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DEGENERATION OF ENTOMOGENOUS FUNGI

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An Ecological and Societal Approach to Biological Control

Part of the book series: Progress in Biological Control ((PIBC,volume 2))

Abstract

Fungi are notorious for losing virulence and changing their morphology when successively subcultured on artificial media. Various terms have been used to describe this phenomenon including phenotypic degeneration, phenotypic instability, phenotypic deterioration, dual phenomenon, saltation and attenuation (Butt, 2002; Kawakami, 1960; Nagaich, 1973; Ibrahim et al., 2002; Ryan et al., 2001). Morphological changes include a change in colour, and growth form as well as reduced sporulation. In this article, the term degenerate is used to cover both attenuation of virulence and phenotypic degeneration. Degenerate cultures are a major concern to manufacturers of fungal biocontrol agents (BCAs) since batches that are inconsistent in spore yield or virulence will make the product commercially unviable. Growers naturally would be reluctant to use any product, which was potentially unstable.

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References

  • Ahn, I-P. & Lee, Y-H. (2001). A viral double-stranded RNA up regulates the fungal virulence of Nectria radicicola. Molecular Plant-Microbe Interactions. 14: 496–507.

    PubMed  CAS  Google Scholar 

  • Akamatsu H, Taga M, Kodama M, Johnson R, Otani H, & Kohmoto K. (1999) Molecular karyotypes for Alternaria plant pathogens known to produce host-specific toxins. Curr. Genet. 35: 647–656.

    Article  PubMed  CAS  Google Scholar 

  • Aizawa, K. (1971). Strain improvement and preservation of virulence, pp 666–668. In H.D. Burges & N.W. Hussey (eds). Microbial control of insects and mites. Academic Press, London, NY.

    Google Scholar 

  • Altre, J. A., Vandenberg, J. D. and Cantone, F. A. (1999). Pathogenicity of Paecilomyces fumosoroseus Isolates to Diamondback Moth, Plutella xylostella: Correlation with Spore Size, Germination Speed, and Attachment to Cuticle. J. Invert. Pathol., 73: 332–338.

    Article  CAS  Google Scholar 

  • Brownbridge, M., Costa, S. and Jaronski, S. T. (2001). Effects of in vitro passage of Beauveria bassiana on virulence of Bemisia argentifolii. J. Invertebr. Pathol. 77: 280–283.

    Article  PubMed  CAS  Google Scholar 

  • Butt, T. M. & Goettel, M. (2000). Bioassays of Entomopathogenic fungi. In: Bioassays of Entomopathogenic microbes and nematodes (ed. Navon, A. and Ascher, K.R.S.) CAB International, Wallingford, Oxon, U.K. Chapter 4. 141–195.

    Google Scholar 

  • Butt, T.M., Hajek, A. E., & Humber, R. A. (1996). Gypsy moth immune defenses in response to hyphal bodies and natural protoplasts of entomophthoralean fungi. J. Invert. Pathol. 68: 278–285.

    Article  Google Scholar 

  • Castro, M., Kramer, K., Valdivia, L., Ortiz, S. & Castillo, A. (2003). A double-stranded RNA mycovirus confers hypovirulence-associated traits to Botrytis cinerea FEMS Microbiology Letters 228: 87–91.

    Article  PubMed  CAS  Google Scholar 

  • Cooper, R.D. & Sweeney, A. W. (1986). Laboratory studies on the recycling potential of the mosquito pathogenic fungus Culincomyces clavisporus. J. Invert. Pathol. 48: 152–158.

    Article  CAS  Google Scholar 

  • Chu, Y.M., Jeon, J.J., Yea, S. J., Kim, Y. H., Yun, S-H., Lee, Y. W. & Kim, K. H. (2002). Double-Stranded RNA Mycovirus from Fusarium graminearum Applied and Environmental Microbiology, 68: 2529–2534.

    Article  PubMed  CAS  Google Scholar 

  • Daboussi, M J. & Langin T (1994) Transposable elements in fungal plant pathogen Fusarium oxysporum. Genetica 93: 49–59.

