as for the management of commercially important forest tree species, such as spruce, pine, and fir.

Key words

bark beetles ethylene methyl jasmonate resin ducts terpene synthases 


  1. Alfaro RI, Borden JH, King JN, Tomlin ES, McIntosh RL and Bohlmann J (2002). Mechanisms of resistance in Conifers against shoot infesting insects. In: Wagner, MR, Clancy, KM, Lieutier, F, and Paine, TD (eds) Mechanisms and Deployment of Resistance in Trees to Insects, pp 101–126. Kluwer Academic Press, Dordrecht, The Netherlands Google Scholar
  2. Bauer Z, Gomez-Gomez L, Boller T and Felix G (2001). Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. J. Biol. Chem. 276: 45669–45676 PubMedCrossRefGoogle Scholar
  3. Bohlmann J, Crock J, Jetter R and Croteau R (1998a). Terpenoid-based defenses in conifers: cDNA cloning, characterization, and functional expression of wound-inducible (E)-alpha-bisabolene synthase from grand fir (Abies grandis). Proc. Natl. Acad. Sci. USA 95: 6756–6761 CrossRefGoogle Scholar
  4. Bohlmann J, Meyer-Gauen G and Croteau R (1998b). Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc. Natl. Acad. Sci. USA 95: 4126–4133 CrossRefGoogle Scholar
  5. Bohlmann J & Croteau R (1999) Diversity and variability of terpenoid defenses in conifers: molecular genetics, biochemistry and evolution of the terpene synthase gene family in grand fir. In: Novartis Foundation Symposium Series 223, (pp. 132–149)Google Scholar
  6. Burke C and Croteau R (2002a). Geranyl diphosphate synthase from Abies grandis: cDNA isolation, functional expression and characterization. Arch. Biochem. Biophys. 405: 130–136 CrossRefGoogle Scholar
  7. Burke C and Croteau R (2002b). 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 CrossRefGoogle Scholar
  8. Burke CC, Wildung MR and Croteau R (1999). Geranyl diphosphate synthase: cloning, expression, and characterization of this prenyltransferase as a heterodimer. Proc. Natl. Acad. Sci. USA 96: 13062–13067 PubMedCrossRefGoogle Scholar
  9. Byun McKay SA, Hunter WL, Godard KA, Wang SX, Martin DM, Bohlmann J and 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 CrossRefGoogle Scholar
  10. Connolly JD and Hill RA (1991). Dictionary of Terpenoids. Chapman and Hall, London Google Scholar
  11. Creelman RA and Mullet JE (1997). Biosynthesis and Action of Jasmonates in Plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 355–381 PubMedCrossRefGoogle Scholar
  12. Creelman RA, Tierney ML and Mullet JE (1992). Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc. Natl. Acad. Sci. USA 89: 4938–4941 PubMedCrossRefGoogle Scholar
  13. Danell K, Gref R and Yazdani R (1990). Effects of mono- and diterpenes in Scots pine needles on moose browsing. Scand. J. For. Res. 5: 535–539 Google Scholar
  14. Eckhardt U, Grimm B and Hortensteiner S (2004). Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol. Biol. 56: 1–14 PubMedCrossRefGoogle Scholar
  15. Fäldt J, Martin D, Miller B, Rawat S and 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 carene synthase. Plant Mol. Biol. 51: 119–133 PubMedCrossRefGoogle Scholar
  16. Fliegmann J, Mithofer A, Wanner G and Ebel J (2004). An ancient enzyme domain hidden in the putative beta-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J. Biol. Chem. 279: 1132–1140 PubMedCrossRefGoogle Scholar
  17. Franceschi VR, Krekling T and Christiansen E (2002). Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am. J. Bot. 89: 578–586 CrossRefGoogle Scholar
