Conifer Defense Against Insects and Fungal Pathogens

Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 220)

Abstract

In this chapter we provide an overview of the many different defense strategies of conifers against insect pests and fungal pathogens. Much of this chapter deals with the economically and ecologically important species of pine (Pinus spp.) and spruce (Picea spp.). We highlight the anatomical and chemical defenses as well as their biochemical, molecular, and genomic underpinnings.

Notes

Acknowledgment

Research in the laboratory of JB has been generously supported with funding from the Natural Science and Engineering Research Council of Canada in the form of NSERC Discovery and Strategic Grants; and with funding from Genome Canada and Genome British Columbia in support of the Treenomix Project (http://www.treenomix.ca), the smart forest project and the Tria Project (http://www.thetriaproject.ca). JB is Distinguished University Scholar of the University of British Columbia, Vancouver, Canada.

References

  1. Abbott E, Hall D, Hamberger B, Bohlmann J (2010) Laser microdissection of conifer stem tissues: Isolation and analysis of high quality RNA, terpene synthase enzyme activity and terpenoid metabolites from resin ducts and cambial zone tissue of white spruce (Picea glauca). BMC Plant Biol 10(106):1–16Google Scholar
  2. Adomas A, Heller G, Li GS, Olson A, Chu TM, Osborne J, Craig D, Van Zyl L, Wolfinger R, Sederoff R, Dean RA, Stenlid J, Finlay R, Asiegbu FO (2007) Transcript profiling of a conifer pathosystem: response of Pinus sylvestris root tissues to pathogen (Heterobasidion annosum) invasion. Tree Physiol 27:1441–1458PubMedGoogle Scholar
  3. Alfaro RI, Vansickle GA, Thomson AJ, Wegwitz E (1982) Tree mortality and radial growth losses caused by the western spruce budworm in a Douglas-fir stand in British-Columbia. Can J Forest Res 12:780–787Google Scholar
  4. Alfaro RI, Borden JH, King JN, Tomlin ES, McIntosh RL, Bohlmann J (2002) Mechanisms of resistance in conifers against shoot infesting insects – The case of the white pine weevil Pissodes strobi (Peck): (Coleoptera: Curculionidae). In: Wagner MR, Clancy KM, Lieutier F, Paine TD (eds) 21st International congress of entomology. Springer, Iguassu Falls, Brazil, pp 105–130Google Scholar
  5. 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 95:9693–9698PubMedPubMedCentralGoogle Scholar
  6. Asiegbu FO, Denekamp M, Daniel G, Johansson M (1995) Immune cytochemical-localization of pathogenesis-related proteins in roots of Norway Spruce infected with Heterobasidion-Annosum. Eur J Forest Pathol 25:169–178Google Scholar
  7. Asiegbu FO, Choi WB, Li GS, Nahalkova J, Dean RA (2003) Isolation of a novel antimicrobial peptide gene (Sp-AMP) homologue from Pinus sylvestris (Scots pine) following infection with the root rot fungus Heterobasidion annosum. FEMS Microbiol Lett 228:27–31PubMedGoogle Scholar
  8. Asiegbu FO, Adomas A, Stenlid J (2005a) Conifer root and butt rot caused by Heterobasidion annosum (Fr.) Bref. s.l. Mol Plant Pathol 6:395–409PubMedGoogle Scholar
  9. Asiegbu FO, Nahalkova J, Li GS (2005b) Pathogen-inducible cDNAs from the interaction of the root rot fungus Heterobasidion annosum with Scots pine (Pinus sylvestris L.). Plant Sci 168:365–372Google Scholar
  10. Bedon F, Levasseur C, Grima-Pettenati J, Seguin A, MacKay J (2009) Sequence analysis and functional characterization of the promoter of the Picea glauca cinnamyl alcohol dehydrogenase gene in transgenic white spruce plants. Plant Cell Rep 28:787–800PubMedGoogle Scholar
  11. Blodgett JT, Eyles A, Bonello P (2007) Organ-dependent induction of systemic resistance and systemic susceptibility in Pinus nigra inoculated with Sphaeropsis sapinea and Diplodia scrobiculata. Tree Physiol 27:511–517PubMedGoogle Scholar
  12. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546PubMedGoogle Scholar
  13. Bohlmann J (2008) Insect-induced terpenoid defenses in spruce. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, New York, pp 173–187Google Scholar
  14. Bois E, Lieutier F (1997) Phenolic response of Scots pine clones to inoculation with Leptographium wingfieldii, a fungus associated with Tomicus piniperda. Plant Physiol Biochem 35:819–825Google Scholar