    Article  CAS  Google Scholar 

  • Dumas, J.L. & Papierok, B. (1989). Virulence de l'entomophthorale Zoophthora radicans (Zygomycetes) a l'égard des adultes de Aedes aegyptii (Dipt. Culicdae). Entomophaga 34: 321–330.

    Article  Google Scholar 

  • Fargues, J. F. & Robert, P. H. (1983). Effect of passaging through scarabaeid hosts on the virulence and host specificity of two strains of the entomopathogenic hyphomycete Metarhizium anisopliae. Canadian Journal of Microbiology 29: 575–583.

    Article  Google Scholar 

  • Fowler, T. J. & Mitton, M. F. (2000). Scooter, a new active transposan in Schizophyllum commune, has disrupted two gene regulating signal transduction. Genetics, 156: 1585–1594.

    PubMed  CAS  Google Scholar 

  • Franzot, S., Mukherjee, J., Cherniak, R., Chen, L., Hamdan, J., & Casadevall, A. (1998). Microevolution of standard strain of Cryptococcus neoformans resulting in differences in virulence and other phenotypes. Infect. Immun. 66: 89–97.

    PubMed  CAS  Google Scholar 

  • Frazzon, A.P.G., da Silva Vaz Junior, L, Masuda, A., Schrank, A. & Vainstein, M.H. (2000). In vitro assessment of Metarhizium anisopliae isolates to control the cattle tick Boophilus microplus. Veterinary Parasitology 94: 117–125.

    Article  PubMed  CAS  Google Scholar 

  • Fries, B.C., Goldman, D.L., Cherniak, R. Ju, R. & Casadevall, A. (1999). Phenotypic Switching in Cryptococcus neoformans Results in Changes in Cellular Morphology and Glucuronoxylomannan Structure. Infection and immunity 67: 6076–6083.

    PubMed  CAS  Google Scholar 

  • Gimenez-Pecci, M., Bogo, M R., Santi, L., Kriger de Moraes, C., Correa, C. T., Vainstein, M.H. & Schrank, A. (2002). Characterization of Mycoviruses and Analyses of Chitinase Secretion in the Biocontrol Fungus Metarhizium anisopliae. Current Microbiology 45: 334–339.

    Article  CAS  Google Scholar 

  • Goettel, M.S. (1987). Serial in vivo passage of the entomopathogenic hyphomycete Tolypocladium cylindrosporum in mosquitoes. Canadian Entomologist 119: 599–601.

    Article  Google Scholar 

  • Hall, R.A., (1980). Effect of repeated subculturing on agar and passaging through an insect host on pathogenicity, morphology, and growth rate of Verticillium lecanii. J. Invertebate. Pathology. 36: 216–222.

    Article  Google Scholar 

  • Han, Y., Liu, X., Benny, U., Kistler, H.C., & VanEtten, H.D. (2001) Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J. 25: 305–314.

    Article  PubMed  CAS  Google Scholar 

  • Hajek, A. E., Humber, R.A. & Griggs, M.H. (1990). Decline in Virulence of Entomophaga maimaiga (Zygomycetes: Entomophthorales) with repeated in vitro Subculture. Journal of Invertebr. Pathol. 56: 91–97.

    Article  Google Scholar 

  • Hartman, G. C. & Wasti, S. S. (1974). Infection of the gypsy moth, Porthetria dispar with the entomogenous fungus, Conidiobolus coronatus. Entomophaga 19: 353–360.

    Article  Google Scholar 

  • Hatta, R., Ito, K., Hosaki, Y., Tanaka, T., Tanaka, A., Yamamoto, M., Akimitsu, K. & Tsuge, T. (2002). A Conditionally Dispensable Chromosome Controls Host-Specific Pathogenicity in the Fungal Plant Pathogen Alternaria alternata. Genetics 161: 59–70.

