Spruce Phenolics: Biosynthesis and Ecological Functions

  • Almuth HammerbacherEmail author
  • Louwrance P. Wright
  • Jonathan Gershenzon
Part of the Compendium of Plant Genomes book series (CPG)


Phenolics are organic compounds that play an important role in the physiology of plants and their ecological interactions with biotic as well as abiotic factors. The genus Picea (spruce) produces a large array of structurally and functionally diverse phenolic compounds, including stilbenes, flavonoids, lignin, and phenylpropanoids. In this chapter, we review the current knowledge on the biosynthesis and ecological roles of the major classes of phenolic compounds in spruce. We also elaborate on the methods used to study the biosynthesis and functions of these compounds in this genus. Finally, we touch on how climate change is expected to affect the biosynthesis of phenolics in spruce and identify the most important directions for future research.


Flavonoids Lignin Lignans Stilbenes Phenylpropanoids Biotic stress Abiotic stress Global climate change 


  1. Auger MA, Jay-Allemand C, Bastien C, Geri C (1994) Quantitative variations of taxifolin and its glucoside in Pinus sylvestris needles consumed by Diprion pini larvae. Ann des sci for 51(2):135–146Google Scholar
  2. Bahnweg G, Schubert R, Kehr RD, Müller-Starck G, Heller W, Langebartels C, Sandermann H Jr (2000) Controlled inoculation of Norway spruce (Picea abies) with Sirococcus conigenus: PCR-based quantification of the pathogen in host tissue and infection-related increase of phenolic metabolites. Trees 14(8):435–441Google Scholar
  3. Bedon F, Levasseur C, Grima-Pettenati J, Séguin 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(5):787–800PubMedGoogle Scholar
  4. Bentz BJ, Régnière J, Fettig CJ, Hansen EM, Hayes JL, Hicke JA, Kelsey RG, Negrón JF, Seybold SJ (2010) Climate change and bark beetles of the western United States and Canada: direct and indirect effects. BioScience 60(8):602–613Google Scholar
  5. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54(1):519–546Google Scholar
  6. Brignolas F, Lieutier F, Sauvard D, Yart A, Drouet A, Claudot AC (1995a) 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(5):253–265Google Scholar
  7. Brignolas F, Lacroix B, Lieutier F, Sauvard D, Drouet A, Claudot AC, Yart A, Berryman AA, Christiansen E (1995b) Induced responses in phenolic metabolism in two Norway spruce clones after wounding and inoculations with Ophiostoma polonicum, a bark beetle-associated fungus. Plant Physiol 109(3):821–827PubMedPubMedCentralGoogle Scholar
  8. Celedon JM, Yuen MM, Chiang A, Henderson H, Reid KE, Bohlmann J (2017) Cell-type-and tissue-specific transcriptomes of the white spruce (Picea glauca) bark unmask fine-scale spatial patterns of constitutive and induced conifer defense. Plant J 92(4):710–726PubMedGoogle Scholar
  9. Cheng C, Xu L, Xu D, Lou Q, Lu M, Sun J (2016) Does cryptic microbiota mitigate pine resistance to an invasive beetle-fungus complex? Implications for invasion potential. Sci Rep 6:e33110Google Scholar
  10. Chiron H, Drouet A, Claudot AC, Eckerskorn C, Trost M, Heller W, Ernst D, Sandermann H (2000) Molecular cloning and functional expression of a stress-induced multifunctional O-methyltransferase with pinosylvin methyltransferase activity from Scots pine (Pinus sylvestris L.). Plant Mol Biol 44(6):733–745Google Scholar
  11. Chong J, Poutaraud A, Hugueney P (2009) Metabolism and roles of stilbenes in plants. Plant Sci 177(3):143–155Google Scholar
