Skip to main content
Log in

Is (−)-Catechin a Novel Weapon of Spotted Knapweed (Centaurea stoebe)?

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The novel weapons hypothesis states that some invasive weed species owe part of their success as invaders to allelopathy mediated by allelochemicals that are new to the native species. Presumably, no resistance has evolved among the native species to this new allelochemical (i.e., the novel weapon). In their native habitat, however, the plants that co-evolved with these invasive species have theoretically evolved defenses that obviate the allelochemical advantage. Previous studies have claimed that catechin is such a novel weapon of spotted knapweed (Centaurea stoebe = C. maculosa), an invasive species in the non-native habitat of North America. These studies indicated that (−)-catechin is more phytotoxic than (+)-catechin. Other studies have not found sufficient catechin in field soils to support this theory. We report that (−)-catechin and (+)-catechin are essentially equal, but poorly phytotoxic to a variety of plant species in bioassays without soil. In a dose/response experiment with Montana soils, we found the lowest dose for a growth reduction of two native Montana grasses (Koeleria macrantha and Festuca idahoensis) by a racemic mixture of (±)-catechin that ranged from about 25 to 50 mM, concentrations, orders of magnitude higher than expected in nature. Autoclaving the soil before adding the catechin did not affect the activity of catechin. We found (−)-catechin to be a potent antioxidant, in contrast to a previous claim that it acts as an allelochemical by causing oxidative stress. Our findings suggest that catechin is not a novel weapon of spotted knapweed and that other allelochemical(s) or alternative mechanisms must be found to explain the success of this species as an invader in North America.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

References

  • Almajano, M. P., Delgado, M. E., and Gordon, M. H. 2007. Albumin causes a synergistic increase in the antioxidant activity of green tea catechins in oil-in-water emulsions. Food Chem 102:1375–1382.

    Article  CAS  Google Scholar 

  • Arnon, D. I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15.

    Article  PubMed  CAS  Google Scholar 

  • Baerson, S. R., Sánchez-Moreiras, A., Pedrol-Bonjoch, N., Schulz, I. A., Kagan, A. K., Reigosa, M. J., and Duke, S. O. 2005. Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one (BOA). J. Biol. Chem 280:21867–21881.

    Article  PubMed  CAS  Google Scholar 

  • Bais, H. P., Walker, T. S., Stermitz, F. R., Hufbauer, R. A., and Vivanco, J. M. 2002. Enantiomeric-dependent phytotoxic and anti-microbial activity of (±)-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiol 128:1173–1179.

    Article  PubMed  CAS  Google Scholar 

  • Bais, H. P., Vepachedu, R., Gilroy, S., Callaway, R. M., and Vivanco, J. M. 2003. Allelopathy and exotic plant invasion: from molecules and genes to species interaction. Science 301:1377–1380.

    Article  PubMed  CAS  Google Scholar 

  • Blair, A. C., Hanson, B. D., Brunk, G. R., Marrs, R. A., Westra, P., Nissen, S. J., and Hufbauer, R. A. 2005. New techniques and findings in the study of a candidate allelochemical implicated in invasion success. Ecol. Lett 8:1039–1047.

    Article  Google Scholar 

  • Blair, A. C., Nissen, S. J., Brunk, G. R., and Hufbauer, R. A. 2006. A lack of evidence for an ecological role of the putative allelochemical (±)-catechin in Centaurea maculosa invasion process. J. Chem. Ecol 32:2327–2331.

    Article  PubMed  CAS  Google Scholar 

  • Blair, A. C., Weston, L. A., Nissen, S. J., Brunk, G. R., and Hufbauer, R. 2009. The importance of analytical techniques in allelopathy studies with the reported allelochemical catechin as an example. Biol. Invasions (in press).

  • Broeckling, C. D., and Vivanco, J. M. 2008. A selective, sensitive, and rapid in-field assay for soil catechin, an allelochemical of Centaurea maculosa. Soil Biol. Biochem 40:1189–1196.

    Article  CAS  Google Scholar 

  • Buta, J. G., and Lusby, W. R. 1986. Catechins as germination and growth inhibitors in Lespediza seeds. Phytochemistry 25:93–95.

