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Effects of Fertilization and Fungal and Insect Attack on Systemic Protein Defenses of Austrian Pine

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Abstract

Despite their economic and ecological importance, defense responses of conifers to pests are little understood. In a 3-year experiment, we monitored systemic fungal (Diplodia pinea)- and insect (Neodiprion sertifer)-induced defense protein activities and total soluble proteins in needles and phloem of Austrian pine (Pinus nigra) across a soil fertility gradient. In both years, total soluble protein content of foliage and phloem declined with increasing fertility across induction treatments, while defensive protein activities generally increased with increasing fertility. In 2005, total soluble protein content in branch phloem was increased by fungal inoculation of the stem. Peroxidase activity was suppressed in needles by insect defoliation in 2006, while polyphenol oxidase activity was systemically induced in branch phloem by insect attack in 2005. Trypsin inhibitor activities in phloem did not respond to any induction or fertility treatment. Nutritive quality of Austrian pine tissue declined with increasing fertility, while several protein-based defenses simultaneously increased.

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References

  • Abeles, F. B., and Forrence, L. E. 1970. Temporal and hormonal control of β-1.3-glucanase in Phaseolus vulgaris L. Plant Physiol. 45:395–400.

    PubMed  CAS  Google Scholar 

  • Blodgett, J. T., Herms, D. A., and Bonello, P. 2005. Effects of fertilization on red pine defense chemistry and resistance to Sphaeropsis sapinea. For. Ecol. Manag. 208:373–382.

    Article  Google Scholar 

  • Bolter, C. J., Latoszek-green, M., and Tenuta, M. 1998. Dependence of methyl jasmonate- and wound-induced cysteine proteinase inhibitor activity on nitrogen concentration. J. Plant Physiol. 152:427–432.

    CAS  Google Scholar 

  • Bonello, P., and Blodgett, J. T. 2003. Pinus nigraSphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol. Mol. Plant Pathol. 63:249–261.

    Article  Google Scholar 

  • Borowicz, V. A., Albrecht, U., and Mayer, R. T. 2003. Effects of nutrient supply on Citrus resistance to root herbivory by Diaprepes abbreviatus L. (Coleoptera: Curculionidae). Environ. Entomol. 32:1242–1250.

    Google Scholar 

  • Cipollini, D. F. 2002. Does competition magnify the fitness costs of induced responses in Arabidopsis thaliana? A manipulative approach. Oecologia 131:514–520.

    Article  Google Scholar 

  • Cipollini, D. F., and Bergelson, J. 2001. Plant density and nutrient availability constrain constitutive and wound-induced expression of trypsin inhibitors in Brassica napus. J. Chem. Ecol. 27:593–610.

    Article  PubMed  CAS  Google Scholar 

  • Cipollini, D. F., Enright, S., Traw, M. B., and Bergelson, J. 2004. Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol. Ecol. 13:1643–1653.

    Article  PubMed  CAS  Google Scholar 

  • Eyles, A., Chorbadjian, R., Wallis, C., Hansen, R., Cipollini, D., Herms, D., and Bonello, P. 2007. Cross-induction of systemic induced resistance between an insect and a fungal pathogen in Austrian pine over a fertility gradient. Oecologia 153:365–374.

    Article  PubMed  Google Scholar 

  • Franceschi, V. R., Krokene, P., Christiansen, E., and Krekling, T. 2005. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 167:353–376.

    Article  PubMed  CAS  Google Scholar 

  • Haruta, M., Pedersen, J. A., and Constabel, C. P. 2001. Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol. Plant. 112:552–558.

    Article  PubMed  CAS  Google Scholar 

  • Hodge, A., Alexander, I. J., and Gooday, G. W. 1995. Chitinolytic activities of Eucalyptus pilularis and Pinus sylvestris roots systems challenged with mycorrhizal and pathogenic fungi. New Phytol. 131:255–261.

    Article  CAS  Google Scholar 

  • Inbar, M., Doostdar, H., and Mayer, R. T. 2001. Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94:228–235.

    Article  Google Scholar 

  • Inbar, M., Doostdar, H., S, onoda, R. M., Leibee, G. L., and Mayer, R. T. 1998. Elicitors of plant defensive systems reduce insect densities and disease incidence. J. Chem. Ecol. 24:135–149.

    Article  CAS  Google Scholar 

  • Johansson, S. M., Lundgren, L. N., and Asiegbu, F. O. 2004. Initial reactions in sapwood of Norway spruce and Scots pine after wounding and infection by Heterobasidion parviporum and H. annosum. For. Pathol. 34:197–210.

    Google Scholar 

  • Jøhnk, N., Hietala, A. M., Fossdal, C. G., Collinge, D. B., and Newman, M.-A. 2005. Defense-related genes expressed in Norway spruce roots after infection with the root rot pathogen Ceratobasidium bicorne (anamorph: Rhizoctonia sp.). Tree Physiol. 25:1533–1543.

    PubMed  Google Scholar 

  • Karban, R., Adamchak, R., and Schnathorst, W. A. 1987. Induced resistance and interspecific competition between spider mites and a vascular wilt fungus. Science 234:678–680.

