Application of salicylic acid induces antioxidant defense responses in the phloem of Picea abies and inhibits colonization by Ips typographus

Forest Ecology and Management

Volumn 261, Issue 3, 2011, Pages 416-426

  Urbanek Krajnc, Andreja ^a   Kristl, Janja ^a   Ivancic, Anton ^a  

^a UNIVERSITY OF MARIBOR   (Slovenia)

Author keywords

Antioxidant defence system; Ascorbic acid; Glutathione; Ips typographus; Phenolics; Picea abies; Salicylic acid

Indexed keywords

ANTIOXIDANT DEFENCE SYSTEM; ASCORBIC ACIDS; GLUTATHIONES; IPS TYPOGRAPHUS; PHENOLICS; PICEA ABIES; SALICYLIC ACIDS;

AMINO ACIDS; DEGRADATION; KETONES; LAKES; ORGANIC ACIDS; OXIDATION; PHENOLS; PLANTS (BOTANY);

FORESTRY;

ADAPTIVE RADIATION; ANTIPARASITE DEFENSE; BEETLE; BIODEGRADATION; CARBOXYLIC ACID; COLONIZATION; ECOPHYSIOLOGY; ENVIRONMENTAL FACTOR; ENVIRONMENTAL STRESS; EVERGREEN TREE; INHIBITION; OXIDATION; PEPTIDE; PHENOLIC COMPOUND; PHENOTYPIC PLASTICITY; PHLOEM; POPULATION DECLINE; REDOX POTENTIAL; SAMPLING; TOLERANCE;

AMINO ACIDS; ASCORBIC ACID; DEGRADATION; FORESTRY; INSECTS; KETONES; LAKES; ORGANIC ACIDS; OXIDATION; PHENOLIC ACIDS; PICEA ABIES; SALICYLIC ACID;

COLEOPTERA; IPS TYPOGRAPHUS; PICEA ABIES; SCOLYTINAE;

EID: 78651250102     PISSN: 03781127     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foreco.2010.10.027     Document Type: Article

References (73)

