Biological indices of the entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae , and assessment of their virulence diversity

Document Type : Paper, Persian

Authors

Department of Plant Protection, Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran

Abstract

Biological indices such as conidial morphology, germination, and surface characteristics influence the virulence of an isolate. Therefore, the growth indices (vegetative growth, conidiogenesis, and germination), hydrophobicity property and Pr1 protease enzyme activity of three isolates of Beauveria bassiana (JS1, JS2 and KA75) and TT1 isolate of Metarhizium anisopliae evaluated. Also, the relationship between these indices and the virulence of the isolates on the last instar larvae of Galleria mellonella and fourth instar larvae of Ephestia kuehniella investigated. There was no significant difference in vegetative growth rate between B. bassiana isolates, but the highest rate (7.05 cm) was related to the TT1 isolate. JS2 isolate showed the highest conidial production (4.11×106 spores / ml) compared to the other isolates evaluated. All isolates showed germination above 80%, and the highest value (100%) was related to the TT1 isolate, which was statistically on par with the conidiogenesis of the KA75 isolate. The lowest hydrophobicity of the conidial surface was related to KA75 isolate, which was significantly different from other isolates. However, the highest percentage was related to TT1 isolate with 91.7%. Also, no differences were observed between the isolates in terms of Pr1 enzyme activity. Bioassays showed that TT1 and JS2 isolates had the highest virulence on the last instar larvae of G. mellonella and fourth instar larvae of E. kuehniella, respectively. Among the evaluated indices, the hydrophobicity and conidiogenesis of these two isolates were higher than the other isolates, which was directly related to their high virulence. Thus, the TT1 isolate of the M. anisopliae and the JS2 isolates of B. bassiana had greater bioefficiency than the other isolates and therefore, they will be more suitable for use in plant pest biological control programs.

