Interaction between crystalline proteins of two Bacillus thuringiensis strains against Spodoptera exigua

Entomologia Experimentalis et Applicata

Volumn 143, Issue 2, 2012, Pages 148-154

  Konecka, Edyta ^a   Baranek, Jakub ^a   Kaznowski, Adam ^a   Ziemnicka, Jadwiga ^b   Ziemnicki, Kazimierz ^a  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b INSTITUTE OF PLANT PROTECTION NATIONAL RESEARCH INSTITUTE   (Poland)

Author keywords

Additive effect; Bacterial toxins; Beet armyworm; Insecticidal activity; Lepidoptera; Noctuidae; Plant protection; Synergism

Indexed keywords

BACTERIUM; CATERPILLAR; CONCENTRATION (COMPOSITION); DEVELOPMENTAL BIOLOGY; ESTIMATION METHOD; INSECTICIDE; MOTH; PEST SPECIES; PROTEIN; SPORE; SYNERGISM; TOXICITY; TOXIN;

BACILLUS THURINGIENSIS; BACILLUS THURINGIENSIS SEROVAR BERLINER; BACTERIA (MICROORGANISMS); HEXAPODA; LEPIDOPTERA; NOCTUIDAE; SPODOPTERA EXIGUA;

EID: 84859571254     PISSN: 00138703     EISSN: 15707458     Source Type: Journal    
DOI: 10.1111/j.1570-7458.2012.01254.x     Document Type: Article

References (52)

