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Distinguishing Defensive Characteristics in the Phloem of Ash Species Resistant and Susceptible to Emerald Ash Borer

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Abstract

We examined the extent to which three Fraxinus cultivars and a wild population that vary in their resistance to Emerald Ash Borer (EAB) could be differentiated on the basis of a suite of constitutive chemical defense traits in phloem extracts. The EAB-resistant Manchurian ash (F. mandshurica, cv. Mancana) was characterized by having a rapid rate of wound browning, a high soluble protein concentration, low trypsin inhibitor activities, and intermediate levels of peroxidase activity and total soluble phenolic concentration. The EAB-susceptible white ash (F. americana, cv. Autumn Purple) was characterized by a slow wound browning rate and low levels of peroxidase activity and total soluble phenolic concentrations. An EAB-susceptible green ash cultivar (F. pennsylvanica, cv. Patmore) and a wild accession were similar to each other on the basis of several chemical defense traits, and were characterized by high activities of peroxidase and trypsin inhibitor, a high total soluble phenolic concentration, and an intermediate rate of wound browning. Lignin concentration and polyphenol oxidase activities did not differentiate resistant and susceptible species. Of 33 phenolic compounds separated by HPLC and meeting a minimum criterion for analysis, nine were unique to Manchurian ash, five were shared among all species, and four were found in North American ashes and not in the Manchurian ash. Principal components analysis revealed clear separations between Manchurian, white, and green ashes on the basis of all phenolics, as well as clear separations on the basis of quantities of phenolics that all species shared. Variation in some of these constitutive chemical defense traits may contribute to variation in resistance to EAB in these species.

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References

  • Appel, H.M. 1993. Phenolics in ecological interactions: the importance of oxidation. J. Chem. Ecol. 19:1521Y1552.

    Article  Google Scholar 

  • Bonello, P. and Pearce, R. 1993. Biochemical defense responses in primary roots of Scots pine challenged in vitro with Cylindrocarpon destructans. Plant Pathol. 42:203Y211.

    Article  Google Scholar 

  • Bonello, P., Heller, W., and Sanderman, H.J. 1993. Ozone effects on root-disease susceptibility and defence responses in mycorrhizal and non-mycorrhizal seedlings of Scots pine (Pinus sylvestris L.). New Phytol. 124:653Y663.

    Article  Google Scholar 

  • Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248Y254.

    Article  Google Scholar 

  • Buschmann, H., Rodriguez, M.X., Tohme, J., and Beeching, J.R. 2000. Accumulation of hydroxycoumarins during post-harvest deterioration of tuberous roots of cassava (Manihot esculenta Crantz). Ann. Bot. 86:1153Y1160.

    Article  Google Scholar 

  • Cabral, M.M.O., Kelecom, A., and Garcia, E.S. 1999. Effects of the lignan, pinoresinol on the moulting cycle of the bloodsucking bug Rhodnius prolixus and of the milkweed bug Oncopeltus fasciatus. Fitoterapia 70:561Y567.

    Article  Google Scholar 

  • Cipollini, D.F. and Redman, A.M. 1999. Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J. Chem. Ecol. 25:271Y281.

    Google Scholar 

  • Cipollini, D.F., Enright, S., Traw, B., and Bergelson, J. 2004. Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol. Ecol. 13:1643Y1653.

    Article  Google Scholar 

  • Cis, J., Nowak, G., and Kisiel, W. 2006. Antifeedant properties and chemotaxonomic implications of sesquiterpene lactones and syringin from Rhaponticum pulchrum. Biochem. Syst. Ecol. 34:862Y867.

    Article  Google Scholar 

  • Chen, Y, Whitehill, J.G.A., Bonello, P., and Poland, T.M. 2011. Differential response in foliar chemistry of three ash species to Emerald Ash Borer adult feeding. J. Chem. Ecol. 37:29Y39.