  12. Cvikrová M, Malá J, Hrubcová M, Eder J, Foretová S (2008) Induced changes in phenolic acids and stilbenes in embryogenic cell cultures of Norway spruce by culture filtrate of Ascocalyx abietina. J Plant Dis Prot 115(2):57–62Google Scholar
  13. Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D (2001) Climate change and forest disturbances: climate change can affect forests by altering the frequency, intensity, duration, and timing of fire, drought, introduced species, insect and pathogen outbreaks, hurricanes, windstorms, ice storms, or landslides. BioScience 51(9):723–734Google Scholar
  14. Dalman K, Wind JJ, Nemesio-Gorriz M, Hammerbacher A, Lundén K, Ezcurra I, Elfstrand M (2017) Overexpression of PaNAC03, a stress induced NAC gene family transcription factor in Norway spruce leads to reduced flavonol biosynthesis and aberrant embryo development. BMC Plant Biol 17(1):e6Google Scholar
  15. Danielsson M, Lundén K, Elfstrand M, Hu J, Zhao T, Arnerup J, Ihrmark K, Swedjemark G, Borg-Karlson AK, Stenlid J (2011) Chemical and transcriptional responses of Norway spruce genotypes with different susceptibility to Heterobasidion spp. infection. BMC Plant Biol. 11(1):e154Google Scholar
  16. Dar AA, Arumugam N (2013) Lignans of sesame: purification methods, biological activities and biosynthesis–a review. Bioorg Chem 50:1–10PubMedGoogle Scholar
  17. Dauwe R, Holliday JA, Aitken SN, Mansfield SD (2012) Metabolic dynamics during autumn cold acclimation within and among populations of Sitka spruce (Picea sitchensis). New Phytol 194(1):192–205PubMedGoogle Scholar
  18. 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(2):453–462PubMedPubMedCentralGoogle Scholar
  19. Deflorio G, Horgan G, Woodward S, Fossdal CG (2011) Gene expression profiles, phenolics and lignin of Sitka spruce bark and sapwood before and after wounding and inoculation with Heterobasidion annosum. Phys. Mol. Plant Path. 75(4):180–187Google Scholar
  20. Delvas N, Bauce É, Labbé C, Ollevier T, Bélanger R (2011) Phenolic compounds that confer resistance to spruce budworm. Entomol Exp Appl 141(1):35–44Google Scholar
  21. Evensen PC, Solheim H, Høiland K, Stenersen J (2000) Induced resistance of Norway spruce, variation of phenolic compounds and their effects on fungal pathogens. For Pathol 30(2):97–108Google Scholar
  22. Faccoli M, Schlyter F (2007) Conifer phenolic resistance markers are bark beetle antifeedant semiochemicals. Agric. For Entomol 9(3):237–245Google Scholar
  23. Fedorova TE, Fedorov SV, Babkin VA (2016) Oligolignans in the wood of Picea obovata Ledeb. Russ J Bioorg Chem 42(7):712–715Google Scholar
  24. Fischbach RJ, Kossmann B, Panten H, Steinbrecher R, Heller W, Seidlitz HK, Sandermann H, Hertkorn N, Schnitzler JP (1999) Seasonal accumulation of ultraviolet‐B screening pigments in needles of Norway spruce (Picea abies (L.) Karst.). Plant Cell Environ 22(1):27–37Google Scholar
  25. Fossdal CG, Nagy NE, Hietala AM, Kvaalen H, Slimestad R, Woodward S, Solheim H (2012) Indications of heightened constitutive or primed host response affecting the lignin pathway transcripts and phenolics in mature Norway spruce clones. Tree Phys 32(9):1137–1147Google Scholar
  26. 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(3):314–326PubMedGoogle Scholar
  27. Fraser CM, Chapple C (2011) The phenylpropanoid pathway in Arabidopsis. Arab Book 9:e152Google Scholar