1. ®) against beet armyworm and fall armyworm larvae (Lepidoptera: Noctuidae). Florida Entomologist 87: 427-432.
2. Bakuniak E (1973) Metodyka badań współdziałania substancji owadobójczych stosowanych w postaci dwuskładnikowych mieszanin. Polskie Pismo Entomologiczne 43: 395-414 [in Polish].
3. Beegle CC, Couch TL, Alls RT, Versoi PL & Lee BL (1986) Standarization of HD-1-S-1980: U.S. Standard for Assay of Lepidopterous-active Bacillus thuringiensis. Bulletin of the Entomological Society of America 32: 44-45.
4. Ben-Dov E, Zaritsky A, Dahan E, Barak Z, Sinai R et al. (1997) Extended screening by PCR for seven cry-group genes from field-collected strains of Bacillus thuringiensis. Applied and Environmental Microbiology 63: 4883-4890.
5. Bessin R (2003) Beet Armyworm in Kentucky, EntFact 308. Available at: (accessed 05 August 2011).
6. Bravo A, Sarabia S, Lopez L, Ontiveros H, Abarca C et al. (1998) Characterization of cry genes in a Mexican Bacillus thuringiensis strain collection. Applied and Environmental Microbiology 64: 4965-4972.
7. Capinera JL (1999) Beet Armyworm, Spodoptera exigua (Hübner) (Insecta: Lepidoptera: Noctuidae). Featured Creatures EENY105. Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL, USA. Available at: (accessed 05 August 2011).
8. Donovan WP, Donovan J & Engleman JT (2001) Gene knockout demonstrates that vip3A contributes to the pathogenesis of Bacillus thuringiensis toward Agrotis ipsilon and Spodoptera exigua. Journal of Invertebrate Pathology 78: 45-51.
9. van Frankenhuyzen K (2009) Insecticidal activity of Bacillus thuringiensis crystal proteins. Journal of Invertebrate Pathology 101: 1-16.
10. Gao Y, Hu Y, Fu Q, Zhang J, Oppert B et al. (2010) Screen of Bacillus thuringiensis toxins for transgenic rice to control Sesamia inferens and Chilo suppressalis. Journal of Invertebrate Pathology 105: 11-15.
11. Gilliland A, Chambers CE, Bone EJ & Ellar DJ (2002) Role of Bacillus thuringiensis Cry1 δ endotoxin binding in determining potency during lepidopteran larval development. Applied and Environmental Microbiology 68: 1509-1515.
12. Ginsburg C (2006a) Aerial spraying of Bacillus thuringiensis kurstaki (Btk). Journal of Pesticide Reform 26: 13-16.
13. Ginsburg C (2006b) The Safety to Humans of Bacillus thuringiensis Insecticidal Sprays: a Reassessment. No Spray Zone, Seattle, WA, USA. Available at: (accessed 05 August 2011).
14. Guz K, Kucińska J, Lonc E & Doroszkiewicz W (2005) Differentiated pattern of protein composition of crystalline inclusions of newly isolated Bacillus thuringiensis strains from Silesia in Poland. Polish Journal of Microbiology 54: 263-269.
15. Hansen BM, Damaard PH, Eilenberg J & Pedersen JCh (1998) Molecular and phenotypic characterization of Bacillus thuringiensis isolated from leaves and insects. Journal of Invertebrate Pathology 71: 106-114.
16. Hernández CS & Ferré J (2005) Common receptor for Bacillus thuringiensis toxins Cry1Ac, Cry1Fa, and Cry1Ja in Helicoverpa armigera, Helicoverpa zea, and Spodoptera exigua. Applied and Environmental Microbiology 71: 5627-5629.
17. Hernandez E, Ramisse F, Cruel T, le Vagueresse R & Cavallo JD (1999) Bacillus thuringiensis serotype H34 isolated from human and insecticidal strains serotypes 3a3b and H14 can lead to death of immunocompetent mice after pulmonary infection. FEMS Immunology and Medical Microbiology 24: 43-47.
18. Hernandez E, Ramisse F, Gros P & Cavallo JD (2000) Super-infection by Bacillus thuringiensis H34 or 3a3b can lead to death in mice infected with the influenza A virus. FEMS Immunology and Medical Microbiology 29: 177-181.
19. Hernández CS, Martínez C, Pocar M, Caballero P & Ferré J (2003) Correlation between serovars of Bacillus thuringiensis and type I β-exotoxin production. Journal of Invertebrate Pathology 82: 57-62.
20. Hernández-Martínez P, Ferré J & Escriche B (2008) Susceptibility of Spodoptera exigua to 9 toxins from Bacillus thuringiensis. Journal of Invertebrate Pathology 97: 245-250.
21. Hernández-Martínez P, Ferré J & Escriche B (2009) Broad-spectrum cross-resistance in Spodoptera exigua from selection with a marginally toxic Cry protein. Pest Management Science 65: 645-650.
22. Huffman R, Fuchs T, Benedict J, Parker R, Sparks S et al. (1996) 1996 Management Guidelines for the Beet Armyworm on Cotton. Texas Agricultural Extension Service, Texas A&M University System, College Station, TX, USA. Available at: (Accessed 05 August 2011).
23. Hughes PA, Stevens MM, Park HW, Federici BA, Dennis ES & Akhurst R (2005) Response of larval Chironomus tepperi (Diptera: Chironomidae) to individual Bacillus thuringiensis var. israelensis toxins and toxin mixtures. Journal of Invertebrate Pathology 88: 34-39.
24. Hurley JM, Bulla LA & Andrews RE (1987) Purification of the mosquitocidal and cytolytic proteins of Bacillus thuringiensis var. israelensis. Applied and Environmental Microbiology 53: 1316-1321.
25. Ibargutxi MA, Muńoz D, de Escudero IR & Caballero P (2008) Interactions between Cry1Ac, Cry2Ab, and Cry1Fa Bacillus thuringiensis toxins in the cotton pests Helicoverpa armigera (Hübner) and Earias insulana (Boisduval). Biological Control 47: 89-96.
26. Konecka E, Kaznowki A, Ziemnicka J, Ziemnicki K & Paetz H (2007) Analysis of cry gene profiles in Bacillus thuringiensis strains isolated during epizootics in Cydia pomonella L. Current Microbiology 55: 217-222.
