Skip to main content
SpringerLink
Log in

Pre-treatment with salicylic acid induces phenolic responses of Norway spruce (Picea abies) bark to bark beetle (Ips typographus) attack

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Keymessage

The temporal gradations of the investigated phenolics in Norway spruce bark after bark beetle (Ips typographus) attack followed the general eco-physiological concept. Treatment with salicylic acid inhibits bark beetle colonisation, alleviates the phenolic responses and activates the synthesis of condensed tannins on later sampling dates.

Abstract

Conifer bark is the target of numerous organisms due to its assimilated transport and nutrient storage functions. In the presented study, 100 mM salicylic acid (SA) was applied onto Norway spruce stems prior to being infested with bark beetles (Ips typographus L.), to study the temporal gradation of changes in condensed tannins (CT) and total phenolics (tPH) and their significance for mediating stress-tolerance. A significant accumulation of CT was monitored in untreated trees in response to progressive bark beetle infestation occurring from May onwards. In SA-treated infested trees, the CT values remained at control levels until May, but after the re-treatment of infested trees in June, the concentrations of CT rose significantly in comparison to the controls. The tPH values dropped 16 days after SA-treatment, independent of infestation, and later on remained at control level until July. In contrast, tPH contents accumulated in untreated infested trees in May, eased in June and increased again in July, when the trees were affected by the second generation of bark beetles. To sum up, in May and July when the highest beetle-flight activity was monitored the metabolic shift of phenolics within untreated infested trees differed significantly from the response of SA-treated trees. In addition, on SA-treated trees less entrance holes were monitored over the whole period of sampling when compared to untreated infested trees. These results provide evidence that SA-treatment alleviates the phenolic responses, activates the synthesis of condensed tannins and inhibits bark beetle colonisation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdalla S, Pizzi A, Ayed N, Charrier-El Bouthoury F, Charrier B, Bahabri F, Ganash A (2014) MALDI-TOF analysis of Aleppo pine (Pinus halepensis) bark tannin. BioResources 9(2):3396–3406

    Article  CAS  Google Scholar 

  • Adamczyk B, Adamczyk S, Smolander A, Kitunen V (2011) Tannic acid and Norway spruce condensed tannins can precipitate various organic nitrogen compounds. Soil Biol Biochem 43(3):628–637

    Article  CAS  Google Scholar 

  • Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat Protoc 2:875–877

    Article  CAS  PubMed  Google Scholar 

  • Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for tannin biosynthesis in Populus. Oecologia 130(4):585–593

    Article  Google Scholar 

  • Barakat A, Bagniewska-Zadworna A, Frost CJ, Carlson JE (2010) Phylogeny and expression profiling of CAD and CAD-like genes in hybrid Populus (P. deltoides x P. nigra): evidence from herbivore damage for subfunctionalization and functional divergence. BMC Plant Biol 10:100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbehenn RV, Cheek S, Gasperut A, Lister E, Maben R (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midgut of Malacosoma disstria and Orgyia leucostigma caterpillars. J Chem Ecol 31:969–988

    Article  CAS  PubMed  Google Scholar 

  • Beckman CH (2000) Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defence responses in plants? Phys Mol Plant Path 57:101–110

    Article  CAS  Google Scholar 

  • 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 Molec Plant Path 68:95–104

    Article  CAS  Google Scholar 

  • Bortz J, Lienert G, Boehnke K (1990) Verteilungsfreie Methoden in der Biostatistik. Springer-Verlag, Berlin

    Book  Google Scholar 

  • 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 28:720–728

    Article  CAS  Google Scholar 

  • 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 19:399–403

    Article  PubMed  Google Scholar 

  • Chupin L, Motillon C, Charrier-El Bouhtoury F, Pizzi A, Charrier B (2013) Characterization of maritime pine (Pinus pinaster) bark tannins extracted under different conditions by spectroscopic methods, FTIR and HPLC. Ind Crop Prod 49:897–903