  28. Friedmann M, Ralph SG, Aeschliman D, Zhuang J, Ritland K, Ellis BE, Bohlmann J, Douglas CJ (2007) Microarray gene expression profiling of developmental transitions in Sitka spruce (Picea sitchensis) apical shoots. J Exp Bot 58(3):593–614PubMedGoogle Scholar
  29. Ganthaler A, Stöggl W, Mayr S, Kranner I, Schüler S, Wischnitzki E, Sehr EM, Fluch S, Trujillo-Moya C (2017) Association genetics of phenolic needle compounds in Norway spruce with variable susceptibility to needle bladder rust. Plant Mol Biol 94(3):229–251PubMedPubMedCentralGoogle Scholar
  30. Gebauer RL, Strain BR, Reynolds JF (1997) The effect of elevated CO2 and N availability on tissue concentrations and whole plant pools of carbon-based secondary compounds in loblolly pine (Pinus taeda). Oecologia 113(1):29–36PubMedGoogle Scholar
  31. Hall D, De Luca V (2007) Mesocarp localization of a bi-functional resveratrol/hydroxycinnamic acid glucosyltransferase of Concord grape (Vitis labrusca). Plant J 49(4):579–591PubMedGoogle Scholar
  32. Hamberger B, Ohnishi T, Hamberger B, Séguin A, Bohlmann J (2011) Evolution of diterpene metabolism: Sitka spruce CYP720B4 catalyzes multiple oxidations in resin acid biosynthesis of conifer defense against insects. Plant Physiol 157(4):1677–1695PubMedPubMedCentralGoogle Scholar
  33. Hammerbacher A, Ralph SG, Bohlmann J, Fenning TM, Gershenzon J, Schmidt A (2011) Biosynthesis of the major tetrahydroxystilbenes in spruce, astringin and isorhapontin, proceeds via resveratrol and is enhanced by fungal infection. Plant Physiol 157(2):876–890PubMedPubMedCentralGoogle Scholar
  34. Hammerbacher A, Schmidt A, Wadke N, Wright LP, Schneider B, Bohlmann J, Brand WA, Fenning TM, Gershenzon J, Paetz C (2013) A common fungal associate of the spruce bark beetle metabolizes the stilbene defenses of Norway spruce. Plant Physiol 162(3):1324–1336PubMedPubMedCentralGoogle Scholar
  35. Hammerbacher A, Paetz C, Wright LP, Fischer TC, Bohlmann J, Davis AJ, Fenning TM, Gershenzon J, Schmidt A (2014) Flavan-3-ols in Norway spruce: biosynthesis, accumulation, and function in response to attack by the bark beetle-associated fungus Ceratocystis polonica. Plant Physiol 164(4):2107–2122PubMedPubMedCentralGoogle Scholar
  36. Hammerbacher A, Raguschke B, Wright LP, Gershenzon J (2018) Gallocatechin biosynthesis via a flavonoid 3′, 5′-hydroxylase is a defense response in Norway spruce against infection by the bark beetle-associated sap-staining fungus Endoconidiophora polonica. Phytochemistry 148:78–86PubMedGoogle Scholar
  37. Hammerbacher A, Kandasamy D, Ullah C, Schmidt A, Wright LP, Gershenzon J (2019) Flavanone-3-hydroxylase plays an important role in the biosynthesis of spruce phenolic defenses against bark beetles and their fungal associates. Front Plant Sci 10 (in press)Google Scholar
  38. Heilemann J, Strack D (1991) Flavonol glucosyltransferase from Norway spruce needles. Phytochemistry 30(6):1773–1776Google Scholar
  39. Higuchi T (1990) Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 24(1):23–63Google Scholar
  40. Holton TA, Brugliera F, Tanaka Y (1993) Cloning and expression of flavonol synthase from Petunia hybrida. Plant J 4(6):1003–1010PubMedGoogle Scholar
  41. Hoque E (1985) Norway spruce dieback: occurrence, isolation and biological activity of p-hydroxy acetophenone and p-hydroxy acetophenone-O-glucoside and their possible roles during stress phenomena. Eur J For Pathol 15(3):129–145Google Scholar
  42. Hoque E, Remus G (1999) Natural UV‐screening mechanisms of Norway spruce (Picea abies [L.] Karst.) needles. Photochem Photobiol 69(2):177–192Google Scholar
