PCR-based identification of Bacillus thuringiensis pesticidal crystal genes

FEMS Microbiology Reviews

Volumn 26, Issue 5, 2003, Pages 419-432

  Porcar, Manuel ^a   Juárez Pérez, Victor ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Endotoxin; Bacillus thuringiensis; Biopesticide; cry gene; cyt gene; Polymerase chain reaction

Indexed keywords

BACTERIAL PROTEIN; PROTEIN CRY; PROTEIN CYT; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACCURACY; ANALYTIC METHOD; BACILLUS THURINGIENSIS; BACTERIAL GENE; BACTERIAL STRAIN; GENE AMPLIFICATION; GENE FREQUENCY; GENE IDENTIFICATION; GENETIC SCREENING; GENETIC VARIABILITY; GEOGRAPHICAL VARIATION (SPECIES); HYBRIDIZATION; INSECTICIDAL ACTIVITY; NONHUMAN; POLYMERASE CHAIN REACTION; PREDICTION; PROTEIN EXPRESSION; PROTEIN INTERACTION; RELIABILITY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; SEQUENCE HOMOLOGY; SEROTYPE; TOXICITY;

BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BASE SEQUENCE; ENDOTOXINS; GENE FREQUENCY; GENES, BACTERIAL; HEMOLYSIN PROTEINS; INSECTICIDES; PEST CONTROL, BIOLOGICAL; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS);

EID: 0037267356     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-6445(02)00128-6     Document Type: Review

References (70)