1. Ainsworth E.A., Gillespie K.M. Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat. Protoc. 2007, 2:875-877.
2. Barna B., Fodor J., Pogány M., Király Z. Role of reactive oxygen species and antioxidants in plant disease resistance. Pest Man. Sci. 2003, 59:459-464.
3. Bloem E., Haneklaus S., Schnug E. Significance of sulfur compounds in the protection of plants against pests and diseases. J. Plant Nut. 2005, 28:763-784.
4. Bloem E., Haneklaus S., Salac I., Wickenhäuser P., Schnug E. Facts and fiction about sulphur metabolism in relation to plant-pathogen interactions. J. Plant Biol. 2007, 9:596-607.
5. Bonello P., Gordon T.R., Herms D.A., Wood D.L., Erbilgin N. Nature and ecological implications of pathogen-induced systemic resistance in conifers: a novel hypothesis. Physiol. Molec. Plant Path. 2006, 68:95-104.
6. Bortz J., Lienert G.A., Boenke K. Verteilungsfreie Methoden in der Biostatistik 2000, Springer Verlag, Berlin, Heidelberg, New York, Tokyo.
7. Chen H.-J., Hou W.-C., Kuć J., Lin Y.-H. Ca2+-dependent and Ca2+-independent excretion modes of salicylic acid in tobacco cell suspension culture. J. Exp. Bot. 2001, 52:1219-1226.
8. Christiansen E., Krokene P., Berryman A.A., Franceschi V.R., 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.
9. Davis J.M., Wu H.G., Cooke J.E.K., Reed J.M., Luce K.S., Michler C.H. Pathogen challenge, salicylic acid, and jasmonic acid regulate expression of chitinase gene homologs in pine. Mol. Plant Microbe In. 2002, 15(4):380-387.
10. Dihazi A., Jaiti F., Zouine J., El Hassniand M., El Hadrami I. Effect of salicylic acid on phenolic compounds related to date palm resistance to Fusarium oxysporum f.sp. albedinis. Phytopath. Mediterr. 2003, 42:9-16.
11. Durrant W.E., Dong X. Systemic acquired resistance. Annu. Rev. Phytopathol. 2004, 42:185-209.
12. Erbilgin N., Krokene P., Christiansen 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.
13. Evensen P.C., 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.
14. Fodor J., Gullner G., Adam A.L., Barna B., Kömives T., Kiraly Z. Local and systemic response of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Role in systemic acquired resistance. Plant Physiol. 1997, 114:1443-1451.
15. Foyer C.H., Noctor G. Redox homeostasis and antioxidant signaling: a metabolic inter-face between stress perception and physiological responses. Plant Cell 2005, 17:1866-1875.
16. Franceschi V.R., 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, 89:602-610.
17. Franceschi V.R., Krokene P., Christiansen E., Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 2005, 167(2):353-375.
18. Franceschi V.R., 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.
19. Freemann J.L., Garcia D., Kim D., Hopf A., Salt D.E. Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol. 2005, 137:1082-1091.
20. Freemann J.L., Persans M.W., Nieman K., Albrecht C., Peer W., Pickering I.J., Salt D.E. Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. The Plant Cell 2004, 16:2176-2191.
21. Grill D., Tausz M., De Kok L.J. In Significance of glutathione in plant adaptation to the environment. Handbook of Plant Ecophysiology 2001, vol. 2. Kluwer, Dordrecht.
22. Grill D., Tausz M., Strnad B., Wonisch A., Müller M., Raschi A. Thiols in acorns and feeding mites collected at sites with naturally elevated atmospheric sulphur concentrations. Sulfur Transport and Assimilation in Plants: Regulation, Interaction, Signaling 2003, 213-215. Backhuys, Leiden, The Netherlands. J.-C. Davidian, D. Grill, L.J. De Kok, I. Stulen, M.J. Hawkesford, E. Schnug, H. Rennenberg (Eds.).
23. Gullner G., Kömives T. The role of glutathione and glutathione-related enzymes in plant-pathogen interaction. Significance of Glutathione to Plant Adaptation to the Environment 2001, 207-239. Kluwer Academic Publishers, Dordrecht, Boston, London. D. Grill, M. Tausz, L.J. De Kok (Eds.).
24. Hayat Q., Hayat S., Irfan M., Ahmad A. Effect of exogenous salicylic acid under changing environment: a review. Environ. Exp. Bot. 2010, 68:14-25.
