Introduction (Historical and Overview)

  • Ken Evans
  • Rosa H. Manzanilla-LópezEmail author
  • Luis V. Lopez-Llorca
Part of the Sustainability in Plant and Crop Protection book series (SUPP)


Biological control is an alternative to chemical control of plant-parasitic nematodes. This is largely due to public demand for biologically-based and environment-friendly management options for safer pest control. Such demands have had an important impact on biological control research expansion and funding. However, the development of any strain of a biological control agent for nematode control requires many years of research, experimentation, validation and safe-use tests before the biological control agent becomes available to farmers or is further developed by industry as a commercial biopesticide or bionematicide. Biological control potential can be unconstrained when biological control agents are used in combination with compatible integrated pest management tactics, which may include some chemical products and other biological control agent-based products that are currently available on the biopesticide market. This chapter presents part of the history behind some of the initial studies that help to illustrate the scientific work carried out by the many scientists who laid the foundations and helped to develop Pochonia chlamydosporia as a viable, sustainable alternative to chemical control in the integrated management of plant-parasitic nematodes.



The information of the MiCoSPa project outputs was kindly provided by Dr. Judith Pell.


  1. Barbosa, P. (1998). Agroecosystems and conservation biological control. In P. Barbosa (Ed.), Conservative Biological control (pp. 39–54). San Diego: Academic.CrossRefGoogle Scholar
  2. Barron, G. L. (1977). The nematode-destroying fungi, Topics in Mycobiology No. 1. Guelph: Canadian Biological Publications.Google Scholar
  3. Bordallo, J. J., Lopez-Llorca, L. V., Salinas, J., et al. (2002). Colonization of plant roots by egg-parasitic and nematode-trapping fungi. The New Phytologist, 154, 491–499.CrossRefGoogle Scholar
  4. Escudero, N., & Lopez-Llorca, L. V. (2012). Effects of plant growth and root-knot nematode infection of an endophytic GFP transformant on the nematophagous fungus Pochonia chlamydosporia. Symbiosis, 57, 33–42.CrossRefGoogle Scholar
  5. Escudero, N., Ferreira, S. R., Lopez-Moya, F., et al. (2016). Chitosan enhances parasitism of Meloidogyne javanica eggs by the nematophagous fungus Pochonia chlamydosporia. Fungal Biology, 120, 572–585.CrossRefPubMedGoogle Scholar
  6. Evans, K., & Manzanilla-López, R. (2017). The history of the nematology Department at Rothamsted. The Annals of Applied Biology, 170, 4–44.CrossRefGoogle Scholar
  7. Finetti-Sialer, M. M., & Manzanilla-López, R. H. (2011). Exploiting “-omics” and molecular approaches in plant nematology research. In R. Rodríguez-Herrera, C. N. Aguilar, J. K. Simpson-Williamson, et al. (Eds.), Phytopathology in the Omics Era, Transworld Research Network (pp. 39–68). Thiruvananthapuram: Research Signpost.Google Scholar
