De Gruyter Open

From December 2015 Agricultura journal will be published in partnership with De Gruyter Open (degruyteropen.com), the world's second largest publisher of Open Access academic content, and part of the De Gruyter group which has over 260 years of publishing history. De Gruyter Open closely cooperates with the majority of abstracting and indexing services, universities and libraries, providing a wide availability of journal's content and increasing its visibility. Agricultura's full-text articles will be found also at the new address on the De Gruyter Open's platform in following weeks.


Publishing support

Publishing of the journal Agricultura is financially supported by Slovenian Research Agency.

Izdajanje revije Agricultura je finančno podprto s strani Javne agencije za raziskovalno dejavnost Republike Slovenije.


Our Profile

The journal AGRICULTURA (A) publishes scientific works from the following fields: animal science, plant production, farm mechanisation, land management, agricultural economics, ecology, biotechnology, microbiology
ISSN 1581-5439

Mateja FELICIJAN, Metka NOVAK, Nada KRAŠEVEC, Andreja URBANEK KRAJNC

pp. 9-18

ABSTRACT

Bark beetles and their fungal associates are integral parts of forest ecosystems, the European spruce bark beetle (Ips typographus Linnaeus, 1758) and the associated pathogenic blue stain fungus Ceratocystis polonica (SIEM.) C. MOREAU, are the most devastating pests regarding Norway spruce [Picea abies (L.) H. KARST.]. Bark beetles commonly inhabit weakened and felled trees as well as vital trees. They cause physiological disorders in trees by destroying a phloem and cambium or interrupt the transpiration flow in the xylem. Conifers have a wide range of effective defence mechanisms that are based on the inner bark anatomy and physiological state of the tree. The basic function of bark defences is to protect the nutrient-and energy-rich phloem, the vital meristematic region of the vascular cambium, and the transpiration flow in the sapwood. The main area of defence mechanisms is secondary phloem, which is physically and chemically protected by polyphenolic parenchyma (PP) cells, sclerenchyma, calcium oxalate crystals and resin ducts. Conifer trunk pest resistance includes constitutive, inducible defences and acquired resistance. Both constitutive and inducible defences may deter beetle invasion, impede fungal growth and close entrance wounds. During a successful attack, systemic acquired resistance (SAR) becomes effective and represents a third defence strategy. It gradually develops throughout the plant and provides a systemic change within the whole tree’s metabolism, which is maintained over a longer period of time. The broad range of defence mechanisms that contribute to the activation and utilisation of SAR, includes antioxidants and antioxidant enzymes, which are generally linked to the actions of reactive oxygen species (ROS). The presented review discusses the current knowledge on the antioxidant defence strategies of spruce inner bark against the bark beetle (Ips typographus) and associated blue stain fungus (Ceratocystis polonica).

Key words: antioxidants, ascorbate-glutathione system, blue-stain fungus Ceratocystis polonica (SIEM.) C. MOREAU, Norway spruce (Picea abies (L.) H. KARST.), phenolics, systemic acquired resistance (SAR)


Slovenian:

ni obrambni odziv lubja navadne smreke ob napadu podlubnikov in z njimi povezanimi glivami modrivkami

