European Journal of Plant Pathology

, Volume 137, Issue 2, pp 295–304 | Cite as

Nematicidal potential of Artemisia annua and its main metabolites

  • Trifone D’Addabbo
  • Teresa Carbonara
  • Maria Pia Argentieri
  • Vincenzo Radicci
  • Paola Leonetti
  • Luciano Villanova
  • Pinarosa Avato


Nematotoxic effect of an aqueous extract of Artemisia annua and its components caffeic acid, chlorogenic acid (5-caffeoylquinic acid, 5-CQA), artemisinin and the related semi-synthetic artesunate, was investigated on the root-knot nematode Meloidogyne incognita and the potato cyst nematode Globodera rostochiensis and on the virus-vector dagger nematode Xiphinema index. Juveniles of M. incognita and G. rostochiensis and females of X. index were exposed to 500, 250 and 125 μl ml−1 solutions of the A. annua aqueous extract, caffeic acid, chlorogenic acid and artesunate and to 50 μl ml−1 solution of artemisinin for 2, 4, 8 and 24 h. Egg masses of M. incognita and cysts of G. rostochiensis were exposed for 24, 48, 96 h and 1 or 2 weeks only to the extract solutions. Aqueous extract was highly effective on G. rostochiensis juveniles, whereas M. incognita juveniles were affected only at long exposure times. Adversely, egg hatch inhibition was strong on M. incognita and poor or minimal on G. rostochiensis. Females of X. index were sensitive only to long exposures to the highest extract concentration. Both caffeic and chlorogenic acid did not affect juveniles of M. incognita but were highly active on G. rostochiensis juveniles and X. index females even at the lowest concentration. Artesunate toxicity was almost zero on M. incognita and low on X. index females, but high on G. rostochiensis juveniles. Artemisinin solution was lethal to more than 50 % of G. rostochiensis juveniles within 24 h, but did not affect M. incognita juveniles and X. index females. Results suggest different roles of the tested compounds in the biocidal activity on each target nematode species. The extract of A. annua and its main phytochemicals seem to have a potential to be developed into new nematicidal formulates, though their activity should be validated in the soil.


Artemisia annua Artemisinin Artesunate Chlorogenic acids Nematicides Meloidogyne incognita Xiphinema index Globodera rostochiensis 



This research was financially supported by Regione Puglia under “Progetto Strategico CIP PS_070”. T. Carbonara acknowledges Regione Puglia for financial support in a form of a grant. The Authors are also grateful to Dr. F. Grasso and Dr. M. Scarcella (CRA-Istituto Sperimentale per i Tabacchi, Monteroni, Lecce) for valuable assistance to grow A. annua plants. Thanks are also due to Prof. F.P. Fanizzi (University of Salento, Lecce) for valuable discussion.


