, Volume 148, Issue 3, pp 426–436 | Cite as

Exogenous application of methyl jasmonate elicits defenses in Norway spruce (Picea abies) and reduces host colonization by the bark beetle Ips typographus

  • Nadir Erbilgin
  • Paal Krokene
  • Erik Christiansen
  • Gazmend Zeneli
  • Jonathan Gershenzon
Plant Animal Interactions


The terpenoid and phenolic constituents of conifers have been implicated in protecting trees from infestation by bark beetles and phytopathogenic fungi, but it has been difficult to prove these defensive roles under natural conditions. We used methyl jasmonate, a well-known inducer of plant defense responses, to manipulate the biochemistry and anatomy of mature Picea abies (Norway spruce) trees and to test their resistance to attack by Ips typographus (the spruce bark beetle). Bark sections of P. abies treated with methyl jasmonate had significantly less I. typographus colonization than bark sections in the controls and exhibited shorter parental galleries and fewer eggs had been deposited. The numbers of beetles that emerged and mean dry weight per beetle were also significantly lower in methyl jasmonate-treated bark. In addition, fewer beetles were attracted to conspecifics tunneling in methyl jasmonate-treated bark. Stem sections of P. abies treated with methyl jasmonate had an increased number of traumatic resin ducts and a higher concentration of terpenes than untreated sections, whereas the concentration of soluble phenolics did not differ between treatments. The increased amount of terpenoid resin present in methyl jasmonate-treated bark could be directly responsible for the observed decrease in I. typographus colonization and reproduction.


Conifers Induced defenses Phenolics Terpenes 



This study was supported by the Norwegian Forest Research Institute, University of California-Berkeley (College of Natural Resources), and the Max Planck Society. Trygve Krekling and Elin Ørmen at the Electron Microscopy Laboratory, Norwegian University of Life Sciences helped with sample processing and microscopy. Torstein Kvamme, Skogforsk, helped with field and lab work. We gratefully acknowledge the permission to utilize trees in the municipal forest in Ås.


