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MECHANISMS OF DEUTEROMYCETE FUNGAL INFECTIONS IN GRASSHOPPERS AND LOCUSTS: AN OVERVIEW

Published online by Cambridge University Press:  31 May 2012

Michael J. Bidochka ,
Raymond J. St. Leger  and
Donald W. Roberts
Michael J. Bidochka
Affiliation:
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York, USA 14850
Raymond J. St. Leger
Affiliation:
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York, USA 14850
Donald W. Roberts
Affiliation:
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York, USA 14850
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Abstract

Several species of entomopathogenic deuteromycetous fungi can produce epizootics in populations of grasshoppers and locusts. Consequently there is considerable interest in development of these fungi as biocontrol agents. To this end we need information about the genetic and molecular basis of deuteromycete pathogenesis in acridids to develop a rational plan for strain improvement. Herein we present an overview of the infection processes of deuteromycetous fungi in acridids. These fungi penetrate through the cuticle which is composed primarily of proteins. Hydrophobic interactions, appressoria formation, and mucus production by the fungus are involved in fungal adhesion to the acridid cuticle. Extracellular proteases produced by Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metchnikoff) Sorokin solubilize cuticle proteins, which assists penetration and provides nutrients for further growth. Fungal infection through the locust gut is rare because indigenous gut microflora produce antifungal metabolites. Little is known of the events providing host specificity or those that lead to insect death once the cuticle is breached by the fungus; however, mechanical damage, nutrient deprivation, and toxic metabolites may be involved.

Résumé

Plusieurs espèces de champignons deutéromycètes entomopathogènes peuvent causer des épizooties chez les populations de criquets. Conséquemment, les chercheurs manifestent un intérêt grandissant pour leur potentiel d'agents de lutte biologique. Dans cette optique, il est nécessaire d'accumuler de l'information sur les bases génétique et moléculaire des effets pathogènes de ces champignons chez les acridiens afin d'établir un plan rationnel d'amélioration des souches. On trouvera ici un aperçu global des processus infectieux des deutéromycètes chez les acridiens. Les champignons pénètrent sous la cuticule de nature principalement protéinique. Des interactions hydrophobes, la formation d'appressoriums et la production de mucus permettent l'attachement du champignon à la cuticule des criquets. Des protéases extracellulaires produites par Beauveria bassiana (Balsamo) Vuillemin et Metarhizium anisopliae (Metchnikoff) Sorokin dissolvent les protéines cuticulaires de l'insecte, ce qui facilite la pénétration, et permettent l'approvisionnement des éléments nutritifs nécessaires à la croissance. Les infections transmises dans le tube digestif des criquets sont rares, car la microflore indigène du tube digestif produit des métabolites antifongiques. Les conditions qui assurent la spécificité d'hôte ou celles qui entraînent la mort après l'invasion de la cuticule sont mal connues, mais il est logique d'assumer que des dommages mécaniques, une carence en éléments nutritifs et une contamination par des métabolites toxiques peuvent être responsables des effets observés. [Traduit par la Rédaction]

Type
Research Article
Information
The Memoirs of the Entomological Society of Canada , Volume 129 , Supplement S171 , 1997 , pp. 213 - 224
Copyright
Copyright © Entomological Society of Canada 1997

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Footnotes

1

Current address: Department of Biology, Trent University, Peterborough, Ontario, Canada K9J 7B8.

2

Current address: Dept. of Entomology, University of Maryland, College Park, Maryland 20742-4454 USA.

3

Current address: Dept. of Biology, Utah State University, Logan, Utah 84322, USA.

