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Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix

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Abstract

Trichoderma (T. asperellum-203, 44 and GH11; T. atroviride-IMI 206040 and T. harzianum-248) parasitism on Meloidogyne javanica life stages was examined in vitro. Conidium attachment and parasitism differed beween the fungi. Egg masses, their derived eggs and second-stage juveniles (J2) were parasitized by Trichoderma asperellum-203, 44, and T. atroviride following conidium attachment. Trichoderma asperellum-GH11 attached to the nematodes but exhibited reduced penetration, whereas growth of T. harzianum-248 attached to egg masses was inhibited. Only a few conidia of the different fungi were attached to eggs and J2s without gelatinous matrix; the eggs were penetrated and parasitized by few hyphae, while J2s were rarely parasitized by the fungi. The gelatinous matrix specifically induced J2 immobilization by T. asperellum-203, 44 and T. atroviride metabolites that immobilized the J2s. A constitutive-GFP-expressing T. asperellum-203 construct was used to visualize fungal penetration of the nematodes. Scanning electron microscopy revealed the formation of coiling and appressorium-like structures upon attachment and parasitism by T. asperellum-203 and T. atroviride. Gelatinous matrix agglutinated T. asperellum-203 and T. atroviride conidia, a process that was Ca2+-dependent. Conidium agglutination was inhibited by carbohydrates, including fucose, as was conidium attachment to the nematodes. All but T. harzianum could grow on the gelatinous matrix, which enhanced conidium germination. A biomimetic system based on gelatinous-matrix-coated nylon fibers demonstrated the role of the matrix in parasitism: T. asperellum-203 and T. atroviride conidia attached specifically to the gelatinous-matrix-coated fibers and parasitic growth patterns, such as coiling, branching and appressoria-like structures, were induced in both fungi, similarly to those observed during nematode parasitism. All Trichoderma isolates exhibited nematode biocontrol activity in pot experiments with tomato plants. Parasitic interactions were demonstrated in planta: females and egg masses dissected from tomato roots grown in T. asperellum-203-treated soil were examined and found to be parasitized by the fungus. This study demonstrates biocontrol activities of Trichoderma isolates and their parasitic capabilities on M. javanica, elucidating the importance of the gelatinous matrix in the fungal parasitism.

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Abbreviations

gm:

Gelatinous matrix

J2:

Second-stage juveniles

RKN:

Root-knot nematode

References

  • Barak, R., Elad, Y., & Chet, I. (1986). The properties of l-fucose-binding agglutinin associated with the cell wall of Rhizoctonia solani. Archives of Microbiology, 144, 346–349.

    Article  CAS  Google Scholar 

  • Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia, 91, 553–556.

    Article  CAS  Google Scholar 

  • Chet, I., Inbar, J., & Hadar, Y. (1997). Fungal antagonists and mycoparasitism. In D. T. Wicklow & B. Söderström (Eds.), The mycota. Volume IV: Environmental and microbial relationships (pp. 165–184). Berlin, Heidelberg: Springer-Verlag.

    Google Scholar 

  • Elad, Y., Barak, R., & Chet, I. (1983). Possible role of lectins in mycoparasitism. Journal of Bacteriology, 154, 1431–1435.

    PubMed  CAS  Google Scholar 

  • Flores, A., Chet, I., & Herrera-Estrella, A. (1997). Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1. Current Genetics, 31, 30–37.

    Article  PubMed  CAS  Google Scholar 

  • Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma spp.—opportunistic avirulent plant symbionts. Nature Microbiology Reviews, 2, 43–56.

    Article  CAS  Google Scholar 

  • Inbar, J., & Chet, I. (1992). Biomimics of fungal cell–cell recognition by use of lectin-coated nylon fibers. Journal of Bacteriology, 174, 1055–1059.

    PubMed  CAS  Google Scholar 

  • Inbar, J., & Chet, I. (1994). A newly isolated lectin from the plant pathogenic fungus Sclerotium rolfsii: purification, characterization, and its role in mycoparasitism. Microbiology, 140, 651–657.