  43. Howles PA, Sewalt VJ, Paiva NL, Elkind Y, Bate NJ, Lamb C, Dixon RA (1996) Overexpression of L-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112(4):1617–1624PubMedPubMedCentralGoogle Scholar
  44. Huang J, Hammerbacher A, Weinhold A, Reichelt M, Gleixner G, Behrendt T, van Dam NM, Sala A, Gershenzon J, Trumbore S, Hartmann H (2019) Eyes on the future–evidence for trade-offs between growth, storage and defense in Norway spruce. New Phytol 222(1):144–158PubMedGoogle Scholar
  45. Hudgins JW, Christiansen E, Franceschi VR (2003) Methyl jasmonate induces changes mimicking anatomical defenses in diverse members of the Pinaceae. Tree Physiol 23(6):361–371PubMedGoogle Scholar
  46. 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(3):251–264PubMedGoogle Scholar
  47. 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(4):e865Google Scholar
  48. Jyske T, Laakso T, Latva-Mäenpää H, Tapanila T, Saranpää P (2014) Yield of stilbene glucosides from the bark of young and old Norway spruce stems. Biomass Bioenergy 71:216–227Google Scholar
  49. Jyske TM, Suuronen JP, Pranovich AV, Laakso T, Watanabe U, Kuroda K, Abe H (2015) Seasonal variation in formation, structure, and chemical properties of phloem in Picea abies as studied by novel microtechniques. Planta 242(3):613–629PubMedGoogle Scholar
  50. Jyske T, Kuroda K, Suuronen JP, Pranovich A, Roig-Juan S, Aoki D, Fukushima K (2016) In planta localization of stilbenes within Picea abies phloem. Plant Physiol 172(2):913–928PubMedPubMedCentralGoogle Scholar
  51. Kim BG, Kim DH, Sung SH, Kim DE, Chong Y, Ahn JH (2010) Two O-methyltransferases from Picea abies: characterization and molecular basis of different reactivity. Planta 232(4):837–844PubMedGoogle Scholar
  52. Kiselev KV, Grigorchuk VP, Ogneva ZV, Suprun AR, Dubrovina AS (2016) Stilbene biosynthesis in the needles of spruce Picea jezoensis. Phytochemistry 131:57–67PubMedGoogle Scholar
  53. Koutaniemi S, Warinowski T, Kärkönen A, Alatalo E, Fossdal CG, Saranpää P, Laakso T, Fagerstedt KV, Simola LK, Paulin L, Rudd S (2007) Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR. Plant Mol Biol 65(3):311–328PubMedGoogle Scholar
  54. Kovalchuk A, Zeng Z, Ghimire RP, Kivimäenpää M, Raffaello T, Liu M, Mukrimin M, Kasanen R, Sun H, Julkunen-Tiitto R, Holopainen JK (2019) Dual RNA-seq analysis provides new insights into interactions between Norway spruce and necrotrophic pathogen Heterobasidion annosum sl. BMC Plant Biol 19(1):e2Google Scholar
  55. Krajnc AU, Novak M, Felicijan M, Kraševec N, Lešnik M, Zupanec N, Komel R (2014) Antioxidative response patterns of Norway spruce bark to low-density Ceratocystis polonica inoculation. Trees 28(4):1145–1160Google Scholar
  56. Kuokkanen K, Julkunen-Tiitto R, Keinänen M, Niemelä P, Tahvanainen J (2001) The effect of elevated CO 2 and temperature on the secondary chemistry of Betula pendula seedlings. Trees 15(6):378–384Google Scholar
  57. Laitinen T, Morreel K, Delhomme N, Gauthier A, Schiffthaler B, Nickolov K, Brader G, Lim KJ, Teeri TH, Street NR, Boerjan W (2017) A key role for apoplastic H2O2 in Norway spruce phenolic metabolism. Plant Physiol 174(3):1449–1475PubMedPubMedCentralGoogle Scholar
  58. Lattanzio V, Kroon PA, Quideau S, Treutter D (2008) Plant phenolics—secondary metabolites with diverse functions. Recent Adv Polyphen Res 1:1–35Google Scholar
