Comparative Phloem Chemistry of Manchurian (Fraxinus mandshurica) and Two North American Ash Species (Fraxinus americana and Fraxinus pennsylvanica)

Abstract

Recent studies have investigated interspecific variation in resistance of ash (Fraxinus spp.) to the exotic wood-boring beetle, emerald ash borer (EAB, Agrilus planipennis). Manchurian ash (Fraxinus mandshurica) is an Asian species that has coevolved with EAB. It experiences little EAB-induced mortality compared to North American ashes. Host phloem chemistry, both constitutive and induced, might partly explain this interspecific variation in resistance. We analyzed the constitutive phloem chemistry of three ash species: Manchurian ash and North American white (Fraxinus americana) and green (Fraxinus pennsylvanica) ash. Analysis of the crude phloem extracts revealed the presence of an array of phenolic compounds including hydroxycoumarins, a monolignol, lignans, phenylethanoids, and secoiridoids. Both qualitative and quantitative differences were observed among the three ash species. Hydroxycoumarins and the phenylethanoids, calceloariosides A and B, were present only in the phloem of Manchurian ash and might represent a mechanism of resistance against EAB.

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References

  1. Adler, L. S., Schmitt, J., and Bowers, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85.

    Article  Google Scholar 

  2. Anderson, R. F. 1944. The relation between host condition and attacks by the bronzed birch borer. J. Econ. Entomol. 37:588–596.

    Google Scholar 

  3. Bianco, A., Buiarelli, F., Cartoni, G., Coccioli, F., Muzzalupo, I., Polidori, A., and Uccella, N. 2001. Analysis by HPLC-MS/MS of biophenolic components in olives and oils. Anal. Lett. 34:1033–1051.

    Article  CAS  Google Scholar 

  4. Biere, A., Marak, H. B., and Van Damme, J. M. M. 2004. Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441.

    PubMed  Article  Google Scholar 

  5. Biggs, A. R., Merrill, W., and Davis, D. D. 1984. Discussion-response of bark tissues to injury and infection. Can. J. For. Res. 14:351–356.

    Article  Google Scholar 

  6. Bodesheim, U. and Holzl, J. 1997. Isolation and receptor binding properties of alkaloids and lignans from Valeriana officinalis L. Pharmazie 52:386–391.

    PubMed  CAS  Google Scholar 

  7. Bostock, R. M., and Stermer, B. A. 1989. Perspectives on wound healing in resistance to pathogens. Annu. Prev. Phytopathol. 27:343–371.

    Article  Google Scholar 

  8. Boyer, L., Elias, R., Taoubi, K., Debrauwer, L., Faure, R., Baghdikian, B., and Balansard, G. 2005. Lignans and secoiridoids from the root bark of Chionanthus virginicus L.: isolation, identification and HPLC analysis. Phytochem. Anal. 16:375–379.

    PubMed  Article  CAS  Google Scholar 

  9. 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 70:561–567.

    Article  CAS  Google Scholar 

  10. 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 

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

    Article  CAS  Google Scholar 

  12. Concannon, S., Ramachandran, V. N., and Smyth, W. F. 2000. A study of the electrospray ionisation of selected coumarin derivatives and their subsequent fragmentation using an ion trap mass spectrometer. Rapid Comm. Mass Spectrom. 14:1157–1166.

    Article  CAS  Google Scholar 

  13. 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 

  14. Ersöz, T., Taşdemir, D., Çaliş, I., and Ireland, C. M. 2002. Phenylethanoid glycosides from Scutellaria galericulata. Turk. J. Chem. 26:465–471.

    Google Scholar 

  15. Evtuguin, D. V. and Amado, F. M. L. 2003. Application of Electrospray ionization mass spectrometry to the elucidation of the primary structure of lignin. Macromol. Biosci. 3:339–343.

    Article  CAS  Google Scholar 

  16. Eyles, A., Davies, N. W., and Mohammed, C. 2003a. Novel detection of formylated phloroglucinol compounds (FPCs) in the wound wood of Eucalyptus globulus and E. nitens. J. Chem. Ecol. 29:881–898.