27. Konecka E, Ziemnicka J, Baranek J & Kaznowski A (2010) Potential usefulness of Bacillus thuringiensis MPU B9 protein crystals for reducing the number of white satin moth (Leucoma salicis L.). Progress in Plant Protection 50: 357-360 [in Polish].
28. Lecadet MM, Cosmao Dumanoir V, Frachon E & Ripouteau H (1994) Collection of Bacillus thuringiensis and Bacillus sphaericus (Classified by H Serotypes) Catalogue No 1. International Entomopathogenic Bacillus Centre, WHO Collaborating Centre, Institut Pasteur Paris, France.
29. Lee MK, Curtiss A, Alcantara E & Dean DH (1996) Synergistic effect of the Bacillus thuringiensis toxins CryIAa and CryIAc on the gypsy moth, Lymantria dispar. Applied and Environmental Microbiology 62: 583-586.
30. Lee IH, Je YH, Chang JH, Roh JY, Oh HW et al. (2011) Isolation and characterization of a Bacillus thuringiensis ssp. kurstaki strain toxic to Spodoptera exigua and Culex pipiens. Current Microbiology 43: 284-287.
31. Li MS, Je YH, Lee IH, Chang JH, Roh JY et al. (2002) Isolation and characterization of a strain of Bacillus thuringiensis ssp. kurstaki containing a new δ-endotoxin gene. Current Microbiology 45: 299-302.
32. 50) w patologii owadów i toksykologii. Prace Naukowe Instytutu Ochrony Roślin 15: 59-83 [in Polish].
33. Luo K, Banks D & Adang MJ (1999a) Toxicity, binding, and permeability analyses of four Bacillus thuringiensis Cry1 δ-endotoxins using brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Applied and Environmental Microbiology 65: 457-464.
34. de Maagd RA, Bakker P, Staykov N, Dukiandjiev S, Stiekema W & Bosch D (1999) Identification of Bacillus thuringiensis delta-endotoxin Cry1C domain III amino acid residues involved in insect specificity. Applied and Environmental Microbiology 65: 4369-4374.
35. de Maagd RA, Bravo A, Berry C, Crickmore N & Schnepf HE (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annual Review of Genetics 37: 409-433.
36. Maheswaran S, Sreeramanan S, Reena Josephine CM, Marimuthu K & Xavier R (2010) Occurrence of Bacillus thuringiensis in faeces of herbivorous farm animals. African Journal of Biotechnology 9: 8013-8019.
37. Martin PA & Travers RS (1989) Worldwide abundance and distribution of Bacillus thuringiensis isolates. Applied and Environmental Microbiology 55: 2437-2442.
38. Masson L, Erlandson M, Puzstai-Carey M, Brousseau R, Juárez-Pérez VM & Frutos R (1998) A holistic approach for determining the entomopathogenic potential of Bacillus thuringiensis strain. Applied and Environmental Microbiology 64: 4782-4788.
39. Meadows MP, Ellis DJ, Butt J, Jarrett P & Burges HD (1992) Distribution, frequency, and diversity of Bacillus thuringiensis in an animal feed mill. Applied and Environmental Microbiology 58: 1344-1350.
40. Milne R, Liu Y, Gauthier D & van Frankenhuyzen K (2008) Purification of Vip3Aa from Bacillus thuringiensis HD-1 and its contribution to toxicity of HD-1 to spruce budworm (Choristoneura fumiferana) and gypsy moth (Lymantria dispar) (Lepidoptera). Journal of Invertebrate Pathology 99: 166-172.
41. Nazarian A, Jahangiri R, Jouzani GS, Seifinejad A, Soheilivand S et al. (2009) Coleopteran-specific and putative novel cry genes in Iranian native Bacillus thuringiensis collection. Journal of Invertebrate Pathology 102: 101-109.
42. Poitout S & Bues R (1970) Élevage de plusieurs espèces de Lépodoptères Noctuidae sur milieu artificiel riche et sur milieu artificiel simplifié. Annales de Zoologie Écologie Animale I: 79-91.
43. Porcar M, Martínez C & Caballero P (2000) Host range and gene contents of Bacillus thuringiensis strains toxic towards Spodoptera exigua. Entomologia Experimentalis et Applicata 97: 339-346.
44. Schnepf E, Crickmore N, van Rie J, Lereclus D, Baum J et al. (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews 62: 775-806.
45. Smirnoff WA (1962) A staining method for differentiating spores, crystals, and cells of Bacillus thuringiensis (Berliner). Journal of Insect Pathology 4: 384-386.
46. Tabashnik BE (1992) Evaluation of synergism among Bacillus thuringiensis toxins. Applied and Environmental Microbiology 58: 3343-3346.
47. Vidal-Quist JC, Castañera P & González-Cabrera J (2009) Diversity of Bacillus thuringiensis strains isolated from citrus orchards in Spain and evaluation of their insecticidal activity against Ceratitis capitata. Journal of Microbiology and Biotechnology 19: 749-759.
48. Wirth MC, Georghiou GP & Federici BA (1997) CytA enables CryIV endotoxins of Bacillus thuringiensis to overcome high levels of CryIV resistance in the mosquito, Culex quinquefasciatus. Proceedings of the National Academy of Sciences of the USA 94: 10536-10540.
49. Xue JL, Cai QX, Zheng DS & Yuan ZM (2005) The synergistic activity between Cry1Aa and Cry1c from Bacillus thuringiensis against Spodoptera exigua and Helicoverpa armigera. Letters in Applied Microbiology 40: 460-465.
50. Zhu YS, Brookes A, Carlson K & Filner P (1998) Separation of protein crystals from spores of Bacillus thuringiensis by Ludox gradient centrifugation. Applied and Environmental Microbiology 55: 1279-1281.
51. Zhu C, Ruan L, Peng D, Yu Z & Sun M (2005) Vegetative insecticidal protein enhancing the toxicity of Bacillus thuringiensis subsp kurstaki against Spodoptera exigua. Letters in Applied Microbiology 42: 109-114.
52. Ziemnicka J & Ziemnicki K (2001) Bacillus thuringiensis: an epizootic agent in laboratory cultures of codling moth (Cydia pomonella L.). Progress in Plant Protection 41: 503-508 [in Polish].