Interspecific Comparison of Constitutive Ash Phloem Phenolic Chemistry Reveals Compounds Unique to Manchurian Ash, a Species Resistant to Emerald Ash Borer

Abstract

The emerald ash borer (Agrilus planipennis, EAB) is an invasive wood-borer indigenous to Asia and is responsible for widespread ash (Fraxinus spp.) mortality in the U.S. and Canada. Resistance and susceptibility to EAB varies among Fraxinus spp., which is a result of their co-evolutionary history with the pest. We characterized constitutive phenolic profiles and lignin levels in the phloem of green, white, black, blue, European, and Manchurian ash. Phloem was sampled twice during the growing season, coinciding with phenology of early and late instar EAB. We identified 66 metabolites that displayed a pattern of variation, which corresponded strongly with phylogeny. Previously identified lignans and lignan derivatives were confirmed to be unique to Manchurian ash, and may contribute to its high level of resistance to EAB. Other compounds that had been considered unique to Manchurian ash, including hydroxycoumarins and the phenylethanoids calceolarioside A and B, were detected in closely related, but susceptible species, and thus are unlikely to contribute to EAB resistance of Manchurian ash. The distinct phenolic profile of blue ash may contribute to its relatively high resistance to EAB.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Agrawal, A. A. 2011. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25:420–432.

    Article  Google Scholar 

  2. Anulewicz, A. C., McCullough, D. G., and Cappaert, D. L. 2007. Emerald ash borer (Agrilus planipennis) density and canopy dieback in three North American ash species. Arboricult. Urban For. 33:338–349.

    Google Scholar 

  3. Baranchikov, Y., Mozolevskaya, E., Yurchenko, G., and Kenis, M. 2008. Occurrence of the emerald ash borer, Agrilus planipennis in Russia and its potential impact on European forestry. EPPO Bull. 38:233–238.

    Article  Google Scholar 

  4. Bonello, P. and Blodgett, J. T. 2003. Pinus nigra-Sphaeropsis 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 

  5. Borg-Karlson, A. K., Nordlander, G., Mudalige, A., Nordenhem, H., and Unelius, C. R. 2006. Antifeedants in the feces of the pine weevil Hylobius abietis: Identification and biological activity. J. Chem. Ecol. 32:943–957.

    PubMed  Article  CAS  Google Scholar 

  6. Cabral, M. M. O., Azambuja, P., Gottlieb, O. R., and Garcia, E. S. 2000. Effects of some lignans and neolignans on the development and excretion of Rhodnius prolixus. Fitoterapia 71:1–9.

    PubMed  Article  CAS  Google Scholar 

  7. Cappaert, D., McCullough, D. G., Poland, T. M., and Siegert, N. 2005. Emerald ash borer in North America: a research and regulatory challenge. Am. Entomol. 51:152–165.

    Google Scholar 

  8. Cardoso, S. M., Guyot, S., Marnet, N., Lopes-Da-Silva, J. A., Renard, C. M. G. C., and Coimbra, M. A. 2005. Characterisation of phenolic extracts from olive pulp and olive pomace by electrospray mass spectrometry. J. Sci. Food Agric. 85:21–32.

    Article  CAS  Google Scholar 

  9. Cipollini, D., Wang, Q., Whitehill, J. G. A., Powell, J., Bonello, P., and Herms, D. 2011. Distinguishing defensive characteristics in the phloem of ash species resistant and susceptible to emerald ash borer. J. Chem. Ecol. 37:450–459.

    PubMed  Article  CAS  Google Scholar 

  10. Coley, P. D. 1986. Costs and benefits of defense by tannins in a neotropical tree. Oecologia 70:238–241.

    Article  Google Scholar 

  11. De la Torre-Carbot, K., Jauregui, O., Gimeno, E., Castellote, A. I., Lamuela-Raventos, R. M., and Lopez-Sabater, M. C. 2005. Characterization and quantification of phenolic compounds in olive oils by solid-phase extraction, HPLC-DAD, and HPLC-MS/MS. J. Agric. Food Chem. 53:4331–4340.

    PubMed  Article  Google Scholar 

  12. 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 83:458–468.