Čeprav so podlubniki in z njimi povezane glive sestavni del gozdnih ekosistemov, sta osmerozobi smrekov lubadar (Ips typographus Linnaeus) in z njim povezana patogena gliva modrivka [Ceratocystis polonica (Siem.) C. Moreau], ena najbolj uničujočih škodljivcev navadne smreke [Picea abies (L.) H. Karsten]. Lubadarji navadno naseljujejo oslabela in podrta drevesa, v specifičnih pogojih pa lahko napadejo tudi vitalna. S poškodbami floema in kambija ter motnjo transpiracijskega toka v ksilemu, drevesu povzročijo številne fiziološke motnje. Iglavci imajo široko paleto obrambnih mehanizmov, ki temeljijo na anatomiji lubja in fiziološkem stanju drevesa. Njihova osnovna funkcija je zaščita hranilno in energetsko bogatega floemskega tkiva, meristematske aktivnosti vaskularnega kambija in transpiracijskega toka v sekundarnem ksilemu debla. Glavno področje obrambnih mehanizmov je namreč sekundarni floem, ki predstavlja fizično in kemično zaščito lubja pred škodljivci, saj vsebuje polifenolne parenhimatske celice, sklerenhim, kristale kalcijevega oksalata in shizogene smolne kanale. Obrambni sistem lubja iglavcev zajema tri vrste obrambnih strategij – konstitutivno in inducirano obrambo ter sistemsko pridobljeno odpornost. Konstitutivna in inducirana obramba zavirata kolonizacijo podlubnikov, rast gliv in zapirata ranitvena mesta. Med uspešnim napadom pa je za drevo ključnega pomena še vzpostavitev sistemsko pridobljene odpornosti (SAR). Le ta se postopoma širi po rastlini ter izzove sistemske spremembe v metabolizmu drevesa, ki se ohranjajo skozi daljše časovno obdobje. Med številnimi obrambnimi odzivi, povezanimi z aktivacijo SAR, sta pomembni sinteza antioksidantov in aktivacija antioksidativnih encimov, ki varujejo rastlino pred reaktivnimi kisikovimi spojinami (ROS). Prispevek zajema pregled dosedanjega znanja o strategijah antioksidativnega odziva lubja smreke pri napadu smrekovega lubadarja (Ips typographus) in z njim povezane patogene glive modrivke (Ceratocystis polonica).

Ključne besede: /


REFERENCES:

1. Adrian M, Jeandet P, Veneau J, Weston LA, Bessis R. Biological activity of resveratrol, a stilbenic compound from grapevines, against Botrytis cinerea, the causal agent for grey mould. J. Chem. Ecol. 1997;23:1689–1702.

2. Adrian M and Jeandet P. Effects of resveratrol on the ultrastructure of Botrytis cinerea conidia and biological significance in plant/pathogen interactions. Fitoterapia 2012;83:1345–1350.

3. Alscher RG. Biosynthesis and antioxidant function of glutathione in plants. Physioi. Plantarum 2006;77:457–464.

4. Baier P, Führer E, Kirisits T, Rosner S. Defence reactions of Norway spruce against bark beetles and the associated fungus Ceratocystis polonica in secondary pure and mixed species stands. For. Ecol. Manage. 2002;159:73–86.

5. Beaver RA. Insect-fungus relationship in the bark and ambrosia beetles. In: Wilding NM, Collins PMH and JFW (Eds). Insect-Fungus Interactions. San Diego, CA, Academic Press, 1989;119–143.

6. Beckman CH. 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. 2000;57:101–110.

7. Bonello P, Gordon TR, Storer AJ. Systemic induced resistance in Monterey pine. For. Pathol. 2001;31:99–106.

8. Bonello P, Blodgett JT. Pinus nigra–Sphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol. Mol. Plant Pathol. 2003;63:249–261.

9. Bonello P, Gordon TR, Herms DA, Wood DL, Erbilgin N. Nature and ecological implications of pathogen-induced systemic resistance in conifers: A novel hypothesis. Physiol. Mol. Plant Pathol. 2006;68(4–6):95–104.

10. Brignolas F, Lacroix B, Lieutier F, Sauvard D, Drouet A, Claudot AC, Yart A, Berryman AA, Christiansen E. Induced responses in phenolic metabolism in two Norway spruce clones after wounding and inoculations with Ophiostoma polonicum, a bark-beetle associated fungus. Plant Physiol. 1995;109(3):821–827.

11. Brignolas F, Lieutier F, Sauvard D, Christiansen E, Berryman AA. Phenolic predictors for Norway spruce resistance to the bark beetle Ips typographus (Coleoptera: Scolytidae) and an associated fungus, Ceratocystis polonica. Can. J. For. Res. 1998;28:720–728.

12. Brodnjak Vončina D. Antioksidanti Analizna kemija II, Univerza v Mariboru, Fakulteta za kemijo in kemijsko tehnologijo. 2006.

13. Cameron JC and Pakrasi HB. Essential role of glutathione in acclimation to environmental and redox perturbations in the cyanobacterium synechocystis sp. PCC 6803. Plant Physiol. 2010;154: 1672–1685.