    Article  Google Scholar 

  • Cheng, G.W. and Crisosto, C. 1995. Browning potential, phenolic composition, and polyphenoloxidase activity of buffer extracts of peach and nectarine skin tissue. J. Amer. Soc. Hort. Sci. 120:835Y838.

    Google Scholar 

  • Dehon, L., Macheix, J.J., and Durand, M. Involvement of peroxidases in the formation of the brown coloration of heartwood in Juglans nigra. J.Exp. Bot.53:303Y311.

    Article  Google Scholar 

  • Deiana, M., Incani, A., Corona, G., Atzeri, A., Loru, D., Melis, M.P., and Dessi, M. 2008. Protective effect of hydroxytyrosol and its metabolite homovanillic alcohol on H2O2 induced lipid peroxidation in renal tubular epithelial cells. Food Chem.Toxicol. 46: 2984–2990.

    Article  PubMed  CAS  Google Scholar 

  • Doledec, S. and Chessel, D. 1987. Rythmes saisonniers et composantes stationnelles en milieu aquatique I—Description d'un plan d'observations complet par projection de variables. Acta Oecol., Oecol. Generalis 8:403Y426.

    Google Scholar 

  • Dowd, P. F. and Norton, R.A. 1995. Browning-associated mechanisms of resistance to insects in corn callus tissue. J. Chem. Ecol. 5:583Y600.

    Google Scholar 

  • Dray, S. and Dufour, A.B. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22:1Y20

    Google Scholar 

  • Dunn, J.P., Potter, D.A., and Kimmerer, T.W. 1990. Carbohydrate reserves, radial growth, and mechanisms of resistance of oak trees to phloem boring insects. Oecologia 83:458Y468.

    Article  Google Scholar 

  • Eyles, A., William, J., Riedl, K., Cipollini, D., Schwartz, S., Chan, K., Herms, D.A., and Bonello, P. 2007. Comparative phloem chemistry of Manchurian (Fraxinus mandshurica) and Two North American Ash species (Fraxinus americana and Fraxinus pennsylvanica). J. Chem. Ecol. 33:1430Y1448.

    Article  Google Scholar 

  • Felton, G.W., Donato, K., Delvecchio, R.J., and Duffey, S. 1989. Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15:2667Y2694.

    Article  Google Scholar 

  • Garcia, E.S., Cabral, M.M.O., Schaub, G.A., Gottlieb, O.R., and Azambuja, P. 2000. Effects of lignoids on a hematophagous bug, Rhodnius prolixus: feeding, ecdysis, and dieresis. Phytochemistry 55:611Y616.

    Article  Google Scholar 

  • Gould, J., Tanner, J. Winograd, T.D., and Lane, S. 2005. Initial studies on the laboratory rearing of emerald ash borer and foreign exploration for natural enemies, pp. 73Y74, in V. Mastro and R. Reardon (eds.). Emerald Ash Borer Research and Technology Development Meeting. U.S. Department of Agriculture, Forest Service, Morgantown, West Virginia.

    Google Scholar 

  • Kehr, J. 2006. Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J. Exp. Bot. 57:767Y774.

    Article  Google Scholar 

  • Levin, D. 1976. The chemical defenses of plants to pathogens and herbivores. Annu. Rev. Ecol. Syst. 7:121Y159.

    Google Scholar 

  • Liu, H.P., Bauer, L.S., Miller, D.L., Zhao, T.H., Gao, R.T., Song, L.W., Luan, Q.S., Jin, R.Z., and Gao, C.Q. 2007. Seasonal abundance of Agrilus planipennis (Coleoptera: Buprestidae) and its natural enemies Oobius agrili (Hymenoptera: Encyrtidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae) in China. Biol. Control. 42:61Y71.

    Google Scholar 

  • Mittapalli, O., Bai, X. Mamidala, P., Rajarapu, S.P., Bonello, P., and Herms, D.A. 2010. Tissue-tissue specific transcriptomics of the exotic invasive insect pest, emerald ash borer (Agrilus planipennis). PLoS ONE 5: e13708 doi:10.1371/journal.pone.0013708.