  15. Bonello P, Blodgett JT (2003) Pinus nigra-Sphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol Mol Plant Pathol 63:249–261Google Scholar
  16. Bonello P, Gordon TR, Storer AJ (2001) Systemic induced resistance in Monterey pine. Forest Pathol 31:99–106Google Scholar
  17. Bonello P, Storer AJ, Gordon TR, Wood DL (2003) Systemic effects of Heterobasidion annosum on ferulic acid glucoside and lignin of presymptomatic ponderosa pine phloem, and potential effects on bark-beetle-associated fungi. J Chem Ecol 29:1167–1182PubMedGoogle Scholar
  18. Bonello P, Gordon TR, Herms DA, Wood DL, Erbilgin N (2006) Nature and ecological implications of pathogen-induced systemic resistance in conifers: A novel hypothesis. Physiol Mol Plant Pathol 68:95–104Google Scholar
  19. Brignolas F, Lacroix B, Lieutier F, Sauvard D, Drouet A, Claudot AC, Yart A, Berryman AA, Christiansen E (1995) Induced responses in phenolic metabolism in 2 Norway spruce clones after wounding and inoculations with Ophiostoma-polonicum, a bark beetle-associated fungus. Plant Physiol 109:821–827PubMedPubMedCentralGoogle Scholar
  20. 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 Forest Res 28:720–728Google Scholar
  21. Butland SL, Chow ML, Ellis BE (1998) A diverse family of phenylalanine ammonia-lyase genes expressed in pine trees and cell cultures. Plant Mol Biol 37:15–24PubMedGoogle Scholar
  22. Celimene CC, Smith DR, Young RA, Stanosz GR (2001) In vitro inhibition of Sphaeropsis sapinea by natural stilbenes. Phytochemistry 56:161–165PubMedGoogle Scholar
  23. Chatthai M, Osusky M, Osuska L, Yevtushenko D, Misra S (2004) Functional analysis of a Douglas-fir metallothionein-like gene promoter: transient assays in zygotic and somatic embryos and stable transformation in transgenic tobacco. Planta 220:118–128PubMedGoogle Scholar
  24. Chiron H, Drouet A, Lieutier F, Payer HD, Ernst D, Sandermann H (2000) Gene induction of stilbene biosynthesis in Scots pine in response to ozone treatment, wounding, and fungal infection. Plant Physiol 124:865–872PubMedPubMedCentralGoogle Scholar
  25. Christiansen E, Krokene P, Berryman AA, Franceschi VR, Krekling T, Lieutier F, Lonneborg A, Solheim H (1999) Mechanical injury and fungal infection induce acquired resistance in Norway spruce. Tree Physiol 19:399–403PubMedGoogle Scholar
  26. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3:31–40PubMedGoogle Scholar
  27. Cordoba E, Salmi M, Leon P (2009) Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J Exp Bot 60:2933–2943PubMedGoogle Scholar
  28. Croteau R, Gurkewitz S, Johnson MA, Fisk HJ (1987) Biochemistry of oleoresinosis 1 – monoterpene and diterpene biosynthesis in lodgepole pine saplings infected with Ceratocystis-clavigera or treated with carbohydrate elicitors. Plant Physiol 85:1123–1128PubMedPubMedCentralGoogle Scholar
  29. Davin LB, Lewis NG (2000) Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiol 123:453–461PubMedPubMedCentralGoogle Scholar
  30. Davin LB, Wang HB, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG (1997) Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275:362–366PubMedGoogle Scholar
  31. Davis JM, Wu HG, Cooke JEK, Reed JM, Luce KS, Michler CH (2002) Pathogen challenge, salicylic acid, and jasmonic acid regulate expression of chitinase gene homologs in pine. Mol Plant Microbe Interact 15:380–387PubMedGoogle Scholar
  32. De Lucca AJ, Cleveland TE, Wedge DE (2005) Plant-derived antifungal proteins and peptides. Can J Microbiol 51:1001–1014PubMedGoogle Scholar
  33. Delorme L, Lieutier F (1990) Monoterpene composition of the preformed and induced resins of Scots pine, and their effect on bark beetles and associated fungi. Eur J Forest Pathol 20:304–316Google Scholar
  34. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang LJ (2002) The phenylpropanoid pathway and plant defence - a genomics perspective. Mol Plant Pathol 3:371–390PubMedGoogle Scholar
  35. Dubos C, Plomion C (2001) Drought differentially affects expression of a PR-10 protein, in needles of maritime pine (Pinus pinaster Ait.) seedlings. J Exp Bot 52:1143–1144PubMedGoogle Scholar