    Article  CAS  Google Scholar 

  • 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 In 15(4):380–387

    Article  CAS  Google Scholar 

  • Erbilgin N, Krokne P, Christian 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 148:426–436

    Article  PubMed  Google Scholar 

  • 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 30:97–108

    Article  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic inter-face between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 spurce (Pinaceae). Am J Bot 87:314–326

    Article  CAS  PubMed  Google Scholar 

  • 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(4):578–586

    Article  CAS  PubMed  Google Scholar 

  • 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(2):353–376

    Article  CAS  PubMed  Google Scholar 

  • Hagerman AE (2002, 2011) Tannin handbook. Miami University, Oxford

  • 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 162:1324–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hassanpour S, Maheri-Sis N, Eshratkhah B, Baghbani Mehmandar F (2011) Plants and secondary metabolites (Tannins): a review. Int J Forest Soil and Erosion 1(1):47–53

    Google Scholar 

  • Hayat S, Ali B, Ahmad A (2007) Salicylic acid: Biosynthesis, metabolism and physiological role in plants. In: Hayat S, Ahmad A (eds) Salicylic acid: A plant hormone. Springer, New York

    Chapter  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25

    Article  CAS  Google Scholar 

  • Hudgins JW, Christiansen E, Franceschi VR (2003a) Methyl jasmonate induces changes mimicking anatomical and chemical defenses in diverse members of the Piniaceae. Tree Physiol 23:361–371

    Article  CAS  PubMed  Google Scholar 

  • Hudgins JW, Krekling T, Franceschi VR (2003b) Distribution of calcium oxalate crystals in the secondary phloem of conifers: a constitutive defense mechanism? New Phytol 159:677–690

    Article  CAS  Google Scholar 

  • 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):865–877

    Article  CAS  PubMed  Google Scholar 

  • Hudings JW, Franceschi VR (2004) Methyl jasmonate-induced ethylene production in responsible for conifer phloem defense responses and reprogramming of stem cambial zone for traumatic resin duct formation. Plant Physiol 13:2134–2149

    Google Scholar 

  • Hunter MD, Schultz JC (1995) Fertilization mitigates chemical induction and herbivore responses within damaged oak trees. Ecology 76:1226–1232

    Article  Google Scholar 

  • Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55(404):1831–1842

    Article  CAS  PubMed  Google Scholar 

  • Kozlowski G, Metraux J-P (1998) Infection of Norway spruce (Picea abies (L.) Karst.) seedling with Pythium irregular Buism. and Pythium ultimum Trow.: histological and biochemical responses. Eurp J Plant Path 104:225–234

    Article  CAS  Google Scholar 

  • Krekling T, Franceschi VR, Berryman AA, Christiansen E (2000) The structure and development of polyphenolic parenchyma cells in Norway spurce (Picea abies) bark. Flora 195:354–369

    Google Scholar 

  • Krogell J, Holmbom B, Pranovich A, Hemming J, Willför S (2012) Extraction and chemical characterization of Norway spruce inner and outer bark. Nordic Pulp Paper Res J 27:6–17

    Article  CAS  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in plant defense. Curr Opin Plant Biol 5:325–331

    Article  CAS  PubMed  Google Scholar 

  • Larcher W (2003) Physiological plant ecology. Springer Verlag, Berlin

    Book  Google Scholar 

  • Maie N, Behrens A, Knicker H, Kögel-Knaber I (2003) Changes in the structure and protein binding ability of condensed tannins during decomposition of fresh needles and leaves. Soil Biol Biochem 35:577–589

    Article  CAS  Google Scholar 

  • Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132:1586–1599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(5):505–515

    Article  CAS  PubMed  Google Scholar 

  • Noctor G (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425

    Article  CAS  PubMed  Google Scholar 

  • Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27(9):1289–1313

    Article  CAS  PubMed  Google Scholar 

  • Percival GC (2001) Induction of systemic acquired disease resistance in plants: potential implications for disease management in urban forestry. J Arboric 27(4):181–192