    PubMed  CAS  Google Scholar 

  • Kerry, B. R., & Hominick, W. M. (2001). Biological control. In D. L. Lee (Ed.), Biology of nematodes (pp. 483–509). London: Taylor and Francis.

    Google Scholar 

  • Khan, A., Williams, K. L., & Nevalainen, H. K. M. (2004). Effects of Pacecilimyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biological Control, 31, 346–352.

    Article  CAS  Google Scholar 

  • Kok, C. J., Papert, A., & Hok-A-Hin, C. H. (2001). Microflora of Meloidogyne egg masses: species composition, population density and effect on the biocontrol agent Verticillium chlamydosporium (Goddard). Nematology, 3, 729–734.

    Article  Google Scholar 

  • Kullnig, C., Krupica, T., Woo, S. L., Mach, R.L., Rey, M., Benitez, T., Lorito, M., & Kubicek, C. P. (2001). Confusion abounds over identities of Trichoderma biocontrol isolates. Mycological Research, 105, 770–772.

    Article  Google Scholar 

  • Kubicek, C. P., Mach, R. L., Peterbauer, C. K., & Lorito, M. (2001). Trichoderma: From genes to biocontrol. Journal of Plant Pathology, 83, 11–23.

    CAS  Google Scholar 

  • Manzanilla-Lopez, R. H., Kenneth, E., & Bridge, J. (2004). Plant diseases caused by nematodes. In Z. X. Chen, S. Y. Chen & D. W. Dickson (Eds.), Nematology—advances and perspectives. Volume II: Nematode management and utilization (pp. 637–716). Cambridge, MA: CABI Publishing.

    Google Scholar 

  • Morton, C. O., Hirsch, P. R., & Kerry, B. (2004). Infection of plant-parasitic nematodes by nematophagous fungi—a review of application of molecular biology to understand infection processes and to improve biological control. Nematology, 6, 161–170.

    Article  CAS  Google Scholar 

  • Omero, C., Inbar, J., Rocha Ramirez, V., Herrera Estrella, A., Chet, I., & Horwitz, B. A. (1999). G protein activators and cAMP promote mycoparasitic behaviour in Trichoderma harzianum. Mycological Research 103, 1637–1642.

    Article  CAS  Google Scholar 

  • Orion, D., Kritzman, G., Meyer, S. L. F., Erbe, E. F., Chitwood, D. J. (2001). A role of the gelatinous matrix in the resistance of root-knot nematode (Meloidogyne spp.) eggs to microorganisms. Journal of Nematology 33, 203–207.

    PubMed  CAS  Google Scholar 

  • Rao, M. S., Reddy, P. P., & Nagesh, M. (1998). Evaluation of plant based formulations of Trichoderma harzianum for the management of Meloidogyne incognita on egg plant. Nematologia Mediterranea, 26, 59–62.

    Google Scholar 

  • Reddy, P. P., Rao, M. S., & Nagesh, M. (1996). Management of citrus nematode, Tylenchulus semipenetrans, by integration of Trichoderma harzianum with oil cakes. Nematologia Mediterranea., 24, 265–267.

    Google Scholar 

  • Rocha-Ramirez, V., Omero, C., Chet, I., Horwitz, B. A., & Herrera-Estrella, A. (2002). Trichoderma atroviride G-protein α-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryotic Cell, 1, 594–605.

    Article  PubMed  CAS  Google Scholar 

  • Saifullah, & Thomas, B. J. (1996). Studies on the parasitism of Globodera rostochiensis by Trichoderma harzianum using low temperature scanning electron microscopy. Afro-Asian Journal of Nematology, 6, 117–122.

    Google Scholar 

  • Samuels, G.J., Dodd, S.L., Gams, W., Castlebury, L.A., & Petrini, O. (2002). Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia, 94, 146–170.