  36. Ekramoddoullah AKM, Yu XS, Sturrock R, Zamani A, Taylor D (2000) Detection and seasonal expression pattern of a pathogenesis-related protein (PR-10) in Douglas-fir (Pseudotsuga menziesii) tissues. Physiol Plant 110:240–247Google Scholar
  37. Elfstrand M, Fossdal CG, Swedjemark G, Clapham D, Olsson O, Sitbon F, Sharma P, Lonneborg A, von Arnold S (2001) Identification of candidate genes for use in molecular breeding - A case study with the Norway spruce defensin-like gene, Spi 1. Silvae Genet 50:75–81Google Scholar
  38. Erbilgin N, Krokene P, Christiansen E, Zeneli G, Gershenzon J (2006) Exogenous application of methyl jasmonate elicits defenses in Norway spruce (Picea abies) and reduces host colonization by the bark beetle Ips typographus. Oecologia 148:426–436PubMedGoogle Scholar
  39. Evensen PC, Solheim H, Hoiland K, Stenersen J (2000) Induced resistance of Norway spruce, variation of phenolic compounds and their effects on fungal pathogens. Forest Pathol 30:97–108Google Scholar
  40. Eyles A, Chorbadjian R, Wallis C, Hansen R, Cipollini D, Herms D, Bonello P (2007) Cross-induction of systemic induced resistance between an insect and a fungal pathogen in Austrian pine over a fertility gradient. Oecologia 153:365–374PubMedGoogle Scholar
  41. Faccoli M, Schlyter F (2007) Conifer phenolic resistance markers are bark beetle antifeedant semiochemicals. Agric Forest Entomol 9:237–245Google Scholar
  42. Faldt J, Martin D, 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 51:119–133PubMedGoogle Scholar
  43. Fliegmann J, Schroder G, Schanz S, Britsch L, Schroder J (1992) Molecular analysis of chalcone and dihydropinosylvin synthase from Scots pine (Pinus-sylvestris), and differential regulation of these and related enzyme-activities in stressed plants. Plant Mol Biol 18:489–503PubMedGoogle Scholar
  44. Fossdal CG, Sharma P, Lonneborg A (2001) Isolation of the first putative peroxidase cDNA from a conifer and the local and systemic accumulation of related proteins upon pathogen infection. Plant Mol Biol 47:423–435PubMedGoogle Scholar
  45. Fossdal CG, Hietala AM, Kvaalen H, Solheim H (2006) Changes in host chitinase isoforms in relation to wounding and colonization by Heterobasidion annosum: early and strong defense response in 33-year-old resistant Norway spruce clone. Tree Physiol 26:169–177PubMedGoogle Scholar
  46. Franceschi VR, Krekling T, Berryman AA, Christiansen E (1998) Specialized phloem parenchyma cells in Norway spruce (Pinaceae) bark are an important site of defense reactions. Am J Bot 85:601–615PubMedGoogle Scholar
  47. 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 87:314–326PubMedGoogle Scholar
  48. Franceschi VR, Krekling T, Christiansen E (2002) Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am J Bot 89:578–586PubMedGoogle Scholar
  49. Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–375PubMedGoogle Scholar
  50. Gehlert R, Schoppner A, Kindl H (1990) Stilbene synthase from seedlings of Pinus-Sylvestris - purification and induction in response to fungal infection. Mol Plant Microbe Interact 3:444–449Google Scholar
  51. Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher-plants. J Chem Ecol 20:1281–1328PubMedGoogle Scholar
  52. Gordon TR (2006) Pitch canker disease of pines. Phytopathology 96:657–659PubMedGoogle Scholar
  53. Gould N, Reglinski T, Spiers M, Taylor JT (2008) Physiological trade-offs associated with methyl jasmonate – induced resistance in Pinus radiata. Can J Forest Res 38:677–684Google Scholar
  54. Gout R, Kovalyova V (2008) Inhibition of growth of the phytopathogenic organisms by Scots pine (Pinus sylvestris L.) defensin. Sylwan 152:54–58Google Scholar
  55. Gronberg H, Hietala AM, Haahtela K (2009) Analysing scots pine defence-related transcripts and fungal DNA levels in seedlings single- or dual-inoculated with endophytic and pathogenic Rhizoctonia species. Forest Pathol 39:377–389Google Scholar
  56. Hall DE, Robert JA, Keeling CI, Domanski D, Qesada AL, Jancsik S, Kuzyk M, Br H, Borchers CH, Bohlmann J (2011) An integrated genomic, proteomic, and biochemical analysis of (+)-3-carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes which are resistant or susceptible to white pine weevil. Plant J 65:936–948PubMedGoogle Scholar