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Main Subjects

References

Alizadeh, Z. (2014). Identification of entomopathogenic fungi from Khosrowshahr region based on phylogenetic analysis of ITS-rDNA sequence. M.Sc. thesis, Azarbaijan Shahid Madani University, 118 pp. (In Persian with English summary).
Altre, J. A., Vandenberg, J. D. & Cantone, F. A. (1999). Pathogenicity of Paecilomyces fumosoroseus isolates to diamondback moth, Plutella xylostella: correlation with spore size, germination speed, and attachment to cuticle. Journal of Invertebrate Pathology 73, 332-338.
Alves, S. B., Moino A. & Almeida, J. E. M. (1998). Produtos fitossanitários e entomopatógenos, pp. 217-238 in Alves, S. B. (Ed) Controle microbiano de insetos. 1163 pp. Piracicaba, FEALQ.
Boucias, D. G. & Pendland, J. C. (1984) Nutritional requirements for conidial germination of several host range pathotypes of the entomopathogenic fungus Nomuraea rileyi. Journal of Invertebrate Pathology 43, 288-292.
Boucias, D. G., Pendland, J. E. & Latge, J.P. (1988) Nonspecific factors involved in attachment of entomopathogenic Deuteromycetes to host insect cuticle. Applied and Environmental Microbiology 54, 1795-1805.
Butt, T., Coates, C., Dubovskiy, I. & Ratcliffe, N. (2016). Entomopathogenic fungi: new insights into host–pathogen interactions. Advanced Genetics 94, 307-64.
Chandler, D. (2017) Basic and applied research on entomopathogenic fungi. pp. 69-89 in Lacey, L. A. (Ed) Microbial Control of Insect and Mite Pests from Theory to Practice. 461 pp. Elsevier Inc. UK.
Dias, B. A., Neves, P. M. O. J., Furlaneto-Maia, L. & Furlaneto, M. C. (2008). Cuticle-degrading proteases produced by the entomopathogenic fungus Beauveria bassiana in the presence of coffee berry borer cuticle. Brazilian Journal of Microbiology 39, 301-306.
Faraji, S., Mehrvar, A. & Derakhshan Shadmehri, A. (2013) Studies on the virulence of different isolates of Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metcsn.) Sorokin against Mediterranean flour moth, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). African Journal of Agricultural Research 8, 4157-4161.
Fuxa, J. (1987) Ecological considerations for the use of entomogenous fungi. Annual Review of Entomology 23, 409-442.
Gillespie, J. P., Bateman, R. & Charnley, A. K. (1998) Role of cuticle-degrading proteases in the virulence of Metarhizium spp. for the desert locust, Schistocerca gregaria. Journal of Invertebrate Pathology 71, 128-137.
Golebiowski, M., Cerkowniak, M., Urbanek, A., Dawgul, M., Kamysz, W., Boguś, M. I.,  Sosnowska, D. & Stepnowski, P. (2014) Antimicrobial activity of untypical lipid compounds in the cuticular and internal lipids of four fly species. Journal of Applied Microbiology 116, 269-287.
Golebiowski, M., Cerkowniak, M., Urbanek, A., Dawgul, M., Kamysz, W., Boguś, M. I. & Stepnowski P. (2015) Identification and antifungal activity of novel organic compounds found in cuticular and internal lipids of medically important flies. Microbiological Research, 170, 213-222.
Golo, P. S., Santos, H. A., Perinotto, W. M. S., Quinelato, S., Angelo, I. C., Camargo, M. G., Sa, F. A., Massard, C. L., Fernandes, E. K. K., Roberts, D. W. & Bittencourt, V. R. E. P. (2015) The influence of conidial Pr1 protease on pathogenicity potential of Metarhizium anisopliae senso latu to ticks. Parasitology Research 114, 2309-2315.
Gutierrez, A. C., Gołębiowski, M., Pennisi, M., Peterson, G., García, J. J., Manfrino, R. G. & López Lastra, C. C. (2015) Cuticle fatty acid composition and differential susceptibility of three species of cockroaches to the entomopathogenic fungi Metarhizium anisopliae (Ascomycota, Hypocreales). Journal of Economic Entomology 108, 752-760. 
Hajek, A. E. & St Leger, R. J. (1994) Interactions between fungal pathogens and insect host. Annual Review of Entomology 39, 293-322.
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 Invertebrate Pathology 56, 91-97.
Hesketh, H., Roy, H. E., Eilenberg, J., Pell, J. K. & Hails, R. S. (2010) Challenges in modeling complexity of fungal entomopathogens in semi-natural populations of insects. Biocontrol 55, 55-73.
Holder, D. J. & Keyhani, N. O. (2005). Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Applied and Environmental Microbiology 71, 5260-5266.
Holder, D. J., Kirkland, B. H., Lewis, M. H. & Keyhani, N. O. (2007). Surface characteristics of the entomopathogenic fungus Beauveria (Cordyceps) bassiana. Microbiology 153, 3448-3457.
Hosseinzadeh, R., Mehrvar, A., Eivazian Kary, N. & Valizadeh, H. (2018). Compatibility of some plant essential oils in combination with the entomopathogenic fungus, Beauveria bassiana against Callosobruchus maculatus (Col.: Bruchidae). Plant Pest Research 8, 1-14.
Hussain, A., Rizwan-ul-Haq, M., Al-Ayedh, H., Ahmed, S. & Al-Jabr, A. M. (2015). Effect of Beauveria bassiana infection on the feeding performance and antioxidant defence of red palm weevil, Rhynchophorus ferrugineus. BioControl 60, 849-859.
Hussain, A., Tian, M. Y., He, Y. R., Ruan, L. & Ahmed, S. (2010) In vitro and in vivo culturing impacts on the virulence characteristics of serially passed entomopathogenic fungi. Journal of Food, Agriculture and Environment 8, 481-487.
Jarrold, S. L., Moore, D., Potter, U. & Charnley, A. K. (2007) The contribution of surface waxes to pre-penetration growth of an entomopathogenic fungus on host cuticle. Mycological Research 111, 240-249.
Keyhani, N. O. (2018) Lipid biology in fungal stress and virulence: entomopathogenic fungi. Fungal Biology 122, 420-429.