References

Andersen, S.O. 1988. Characterization of proteins from pharate adult wing cuticle of the migratory locust, Locusta migratoria. Insect Biochemistry 5: 415–421.Google Scholar
Andersen, S.O., Hojrup, P. and Roepstorff, P.. 1986. Characterization of cuticular proteins from the migratory locust, Locusta migratoria. Insect Biochemistry 16: 441–447.Google Scholar
Ashida, M., Ishizaki, Y. and Iwahana, H.. 1983. Activation of pro-phenoloxidase by bacterial cell walls or (β–1,3-glucans in plasma of the silkworm, Bombyx mori. Biochemical and Biophysical Research Communications 113: 562–568.Google Scholar
Bidochka, M.J. 1989. Interaction of the Entomopathogenic Fungus Beauveria bassiana with the Migratory Grasshopper, Melanoplus sanguinipes: A Systematic Study of Pathogenesis. Ph.D. thesis, University of Saskatchewan, Saskatoon, SK. 246 pp.Google Scholar
Bidochka, M.J., Gillespie, J.P. and Khachatourians, G.G.. 1989. Phenoloxidase activity of acridid grasshoppers from the subfamilies Melanoplinae and Oedipodinae. Comparative Biochemistry and Physiology 94B: 117–124.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1987. Hemocytic defense response to the entomopathogenic fungus Beauveria bassiana in the migratory grasshopper Melanoplus sanguinipes. Entomologia Experimentalis Applicata 45: 151–156.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1988 a. Regulation of extracellular protease in the entomopathogenic fungus Beauveria bassiana. Experimental Mycology 12: 161–168.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1988 b. N-acetyl-d-glucosamine-mediated regulation of extracellular protease in the entomopathogenic fungus Beauveria bassiana. Applied Environmental Microbiology 54: 2699–2704.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1990. Identification of Beauveria bassiana extracellular protease as a virulence factor in pathogenicity toward the migratory grasshopper, Melanoplus sanguinipes. Journal of Invertebrate Pathology 56: 362–370.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1991 a. Microbial and protozoan pathogens of grasshoppers and locusts as potential biocontrol agents. Biocontrol Science and Technology 1: 243–259.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1991 b. The implication of metabolic acids produced by Beauveria bassiana in pathogenesis of the migratory grasshopper Melanoplus sanguinipes. Journal of Invertebrate Pathology 58: 106–117.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1992 a. Growth of the entomopathogenic fungus Beauveria bassiana on cuticular components from the migratory grasshopper, Melanoplus sanguinipes. Journal of Invertebrate Pathology 59: 165–173.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1992 b. Partial purification and characterization of two extracellular N-acetyl-D-glucosaminidases produced by the entomopathogenic fungus Beauveria bassiana. Canadian Journal of Microbiology 39: 40–45.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1992 c. Regulation of extracellular N-acetyl-D-glucosaminidase production in the entomopathogenic fungus Beauveria bassiana. Canadian Journal of Microbiology 39: 6–12.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1993. Oxalic acid hyperproduction in Beauveria bassiana mutants is related to a utilizable carbon source but not to virulence. Journal of Invertebrate Pathology 62: 53–57.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1994 a. Hydrolysis of migratory grasshopper, Melanoplus sanguinipes, cuticle by proteolytic enzymes in culture supernatants of entomopathogenic fungi. Journal of Invertebrate Pathology 63: 7–13.Google Scholar