  57. Hamberger B, Bohlmann J (2006) Cytochrome P450 mono-oxygenases in conifer genomes: discovery of members of the terpenoid oxygenase superfamily in spruce and pine. Biochem Soc Trans 34:1209–1214PubMedGoogle Scholar
  58. Hietala AM, Kvaalen H, Schmidt A, Johnk N, Solheim H, Fossdal CG (2004) Temporal and spatial profiles of chitinase expression by Norway spruce in response to bark colonization by Heterobasidion annosum. Appl Environ Microbiol 70:3948–3953PubMedPubMedCentralGoogle Scholar
  59. Himejima M, Hobson KR, Otsuka T, Wood DL, Kubo I (1992) Antimicrobial terpenes from oleoresin of Ponderosa pine Tree Pinus-ponderosa - a defense-mechanism against microbial invasion. J Chem Ecol 18:1809–1818PubMedGoogle Scholar
  60. Huber DPW, Ralph S, Bohlmann J (2004) Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. J Chem Ecol 30:2399–2418PubMedGoogle Scholar
  61. Huber DPW, Philippe RN, Madilao LL, Sturrock RN, Bohlmann J (2005) Changes in anatomy and terpene chemistry in roots of Douglas-fir seedlings following treatment with methyl jasmonate. Tree Physiol 25:1075–1083PubMedGoogle Scholar
  62. 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 135:2134–2149PubMedPubMedCentralGoogle Scholar
  63. Hudgins JW, Christiansen E, Franceschi VR (2003) Methyl jasmonate induces changes mimicking anatomical defenses in diverse members of the Pinaceae. Tree Physiol 23:361–371PubMedGoogle Scholar
  64. Hudgins JW, Christiansen E, Franceschi VR (2004) Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiol 24:251–264PubMedGoogle Scholar
  65. Hudgins JW, McDonald GI, Zambino PJ, Klopfenstein NB, Franceschi VR (2005) Anatomical and cellular responses of Pinus monticola stem tissues to invasion by Cronartium ribicola. Forest Pathol 35:423–443Google Scholar
  66. Hudgins JW, Ralph SG, 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 224:865–877PubMedGoogle Scholar
  67. Islam MA, Sturrock RN, Holmes TA, Ekramoddoullah AKM (2009) Ultrastructural studies of Phellinus sulphurascens infection of Douglas-fir roots and immunolocalization of host pathogenesis-related proteins. Mycol Res 113:700–712PubMedGoogle Scholar
  68. Kasprzewska A (2003) Plant chitinases - regulation and function. Cell Mol Biol Lett 8:809–824PubMedGoogle Scholar
  69. Katoh S, Croteau R (1998) Individual variation in constitutive and induced monoterpene biosynthesis in grand fir. Phytochemistry 47:577–582Google Scholar
  70. Keeling CI, Bohlmann J (2006a) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675PubMedGoogle Scholar
  71. Keeling CI, Bohlmann J (2006b) Diterpene resin acids in conifers. Phytochemistry 67:2415–2423PubMedGoogle Scholar
  72. Kim YB, Kim SM, Kang MK, Kuzuyama T, Lee JK, Park SC, Shin SC, Kim SU (2009) Regulation of resin acid synthesis in Pinus densiflora 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 29:737–749PubMedGoogle Scholar
  73. King JN, Alfaro RI (2009) Developing Sitka spruce populations for resistance to the white pine weevil: summary of research and breeding program. Technical Report 50, Ministry of Forests and Range, Forest Science Program, Victoria, BC. http://www.for.gov.bc.ca/hfd/pubs/Docs/Tr/Tr050.htm
  74. Kiraly L, Barnaz B, Kiralyz Z (2007) Plant resistance to pathogen infection: Forms and mechanisms of innate and acquired resistance. J Phytopathol 155:385–396Google Scholar
  75. Kirst M, Johnson AF, Baucom C, Ulrich E, Hubbard K, Staggs R, Paule C, Retzel E, Whetten R, Sederoff R (2003) Apparent homology of expressed genes from wood-forming tissues of loblolly pine (Pinus taeda L.) with Arabidopsis thaliana. Proc Natl Acad Sci USA 100:7383–7388PubMedPubMedCentralGoogle Scholar
  76. Kodan A, Kuroda H, Sakai F (2002) A stilbene synthase from Japanese red pine (Pinus densiflora): Implications for phytoalexin accumulation and down-regulation of flavonoid biosynthesis. Proc Natl Acad Sci USA 99:3335–3339PubMedPubMedCentralGoogle Scholar
  77. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844PubMedPubMedCentralGoogle Scholar