Khachatourians, G. G. (1998) Biochemistry and molecular biology of entomopathogenic fungi. pp. 331-363 in Howard, D. H. & Miller, J. D. (Eds) The Mycota, human and animal relationships. Vol. 6. 307 pp. Springer Verlag, Berlin.
Lacey, L. A. (2017) Entomopathogens used as microbial control agents. pp. 3-12 in Lacey, L. A. (Ed) Microbial Control of Insect and Mite Pests from Theory to Practice. 461 pp. Elsevier Inc.
Lewis, M. W., Ines V. Robalino, I. V. & Keyhani, N. O. (2009) Uptake of the fluorescent probe FM4-64 by hyphae and haemolymph-derived in vivo hyphal bodies of the entomopathogenic fungus Beauveria bassiana. Microbiology 155, 3110-3120.
Liu, H., Skinner, M., Brownbridge, M. & Parker, B. L. (2003) Characterization of Beauveria bassiana and Metarhizium anisopliae isolates for management of tarnished plant bug, Lygus lineolaris (Hemiptera: Miridae). Journal of Invertebrate Pathology 82, 139-147.
Mascarin, G. M., Kobori, N. N., Quintela, E. D. & Delalibera, I. (2013) The virulence of entomopathogenic fungi against Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation. Biological Control 66, 209-218.
Mehrvar, A. (2015) An introduction to pathology and microbial control of pests. 301 pp. Azarbaijan Shahid Madani University Press. Tabriz, Iran. [In Persian].
Ortiz-Urquiza, A. & Keyhani, N. O. (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4, 357-374.
Pedrini, N. (2018). Molecular interactions between entomopathogenic fungi (Hypocreales) and their insect host: perspectives from stressful cuticle and hemolymph battlefields and the potential of dual RNA sequencing for future studies. Fungal Biology 122, 538-45.
Pedrini, N., Zhang, S., Juarez, M. P. & Keyhani, N.O. (2010) Molecular characterization and expression analysis of a suite of cytochrome P450 enzymes implicated in insect hydrocarbon degradation in the entomopathogenic fungus Beauveria bassiana. Microbiology 156, 2549-2557.
Raafat, I., Meshrif, W. S., El Husseiny, E. M., El-Hariry, M. & Seif, A. I. (2015) Nezara viridula (Hemiptera: Pentatomidae) cuticle as a barrier for Beauveria bassiana and Paecilomyces sp. Infection. African Entomology 23, 75-87.
Rella, A., Farnoud, A. M. & Del Poeta, M. (2016) Plasma membrane lipids and their role in fungal virulence. Progress in Lipid Research 61, 63-72.
Rios-Velasco, C., Pérez-Corral, D. A., Salas-Marina, M. A., Berlanga-Reyes, D. I., Ornelas-Paz, J. J., Acosta Muñiz, C. H., Cambero-Campos, J. & Jacobo-Cuellar, J. L. (2014). Pathogenicity of the Hypocreales fungi Beauveria bassiana and Metarhizium anisopliae against insect pests of tomato. Southwestern Entomologists 39, 739-750.
Rodriguez-Gomez, D., Loera, O., Saucedo-Castaneda, G. & Viniegra-Gonzalez, G. (2009) Substrate influence on physiology and virulence of Beauveria bassiana acting on larvae and adults of Tenebrio molitor. World Journal of Microbiology and Biotechnology 25, 513-518.
Samuels, K. D. Z., Heale, J. B. & Liewellyn, M. (1989) Characteristics relating to the pathogenicity of Metarhizium anisopliae toward Nilaparvata lugens. Journal of Invertebrate Pathology 53, 25-31.
Santi, L., Silva, W. O. B., Pinto, A. F. M, Schrank, A. & Vainstein, M. H. (2010) Metarhizium anisopliae host–pathogen interaction: differential immunoproteomics reveals proteins involved in the infection process of arthropods. Fungal Biology 114, 312-319.
Schmid-Hempel, P. (2005) Evolutionary ecology of insect immune defenses. Annual Review of Entomology 50, 529-551.
Shah, F. A., Allen, N., Wright, C. J. & Butt, T.M. (2007) Repeated in vitro subculturing alters spore surface properties and virulence of Metarhizium anisopliae. FEMS Microbiology Letters 276, 60-66.
Shapiro, M. & Argauer, R. (2001) Relative effectiveness of selected stilbene optical brighteners as enhancers of the beet armyworm (Lepidoptera: Noctuidae) nuclear polyhedrosis virus. Biological and Microbial Control 94, 339-43.
Siebers, M., Brands, M., Wewer, V., Duan, Y., Hölzl, G. & Dörmann, P. (2016) Lipids in plant–microbe interactions. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 1861: 1379-1395.
St Leger, R. J., Charnley, A. K. & Cooper, R. M. (1986) Cuticle-degrading enzymes of entomopathogenic fungi: synthesis in culture on cuticle. Journal of Invertebrate Pathology 48, 85-95.
St Leger, R. J., Goettel, M., Roberts, D. W. & Staples, R. C. (1991) Prepenetration events during infection of host cuticle by Metarhizium anisopliae. Journal of Invertebrate Pathology 58, 168-179.
Talaei-Hassanloui, R., Kharazi-Pakdel, A., Goettel, M. S., Little, S. & Mozaffari, J. (2007). Germination polarity of Beauveria bassiana conidia and its possible correlation with virulence. Journal of Invertebrate Pathology 94, 102-107.
Ummidi, V. R. S. & Vadlamani, P. (2014). Preparation and use of oil formulations of Beauveria bassiana and Metarhizium anisopliae against Spodoptera litura larvae. African Journal of Microbiology Research 8, 1638-1644.
Wanchoo, A., Lewis, M. W. & Keyhani, N.O. (2009) Lectin mapping reveals stage-specific display of surface carbohydrates in in vitro and haemolymph-derived cells of the entomopathogenic fungus Beauveria bassiana. Microbiology 155, 3121-3133.
Wraight, S. P., Carruthers, R. I., Jaronski, S. T., Bradley, C. A., Garza, C. J. & Galaini-Wraight, S. (2000) Evaluation of the entomopathogenic fungi Beauveria bassiana and Paecilomyces fumosoroseus for microbial control of the silverleaf whitefly, Bemisia argentifolii. Biological Control 17, 203-217.
Zimmermann, G. (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Science and Technology, 17 (5/6): 553-596.

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