    Google Scholar 

  • Pervieux I, Bourassa M, Laurans F, Hamelin R, Séguin A (2004) A spruce defensin showing strong antifungal activity and increased transcript accumulation after wounding and jasmonate treatments. Physiol Mol Plant Pathol 64:331–341

    Article  CAS  Google Scholar 

  • Peters D, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning, expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant Journal 32:701–712

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7:456–464

    Article  CAS  PubMed  Google Scholar 

  • Radwan DEM, Fayez KA, Mahmound SY, Hamad A, Lu G (2007) Physiological and metabolic changes of Cucurbita pepo leaves in response to zucchini yellow mosaic virus (ZYMV) infection and salicylic acid treatments. Plant Phys Biochem 45:480–489

    Article  CAS  Google Scholar 

  • Ralph SG, Yueh H, Friedmann M, Aeschliman D, Zeznik JA, Nelson CC, Butterfield YSN, Kirkpatrick R, Liu J, Jones SJM et al (2006) Conifer defence against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworms (Choristoneura occidentalis) or white pine weevils (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant Cell Environ 29:1545–1570

    Article  PubMed  Google Scholar 

  • Rodrigues KCS, Fett-Neto G (2009) Oleoresin yield of Pinus elliottii in a subtropical climate: seasonal variation and effect of auxin and salicylic acid-based stimulant paste. Ind Crops Prod 30:316–320

    Article  CAS  Google Scholar 

  • Rohde M, Waldmann R, Lunderstadt J (1996) Induced defence reaction in the phloem of spruce (Picea abies) and larch (Larix deciduas) after attack by Ips typographus and Ips cembrae. For Ecol Manag 86:51–59

    Article  Google Scholar 

  • Roitto M, Rautio P, Markkola A, Julkunen-Tiitto R, Varama M, Saravesi K, Tuomi J (2009) Induced accumulation of phenolics and sawfly performance in Scots pine in response to previous defoliation. Tree Physiol 29:207–216

    Article  CAS  PubMed  Google Scholar 

  • Rossi AM, Stiling P, Moon DC, Cattell MV, Drake BG (2004) Induced defensive response of myrtle oak to foliar insect herbivory in ambient and elevated CO2. J Chem Ecol 30:1143–1152

    Article  CAS  PubMed  Google Scholar 

  • Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Special issue: evolutionary ecology of plant defences against herbivores. Funct Ecol 25(2):325–338

    Article  Google Scholar 

  • Schmidt A, Zeneli G, Hietala AM, Fossdal CG, Krokene P, Christiansen E, Gershenzon J (2005) Induced chemical defenses in conifers: Biochemical and molecular approaches to studying their function. In: Schmidt A, Zeneli G, Hietala AM, Fossdal CG, Krokene P, Christiansen E, Gershenzon J, Romeo JT (eds) Chemical ecology and phytochemistry in forest ecosystems. Elsevier, Amsterdam

    Google Scholar 

  • Schofield P, Mbugua DM, Pell AN (2001) Analysis of condensed tannins: a review. Anim Feed Sci Tech 91:21–40

    Article  CAS  Google Scholar 

  • Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151

    Article  CAS  PubMed  Google Scholar 

  • Simmonds MSJ (2003) Flavonoid-insect interactions: recent advances in our knowledge. Phytochemistry 64:21–30

    Article  CAS  PubMed  Google Scholar 

  • Stevens MT, Lindroth RL (2005) Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306

    Article  PubMed  Google Scholar 

  • Tausz M, Wonisch A, Grill D, Morales D, Jimenez MS (2003) Measuring antioxidants in tree species in the natural environment: from sampling to data evaluation. J Exp Bot 54(387):1505–1510

    Article  CAS  PubMed  Google Scholar 

  • Tsai C-J, Hardig SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006) Genome-wide analysis of the structural genes regulating defence phenylpropanoid metabolism in Populus. New Phytol 172(1):47–62