  1. Akhtar, M., & Malik, A. (2000). Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresource Technology, 74, 35–47.CrossRefGoogle Scholar
  2. Al-Banna, L., Darwish, R. M., & Aburjai, T. (2003). Effect of plant extracts and essential oils on root-knot nematode. Phytophathogia Mediterranea, 42, 123–128.Google Scholar
  3. Argentieri, M. P., D’Addabbo, T., Tava, A., Agostinelli, A., Jurzysta, M., & Avato, P. (2008). Evaluation of nematicidal properties of saponins from Medicago spp. European Journal of Plant Pathology, 120, 189–197.CrossRefGoogle Scholar
  4. Balint, G. B. (2001). Artemisinin and its derivatives. An important new class of antimalarial agents. Pharmacology & Therapeutics, 90, 261–265.CrossRefGoogle Scholar
  5. Bhakuni, R. S., Jain, D. C., Sharma, R. P., & Kumar, S. (2001). Secondary metabolites of Artemisia annua and their biological activity. Current Science, 80, 35–48.Google Scholar
  6. Carbonara, T., Pascale, R., Argentieri, M. P., Papadia, P., Fanizzi, F. P., Villanova, L., & Avato, P. (2012). Phytochemical analysis of a herbal tea from Artemisia annua L. Journal of Pharmaceutical and Biomedical Analysis, 62, 79–86.PubMedCrossRefGoogle Scholar
  7. Chitwood, D. J. (2002). Phytochemical based strategies for nematode control. Annual Review of Phytopathology, 40, 221–249.PubMedCrossRefGoogle Scholar
  8. Clarke, A. J., & Shepherd, A. M. (1968). Hatching agents for the potato cyst-nematode, Heterodera rostochiensis Woll. Annals of Applied Biology, 61, 139–149.CrossRefGoogle Scholar
  9. D’Addabbo, T., Avato, P., & Tava, A. (2009). Nematicidal potential of materials from Medicago spp. European Journal of Plant Pathology, 125, 39–49.CrossRefGoogle Scholar
  10. D’Addabbo, T., Carbonara, T., Leonetti, P., Radicci, V., Tava, A., & Avato, P. (2011). Control of parasitic nematodes with active saponins and biomass from Medicago sativa. Phytochemistry Reviews, 10, 503–519.CrossRefGoogle Scholar
  11. Davies, K. G., & Curtis, R. H. C. (2011). Cuticle surface coat of plant-parasitic nematodes. Annual Review of Phytopathology, 49, 135–156.PubMedCrossRefGoogle Scholar
  12. De Donno, A., Grassi, T., Idolo, A., Guido, M., Papadia, P., Caccioppola, A., Villanova, L., Merendino, A., Bagordo, F., & Fanizzi, F. P. (2012). First-time comparison of the in vitro antimalarial activity of Artemisia anna herbal tea and artemisinin. Transactions of the Royal Society of Tropical Medicine and Hygiene. doi: 10.1016/j.trstmh.2012.07.008.PubMedGoogle Scholar
  13. Dias, C. R., Schwan, A. V., Ezequiel, D. P., Sarmento, M. C., & Ferraz, S. (2000). Efeito de extractos aquosos de plantas medicinais na sobrevivencia de juvenis de Meloidogyne incognita. Nematologia Brasileira, 24, 203–210.Google Scholar
  14. Ferreira, J.F.S., Ritchey, K.D., Cassida, K.L., Turner, K.E., Gonzalez, J.M. (2006). Agrotechnological aspects of the antimalarial plant Artemisia annua and its potential use in animal health in Appalachia. Revue des Régions Arides, 797–804Google Scholar
  15. Ferris, H., & Zheng, L. J. (1999). Plant sources of Chinese herbal remedies: effects on Pratylenchus vulnus and Meloidogyne javanica. Journal of Nematology, 31, 241–263.PubMedGoogle Scholar
  16. Finney, D. J. (1978). Statistical method in biological assay. Statistical method in biological assay. London: Griffin.Google Scholar
  17. Hooper, D. J., Hallmann, J., & Subbotin, S. A. (2005). Methods for extraction, processing and detection of plant and soil nematodes. In Sikora & Bridge (Ed.), Plant parasitic nematodes in subtropical and tropical agriculture (pp. 53–86). Wallingford, UK: CAB International.CrossRefGoogle Scholar
  18. 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
  19. Hynes, R. K., & Boyetchko, S. M. (2006). Research initiatives in the art and science of biopesticide formulations. Soil Biology and Biochemistry, 38, 845–849.CrossRefGoogle Scholar
  20. Korayem, A. M., Hasabo, S. A., & Ameen, H. H. (1993). Effects and mode of action of some plant extracts on certain plant-parasitic nematodes. Journal of Pest Science, 66, 32–36.Google Scholar
  21. Krishna, S., Uhlemann, A.-C., & Haynes, R. K. (2004). Artemisinins: their growing importance in medicine. Drug Resistance Update, 7, 233–244.CrossRefGoogle Scholar
  22. Krishna, S., Bustamante, L., Haynes, R. K., & Staines, H. M. (2008). Artemisinins: mechanisms of action and potential for resistance. Trends in Pharmacological Science, 29, 520–527.CrossRefGoogle Scholar