    PubMed  Article  CAS  Google Scholar 

  17. Eyles, A., Davies, N. W., and Mohammed, C. 2003b. Wound wood formation in Eucalyptus globulus and Eucalyptus nitens: anatomy and chemistry. Can. J. Forest Res. 33:2331–2339.

    Article  Google Scholar 

  18. Fabre, N., Rustan, I., De Hoffmann, E., and Quetin-Leclercq, J. 2001. Determination of flavone, flavonol, and flavanone aglycones by negative ion liquid chromatography electrospray ion trap mass spectrometry. J. Am. Soc. Mass Spectrom. 12:707–715.

    PubMed  Article  CAS  Google Scholar 

  19. Fernandes, G. W. 1990. Hypersensitivity—a neglected plant resistance mechanism against insect herbivores. Environ. Entomol. 19:1173–1182.

    Google Scholar 

  20. 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. 167:353–375.

    PubMed  Article  CAS  Google Scholar 

  21. 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 

  22. Godecke, T., Kaloga, M., and Kolodziej, H. 2005. A phenol glucoside, uncommon coumarins and flavonoids from Pelargonium sidoides DC. J. Chem. Sci. 60:677–682.

    Article  CAS  Google Scholar 

  23. Gould, J., Tanner, J., Winograd, D., and Lane, S. 2005. Initial studies on the laboratory rearing of emerald ash borer and foreign exploration for natural enemies, pp. 73–74, in V. C. Mastro and R. Reardon (eds.). Proceedings of Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Health Technology Enterprise Team Publication FHTET-2004-15. USDA Forest Service, Morgantown, W.Va.

  24. Griffith, D. M., Digiovanni, D. M., Witzel, T. L., and Wharton, E. H. 1991. Forest statistics for Ohio, 1991. USDA Forest Service NE For. Exper. Stat. Res. Bull. NE-128.

  25. Haack, R. A., Jendek, E., Liu, H., Marchant, K. R., Petrice, T. R., Poland, T. M., and Ye, H. 2002. The emerald ash borer: a new exotic pest in North America. Michigan Entomological Soc, Newsletter 47:1–5.

    Google Scholar 

  26. Hanks, L. M., Paine, T. D., Millar, J. G., Campbell, C. D., and Schuch, U. K. 1999. Water relations of host trees and resistance to the phloem-boring beetle Phoracantha semipunctata F (Coleoptera : Cerambycidae). Oecologia 119:400–407.

    Article  Google Scholar 

  27. Harvey, J. A., Van Nouhuys, S., and Biere, A. 2005. Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. J. Chem. Ecol. 31:287–302.

    PubMed  Article  CAS  Google Scholar 

  28. Herms, D. A., Stone, A. K., and Chatfield, J. A. 2004. Emerald ash borer: the beginning of the end of Ash in North America? pp. 62–71, in J. A. Chatfield, E. A. Draper, H. M. Mathers, D. E. Dyke, P. J. Bennett, and J. F. Boggs (eds.) Ornamental plants: Annual Reports and Research Reviews 2003, Ohio Agricultural Research and Development Center / Ohio State University Extension Special Circular 193.

  29. Iossifova, T., Kostova, I., and Evstatieva, L. N. 1997. Secoiridoids and hydroxycoumarins in Bulgarian Fraxinus species. Biochem. Syst. Ecol. 25:271–274.

    Article  CAS  Google Scholar 

  30. Iossifova, T., Vogler, B., and Kostova, I. 1998. Secoiridoid glucosides from Fraxinus ornus bark. Phytochemistry 49:1329–1332.

    Article  CAS  Google Scholar 

  31. Iossifova, T., Vogler, B., Klaiber, I., Kostova, I., and Kraus, W. 1999. Caffeic acid esters of phenylethanoid glycosides from Fraxinus ornus bark. Phytochemistry 50:297–301.

    Article  CAS  Google Scholar 

  32. Jensen, S. R. and Nielsen, B. J. 1976. A new coumarin, fraxidin 8-O-beta-d-glucoside and 10-hydroxyligustroside from bark of Fraxinus exelsior. Phytochemistry 15:221–223.

    Article  CAS  Google Scholar 

  33. Jensen, S. R., Franzyk, H., and Wallander, E. 2002. Chemotaxonomy of the Oleaceae: iridoids as taxonomic markers. Phytochemistry 60:213–231.