  18. Franceschi VR, Krokene P, Christiansen E and Krekling T (2005). Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 167: 353–375 PubMedCrossRefGoogle Scholar
  19. Funk C and Croteau R (1994). Diterpenoid resin acid biosynthesis in conifers: characterization of two cytochrome P450-dependent monooxygenases and an aldehyde dehydrogenase involved in abietic acid biosynthesis. Arch. Biochem. Biophys. 308: 258–266 PubMedCrossRefGoogle Scholar
  20. Funk C, Lewinsohn E, Stofer Vogel B, Steele CL and Croteau R (1994). Regulation of oleoresinosis in grand fir (Abies grandis) (coordinate induction of monoterpene and diterpene cyclases and two cytochrome p450-dependent diterpenoid hydroxylases by stem wounding). Plant Physiol. 106: 999–1005 PubMedGoogle Scholar
  21. Futai K and Furano T (1979). The variety of resistances among pine species to pine wood nematode Bursaphelenchus lignicolus. Bull. Kyoto Univ. For. 51: 23–26 Google Scholar
  22. Galichet A and Gruissem W (2003). Protein farnesylation in plants – conserved mechanisms but different targets. Curr. Opin. Plant Biol. 6: 530–535 PubMedCrossRefGoogle Scholar
  23. Gershenzon J and Kreis W (1999). Biochemistry of terpenoids: monoterpenes, sesquiterpenes, diterpenes, sterols, cardiac glycosides and steroid saponins. In: Wink, M (eds) Biochemistry of Plant Secondary Metabolism,, pp 222–299. Sheffield Academic Press, Sheffield England Google Scholar
  24. Gijzen M, Lewinsohn E and Croteau R (1992). Antigenic cross-reactivity among monoterpene cyclases from grand fir and induction of these enzymes upon stem wounding. Arch. Biochem. Biophys. 294: 670–674 PubMedCrossRefGoogle Scholar
  25. Hohf RS, Ratti JT and Croteau R (1987). Experimental analysis of winter food selection by spruce goose. J. Wildlife Manag. 51: 159–167 CrossRefGoogle Scholar
  26. Huber DP, Philippe RN, Madilao LL, Sturrock RN and Bohlmann J (2005). Changes in anatomy and terpene chemistry in roots of Douglas-fir seedlings following treatment with methyl jasmonate. Tree Physiol. 25: 1075–1083 PubMedGoogle Scholar
  27. Huber DP, Ralph S and Bohlmann J (2004). Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. J. Chem. Ecol. 30: 2399–2418 PubMedCrossRefGoogle Scholar
  28. Hudgins JW, Christiansen E and Franceschi VR (2003). Methyl jasmonate induces changes mimicking anatomical defenses in diverse members of the Pinaceae. Tree Physiol. 23: 361–371 PubMedGoogle Scholar
  29. Hudgins JW, Christiansen E and Franceschi VR (2004). Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiol. 24: 251–264 PubMedGoogle Scholar
  30. Hudgins JW and 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: 2134–2149 PubMedCrossRefGoogle Scholar
  31. Jennewein S, Wildung MR, Chau M, Walker K and Croteau R (2004). Random sequencing of an induced Taxus cell cDNA library for identification of clones involved in Taxol biosynthesis. Proc. Natl. Acad. Sci. USA 101: 9149–9154 PubMedCrossRefGoogle Scholar
  32. Ketchum RE, Gibson DM, Croteau RB and Shuler ML (1999). The kinetics of taxoid accumulation in cell suspension cultures of Taxus following elicitation with methyl jasmonate. Biotechnol. Bioeng. 62: 97–105 PubMedCrossRefGoogle Scholar
  33. Leon J, Rojo E and Sanchez-Serrano JJ (2001). Wound signalling in plants. J. Exp. Bot. 52: 1–9 PubMedCrossRefGoogle Scholar
  34. Lewinsohn E, Gijzen M and Croteau R (1991). Defense mechanisms of conifers: differences in constitutive and wound-induced monoterpene biosynthesis among species. Plant Physiol. 96: 44–49 PubMedCrossRefGoogle Scholar
