Susceptibility of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) to the entomopathogenic fungus Metarhizium anisopliae when feeding on Bacillus thuringiensis Cry3Bb1-expressing maize

Applied and Environmental Microbiology

Volumn 75, Issue 12, 2009, Pages 3937-3943

  Meissle, Michael ^a   Pilz, Christina ^a,b   Romeis, Jörg ^a  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

^b AUSTRIAN AGENCY FOR HEALTH AND FOOD SAFETY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS THURINGIENSIS; BIOLOGICAL CONTROLS; CHRYSOMELIDAE; COLEOPTERA; ENTOMOPATHOGENIC FUNGUS; INSECTICIDAL PROTEIN; MAIZE PESTS; MAIZE SEEDLINGS; METARHIZIUM ANISOPLIAE; VIRGIFERA LARVAE; WEIGHT GAIN;

BACTERIOLOGY;

FEEDING;

BACTERIAL PROTEIN; PROTEIN CRY3BB1; UNCLASSIFIED DRUG;

ADULT; BACTERIUM; BEETLE; BIOLOGICAL CONTROL; CROP PEST; ENTOMOPATHOGENIC ORGANISM; FUNGUS; GENETIC ENGINEERING; MAIZE; PROTEIN;

ARTICLE; BACILLUS THURINGIENSIS; COLEOPTERA; CONTROLLED STUDY; DIABROTICA VIRGIFERA VIRGIFERA; MAIZE; METARHIZIUM ANISOPLIAE; MORTALITY; NONHUMAN; PROTEIN EXPRESSION; SEEDLING;

ANIMALS; BEETLES; BODY WEIGHT; ENDOTOXINS; LARVA; METARHIZIUM; PLANTS, GENETICALLY MODIFIED; RECOMBINANT PROTEINS; SURVIVAL ANALYSIS; ZEA MAYS;

EURASIA; EUROPE; NORTH AMERICA;

BACILLUS THURINGIENSIS; CHRYSOMELIDAE; COLEOPTERA; DIABROTICA; DIABROTICA VIRGIFERA VIRGIFERA; FUNGI; METARHIZIUM ANISOPLIAE; ZEA MAYS;

EID: 67149090633     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00432-09     Document Type: Article

References (50)