    Article  Google Scholar 

  • Larsson, S., Ekbom, B., and Björkman, C. 2000. Influence of plant quality on pine sawfly population dynamics. Oikos 89:440–450.

    Article  Google Scholar 

  • Lippert, D., Chowrira, S., Ralph, S. G., Zhuang, J., Aeschliman, D., Ritland, C., Ritland, K., and Bohlmann, J. 2007. Conifer defense against insects: proteome analysis of Sitka spruce (Picea sitchensis) bark induced by mechanical wounding or feeding by white pine weevils (Pissodes strobii). Proteomics 7:248–270.

    Article  PubMed  CAS  Google Scholar 

  • Liu, J.-J., Ekramoddoullah, A. K. M., and Yu, X. 2003. Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol. Plant. 119:544–553.

    Article  CAS  Google Scholar 

  • Liu, J.-J., Ekramoddoullah, A. K. M., and Zamani, A. 2005. A class IV chitinase is up-regulated by fungal infection and abiotic stresses and associated with slow-canker-growth resistance to Cronartium ribicola in Western White Pine (Pinus monticola). Phytopathology 95:284–291.

    Article  PubMed  CAS  Google Scholar 

  • Major, I. T., and Constabel, C. P. 2008. Functional analysis of the Kunitz trypsin inhibitor family in poplar reveals biochemical diversity and multiplicity in defense against herbivores. Plant Physiol. 146:888–903.

    Article  PubMed  CAS  Google Scholar 

  • Mcintyre, J. L., Dodds, J. A., and Hare, J. D. 1981. Effects of localized infections of Nicotiana tabacum by tobacco mosaic virus on systemic resistance against diverse pathogens and an insect. Phytopathology 71:297–301.

    Article  Google Scholar 

  • Musser, R. O., Cipollini, D. F., Hum-Musser, S. M., Williams, S. A., Brown, J. K., and Felton, G. W. 2005. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Arch. Insect Biochem. Physiol. 58:128–137.

    Article  PubMed  CAS  Google Scholar 

  • Peterson, G. W. 1977. Infection, epidemiology, and control of Diplodia blight of Austrian, ponderosa, and Scots pine. Phytopathology 67:511–514.

    Article  Google Scholar 

  • Pirttilä, A. M., Laukkanen, H., and Hohtola, A. 2002. Chitinase production in pine callus (Pinus sylvestris L.): a defense reaction against endophytes? Planta 214:848–852.

    Article  PubMed  CAS  Google Scholar 

  • Ralph, S. G., Jancsik, S., and Bohlmann, J. 2007. Dirigent proteins in conifer defense II: extended discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry 68:1975–1991.

    Article  PubMed  CAS  Google Scholar 

  • Ralph, S. G., Yueh, H., Friedmann, M., Aeschliman, D., Zeznik, J. A., Nelson, C. C., Butterfield, Y. S. N., Kirkpatrick, R., Liu, J., Jones, S. J. M., Marra, M. A., Douglas, C. J., Ritland, K., and Bohlmann, J. 2006. Conifer defense 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 

  • Richard, S., Lapointe, G., Rutledge, R. G., and Séguin, A. 2000. Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol. 41:982–987.

    Article  PubMed  CAS  Google Scholar 

  • Stanosz, G. R., Trobaugh, J., Guthmiller, M. A., and Stanosz, J. C. 2004. Sphaeropsis shoot blight and altered nutrition in red pine plantations treated with paper mill waste sludge. For. Pathol. 34:245–253.

    Google Scholar 

  • Vollmann, J., Grawusgruber, H., Wagentristl, H., Wohleser, H., and Michele, P. 2003. Trypsin inhibitor activity of soybean as affected by genotype and fertilisation. J. Sci. Food Agric. 83:1581–1586.

    Article  CAS  Google Scholar 

  • Wallis, C., Eyles, A., Chorbadjian, R., Mcspadden Gardener, B., Hansen, R., Cipollini, D., Herms, D. A., and Bonello, P. 2008. Systemic induction of phloem secondary metabolism and its relationship to resistance to a canker pathogen in Austrian pine. New Phytol. 177:767–789.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Eusondia Arnett, Bryant Chambers, Alejandro Chiriboga, Ilka Gomez, Diane Hartzler, Anuprit Kaur, Cherissa Rainey, Matt Solensky, Duan Wang, and Justin Whitehill for the assistance in the field and in the laboratory and Kurtz Bros for the nursery supplies. The comments by two anonymous reviewers improved the manuscript. Funding was provided by the USDA National Research Initiative Competitive Grants Program No. 2004-35302-14667 and by the State and Federal funds appropriated to the Ohio Agricultural Research and Development Center, the Ohio State University. These experiments comply with the laws of the USA.

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Correspondence to Don Cipollini.

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Barto, K., Enright, S., Eyles, A. et al. Effects of Fertilization and Fungal and Insect Attack on Systemic Protein Defenses of Austrian Pine. J Chem Ecol 34, 1392–1400 (2008). https://doi.org/10.1007/s10886-008-9550-z

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  • DOI: https://doi.org/10.1007/s10886-008-9550-z

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