    PubMed  CAS  Google Scholar 

  • Hayden, T.P., Bidochka, M.J. & Khachatourians, G.G., (1992). Entomopathogenicity of several fungi toward the English grain aphid (Homoptera: Aphididae) and enhancement of virulence with host passage of Paecilomyces farinosus. J. Econ. Entomol. 85, pp. 58–64.

    Google Scholar 

  • Horgen, P.A., Carvalho, D., Sonnenberg, A., Li, A., & van Griensven, L. J. L. D. (1996). Chromosomal abnormalities associated with strain degeneration in the cultivated mushroom Agaricus bisporus. Fungal Genet. Biol. 20: 229–241.

    Article  CAS  Google Scholar 

  • Ibrahim, L. Butt, T. M. & Jenkinson, P. (2002). Effect of artificial culture media on germination, growth, virulence and surface properties of the entomopathogenic hyphomycete Metarhizium anisopiae. Mycol. Res. 106: 705–715.

    Article  Google Scholar 

  • Ignoffo, C. M. McIntosh, A. H. Garcia, C. Kroha, M. & Johnson, J. M. (1992). Effective of successive in vitro and in vivo passages on the virulence of the Entomopathogenic fungus, Nomuraea rileyi. Entomophaga. 27: 371–378.

    Article  Google Scholar 

  • Inglis, D. G., 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. Butt T.M., Jackson, C. W. & Magan, N. (eds). CAB International, Wallingford, Oxon, U.K. Chapter 3. 23–69.

    Google Scholar 

  • Inglis, P.W & Valaderes-Inglis, M. C. (1997). Rapid isolation of double-stranded RNA viruses from entomopathogenic species of the fungus Paecilomyces using a commercial minicolumn system. Journal of Virological Methods 67: 113–116.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, L.J., Johnson, R.D., Akamatsu, H., Salamiah, A., Otani, H., Kohmoto, K. & Kodama, M. (2001) Spontaneous loss of a conditionally dispensable chromosome from the Alternaria alternata apple pathotype leads to loss of toxin production and pathogenicity. Curr. Genet. 40: 65–72.

    Article  PubMed  CAS  Google Scholar 

  • Kawakami, K. (1960). On the change of characteristics of the silkworrm muscardines through successive cultures. Bulletin Sericultural Experiment Station, Japan, 16: 83–99.

    Google Scholar 

  • Kempken, F., & Kuck, U. (1998). Transposons in filamentous fungi— facts and perspectives. BioEssays 20: 652–659.

    Article  PubMed  CAS  Google Scholar 

  • Kempken, F., & Kuck, U. (2000) Tagging of a nitrogen pathway-specific regulator gene in Tolypocladium inflatum by the transposon Restless. Mol. Gen. Genet. 263: 302–308.

    Article  PubMed  CAS  Google Scholar 

  • Latch, G.C.M. (1965). Metarhizium anisopliae (Metschnikoff) Sorokin strains in New Zealand and their possible use for controlling pasture inhabiting insects. N.Z.J. Agr. Res. 8: 384–396.

    Google Scholar 

  • Latch, G.C.M. (1976). Studies on the susceptibility of Oryctes rhinoceros to some entomogenous fungi. Entomophaga 21: 31–38.

    Article  Google Scholar 

  • Lord, J. C. & Roberts, D. W. (1986). The effects of culture medium quality and host passage on Zoosporogenesis, Oosporogenesis, and infectivity of Lagenidium giganteum (Oomycetes; Lagenidiales). J. Invertebr. Pathol. 48: 355–361.

    Article  Google Scholar 

  • Masel, A.M., Irwin, J.A.G. & Manners, J.M. (1993) DNA addition or deletion is associated with a major karyotype polymorphism in the fungal phytopathogen Cottetotrichum gloeosporoides. Mol. Gen. Genet. 237, 73–80.

    Article  PubMed  CAS  Google Scholar 

  • Morrow, B.J., & Boucias, D.G. (1988). Comparative analysis of the in vitro growth of the hyphal body and mycelial stage of the entomopathogenic fungus Nomuraea rileyi. Journal of Invertebrate Pathology 51: 197–206.

