Skip to main content Accessibility help
×
Home
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 4
  • Print publication year: 2007
  • Online publication date: October 2013

17 - Fungal parasites of invertebrates: multimodal biocontrol agents?

from V - Fungal biocontrol of pests

Summary

Introduction

Nematophagous and entomopathogenic fungi (NEF) comprise an important group of fungal parasites of invertebrates (FPI). NEF belong to a wide range of fungal taxa, but most of them are anamorphic fungi and facultative parasites. These fungi can infect, kill and digest nematodes and insects, respectively, which we will call their canonical, or normal, hosts. These hosts have barriers to the environment (eggshells and cuticles) that have common structural features. Therefore, the infection cycles share common strategies (e.g. adhesion to the host) or metabolites (e.g. proteases and chitinases for host penetration). Some species (e.g. Lecanicillium lecanii) can even be isolated from both infected nematodes and insects. The NEF may also infect other organisms (other fungi and plants) apart from their canonical hosts in a similar or different mode. We will use the term multimodal to describe the mode of action of these biological activities (Fig. 17.1). However, to date, the main emphasis in research has covered their mode of action on their canonical hosts (e.g. nematodes for nematophagous fungi). Many of these fungi are used for biological control of plant-parasitic organisms.

In this review we will describe the NEF and their hosts in general terms (both canonical and non-canonical) at biological, ecological and physiological-molecular levels. We will also analyze the reasons for this multitrophic behaviour, trying to use a comparative approach of both types of hosts (canonical and non-canonical) and pathogens (nematophagous and entomopathogenic fungi) under an evolutionary perspective.

References
Åhman, J., Ek, B., Rask, L. & Tunlid, A. (1996). Sequence analysis and regulation of a gene encoding a cuticle-degrading serine protease from the nematophagous fungus Arthrobotrys oligospora. Microbiology, 142, 1605–16.
Ahrén, D., Ursing, B. M. & Tunlid, A. (1998). Phylogeny of nematode trapping fungi based on 18S rDNA sequences. FEMS Microbiology Letters, 158, 179–84.
Altre, J. A. & Vanderberg, J. D. (2001). Penetration of cuticle and proliferation in hemolymph by Paecilomyces fumosoroseus isolates that differ in virulence against lepidopteran larvae. Journal of Invertebrate Pathology, 78, 81–6.
Andersen, S. O. (1979). Biochemistry of insect cuticle. Annual Review of Entomology, 24, 29–61.
Asensio, L. (2004). Control biologic de plagues i malalties de palmeres per fongs entomopatógens. Ph.D. thesis, University of Alicante, Alicante, Spain.
Asensio, L., Lopez-Llorca, L. V. & Lopez-Jiménez, J. A. (2005). Use of light, scanning electron microscopy and bioassays to evaluate paratism by entomopathogenic fungi of the red scale insect of palms (Phoenicococcus marlatti Ckll., 1899). Micron, 36, 169–75.
Azevedo, J. L., Maccheroni, W., Pereira, J. O. & Araujo, W. L. (2000). Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electronic Journal of Biotechnology, 3, 40–65.
Barron, G. L. (1977). The Nematode-Destroying Fungi. Topics in Mycobiology No. 1. Guelph: Canadian Biological Publications Ltd.
Barron, G. L. (1992). Ligninolytic and cellulolytic fungi as predators and parasites. In The Fungal Community: Its Organisation and Role in the Ecosystem, eds. Carroll, G. C. & Wicklow, T. D.. New York: Marcel Dekker, pp. 311–26.
Benhamou, N. (2004). Potential of the mycoparasite, Verticillium lecanii, to protect citrus fruit against Penicillium digitatum, the causal agent of green mold: a comparison with the effect of chitosan. Phytopathology, 94, 693–705.
Benhanou, N. & Brodeur, J. (2001) Pre-inoculation of Ri T-DNA transformed cucumber roots with the mycoparasite, Verticillium lecanii, induces host defence reactions against Pythium ultimum infection. Physiological and Molecular Plant Pathology, 58, 133–46.