14. Christiansen E in Bakke A. The spruce bark beetle of Eurasia. In: Berryman AA (Ed). Population ecology: theory and application. New York,Plenum Press, 1988;479–503.

15. Christiansen E, Krokene P, Berryman AA, Franceschi VR, Krekling T, Lieutier F, Lonneborg A, Solheim H. Mechanical injury and fungal infection induce acquired resistance in Norway spruce. Tree Physiol. 1999;19:399–403.

16. Erbilgin N, Krokne P, Christian E, Zeneli G, Gershenzon J. Exogenous application of methyl jasmonate elicits defenses in Norway spruce (Picea abies) and reduces host colonization by the bark beetle Ips typographus. Oecologia 2006;148:426–436.

17. Evensen PC, Solheim H, Hoiland K, Stenersen J. Induced resistance of Norway spruce, variation of phenolic compounds and their effects on fungal pathogens. Forest Pathol. 2000;30:97–108.

18. Eyles A, Bonello P, Ganley R, Mohammed C. Induced resistance to pests and pathogens in trees. New Phytol. 2009;185:893–908.

19. Fäldt J, Martin D, Miller B, Rawat S, Böhlmann J. 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. 2003;51:119–133.

20. Felicijan M. Časovna analiza vsebnosti kondenziranih taninov v lubju navadne smreke pri napadu podlubnikov. Univerza v Mariboru. Fakulteta za kmetijstvo in biosistemske vede. Diplomsko delo 2011.

21. Foyer CH, Rennenberg H. Regulation of glutathione synthesis and its role in abiotic and biotic stress defence. In: Brunold C, Rennenberg H, De Kok LJ, Stulen I, Davidian J-C (Eds). Sulfur nutrition and sulfur assimilation in higher plants. Paul Haupt, Bern 2000;127–153.

22. Foyer CH in Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 2011;155:2–18.

23. Franceschi VR, Krokene P, Krekling T, Christiansen E. 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. 2000;87:314–326.

24. Franceschi VR, Krekling T, Christiansen E. Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am. J. Bot. 2002;89(4):578–586, 602–610.

25. Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New phytol. 2005;167(2):353–376.

26. Grant CM, MacIver FH, Dawes IW. Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr. Genet. 1996;29(6):511-515.

27. Grill D, Tausz M and De Kok LJ. Significance of glutathione in plant adaptation to the environment. In: De Kok LJ (Ed). Handbook of Plant Ecophysiology. Kluwer Academic Publishers, Dordrecht, 2001.

28. Gullner G, Komives T. The role of glutathione and glutathione-related enzymes in plant-pathogen interaction. In: Grill D, Tausz M, De Kok LJ (Eds). Significance of glutathione to plant adaptation to the environment. Kluwer Academic Publishers, Dordrecht, Boston, London, 2001;207–239.

29. Hammerbacher A, Ralph SG, Bohlmann J, Fenning TM, Gershenzon J, Schmidt A. Biosynthesis of the major tetrahydroxystilbenes in spruce, astringin and isorhapontin, proceeds via resveratrol and is enhanced by fungal infection. Plant Physiol. 2011;157:876–890.

30. Hammerbacher A, Schmidt A, Wadke N, Wright LP, Schneider B, Bohlmann J, Brand WA, Fenning TM, Gershenzon J, Paetz C. A common fungal associate of the spruce bark beetle metabolizes the stilbene defenses of Norway spruce. Plant Physiol. 2013;162:1324–1336.

31. Harris C, Hansen JM. Oxidative stress, thiols, and redox profiles. Methods Mol. Biol. 2012;889:325–46.

32. Hayat Q, Hayat S, Ifran M Ahmad A. Effect of exogenous salicylic acid under changing enviroment: A review. Envirom. Exp. Bot. 2009;68:14–25.

33. Havsteen BH. The biochemistry and medical significance of the flavonoids. Pharmacol. Ther. 2002;96(2–3):67–202.

34. He S, Wu B, Pan YJ, Jiang LY. Stilbene oligomers from Parthenocissus laetevirens: isolation, biomimetic synthesis, absolute configuration, and implication of antioxidative defense system in the plant. J. Org. Chem. 2008;73(14):5233–5241.