  1. Alfaro RI (1995) An induced defence reaction in white spruce to attack by the white pine weevil, Pissodes strobi. Can J For Res 25:1725–1730CrossRefGoogle Scholar
  2. Anderbrant O (1988) Survival of parent and brood adult bark beetles, Ips typographus, in relation to size, lipid content and re-emergence or emergence day. Physiol Ent 13:121–129CrossRefGoogle Scholar
  3. Anderbrant O, Schlyter F, Birgersson G (1985) Intraspecific competition affecting parents and offspring in the bark beetle Ips typographus. Oikos 45:89–98CrossRefGoogle Scholar
  4. Bannan MW (1936) Vertical resin ducts in the secondary wood of the abietineae. New Phytol 35:11–46CrossRefGoogle Scholar
  5. Berryman AA (1972) Resistance of conifers to invasion by bark beetle-fungus associations. Bioscience 22:598–602CrossRefGoogle Scholar
  6. Blodgett JT, Herms DA, Bonello P (2005) Effects of fertilization on red pine defense chemistry and resistance to Sphaeropsis sapinea. For Ecol Manag 208:373–382Google Scholar
  7. Birgersson G, Bergström G (1989) Volatiles released from individual spruce bark beetle entrance holes—quantitative variations during the first week of attack. J Chem Ecol 15:2465–2483Google Scholar
  8. Bonello P, Blodgett JT (2003) Pinus nigraSphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol Mol Plant Path 63:249–261CrossRefGoogle Scholar
  9. Borden JH (1982) Aggregation pheromones. In: Milton JB, Sturgeon KB (eds) Bark beetles in North American conifers. University of Texas Press, Austin, TX, pp 74–139Google Scholar
  10. Borden JH (1989) Semiochemials and bark beetle populations: exploitation of natural phenomena by pest management strategists. Hol Ecol 12:501–510Google Scholar
  11. Brignolas F, Lieutier F, Sauvard D, Yart A, Drouet A, Claudot AC (1995) Changes in soluble-phenol content of Norway spruce (Picea abies) phloem in response to wounding and inoculation with Ophiostoma polonicum. Eur J For Path 25:253–265CrossRefGoogle Scholar
  12. Brignolas F, Lieutier F, Sauvard D, Christiansen E, Berryman AA (1998) Phenolic predictors for Norway spruce resistance to the bark beetle Ips typographus (Coleoptera : Scolytidae) and an associated fungus, Ceratocystis polonica. Can J For Res 28:720–728Google Scholar
  13. Byers JA, Birgersson G, Lofqvist J, Bergström G (1988) Synergistic pheromones and monoterpenes enable aggregation and host recognition by a bark beetle. Naturwissenschaften 75:153–155Google Scholar
  14. Camacho AD, Pierce HD Jr, Borden JH (1994) Aggregation pheromones in Dryocoetes affaber (Mann.) (Coleoptera: Scolytidae): stereoisomerism and species specificity. J Chem Ecol 20:111–124CrossRefGoogle Scholar
  15. Christiansen E (1985). Ceratocystis polonica inoculated in Norway spruce: blue-staining in relation to inoculum density, resinosis and tree growth. Eur J For Path 15:160–167CrossRefGoogle Scholar
  16. Christiansen E, Bakke A (1988) The spruce bark beetle of Eurasia. In: Berryman AA (eds) Dynamics of forest insect populations. Plenum, New York, pp 479–503Google Scholar
  17. Christiansen E, Krokene P (1999) Can Norway spruce trees be “vaccinated” against attack by Ips typographus? Agric For Ent 1:185–187CrossRefGoogle Scholar
  18. Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381CrossRefPubMedGoogle Scholar
  19. Croteau R, Gurkewitz S, Johnson MA, Fisk HJ (1987) Biochemistry of oleoresinosis: monoterpene and diterpene biosynthesis in lodgepole pine saplings infected with Cer-atocystis clavigera or treated with carbohydrate elicitors. Plant Physiol 85:1123–2840PubMedCrossRefGoogle Scholar
  20. Del Cerro M, Cogen J, Del Cerro C (1980) Stevenel’s blue, an excellent stain for optical microscopical study of plastic embedded tissue. Microsc Acta 83:117–121PubMedGoogle Scholar
  21. Erbilgin N, Raffa KF (2000) Effects of host tree species on attractiveness of tunnelling pine engravers, Ips pini, to conspecifics and insect predators. J Chem Ecol 26:823–840CrossRefGoogle Scholar
  22. Evensen PC, Solheim H, Hoiland K, Stenersen J (2000) Induced resistance of Norway spruce, variation of phenolic compounds and their effects on fungal pathogens. For Path 30:97–108Google Scholar
