Abstract
This study characterized the chemical response of healthy red pine to artificial inoculation with the bark beetle-vectored fungusLeptographium terebrantis. In addition, we sought to determine whether stress altered this induced response and to understand the implications of these interactions to the study of decline diseases. Twenty-five-year-old trees responded to mechanical wounding or inoculation withL. terebrantis by producing resinous reaction lesions in the phloem. Aseptically wounded and wound-inoculated phloem contained higher concentrations of phenolics than did constitutive tissue. Trees inoculated withL. terebrantis also contained higher concentrations of six monoterpenes,α-pinene,β-pinene, 3-carene, limonene, camphene, and myrcene, and higher total monoterpenes than did trees that were mechanically wounded or left unwounded. Concentrations of these monoterpenes increased with time after inoculation. Total phenolic concentrations in unwounded stem tissue did not differ between healthy and root-diseased trees. Likewise, constitutive monoterpene concentrations in stem phloem were similar between healthy and root-diseased trees. However, when stem phloem tissue was challenged with fungal inoculations, reaction tissue from root-diseased trees contained lower concentrations ofα-pinene, the predominant monoterpene in red pine, than did reaction tissue from healthy trees. Seedlings stressed by exposure to low light levels exhibited less extensive induced chemical changes when challenge inoculated withL. terebrantis than did seedlings growing under higher light. Stem phloem tissue in these seedlings contained lower concentrations ofα-pinene than did nonstressed seedlings also challenge inoculated withL. terebrantis. It is hypothesized that monoterpenes and phenolics play a role in the defensive response of red pine against insect-fungal attack, that stress may predispose red pine to attack by insect-fungal complexes, and that such interactions are involved in red pine decline disease. Implications to plant defense theory and interactions among multiple stress agents in forest decline are discussed.
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References
Abacus Concepts. 1989. SuperANOVA. Abacus Concepts, Inc., Berkeley, California.
Bordasch, R.P., andBerryman, A.A. 1977. Host resistance to the fir engraver beetle,Scolytus ventralis (Coleoptera: Scolytidae) 2. Repellancy ofAbies grandis resins and some monoterpenes.Can. Entomol. 109:95–100.
Bridges, J.R. 1987. Effects of terpenoid compounds on growth of symbiotic fungi associated with the southern pine beetle.Phytopathology 77:83–85.
Cates, R.G., andAlexander, H. 1982. Host resistance and susceptibility, pp. 212–263,in J.B. Mitton and K.B. Sturgeon (eds.). Bark Beetles in North American Conifers. A.P.S. Press, St. Paul, Minnesota.
Christensen, E., andEricsson, A. 1986. Starch reserves inPicea abies in relation to defense reaction against a bark beetle transmitted blue-stain fungus,Ceratocystis polonica.Can. J. For. Res. 16:78–83.
Cobb, F.W., Jr., Krstic, M., Zavarin, E., andBarber, H.W., Jr. 1968. Inhibitory effects of volatile oleoresin components onFomes annosus and fourCeratocystis species.Phytopathology 58:1327–1335.
Cook, S.P., andHain, F.P. 1986. Defensive mechanisms of loblolly and shortleaf pine against attack by sourthern pine beetle,Dendroctonus frontalis Zimmerman (Coleoptera: Scolytidae) and its fungal associate,Ceratocystis minor (Hedgecock) Hunt.J. Chem. Ecol. 12:1397–1406.
Coyne, J.F., andLott, L.H. 1976. Toxicity of substances in pine oleoresin to southern pine beetles.J. Ga. Entomol. Soc. 11:301–305.
DeGroot, R.C. 1972. Growth of wood-inhabiting fungi in saturated atmospheres of monoterpenoids.Mycologia 64:863–870.
Delorme, L., andLieutier, F. 1990. Monoterpene composition of the preformed and induced resins of Scots pine, and their effect on bark beetles and associated fungi.Eur. J. For. Pathol. 20:304–316.
Entry, J.A., Cromack, K., Jr., Hansen, E., andWaring, R. 1991. Response of western coniferous seedlings to infection byArmillaria ostoyae under limited light and nitrogen.Phytopathology 81:89–94.
Gershenzon, J. 1994. Metabolic costs of terpenoid accumulation in higher plants.J. Chem. Ecol. 20:1281–1328.
Gijzen, M. Lewinsohn, E., andCroteau, R. 1991. Characterization of the constitutive and wound-inducible monoterpene cyclases.Arch. Biochem. Biophys. 289:267–273.
Jorgenson, E. 1961. The formation of pinosylvin and its monomethyl ether in the sapwood ofPinus resinosa Ait.Can. J. Bot. 39:1765–1772.
Julkunen-Tijto, R. 1985. Phenolic constituents in the leaves of northern willows: Methods for the analysis of certain phenolics.J. Agric. Food Chem. 33:213–217.
Kelsey, R.G., andHarmon, M.E. 1989. Distribution and variation of extractable total phenols and tannins in the logs of four conifers after 1 year on the ground.Can. J. For. Res. 19:1030–1036.
Klein, R.M., andPerkins, T.D. 1988. Primary and secondary causes and consequences of contemporary forest decline.Bot. Rev. 54:1–43.
Klepzig, K.D. 1994. Interactions of stress, plant chemical defenses and subcortical insect-fungal complexes in red pine decline. PhD dissertation. University of Wisconsin-Madison. 246 pp.
Klepzig, K.D., Raffa, K.F., andSmalley, E.B. 1991. Association of an insect-fungal complex with red pine decline in Wisconsin.For. Sci. 37:1119–1139.