    Article  CAS  Google Scholar 

  • Callaway, R. M., and Ridenour, W. M. 2004. Novel weapons: invasive success and the evolution of increased competitive ability. Front. Ecol. Environ 2:436–443.

    Article  Google Scholar 

  • Callaway, R. M., Ridenour, W. M., Laboski, T., Weir, T., and Vivanco, J. M. 2005. Natural selection for resistance to the allelopathic effects of invasive plants. J. Ecol 93:576–583.

    Article  Google Scholar 

  • Cantrell, C. L., Duke, S. O., Fronczek, F. R., Osbrink, W. L. A., Mamonov, L. K., Vassilyev, J. I., Wedge, D. E., and Dayan, F. E. 2007. Phytotoxic eremophilanes from Ligularia macrophylla. J. Agric. Food Chem 55:10656–10663.

    Article  PubMed  CAS  Google Scholar 

  • Cespedes, C. L., Hoeneisen, M., Bittner, M., Beccerra, J., and Silva, M. 2001. Comparative study of ovatifolin antioxidant and growth inhibition activities. J. Agric. Food Chem 49:4243–4251.

    Article  PubMed  CAS  Google Scholar 

  • Cheng, H. H. 1995. Characterization of the mechanisms of allelopathy: modeling and experimental approaches. Amer. Chem. Soc. Symp. Ser 582:132–141.

    CAS  Google Scholar 

  • Courbat, P., Weith, A., Albert, A., and Pelter, A. 1977. Contribution to the study of the behavior of catechin in alkaline medium. Helv. Chim. Acta 60:1665–1675.

    Article  CAS  Google Scholar 

  • D’Abrosca, B., Della Greca, M., Fiorentino, A., Isidori, M., Manaco, P., and Pacifico, S. 2006. Chemical constituents of the aquatic plant Schoenoplectus lacustris: evaluation of phytotoxic effects on the green alga Selanastrum capricornutum. J. Chem. Ecol 32:81–96.

    Article  PubMed  CAS  Google Scholar 

  • Dayan, F. E., Duke, S. O., Sauldubois, A., Singh, N., McCurdy, C., and Cantrell, C. L. 2007. P-Hydroxyphenylpyruvate dioxygenase is a herbicidal target site for β-triketones from Leptospermum scoparium. Phytochemistry 68:2004–2014.

    Article  PubMed  CAS  Google Scholar 

  • Dayan, F. E., Romagni, J. G., and Duke, S. O. 2000. Investigating the mode of action of natural phytotoxins. J. Chem. Ecol 26:2079–2094.

    Article  CAS  Google Scholar 

  • Dayan, F. E., Watson, S. B., Galindo, J. C. G., Hernández, A., Dou, J., McChesney, J. D., and Duke, S. O. 1999. Phytotoxicity of quassinoids: physiological responses and structural requirements. Pestic. Biochem. Physiol 65:15–24.

    Article  CAS  Google Scholar 

  • Donovan, J. L., Crespy, V., Oliveira, M., Cooper, K. A., Gibson, B. B., and Williamson, G. 2006. (+)-Catechin is more bioavailable than (−)-catechin: relevance to the bioavailability of catechin from cocoa. Free Radical Res 40:1029–1034.

    Article  CAS  Google Scholar 

  • Duke, S. O., Williams, R. D., and Markhart, A. H. 1983. Interaction of moisture stress and three phenolic compounds on lettuce seed germination. Ann. Bot 52:923–926.

    CAS  Google Scholar 

  • Duke, S. O., Cedergreen, N., Velini, E. D., and Belz, R. G. 2006. Hormesis: Is it an important factor in herbicide use and allelopathy? Outlooks on Pest Manag 17:29–33.

    Google Scholar 

  • Duke, S. O., Wedge, D. E., Cerdeira, A. L., and Matallo, M. B. 2007. Interactions of synthetic herbicides with plant disease and microbial herbicides. pp 277–296 in Vurro M, Gressel J (eds) Novel Biotechnologies for Biocontrol Agent Enhancement and Management. Springer, Dordrecht, The Netherlands.