  59. Le TK, Jang HH, Nguyen HT, Doan TT, Lee GY, Park KD, Ahn T, Joung YH, Kang HS, Yun CH (2017) Highly regioselective hydroxylation of polydatin, a resveratrol glucoside, for one-step synthesis of astringin, a piceatannol glucoside, by P450 BM3. Enz Microb Technol 97:34–42Google Scholar
  60. Lee YK, Alexander D, Wulff J, Olsen JE (2014) Changes in metabolite profiles in Norway spruce shoot tips during short-day induced winter bud development and long-day induced bud flush. Metabolomics 10(5):842–858Google Scholar
  61. Li SH, Niu XM, Zahn S, Gershenzon J, Weston J, Schneider B (2008) Diastereomeric stilbene glucoside dimers from the bark of Norway spruce (Picea abies). Phytochemistry 69(3):772–782PubMedGoogle Scholar
  62. Li SH, Nagy NE, Hammerbacher A, Krokene P, Niu XM, Gershenzon J, Schneider B (2012) Localization of phenolics in phloem parenchyma cells of Norway spruce (Picea abies). ChemBioChem 13(18):2707–2713PubMedGoogle Scholar
  63. Lind M, Källman T, Chen J, Ma XF, Bousquet J, Morgante M, Zaina G, Karlsson B, Elfstrand M, Lascoux M, Stenlid JA (2014) Picea abies linkage map based on SNP markers identifies QTLs for four aspects of resistance to Heterobasidion parviporum infection. PLoS ONE 9(7):e101049PubMedPubMedCentralGoogle Scholar
  64. Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36(1):2–21PubMedGoogle Scholar
  65. Loscher R, Heide L (1994) Biosynthesis of p-hydroxybenzoate from p-coumarate and p-coumaroyl-coenzyme A in cell-free extracts of Lithospermum erythrorhizon cell cultures. Plant Physiol 106(1):271–279PubMedPubMedCentralGoogle Scholar
  66. Luo J, Nishiyama Y, Fuell C, Taguchi G, Elliott K, Hill L, Tanaka Y, Kitayama M, Yamazaki M, Bailey P, Parr A (2007) Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J 50(4):678–695PubMedGoogle Scholar
  67. Mageroy MH, Parent G, Germanos G, Giguère I, Delvas N, Maaroufi H, Bauce É, Bohlmann J, Mackay JJ (2015) Expression of the β-glucosidase gene Pgβglu-1 underpins natural resistance of white spruce against spruce budworm. Plant J 81(1):68–80PubMedGoogle Scholar
  68. Mageroy MH, Jancsik S, Saint Yuen MM, Fischer M, Withers SG, Paetz C, Schneider B, Mackay J, Bohlmann J (2017a) A conifer UDP-sugar dependent glycosyltransferase contributes to acetophenone metabolism and defense against insects. Plant Physiol 175(2):641–651PubMedPubMedCentralGoogle Scholar
  69. Mageroy MH, Lachance D, Jancsik S, Parent G, Séguin A, Mackay J, Bohlmann J (2017b) In vivo function of Pgβglu-1 in the release of acetophenones in white spruce. PeerJ 5:e3535PubMedPubMedCentralGoogle Scholar
  70. Malá J, Hrubcová M, Máchová P, Cvrčková H, Martincová O, Cvikrová M (2011) Changes in phenolic acids and stilbenes induced in embryogenic cell cultures of Norway spruce by two fractions of Sirococcus strobilinus mycelian. J For Sci 57(1):1–7Google Scholar
  71. Nagy NE, Fossdal CG, Krokene P, Krekling T, Lönneborg 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(5):505–515PubMedGoogle Scholar
  72. Neish AC (1959) Biosynthesis of pungenin from C14-labelled compounds by Colorado spruce. Can J Bot 37(5):1085–1100Google Scholar
  73. Nemesio-Gorriz M, Hammerbacher A, Ihrmark K, Källman T, Olson Å, Lascoux M, Stenlid J, Gershenzon J, Elfstrand M (2016) Different alleles of a gene encoding leucoanthocyanidin reductase (PaLAR3) influence resistance against the fungus Heterobasidion parviporum in Picea abies. Plant Physiol 171(4):2671–2681PubMedPubMedCentralGoogle Scholar
  74. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, Vicedomini R (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497(7451):579PubMedGoogle Scholar