35. Holger L, Bjørn Ø and Krokene P Thresholds in the life cycle of the spruce bark beetle under climate change. Int. J. 2006;1–10.

36. Hudings JW, Christiansen E, Franceschi VR. Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiol. 2004;24:251–264.

37. Hudings JW and Franceschi VR. 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. 2004;135(4):2134–2149.

38. Johnson MA and Croteau R. Ecology and metabolism of plant lipids In: Fuller G and Nes WD (Eds). Washington DC, American Chemical Society, 1987.

39. Jurc M. Gozdna zoologija. Ljubljana. Biotehniška fakulteta. Oddelek za gozdarstvo in obnovljive gozdne vire. Narodna in univerzitetna knjižnica. 2011.

40. Kawano T and Muto S. Mechanism of peroxidase actions for salicylic acid induced generation of active oxygen species and an increase in cytosolic calcium in tobacco cell suspension culture. J. Exp. Bot. 2000;345(51):685–693.

41. Klepzig KD, Adams AS, Handelsman J, Raffa KF. Symbioses: A key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans. Environ. Entomol. 2009;38(1):67–77.

42. Kozlowski G, Buchala A, Metraux JP. Methyl jasmonate protects Norway spruce (Picea abies (L.) Karst.) seedlings against Pythium ultimum Trow. Phys. Mol. Plant Path. 1999;55(1):53–58.

43. Kreft I, Škrabanja V, Bonafaccia G. Temelji prehranskih in biotskih vplivov antioksidantov. In: Žlender B, Gašperlin L. (Eds). Antioksidanti v živilstvu. 20. Bitenčevi živilski dnevi 2000. Ljubljana, Biotehniška fakulteta, Oddelek za živilstvo. 2000;33–37.

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

45. Krekling T, Franceschi VR, Krokene P, Solheim H. Differential anatomical responses of Norway spruce stem tissues to sterile and fungus infected inoculations. Trees 2004;18:1–9.

46. Krokene P and Solheim H. Pathogenicity of four blue-stain fungi associated with aggressive and nonaggressive bark beetles. Phytopatology 1998;88:39–44.

47. Krokene P and Solheim H. What do low-density inoculations with fungus tell us about fungal virulence and tree resistance?. In: Lieutier F, Mattson WJ and Wagner MR (Eds). Physiology and genetics of tree-phytophage interactions. INRA Editions Versailles, France, 1999;353–362.

48. Kugler N. Vpliv temperature in čas ekstrakcije na vsebnost antioksidativnih učinkovin iz iglavcev. Univerza v Mariboru, Fakulteta za kemijo in kemijsko tehnologijo. Diplomsko delo 2011.

49. Larcher, W. Physiological plant ecology. Springer Verlag, Berlin, 2003.

50. Li S-H, Nagy NE, Hammerbacher A, Krokene P, Niu X-M, Gershenzon J, Schneider B. Localization of phenolics in phloem parenchyma cells of Norway spruce (Picea abies). ChemBio-Chem. 2012;13:2707–2713.

51. Lieutier F, Brignolas F, Sauvard D, Yart A, Galet C, Brunet M, Van de Sype H. Intra- and inter-provenance variability in phloem phenols of Picea abies and relationship to a bark beetle-associated fungus. Tree Physiol. 2003;23(4):247–256.

52. Linnakoski R, Beer ZW, Niemelä P, in Wingfield MJ. Associations of conifer-infesting bark beetles and fungi in fennoscandia. Insects 2012;3:200–227.
53. Likar M and Regvar M. Praktikum fiziologije rastlin. Ljubljana, Študentska založba. 2003;94.

54. Malá J, Hrubcová M, Máchová P, Cvrčková H, Martincová O, Cvikrová M. Changes in phenolic acids and stilbenes induced in embryogenic cell cultures of Norway spruce by two fractions of Sirococcus strobilinus mycelia. J. For. Sci. 2011;57:1–7.

55. Martin D, Tholl D, Gershenzon J, Bohlmann J. Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol. 2002;129:1003–1018.