    PubMed  Article  CAS  Google Scholar 

  34. 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 

  35. Kehr, J. 2006. Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J. Exp. Bot. 57:767–774.

    PubMed  Article  CAS  Google Scholar 

  36. Kemp, M. S. and Burden, R. S. 1986. Review Article 17. Phytoalexins and stress metabolites in the sapwood of trees. Phytochemistry 25:1261–1269.

    Article  CAS  Google Scholar 

  37. Konno, K., Hirayama, C., Yasui, H., and Nakamura, M. 1999. Enzymatic activation of oleuropein: a protein crosslinker used as a chemical defense in the privet tree. Proc. Natl. Acad. Sci. USA 96:9159–9164.

    PubMed  Article  CAS  Google Scholar 

  38. Konno, K., Okada, S., and Hirayama, C. 2001. Selective secretion of free glycine, a neutralizer against a plant defense chemical, in the digestive juice of the privet moth larvae. J. Insect Physiol. 47:1451–1457.

    PubMed  Article  CAS  Google Scholar 

  39. Kostova, I. 2001. Fraxinus ornus L. Fitoterapia 72:471–480.

    PubMed  Article  CAS  Google Scholar 

  40. Kostova, I., Dinchev, D., Mikhova, B., and Iossifova, T. 1995. Epoxyconiferyl alcohol from Fraxinus oxycarpa bark. Phytochemistry 38:801–802.

    Article  CAS  Google Scholar 

  41. Leszczynski, B., Tjallingii, W. F., Dixon, A. F. G., and Swiderski, R. 1995. Effect of methoxyphenols on grain aphid feeding behavior. Entomol. Exp. Appl. 76:157–162.

    Article  CAS  Google Scholar 

  42. Liu, H. P., Bauer, L. S., Gao, R. T., Zhao, T. H., Petrice, T. R., and Haack, R. A. 2003. Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera : Buprestidae), and its natural enemies in China. Great Lakes Entomol. 36:191–204.

    Google Scholar 

  43. Liu, R. M., Sun, Q. H., Sun, A. L., and Cui, J. C. 2005. Isolation and purification of coumarin compounds from Cortex fraxinus by high-speed counter-current chromatography. J. Chromatogr. A 1072:195–199.

    PubMed  Article  CAS  Google Scholar 

  44. March, R. E., Lewars, E. G., Stadey, C. J., Miao, X. S., Zhao, X. M., and Metcalfe, C. D. 2006. A comparison of flavonoid glycosides by electrospray tandem mass spectrometry. Int. J. Mass. Spectrom. 248:61–85.

    Article  CAS  Google Scholar 

  45. Mulinacci, N., Giaccherini, C., Innocenti, M., Romani, A., Vincieri, F. F., Marotta, F., and Mattei, A. 2005. Analysis of extra virgin olive oils from stoned olives. J. Sci. Food Agric. 85:662–670.

    Article  CAS  Google Scholar 

  46. Mullick, D. B. 1977. The non-specific nature of defense in bark and wood during wounding, insect and pathogen attack. Recent Adv. Phytochem. 11:395–441.

    CAS  Google Scholar 

  47. Mullick, D. B. and Jensen, G. D. 1973. New concepts and terminology of coniferous periderms: necrophylactic and exophylactic periderms. Can. J. Bot. 51:1459–1470.

    Google Scholar 

  48. Nicoletti, M., Galeffi, C., Messana, I., Garbarino, J. A., Gambaro, V., Nyandat, E., and Marinibettolo, G. B. 1986. New phenylpropanoid glucosides from Calceolaria hypericina. Gaz. Chim. Ital. 116:431–433.

    CAS  Google Scholar 

  49. Nieminen, M., Suomi, J., Van Nouhuys, S., Sauri, P., and Riekkola, M. L. 2003. Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore. J. Chem. Ecol. 29:823–844.

    PubMed  Article  CAS  Google Scholar 

  50. Nykolov, N., Iossifova, T., Vassileva, E., Kostova, I., and Stoev, G. 1993. Reverse-phase high-pressure liquid-chromatographic analysis of hydroxycoumarins in plant-extracts—quantitative determination of hydroxycoumarins in Fraxinus ornus. Phytochem. Anal. 4:86–88.