  35. Lippert D, Zhuang J, Ralph S, Ellis DE, Gilbert M, Olafson R, Ritland K, Ellis B, Douglas CJ and Bohlmann J (2005). Proteome analysis of early somatic embryogenesis in Picea glauca. Proteomics 5: 461–473 PubMedCrossRefGoogle Scholar
  36. Litvak ME and Monson RK (1998). Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory. Oecologia 114: 531–540 CrossRefGoogle Scholar
  37. Lois LM, Rodriguez-Concepcion M, Gallego F, Campos N and Boronat A (2000). Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J. 22: 503–513 PubMedCrossRefGoogle Scholar
  38. Luchi N, Ma R, Capretti P and Bonello P (2005). Systemic induction of traumatic resin ducts and resin flow in Austrian pine by wounding and inoculation with Sphaeropsis sapinea and Diplodia scrobiculata. Planta 221: 75–84 PubMedCrossRefGoogle Scholar
  39. Martin D, Tholl D, Gershenzon J and 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 PubMedCrossRefGoogle Scholar
  40. Martin DM, Faldt J and 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 PubMedCrossRefGoogle Scholar
  41. Martin DM, Gershenzon J and Bohlmann J (2003). Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol. 132: 1586–1599 PubMedCrossRefGoogle Scholar
  42. Meindl T, Boller T and Felix G (2000). The bacterial elicitor flagellin activates its receptor in tomato cells according to the address-message concept. Plant Cell 12: 1783–1794 PubMedCrossRefGoogle Scholar
  43. Miller B, Madilao LL, Ralph S and 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 PubMedCrossRefGoogle Scholar
  44. Mueller MJ, Brodschelm W, Spannagl E and Zenk MH (1993). Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc. Natl. Acad. Sci. USA 90: 7490–7494 PubMedCrossRefGoogle Scholar
  45. Nordlander G (1990). Limonene inhibits attraction to α-pinene in the pine weevils Hylobius abietis and H. pinastri. J. Chem. Ecol. 16: 1307–1320 CrossRefGoogle Scholar
  46. Okada M, Matsumura M, Ito Y and Shibuya N (2002). High-affinity binding proteins for N-acetylchitooligosaccharide elicitor in the plasma membranes from wheat, barley and carrot cells: conserved presence and correlation with the responsiveness to the elicitor. Plant Cell Physiol. 43: 505–512 PubMedCrossRefGoogle Scholar
  47. Phillips MA and Croteau RB (1999). Resin-based defenses in conifers. Trends Plant Sci. 4: 184–190 PubMedCrossRefGoogle Scholar
  48. Raffa KF, Aukema BH, Erbigin 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 process. Recent Adv Phytochem 39: 79–118Google Scholar
  49. Raffa KF and Berryman AA (1983). The role of host plant-resistance in the colonization behavior and ecology of bark beetles (Coleoptera, Scolytidae). Ecol. Monogr. 53: 27–49 CrossRefGoogle Scholar
  50. Ralph S, Park YS, Bohlmann J & Mansfeld SJ (2006) Dirigent proteins in conifer defense: full-length cDNA discovery, phylogeny, and differential wound- and insect-induced expression of a family of DIR and DIR-like genes in spruce (Picea spp.). Plant Mol. Biol. (in press)Google Scholar
  51. Ro DK, Arimura G, Lau SY, Piers E and 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 PubMedCrossRefGoogle Scholar
  52. Rungis D, Berube Y, Zhang J, Ralph S, Ritland CE, Ellis BE, Douglas C, Bohlmann J and Ritland K (2004). Robust simple sequence repeat markers for spruce (Picea spp.) from expressed sequence tags. Theor. Appl. Genet. 109: 1283–1294 PubMedCrossRefGoogle Scholar
  53. Scagel RF (1965). An Evolutionary Survey of the Plant Kingdom. Wadsworth Publishers, CA, USA Google Scholar