25. Hayat S., Ali B., Ahmad A. Salicylic acid: biosynthesis, metabolism and physiological role in plants. Salicylic Acid-A Plant Hormone 2007, 1-14. Springer Verlag, Dordrecht, Boston, London. S. Hayat, A. Ahmad (Eds.).
26. Hell R., Wirtz M. Metabolism of cysteine in plants and phototrophic bacteria. Advances in Photosynthesis and Respiration 2008, 417-435. Springer, Dordrecht. R. Hell, C. Dahl, D. Knaff, T. Leustek (Eds.).
27. Herbinger K., Then Ch., Löw M., Haberer K., Alexous M., Koch N., Remele K., Heerdt C., Grill D., Rennenberg H., Häberle K.H., Matyssek R., Tausz M., Wieser G. Tree age dependence and within-canopy variation of leaf gas exchange and antioxidative defence in Fagus sylvatica under experimental free-air ozone exposure. Environ. Pollut. 2005, 137:476-482.
28. Herschbach C., Rennenberg H. Significance of phloem-translocated organic sulphur compounds for the regulation of sulphur nutrition. Progr. Bot. 2001, 62:177-193.
29. Herschbach C., Rennenberg H. Sulfur nutrition of deciduous trees. Naturwissenschaften 2001, 88:25-36.
30. Hofer N., Alexou M., Heerdt C., Löw M., Werner H., Matyssek R., Rennenberg H., Haberer K. Seasonal differences and within-canopy variations of antioxidants in mature spruce (Picea abies) trees under elevated ozone in a free-air exposure system. Environ. Poll. 2008, 154:241-253.
31. Hudgins J.W., Franceschi V.R. 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. 2004, 135(4):2134-2149.
32. Jameson P.E., Clarke S.F. Hormone-virus interactions in plants. Crit. Rev. Plant Sci. 2002, 21:205-228.
33. Khan N.A., Syeed S., Masood A., Nazar R., Iqbal N. Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. Int. J. Plant Biol. 2010, 1:1-8.
34. Kawano T., Furuichi T., Muto S. Controlled salicylic acid levels and corresponding signaling mechanisms in plants. Plant Biotechnol. 2004, 21(5):319-335.
35. Kawano T., 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.
36. Kostner B., Schnupp R., Schulze E.D., Rennenberg H. Organic and inorganic sulfur transport in the xylem sap and the sulfur budget of Picea abies trees. Tree Physiol. 1998, 18:1-9.
37. Kozlowski G., Metraux J.-P. 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. 1998, 104:225-234.
38. Krekling T., Franceschi V.R., Berryman A.A., Christiansen E. The structure and development of polyphenolic parenchyma cells in Norway spruce (Picea abies) bark. Flora 2000, 195:354-369.
39. Larcher W. Physiological Plant Ecology 2003, Springer Verlag, Berlin.
40. 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(3):1586-1599.
41. Mattanovich J., Ehrenhöfer M., Schafellner C., Tausz M., Führer E. The role of sulphur compounds for breeding success of Ips typographus L. (Col., Scolytidae) on Norway Spruce (Picea abies [L.] Karst.). J. Appl. Ent. 2001, 125:425-431.
42. Maughan S., Foyer C.H. Engineering and genetic approaches to modulating the glutathione network in plants. Physiol. Plantarum 2006, 126:382-397.
43. Meyer A.J., Rausch T. Biosynthesis, compartmentation and cellular functions of glutathione in plant cells. Advances in Photosynthesis and Respiration 2008, 417-435. Springer, Dordrecht. R. Hell, C. Dahl, D. Knaff, T. Leustek (Eds.).
44. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trend. Plant Sci. 2002, 7(9):405-410.
45. Nagy N.E., Fossdal C.G., Krokene P., Krekling T., Lonneborg 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(5):505-515.
46. Noctor G. Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ. 2006, 29:409-425.
47. Noctor G., Foyer C.H. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49:249-279.
48. Noctor G., Gomez L., Vanacker H., Foyer C.H. Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and sigmalling. J. Exp. Bot. 2002, 53:1283-1304.
49. Ohashi Y., Murakami T., Mitsuhara I., Seo S. Rapid down and upward translocation of salicylic acid in tobacco plants. Plant Biotechnol. 2004, 21:95-101.
50. Pasqualini S., Della Torre G., Ferranti F., Ederli L., Piccioni C., Reale L., Antonielli M. Salicylic acid modulates ozone-induced hypersensitive cell death in tobacco plants. Physiol. Plantarum 2002, 115:204-212.