  75. OuYang F, Mao JF, Wang J, Zhang S, Li Y (2015) Transcriptome analysis reveals that red and blue light regulate growth and phytohormone metabolism in Norway spruce [Picea abies (L.) Karst.]. PloS One 10(8):e0127896Google Scholar
  76. Parent GJ, Giguère I, Mageroy M, Bohlmann J, MacKay JJ (2018) Evolution of the biosynthesis of two hydroxyacetophenones in plants. Plant Cell Environ 41(3):620–629PubMedGoogle Scholar
  77. Pavy N, Pelgas B, Laroche J, Rigault P, Isabel N, Bousquet J (2012) A spruce gene map infers ancient plant genome reshuffling and subsequent slow evolution in the gymnosperm lineage leading to extant conifers. BMC Biol 10(1):e84Google Scholar
  78. Pelletier MK, Shirley BW (1996) Analysis of flavanone 3-hydroxylase in Arabidopsis seedlings (Coordinate regulation with chalcone synthase and chalcone isomerase). Plant Physiol 111(1):339–345PubMedPubMedCentralGoogle Scholar
  79. Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32(5):701–712PubMedGoogle Scholar
  80. Piispanen R, Willför S, Saranpää P, Holmbom B (2008) Variation of lignans in Norway spruce (Picea abies [L.] Karst.) knotwood: within-stem variation and the effect of fertilisation at two experimental sites in Finland. Trees 22(3):317–328Google Scholar
  81. Porth I, Hamberger B, White R, Ritland K (2011) Defense mechanisms against herbivory in Picea: sequence evolution and expression regulation of gene family members in the phenylpropanoid pathway. BMC Genomics 12(1):e608Google Scholar
  82. Prunier J, Laroche J, Beaulieu J, Bousquet J (2011) Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Mol Ecol 20(8):1702–1716PubMedGoogle Scholar
  83. Pukacki PM (2004) Effect of water deficit on oxidative stress and degradation of cell membranes in needles of Norway spruce (Picea abies). Acta Physiol Plant 26(4):431–442Google Scholar
  84. Pukacki PM, Modrzyński J (1998) The influence of ultraviolet-B radiation on the growth, pigment production and chlorophyll fluorescence of Norway spruce seedlings. Acta Physiol Plant 20(3):245–250Google Scholar
  85. Pukacki PM, Kamińska-Rożek E (2013) Reactive species, antioxidants and cold tolerance during deacclimation of Picea abies populations. Acta Physiol Plant 35(1):129–138Google Scholar
  86. Ralph SG, Yueh H, Friedmann M, Aeschliman D, Zeznik JA, Nelson CC, Butterfield YS, Kirkpatrick R, Liu J, Jones SJ, Marra MA (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(8):1545–1570PubMedGoogle Scholar
  87. 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(1):e21Google Scholar
  88. Ralph SG, Jancsik S, Bohlmann J (2007) Dirigent proteins in conifer defense II: Extended gene discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry 68(14):1975–1991Google Scholar
  89. Richard S, Lapointe G, Rutledge RG, Séguin A (2000) Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol 41(8):982–987PubMedGoogle Scholar
  90. Riikonen J, Kontunen-Soppela S, Ossipov V, Tervahauta A, Tuomainen M, Oksanen E, Vapaavuori E, Heinonen J, Kivimäenpää M (2012) Needle metabolome, freezing tolerance and gas exchange in Norway spruce seedlings exposed to elevated temperature and ozone concentration. Tree Physiol 32(9):1102–1112PubMedGoogle Scholar
  91. Rimando AM, Pan Z, Polashock JJ, Dayan FE, Mizuno CS, Snook ME, Liu CJ, Baerson SR (2012) In planta production of the highly potent resveratrol analogue pterostilbene via stilbene synthase and O-methyltransferase co-expression. Plant Biotech J 10(3):269–283Google Scholar