    Article  Google Scholar 

  • Morrow, B.J., Boucias, D.G. & Heath, M.A., (1989). Loss of virulence in an isolate of an entomopathogenic fungus, Nomuraea rileyi after serial in vitro passage. J. Econ. Entomol. 82: 404–407.

    Google Scholar 

  • Nagaich, B. B. (1973). Verticittium species pathogenic on aphids. Indian Pathol. 26: 163–165.

    Google Scholar 

  • Pfeifer, T.A. & Khachatourians, G.G. (1993) Electrophoretic karyotype of the entomopathogenic deuteromycete Beauveria bassiana. J. Invertebr. Pathol. 61: 231–235.

    Article  Google Scholar 

  • Pitkin, J.W., Nikolskaya, A., Ahn, J.H. & Walton, J.D. (2000) Reduced virulence caused by meiotic instability of the TOX2 chromosome of the maize pathogen Cochliobolus carbonum. Mol. Plant- Microbe Interact. 13: 80–87.

    PubMed  CAS  Google Scholar 

  • Prenerova, E. (1994). Pathogenicity of Paecilomyces farinosus toward Cephalcia abietis eonymphs (Insects, Hymenoptera): enhancement of bioactivity by in vivo passaging. J. Invert. Pathol. 64: 62–64.

    Article  Google Scholar 

  • Rockwood, L. P. 1950. Entomogenous fungi of the family Entomophthoraceae in the Pacific Northwest. J. Economic Entomology 43: 704–707.

    Google Scholar 

  • Ryan, M. J. Bridge, P. D. Smith, D. & Jeffries, P. (2002). Phenotypic degeneration occurs during sector formation in Metarhizium anisopliae. J. App. Microbiol. 93: 163–168.

    Article  CAS  Google Scholar 

  • SamÅ¡iňaková, A. & Kálalová, S. (1983M). The Influence of a Single-Spore Isolate and Repeated Subculturing on the Pathogenicity of Conidia of the Entomophagous Fungus Beauveria bassiana. J. Invert. Pathol. 42: 156–161.

    Article  Google Scholar 

  • Schaerffenberg, B., (1964). Biological and environmental conditions for the development of mycoses caused by Beauveria and Metarhizium. J. Insect Pathol. 6: 8–20.

    Google Scholar 

  • Selker, E.U., & Garrett, P.W. (1988). DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proceedings National Academy of Sciences USA 85: 6870–6874.

    Article  CAS  Google Scholar 

  • Shah, F. A. & Butt, T. M. (2005) Influence of nutrition on the production and physiology of sectors produced by the insect pathogenic fungus Metarhizium anisopliae. FEMS Microbiol. Lett. 250: 201–207

    Article  PubMed  CAS  Google Scholar 

  • Shah, F. A., Wang, C-S, & Butt, T. M. (2005). Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol. Lett. 251: 259–266.

    Article  PubMed  CAS  Google Scholar 

  • Shimizu, S., Arai, Y. & Matsumoto, T. (1992) Electrophoretic karyotype of Metarhizium anisopliae. J. Invertebr. Pathol. 60: 185–187.

    Article  CAS  Google Scholar 

  • Shimizu, S., Nishida, Y., Yoshioka, H. & Matsumoto, T. (1991) Separation of chromosomal DNA molecules from Paecilomyces fumosoroseus by pulsed-field electrophoresis. J. Invertebr. Pathol. 58: 461–463.

    Article  CAS  Google Scholar 

  • Steinkraus, D.C., Geden, C.J. & Rutz, D.A. (1991). Susceptibility of lesser mealworm (Coleoptera: Tenebrionidae) to Beauveria bassiana (Moniliales: Moniliaceae): Effects of host stage, substrate, formulation and host passage. Journal of Medical Entomology 28: 314–321.

    Google Scholar 

  • Stimberg, N., Walz, M., Schorgendorfer, K. & Kuck, U. (1992) Electrophoretic karyotyping from Tolypocladium inflatum and 6 related strains allows differentiation of morphologically similar species. Appl. Microbiol. Biotechnol. 37, 485–489.