  23. Li, Y., Huang, H., Wu, Y-L. (2000). Qinghaosu (Artemisinin)—A fantastic antimalarial drug from a traditional Chinese medicine. In Liang & Fang (Eds.), Medicinal chemistry of bioactive natural products. Wiley, pp. 183–256.Google Scholar
  24. Marco, J.A., Barbera, O. (1990). Natural products from the genus Artemisia L. In Atta-ur-Rahman (Ed.), Studies in natural products chemistry. Wiley & Sons, pp. 201–263.Google Scholar
  25. Marinova, E. M., Toneva, A., & Yanishlieva, N. (2009). Comparison of the antioxidative properties of caffeic and chlorogenic acids. Food Chemistry, 114, 1498–1502.CrossRefGoogle Scholar
  26. Meshnick, S. R. (2002). Artemisinin: mechanisms of action, resistance and toxicity. International Journal of Parasitolology, 32, 1655–1660.CrossRefGoogle Scholar
  27. Ntalli, N. G., & Caboni, P. (2012). Botanical nematicides: a review. Journal of food and agricultural chemistry, 60, 9929–9940.CrossRefGoogle Scholar
  28. O’Neill, P. M., Barton, V. E., & Ward, S. A. (2010). The molecular mechanism of action of artemisinin—The debate continues. Molecules, 15, 1705–1721.PubMedCrossRefGoogle Scholar
  29. Pandey, R. (1990). Studies on phytonematotoxic properties in the extract of some medicinal and aromatic plants. International Nematology Network Newsletter, 7, 19–20.Google Scholar
  30. Perry, R. N., & Moens, M. (2011). Introduction to plant-parasitic nematodes; modes of parasitism. Genomics and Molecular Genetics of Plant-Nematode Interactions, 3–20.Google Scholar
  31. Regulation EC No 1095/2007 of the European Parliament and of the Council of Europe.
  32. Regulation EC No 396/2005 of the European Parliament and of the Council of Europe. Scholar
  33. Sato, Y., Itagaki, S., Kurokawa, T., Ogura, J., Kobayashi, M., Hirano, T., Sugawara, M., & Iseki, K. (2011). In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. International Journal of Pharmacology, 403, 136–138.CrossRefGoogle Scholar
  34. Seinhorst, J. W., & den Ouden, H. (1966). An improvement of Bijloo’s Method for determining the egg content of Heterodera Cysts. Nematologica, 12, 170–171.CrossRefGoogle Scholar
  35. Shakil, N. A., Prasad, D., Saxena, D. B., & Gupta, A. K. (2004). Nematicidal activity of essential oils of Artemisia annua against root-knot and reniform nematodes. Annals of Plant Protection Sciences, 12, 403–408.Google Scholar
  36. Tan, R. X., Zhang, W. F., & Tang, H. Q. (1998). Biologically active substances from the genus Artemisia. Planta Medica, 64, 293–302.CrossRefGoogle Scholar
  37. Trudgill, D. L., & Blok, V. C. (2001). Apomistic, polyphagus root-knot nematode. Annual Review of Phytopathology, 39, 53–77.PubMedCrossRefGoogle Scholar
  38. Turner, S. J., & Evans, K. (1998). The origin, global distribution and biology of potato cyst nematodes (Globodera rostochiensis Woll. and Globodera pallida Stone). In R. J. Marks & B. B. Brodie (Eds.), Potato cyst nematodes—biology, distribution and control (pp. 7–26). Wallingford, UK: CAB International.Google Scholar
  39. UNEP, United Nations Environment Programme. (2000). The Montreal protocol on substances that deplete the ozone layer.Google Scholar
  40. van Zyl, S., Vivier, M. A., & Walker, M. A. (2012). Xiphinema index and its relationship to grapevines: a review. South African Journal of Enology and Viticulture, 33(1).Google Scholar
  41. Willcox, M., Bodeker, G., Bourdy, G., Dhingra, V., Falquet, J., Ferreira, J. F. S., Graz, B., Hirt, H.-M., Hsu, E., de Magalhães, P. M., Provendier, D., & Wright, C. W. (2004). Artemisia annua as a traditional herbal antimalarial. In M. L. Willcox, G. Bodeker, & P. Rasoanaivo (Eds.), Traditional medicinal plants and malaria (pp. 43–59). Boca Raton, FL: CRC Press.Google Scholar
  42. Yeats, G. W., Bongers, T., De Goede, R. G. M., Freckman, D. W., & Georgieva, S. S. (1993). Feeding habits in soil nematode families and genera—An outline for soil ecologists. Journal of Nematology, 25, 315–331.Google Scholar

Copyright information

© KNPV 2013

Authors and Affiliations

  • Trifone D’Addabbo
    • 2
  • Teresa Carbonara
    • 1
  • Maria Pia Argentieri
    • 1
  • Vincenzo Radicci
    • 2
  • Paola Leonetti
    • 2
  • Luciano Villanova
    • 3
  • Pinarosa Avato
    • 1
  1. 1.Dipartimento di Farmacia-Scienze del FarmacoUniversitá degli Studi di Bari Aldo MoroBariItaly
  2. 2.Istituto per la Protezione delle PianteCNRBariItaly
  3. 3.LACHIFARMA s.r.l.ZollinoItaly

Personalised recommendations