Bidochka, M. J., Kamp, A. M. & de Croos, A. (2000). Insect pathogenic fungi: from genes to populations. In Fungal Pathology, ed. Kronstad, J. W.. Dordrecht: Kluwer, pp. 171–93.
Bidochka, M. J., St. Leger, R. J., Stuart, A. & Gowanlock, K. (1999). Nuclear rDNA phylogeny in the fungal genus Verticillium and its relationship to insect and plant virulence, extracellular proteases and carbohydrates. Microbiology, 145, 955–63.
Bing, L. A. & Lewis, L. C. (1991). Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environmental Entomology, 20, 1207–11.
Bing, L. A. & Lewis, L. C. (1993). Occurrence of the entomopathogen Beauveria bassiana (Balsamo) Vuillemin in different tillage regimes and in Zea mays L. and virulence towards Ostrinia nubilalis (Hübner). Agriculture, Ecosystems and Environment, 45, 147–56.
Bird, A. F. (1985). The nature of the adhesion of Corynebacterium rathayi to the cuticle of the infective larva of Anguina agrostis. International Journal of Parasitology, 15, 301–8.
Bird, A. F. & Bird, J. (1991). The Structure of Nematodes. San Diego: Academic Press.
Bordallo, J. J., Lopez-Llorca, L. V., Jansson, H.-B., Salinas, J., Persmark, L., Asensio, L. (2002). Effects of egg-parasitic and nematode-trapping fungi on plant roots. New Phytologist, 154, 491–9.
Boucias, D. G. & Pendland, J. C. (1998). Entomopathogenic fungi: fungi imperfecti. In Principles of Insect Pathology, eds. Boucias, D. G. & Pendland, J. C.. Dordrecht: Kluwer, pp. 321–64.
Burges, H. D. (1998). Formulation of mycoinsecticides. In Formulation of Microbial Pesticides. Beneficial Microorganisms, Nematodes and Seed Treatment, ed. Burges, H. D.. Dordrecht: Kluwer, pp. 131–85.
Butt, T. M. (2002). Use of entomogenous fungi for the control of insect pests. In The Mycota XI: Agricultural Applications, ed. Kempken, F.. Berlin: Springer-Verlag, pp. 111–34.
Charnley, A. K. (1997). Entomopathogenic fungi and their role in pest control. In The Mycota IV: Environmental and Microbial Relationships, eds. Wicklow, T. D. & Söderström, B.. Berlin: Springer-Verlag, pp. 185–201.
Charnley, A. K. (2003). Fungal pathogens of insects: cuticle degrading enzymes and toxins. Advances in Botanical Research, 40, 241–321.
Charnley, A. K. & St. Leger, R. J. (1991). The role of cuticle degrading enzymes in fungal pathogenesis of insects. In Fungal Spore and Disease Initiation in Plants and Animals, eds. Cole, G. T. & Hoch, H. C.. London: Plenum Press, pp. 129–56.
Chen, S. Y., Dickson, D. W. & Mitchell, D. J. (1996). Pathogenicity of fungi to eggs of Heterodera glycines. Journal of Nematology, 28, 148–58.
Clarke, A. J., Cox, P. M. & Shepherd, A. M. (1967). The chemical composition of the egg shells of the potato cyst-nematode, Heterodera rostochiensis Woll. Biochemical Journal, 104, 1056–60.
Clarkson, J. M., Scree, S., Bailey, A., Cob, B. & Charnley, K. (1998). Fungal pathogenesis in insects. In Molecular Variability of Fungal Pathogens, eds. Bridge, P. D., Couteaudier, Y. & Clarkson, J. M.. Wallingford: CAB International, pp. 83–94.
De Nobel, H., Sietsma, J. H., van den Ende, H. & Klis, F. M. (2001). Molecular organization and construction of the fungal cell wall. In The Mycota VIII: Biology of the Fungal Cell Wall, eds. Howard, R. J. & Gow, N. A. R.. Berlin: Springer-Verlag, pp. 181–200.