  92. Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194(2):321–336PubMedGoogle Scholar
  93. Rohde M, Waldmann R, Lunderstädt J (1996) Induced defence reaction in the phloem of spruce (Picea abies) and larch (Larix decidua) after attack by Ips typographus and Ips cembrae. For Ecol Manag 86(1–3):51–59Google Scholar
  94. Sallas L, Luomala EM, Utriainen J, Kainulainen P, Holopainen JK (2003) Contrasting effects of elevated carbon dioxide concentration and temperature on Rubisco activity, chlorophyll fluorescence, needle ultrastructure and secondary metabolites in conifer seedlings. Tree Physiol 23(2):97–108PubMedGoogle Scholar
  95. Schiebe C, Hammerbacher A, Birgersson G, Witzell J, Brodelius PE, Gershenzon J, Hansson BS, Krokene P, Schlyter F (2012) Inducibility of chemical defenses in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia 170(1):183–198PubMedGoogle Scholar
  96. Schmidt A, Wächtler B, Temp U, Krekling T, Séguin A, Gershenzon J (2010) A bifunctional geranyl and geranylgeranyl diphosphate synthase is involved in terpene oleoresin formation in Picea abies. Plant Physiol 152(2):639–655PubMedPubMedCentralGoogle Scholar
  97. Serreze MC, Walsh JE, Chapin FS, Osterkamp T, Dyurgerov M, Romanovsky V, Oechel WC, Morison J, Zhang T, Barry RG (2000) Observational evidence of recent change in the northern high-latitude environment. Climat. Change 46(1–2):159–207Google Scholar
  98. Slimestad R (2003) Flavonoids in buds and young needles of Picea, Pinus and Abies. Biochem Syst Ecol 31(11):1247–1255Google Scholar
  99. Slimestad R, Hostettmann K (1996) Characterisation of phenolic constituents from juvenile and mature needles of Norway spruce by means of high performance liquid chromatography–mass spectrometry. Phytochem Anal 7(1):42–48Google Scholar
  100. Song F, Song G, Dong A, Kong X (2011) Regulatory mechanisms of host plant defense responses to arbuscular mycorrhiza. Acta Ecol Sin 31(6):322–327Google Scholar
  101. Stafford HA (2000) The evolution of phenolics in plants. Recent Adv Phytochem 34:25–54Google Scholar
  102. Stenlid J, Johansson M (1987) Infection of roots of Norway spruce (Picea abies) by Heterobasidion annosum: II. Early changes in phenolic content and toxicity. Eur J Forest Pathol 17(4–5):217–226Google Scholar
  103. Storer AJ, Speight MR (1996) Relationships between Dendroctonus micans Kug. (Coleoptera: Scolytidae) survival and development and biochemical changes in Norway spruce, Picea abies (L.) Karst., phloem caused by mechanical wounding. J Chem Ecol 22(3):559–573Google Scholar
  104. Strack D, Heilemann J, Wray V, Dirks H (1989) Structures and accumulation patterns of soluble and insoluble phenolics from Norway spruce needles. Phytochemistry 28(8):2071–2078Google Scholar
  105. Taylor RJ, Shaw DC (1983) Allelopathic effects of Engelmann spruce bark stilbenes and tannin–stilbene combinations on seed germination and seedling growth of selected conifers. Can J Bot 61(1):279–289Google Scholar
  106. Vialart G, Hehn A, Olry A, Ito K, Krieger C, Larbat R, Paris C, Shimizu BI, Sugimoto Y, Mizutani M, Bourgaud F (2012) A 2‐oxoglutarate‐dependent dioxygenase from Ruta graveolens L. exhibits p‐coumaroyl CoA 2′‐hydroxylase activity (C2′ H): a missing step in the synthesis of umbelliferone in plants. Plant J 70(3):460–770Google Scholar
  107. Viiri H, Annila E, Kitunen V, Niemelä P (2001) Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees 15(2):112–122Google Scholar