1. Al-Deeb, M. A., and G. E. Wilde. 2005. Effect of Bt corn expressing the Cry3Bb1 toxin on western corn rootworm (Coleoptera: Chrysomelidae) biology. J. Kansas Entomol. Soc. 78:142-152.
2. Brousseau, C., G. Charpentier, and S. Belloncik. 1998. Effects of Bacillus thuringiensis and destruxins (Metarhizium anisopliae mycotoxins) combinations on spruce budworm (Lepidoptera: Tortricidae). J. Invertebr. Pathol. 72:262-268.
3. Bruck, D. J., and L. C. Lewis. 2001. Adult Diabrotica spp. (Coleoptera: Chrysomelidae) infection at emergence with indigenous Beauveria bassiana (Deuteromycotina: Hyphomycetes). J. Invertebr. Pathol. 77:288-289.
4. Bruck, D. J., and L. C. Lewis. 2002. Whorl and pollen-shed stage application of Beauveria bassiana for suppression of adult western corn rootworm. Entomol. Exp. Appl. 103:161-169.
5. Butt, T. M., C. Jackson, and N. Magan. 2001. Fungi as biocontrol agents. CABI Publishing, Wallingford, United Kingdom.
6. Chiang, H. C. 1973. Bionomics of northern and western corn rootworms. Annu. Rev. Entomol. 18:47-72.
7. Costa, S. D., M. E. Barbercheck, and G. G. Kennedy. 2001. Mortality of Colorado potato beetle (Leptinotarsa decemlineata) after sublethal stress with the CryIIIA delta-endotoxin of Bacillus thuringiensis and subsequent exposure to Beauveria bassiana. J. Invertebr. Pathol. 77:173-179. (Pubitemid 32507616)
8. Demont, M., and E. Tollens. 2005. Potential impact of biotechnology in Eastern Europe: transgenic maize, sugar beet and oilseed rape in Hungary. In 9th International Conference on Agricultural Biotechnology: Ten Years After. International Consortium on Agricultural Biotechnology Research, Ravello, Italy. http://www.economia.uniroma2.it/conferenze/icabr2005/papers/Demont-Tollens- Paper.pdf. Accessed 20 February 2009.
9. Ferré, J., J. Van Rie, and S. C. MacIntosh. 2008. Insecticidal genetically modified crops and insect resistance management (IRM), p. 41-85. In J. Romeis, A. M. Shelton, and G. G. Kennedy (ed.), Integration of insect-resistant genetically modified crops within IPM programs. Springer, Dordrecht, The Netherlands.
10. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43:701-726.
11. Hare, J. D. 2002. Plant genetic variation in tritrophic interactions, p. 8-43. In T. Tscharntke and B. A. Hawkins (ed.), Multitrophic level interactions. Cambridge University Press, Cambridge, United Kingdom.
12. Hellmich, R. L., R. Albajes, D. Bergvinson, J. R. Prasifka, Z. Y. Wang, and M. J. Weiss. 2008. The present and future role of insect-resistant genetically modified maize in IPM, p. 119-158. In J. Romeis, A. M. Shelton, and G. G. Kennedy (ed.), Integration of insect-resistant genetically modified crops within IPM programs. Springer, Dordrecht, The Netherlands.
13. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6:65-70.
14. International Conference on Harmonisation of Technical Requirements for Registration of Pharmaceuticals for Human Use. 2005. Harmonised tripartite guideline: validation of analytical procedures: Text and methodology Q2(R1). International Conference on Harmonisation of Technical Requirements for Registration of Pharmaceuticals for Human Use. http://www.ich.org/LOB/media/ MEDIA417.pdf. Accessed 20 February 2009.
15. James, C. 2007. Global status of commercialized biotech/GM crops, 2007. ISAAA brief no. 37. ISAAA, Ithaca, NY.
16. Johnson, M. T., F. Gould, and G. G. Kennedy. 1997. Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants. Entomol. Exp. Appl. 82:219-230.
17. Johnson, M. T., F. Gould, and G. G. Kennedy. 1997. Effect of an entomopathogen on adaptation of Heliothis virescens populations to transgenic host plants. Entomol. Exp. Appl. 83:121-135.
18. Krueger, S. R., and D. W. Roberts. 1997. Soil treatment with entomopathogenic fungi for corn rootworm (Diabrotica spp.) larval control. Biol. Control 9:67-74.
19. Krysan, J. L. 1986. Biology, distribution, and identification of pest Diabrotica, p. 1-23. In J. L. Krysan and T. A. Miller (ed.), Methods for the study of pest Diabrotica. Springer, New York, NY.
20. Kuhlmann, U., and W. A. C. M. van der Burgt. 1998. Possibilities for biological control of the western corn rootworm, Diabrotica virgifera virgifera LeConte, in Central Europe. Biocontrol News Inf. 19:59N-68N.
21. Lance, D. R., and J. R. Fisher. 1987. Food quality of various plant-tissues for adults of the northern corn-rootworm (Coleoptera: Chrysomelidae). J. Kansas Entomol. Soc. 60:462-466.
22. Lawo, N. C., R. J. Mahon, R. J. Milner, B. K. Sarmah, T. J. V. Higgins, and J. Romeis. 2008. Effectiveness of Bacillus thuringiensis-transgenic chickpeas and the entomopathogenic fungus Metarhizium anisopliae in controlling Helicoverpa armigera (Lepidoptera: Noctuidae). Appl. Environ. Microbiol. 74:4381-4389.
23. Levine, E., and H. Oloumi-Sadeghi. 1991. Management of diabroticite rootworms in corn. Annu. Rev. Entomol. 36:229-255.
24. Li, Y., M. Meissle, and J. Romeis. 2008. Consumption of Bt maize pollen expressing Cry1Ab or Cry3Bb1 does not harm adult green lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae). PLoS ONE 3:e2909.
25. Lord, J. C. 2005. From Metchnikoff to Monsanto and beyond: the path of microbial control. J. Invertebr. Pathol. 89:19-29.
26. Ludwig, K. A., and R. E. Hill. 1975. Comparison of gut contents of adult western and northern corn rootworms in northeast Nebraska. Environ. Entomol. 4:435-438.
27. Meier, U. 2001. Growth stages of mono- and dicotyledonous plants. BBCH monograph, 2nd ed. Federal Biological Research Centre for Agriculture and Forestry, Braunschweig, Germany. http://www.bba.de/veroeff/bbch/bbcheng.pdf. Accessed 20 February 2009.