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

57. Meyer AJ and Hell R. Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth. Res. 2005;86:435–457.

58. Miller B, Madilao LL, Ralph S, Bohlmann J. Insect-induced conifer defense: White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and octadecanoid pathway transcripts in Sitka spruce. Plant Physiol. 2005;137:369–382.

59. Müller M and Job H. Managing natural disturbance in protected areas: Tourists attitude towards the bark beetle in a German national park. Biol. Conserv. 2009;142:375–383.

60. Nagy NE, Fossdal CG, Krokene P, Krekling T, Lönneborg A, Solheim H. Induced responses to pathogen infection in Norway spruce phloem: changes in polyphenolic parenchyma cells, chalcone synthase transcript levels and peroxidase activity. Tree physiol. 2004;24:505–15.

61. Nagy NE, Franceschi VR, Kvaalen H, Solheim H.. Callus cultures and bark from Norway spruce clones show similar cellular features and relative resistance to fungal pathogens. Trees 2005;19(6):695–703.

62. Nebeker T and Hodges J. Host response to bark beetle and pathogen colonization. Schowalter GF (Ed). In: Beetle - pathogen interactions in conifer forests, San Diego, Academic, 1993;157–173 pp.

63. Noctor G, Arisi A-CM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J. Exp. Bot. 1998;49:321;623–647.

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

65. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G in Foyer CH. Glutathione in plants: an integrated overview. Plant Cell Environ. 2012;35(2):454–484.

66. Novak M, Urbanek Krajnc A, Lah L, Zupanec N, Kraševec N, Križman M, Bohlmann J, Komel R. Low density Ceratocystis polonica inoculation of Norway spruce (Picea abies) triggers accumulation of monoterpenes with antifungal properties. Eur. J. For. Res. 2014;133:573-583.

67. Novak M. Cytochromes P450 from blue-stain fungi involved in monoterpene biotransformation. Univerza v Ljubljani. Medicinska fakulteta. Doktorska disertacija 2014.

68. Paine TD, Raffa KF, Harrington TC. Interactions among Scolytid bark beetles, their associated fungi, and live host conifers. Ann. Rev. Entomol. 1997;42:179–206.

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

70. Pont V and Pezet R. Relation between the chemical structure and the biological activity of hydroxystilbenes against Botrytis cinerea. J. Phytopathol. 2008;130(1):1–8.

71. Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG, Romme WH. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: The dynamics of bark beetle eruptions. BioScience 2008;58:501.

72. Ralph SG, Yueh H, Friedmann M, Aeschliman D, Zeznik JA, Nelson CC, Butterfield YSN, Kirkpatrick R, Liu J, Jones SJM et al. 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. 2006;29:1545–1570.

73. Riedle-Bauer M. Role of reactive oxygen species and antioxidant enzymes in systemic virus infections of plants. J. Phytopathol. 2000;148:297–302.

74. Rodrigues, KCS, Fett-Neto AG. Oleoresin yield of Pinus elliottii in a subtropical climate: Seasonal variation and effect of auxin and salicylic acid-based stimulant paste. Ind. Crops Prod. 2009;30:316–320.

75. Rohde M, Waldmann R, Lunderstädt. Induced defence reaction in the -phloem of spruce (Picea abies) and larch (Larix decidua) after attack by Ips typographus and Ips cembrae. Forest. Ecol. Manag. 1996;86:51–59.

76. Sallé A, Monclus R, Yart A, Garcia J, Romary PLF. Fungal flora associated with Ips typographus: frequency, virulence, and ability to stimulate the host defence reaction in relation to insect population levels. Can. J. For. Res. 2005;35:365–373.

77. Schmidt A, Zeneli G, Hietala AM, Fossdal CG, Krokene P, Christiansen E, Gershenzon J. Induced chemical defenses in conifers: Biochemical and molecular approaches to studyung their function. In: Schmidt A, Zeneli G, Hietala AM, Fossdal CG, Krokene P, Christiansen, Gershenzon J,Romeo JT (Eds). Chemical ecology and phytochemistry in forest ecosystems, Vol. 39. Elsevier, Amsterdam, 2005;1–28.