  108. Virjamo V, Sutinen S, Julkunen-Tiitto R (2014) Combined effect of elevated UVB, elevated temperature and fertilization on growth, needle structure and phytochemistry of young Norway spruce (Picea abies) seedlings. Glob Chang Biol 20(7):2252–2260PubMedGoogle Scholar
  109. Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–10PubMedGoogle Scholar
  110. Wadke N, Kandasamy D, Vogel H, Lah L, Wingfield BD, Paetz C, Wright LP, Gershenzon J, Hammerbacher A (2016) The bark-beetle-associated fungus, Endoconidiophora polonica, utilizes the phenolic defense compounds of its host as a carbon source. Plant Physiol 171(2):914–931PubMedPubMedCentralGoogle Scholar
  111. Waldeck DH (1991) Photoisomerization dynamics of stilbenes. Chem Rev 91(3):415–436Google Scholar
  112. Warren RL, Keeling CI, Yuen MM, Raymond A, Taylor GA, Vandervalk BP, Mohamadi H, Paulino D, Chiu R, Jackman SD, Robertson G (2015) Improved white spruce (Picea glauca) genome assemblies and annotation of large gene families of conifer terpenoid and phenolic defense metabolism. Plant J 83(2):189–212PubMedGoogle Scholar
  113. Whitehill JG, Henderson H, Strong W, Jaquish B, Bohlmann J (2016a) Function of Sitka spruce stone cells as a physical defence against white pine weevil. Plant Cell Environ 39(11):2545–2556PubMedGoogle Scholar
  114. Whitehill JG, Henderson H, Schuetz M, Skyba O, Yuen MM, King J, Samuels AL, Mansfield SD, Bohlmann J (2016b) Histology and cell wall biochemistry of stone cells in the physical defence of conifers against insects. Plant Cell Environ 39(8):1646–1661PubMedGoogle Scholar
  115. Whitehill JG, Yuen MM, Henderson H, Madilao L, Kshatriya K, Bryan J, Jaquish B, Bohlmann J (2019) Functions of stone cells and oleoresin terpenes in the conifer defense syndrome. New Phytol 221(3):1503–1517PubMedGoogle Scholar
  116. Wilmouth RC, Turnbull JJ, Welford RW, Clifton IJ, Prescott AG, Schofield CJ (2002) Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana. Structure 10(1):93–103PubMedGoogle Scholar
  117. 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(1):127–149Google Scholar
  118. Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299(5605):396–399PubMedGoogle Scholar
  119. Yaqoob N, Yakovlev IA, Krokene P, Kvaalen H, Solheim H, Fossdal CG (2012) Defence-related gene expression in bark and sapwood of Norway spruce in response to Heterobasidion parviporum and methyl jasmonate. Physiol Mol Plant Pathol 77(1):10–16Google Scholar
  120. Zhang Y, Virjamo V, Du W, Yin Y, Nissinen K, Nybakken L, Guo H (2018) Julkunen-Tiitto R (2018) Effects of soil pyrene contamination on growth and phenolics in Norway spruce (Picea abies) are modified by elevated temperature and CO2. Environ Sci Pollut Res 1:1–12Google Scholar
  121. Zhao T, Solheim H, Långström B, Borg-Karlson AK (2011) Storm-induced tree resistance and chemical differences in Norway spruce (Picea abies). Ann For Sci 8(3):657–665Google Scholar
  122. Zhao T, Kandasamy D, Krokene P, Chen J, Gershenzon J, Hammerbacher A (2019) Fungal associates of the tree-killing bark beetle, Ips typographus, vary in virulence, ability to degrade conifer phenolics and influence bark beetle tunneling behavior. Fungal Ecol 38:71–79Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Almuth Hammerbacher
    • 1
    Email author
  • Louwrance P. Wright
    • 2
  • Jonathan Gershenzon
    • 2
  1. 1.Department of Zoology and EntomologyForestry and Agricultural Biotechnollogy Institute, University of PretoriaPretoriaSouth Africa
  2. 2.Max Planck Institute for Chemical EcologyJenaGermany

Personalised recommendations