1. Ishiwata S. On a kind of severe flacherie (sotto disease). Dainihon Sanshi Kaiho. 114:1901;1-5.
2. Berliner E. Über die Schlaffsucht der Mehlmottenraupe. Z. Gesamte Getreidewes. (Berlin). 3:1911;63-70.
3. Goldberg L.H., Margalit J. A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitatus, Aedes aegypti and Culex pipiens. Mosq. News. 37:1977;355-358.
4. Krieg A., Huger A.M., Langenbruch G.A., Schnetter W. Bacillus thuringiensis var. tenebrionis: ein neuer gegenuber arven von Coleopteren wirksamer athotyp. Z. Ang. Ent. 96:1983;500-508.
5. Feitelson, J.S. (1993) The Bacillus thuringiensis family tree. In: Advanced Engineered Pesticides (Kim, L., Ed.), pp. 63-71. Marcel Dekker, New York.
6. Höfte H., Whiteley H.R. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 53:1989;242-255.
7. Lüthy, P. and Wolfersberger, M.G. (2000) Pathogenisis of Bacillus thuringiensis toxins. In: Entomopathogenic Bacteria: From Laboratory to Field Application (Charles, J.F., Delécluse, A. and Nielsen-LeRoux, C., Eds.), pp. 167-180. Kluwer Academic Publishers, Dordrecht.
8. Schwart, J.L. and Laprade, R. (2000) Membrane permeabilization by Bacillus thuringiensis toxins: protein formation and pore insertion. In: Entomopathogenic Bacteria: From Laboratory to Field Application (Charles, J.F., Delécluse, A. and Nielsen-LeRoux, C., Eds.), pp. 199-218. Kluwer Academic Publishers, Dordrecht.
9. Martínez, C. (2002) Biological and Genetic Characterization of Bacillus thuringiensis Strains Toxic against Helicoverpa armigera, 573 pp. UPNA, Pamplona.
10. Kleppe K., Ohtsuka E., Kleppe R., Molineaux I., Khorana H.G. Studies on polynucleotides. XCVI. Repair replications of short synthetic DNA's catalyzed by DNA polymerases. J. Mol. Biol. 56:1971;341-361.
11. Saiki R.K., Gelfand D.H., Stoffel S., Scharf S.J., Higuchi R., Horn G.T., Mullis K.B., Erlich H.A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 239:1988;487-489.
12. Carozzi N.B., Kramer V.C., Warren G.W., Evola S., Koziel M.G. Prediction of insecticidal activity of Bacillus thuringiensis strains by polymerase chain reaction product profiles. Appl. Environ. Microbiol. 57:1991;3057-3061.
13. Gleave A.P., Williams R., Hedges R.J. Screening by polymerase chain reaction of Bacillus thuringiensis serotypes for the presence of cryV-like insecticidal protein genes and characterization of a cryV gene cloned from B. thuringiensis subsp. kurstaki. Appl. Environ. Microbiol. 59:1993;1683-1687.
14. Chak K.-F., Chao D.-C., Tseng M.-Y., Kao S.-S., Tuan S.-J., Feng T.-Y. Determination and distribution of cry-type genes of Bacillus thuringiensis isolates from Taiwan. Appl. Environ. Microbiol. 60:1994;2415-2420.
15. Cerón J., Ortíz A., Quintero R., Güereca L., Bravo A. Specific PCR primers directed to identify cryI and cryIII genes within a Bacillus thuringiensis strain collection. Appl. Environ. Microbiol. 61:1995;3826-3831.
16. Ben-Dov E., Zaritsky A., Dahan E., Barak Z., Sinai R., Manasherob R., Khamraev A., Troitskaya E., Dubitsky A., Berezina N., Margalith Y. Extended screening by PCR for seven cry-group genes from field-collected strains of Bacillus thuringiensis. Appl. Environ. Microbiol. 63:1997;4883-4890.
17. Bravo A., Sarabia S., Lopez L., Ontiveros H., Abarca C., Ortiz A., Ortiz M., Lina L., Villalobos F.J., Peña G., Nuñez-Valdez M.E., Soberon M., Quintero R. Characterization of cry genes in a Mexican Bacillus thuringiensis strain collection. Appl. Environ. Microbiol. 64:1998;4965-4972.
18. Ferrandis M.D., Juárez-Pérez V.M., Frutos R., Bel Y., Ferré J. Distribution of cryI, cryII and cryV genes within Bacillus thuringiensis isolates from Spain. Syst. Appl. Microbiol. 22:1999;179-185.
19. Guerchicoff A., Ugalde R.A., Rubinstein C.P. Identification and characterization of a previously undescribed cyt gene in Bacillus thuringiensis subsp. israelensis. Appl. Environ. Microbiol. 63:1997;2716-2721.
20. Guerchicoff A., Delécluse A., Rubinstein C.P. The Bacillus thuringiensis cyt genes for hemolytic endotoxins constitute a gene family. Appl. Environ. Microbiol. 67:2001;1090-1096.
21. Ejiofor A.O., Johnson T. Physiological and molecular detection of crystalliferous Bacillus thuringiensis strains from habitats in the South Central United States. J. Indian Microbiol. Biotechnol. 28:2002;284-290.
22. Masson L., Erlandson M., Puzstai-Carey M., Brousseau R., Juárez-Pérez V., Frutos R. A holistic approach for determining the entomopathogenic potential of Bacillus thuringiensis strains. Appl. Environ. Microbiol. 64:1998;4782-4788.
23. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:1998;775-806.
24. Juárez-Pérez V.M., Ferrandis M.D., Frutos R. PCR-based approach for detection of novel Bacillus thuringiensis cry genes. Appl. Environ. Microbiol. 63:1997;2997-3002.
25. Juárez-Pérez, V. (1998) Caractérisation de Nouveaux Gènes d'Endotoxines de Bacillus thuringiensis Berliner, 156 pp. ENSA/AGRO, Montpellier.
26. Bourque S.N., Valero J.R., Mercier J., Lavoie M.C., Levesque R.C. Multiplex polymerase chain reaction for detection and differentiation of the microbial insecticide Bacillus thuringiensis. Appl. Environ. Microbiol. 59:1993;523-527.
27. Shin B.-S., Park S.-H., Choi S.-K., Koo B.-T., Lee S.-T., Kim J.-I. Distribution of cryV-type insecticidal protein genes in Bacillus thuringiensis and cloning of cryV-type genes from Bacillus thuringiensis subsp. kurstaki and Bacillus thuringiensis subsp. entomocidus. Appl. Environ. Microbiol. 61:1995;2402-2407.
28. Cerón J., Covarrubias L., Quintero R., Ortíz A., Ortíz M., Aranda E., Lina L., Bravo A. PCR analysis of the cryI insecticidal family genes from Bacillus thuringiensis. Appl. Environ. Microbiol. 60:1994;353-356.
29. Kalman S., Kiehne K.L., Libs J.L., Yamamoto T. Cloning of a novel cryIC-type gene from a strain of Bacillus thuringiensis subsp. galleriae. Appl. Environ. Microbiol. 59:1993;1131-1137.
30. Kim H.S., Lee D.W., Woo S.D., Yu Y.M., Kang S.K. Distribution, serological identification, and PCR analysis of Bacillus thuringiensis isolated from soils of Korea. Curr. Microbiol. 37:1998;195-200.
31. Wilson I.G., Cooper J.E., Gilmour A. Detection of enterotoxigenic Staphylococcus aureus in dried skimmed milk: use of the polymerase chain reaction for amplification and detection of staphylococcal enterotoxin genes entB and entC1 and the thermonuclease gene nuc. Appl. Environ. Microbiol. 57:1991;1793-1798.
32. Wilson I.G. Inhibition and facilitation of nucleic acid amplification. Appl. Environ. Microbiol. 63:1997;3741-3751.
33. Roux K.H. Optimization and troubleshooting in PCR. PCR Methods Appl. 4S:1995;185-194.
34. Kwok S., Seng-Yung C., Sninsky J.J., Wang A. A guide to design and use of mismatched and degenerated primers. PCR Methods Appl. 4S:1994;39-47.
35. Aronson A.I., Wu D., Zhang C. Mutagenesis of specificity and toxicity regions of a Bacillus thuringiensis protoxin gene. J. Bacteriol. 177:1995;4059-4065.
36. Dean D.H., Rajamohan F., Lee M.K., Wu S.J., Chen X.J., Alcantara E., Hussain S.R. Probing the mechanism of action of Bacillus thuringiensis insecticidal proteins by site-directed mutagenesis: a minireview. Gene. 179:1996;111-117.
37. Barboza-Corona J.E., Lopez-Meza J.E., Ibarra J.E. Cloning and expression of the cry1Ea4 gene of Bacillus thuringiensis and the comparative toxicity of its gene product. World J. Microbiol. Biotechnol. 14:1998;437-441.
38. Kostichka K., Warrren G.W., Mullins M., Mullins A.D., Craig J.A., Koziel M.G., Estruch J.J. Cloning of a cryV-type insecticidal protein gene from Bacillus thuringiensis: the cryV-encoded protein is expressed early in stationary phase. J. Bacteriol. 178:1996;2141-2144.
39. Cheng P., Wu L., Ziniu Y., Aronson A.I. Subspecies-dependent regulation of Bacillus thuringiensis protoxin genes. Appl. Environ. Microbiol. 65:1999;1849-1853.
40. Wu D., Chang F.N. Synergism in mosquitocidal activity of 26 and 65 kDa proteins from Bacillus thuringiensis subsp. israelensis crystal. FEBS Lett. 190:1985;232-236.
41. Ibarra J.E., Federici B.A. Parasporal bodies of Bacillus thuringiensis subsp. morrisoni (PG-14) and Bacillus thuringiensis subsp. israelensis are similar in protein composition and toxicity. FEMS Microbiol. Lett. 34:1986;79-84.
42. Delécluse, A., Juárez-Pérez, V. and Berry, C. (2000) Vector-active toxins: structure and diversity. In: Entomopathogenic Bacteria: From Laboratory to Field Application (Charles, J.F., Delécluse, A. and Nielsen-LeRoux, C., Eds.), pp. 101-125. Kluwer Academic Publishers, Dordrecht.
43. Wirth M.C., Walton W.E., Federici B.A. Cyt1A from Bacillus thuringiensis restores toxicity of Bacillus sphaericus against resistant Culex quinquefasciatus (Diptera: Culicidae). J. Med. Entomol. 37:2000;401-407.
44. Federici B.A., Bauer L.S. Cyt1Aa protein of Bacillus thuringiensis is toxic to the cottonwood leaf beetle, Chrysomela scripta, and suppresses high levels of resistance to Cry3Aa. Appl. Environ. Microbiol. 64:1998;4368-4371.
