Journal of Chemical Ecology

, Volume 36, Issue 3, pp 286–297 | Cite as

Biosynthesis of Phenolic Glycosides from Phenylpropanoid and Benzenoid Precursors in Populus

  • Benjamin A. Babst
  • Scott A. Harding
  • Chung-Jui Tsai
Article

Abstract

Salicylate-containing phenolic glycosides (PGs) are abundant and often play a dominant role in plant-herbivore interactions of Populus and Salix species (family Salicaceae), but the biosynthetic pathway to PGs remains unclear. Cinnamic acid (CA) is thought to be a precursor of the salicyl moiety of PGs. However, the origin of the 6-hydroxy-2-cyclohexen-on-oyl (HCH) moiety found in certain PGs, such as salicortin, is not known. HCH is of interest because it confers toxicity and antifeedant properties against herbivores. We incubated Populus nigra leaf tissue with stable isotope-labeled CA, benzoates, and salicylates, and measured isotopic incorporation levels into both salicin, the simplest PG, and salicortin. Labeling of salicortin from [13C6]-CA provided the first evidence that HCH, like the salicyl moiety, is a phenylpropanoid derivative. Benzoic acid and benzaldehyde also labeled both salicyl and HCH, while benzyl alcohol labeled only the salicyl moiety in salicortin. Co-administration of unlabeled benzoates with [13C6]-CA confirmed their contribution to the biosynthesis of the salicyl but not the HCH moiety of salicortin. These data suggest that benzoate interconversions may modulate partitioning of phenylpropanoids to salicyl and HCH moieties, and hence toxicity of PGs. Surprisingly, labeled salicyl alcohol and salicylaldehyde were readily converted to salicin, but did not result in labeled salicortin. Co-administration of unlabeled salicylates with labeled CA suggested that salicyl alcohol and salicylaldehyde may have inhibited salicortin biosynthesis. A revised metabolic grid model of PG biosynthesis in Populus is proposed, providing a guide for functional genomic analysis of the PG biosynthetic pathway.

Keywords

Poplar Salicaceae Isotope labeling Phenolic glycosides Herbivore defense Carbon-13 LC-MS 

Supplementary material

10886_2010_9757_MOESM1_ESM.docx (132 kb)
Fig S1(DOCX 143 kb)
10886_2010_9757_MOESM2_ESM.docx (208 kb)
Fig S2(DOCX 222 kb)
10886_2010_9757_MOESM3_ESM.docx (276 kb)
Fig S3(DOCX 288 kb)
10886_2010_9757_MOESM4_ESM.docx (95 kb)
Fig S4(DOCX 106 kb)
10886_2010_9757_MOESM5_ESM.docx (74 kb)
Fig S5(DOCX 84.5 kb)