  8. Giné, A., Bonmati, M., Sarro, A., et al. (2016). Natural occurrence of fungal egg parasites of root-knot nematodes, Meloidogyne spp. in organic and integrated vegetable production systems in Spain. BioControl, 58, 407–416.CrossRefGoogle Scholar
  9. Gintis, B. O. G., Morgan-Jones, G., & Rodríguez-Kábana, R. (1982). Mycoflora of young cysts of Heterodera glycines in North Carolina soils. Nematropica, 12, 295–303.Google Scholar
  10. Gintis, B. O., Morgan-Jones, G., & Rodríguez-Kábana, R. (1983). Fungi associated with several developmental stages of Heterodera glycines from Alabama field soil. Nematropica, 13, 181–200.Google Scholar
  11. Godoy, G., Rodríguez-Kábana, R., & Morgan-Jones, G. (1982). Fungal parasites of Meloidogyne arenaria eggs in an Alabama soil. A mycological survey and greenhouse studies. Nematropica, 13, 201–213.Google Scholar
  12. Gowen, S. R. (2002). Integrated management of root-knot nematodes on vegetables in Kenya R 7472 (Za 0324). Final technical report (1 October 1999–30 September 2002). DFID R7472 Crop Protection Programme. Reading, UK, p. 52.Google Scholar
  13. Gowen, S. R. (2005). Promotion of sustainable approaches for the management of root-knot nematodes of vegetables in Kenya (R8296 (ZA 0568)). Crop protection programme. Final Report, DFID, p. 39.Google Scholar
  14. Hidalgo-Díaz, L. (2004) Registration of biological pesticides in Cuba. In M. N. Wabule, P. N. Ngaruiga, & F. K. Kimmins et al. (Eds.), Registration for biological control agents in Kenya, Proceedings of the Pest Control Products Board/Kenya/Agricultural Research Institute/Department for International Development Crop Protection Programme Workshop, Nakuru, Kenya, 14–16 May 2003. KARI/PCPB, Nairobi, Kenya, and Natural Resources International Ltd., Aylesford, UK, pp. 117–133Google Scholar
  15. Jacobs, H., Gray, S. N., & Crump, D. H. (2003). Interactions between nematophagous fungi and consequences for their potential as biological agents for the control of potato cyst nematodes. Mycological Research, 107, 47–56.CrossRefPubMedGoogle Scholar
  16. Kerry, B. R. (1991). Preface. In B. R. Kerry, & D. H. Crump (Eds.), Methods for studying nematophagous fungi. Working group “Integrated control of soil pests” (pp. I–II). IOBC/WPRS/Bulletin XIV/2.Google Scholar
  17. Kerry, B. R. (2000). Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annual Review of Phytopathology, 38, 423–441.CrossRefPubMedGoogle Scholar
  18. Kerry, B. R., & Bourne, J. (2002). A manual for research on Verticillium chlamydosporium a potential biocontrol agent for root-knot nematodes. Gent: IOBC/WPRS.Google Scholar
  19. Kerry B. R., & Crump D. H. (1991). Methods for studying nematophagous fungi. IOBC/WPRS Bulletin XIV (2).Google Scholar
  20. Larriba, E., Jaime, M. D. L. A., Carbonell-Caballero, J., et al. (2014). Sequencing and functional analysis of the genome of a nematode egg-parasitic fungus, Pochonia chlamydosporia. Fungal Genetics and Biology, 65, 69–80.CrossRefPubMedGoogle Scholar
  21. Larriba, E., Jaime, M. D. L. A., Nislow, C., et al. (2015). Endophytic colonization of barley (Hordeum vulgare) roots by the nematophagous fungus Pochonia chlamydosporia reveals plant growth promotion and a general defense and stress transcriptomic response. Journal of Plant Research. doi: 10.1007/s10265-015-0731-x.