    Article  CAS  PubMed  Google Scholar 

  • Ucar MB, Ucar G, Pizzi A, Gonultas O (2013) Characterization of Pinus brutia bark tannin by MALDI-TOF MS and 13 C NMR. Ind Crop and Prod 49:697–704

    Article  CAS  Google Scholar 

  • Urbanek Krajnc A (2009) A temporal analysis of antioxidative defense responses in the phloem of Picea abies after attack by Ips typographus. Tree Physiol 29(8):1059–1068

    Article  CAS  PubMed  Google Scholar 

  • Urbanek Krajnc A, Kristl J, Ivančič A (2011) Application of salicylic acid induces antioxidant defense responses in the phloem of Picea abies and inhibits colonization by Ips typographus. Forest Ecol Manag 261:416–426

    Article  Google Scholar 

  • Urbanek Krajnc A, 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):1145–1160

    Article  CAS  Google Scholar 

  • War AR, Paulraj MG, War MY, Ignacimuthu S (2011a) Jasmonic acid- mediated induced resistance in groundnut (Arachis hypogaea L.) against Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). J of Plant Growth Regul 30:512–523

    Article  CAS  Google Scholar 

  • War AR, Paulraj MG, War MY, Ignacimuthu S (2011b) Herbivore- and elicitor-induced resistance in groundnut to Asian armyworm, Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). Plant Signal Behav 6:1769–1777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • War AR, Paulray MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S (2012) Mechanisms of plant defence against insect herbivores. Plant Signal Behav 7(10):1306–1320

    Article  PubMed  PubMed Central  Google Scholar 

  • Wermelinger B (2004) Ecology and management of the spruce bark beetle Ips typographus–a review of recent research. Forest Ecol Manag 202(1–3):67–82

    Article  Google Scholar 

  • Witzell J, Martın JA (2008) Phenolic metabolites in the resistance of northern forest trees to pathogens—past experiences and future prospects. Can J For Res 38:2711–2727

    Article  Google Scholar 

  • Yu Z, Dahlgren RA (2000) Evaluation of methods for measuring polyphenols in conifer foliage. J Chem Ecol 26(9):2119–2140

    Article  CAS  Google Scholar 

  • Zhao FJ, Tausz M, De Kok LJ (2008) Role of sulfur for plant production in agricultural and natural ecosystems. In: Hell R, Dahl C, Knaff D, Leustek T (eds) Advances in photosynthesis and respiration. Springer, Dordrecht

    Google Scholar 

  • Zhao LY, Chen JL, Cheng DF, Sun JR, Liu Y, Tian Z (2009) Biochemical and molecular characterizations of Sitobion avenae–induced wheat defense responses. Crop Prot 28:435–442

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by the Slovenian Research Agency (ARRS, Z1-9602 and P1-0164). The authors thank Andreja Šober and Anja Ivanuš for laboratory assistance and Vilma Sem for statistical evaluation of results. Peter Kramer from the Maribor University Agriculture Centre, as well as Alojz Pucko from the Slovenian Forestry Service, were acknowledged for permission to use the experimental field, and support during the experimental work. The authors also thank the reviewers for valuable comments and suggestions.

Author information

Authors and Affiliations

  1. Faculty of Agriculture and Life Sciences, Pivola 10, 2311, Hoče, Slovenia

    Mateja Felicijan, Janja Kristl & Andreja Urbanek Krajnc

Authors
  1. Mateja Felicijan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Janja Kristl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreja Urbanek Krajnc
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreja Urbanek Krajnc.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Communicated by T. Koike.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Felicijan, M., Kristl, J. & Krajnc, A.U. Pre-treatment with salicylic acid induces phenolic responses of Norway spruce (Picea abies) bark to bark beetle (Ips typographus) attack. Trees 30, 2117–2129 (2016). https://doi.org/10.1007/s00468-016-1438-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-016-1438-x

Keywords

Search

Navigation