References

  1. Boatright, J., Negre, F., CHEN, X., KISH, C. M., WOOD, B., PEEL, G., ORLOVA, I., GANG, D. R., RHODES, D., and DUDAREVA, N., 2004. Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 135, 1993–2011.CrossRefPubMedGoogle Scholar
  2. DEAN, J. V., SHAH, R. P., and MOHAMMED, L. A., 2003. Formation and vacuolar localization of salicylic acid glucose conjugates in soybean cell suspension cultures. Physiol. Plantarum 118, 328–336.CrossRefGoogle Scholar
  3. DONALDSON, J. R., KRUGER, E. L., and LINDROTH, R. L. 2006. Competition- and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytol. 169, 561–570.CrossRefPubMedGoogle Scholar
  4. HWANG, S. Y. and LINDROTH, R. L., 1997. Clonal variation in foliar chemistry of aspen: Effects on gypsy moth and forest tent caterpillar. Oecologia 111, 99–108.CrossRefGoogle Scholar
  5. JARVIS, A. P., SCHAAF, O., and OLDHAM, N. J., 2000. 3-Hydroxy-3-phenylpropanoic acid is an intermediate in the biosynthesis of benzoic acid and salicylic acid but benzaldehyde is not. Planta 212, 119–126.CrossRefPubMedGoogle Scholar
  6. 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. Analysis 16, 470–478.CrossRefGoogle Scholar
  7. LARSON, P. R. and ISEBRANDS, J. G., 1971. The plastochron index as applied to developmental studies of cottonwood. Can. J. Forest Res. 1, 1–11.CrossRefGoogle Scholar
  8. LINDROTH, R. L. and HWANG, S. Y., 1996. Clonal variation of foliar chemistry of quaking aspen (Populus tremuloides Michx.). Biochem. Syst. Ecol. 24, 357–364.CrossRefGoogle Scholar
  9. LONG, M. C., NAGEGOWDA, D. A., KAMINAGA, Y., HO, K. K., KISH, C. M., SCHNEPP, J., SHERMAN, D., WEINER, H., RHODES, D., and DUDAREVA, N. 2009. Involvement of snapdragon benzaldehyde dehydrogenase in benzoic acid biosynthesis. Plant J. 59:256–265.CrossRefPubMedGoogle Scholar
  10. MOKLE, S. S., DAWANE, B. S., SAYYED, M. A., and VIBHUTE, Y. B., 2006. An improved procedure for the synthesis of 2-hydroxybenzaldehyde and 2-hydroxynaphthalene-1-carbaldehyde. J. Chem. Res. 101, 101.CrossRefGoogle Scholar
  11. MORSE, A. M., TSCHAPLINSKI, T. J., DERVINIS, C., PIJUT, P. M., SCHMELZ, E. A., DAY, W., and DAVIS, J. M., 2007. Salicylate and catechol levels are maintained in nahG transgenic poplar. Phytochemistry 68, 2043–2052.CrossRefPubMedGoogle Scholar
  12. ORLOVA, I., MARSHALL-Colon, A., SCHNEPP, J., WOOD, B., VARBANOVA, M., FRIDMAN, E., BLAKESLEE, J. J., PEER, W. A., MURPHY, A. S., RHODES, D., PICHERSKY, E., and DUDAREVA, N.. 2006. Reduction of benzenoid synthesis in petunia flowers reveals multiple pathways to benzoic acid and enhancement in auxin transport. Plant Cell 18:3458–3475.CrossRefPubMedGoogle Scholar
  13. OSIER, T. L. and LINDROTH, R. L., 2001. Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J. Chem. Ecol. 27, 1289–1313.CrossRefPubMedGoogle Scholar
  14. PALO, R. T., 1984. Distribution of birch (Betula spp.), willow (Salix spp.), and poplar (Populus spp.) secondary metabolites and their potential role as chemical defense against herbivores. J. Chem. Ecol. 10, 499–520.CrossRefGoogle Scholar
  15. PEARL, I. A. and DARLING, S. F., 1970. The structures of salicortin and tremulacin. Tetrahedron Lett. 11, 3827–3830.CrossRefGoogle Scholar
  16. PEARL, I. A. and DARLING, S. F., 1971. The structures of salicortin and tremulacin. Phytochemistry 10, 3161–3166.CrossRefGoogle Scholar
  17. PIERPONT, W. S., 1994. Salicylic acid and its derivatives in plants: Medicines, metabolites and messenger molecules. Adv. Bot. Res. 20, 163–235.CrossRefGoogle Scholar
  18. RUUHOLA, T. and JULKUNEN-TIITTO, R., 2003. Trade-off between synthesis of salicylates and growth of micropropagated Salix pentandra. J. Chem. Ecol. 29, 1565–1588.CrossRefPubMedGoogle Scholar
  19. RUUHOLA, T., TIKKANEN, O. P., and TAHVANAINEN, J., 2001. Differences in host use efficiency of larvae of a generalist moth, Operophtera brumata on three chemically divergent Salix species. J. Chem. Ecol. 27, 1595–1615.CrossRefPubMedGoogle Scholar
  20. RUUHOLA, T., JULKUNEN-TIITTO, R., and VAINIOTALO, P., 2003. In vitro degradation of willow salicylates. J. Chem. Ecol. 29, 1083–1097.CrossRefPubMedGoogle Scholar
  21. SETAMDIDEH, D. and ZEYNIZADEH, B., 2006. Mild and convenient method for reduction of carbonyl compounds with the NaBH4/charcoal system in wet THF. Z. Naturforsch. B 61, 1275–1281.Google Scholar
  22. TSAI, C.-J., HARDING, S. A., TSCHAPLINSKI, T. J., LINDROTH, R. L., and YUAN, Y., 2006. Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol. 172, 47–62.CrossRefPubMedGoogle Scholar
  23. TUSKAN, G. A., DIFAZIO, S. P., JANSSON, S., BOHLMANN, J., et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596–1604.CrossRefPubMedGoogle Scholar
  24. VOGT, T. and JONES, P., 2000. Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci. 5, 359–403.CrossRefGoogle Scholar
  25. WINKEL, B. S. J., 2004. Metabolic channeling in plants. Annu. Rev. Plant Biol. 55, 85–107.CrossRefPubMedGoogle Scholar
  26. ZENK, M. H., 1967. Pathways of salicyl alcohol and salicin formation in Salix purpurea L. Phytochemistry 6, 245–252.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Benjamin A. Babst
    • 1
    • 2
  • Scott A. Harding
    • 1
    • 2
  • Chung-Jui Tsai
    • 1
    • 2
    • 3
  1. 1.School of Forest Resources and Environmental ScienceMichigan Technological UniversityHoughtonUSA
  2. 2.Warnell School of Forestry and Natural ResourcesUniversity of GeorgiaAthensUSA
  3. 3.Department of GeneticsUniversity of GeorgiaAthensUSA

Personalised recommendations