28. Meihls, L. N., M. L. Higdon, B. D. Siegfried, N. J. Miller, T. W. Sappington, M. R. Ellersieck, T. A. Spencer, and B. E. Hibbard. 2008. Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. Proc. Natl. Acad. Sci. USA 105:19177-19182.
29. Meinke, L. J., T. W. Sappington, D. W. Onstad, T. Guillemaud, N. J. Miller, J. Komáromi, N. Levay, L. Furlan, J. Kiss, and F. Toth. 2009. Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agric. Forest Entomol. 11:29-46.
30. Miller, N. J., T. Guillemaud, R. Giordano, B. D. Siegfried, M. E. Gray, L. J. Meinke, and T. W. Sappington. 2009. Genes, gene flow and adaptation of Diabrotica virgifera virgifera. Agric. Forest Entomol. 11:47-60.
31. Moeser, J., and B. E. Hibbard. 2005. A synopsis of the nutritional ecology of larvae and adults of Diabrotica virgifera virgifera (Le Conte) in the New and Old World - nouvelle cuisine for the invasive maize pest Diabrotica virgifera virgifera in Europe? p. 41-65. In S. Vidal, U. Kuhlmann, and C. R. Edwards (ed.), Western corn rootworm - ecology and management. CABI Publishing, Wallingford, United Kingdom.
32. Monsanto. 2004. Petition for the determination of nonregulated status for MON 88017 Corn. Monsanto Company, St. Louis, MO. http://www.agbios.com/docroot/ decdocs/05-242-047.pdf. Accessed 20 February 2009.
33. Mulock, B., and L. Chandler. 2000. Field-cage studies of Beauveria bassiana (Hyphomycetes: Moniliaceae) for the suppression of adult western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Biocontrol Sci. Technol. 10:51-60.
34. Mulock, B. S., and L. D. Chandler. 2001. Effect of Beauveria bassiana on the fecundity of western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Biol. Control 22:16-21.
35. Oyediran, I. O., M. L. Higdon, T. L. Clark, and B. E. Hibbard. 2007. Interactions of alternate hosts, postemergence grass control, and rootworm-resistant transgenic corn on western corn rootworm (Coleoptera: Chrysomelidae) damage and adult emergence. J. Econ. Entomol. 100:557-565.
36. Pilz, C. 2008. Biological control of the invasive maize pest Diabrotica virgifera virgifera by the entomopathogenic fungus Metarhizium anisopliae. University of Natural Resources and Applied Life Sciences, Vienna, Austria.
37. Pilz, C., R. Wegensteiner, and S. Keller. 2007. Selection of entomopathogenic fungi for the control of the western corn rootworm Diabrotica virgifera virgifera. J. Appl. Entomol. 131:426-431.
38. Pilz, C., R. Wegensteiner, and S. Keller. 2008. Natural occurrence of insect pathogenic fungi and insect parasitic nematodes in Diabrotica virgifera virgifera populations. Biocontrol 53:353-359.
39. Rice, M. E. 2004. Transgenic rootworm corn: assessing potential agronomic, economic, and environmental benefits. Plant Health Progress, doi:10.1094/PHP-2004-0301-01-RV. http://www.plantmanagementnetwork.org/pub/php/ review/2004/rootworm/. Accessed 20 February 2009.
40. Romeis, J., M. Meissle, A. Raybould, and R. L. Hellmich. 2009. Impact of insect-resistant genetically modified crops on above-ground non-target arthropods, p. 165-198. In N. Ferry and A. M. R. Gatehouse (ed.), Environmental impact of genetically modified crops. CABI Publishing, Wallingford, United Kingdom.
41. Shelton, A. M., J. Z. Zhao, and R. T. Roush. 2002. Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol. 47:845-881.
42. Siegfried, B. D., T. T. Vaughn, and T. Spencer. 2005. Baseline susceptibility of western corn rootworm (Coleoptera: Crysomelidae) to Cry3Bb1 Bacillus thuringiensis toxin. J. Econ. Entomol. 98:1320-1324.
43. Strasser, H., A. Forer, and F. Schinner. 1996. Development of media for the selective isolation and maintenance of virulence of Beauveria brongniartii, p. 125-130. In T. A. Jackson, and T. R. Glare (ed.), Proceedings of the 3rd International Workshop on Microbial Control of Soil Dwelling Pests. AgResearch, Lincoln, New Zealand.
44. Tabashnik, B. E., Y. Carriere, T. J. Dennehy, S. Morin, M. S. Sisterson, R. T. Roush, A. M. Shelton, and J. Z. Zhao. 2003. Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J. Econ. Entomol. 96:1031-1038.
45. Tallamy, D. W., B. E. Hibbard, T. L. Clark, and J. J. Gillespie. 2005. Western corn rootworm, cucurbits and curcurbitacins, p. 67-93. In S. Vidal, U. Kuhlmann, and C. R. Edwards (ed.), Western corn rootworm - ecology and management. CABI Publishing, Wallingford, United Kingdom.
46. Toepfer, S., and U. Kuhlmann. 2004. Survey for natural enemies of the invasive alien chrysomelid, Diabrotica virgifera virgifera, in Central Europe. BioControl 49:385-395.
47. Toepfer, S., and U. Kuhlmann. 2006. Constructing life-tables for the invasive maize pest Diabrotica virgifera virgifera (Col.: Chrysomelidae) in Europe. J. Appl. Entomol. 130:193-205.
48. Toth, F., L. Horvath, J. Komaromi, J. Kiss, and E. Szell. 2002. Field data on the presence of spiders preying on western corn rootworm (Diabrotica virgifera virgifera LeConte) in Szeged Region, Hungary. Acta Phytopathol. Entomol. Hung. 37:163-168.
49. Vaughn, T., T. Cavato, G. Brar, T. Coombe, T. DeGooyer, S. Ford, M. Groth, A. Howe, S. Johnson, K. Kolacz, C. Pilcher, J. Purcell, C. Romano, L. English, and J. Pershing. 2005. A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci. 45:931-938.
50. Wraight, S. P., and M. E. Ramos. 2005. Synergistic interaction between Beauveria bassiana- and Bacillus thuringiensis tenebrionis-based biopesticides applied against field populations of Colorado potato beetle larvae. J. Invertebr. Pathol. 90:139-150.