    Article  Google Scholar 

  13. Efron, B., Halloran, E., and Holmes, S. 1996. Bootstrap confidence levels for phylogenetic trees (vol 93, p. 7085, 1996). Proc. Natl. Acad. Sci. USA. 93:13429–13434.

    PubMed  Article  CAS  Google Scholar 

  14. Eyles, A., Jones, W., Riedl, K., Herms, D. A., Cipollini, D., Schwartz, S., Chan, K., and Bonello, P. 2007. Comparative phloem chemistry of Manchurian (F. mandshurica) and two North American ash species (F. americana and F. pennsylvanica). J. Chem. Ecol. 33:1430–1448.

    PubMed  Article  CAS  Google Scholar 

  15. Fang, N. B., Yu, S. G., and Prior, R. L. 2002. LC/MS/MS characterization of phenolic constituents in dried plums. J. Agric. Food Chem. 50:3579–3585.

    PubMed  Article  CAS  Google Scholar 

  16. 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 diuresis. Phytochemistry 55:611–616.

    PubMed  Article  CAS  Google Scholar 

  17. Godecke, T., Kaloga, M., and Kolodziej, H. 2005. A phenol glucoside, uncommon coumarins and flavonoids from Pelargonium sidoides. Naturforsch B 60:677–682.

    Google Scholar 

  18. Guo, H., Liu, A. H., Ye, M., Yang, M., and Guo, D. A. 2007. Characterization of phenolic compounds in the fruits of Forsythia suspensa by high-performance liquid chromatography coupled with electrospray ionization tandem mass spectrometry. Rapid Commun. Mass Sp. 21:715–729.

    Article  CAS  Google Scholar 

  19. Harris, M. K. and Frederiksen, R. A. 1984. Concepts and methods regarding host plant resistance to arthropods and pathogens. Annu. Rev. Phytophathol. 22:247–272.

    Article  Google Scholar 

  20. Herms, D. A., McCullough, D. G., and Smitley, D. R. 2004. Under attack: the current status of the emerald ash borer infestation and the program to eradicate it. Am. Nurseryman 7:20–27.

    Google Scholar 

  21. Hosny, M. 1998. Secoiridoid glucosides from Fraxinus oxycarpa. Phytochemistry 47:1569–1576.

    Article  CAS  Google Scholar 

  22. Iossifova, T., Vogler, B., and Kostova, I. 2002. Escuside, a new coumarin-secoiridoid from Fraxinus ornus bark. Fitoterapia 73:386–389.

    PubMed  Article  CAS  Google Scholar 

  23. Jeandroz, S., Roy, A., and Bousquet, J. 1997. Phylogeny and phylogeography of the circumpolar genus Fraxinus (Oleaceae) based on internal transcribed spacer sequences of nuclear ribosomal DNA. Mol. Phylogenet. Evol. 7:241–251.

    PubMed  Article  CAS  Google Scholar 

  24. Jimenez, P., Masson, L., Barriga, A., Chavez, J., and Robert, P. 2010. Oxidative stability of oils containing olive leaf extracts obtained by pressure, supercritical and solvent-extraction. Eur. J. Lipid Sci. Technol. 113:497–505.

    Article  Google Scholar 

  25. Johnson, R. and Wichern, D. A. 2002. Applied Multivariate Statistical Analysis, 5th ed. Prentice-Hall, Upper Saddle River.

    Google Scholar 

  26. Kammerer, B., Kahlich, R., Biegert, C., Gleiter, C. H., and Heide, L. 2005. HPLC-MS/MS analysis of willow bark extracts contained in pharmaceutical preparations. Phytochem. Anal. 16:470–478.

    PubMed  Article  CAS  Google Scholar 

  27. KEENA, M. A., GOULD, J., and BAUER, L. S. 2010. Developing an effective and efficient rearing method for the emerald ash borer, in, Proceedings of the Emerald Ash Borer Research and Technology Development Meeting, October 20–21, 2009, Pittsburgh, Pennsylvania. Lance D, Buck J, Binion D, Reardon R, and Mastro V, compilers. USDA Forest Health Technology Enterprise Team, FHTET-2010-01. p. 136.