    Google Scholar 

  • Sweeney, A. W. (1981). Prospects for the use of Culicinomyces fungi for biocontrol of mosquitoes. In Biocontrol of Medical and Veterinary Pests. (M. Laired, ed.), 105–121. Praeger, New York.

    Google Scholar 

  • Taga, M., Murata, M. & VanEtten, H. D. (1999). Visualization of a conditionally dispensable chromosome in the filamentous ascomycete Nectria haematococca by fluorescence in situ hybridization. Fungal Genet Biol 26, 169–177.

    Article  PubMed  CAS  Google Scholar 

  • Tzeng, T-H., Lyngholm, L.K., Ford, C.F. & Bronson, C.R. (1992) A restriction fragment length polymorphism map and electrophoresis karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 130, 81–96.

    PubMed  CAS  Google Scholar 

  • Vandenberg, J. D. & Cantone, F. A. (2004). Effect of serial transfer of three strains of Paecilomyces fumosoroseus on growth in vitro, virulence and host specificity. J. Invertebr. Pathol. 85: 40–45.

    Article  PubMed  Google Scholar 

  • Vey, A., Hoagland, R. & Butt, T. M. (2001). Toxic metabolites of fungal biological control agents. In: Fungi as biocontrol agents: Progress, Problems and Potential. Butt T.M., Jackson, C. W. & Magan, N. (eds). CAB International, Wallingford, Oxon, U.K Chapter 12. p 311–346.

    Google Scholar 

  • Viaud, M., Couteaudier, Y., Levis, C. & Riba, G. (1996). Genome organization in Beauveria bassiana: electrophoretic karyotype, gene mapping, and telomeric fingerprint. Fungal Genet. Biol 20, 175–183.

    Article  CAS  Google Scholar 

  • Wang, C-S, Butt, T.M. & St Leger, R.J. 2005. Colony sectorization of Metarhizium anisopliae is a sign of aging. Microbiology 151: 3223–3236

    Article  PubMed  CAS  Google Scholar 

  • Wang, C., Typas, M.A. & Butt, T.M. (2002). Detection and characterisation of pr1 virulent gene deficiencies in the insect pathogenic fungus Metarhizium anisopliae. FEMS Microbiology Letters, 213: 251–255.

    Article  PubMed  CAS  Google Scholar 

  • Wang, C. S., Skrobek, A. & Butt, T.M. (2003) Concurrence of losing a chromosome and the ability to produce destruxins in a mutant of Metarhizium anisopliae. FEMS Microbiol. Lett. 226: 373–378.

    Article  PubMed  CAS  Google Scholar 

  • Wasti, S. S & Hartman, G. C. (1975). Experimental parasitization of larvae of the gypsy moth, Porthetria dispar (L) with the entomogenous fungus, Beauveria bassiana (Balsamo) Vuill. Parasitology 70: 341–346.

    Article  Google Scholar 

  • Zhang, L., Churchill, A.C.L., Kazmierczak, P. Dae-Hyuk, K. & Van Alfen, N. K. (1993). Hypovirulence-associated traits induced by mycoviruses of Cryphonectria parasitica are mimicked by targeted inactivation of a host gene. Molecular and Cellular Biology 13: 7782–7792.

    PubMed  CAS  Google Scholar 

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Authors
  1. Tariq M. Butt
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  2. Chengshu Wang
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  3. Farooq A. Shah
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  4. Richard Hall
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Editors and Affiliations

  1. The Royal Veterinary and Agricultural University, Copenhagen, Denmark

    J. EILENBERG

  2. University of Helsinki, Finland

    H.M.T. HOKKANEN

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Butt, T.M., Wang, C., Shah, F.A., Hall, R. (2006). DEGENERATION OF ENTOMOGENOUS FUNGI. In: EILENBERG, J., HOKKANEN, H. (eds) An Ecological and Societal Approach to Biological Control. Progress in Biological Control, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-4401-4_10

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