51. Percival G.C. Induction of systemic acquired disease resistance in plants: potential implications for disease management in urban forestry. J. Arboric. 2001, 27(4):181-192.
52. Pučko M., Grebenc T., Ribarič Lasnik C., Božič G., Konnert M., Kraigher H. Effects of biotic stress on seed quality and antioxidant content in Norway spruce trees from approved seed stands in Slovenia. Phyton-Ann. Rei Bot. 2005, 45(3):331-339.
53. Radwan D.E.M., Fayez K.A., Mahmound S.Y., Hamad A., Lu G. Physiological and metabolic changes of Cucurbita pepo leaves in response to zucchini yellow mosaic virus (ZYMV) infection and salicylic acid treatments. Plant Phys. Biochem. 2007, 45:480-489.
54. Rodrigues K.C.S., Fett-Neto A.G. 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.
55. Ross J.R., Nam K.H., John C., Auria D., Pichersky E. S-adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch. Biochem. Biophys. 1999, 367:9-16.
56. Schmidt A., Zeneli G., Hietala A.M., Fossdal C.G., Krokene P., Christiansen E., Gershenzon J. Induced chemical defences in conifers: biochemical and molecular approaches to studying their function. Chemical Ecology and Phytochemistry in Forest Ecosystems 2005, vol. 39:1-28. Elsevier, Amsterdam.
57. Shah J. The salicylic acid loop in plant defense. Curr. Opin. Plant Biol. 2003, 6:365-371.
58. Shi Q., Zhu Z. Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environ. Exp. Bot. 2008, 63:317-326.
59. Slaymaker D.H., Navarre D.A., Clark D., Del-Pozo O., Martin G.B., Klessig D.F. The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11640-11645.
60. Smirnoff N., Wheeler G.L. Ascorbic acid in plants: biosynthesis and function. Crit. Rev. Plant Sci. 2000, 19:267-290.
61. Struis R.P.W.J., Ludwig C., Barrelet T., Krähenbühl U., Rennenberg H. Studying sulfur functional groups in Norway spruce year rings using S L-edge total electron yield spectroscopy. Sci. Total Environ. 2008, 403:196-206.
62. Tausz M. Sulfur in forest ecosystems. Sulfur in Plants-An Ecological Perspective. Series: Plant Ecophysiology 2007, 59-75. Springer Verlag, Dordrecht, Boston, London. M.J. Hawkesford, L.J. De Kok (Eds.).
63. Tausz M., Wonisch A., Grill D., Morales D., Jimenez M.S. Measuring antioxidants in tree species in the natural environment: from sampling to data evaluation. J. Exp. Bot. 2003, 54(387):1505-1510.
64. Tausz M., Wonisch A., Peters J., Jimenez M.S., Morales D., Grill D. Short-term changes in free-radical scavengers and chloroplast pigments in Pinus canariensis needles as affected by mild drought stress. J. Plant Physiol. 2001, 158:213-219.
65. Tausz M., Šircelj H., Grill D. The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid?. J. Exp. Bot. 2004, 55(404):1955-1962.
66. Tausz M., Löffler S., Posch S., Monschein S., Grill D., Kätzel R. Do photoprotective pigments and antioxidants in needles of Pinus sylvestris relate to high N or water availability at field plots in a dry year?. Phyton Ann. Rei Bot. 2005, 45:107-116.
67. Urbanek Krajnc A., Zechmann B., Stabentheiner E., Müller M. Artificial elevation of salicylic acid affects thiol contents in symptom development in Cucurbita pepo during Zucchini yellow mosaic virus (ZYMV) infection. Phyton 2008, 48:13-35.
68. Urbanek Krajnc A. A temporal analysis of antioxidative defense response in the phloem of Picea abies after attack by Ips typographus. Tree Physiol. 2009, 29:1059-1068.
69. Vallad G.E., Goodman R.M. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci. 2004, 44:1920-1934.
70. Verberne M.C., Brouwer N., Delbianco F., Linthorst H.J.M., Bol J.F., Verpoorte R. Method for the extraction of the volatile compound salicylic acid from tobacco leaf material. Phytochem. Anal. 2002, 13:45-50.
71. 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.
72. 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.
73. Zhao F.-J., Tausz M., De Kok L.J. Role of sulfur for plant production in agricultural and natural ecosystems. Advances in Photosynthesis and Respiration 2008, 417-435. Springer, Dordrecht. R. Hell, C. Dahl, D. Knaff, T. Leustek (Eds.).