  78. Kopper BJ, Illman BL, Kersten PJ, Klepzig KD, Raffa KF (2005) Effects of diterpene acids on components of a conifer bark beetle-fungal interaction: Tolerance by Ips pini and sensitivity by its associate Ophiostoma ips. Environ Entomol 34:486–493Google Scholar
  79. Koutaniemi S, Warinowski T, Karkonen A, Alatalo E, Fossdal CG, Saranpaa P, Laakso T, Fagerstedt KV, Simola LK, Paulin L, Rudd S, Teeri TH (2007) Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR. Plant Mol Biol 65:311–328PubMedGoogle Scholar
  80. Kovalyova VA, Gout RT (2008) Molecular cloning and characterization of Scotch pine defensin 2. Cytol Genet 42:408–412Google Scholar
  81. Kozlowski G, Metraux JP (1998) Infection of Norway spruce (Picea abies (L) Karst) seedlings with Pythium irregulare Buism and Pythium ultimum Trow: histological and biochemical responses. Eur J Plant Pathol 104:225–234Google Scholar
  82. 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 55:53–58Google Scholar
  83. Kramer KJ, Muthukrishnan S (1997) Insect chitinases: Molecular biology and potential use as biopesticides. Insect Biochem Mol Biol 27:887–900PubMedGoogle Scholar
  84. Krekling T, Franceschi VR, Krokene P, Solheim H (2004) Differential anatomical response of Norway spruce stem tissues to sterile and fungus infected inoculations. Trees 18:1–9Google Scholar
  85. Krokene P, Christiansen E, Solheim H, Franceschi VR, Berryman AA (1999) Induced resistance to pathogenic fungi in Norway spruce. Plant Physiol 121:565–569PubMedPubMedCentralGoogle Scholar
  86. 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
  87. Krokene P, Nagy NE, Solheim H (2008) Methyl jasmonate and oxalic acid treatment of Norway spruce: anatomically based defense responses and increased resistance against fungal infection. Tree Physiol 28:29–35PubMedGoogle Scholar
  88. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331PubMedGoogle Scholar
  89. Langenheim JH (2003) Plant resins: chemistry, evolution, ecology, and ethnobotany. Timber, Portland, OR, p 586Google Scholar
  90. Li SH, Schneider B, Gershenzon J (2007) Microchemical analysis of laser-microdissected stone cells of Norway spruce by cryogenic nuclear magnetic resonance spectroscopy. Planta 225:771–779PubMedGoogle Scholar
  91. Lieutier F (2002) Mechanisms of resistance in conifers and bark beetle attack strategies. In: Wagner MR, Clancy KM, Lieutier F, Paine TD (eds) 21st International congress of entomology. Springer, Iguassu Falls, Brazil, pp 105–130Google Scholar
  92. 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 7:248–270PubMedGoogle Scholar
  93. Liu JJ, Ekramoddoullah AKM, Yu XS (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant 119:544–553Google Scholar
  94. Liu RJ, Ekramoddoullah AKM, Zamani A (2005) A class IV chitinase is up-regulated by fungal infection and abiotic stresses and associated with slow-canker-growth resistance to Cronartium ribicola in Western white pine (Pinus monticola). Phytopathology 95:284–291PubMedGoogle Scholar
  95. 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 221:75–84PubMedGoogle Scholar
  96. Manninen AM, Utriainen J, Holopainen T, Kainulainen P (2002) Terpenoids in the wood of Scots pine and Norway spruce seedlings exposed to ozone at different nitrogen availability. Can J Forest Res 32:2140–2145Google Scholar
  97. 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 129:1003–1018PubMedPubMedCentralGoogle Scholar
  98. 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 132:1586–1599PubMedPubMedCentralGoogle Scholar
  99. Mattheus N, Ekramoddoullah AKM, Lee SP (2003) Isolation of high-quality RNA from white spruce tissue using a three-stage purification method and subsequent cloning of a transcript from the PR-10 gene family. Phytochem Anal 14:209–215PubMedGoogle Scholar
  100. Mauch F, Mauchmani B, Boller T (1988) Antifungal hydrolases in pea tissue.2. inhibition of fungal growth by combinations of chitinase and beta-1,3-Glucanase. Plant Physiol 88:936–942PubMedPubMedCentralGoogle Scholar
  101. McKay SAB, 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 133:368–378PubMedPubMedCentralGoogle Scholar
  102. Meins F, Fritig B, Linthorst H, Mikkelsen J, Neuhaus J, Ryals J (1994) Plant chitinase genes. Plant Mol Biol Rep 12:S22–S28Google Scholar