  • Furubayashi, A., Hiradate, S., and Fujii, Y. 2007. Role of catechol structure in the adsorption and transformation reactions of l-DOPA in soils. J. Chem. Ecol 33:239–250.

    Article  PubMed  CAS  Google Scholar 

  • Gamborg, O. L., Miller, R. A., and Ojima, K. 1968. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res 50:151–158.

    Article  PubMed  CAS  Google Scholar 

  • Gerig, T. M., Blum, U., and Meier, K. 1889. Statistical analysis of the joint inhibitory action of similar compounds. J. Chem. Ecol 15:2403–2412.

    Article  Google Scholar 

  • Hashida, K., Ohara, S., and Makino, R. 2003. Base-catalyzed reactions of (−)-epicatechin: Formation of enantiomers of base-catalyzed reaction products from (+)-catechin. J. Wood Chem. Technol 23:227–232.

    Article  CAS  Google Scholar 

  • Hiscox, J. D., and Israelstam, G. F. 1980. A method for the extraction of chlorophyll from leaf tissue without maceration. Can. J. Bot 57:1332–1334.

    Article  Google Scholar 

  • Ho, Y., Lee, Y. L., and Hsu, K. Y. 1995. Determination of (+)-catechin in plasma by high-performance liquid-chromatography using fluorescence detection. J. Chromatog. B- Biomed. Appl 665:383–389.

    Article  CAS  Google Scholar 

  • Hollman, P. C. H., van Trijp, J. M. P., Buysman, M. N. C. P., Gaag, M. S. v. d., Mengelers, M. J. B., de Vries, J. H. M., and Katan, M. B. 1997. Relative bioavailability of the antioxidant flavanoid quercetin from various foods in man. FEBS Lett 418:152–156.

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, C. R. M., and Vivanco, J. M. 2006. Can plant biochemistry contribute to understanding of invasion ecology? Trends Plant Sci 11:574–580.

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, P. J. L., Callaway, R. M., and Hoben, W. 2008. Phytotoxic effects of (±)-catechin In vitro, in soil, and in the field. PLoS ONE 3(7): e2536. doi:10.1371/journal.pone.0002536.

  • Jia, C., Kudsk, P., and Mathiassen, S. K. 2006. Joint action of benzoxazinone derivatives and phenolic acids. J. Agric. Food Chem 54:1049–1057.

    Article  PubMed  CAS  Google Scholar 

  • Kiatgrajai, P., Wellons, J. D., Gollob, L., and White, J. D. 1982. Kinetics of epimerization of (+)-catechin and its rearrangement to catechinic acid. J. Org. Chem 47:2910–2912.

    Article  CAS  Google Scholar 

  • Labrouche, F., Clark, A. C., Prenzler, P. D., and Scollary, G. R. 2005. Isomeric influence on the oxidative coloration of phenolic compounds in a model white wine: comparison of (+)-catechin and (–)-epicatechin. J.Agric. Food Chem 53:9993–9998.

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto, H., and Duke, S. O. 1990. Acifluorfen-methyl effects on porphyrin synthesis in intact Lemna pausicostata Hegelm. 6746 plants. J. Agric. Food Chem 38:2066–2071.

    Article  CAS  Google Scholar 

  • Michel, A., Johnson, R. D., Duke, S. O., and Scheffler, B. E. 2004. Dose-response relationships between herbicides with different modes of action and growth of Lemna paucicostata—an improved ecotoxicological method. Environ. Toxicol. Chem 23:1074–1079.

    Article  PubMed  CAS  Google Scholar 

  • Murashigi, T., and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15:473–497.

    Article  Google Scholar 

  • Perry, G. L., Thelen, G. C., Ridenour, W. M., Weir, T. L., Callaway, R. M., Pashke, M. W., and Vivanco, J. M. 2005. Dual role for an allelochemical: (±)-catechin from Centauria maculosa root exudates regulates conspecific seedling establishment. J. Ecol 93:1126–1135.

    Article  CAS  Google Scholar 

  • Perry, G. L., Thelen, G. C., Ridenour, W. M., Callaway, R. M., Paschke, M. V., and Vivanco, J. M. 2007. Concentrations of the allelochemical (±)-catechin in Centaurea maculosa soils. J. Chem. Ecol 33:2337–2344.

