Effects of plants containing pyrrolizidine alkaloids on the northern root-knot nematode Meloidogyne hapla

  • Tim C. ThodenEmail author
  • Johannes Hallmann
  • Michael Boppré


1,2-Dehydropyrrolizidine alkaloids (PAs), known to be nematotoxic in vitro, represent a class of secondary plant metabolites from hundreds of plant species worldwide. Pot experiments with the commercially available PA-containing plants Ageratum houstonianum, Borago officinalis, Senecio bicolor, and Symphytum officinalis demonstrate that Meloidogyne hapla is not per se repelled by these plants as all species were infested with nematodes. However, the development of M. hapla juveniles was completely suppressed on A. houstonianum and S. bicolor. Soil in which A. houstonianum and S. bicolor were cultivated and incorporated contained 200–400 times less nematodes than soil treated with Lycopersicon esculentum. Depending on their qualitative composition of PAs at least some of these plants thus appear to be valuable tools for integrated root-knot nematode management.


Biological control Integrated pest management (IPM) Secondary plant metabolites Soil amendment Green manure Botanicals Crotalaria spp. 



pyrrolizidine alkaloids = 1,2-dehydropyrrolizidines



We are most grateful to Tim Burzlaff and John Edgar for their valuable contributions, to R.I. Vane-Wright for critical revision of the English, to the staff of both the Forstzoologisches Institut and the Julius Kühn-Institut für Kulturpflanzen for technical assistance and to the Deutsche Bundesstiftung Umwelt for financial support. Further, we would like to thank S. Schlag for advice on statistical questions.