  103. Miller RH, Berryman AA, Ryan CA (1986) Biotic elicitors of defense reactions in lodgepole pine. Phytochemistry 25:611–612Google Scholar
  104. 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 137:369–382PubMedPubMedCentralGoogle Scholar
  105. Moreira X, Sampedro L, Zas R (2009) Defensive responses of Pinus pinaster seedlings to exogenous application of methyl jasmonate: Concentration effect and systemic response. Environ Exp Bot 67:94–100Google Scholar
  106. 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 87:302–313PubMedGoogle Scholar
  107. Nagy NE, Fossdal CG, Krokene P, Krekling T, Lonneborg A, Solheim H (2004) Induced responses to pathogen infection in Norway spruce phloem: changes in polyphenolic parenchyma cells, chalcone synthase transcript levels and peroxidase activity. Tree Physiol 24:505–515PubMedGoogle Scholar
  108. Nealis VG, Noseworthy MK, Turnquist R, Waring VR (2009) Balancing risks of disturbance from mountain pine beetle and western spruce budworm. Can J Forest Res 39:839–848Google Scholar
  109. Neuhaus JM (1999) Plant chitinases (PR-3, PR-4, PR-8, PR-11). In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC, Boca Ranton, pp 77–105Google Scholar
  110. Nordlander G (1990) Limonene inhibits attraction to alpha-pinene in the pine weevils Hylobius-abietis and H-pinastri. J Chem Ecol 16:1307–1320PubMedGoogle Scholar
  111. Paine TD, Hanlon CC (1994) Influence of oleoresin constituents from Pinus-Ponderosa and Pinus-Jeffreyi on growth of mycangial fungi from Dendroctonus-Ponderosae and Dendroctonus-Jeffreyi. J Chem Ecol 20:2551–2563PubMedGoogle Scholar
  112. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206PubMedGoogle Scholar
  113. Pan HF, Lundgren LN (1996) Phenolics from inner bark of Pinus sylvestris. Phytochemistry 42:1185–1189Google Scholar
  114. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265PubMedGoogle Scholar
  115. Pearce RB (1996) Antimicrobial defences in the wood of living trees. New Phytol 132:203–233Google Scholar
  116. Pervieux I, Bourassa M, Laurans F, Hamelin R, Seguin A (2004) A spruce defensin showing strong antifungal activity and increased transcript accumulation after wounding and jasmonate treatments. Physiol Mol Plant Pathol 64:331–341Google Scholar
  117. Phillips MA, Croteau RB (1999) Resin-based defenses in conifers. Trends Plant Sci 4:184–190PubMedGoogle Scholar
  118. Phillips MA, Walter MH, Ralph SG, Dabrowska P, Luck K, Uros EM, Boland W, Strack D, Rodriguez-Concepcion 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 65:243–257PubMedGoogle Scholar
  119. Piggott N, Ekramoddoullah AKM, Liu JJ, Yu XS (2004) Gene cloning of a thaumatin-like (PR-5) protein of western white pine (Pinus monticola D. Don) and expression studies of members of the PR-5 group. Physiol Mol Plant Pathol 64:1–8Google Scholar
  120. Popp MP, Johnson JD, Lesney MS (1995) Changes in ethylene production and monoterpene concentration in slash pine and loblolly-pine following inoculation with bark beetle vectored fungi. Tree Physiol 15:807–812Google Scholar
  121. Preisig-Muller R, Schwekendiek A, Brehm I, Reif HJ, Kindl H (1999) Characterization of a pine multigene family containing elicitor-responsive stilbene synthase genes. Plant Mol Biol 39:221–229PubMedGoogle Scholar
  122. Raffa KF, Berryman AA (1982) Physiological differences between lodgepole pines resistant and susceptible to the mountain pine-beetle (Coleoptera, Scolytidae) and associated microorganisms. Environ Entomol 11:486–492Google Scholar
  123. Raffa K, Aukema B, Erbilgin N, Klepzig K, Wallin K (2005) Interactions among conifer terpenoids and bark beetles across multiple levels of scale: an attempt to understand links between population patterns and physiological processes. Recent Adv Phytochem 39:80–118Google Scholar
  124. Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG, Romme WH (2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: The dynamics of bark beetle eruptions. Bioscience 58:501–517Google Scholar
  125. Ralph SG, Yueh H, Friedmann M, Aeschliman D, Zeznik JA, Nelson CC, Butterfield YSN, Kirkpatrick R, Liu J, Jones SJM, Marra MA, Douglas CJ, Ritland K, Bohlmann J (2006a) 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 29:1545–1570PubMedGoogle Scholar