    Article  PubMed  CAS  Google Scholar 

  • Prithiviraj, B., Perry, G. L., Badri, D. V., and Vivanco, J. M. 2007. Chemical facilitation and induced pathogen resistance mediated by root-secreted phytotoxin. New Phytol 173:852–860.

    Article  PubMed  CAS  Google Scholar 

  • Ridenour, W. M., and Callaway, R. M. 2001. The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450.

    Article  Google Scholar 

  • Ritz, C., and Streibig, J. C. 2005. Bioassay Analysis using R. Journal of Statistical Software 12, 1-22. URL http://www.bioassay.dk.

  • R Development Core Team, 2005. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www. R-project.org. ISBN 3-900051-07-0.

  • Romeo, J. T. 2000. Raising the beam: moving beyond phytotoxicity. J. Chem. Ecol 26:2011–2014.

    Article  CAS  Google Scholar 

  • Simões, K., Du, J., Kretzschmar, F. S., Broekling, C. D., Stermitz, F. S., Vivanco, J. M., and Braga, M. R. 2008. Phytotoxic catechin leached by seeds of the tropical weed Sesbania virgata. J. Chem. Ecol 34:681–687.

    Article  PubMed  Google Scholar 

  • Tharayil, N., Bhowmik, P. C., and Xing, B. 2006. Preferential sorption of phenolic phytotoxins to soil: implications for altering the availability of allelochemicals. J. Agric. Food Chem 54:3033–3040.

    Article  PubMed  CAS  Google Scholar 

  • Tharayil, N., Bhowmik, P. C., and Xing, B. 2008. Bioavailability of allelochemicals as affected by companion compounds in soil matrices. J. Agric. Food Chem 56:3706–3713.

    Article  PubMed  CAS  Google Scholar 

  • Thelen, C. C., Vivanco, J. M., Newingham, B., Good, W., Bais, H. P., Landres, P., Caesar, A., and Callaway, R. M. 2005. Insect herbivory stimulates allelopathic exudation by an invasive plant and the suppression of natives. Ecol. Lett 8:209–217.

    Article  Google Scholar 

  • Veluri, R., Weir, T. L., Bais, H. P., Stermitz, F. R., and Vivanco, J. M. 2004. Phytotoxic and antimicrobial activities of catechin derivatives. J. Agric. Food Chem 52:1077–1082.

    Article  PubMed  CAS  Google Scholar 

  • Weir, T. L., Bais, H. P., and Vivanco, J. M. 2003. Intraspecific and interspecific interactions mediated by a phytotoxin (−)-catechin, secreted by the roots of. Centauria maculosa (spotted knapweed). J. Chem. Ecol 29:2397–2412.

    Article  PubMed  CAS  Google Scholar 

  • Weir, T. L., Bais, H. P., Stull, V. J., Callaway, R. M., Thelen, G. C., Redenhour, W. M., Bhamidi, S., Stermitz, F. R., and Vivanco, J. M. 2006. Oxalate contributes to the resistance of Gaillardia grandiflora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa. Planta 223:785–795.

    Article  PubMed  CAS  Google Scholar 

  • Weston, L. A., and Duke, S. O. 2003. Weed and crop allelopathy. Crit. Rev. Plant Sci 22:367–389.

    Article  CAS  Google Scholar 

  • Zhang, J., Stanley, R. A., Adaim, A., Melton, L. D., and Skinner, M. A. 2008. Free radical scavenging and cytoprotective activities of phenolic antioxidants. Molec. Nutrition Food Res 50:996–1005.

    Article  Google Scholar 

Download references

Acknowledgment

We thank C. Duncan for soil collections.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen O. Duke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duke, S.O., Blair, A.C., Dayan, F.E. et al. Is (−)-Catechin a Novel Weapon of Spotted Knapweed (Centaurea stoebe)?. J Chem Ecol 35, 141–153 (2009). https://doi.org/10.1007/s10886-008-9587-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-008-9587-z

Keywords

Navigation