    Article  Google Scholar 

  • Schirmböck, M., Lorito, M., Wong, Y.-L., Hayes, C. K., Arisan-Atac, I., Scala, F., Harman, G. E., & Kubicek, C. P. (1994). Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotic action of Trichoderma harzianum against phytopathogenic fungi. Applied and Environmental Microbiology, 60, 4364–4370.

    PubMed  Google Scholar 

  • Sharon, E., Bar-Eyal, M., Chet, I., Herrera-Estrella, A., Kleifeld, O., & Spiegel, Y. (2001). Biocontrol of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology, 91, 687–693.

    Article  PubMed  CAS  Google Scholar 

  • Sharon, E., Orion, D., & Spiegel, Y. (1993). Binding of soil microorganisms and red blood cells by the gelatinous matrix and eggs of Meloidogyne javanica and Rotylenchulus reniformis. Fundamental and Applied Nematology, 16, 5–9.

    Google Scholar 

  • Sharon, E., & Spiegel, Y. (1993). Glycoprotein characterization of the gelatinous matrix in the root-knot nematode Meloidogyne javanica. Journal of Nematology, 25, 585–589.

    CAS  PubMed  Google Scholar 

  • Sivan, A., Elad, Y., & Chet, I. (1984). Biological control effects of a new isolate of Trichoderma harzianum on Pythium aphanidermatum. Phytopathology, 74, 498–501.

    Article  Google Scholar 

  • Spiegel, Y., Inbar, J., Kahane, I., & Sharon, E. (1995). Carbohydrate-recognition domains on the surface of phytophagous nematodes. Experimental Parasitology, 80, 220–227.

    Article  PubMed  CAS  Google Scholar 

  • Spiegel, Y., & McClure, M. A. (1995). The surface coat of plant-parasitic nematodes: chemical composition, origin and biological role: A review. Journal of Nematology, 27, 127–134.

    PubMed  CAS  Google Scholar 

  • Spiegel Y., Sharon, E., Bar-Eyal, M., Van Assche, A., Van Kerckhove, S., Vanachter, A., Viterbo, A. & Chet, I. (2006). Evaluation and mode of action of Trichoderma isolates as a biocontrol agent against plant-parasitic nematodes. In Proceedings of IOBC Meeting, Spa, Belgium, IOBC Bulletin, in press.

  • Tikhonov, V. E., Lopez-Llorca, L.V., Salinas, J., & Jansson, H. B. (2002). Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V. suchlasporium. Fungal Genetics and Biology, 35, 67–78.

    Article  PubMed  CAS  Google Scholar 

  • Trudgill, D. L., & Blok, V. C. (2001). Apomictic, polyphagous root-knot nematodes: Exceptionally successful and damaging biotrophic root pathogens. Annual Review of Phytopathology, 39, 53–77.

    Article  PubMed  CAS  Google Scholar 

  • Windham, G. L., Windham, M. T., & Williams, W. P. (1989). Effects of Trichoderma spp. on maize growth and Meloidogyne arenaria reproduction. Plant Disease, 73, 493–494. .

    Article  Google Scholar 

  • Yedidia, I., Benhamou, N., & Chet, I. (1999). Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Applied and Environmental Microbiology, 65, 1061–1070.

    PubMed  CAS  Google Scholar 

  • Zeilinger, S., Reithner, B., Scala, V., Peissl, I., Lorito, M., & Mach, R. L. (2005). Signal transduction by Tga3, a novel G protein α subunit of Trichoderma atroviride. Applied and Environmental Microbiology, 71, 1591–1597.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Mr. Adnan Ismaiel (US Department of Agriculture, ARS, Systematic Botany and Mycology Laboratory, Beltsville, MD, USA) for providing fungal sequences. This work was kindly supported by the Dr. Eva Ehrlich memorial fund, Israel.

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Correspondence to Edna Sharon.

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Sharon, E., Chet, I., Viterbo, A. et al. Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur J Plant Pathol 118, 247–258 (2007). https://doi.org/10.1007/s10658-007-9140-x

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