  126. Ralph S, Park JY, Bohlmann J, Mansfield SD (2006b) Dirigent proteins in conifer defense: gene 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 60:21–40PubMedGoogle Scholar
  127. Ralph SG, Jancsik S, Bohlmann J (2007a) Dirigent proteins in conifer defense II: Extended gene discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry 68:1975–1991PubMedGoogle Scholar
  128. Ralph SG, Hudgins JW, Jancsik S, Franceschi VR, Bohlmann J (2007b) Aminocyclopropane carboxylic acid 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 143:410–424PubMedPubMedCentralGoogle Scholar
  129. Ralph SG, Chun HJE, Kolosova N, Cooper D, Oddy C, Ritland CE, Kirkpatrick R, Moore R, Barber S, Holt RA, Jones SJM, Marra MA, Douglas CJ, Ritland K, Bohlmann J (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 9:484PubMedPubMedCentralGoogle Scholar
  130. Richard S, Lapointe G, Rutledge RG, Seguin A (2000) Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol 41:982–987PubMedGoogle Scholar
  131. 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 67:1572–1578PubMedGoogle Scholar
  132. 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 102:8060–8065PubMedPubMedCentralGoogle Scholar
  133. Salle A, Monclus R, Yart A, Lieutier F (2005) Effect of phenolic compounds on the in vitro growth of two fungi associated with Ips typographus. Forest Pathol 35:298–304Google Scholar
  134. Sato Y, Bao WL, Sederoff R, Whetten R (2001) Molecular cloning and expression of eight laccase cDNAs in loblolly pine (Pinus taeda). J Plant Res 114:147–155Google Scholar
  135. 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 68:2649–2659PubMedGoogle Scholar
  136. Schmidt A, Gershenzon J (2008) Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 69:49–57PubMedGoogle Scholar
  137. 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 (ed) Chemical ecology and phytochemistry in forest ecosystems. Elsevier, Amsterdam, pp 1–28Google Scholar
  138. Schmidt A, Wachtler B, Temp U, Krekling T, Seguin A, Gershenzon J (2009) A bifunctional geranyl and geranylgeranyl diphosphate synthase is involved in terpene oleoresin formation in Norway spruce (Picea abies). Plant Physiol 152(2):639–655PubMedGoogle Scholar
  139. Schwekendiek A, Pfeffer G, Kindl H (1992) Pine stilbene synthase cDNA, a tool for probing environmental-stress. FEBS Lett 301:41–44PubMedGoogle Scholar
  140. Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC (2008) Plant pathogenesis-related (PR) proteins: A focus on PR peptides. Plant Physiol Biochem 46:941–950PubMedGoogle Scholar
  141. Sharma P, Lonneborg A (1996) Isolation and characterization of a cDNA encoding a plant defensin-like protein from roots of Norway spruce. Plant Mol Biol 31:707–712PubMedGoogle Scholar
  142. Sharma P, Borja D, Stougaard P, Lonneborg A (1993) Pr-proteins accumulating in spruce roots infected with a pathogenic Pythium sp isolate include chitinases, chitosanases and beta-1,3-glucanases. Physiol Mol Plant Pathol 43:57–67Google Scholar
  143. Six DL, Paine TD (1998) Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environ Entomol 27:1393–1401Google Scholar
  144. Stasolla C, van Zyl L, Egertsdotter U, Craig D, Liu WB, Sederoff RR (2003) The effects of polyethylene glycol on gene expression of developing white spruce somatic embryos. Plant Physiol 131:49–60PubMedPubMedCentralGoogle Scholar
  145. Steele CL, Katoh S, Bohlmann J, Croteau R (1998) Regulation of oleoresinosis in grand fir (Abies grandis) - Differential transcriptional control of monoterpene, sesquiterpene, and diterpene synthase genes in response to wounding. Plant Physiol 116:1497–1504PubMedPubMedCentralGoogle Scholar
  146. Thomma B, Penninckx I, Broekaert WF, Cammue BPA (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68PubMedGoogle Scholar
  147. Tomlin ES, Borden JH, Pierce HD (1996) Relationship between cortical resin acids and resistance of Sitka spruce to the white pine weevil. Can J Bot 74:599–606Google Scholar
  148. Tomlin ES, Antonejevic E, Alfaro RI, Borden JH (2000) Changes in volatile terpene and diterpene resin acid composition of resistant and susceptible white spruce leaders exposed to simulated white pine weevil damage. Tree Physiol 20:1087–1095PubMedGoogle Scholar