Dijksterhuis, J., Veenhuis, M. & Harder, W. (1990). Ultrastructural study of adhesion and initial stages of infection of nematodes by conidia of Drechmeria coniospora. Mycological Research, 94, 1–8.
Domsch, K. H., Gams, W. & Anderson, T-H. (1993). Compendium of Soil Fungi, Vol. 1. Eching, Germany: IHW-Verlag.
Dupont, A., Segers, R. & Coosemans, J. (2002). The effect of chitinase from Verticillium chlamydosporium on the egg of Meloidogyne incognita. Mededelingen Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent, 64, 383–9.
Fry, S. C. (2001). Plant cell walls. Encyclopedia of life sciences. Nature Publishing Group/www.els.net.
Gams, W. & Zare, R. (2001). A revision of Verticillium sect. Prostrata. III. Generic classification. Nova Hedwigia, 72, 329–37.
Gómez-Vidal, S., Lopez-Llorca, L. V., Jansson, H.-B. & Salinas, J. (2006). Endophytic colonization of date palm (Phoenix dactylifera L.) leaves by entomopathogenic fungi. Micron, 37, 624–32.
Hagedorn, G. & Scholler, M. (1999). A reevaluation of predatory orbiliaceous fungi. I. Phylogenetic analysis using rDNA sequence data. Sydowia, 51, 27–48.
Hajek, A. E. & St. Leger, R. J. (1994). Interactions between fungal pathogens and insect hosts. Annual Review of Entomology, 39, 293–322.
Hu, G. & St. Leger, R. J. (2002). Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Applied and Environmental Microbiology, 68, 6383–7.
Inglis, G. D., Goettel, M. S., Butt, T. M. & Strasser, H. (2001). Use of hyphomycetous fungi for managing insect pests. In Fungi as Biocontrol Agents: Progress, Problems and Potential, eds. Butt, T. M., Jackson, C. & Magan, N.. Wallingford: CABI Publishing, pp. 23–69.
Inyang, E. N., Butt, T. M., Beckett, A. & Archer, S. (1999). The effect of crucifer epicuticular waxes and leaf extracts of the germination and virulence of Metarhizium anisopliae conidia. Mycological Research, 103, 419–26.
Jansson, H.-B. (1993). Adhesion to nematodes of conidia from the nematophagous fungus Drechmeria coniospora. Journal of General Microbiology, 139, 1899–906.
Jansson, H.-B., Hofsten, A. V. & Mecklenburg, C. V. (1984). Life cycle of the endoparasitic nematophagous fungus Meria coniospora: a light and electron microscopic study. Antonie van Leeuwenhoek, 50, 321–7.
Jansson, H.-B. & Lopez-Llorca, L. V. (2001). Biology of nematophagous fungi. In Trichomyces and Other Fungal Groups, eds. Misra, J. K. & Horn, B. W.. Enfield: Science Publishers, pp. 145–73.
Jansson, H.-B. & Lopez-Llorca, L. V. (2004). Control of nematodes by fungi. In Fungal Biotechnology in Agriculture, Food, and Environmental Applications, ed. Arora, D. K.. New York: Marcel Dekker, pp. 205–15.
Jansson, H.-B. & Nordbring-Hertz, B. (1979). Attraction of nematodes to living mycelium of nematophagous fungi. Journal of General Microbiology, 112, 89–93.
Jansson, H.-B. & Nordbring-Hertz, B. (1988). Infection events in the fungus-nematode system. In Diseases of Nematodes, Volume 2, eds. Poinar, G. O. & Jansson, H.-B.. Boca Raton: CRC Press, pp. 59–72.
Jansson, H.-B., Tunlid, A., & Nordbring-Hertz, B. (1997). Nematodes. In Fungal Biotechnology, ed. Anke, T.. Weinheim: Chapman & Hall, pp. 38–50.
Kavková, M. & Curn, V. (2005). Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) as a potential mycoparasite on Sphaerotheca fuliginea (Ascomycotina: Erysiphales). Mycopathologia, 159, 53–63.