  23. Franceschi VR, Krekling T, Berryman AA, Christiansen E (1998) Specialized phloem parenchyma cells in Norway spruce (Pinaceae) bark are an important site of defence reactions. Am J Bot 85:601–615CrossRefGoogle Scholar
  24. Franceschi VR, Krokene P, Krekling T, Christiansen E (2000) Phloem parenchyma cells are involved in local and distant defense responses to fungal inoculation or bark-beetle attack in Norway spruce (Pinaceae). Am J Bot 87:314–326PubMedCrossRefGoogle Scholar
  25. Franceschi VR, Krekling T, Christiansen E (2002) Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am J Bot 89:602–610CrossRefGoogle Scholar
  26. Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–376Google Scholar
  27. Hudgins JW, Franceschi V (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: 2134–2149CrossRefPubMedGoogle Scholar
  28. Hudgins JW, Christiansen E, Franceschi VR (2003) Methyl jasmonate induces changes mimicking anatomical and chemical defenses in diverse members of the Pinaceae. Tree Physiol 23:361–371PubMedGoogle Scholar
  29. Hudgins JW, Christiansen E, Franceschi V (2004) Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiol 24:251–264PubMedGoogle Scholar
  30. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144CrossRefPubMedGoogle Scholar
  31. Ketchum REB, 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 62:97–105CrossRefPubMedGoogle Scholar
  32. Klepzig KD, Kruger EL, Smalley EB, Raffa KF (1995) Effects of biotic and abiotic stress on induced accumulation of terpenes and phenolics in red pines inoculated with bark beetle-vectored fungus. J Chem Ecol 21:601–626CrossRefGoogle Scholar
  33. Krokene P, Solheim H, Krekling T, Christiansen E (2003) Inducible anatomical defense responses in Norway spruce stems and their possible role in induced resistance. Tree Physiol 23:191–197PubMedGoogle Scholar
  34. Kozlowski G, Buchala A, Metraux JP (1999) Methyl jasmonate protects Norway spruce [Picea abies (L.) Karst.] seedlings against Pythium ultimum Trow. Physiol Mol Plant Path 55:53–58CrossRefGoogle Scholar
  35. Laitinen M-L, Julkunen-Tiitto R, Rousi M (2002) Foliar phenolic composition of European white birch during bud unfolding and leaf development. Physiol Plant 114:450–460CrossRefPubMedGoogle Scholar
  36. Lieutier F, Brignolas F, Sauvard D, Yart A, Galet C, Brunet M, van de Sype H (2003) Intra- and inter-provenance variability in phloem phenols of Picea abies and relationship to a bark beetle-associated fungus. Tree Phys 23:247–256Google Scholar
  37. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS System for mixed models. SAS Institute Inc., Cary, NCGoogle Scholar
  38. Luchi N, Ma R, Capretti P, 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 221:75–84CrossRefPubMedGoogle Scholar
  39. Maie N, Behrens A, Knicker H, Kogel-Knabner I (2003) Changes in the structure and protein binding ability of condensed tannins during decomposition of fresh needles and leaves. Soil Biophys Biochem 35:577–589CrossRefGoogle Scholar
  40. 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 129:1003–1018PubMedCrossRefGoogle Scholar
  41. Martin D, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132:1586–1599PubMedCrossRefGoogle Scholar
  42. McNee WR, Bonello P, Storer AJ, Wood DL, Gordon TR (2003) Feeding response of Ips paraconfusus to phloem and phloem metabolites of Heterobasidion annosum-inoculated ponderosa pine, Pinus ponderosa. J Chem Ecol 29:1183–1202Google Scholar
  43. Moeck HA, Wood DL, Lindahl KQ Jr (1981) Host selection behavior of bark beetles (Coleoptera: Scolytidae) attacking Pinus ponderosa, with special emphasis on the western pine beetle, Dendroctonus brevicomis. J Chem Ecol 7:49–83CrossRefGoogle Scholar
  44. 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 87:302–313PubMedCrossRefGoogle Scholar
  45. Nebeker TE, Hodges JD, Blanche CA (1993) Host response to bark beetle and pathogen colonization. In: Schowalter RD, Filip G (eds) Beetle–pathogen interactions in conifer forests. Academic, New York, pp 157–178Google Scholar