Bidochka, M.J. and Khachatourians, G.G.. 1994 b. Basic proteases of entomopathogenic fungi differ in their adsorption properties to host cuticle substrate. Journal of Invertebrate Pathology 64: 26–32.Google Scholar
Bidochka, M.J., Low, N.H. and Khachatourians, G.G.. 1990. Carbohydrate storage in the entomopathogenic fungus Beauveria bassiana. Applied Environmental Microbiology 56: 3186–3190.Google Scholar
Bidochka, M.J., McDonald, M.A., St. Leger, R.J. and Roberts, D.W.. 1994. Differentiation of species and strains of entomopathogenic fungi by random amplification of polymorphic DNA (RAPD). Current Genetics 25: 107–113.Google Scholar
Bidochka, M.J., Pfeifer, T.A. and Khachatourians, G.G.. 1987. Development of the entomopathogenic fungus Beauveria bassiana in liquid cultures. Mycopathologia 99: 77–83.Google Scholar
Blackwell, J. and Weih, M.A.. 1980. Structure of chitin-protein complexes: Ovipositor of the Ichneumon fly Megarhyssa. Journal of Molecular Biology 137: 49–60.Google Scholar
Blomquist, G.J. and Jackson, L.L.. 1973. Incorporation of labeled dietary n-alkanes into cuticular lipids of the grasshopper Melanoplus sanguinipes. Journal of Insect Physiology 19: 1639–1647.Google Scholar
Boucias, D.G., Pendland, J.C. and Latge, J.P.. 1988. Nonspecific factors involved in the attachment of entomopathogenic deuteromycetes to host insect cuticle. Applied Environmental Microbiology 54: 1795–1805.Google Scholar
Campbell, R.K., Barnes, G.L., Cartwright, B.O. and Eikenbary, R.D.. 1983. Growth and sporulation of Beauveria bassiana and Metarhizium anisopliae in a basal medium containing various carbohydrate sources. Journal of Invertebrate Pathology 41: 117–121.Google Scholar
Campbell, R.K., Perring, T.M., Barnes, G.L., Eikenbary, R.D. and Gentry, C.R.. 1978. Growth and sporulation of Beauveria bassiana and Metarhizium anisopliae on media containing various amino acids. Journal of Invertebrate Pathology 31: 289–295.Google Scholar
Charnley, A.K. 1989. Mechanisms of fungal pathogenesis in insects, pp. 85–125in Whipps, J.M., and Lumsden, R.D. (Eds.), Biotechnology of Fungi for Improving Plant Growth. Cambridge University Press, Cambridge.Google Scholar
Charnley, A.K. 1992. Mechanisms of fungal pathogenesis in insects with particular reference to locusts, pp. 181–190 in Lomer, C.J., and Prior, C. (Eds.), Biological Control of Locusts and Grasshoppers. CAB International, UK. 394 pp.Google Scholar
Cox, D.L. and Willis, J.H.. 1985. The cuticular proteins of Hyalphora cecropia from different anatomical regions and metamorphic stages. Insect Biochemistry 15: 349–362.Google Scholar
Dillon, R.J. and Charnley, A.K.. 1986 a. Invasion of the pathogenic fungus Metarhizium anisopliae through the guts of germ-free desert locusts, Schistocerca gregaria. Mycopathologia 96: 59–66.Google Scholar
Dillon, R.J. and Charnley, A.K.. 1986 b. Inhibition of Metarhizium anisopliae by the gut bacterial flora of the desert locust, Schistocerca gregaria: Evidence for an antifungal toxin. Journal of Invertebrate Pathology 47: 350–360.Google Scholar
Dillon, R.J. and Charnley, A.K.. 1988. Inhibition of Metarhizium anisopliae by the gut bacterial flora of the desert locust; characterization of antifungal toxins. Canadian Journal of Microbiology 34: 1075–1080.Google Scholar
Gillespie, J.P., Bidochka, M.J. and Khachatourians, G.G.. 1991. Separation and characterization of grasshopper hemolymph phenoloxidases by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Comparative Biochemistry and Physiology 98C: 351–358.Google Scholar