  54. Schopf R (1986). The effect of secondary needle compounds on the development of phytophagous insects. For. Ecol. Manag. 15: 55–64 CrossRefGoogle Scholar
  55. Seybold SJ, Bohlmann J and Raffa KF (2000). Biosynthesis of coniferophagous bark beetle pheromones and conifer isoprenoids: evolutionary perspective and synthesis. Can. Entomol. 132: 697–753 CrossRefGoogle Scholar
  56. Steele CL, Crock J, Bohlmann J and Croteau R (1998a). Sesquiterpene synthases from grand fir (Abies grandis) – comparison of constitutive and wound-induced activities, and cDNA isolation, characterization and bacterial expression of delta-selinene synthase and gamma-humulene synthase. J. Biol. Chem. 273: 2078–2089 CrossRefGoogle Scholar
  57. Steele CL, Katoh S, Bohlmann J and Croteau R (1998b). Regulation of oleoresinosis in grand fir (Abies grandis). Differential transcriptional control of monoterpene, sesquiterpene, and diterpene synthase genes in response to wounding. Plant Physiol. 116: 1497–1504 CrossRefGoogle Scholar
  58. Steele CL, Lewinsohn E and Croteau R (1995). Induced oleoresin biosynthesis in grand fir as a defense against bark beetles. Proc. Natl. Acad. Sci. USA 92: 4164–4168 PubMedCrossRefGoogle Scholar
  59. Swain SM and Singh DP (2005). Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends Plant Sci. 10: 123–129 PubMedGoogle Scholar
  60. Tholl D, Croteau R and 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 PubMedCrossRefGoogle Scholar
  61. Trapp S and Croteau R (2001). Defensive resin biosynthesis in conifers. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 689–724 PubMedCrossRefGoogle Scholar
  62. Wang KLC, Li H and Ecker JR (2002). Ethylene biosynthesis and signaling networks. Plant Cell 14: S131–S151 PubMedGoogle Scholar
  63. Yukimune Y, Tabata H, Higashi Y and Hara Y (1996). Methyl jasmonate-induced overproduction of paclitaxel and baccatin III in Taxus cell suspension cultures. Nat. Biotechnol. 14: 1129–1132 PubMedCrossRefGoogle Scholar
  64. Zeneli G, Krokene P, Christiansen E, Krekling T & Gershenzon J (2006) Methyl jasmonate treatment of large Norway spruce (Picea abies) trees increases the accumulation of terpenoid resin components and protects against infection by Ceratocystis polonica, a bark beetle-associated fungus. Tree Physiol. 26 (in press)Google Scholar
  65. Zhao J, Davis LC and Verpoorte R (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol. Adv. 23: 283–333 PubMedCrossRefGoogle Scholar
  66. Zhao J, Guo YQ, Fujita K and Sakai K (2004a). Involvement of cAMP signaling in elicitor-induced phytoalexin accumulation in Cupressus lusitanica cell cultures. New Phytol. 161: 723–733 CrossRefGoogle Scholar
  67. Zhao J, Zheng SH, Fujita K and Sakai K (2004b). Jasmonate and ethylene signalling and their interaction are integral parts of the elicitor signalling pathway leading to beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J. Exp. Bot. 55: 1003–1012 CrossRefGoogle Scholar
  68. Zhao J & Sakai K (2003) Multiple signalling pathways mediate fungal elicitor-induced beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J. Exp. Bot. 54: 647–656Google Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Michael A. Phillips
    • 1
    Email author
  • Jörg Bohlmann
    • 2
  • Jonathan Gershenzon
    • 1
  1. 1.Department of BiochemistryMax Planck Institute for Chemical EcologyJena
  2. 2.Michael Smith Laboratories and Departments of Botany and Forest SciencesUniversity of British ColumbiaEast MallCanada

Personalised recommendations