  28. KOCH J. L., MASON M. E., CAREY D. W., KNIGHT K. S., POLand T. M., and HERMS D. A. 2010. Survey for tolerance to emerald ash borer within North American ash species, pp. 64, in C. H. Michler, M.D. Ginzel (eds.), Proceedings of Symposium on Ash in North America, Gen. Tech. Rep. NRS-P-72. Newtown Square, PA: USDA Forest Service, Northern Research Station.

  29. Kostova, I. and Iossifova, T. 2007. Chemical components of Fraxinus species. Fitoterapia 78(2):85–106.

    PubMed  Article  CAS  Google Scholar 

  30. Kurokawa, H., Kitahashi, Y., Koike, T., Lai, J., and Nakashizuka, T. 2004. Allocation to defense or growth in dipterocarp forest seedlings in Borneo. Oecologia 140(2):261–270.

    PubMed  Article  Google Scholar 

  31. Lin, L. Z. and Harnly, J. N. 2008. Phenolic compounds and chromatographic profiles of pear skins (Pyrus spp.). J. Agric. Food Chem. 56:9094–9101.

    PubMed  Article  CAS  Google Scholar 

  32. 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. 42:61–71.

    Article  Google Scholar 

  33. Miyazawa, M., Ishikawa, Y., Kasahara, H., Yamanaka, J., and Kameoka, H. 1994. An insect growth-inhibitory lignan from flower buds of Magnolia-fargesii. Phytochemistry 35:611–613.

    Article  CAS  Google Scholar 

  34. Parejo, I., Jauregui, O., Sanchez-Rabaneda, F., Viladomat, F., Bastida, J., and Codina, C. 2004. Separation and characterization of phenolic compounds in fennel (Foeniculum vulgare) using liquid chromatography-negative electrospray ionization tandem mass spectrometry. J. Agric. Food Chem. 52:3679–3687.

    PubMed  Article  CAS  Google Scholar 

  35. 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. 104:118–124.

    Google Scholar 

  36. R DEVELOPMENT CORE TEAM 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  37. 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. 37:242–246.

    PubMed  Article  Google Scholar 

  38. Ryan, D., Robards, K., and Lavee, S. 1999. Determination of phenolic compounds in olives by reversed-phase chromatography and mass spectrometry. J. Chromatogr. A 832:87–96.

    Article  CAS  Google Scholar 

  39. Ryan, D., Antolovich, M., Herlt, T., Prenzler, P. D., Lavee, S., and Robards, K. 2002. Identification of phenolic compounds in tissues of the novel olive cultivar Hardy’s mammoth. J. Agric. Food Chem. 50:6716–6724.

    PubMed  Article  CAS  Google Scholar 

  40. Savarese, M., de Marco, E., and Sacchi, R. 2007. Characterization of phenolic extracts from olives (Olea europaea cv. Pisciottana) by electrospray ionization mass spectrometry. Food Chem. 105:761–770.

    Article  CAS  Google Scholar 

  41. SMITH E. L., STORER A. J., and ROOSIEN B. K. Emerald ash borer infestation rates in Michigan, Ohio, and Indiana. McManus K, Gottschalk KW, eds. p. 82 in: Proceedings. 20th USDA Interagency Research Forum on Invasive Species 2009. Jan. 13–16, 2009, Annapolis, MD. USDA FS GTR NRC-P-51, Newtown Square, PA: USDA, Forest Service, Northern Research Station. 114 pp.

  42. SPSS STATISTICS FOR MAC. Version 19. 2010. IBM-SPSS Inc., Chicago, IL. USA.

  43. Strack, D. 1997. Phenolic metabolism, pp. 387–416, in P. M. Dey and J. B. Harborne (eds.), Plant Biochemistry. Academic Press, New York.

    Google Scholar 

  44. Suzuki, R. and Shimodaira, H. 2006. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542.

    PubMed  Article  CAS  Google Scholar 

  45. Tanahashi, T., Takenaka, Y., and Nagakura, N. 1996. Two dimeric secoiridoid glucosides from Jasminum polyanthum. Phytochemistry 41:1341–1345.