78. Six DL and Wingfield MJ. The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Ann. Rev. Entomol. 2011;56:255–72.

79. Sjostrom E. Wood chemistry, fundamentals and applications. Second Edition. Academic press, Inc., Harcourt Brace Jovanovich, Boston, London, Sydney, Tokyo, Toronto, 1993;293.

80. Smirnoff N and Wheeler GL. Ascorbic acid in plants: biosynthesis and function. Crit. Rev. Plant. Sci. 2000;19:267–290.

81. Smith GD, Carroll AL, Lindgren BS. Facilitation in bark beetles: endemic mountain pine beetle gets a helping hand. Agric. For. Entomol. 2011;13:37–43.

82. Šuštaršič S. Kako meriti stres pri rastlinah? Univerza v Ljubljani, Biotehniška fakulteta. Diplomski projekt 2012.

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

84. Tausz M, Šircelj H, Grill D. The glutathione system as a stress marker in plant ecopysiology: is a stress-response concept valid? J. Exp. Bot. 2004;55(404):1955–1962.

85. Tegischer K, Tausz M, Wieser G, Grill D. Tree-age and needle-age dependent variations of antioxidants and photoprotective pigments in spruce needles at the alpine timberline. Tree Physiol. 2002;22:591–596.

86. Torres P, Avila JG, Romo de Vivar A, García AM, Marín JC, Aranda E, Céspedes CL. Antioxidant and insect growth regulatory activities of stilbenes and extracts from Yucca periculosa. Phytochemistry 2003;64:463–473.

87. Urbanek Krajnc A. Effects of endogenously increased levels of thiol compounds and salicylic acid on Zucchini yellow mosaic virus infected Styrian oil pumpkin plants. Thesis. Uni Graz. 2004.

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

89. Urbanek Krajnc A, Kristl J, Ivancic A. Application of salicylic acid induces antioxidant defense responses in the phloem of Picea abies and inhibits colonization by Ips typographus. ForEcol Manage. 2011;261:416–426.

90. Urbanek Krajnc A, Novak M, Felicijan M, Kraševec N, Lešnik M, Zupanec N, Komel R. Antioxidative response patterns of Norway spruce bark to low-density Ceratocystis polonica inoculation. Trees 2014;28(4):1145–1160.

91. Veberič R. Bioactive compounds in fruit plants. el. knjiga. Ljubljana. Narodna in univerzitetna knjižnica, Biotehniška fakulteta. 2010. (URL): http://www.bf.uni-lj.si/agronomija/ooddelku/katedre-in-druge-org-enote/za-sadjarstvo-vinogradnistvo-invrtnarstvo/sadjarstvo/

92. Viiri H, Annila E, Kitunen V, Niemelä P. Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus Ceratocystis polonica. Trees 2001;15:112–122.

93. Wallis C, Eyles A, Chorbadjian R, McSpadden Gardener B, Hansen R, Cipollini D, Herms DA, Bonello P. Systemic induction of phloem secondary metabolism and its relationship to resistance to a canker pathogen in Austrian pine. New Phytol. 2008;177:767–778.

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

95. Whitney H. Relationships between bark beetles and symbiotic organisms. Mitton J, Sturgeon K (Eds). In: Bark beetles in north American conifers. Austin: Univ. Texas, 1982;183–211pp.

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

97. Woods JA, Hadfield JA, Pettit GR, Fox BW, McGown AT. The interaction with tubulin of a series of stilbenes based on combretastatin A-4. Br. J. Cancer 1995;71:705–711.

98. Xiang C, Werner BL, Christensen EM and Oliver DJ. The biological functions of glutathione revisited in arabidopsis transgenic plants with altered glutathione levels. Plant Physiol. 2001;126:564–574.

99. Zechmann B, Zellnig G, Urbanek Krajnc A and Muller M. Artificial elevation of glutathione affects symptom development in ZYMV-infected Cucurbita pepo L. plants. Arch. Virol. 2007;152:747–762.

100. Zeneli G, Krokene P, Christiansen E, Krekling T, Gershenzon J. 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. 2006;26:988–997.

101. Zhao FJ, Tausz M, De Kok LJ. 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 2008;417–435.

logo dg open        cm stacked 064 plain