    Article  CAS  Google Scholar 

  51. 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 

  52. Pearce, R. B. 1996. Antimicrobial defences in the wood of living trees. New Phytol. 132:203–233.

    Article  CAS  Google Scholar 

  53. Penuelas, J., Sardans, J., Stefanescu, C., Parella, T., and Filella, I. 2006. Lonicera implexa leaves bearing naturally laid eggs of the specialist herbivore Euphydryas aurinia have dramatically greater concentrations of iridoid glycosides than other leaves. J. Chem. Ecol. 32:1925–1933.

    PubMed  Article  CAS  Google Scholar 

  54. Perez, J. A., Hernandez, J. M., Trujillo, J. M., and Lopez, H. 2005. Iridoids and secoiridoids from Oleaceae, pp. 303–363 in A. Rahman (ed.). Studies in Natural Products Chemistry. Elsevier, Amsterdam.

    Google Scholar 

  55. 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. Forestry 104:118–124.

    Google Scholar 

  56. Raffa, K. F. and Klepzig, K. D. 1992. Tree defense mechanisms against fungi associated with insects, pp. 354–389, in R. A. Blanchette and A. R. Biggs (eds). Defense Mechanisms of Woody Plants against Fungi. Springer-Verlag, NY.

  57. Rebek, E., Herms, D. A., Smitley, D. R., Bonello, P., Eyles, A., and Cipollini, D. 2006. Interspecific variation in ash resistance to emerald ash borer, p. 17, in V. C. Mastro, R. Reardon, and G. Parra (eds). Proceedings of 2005 Emerald Ash Borer Research and Technology Development Meeting, Pittsburg, PA. USDA Forest Health Technology Enterprise Team Publication FHTET-2005-16. USDA Forest Service, Morgantown, W.Va.

  58. Robinson, R. M., Jensen, G. D., and Morrison, D. J. 2004. Necrophylactic periderm formation in the roots of western larch and Douglas-fir trees infected with Armillaria ostoyae. I. The response to abiotic wounding in non-infected roots. Forest Pathol. 34:105–118.

    Article  Google Scholar 

  59. Roseland, C. R. and Grosz, T. J. 1997. Induced responses of common annual sunflower Helianthus annuus L from geographically diverse populations and deterrence to feeding by sunflower beetle. J. Chem. Ecol. 23:517–542.

    Article  CAS  Google Scholar 

  60. 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 

  61. Santamour, F. S. 1981. Flavonoids and coumarins in Fraxinus and their potential utility in hybrid verification. Proceedings of the Northeastern Forest Tree Improvement Conference (27th). USDA pp. 63–71

  62. Schaefer, P. W. 2005. Foreign exploration for emerald ash borer and its natural enemies, pp. 67–68, in V. C. Mastro and R. Reardon (eds.). Proceedings of 2004 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Health Technology Enterprise Team Publication FHTET-2004-15. USDA Forest Service, Morgantown, W.Va.

  63. Schroeder, F. C., Del Campo, M. L., Grant, J. B., Weibel, D. B., Smedley, S. R., Bolton, K. L., Meinwald, J., and Eisner, T. 2006. Pinoresinol: a lignol of plant origin serving for defense in a caterpillar. Proc. Natl. Acad. Sci. USA 103:15497–15501.

    PubMed  Article  CAS  Google Scholar 

  64. Silva, M. C. P., Terra, W. R., and Ferreira, C. 2006. Absorption of toxic beta-glucosides produced by plants and their effect on tissue trehalases from insects. Comp. Biochem. Physiol. B 143:367–373.

    PubMed  Article  CAS  Google Scholar 

  65. Smeds, A. I., Hakala, K., Hurmerinta, T. T., Kortela, L., Saarinen, N. M., and Makela, S. I. 2006. Determination of plant and enterolignans in human serum by high-performance liquid chromatography with tandem mass spectrometric detection. J. Pharmaceut. Biomed. 41:898–905.