    Article  CAS  Google Scholar 

  46. Terazawa, M. and Sasaya, T. 1970. Studies on the extractives of Yachidamo, Fraxinus mandshurica Ruprecht var. japonica Maxim. II. Glucosides in bark. J. Jpn. Wood Res. Soc. 16:192–199.

    CAS  Google Scholar 

  47. Wainhouse, D., Cross, D. J., and Howell, R. S. 1990. The role of lignin as a defense against the spruce bark beetle Dendroctonus micans—effect on larvae and adults. Oecologia 85:257–265.

    Article  Google Scholar 

  48. Wallander, E. 2008. Systematic of Fraxinus (Oleaceae) and evolution of dioecy. Plant Syst. Evol. 273:25–49.

    Article  Google Scholar 

  49. Wei, X., Reardon, D., Wu, Y., and Sun, J. H. 2004. Emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), in China: a review and distribution survey. Acta Entomol. Sin. 47:679–685.

    Google Scholar 

  50. Whitehill, J. G. A. 2011. Investigations into Mechanisms of Ash Resistance to the Emerald Ash Borer. The Ohio State University, Columbus. 250 p.

    Google Scholar 

  51. Whitehill, J. G. A., Popova-Butler, A., Green-Church, K. B., Koch, J. L., Herms, D. A., and Bonello, P. 2011. Interspecific proteomic comparisons reveal ash phloem genes potentially involved in constitutive resistance to the emerald ash borer. PLoS One 6:e24863.

    PubMed  Article  CAS  Google Scholar 

  52. Yasuda, T., Fukui, M., Nakazawa, T., Hoshikawa, A., and Ohsawa, K. 2006. Metabolic fate of fraxin administered orally to rats. J. Nat. Prod. 69:755–757.

    PubMed  Article  CAS  Google Scholar 

  53. Ye, M., Yan, Y. N., and Guo, D. A. 2005. Characterization of phenolic compounds in the Chinese herbal drug Tu-Si-Zi by liquid chromatography coupled to electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 19:1469–1484.

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

Bailey Nursery, Inc. (St. Paul MN, USA), Moon Dancer Farm (Lexington KY, USA), and the USDA Forest Service, Northern Research Station (Delaware OH, USA) provided trees used in this study. We thank David S. Bienemann, Municipal Arborist, City of Bowling Green, Ohio, for providing the site for the ash plantation, and for his assistance with establishing and maintaining the trees. We thank Bryant Chambers, Diane Hartzler, and Ohio State University Extension Master Gardeners for their help planting the trees, and Karla Medina-Ortega and Gerardo Suazo for technical assistance. This project was funded by the Tree Research and Education Endowment Fund, the Horticultural Research Institute, Ohio Plant Biotechnology Consortium, USDA APHIS Accelerated Emerald Ash Borer Research Program, USDA Forest Service Northern Research Station, and by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University, and Wright State University.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Justin G. A. Whitehill.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Results

(DOCX 32 kb)

Supplemental Materials and Methods

(DOCX 31 kb)

Supplemental References

(DOCX 16 kb)

Table S1

(DOCX 37 kb)

Table S2

(DOCX 29 kb)

Figure S1

(DOCX 825 kb)

Figure S2

(DOCX 1363 kb)

Figure S3

(DOCX 519 kb)

Figure S4

(DOCX 810 kb)

Figure S5

(DOCX 733 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Whitehill, J.G.A., Opiyo, S.O., Koch, J.L. et al. Interspecific Comparison of Constitutive Ash Phloem Phenolic Chemistry Reveals Compounds Unique to Manchurian Ash, a Species Resistant to Emerald Ash Borer. J Chem Ecol 38, 499–511 (2012). https://doi.org/10.1007/s10886-012-0125-7

Download citation

Keywords

  • Agrilus planipennis
  • Fraxinus
  • Wood-borer
  • HPLC
  • Host plant resistance
  • Plant–insect interactions
  • Invasive species
  • Emerald ash borer
  • Coleoptera
  • Buprestidae