  149. Trapp S, Croteau R (2001) Defensive resin biosynthesis in conifers. Annu Rev Plant Physiol Plant Mol Biol 52:689–724PubMedGoogle Scholar
  150. Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97Google Scholar
  151. Vargas-Arispuro I, Reyes-Baez R, Rivera-Castaneda G, Martinez-Tellez MA, Rivero-Espejel I (2005) Antifungal lignans from the creosotebush (Larrea tridentata). Ind Crops Prod 22:101–107Google Scholar
  152. Viiri H, Annila E, Kitunen V, Niemela P (2001) Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees 15:112–122Google Scholar
  153. Wadenback J, von Arnold S, Egertsdotter U, Walter MH, Grima-Pettenati J, Goffner D, Gellerstedt G, Gullion T, Clapham D (2008) Lignin biosynthesis in transgenic Norway spruce plants harboring an antisense construct for cinnamoyl CoA reductase (CCR). Transgenic Res 17:379–392PubMedGoogle Scholar
  154. Wagner A, Donaldson L, Kim H, Phillips L, Flint H, Steward D, Torr K, Koch G, Schmitt U, Ralph J (2009) Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol 149:370–383PubMedPubMedCentralGoogle Scholar
  155. Wainhouse D, Cross DJ, Howell RS (1990) The role of lignin as a defense against the spruce bark beetle Dendroctonus-Micans - effect on larvae and adults. Oecologia 85:257–265Google Scholar
  156. Wainhouse D, Rose DR, Peace AJ (1997) The influence of preformed defences on the dynamic wound response in Spruce bark. Funct Ecol 11:564–572Google Scholar
  157. Wainhouse D, Ashburner R, Ward E, Boswell R (1998) The effect of lignin and bark wounding on susceptibility of spruce trees to Dendroctonus micans. J Chem Ecol 24:1551–1561Google Scholar
  158. Wallis C, Eyles A, Chorbadjian R, Gardener BM, Hansen R, Cipollini D, Herms DA, Bonello P (2008) Systemic induction of phloem secondary metabolism and its relationship to resistance to a canker pathogen in Austrian pine. New Phytol 177:767–778PubMedGoogle Scholar
  159. Walters DR (2009) Are plants in the field already induced? Implications for practical disease control. Crop Prot 28:459–465Google Scholar
  160. Weng J, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285PubMedGoogle Scholar
  161. Whetten RW, Sederoff RR (1992) Phenylalanine ammonia-lyase from loblolly-pine - purification of the enzyme and isolation of complementary-DNA clones. Plant Physiol 98:380–386PubMedPubMedCentralGoogle Scholar
  162. Wiweger M, Farbos I, Ingouff M, Lagercrantz U, von Arnold S (2003) Expression of Chia4-Pa chitinase genes during somatic and zygotic embryo development in Norway spruce (Picea abies): similarities and differences between gymnosperm and angiosperm class IV chitinases. J Exp Bot 54:2691–2699PubMedGoogle Scholar
  163. Woodward S, Pearce RB (1988) The role of stilbenes in resistance of Sitka Spruce (Picea-Sitchensis (Bong) Carr) to entry of fungal pathogens. Physiol Mol Plant Pathol 33:127–149Google Scholar
  164. Wu JQ, Baldwin IT (2009) Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 32:1161–1174PubMedGoogle Scholar
  165. Wu HG, Echt CS, Popp MP, Davis JM (1997) Molecular cloning, structure and expression of an elicitor-inducible chitinase gene from pine trees. Plant Mol Biol 33:979–987PubMedGoogle Scholar
  166. Yamaoka Y, Hiratsuka Y, Maruyama PJ (1995) The ability of Grosmannia clavigera to kill mature lodgepole pine trees. Eur J Forest Pathol 25:401–404Google Scholar
  167. Zareie R, Melanson DL, Murphy PJ (2002) Isolation of fungal cell wall degrading proteins from barley (Hordeum vulgare L.) leaves infected with Rhynchosporium secalis. Mol Plant Microbe Interact 15:1031–1039PubMedGoogle Scholar
  168. Zeneli G, Krokene P, Christiansen E, Krekling T, Gershenzon J (2006) Methyl jasmonate treatment of mature 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 26:977–988PubMedGoogle Scholar
  169. Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97PubMedGoogle Scholar
  170. 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 60:1015–1030PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Michael Smith LaboratoriesUniversity of British ColumbiaVancouverCanada

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