Goettel, M.S., St. Leger, R.J.Rizzo, N.W.Staples, R.C. and Roberts, D.W.. 1989. Ultrastructural localization of a cuticle-degrading protease produced by the entomopathogenic fungus Metarhizium anisopliae during penetration of host (Manduca sexta) cuticle. Journal of General Microbiology 135: 2233–2239.Google Scholar
Gotz, P. and Boman, H.G.. 1985. Insect immunity, pp. 453–485in Kerkut, G.A., and Gilbert, L.I. (Eds.), Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 3. Pergamon Press, Oxford.Google Scholar
Gunnarsson, S.G.S. 1988. Infection of Schistocerca gregaria by the fungus Metarhizium anisopliae: Cellular reactions in the integument studied by scanning electron and light microscopy. Journal of Invertebrate Pathology 52: 9–17.Google Scholar
Hapner, K.D. 1983. Haemagglutinin activity in the haemolymph of individual Acrididae (grasshopper) specimens. Journal of Insect Physiology 28: 177–181.Google Scholar
Hassan, A.E.M. and Charnley, A.K.. 1989. Ultrastructural study of the penetration by Metarhizium anisopliae through dimilin-affected cuticle of Manduca sexta. Journal of Invertebrate Pathology 54: 117–124.Google Scholar
Hsiao, W.-F., Bidochka, M.J. and Khachatourians, G.G.. 1992. Effects of diphenols on the growth of three entomopathogenic fungi. Canadian Journal of Microbiology 38: 1000–1003.Google Scholar
Huxham, I.M., Lackie, A.M. and McCorkindale, N.J.. 1989. Inhibitory effects of cyclodepsipeptides, destruxins, from the fungus Metarhizium anisopliae, on cellular immunity in insects. Journal of Insect Physiology 35: 97–105.Google Scholar
Jackson, L.L. 1981. Cuticular lipids of insects—IX. Surface lipids of the grasshoppers Melanoplus bivittatus, Melanoplus femurruhrum and Melanoplus dawsoni. Comparative Biochemistry and Physiology 70B: 441–445.Google Scholar
Joshi, L., Charnley, A.K., Arnold, G., Brain, P. and Bateman, R.. 1992. Synergism between entomopathogenic fungi, Metarhizium spp., and the benzoylphenyl urea insecticide, teflubenzuron, against the desert locust, Schistocerca gregaria. pp. 369–373 (Abstract) in Brighton Crop Protection Conference—Pests and Diseases—1992. British Crop Protection Council, Farnham, UK.Google Scholar
Kanost, M.R., Kawooya, J.K., Law, J.H., Ryan, R.O., Van Heusden, M.C. and Ziegler, R.. 1990. Insect haemolymph proteins. Advances in Insect Physiology 22: 299–396.Google Scholar
Latge, J.P., Sampedro, L., Brey, P. and Diaquin, M.. 1987. Aggressiveness of Conidiobolus obscurum against the pea aphid: Influence of cuticular extracts on ballistospore germination of aggressive and non-aggressive strains. Journal of General Microbiology 133: 1989–1997.Google Scholar
Lecuona, R., Riba, G., Cassier, P. and Clement, J.L.. 1991. Alteration of insect epicuticular hydrocarbons during infection with Beauveria bassiana or B. brongniartii. Journal of Invertebrate Pathology 58: 10–18.Google Scholar
Miranpuri, G.S., Bidochka, M.J. and Khachatourians, G.G.. 1991. Morphology and cytochemistry of hemocytes and analysis of hemolymph from Melanoplus sanguinipes (Orthoptera: Acrididae). Journal of Economic Entomology 84: 371–378.Google Scholar
Pendland, J.C., Hung, S.-Y. and Boucias, D.G.. 1993. Evasion of host defense by in vivo-produced protoplast-like cells of the insect mycopathogen Beauveria bassiana. Journal of Bacteriology 175: 5962–5969.Google Scholar
Prior, C., Lomer, C.J., Herren, H., Paraiso, A., Kooyman, C. and Smit, J.J.. 1992. The IIBC/IITA/DFPV collaborative research programme on the biological control of locusts and grasshoppers, pp. 8–18 in Lomer, C.J., and Prior, C. (Eds.), Biological Control of Locusts and Grasshoppers. CAB International, UK. 394 pp.Google Scholar