  1. Bandoniene, D., & Murkovic, M. (2002). The detection of radical scavenging compounds in crude extracts of borago (Borago officinalis L.) by using an on-line HPLC-DPPH method. Journal of Biochemical and Biophysical Methods, 53, 45–49.PubMedCrossRefGoogle Scholar
  2. Belair, G., & Benoit, D. L. (1996). Host suitability of 32 common weeds to Meloidogyne hapla in organic soils of southwestern Quebec. Journal of Nematology, 28, 643–647.PubMedGoogle Scholar
  3. Bernard, E. C., & Jennings, P. L. (1997). Host range and distribution of the clover root-knot nematode, Meloidogyne trifoliophila. Journal of Nematology, 294, 662–672.Google Scholar
  4. Brinkmann, H., Goosens, J. J. M., & van Riel, H. R. (1996). Comparative host suitability of selected crop plants to Meloidogyne chitwoodi Golden et al. 1980 and M. fallax Karssen 1996. Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz, 696, 127–129.CrossRefGoogle Scholar
  5. Byrd, D. W., Kirkpatrick, T., & Barker, K. R. (1983). An improved technique for clearing and staining plant tissue for detection of nematodes. Journal of Nematology, 15, 142–143.Google Scholar
  6. Chitwood, D. J. (2002). Phytochemical based strategies for nematode control. Annual Review of Phytopathology, 40, 221–249.PubMedCrossRefGoogle Scholar
  7. Costa, M. N., Oliveira, S., Coelho, S. J., & Campos, V. P. (2001). Nematodes in ornamental plant roots. Ciencia Agrotec, 255, 1127–1332.Google Scholar
  8. Dias, R. D., Schwan, A. V., Ezequiel, D. P., Sarmento, M. C., & Ferraz, S. (2000). Effect of aqueous extracts of some medical plants on the survival of Meloidogyne incognita juveniles. Nematologia Brasileira, 242, 203–210.Google Scholar
  9. Ehwaeti, M. E., Fargette, M., Phillips, M. S., & Trudgill, D. L. (1999). Host status differences and their relevance to damage by Meloidogyne incognita. Nematology, 1, 421–432.CrossRefGoogle Scholar
  10. Germani, G., & Plenchette, C. (2004). Potential of Crotalaria species as green manure crops for the management of pathogenic nematodes and beneficial mycorrhizal fungi. Plant and Soil, 266, 333–342.CrossRefGoogle Scholar
  11. Halbrendt, J. M. (1996). Allelopathy in the management of plant-parasitic nematodes. Journal of Nematology, 28, 8–14.PubMedGoogle Scholar
  12. Hallmann, J., Frankenberg, A., Paffrath, A., & Schmidt, H. (2007). Occurrence and importance of plant-parasitic nematodes in organic farming in Germany. Nematology, 9, 869–879.CrossRefGoogle Scholar
  13. Hooper, D. J., Hallmann, J., & Subbotin, S. A. (2005). Methods for extraction, processing and detection of plant and soil nematodes. In M. Luc, R. A. Sikora, & J. Bridge (Eds.), Plant parasitic nematodes in subtropical and tropical agriculture (p. 53–86, 2nd ed.). Wallingford: CABI.Google Scholar
  14. Hussey, R. S., & Barker, K. R. (1973). A comparison of methods of collecting inocula of Meloidogyne spp. including a new technique. Plant Disease Reporter, 57, 1025–1028.Google Scholar
  15. Kim, N. C., Oberlies, N. H., Brine, D. R., Handy, R. W., Wani, M. C., & Wall, M. E. (2001). Isolation of symlandine from the roots of common comfrey (Symphytum officinale) using countercurrent chromatography. Journal of Natural Products, 64, 251–253.PubMedCrossRefGoogle Scholar
  16. Larson, K. M., Roby, M. R., & Stermitz, F. R. (1984). Unsaturated pyrrolizidines from borage (Borago officinalis), a common garden herb. Journal of Natural Products, 47, 747–748.CrossRefGoogle Scholar
  17. Lazzeri, L., Curto, G., Leoni, O., & Dallavalle, E. (2004). Effects of glucosinolates and their enzymatic hydrolysis products via myrosinase on the root-knot nematode Meloidogyne incognita. Journal of Agricultural and Food Chemistry, 52, 6703–6707.PubMedCrossRefGoogle Scholar
  18. Lordello, A. I. L., & Lordello, R. R. A. (1996). Identification of Meloidogyne incognita races in some plants. Summa Phytopathologica, 221, 43–45.Google Scholar
  19. Mattocks, A. R. (1968). Toxicity of pyrrolizidine alkaloids. Nature, 217, 223–228.CrossRefGoogle Scholar
  20. McSorley, R., & Frederick, J. J. (1994). Response of some common annual bedding plants to three Species of Meloidogyne. Journal of Nematology, 26, 773–777.PubMedGoogle Scholar
  21. Molyneux, R. J., & Roitman, J. N. (1980). Specific detection of pyrrolizidine alkaloids on thin-layer chromatograms. Journal of Chromatography, 195, 412–415.CrossRefGoogle Scholar
  22. Moreno, J. E., Rich, J. R., French, E. C., Prine, G. M., & Dunn, R. A. (1992). Reactions of selected herbs to three Meloidogyne spp. Nematropica, 22, 217–225.Google Scholar
  23. Narberhaus, I., Zintgraf, V., & Dobler, S. (2005). Pyrrolizidine alkaloids on three trophic levels—evidence for toxic and deterrent effects on phytophages and predators. Chemoecology, 15, 121–125.CrossRefGoogle Scholar
  24. Ploeg, A. T. (2002). Effects of selected marigold varieties on root-knot nematodes and tomato and melon yields. Plant Disease, 86, 505–508.CrossRefGoogle Scholar
  25. Quijano, L., Calderon, J. S., Gomez, F., Escobar, E., & Rio, T. (1985). Octasubstituted flavones from Ageratum houstonianum. Phytochemistry, 24, 1085–1088.CrossRefGoogle Scholar
  26. Rizk, A. F. M. (1991). Naturally occurring pyrrolizidine alkaloids. Boca Raton: CRC.Google Scholar
  27. Thoden, T., Boppré, M., & Hallmann, J. (2007). Pyrrolizidine alkaloids of Chromolaena odorata act as nematicidal agents and reduce infection of lettuce roots by Meloidogyne incognita. Nematology, 9, 343–349.CrossRefGoogle Scholar
  28. Topp, E., Millar, S., Bork, H., & Welsh, M. (1998). Effects of marigold (Tagetes sp.) roots on soil microorganisms. Biology and Fertility of Soils, 27, 149–154.CrossRefGoogle Scholar
  29. Townshend, J. L., & Davidson, T. R. (1962). Some weed hosts of the northern root knot nematode Meloidogyne hapla in Ontario. Canadian Journal of Botany, 23, 543–548.CrossRefGoogle Scholar
  30. Walker, J. T., Melin, J. B., & Davis, J. (1994). Sensitivity of bedding plants to southern root-knot nematode, Meloidogyne incognita race 3. Journal of Nematology, 26, 778–781.PubMedGoogle Scholar
  31. Wang, K. H., Sipes, B. S., & Schmitt, D. P. (2002). Crotalaria as a cover crop for nematode management. Nematropica, 32, 35–57.Google Scholar
  32. Wiedenfeld, H., & Andrade-Cetto, A. (2001). Pyrrolizidine alkaloids from Ageratum houstonianum Mill. Phytochemistry, 57, 1269–1271.PubMedCrossRefGoogle Scholar
  33. Wiedenfeld, H., Montes, C., Tawil, B., Contin, A., & Wynsma, R. (2006). Pyrrolizidine alkaloid level in Senecio bicolor, ssp. cineraria from Middle Europe. Pharmazie, 616, 559–661.Google Scholar
  34. Wuyts, N., Swennen, R., & De Waele, D. (2006). Effects of phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of plant parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology, 8, 89–101.CrossRefGoogle Scholar
  35. Zasada, I. A., & Ferris, H. (2004). Nematode suppression with brassicaceous amendments: application based upon glucosinolate profiles. Soil Biology & Biochemistry, 36, 1017–1024.CrossRefGoogle Scholar
  36. Zeck, W. M. (1971). A rating scheme for field evaluation of root-knot nematode infestation. Pflanzenschutznachrichten Bayer, 24, 141–144.Google Scholar

Copyright information

© KNPV 2008

Authors and Affiliations

  • Tim C. Thoden
    • 1
    Email author
  • Johannes Hallmann
    • 2
  • Michael Boppré
    • 1
  1. 1.Forstzoologisches InstitutAlbert-Ludwigs-UniversitätFreiburg i.Br.Germany
  2. 2.Julius Kühn-Institut, Bundesforschungsinstitut für Kulturpflanzen, Institut für Epidemiologie und PathogendiagnostikMünsterGermany

Personalised recommendations