Kerry, B. R. & Jaffee, B. A. (1997). Fungi as biological control agents for plant parasitic nematodes. In The Mycota, eds. Esser, K. & Lemke, P. A.. Berlin: Springer-Verlag, pp. 204–18.
Leinhos, G. M. E. & Buchenauer, H. (1992). Hyperparasitism of selected fungi on rust fungi of cereal. Journal of Plant Disease and Protection, 99, 482–98.
Lecuona, R. (1996). Control microbiano, utopia o realidad. In Microorganismos Patógenos Empleados en el Control de Insectos Plaga, ed. Leucona, E.. Buenos Aires: Talleres Gráficos Mariano Mas, pp. 13–16.
Lodge, D. J., Fisher, P. J. & Sutton, B. C. (1996). Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia, 88, 733–8.
Lopez-Llorca, L. V. (1990a). Purification and properties of extracellular proteases produced by the nematophagous fungus Verticillium suchlasporium. Canadian Journal of Microbiology, 36, 530–7.
Lopez-Llorca, L. V. (1992b). Coleóptero radicícola infectado por el hongo entomopatógeno Beauveria Bassiana. Boletín de la Sociedad Micológica de Madrid, 17, 13–17.
Lopez-Llorca, L. V. & Boag, B. (1993). A contribution to the ecology of fungi associated with female and cysts of the cereal cyst nematode Heterodera avenae in Eastern Scotland. Nematologica Mediterranea, 21, 187–97.
Lopez-Llorca, L. V., Bordallo, J. J., Salinas, J., Monfort, E. & Lopez-Serna, M. L. (2002a). Use of light and scanning electron microscopy to examine colonisation of barley rhizosphere by the nematophagous fungus Verticillium chlamydosporium. Micron, 33, 61–7.
Lopez-Llorca, L. V. & Carbonell, T. (1998). Use of almond mesocarp for production of the entomopathogenic fungus Verticillium Lecanii. Canadian Journal of Microbiology, 44, 886–95.
Lopez-Llorca, L. V., Carbonell, T. & Gomez-Vidal, S. (2002). Degradation of insect cuticle by Proteases of Paecilomyces farinosus. Mycological Progress, 1, 249–56.
Lopez-Llorca, L. V., Carbonell, T. & Salinas, J. (1999). Colonization of plant waste substrates by entomopathogenic and mycoparasitic fungi – a SEM study. Micron, 30, 325–33.
Lopez-Llorca, L. V. & Claugher, D. (1990). Appressoria of the nematophagous fungus Verticillium suchlasporium. Micron and Microscopica Acta, 21, 125–30.
Lopez-Llorca, L. V. & Fry, S. C. (1989). Dityrosine, trityrosine and tetratyrosine, potential cross-links in proteins of plant parasitic nematodes. Nematologica, 35, 165–79.
Lopez-Llorca, L. V., Jansson, H.-B., Maciá Vicente, J. G. & Salinas, J. (2006). Nematophagous fungi as root endophytes. In Soil Biology, Volume 9. Microbial Root Endophytes, eds. Schulz, B., Boyle, C. & Sieber, T. N.. Berlin: Springer Verlag, pp. 191–206.
Lopez-Llorca, L. V., Olivares-Bernabeu, C., Salinas, J., Jansson, H.-B. & Kolattukudy, P. E. (2002b). Pre-penetration events in fungal parasitism of nematode eggs. Mycological Research, 106, 499–506.
Lopez-Llorca, L. V. & Robertson, W. (1992a). Ultrastructure of infection of cyst nematode eggs by the nematophagous fungus Verticillium suchlasporium. Nematologica, 39, 65–74.
Lopez-Llorca, L. V. & Robertson, W. M. (1992b). Immunocytochemical localization of a 32-kDa protease from the nematophagous fungus Verticillium suchlasporium in infected nematode eggs. Experimental Mycology, 16, 261–7.