Renwratz, L. 1983. Involvement of agglutinins (lectins) in invertebrate defense reactions: The immuno-biological importance of carbohydrate-specific binding molecules. Developmental and Comparative Immunology 7: 603–608.Google Scholar
Roberts, D.W., Gupta, S. and St. Leger, R.J.. 1992. Metabolite production by entomopathogenic fungi. Pesquisa Agropecuaria Brasileira, Brasilia 27: 325–347.Google Scholar
St. Leger, R.J. 1993. Biology and mechanisms of insect-cuticle invasion by Deuteromycete fungal pathogens. pp. 211–229in Beckage, N.E., Thompson, S.N., and Federici, B.A. (Eds.), Parasites and Pathogens of Insects. Chapter 10, Vol. 2: Pathogens. Academic Press, San Diego, CA.Google Scholar
St. Leger, R.J., Butt, T.M., Goettel, M.S., Staples, R.C. and Roberts, D.W.. 1989. Production in vitro of appressoria by the entomopathogenic fungus Metarhizium anisopliae. Experimental Mycology 13: 274–288.Google Scholar
St. Leger, R.J., Charnley, A.K. and Cooper, R.M.. 1986 a. Cuticle-degrading enzymes of entomopathogenic fungi: Synthesis in culture on cuticle. Journal of Invertebrate Pathology 48: 85–95.Google Scholar
St. Leger, R.J., Charnley, A.K. and Cooper, R.M.. 1986 b. Cuticle-degrading enzymes of entomopathogenic fungi: Mechanisms of interaction between pathogen enzymes and insect cuticle. Journal of Invertebrate Pathology 47: 295–302.Google Scholar
St. Leger, R.J., Charnley, A.K. and Cooper, R.M.. 1991. Kinetics of the digestion of insect cuticles by a protease (Prl) from Metarhizium anisopliae. Journal of Invertebrate Pathology 57: 146–147.Google Scholar
St. Leger, R.J., Cooper, R.M. and Charnley, A.K.. 1986 a. Cuticle-degrading enzymes of entomopathogenic fungi: Cuticle degradation in vitro by enzymes from entomopathogens. Journal of Invertebrate Pathology 47: 167–177.Google Scholar
St. Leger, R.J., Cooper, R.M. and Charnley, A.K.. 1986 b. Cuticle-degrading enzymes of entomopathogenic fungi: Regulation of production of chitinolytic enzymes. Journal of General Microbiology 132: 1509–1517.Google Scholar
St. Leger, R.J., Cooper, R.M. and Charnley, A.K.. 1987. Distribution of chymoelastases and trypsin-like enzymes in five species of entomopathogenic deuteromycetes. Archives of Biochemistry and Biophysics 258: 123–131.Google Scholar
St. Leger, R.J., Cooper, R.M. and Charnley, A.K.. 1988 a. Utilization of alkanes by entomopathogenic fungi. Journal of Invertebrate Pathology 52: 356–359.Google Scholar
St. Leger, R.J., Cooper, R.M. and Charnley, A.K.. 1988 b. The effect of melanization of Manduca sexta cuticle on growth and infection by Metarhizium anisopliae. Journal of Invertebrate Pathology 52: 459–470.Google Scholar
St. Leger, R.J., Cooper, R.M. and Charnley, A.K.. 1993. Analysis of aminopeptidase and dipeptidylpeptidase IV from the entomopathogenic fungi Metarhizium anisopliae. Journal of General Microbiology 139: 237–243.Google Scholar
St. Leger, R.J., Durrands, P.K., Cooper, R.M. and Charnley, A.K.. 1988. Regulation of production of proteolytic enzymes by the entomopathogenic fungus Metarhizium anisopliae. Archives of Microbiology 150: 413–416.Google Scholar
St. Leger, R.J., Goettel, M., Roberts, D.W. and Staples, R.C.. 1991. Prepenetration events during infection of host cuticle by Metarhizium anisopliae. Journal of Invertebrate Pathology 58: 168–179.Google Scholar
St. Leger, R.J., May, B., Allee, L.L., Frank, D.C. and Roberts, D.W.. 1992. Genetic differences in allozymes and in formation of infection structures among isolates of the entomopathogenic fungus, Metarhizium anisopliae. Journal of Invertebrate Pathology 60: 89–101.Google Scholar