  22. Lin, R., Liu, C., Shen, B., et al. (2015). Analysis of the complete mitochondrial genome of Pochonia chlamydosporia suggests a close relationship to the invertebrate-pathogenic fungi in Hypocreales. BMC Microbiology, 15, 5.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lopez-Llorca, L. V. (1990). Purification and properties of extracellular proteases produced by the nematophagous fungus Verticillium suchlasporium. Canadian Journal of Microbiology, 36, 530–537.CrossRefGoogle Scholar
  24. Lopez-Llorca, L. V., & Claugher, D. (1990). Appressoria of the nematophagous fungus Verticillium suchlasporium. Micron and Microscopica Acta, 21, 125–130.CrossRefGoogle Scholar
  25. Lopez-Llorca, L. V., & Fry, S. C. (1989). Dityrosine and tetratyrosine, potential croos-links in proteins of plant parasitic nematodes. Nematologica, 35, 165–179.CrossRefGoogle Scholar
  26. Lopez-Llorca, L. V., & Robertson, W. M. (1992a). Ultrastructure of infection of cyst nematode eggs by the nematophagous fungus Verticillium suchlasporium. Nematologica, 39, 65–74.CrossRefGoogle Scholar
  27. Lopez-Llorca, L. V., & Robertson, W. (1992b). Immunocytochemical localization of a 32 kDa protease from the nematophagous fungus Verticillium suchlasporium in infected nematode eggs. Experimental Mycology, 16, 261–267.CrossRefGoogle Scholar
  28. Lopez-Llorca, L. V., Maciá-Vicente, J. G., & Jansson, H. B. (2008). Mode of action and interactions of nematophagous fungi. In A. Ciancio & K. G. Mukerji (Eds.), Integrated management and biocontrol of vegetable and grains crops Nematodes (pp. 51–76). Heidelberg: Springer.Google Scholar
  29. Maciá-Vicente, J. G., Jansson, H. B., Talbot, N. J., et al. (2009). Real-time PCR quantification and live-cell imaging of endophytic colonization of barley (Hordeum vulgare) roots by Fusarium equiseti and Pochonia chlamydosporia. The New Phytologist, 182, 213–228.CrossRefPubMedGoogle Scholar
  30. Manzanilla-López, R. H., Esteves, I., Finetti-Sialer, M. M., et al. (2013). Pochonia chlamydosporia: Advances and challenges to improve its performance as a biological control agent of sedentary endo-parasitic nematodes. Journal of Nematology, 45, 1–7.PubMedPubMedCentralGoogle Scholar
  31. Monfort, E., Lopez-Llorca, L. V., Jansson, H. B., et al. (2005). Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaeumannomyces graminis var. tritici and development of root-rot. Soil Biology and Biochemistry, 37, 129–1235.CrossRefGoogle Scholar
  32. Morgan-Jones, G., & Rodríguez-Kábana, R. (1981). Fungi associated with cysts of Heterodera glycines in an Alabama soil. Nematropica, 11, 69–74.Google Scholar
  33. Morgan-Jones, G., & Rodriguez-Kabana, R. (1987). Fungal biocontrol for the management of nematodes. In J. A. Veech & D. W. Dickson (Eds.), Vistas on Nematology: A commemoration of the twenty-fifth anniversary of the Society of Nematologists (pp. 94–99). De Leon Springs: E.O. Painter Printing.Google Scholar
  34. Morgan-Jones, G., Godoy, G., & Rodríguez-Kábana, R. (1981a). Verticillium chlamydosporium, fungal parasite of Meloidogyne arenaria females. Nematropica, 11, 115–119.Google Scholar
  35. Morgan-Jones, G., Gintis, B. O., & Rodríguez-Kábana, R. (1981b). Fungal colonization of Heterodera glycines cysts in Arkansas, Florida, Mississippi and Missouri soils. Nematropica, 11, 155–163.Google Scholar
  36. Morgan-Jones, G., White, J. F., & Rodríguez-Kábana, R. (1983). Phytonematode pathology; ultrastructural studies. I. Parasitism of Meloidogyne arenaria eggs by Verticillium chlamydosporium. Nematropica, 13, 245–260.Google Scholar
  37. Morton, C. O., Hirsch, P. R., Peberdy, J. P., et al. (2003). Cloning of and genetic variation in protease VCP1 from the nematophagous fungus Pochonia chlamydosporia. Mycological Research, 107, 38–46.CrossRefPubMedGoogle Scholar
  38. Pérez-Rodríguez, I., Doroteo-Mendoza, A., Franco-Navarro, F., et al. (2007). Isolates of Pochonia chlamydosporia var. chlamydosporia from Mexico as potential biological control agents of Nacobbus aberrans. Nematropica, 37, 127–134.Google Scholar
