Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-06T05:07:32.141Z Has data issue: false hasContentIssue false

17 - Fungal parasites of invertebrates: multimodal biocontrol agents?

from V - Fungal biocontrol of pests

Published online by Cambridge University Press:  05 October 2013

By
L. V. Lopez-Llorca  and
H.-B. Jansson
Edited by
G. D. Robson ,
Pieter van West  and
Geoffrey Gadd
L. V. Lopez-Llorca
Affiliation:
Department of Marine Sciences and Applied Biology University of Alicante Apartado 99 E-03080 Alicante Spain
H.-B. Jansson
Affiliation:
Department of Marine Sciences and Applied Biology University of Alicante Apartado 99 E-03080 Alicante Spain
G. D. Robson
Affiliation:
University of Manchester
Pieter van West
Affiliation:
University of Aberdeen
Geoffrey Gadd
Affiliation:
University of Dundee
Get access

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.

Type
Chapter
Information
Exploitation of Fungi , pp. 310 - 335
Publisher: Cambridge University Press
Print publication year: 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

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.CrossRefGoogle ScholarPubMed
Ahrén, D., Ursing, B. M. & Tunlid, A. (1998). Phylogeny of nematode trapping fungi based on 18S rDNA sequences. FEMS Microbiology Letters, 158, 179–84.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Andersen, S. O. (1979). Biochemistry of insect cuticle. Annual Review of Entomology, 24, 29–61.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Barron, G. L. (1977). The Nematode-Destroying Fungi. Topics in Mycobiology No. 1. Guelph: Canadian Biological Publications Ltd.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Bird, A. F. & Bird, J. (1991). The Structure of Nematodes. San Diego: Academic Press.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
Charnley, A. K. (2003). Fungal pathogens of insects: cuticle degrading enzymes and toxins. Advances in Botanical Research, 40, 241–321.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Chen, S. Y., Dickson, D. W. & Mitchell, D. J. (1996). Pathogenicity of fungi to eggs of Heterodera glycines. Journal of Nematology, 28, 148–58.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Domsch, K. H., Gams, W. & Anderson, T-H. (1993). Compendium of Soil Fungi, Vol. 1. Eching, Germany: IHW-Verlag.Google Scholar
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.Google Scholar
Fry, S. C. (2001). Plant cell walls. Encyclopedia of life sciences. Nature Publishing Group/www.els.net.Google Scholar
Gams, W. & Zare, R. (2001). A revision of Verticillium sect. Prostrata. III. Generic classification. Nova Hedwigia, 72, 329–37.Google Scholar
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.CrossRefGoogle ScholarPubMed
Hagedorn, G. & Scholler, M. (1999). A reevaluation of predatory orbiliaceous fungi. I. Phylogenetic analysis using rDNA sequence data. Sydowia, 51, 27–48.Google Scholar
Hajek, A. E. & St. Leger, R. J. (1994). Interactions between fungal pathogens and insect hosts. Annual Review of Entomology, 39, 293–322.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Jansson, H.-B. (1993). Adhesion to nematodes of conidia from the nematophagous fungus Drechmeria coniospora. Journal of General Microbiology, 139, 1899–906.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
Jansson, H.-B. & Nordbring-Hertz, B. (1979). Attraction of nematodes to living mycelium of nematophagous fungi. Journal of General Microbiology, 112, 89–93.CrossRefGoogle Scholar
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.Google Scholar
Jansson, H.-B., Tunlid, A., & Nordbring-Hertz, B. (1997). Nematodes. In Fungal Biotechnology, ed. Anke, T.. Weinheim: Chapman & Hall, pp. 38–50.Google Scholar
Kavková, M. & Curn, V. (2005). Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) as a potential mycoparasite on Sphaerotheca fuliginea (Ascomycotina: Erysiphales). Mycopathologia, 159, 53–63.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Lodge, D. J., Fisher, P. J. & Sutton, B. C. (1996). Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia, 88, 733–8.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Lopez-Llorca, L. V. (1992b). Coleóptero radicícola infectado por el hongo entomopatógeno Beauveria Bassiana. Boletín de la Sociedad Micológica de Madrid, 17, 13–17.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Lopez-Llorca, L. V., Carbonell, T. & Gomez-Vidal, S. (2002). Degradation of insect cuticle by Proteases of Paecilomyces farinosus. Mycological Progress, 1, 249–56.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Lopez-Llorca, L. V. & Claugher, D. (1990). Appressoria of the nematophagous fungus Verticillium suchlasporium. Micron and Microscopica Acta, 21, 125–30.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Lopez-Llorca, L. V. & Robertson, W. (1992a). Ultrastructure of infection of cyst nematode eggs by the nematophagous fungus Verticillium suchlasporium. Nematologica, 39, 65–74.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Nordbring-Hertz, B. & Mattiasson, B. (1979). Action of a nematode-trapping fungus shows lectin-mediated host-microorganism interaction. Nature, 281, 477–9.CrossRefGoogle Scholar
Nordbring-Hertz, B. & Stålhammar-Carlemalm, M. (1978). Capture of nematodes by Arthrobotrys oligospora, an electron microscopic study. Canadian Journal of Botany, 56, 1297–307.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Pfister, D. H. (1997). Castor, Pollux and life histories of predacious hyphomycetes. Mycologia, 89, 1–23.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Tanada, Y. & Kaya, H. K. (1993). Insect Pathology. San Diego: Academic Press.Google Scholar
Thorn, R. G. & Barron, G. L. (1984). Carnivorous mushrooms. Science, 224, 76–8CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Tunlid, A., Jansson, H.-B. & Nordbring-Hertz, B. (1992). Fungal attachment to nematodes. Mycological Research, 96, 401–12.CrossRefGoogle Scholar
Tunlid, A. & Talbot, N. J. (2002). Genomics of parasitic and symbiotic fungi. Current Opinion in Microbiology, 5, 513–19.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Wharton, D. A. (1980). Nematode egg-shells. Parasitology, 81, 447–63.CrossRefGoogle ScholarPubMed
Zare, R. & Gams, W. (2001). A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia, 73, 1–50.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×