Lewinsohn, E., Gijzen, M., Savage, T.J., andCroteau, R. 1991a. Defense mechanisms of conifers: Relationships of monoterpene cyclase activity to anatomical specialization and oleoresin monoterpene content.Plant Physiol. 96:38–43.
Lewinsohn, E., Guzen, M., andCroteau, R. 1991b. Defense mechanisms of conifers: Differences in constitutive and wound-induced monoterpene biosynthesis among species.Plant Physiol. 96:44–49.
Lerdau, M., Litvak, M., andMonson, R. 1994. Plant chemical defense: Monoterpenes and the growth-differentiation balance hypothesis.Tree 9:58–61.
Lieutier, F. 1993. Induced defense reaction of conifers to bark beetles and their associated Ophiostoma species, pp. 225–233,in M.J. Wingfield, K.A. Seifert, and J.F. Webber (eds.).Ceratocystis andOphiostoma: Taxonomy, Ecology, and Pathogenicity. A.P.S. Press, St. Paul, Minnesota.
Lorio, P.L. 1986. Growth-differentiation balance: A basis for understanding southern pine beetle-tree interactions.For. Ecol. Manage. 14:259–273.
Lorio, P.L., andHodges, J.D. 1968. Microsite effects on oleoresin pressure of large loblolly pines.Ecology 49:1207–1210.
Manion, P.D. 1991. Tree Disease Concepts, 2nd ed. Prentice-Hall, Englewood Cliffs, New Jersey, 402 p.
Nebeker, T.E., Hodges, J.D., andBlanche, C.A. 1993. Host response to bark beetle and pathogen colonization, pp. 225–233,in T.D. Schowalter, and G.M. Filip (eds.). Beetle-Pathogen Interactions in Conifer Forests. Academic Press, New York.
Nevill, R.J., andAlexander, S.A. 1992. Transmission ofLeptographium procerum to eastern white pine byHylobius pales andPissodes nemorensis (Coleoptera: Curculionidae).Plant Dis. 76:307–310.
Oren, R., Schulze, E.-D. Werk, K.S., Meyer, J., Schneider, B.V., andHilmeis, H. 1988. Performance of twoPicea abies (L.) Karst. stands at different stages of decline: I. Carbon relations and stand growth.Oecologia 75:25–37.
Paine, T.D., andStephen, F.M. 1987. Influence of tree stresses and site quality on the induced defensive system of loblolly pine.Can. J. For. Res. 17:569–571.
Paine, T.D., Blanche, C.A., Nebeker, T.E., andStephen, F.M. 1987. Composition of loblolly pine resin defenses: Comparison of monoterpenes from induced lesion and sapwood resin.Can. J. For. Res. 17:1202–1206.
Raffa, K.F., andBerryman, A.A. 1982. Accumulation of monoterpenes and associated volatiles following fungal inoculation of grand fir with a fungus vectored by the fir engraverScolytus ventralis (Coleoptera: Scolytidae).Can. Entomol. 114:797–810.
Raffa, K.F., andBerryman, A.A. 1983. Physiological aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle,Dendroctonus ponderosae (Coleoptera: Scolytidae).Can. Entomol. 115:723–734.
Raffa, K.F., andHall, D.J. 1988. Seasonal activities of the pine root collar weevil,Hylobius radicis Buchanan (Coleoptera: Curculionidae), in red pine stands undergoing decline.Great Lakes Entomol. 21:69–74.
Raffa, K.R., andKlepzig, K.D. 1995. Effects of root inhabiting insect-fungal complexes on aspects of host resistance to bark beetles,in W. Mattson and P. Niemela (eds.). Mechanisms of Woody Plant Defenses against Herbivores. USDA Forest Service, Gen. Tech. Rep. NC-, North Central Experiment Station. St. Paul, Minnesota.
Raffa, K. R., andSmalley, E.B. 1995. Interaction of pre-attack and induced monoterpenes in conifer defense against bark beetle-fungal complexes.Oecologia. In press.
Raffa K.F., andSteffeck, R.J. 1988. Computation of response factors for quantitative analysis of monoterpenes by gas-liquid chromatography.J. Chem. Ecol. 14:1385–1390.
Raffa, K.F., Berryman, A.A., Simasko, J., Teal, W., andWong, B.L. 1985. Effects of grand fir monoterpenes on the fir engraver,Scolytus ventralis (Coleoptera: Scolytidae), and its symbiotic fungus.Environ. Entomol. 14:552–556.
Russell, C.E., andBerryman, A.A. 1976. Host resistance to the fir engraver beetle. 1. Monoterpene composition ofAbies grandis pitch blisters and fungus-infected wounds.Can. J. Bot. 54:14–18.
Shain, L. 1967. Resistance of sapwood in stems of loblolly pine to infection byFomes annosus.Phytopathology 57:1034–1045.
Shrimpton, D.M., andWhitney, H.S. 1968. Inhibition of growth of blue stain fungi by wood extractives.Can. J. Bot. 46:757–761.
Smith, R.H. 1963. Toxicity of pine resin vapors to three species ofDendroctonus bark beetles.J. Econ. Entomol. 56:827–831.
Werner, R.A., andIllman, B.L. 1994. Response of Lutz, Sitka, and white spruce to attack byDendroctonus rufipennis (Coleoptera: Scolytidae) and blue stain fungi.Environ. Entomol. 23:472–478.
Wright, E. 1933. A cork-borer method for inoculating trees.Phytopathology, 23:487–488.
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Klepzig, K.D., Kruger, E.L., Smalley, E.B. et al. Effects of biotic and abiotic stress on induced accumulation of terpenes and phenolics in red pines inoculated with bark beetle-vectored fungus. J Chem Ecol 21, 601–626 (1995). https://doi.org/10.1007/BF02033704
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DOI: https://doi.org/10.1007/BF02033704