  39. Pyrowolakis, A., Westphal, A., Sikora, R. A., et al. (2002). Identification of root-knot nematode suppressive soils. Applied Soil Ecology, 19, 51–56.CrossRefGoogle Scholar
  40. Rodríguez-Kábana, R., Morgan-Jones, G., Godoy, G., et al. (1984). Effectiveness of species of Gliocladium, Paecilomyces and Verticillium for control of Meloidogyne arenaria in field soil. Nematropica, 14, 155–170.Google Scholar
  41. Segers, R., Butt, T. M., Keen, J. N., et al. (1995). The subtilisins of the invertebrate mycopathogens Verticillium chlamydosporium and Metarhizium anisopliae are serologically and functionally related. FEMS Microbiology Letters, 126, 227–232.CrossRefPubMedGoogle Scholar
  42. Sellitto, V. M., Curto, G., Dallavalle, E., et al. (2016). Effect of Pochonia chlamydosporia-based formulates on the regulation of root-knot nematodes and plant growth response. Frontiers in Life Science, 9(3), 177–181. Scholar
  43. Stirling, G. R. (1991). Biological control of plant parasitic nematodes: Progress, problems and prospects. Wallingford: CABI Publishing.Google Scholar
  44. Stirling, G. R. (2014). Biological control of plant-parasitic nematodes: Soil ecosystem management in sustainable agriculture (2nd ed.). Croydon: CABI.Google Scholar
  45. Timper, P. (2014). Conserving and enhancing biological control of nematodes. Journal of Nematology, 46, 75–89.PubMedPubMedCentralGoogle Scholar
  46. Tobin, J. D., Haydock, P. P. J., Hare, M. C., et al. (2008). The compatibility of the fungicide azoxistrobin with Pochonia chlamydosporia, a biological control agent for potato cyst nematodes (Globodera spp.) The Annals of Applied Biology, 152, 301–305.CrossRefGoogle Scholar
  47. Verdejo-Lucas, S., Ornat, C., Sorribas, F. J., & Stchiegel, A. (2002). Species of root-knot nematodes and fungal egg parasites recovered from vegetables in Almería and Barcelona, Spain. Journal of Nematology, 34, 405–408.PubMedPubMedCentralGoogle Scholar
  48. Ward, E., Kerry, B. R., Manzanilla-López, R. H., et al. (2012). The Pochonia chlamydosporia serine protease gene vcp1 is subject to regulation by carbon, nitrogen and pH: Implications for nematode biocontrol. PLoS One, 7(4), e35657.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Westphal, A., & Becker, J. O. (1999). Biological suppression and natural population decline of Heterodera schachtii in a California field. Phytopathology, 89, 434–440.CrossRefPubMedGoogle Scholar
  50. Westphal, A., & Becker, J. O. (2000). Transfer of biological soil suppressiveness against Heterodera schachtii. Phytopathology, 90, 401–406.CrossRefPubMedGoogle Scholar
  51. Westphal, A., & Becker, J. O. (2001). Components of soil suppressiveness against Heterodera schachtii. Soil Biology and Biochemistry, 33, 9–16.CrossRefGoogle Scholar
  52. Zavala-Gonzalez, E. A., Escudero, N., Lopez-Moya, F., et al. (2015). Some isolates of the nematophagous fungus Pochonia chlamydosporia promote root growth and reduce flowering time of tomato. The Annals of Applied Biology, 166, 472–483.CrossRefGoogle Scholar
  53. Zavala-González, E. A., Rodríguez-Cazorla, E., Escudero, N., et al. (2017). Arabidopsis thaliana root colonization by the nematophagous fungus Pochonia chlamydosporia is modulated by jasmonate signalling and leads to accelerated flowering and improved yield. The New Phytologist, 213, 351–364.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Ken Evans
    • 1
  • Rosa H. Manzanilla-López
    • 2
    Email author
  • Luis V. Lopez-Llorca
    • 3
  1. 1.Formerly at Rothamsted ResearchHarpendenUK
  2. 2.Centro de Desarrollo de Productos Bióticos (Visiting Professor)YautepecMexico
  3. 3.Laboratory of Plant Pathology, Multidisciplinary Institute for Environmental Studies (MIES) Ramón Margalef, Department of Marine Sciences and Applied BiologyUniversity of AlicanteAlicanteSpain

Personalised recommendations