López Serna, M. L. (2004). Interrelaciones entre hongos patógenos de invertebrados: hongos nematófagos y hongos entomopathógenos. Ph.D. thesis, University of Alicante, Alicante, Spain.
Meyer, S. L. F., Roberts, D. P. & Wergin, W. P. (1998). Association of the plant-beneficial fungus Verticillium lecanii with soybean roots and rhizosphere. Journal of Nematology, 30, 451–60.
Monfort, E. (2004). Interacciones tróficas entre hongos nematófagos, la rizosfera y sus patógenos fúngicos. Ph.D. thesis, University of Alicante, Alicante, Spain.
Monfort, E., Lopez-Llorca, L. V., Jansson, H.-B., Salinas, J., Park, J. O. & Sivasithamparam, K. (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, 1229–35.
Morgan-Jones, G. & Rodrigues-Kábana, R. (1988). Fungi colonising cysts and eggs. In Diseases of Nematodes, Volume 2, eds. Poinar, G. O. & Jansson, H.-B.. Boca Raton: CRC Press, pp. 39–58.
Morton, C. O., Hirsch, P. R. & Kerry, B. R. (2004). Infection of plant-parasitic nematodes by nematophagous fungi – a review of the application of molecular biology to understand infection processes and improve biological control. Nematology, 6, 161–70.
Nicholson, R. L. (1996). Adhesion of fungal propagules. In Histology, Ultrastructure and Molecular Cytology of Plant–Microorganism Interactions, eds. Nicole, M. and Gianinazzi-Pearson, V.. Amsterdam: Kluwer, pp. 117–34.
Nordbring-Hertz, B. & Mattiasson, B. (1979). Action of a nematode-trapping fungus shows lectin-mediated host-microorganism interaction. Nature, 281, 477–9.
Nordbring-Hertz, B. & Stålhammar-Carlemalm, M. (1978). Capture of nematodes by Arthrobotrys oligospora, an electron microscopic study. Canadian Journal of Botany, 56, 1297–307.
Obroník, M., Jirku, M. & Dolezel, D. (2001). Phylogeny of mitosporic entomopathogenic fungi: is there a genus Paecilomyces polyphletic?Canadian Journal of Microbiology, 47, 813–19.
Obroník, M., Klic, M. & Zizka, L. (2000). Genetic variability and phylogeny inferred from random amplified polymorphic DNA data reflect life strategy of entomopathogenic fungi. Canadian Journal of Botany, 78, 1150–5.
Olivares-Bernabeu, C. & Lopez-Llorca, L. V. (2002). Fungal egg-parasites of plant-parasitic nematodes from Spanish soils. Revista Iberoamericana de Micología, 19, 104–10.
Persson, C., Olsson, S. & Jansson, H.-B. (2000). Growth of Arthrobotrys superba from a birch wood food base into soil determined by radioactive tracing. FEMS Microbiology Ecology, 31, 47–51.
Persson, Y., Veenhuis, M. & Nordbring-Hertz, B. (1985). Morphogenesis and significance of hyphal coiling by nematode-trapping fungi in mycoparasitic relationships. FEMS Microbiology Ecology, 31, 283–91.
Pfister, D. H. (1997). Castor, Pollux and life histories of predacious hyphomycetes. Mycologia, 89, 1–23.
Schulz, B., Boyle, C., Draeger, S., Römmert, A. & Krohn, K. (2002). Endophytic fungi: a source of novel biologically active secondary metabolites. Mycological Research, 106, 996–1004.
Segers, R., Butt, T. M., Carder, J. H., Keen, J. N., Kerry, B. R. & Perderby, J. F. (1999). The subtilisins of fungal pathogens of inscects, nematodes and plants: distribution and variation. Mycological Research, 103, 395–402.
Segers, R., Butt, T. M., Keen, J. N., Kerry, B. R. & Peberdy, J. F. (1995). The subtilisins of the invertebrate mycopathogens Verticillium chlamydosporium and Metarhizium anisopliae are serologically and functionally related. FEMS Microbiology Letters, 126, 227–32.