  46. Neter J, Wasserman W, Kutner MH (1983) Applied linear regression models. Irwin, Homewood, ILGoogle Scholar
  47. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Ann Rev Entomol 42:179–206CrossRefGoogle Scholar
  48. Phillips MA, Croteau RB (1999) Resin-based defenses in conifers. Trends Plant Sci 4:184–190CrossRefPubMedGoogle Scholar
  49. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defence. Curr Opin Plant Biol 5:237–243PubMedCrossRefGoogle Scholar
  50. Raffa KF, Berryman AA (1983) The role of host plant-resistance in the colonization behavior and ecology of bark beetles (Coleoptera, Scolytidae). Ecolog Monog 53:27–49CrossRefGoogle Scholar
  51. Raffa KF, Smalley EB (1995) Interactions of pre-attack and induced monoterpene concentrations in host conifer-defense against bark beetle–fungal complexes. Oecologia 102:285–295CrossRefGoogle Scholar
  52. Richard S, Lapointe G, Rutledge G, Séguin A (2000) Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol 41:982–987Google Scholar
  53. Schmidt A, Zeneli G, Hietala AM, Fossdal CG, Krokene P, Christiansen E, Gershenzon J (2005) Induced chemical defences in conifers: biochemical and molecular approaches to studying their function. In: Romeo JT (eds) Chemical ecology and phytochemistry in forest ecosystems, vol 39. Elsevier, Amsterdam, pp 1–28Google Scholar
  54. Slansky F Jr, Haack RA (1986) Age-specific flight behavior in relation to body weight and lipid content of Ips calligraphus reared in slash pine bolts with thick or thin inner bark (phloem). Entomol Exp Appl 40:197–207Google Scholar
  55. Strack D, Heilemann J, Klinkott ES, Wray V (1988) Cell wall-bound phenolics from Norway spruce (Picea abies) needles. Z Naturforsch C 43:37–41Google Scholar
  56. Strom BL, Roton LM, Goyer RA, Meeker JR (1999) Visual and semiochemical disruption of host finding in the southern pine beetle. Ecol App 9:1028–1038CrossRefGoogle Scholar
  57. Thaler JS, Stout MJ, Karban R, Duffey SS (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312–324CrossRefGoogle Scholar
  58. Wallin KF, Raffa KF (2000) Influences of host chemicals and internal physiology on the multiple steps of postlanding host acceptance behavior of Ips pini (Coleoptera: Scolytidae). Environ Entomol 29:442–453CrossRefGoogle Scholar
  59. Wallin KF, Raffa KF (2004) Feedback between individual host selection behavior and population dynamics in an eruptive herbivore. Ecol Monog 74:101–116CrossRefGoogle Scholar
  60. Wood DL (1982) The role of pheromones, kairomones, and allomones in the host selection and colonization behavior of bark beetles. Annu Rev Entomol 27:411–446CrossRefGoogle Scholar
  61. Woodward S, Pearce RB (1988) The role of stilbenes in resistance of sitka spruce (Picea sitchensis (Bong) Carr) to entry of fungal pathogens. Phys Mol Plant Path 33:127–149CrossRefGoogle Scholar
  62. Worrell R (1983) Damage by the spruce bark beetle in south Norway 1970–80: a survey, and factors affecting its occurrence. Medd Nor Inst Skogforsk 38:1–34Google Scholar
  63. Yukimune Y, Tabata H, Higashi Y, Hara Y (1996) Methyl-jasmonate induced overproduction of paclitaxel and baccatin III in Taxus cell suspension cultures. Nat Biotechnol 14:1129–1132CrossRefPubMedGoogle Scholar
  64. Zar JH (1996) Biostatistical analysis. 3rd edn. Prentice Hall, Upper Saddle River, NJ, pp 622Google Scholar
  65. Zeneli G, Krokene P, Christiansen E, Krekling T, Gershenzon J (2006) Methyl jasmonate treatment of mature Norway spruce (Picea abies (L) Karst) protects trees against Ceratocystis polonica infection and increases the accumulation of terpenoid resin components. Tree Physiol 26 (in press)Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Nadir Erbilgin
    • 1
  • Paal Krokene
    • 2
  • Erik Christiansen
    • 2
  • Gazmend Zeneli
    • 3
  • Jonathan Gershenzon
    • 3
  1. 1.Division of Insect Biology Department of Environmental SciencePolicy and Management University of CaliforniaBerkeleyUSA
  2. 2.Norwegian Forest Research InstituteÅsNorway
  3. 3.Max Planck Institute for Chemical EcologyJenaGermany

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