    Article  PubMed  Google Scholar 

  • Poland, T.M. and Mccullough, D.G. 2006. Emerald ash borer: Invasion of the urban forest and the threat to North America’s ash resource. J. Forest. 104:118Y124.

    Google Scholar 

  • Pureswaran, D.S. and Poland, T.M. 2009. Host selection and feeding preference of Agrilus planipennis (Coleoptera: Buprestidae) on ash (Fraxinus spp.). Environ. Entomol. 38:757Y765.

    Article  Google Scholar 

  • R Development Core Team. 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  • Rebek, E.J., Herms, D.A., and Smitley, D.R. 2008. Interspecific variation in resistance to Emerald Ash Borer (Coleoptera: Buprestidae) among North American and Asian ash (Fraxinus spp.). Environ. Entomol. 37:242Y246.

    Article  Google Scholar 

  • Rios, J.L., Giner, R.M., and Prieto, J.M. 2002. New findings on the bioactivity of lignans. Stud. Nat. Prod. Chem. 26:183Y292.

    Google Scholar 

  • Rodriguez, M.X., Buschmann, H., Iglesias, C., and Beeching, J.R. 2000. Production of antimicrobial compounds in cassava (Manihot esculenta Crantz) roots during post-harvest physiological deterioration, pp320Y328, in L.J.C.B. Carvalho, A.M. Thro, A.D. Vilarinhos, (eds.). Cassava Biotechnology. IVth International Scientific Meeting Cassava Biotechnology Network. Embrapa, Brasilia.

    Google Scholar 

  • Schroeder, F.C., Del Campo, M.L., Grant, J.B., Weibel, D.B., Smedley, S.R., Bolton, K.L., Meinwald, J., and Eisner, T.S. 2006. Pinoresinol: a lignol of plant origin serving for defense in a caterpillar. Proc. Natl. Acad. Sci, USA. 103:15497Y15501.

    Google Scholar 

  • Silva, M.C.P., Terra, W.R., and Ferreia, C. 2006. Absorption of toxic beta-glucosides produced by plants and their effect on tissue trehalases from insects. Comp. Biochem. Physiol. B 143:367Y373.

    Article  Google Scholar 

  • Wainhouse, D., Cross, D.J., and Howell, R.S. 1990. The role of lignin as a defence against the spruce bark beetle Dendroctonus micans: Effect on larvae and adults. Oecologia 85:257Y265.

    Article  Google Scholar 

  • Wainhouse, D., Ashburner, R., Ward, E. and Boswell, R. 1998. The effect of lignin and bark wounding on susceptibility of spruce trees to Dendroctonus micans. J. Chem. Ecol. 24:1551Y1561.

    Article  Google Scholar 

  • Wallander, E. 2008. Systematics of Fraxinus (Oleaceae) and evolution of dioecy. Plant Syst. Evol. 273:25Y49.

    Article  Google Scholar 

Download references

Acknowledgements

This research was funded by the Ohio Plant Biotechnology Consortium, the USDA APHIS Accelerated Emerald Ash Borer Research Initiative, state and federal funds appropriated to The Ohio State University and Ohio Agricultural Research and Development Center, and Wright State University. We thank Bailey’s Nursery, Inc. of St. Paul, MN, USA and Jennifer Koch, USDA Forest Service, Northern Research Station, Delaware, OH, USA for donating the ash trees used in the study. We thank Deah Lieurance for technical assistance.

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Correspondence to Don Cipollini.

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Cipollini, D., Wang, Q., Whitehill, J.G.A. et al. Distinguishing Defensive Characteristics in the Phloem of Ash Species Resistant and Susceptible to Emerald Ash Borer. J Chem Ecol 37, 450–459 (2011). https://doi.org/10.1007/s10886-011-9954-z

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  • DOI: https://doi.org/10.1007/s10886-011-9954-z

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