    Article  CAS  Google Scholar 

  66. Steinegger, E. and Brantschen, A. 1959. New occurrences of coumarin derivatives in Fraxinus ornus. Pharm. Acta Helv. 34:334–344.

    PubMed  CAS  Google Scholar 

  67. Tanahashi, T., Parida, Y. T., Nagakura, N., Inoue, K., Kuwajima, H., and Chen-Chang, C. 1998. Four secoiridoid glucosides from Fraxinus insularis. Phytochemistry 49:1333–1337.

    Article  CAS  Google Scholar 

  68. Terazawa, M. and Sasaya, T. 1970. Studies on the extractives of Yachidamo Fraxinus mandshurica Rupr. var. japonica maxim. II. glucosides in bark. Mokuzai Gakkaishi 16:192–199.

    CAS  Google Scholar 

  69. Tolonen, A., Gyorgy, Z., Jalonen, J., Neubauer, P., and Hohtola, A. 2004. LC/MS/MS identification of glycosides produced by biotransformation of cinnamyl alcohol in Rhodiola rosea compact callus aggregates. Biomed. Chrom. 18:550–558.

    Article  CAS  Google Scholar 

  70. Tsukamoto, H., Hisada, S., and Nishibe, S. 1984. Lignans from bark of Fraxinus mandshurica var Japonica and Fraxinus japonica. Chem. Pharm. Bull. 32:4482–4489.

    PubMed  CAS  Google Scholar 

  71. Tsukamoto, H., Hisada, S., and Nishibe, S. 1985. Coumarins from bark of Fraxinus japonica and Fraxinus mandshurica var japonica. Chem. Pharm. Bull. 33:4069–4073.

    CAS  Google Scholar 

  72. Vereecke, D., Messens, E., Klarskov, K., Debruyn, A., Vanmontagu, M., and Goethals, K. 1997. Patterns of phenolic compounds in leafy galls of tobacco. Planta 201:342–348.

    Article  CAS  PubMed  Google Scholar 

  73. Wallander, E. 2001. Evolution of wind-pollination in Fraxinus (Oleaceae)—an ecophylogenetic approach. PhD dissertation. Botanical Institute. Sweden, Göteborg University.

  74. Wallander, E. and Albert, V. A. 2000. Phylogeny and classification of Oleaceae based on rps16 and trnL-F sequence data. Am. J. Bot. 87:1827–1841.

    Article  PubMed  CAS  Google Scholar 

  75. Wang, Z. and Sun, Y. 2005. Rapid analysis of the stem bark of Acanthopanax giraldii Harms by HPLC/DAD/ESI/MS2. J. Liquid Chrom. Related Technologies 28:1291–1298.

    CAS  Google Scholar 

  76. Willfor, S., Hemming, J., Reunanen, M., and Holmbom, B. 2003. Phenolic and lipophilic extractives in Scots pine knots and stemwood. Holzforschung 57:359–372.

    Article  Google Scholar 

  77. Ye, M., Yan, Y., and Guo, D. 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. Spec. 19:1469–1484.

    Article  CAS  Google Scholar 

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Acknowledgements

Thanks to Duan Wang for technical assistance. Use of the 400 MHz NMR spectrometer was permitted by the Ohio State University College of Pharmacy. We thank an anonymous reviewer for helpful comments. This work was supported in part by The Ohio Plant Biotechnology Consortium (Award No. 2005-025 to DAH, PB, and DFC), USDA Forest Service North Central Research Station (Award No. 03-JV-90 to DAH), USDA Northeastern Research Station (Research Joint Venture No. 05-JV-11242328-091 to DAH and PB), USDA ARS (Agreement No. 58-3607-4-175 to DAH), and by State and Federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University.

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Eyles, A., Jones, W., Riedl, K. et al. Comparative Phloem Chemistry of Manchurian (Fraxinus mandshurica) and Two North American Ash Species (Fraxinus americana and Fraxinus pennsylvanica). J Chem Ecol 33, 1430–1448 (2007). https://doi.org/10.1007/s10886-007-9312-3

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Keywords

  • Agrilus planipennis
  • LC-MS
  • Hydroxycoumarins
  • Phenolics
  • Coevolution
  • Host resistance
  • Invasive species