St. Leger, R.J., Staples, R.C. and Roberts, D.W.. 1992 a. Molecular cloning and regulatory analysis of the cuticle-degrading protease structural gene from the entomopathogenic fungus Metarhizium anisopliae. European Journal of Biochemistry 204: 991–1001.Google Scholar
St. Leger, R.J., Staples, R.C. and Roberts, D.W.. 1992 b. Cloning and regulatory analysis of starvation-stress gene, SSGA, encoding a hydrophobin-like protein from the entomopathogenic fungus Metarhizium anisopliae. Gene 120: 119–124.Google Scholar
St. Leger, R.J., Staples, R.C. and Roberts, D.W.. 1993. Entomopathogenic isolates of Metarhizium anisopliae, Beauveria bassiana, and Aspergillus flavus produce multiple extracellular chitinase isozymes. Journal of Invertebrate Pathology 61: 81–84.Google Scholar
Saito, T. and Aoki, J.. 1983. Toxicity of free fatty acids on the larval surfaces of two lepidopterous insects toward Beauveria bassiana (Bals.) Vuill. and Paecilomyces fumoso-roseus (Wize) Brown et Smith (Deuteromycetes: Moniliales). Applied Entomology and Zoology 18: 225–233.Google Scholar
Samuels, R.I., Charnley, A.K. and Reynolds, S.E.. 1988. The role of destraxins in the pathogenicity of 3 strains of Metarhizium anisopliae for the tobacco hornworm Manduca sexta. Mycopathologia 104: 51–58.Google Scholar
Samuels, R.I., Reynolds, S.E. and Charnley, A.K.. 1988. Calcium channel activation of insect muscle by destruxins, insecticidal compounds produced by the entomopathogenic fungus Metarhizium anisopliae. Comparative Biochemistry and Physiology 90C: 403–412.Google Scholar
Smith, R.J. and Grula, E.A.. 1981. Nutritional requirements for conidial germination and hyphal growth of Beauveria bassiana. Journal of Invertebrate Pathology 37: 222–230.Google Scholar
Smith, R.J. and Grula, E.A.. 1982. Toxic components on the larval surface of the corn earworm (Heliothis zea) and their effects on germination and growth of Beauveria bassiana. Journal of Invertebrate Pathology 39: 15–22.Google Scholar
Soderhall, K. and Smith, V.J.. 1986. The prophenoloxidase activating system: The biochemistry of its activation and role in arthropod cellular immunity with special reference to crustaceans, pp. 208–233in Brehelin, M. (Ed.), Immunity in Invertebrates. Springer-Verlag, New York.Google Scholar
Soliday, C.L., Blomquist, G.J. and Jackson, L.L.. 1974. Cuticular lipids of insect. VI. Cuticular lipids of the grasshoppers Melanoplus sanguinipes and Melanoplus packardii. Journal of Eipid Research 15: 399–405.Google Scholar
Stebbins, M.R. and Hapner, K.D.. 1985. Preparation and properties of haemagglutinin from hemolymph of Acrididae (Grasshoppers). Insect Biochemistry 15: 451–462.Google Scholar
Stiles, B., Bradley, R.S., Stuart, G.S. and Hapner, K.D.. 1988. Site of synthesis of the hemolymph agglutinin of Melanoplus differentialis (Acrididae: Orthoptera). Journal of Insect Physiology 34: 1077–1085.Google Scholar
Veen, K.H. 1966. Oral infection of second-instar nymphs of Schistocerca gregaria by Metarhizium anisopliae. Journal of Invertebrate Pathology 8: 254–256.Google Scholar
Wheeler, M.B., Stuart, G.S. and Hapner, K.D.. 1993. Agglutinin mediated opsonization of fungal blastospores in Melanoplus differentialis (Insecta). Journal of Insect Physiology 39: 477–483.Google Scholar
Willis, J.H. 1987. Cuticular proteins: The neglected component. Archives of Insect Biochemistry and Physiology 6: 203–215.Google Scholar
Woods, S.P. and Grula, E.A.. 1984. Utilizable surface nutrients on Heliothis zea available for growth of Beauveria bassiana. Journal of Invertebrate Pathology 43: 359–369.Google Scholar