Segers, R., Butt, T. M., Kerry, B. R. & Peberdy, J. F. (1994). The nematophagous fungus Verticillium chlamydosporium Goddard produces a chymoelastase-like protease which hydrolyses host nematode proteins in situ. Microbiology, 140, 2715–23.
Shimizu, S., Tsuchitani, Y. & Matsumoto, T. (1993). Serology and substrate specificity of extracellular proteases from four species of entomopathogenic hyphomycetes. Journal of Invertebrate Pathology, 61, 192–5.
Sneh, B., Humble, S. J. & Lockwood, J. L. (1977). Parasitism of oospores of Phytophthora megasperma var. sojae, P. cactorum, Pythium, and Aphanomyces euteiches by oomycetes, chytridomycetes, hyphomycetes, actinomycetes and bacteria. Phytopathology, 67, 622–8.
St. Leger, R. J. (1993). Biology and mechanisms of insect-cuticle invasion by deuteromycete fungal pathogens. In Parasites and Pathogens of Insects. Volume 2: Pathogens, eds. Beckage, M. E., Federici, B. A. & Thompson, S. N.. New York: Academic Press, pp. 211–29.
St. Leger, , Butt, R. J., Goettel, T. M., Staples, M. S., , R. C. & Roberts, D. W. (1989). Production in vitro of appressoria by the entomopathogenic fungus Metarhizium anisopliae. Experimental Mycology, 13, 273–88.
St. Leger, , Joshi, R. J., , L. & Roberts, D. W. (1997). Adaptation of proteases and carbohydrases of saprophytic, pathogenic and entomopathogenic fungi to the requirements of their ecological niches. Microbiology, 143, 1983–92.
Tanada, Y. & Kaya, H. K. (1993). Insect Pathology. San Diego: Academic Press.
Thorn, R. G. & Barron, G. L. (1984). Carnivorous mushrooms. Science, 224, 76–8
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.
Tunlid, A., Jansson, H.-B. & Nordbring-Hertz, B. (1992). Fungal attachment to nematodes. Mycological Research, 96, 401–12.
Tunlid, A. & Talbot, N. J. (2002). Genomics of parasitic and symbiotic fungi. Current Opinion in Microbiology, 5, 513–19.
Varma, A., Verma, S., Sudha, , Sahay, N., Bütehorn, B. & Franken, P. (1999). Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Applied and Environmental Microbiology, 65, 2741–4.
Veenhuis, M., Nordbring-Hertz, B. & Harder, W. (1985). An electron microscopical analysis of capture and initial stages of penetration of nematodes by Arthrobotrys oligospora. Antonie van Leeuwenhoek, 51, 385–98.
Verdejo-Lucas, S., Ornat, C., Sorribas, F. J. & Stchiegel, A. (2002). Species of root-knot nematodes and fungal egg parasites recovered from vegetables in Almeria and Barcelona, Spain. Journal of Nematology, 34, 405–8.
Verdejo-Lucas, S., Sorribas, F. J., Ornat, C. & Galeano, M. (2003). Evaluating Pochonia chlamydosporia in a double-cropping system of lettuce and tomato in plastic houses infested with Meloidogyne javanica. Plant Pathology, 52, 521–8.
Verhaar, M. A., Hijwegen, T. & Zadoks, J. C. (1998). Selection of Verticillium lecanii isolates with high potential for biological control of cucumber powdery mildew by means of component analysis at different humidity regimes. Biocontrol Science and Technology, 8, 465–77.
Wagner, B. L. & Lewis, L. C. (2000). Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology, 66, 3468–73.
Walsh, T. J. & Groll, A. H. (1999). Emerging fungal pathogens: evolving challenges to immunocompromised patients for the tweny-first century. Transplant Infectious Disease, 1, 247–61.
Wharton, D. A. (1980). Nematode egg-shells. Parasitology, 81, 447–63.
Zare, R. & Gams, W. (2001). A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia, 73, 1–50.