45. Lee M.K., Curtiss A., Alcantara E., Dean D.H. Synergistic effect of the Bacillus thuringiensis toxins Cry1Aa and Cry1Ac on the gypsy moth, Lymantria dispar. Appl. Environ. Microbiol. 62:1996;583-586.
46. Aronson A.I., Han E.-S., McGaughey W., Johnson D. The solubility of inclusion proteins from Bacillus thuringiensis is dependent upon protoxin composition and is a factor in toxicity to insects. Appl. Environ. Microbiol. 57:1991;981-986.
47. Del Rincón-Castro M.C., Barajas-Huerta J., Ibarra J.E. Antagonism between Cry1Ac1 and Cyt1A1 toxins of Bacillus thuringiensis. Appl. Environ. Microbiol. 65:1999;2049-2053.
48. Li R.S., Jarrett P., Burges H.D. Importance of spores, crystals, and delta-endotoxins in the pathogenicity of different varieties of Bacillus thuringiensis in Galleria mellonella and Pieris brassicae. J. Invertebr. Pathol. 50:1987;277-284.
49. Miyasono M., Inagaaki S., Yamamoto M., Ohba K., Ishiguro T., Takeda R., Hayashi Y. Enhancement of δ-endotoxin activity by toxin-free spore of Bacillus thuringiensis against the Diamondback Moth, Plutella xylostella. J. Invertebr. Pathol. 63:1994;111-112.
50. Johnson D.E., McGaughey W.H. Contribution of Bacillus thuringiensis spores to toxicity of purified Cry proteins towards indianmeal moth larvae. Curr. Microbiol. 33:1996;54-59.
51. Porcar M., Martínez C., Caballero P. Host range and gene contents of Bacillus thuringiensis strains toxic towards Spodoptera exigua. Entomol. Exp. Appl. 97:2000;339-346.
52. Chambers J.A., Jelen A., Gilbert M.P., Jany C.S., Johnson T.B., Gawron-Burke C. Isolation and characterization of a novel insecticidal crystal protein gene from Bacillus thuringiensis subsp. aizawai. J. Bacteriol. 173:1991;3966-3976.
53. Sanchis V., Lereclus D., Menou G., Chaufaux J., Lecadet M.-M. Multiplicity of δ-endotoxin genes with different specificities in Bacillus thuringiensis aizawai 7.29. Mol. Microbiol. 2:1988;393-404.
54. Hongyu Z., Ziniu Y., Wangxi D. Composition and ecological distribution of Cry proteins and their genotypes of Bacillus thuringiensis isolates from warehouses in China. J. Invertebr. Pathol. 76:2000;191-197.
55. Lereclus, D., Delécluse, A. and Lecadet, M.-M. (1993) Diversity of Bacillus thuringiensis toxins and genes. In: Bacillus thuringiensis and Environmental Biopesticide: Theory and Practice (Entwistle, P.S., Cory, J.S., Bailey, M.J. and Higgs, S.R., Eds.), pp. 309-329. Wiley, London.
56. Lecadet M.M., Frachon E., Dumanoir V.C., Ripouteau H., Hamon S., Laurent P., Thiéry I. Updating the H-antigen classification of Bacillus thuringiensis. J. Appl. Microbiol. 86:1999;660-672.
57. Dulmage, H.T. (1981) Insectidal activity of isolates of Bacillus thuringiensis and their potential for pest control. In: Microbial Control of Pests and Plant Diseases (Burges, H.D., Ed.), pp. 193-223. Academic Press, London.
58. Glare, T.R. and O'Callaghan, M. (2000) A case study: toxicity of Dipal, Bt kurstaki produced by Abbatt Laboratories. In: Bacillus thuringiensis: Biology, Ecology and Safety, pp. 311-316. Wiley, Chichester.
59. Kuo W.S., Lin J.H., Tzeng C.C., Kao S.S., Chak K.F. Cloning of two new cry genes from Bacillus thuringiensis subsp wuhanensis strain. Curr. Microbiol. 40:2000;227-232.
60. Kuo W.S., Chak K.F. Identification of novel cry-type genes from Bacillus thuringiensis strains on the basis of restriction fragment length polymorphism of the PCR-amplified DNA. Appl. Environ. Microbiol. 62:1996;1367-1377.
61. Crickmore N., Zeigler D.R., Feitelson J., Schnepf E., Van Rie J., Lereclus D., Baum J., Dean D.H. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:1998;807-813.
62. Beard C.E., Ranasinghe C., Akhurst R.J. Screening for novel cry genes by hybridization. Lett. Appl. Microbiol. 33:2001;241-245.
63. Chestukhina G.C., Kostina L.I., Mikahilova S.A., Tyurin F., Klepikova S., Stepanov M. Production of multiple δ-endotoxins by Bacillus thuringiensis: δ-endotoxins produced by strains of the subspecies galleriae and wuhanensis. Can. J. Microbiol. 40:1994;1026-1034.
64. Rabilloud T. Two-dimensional gel electrophoresis in proteomics: old, old-fashioned but it still climbs up the mountains. Proteomics. 2:2002;3-10.
65. Tabashnik B.E. Evaluation of synergism among Bacillus thuringiensis toxins. Appl. Environ. Microbiol. 58:1992;3343-3346.
66. Ben-Dov E., Manasherob R., Zaritsky A., Barak Z., Margalith Y. PCR analysis of cry7 genes in Bacillus thuringiensis by the five conserved blocks of toxins. Curr. Microbiol. 42:2001;96-99.
67. Wasano N., Ohba M., Miyamoto K. Two δ-endotoxin genes, cry9Da and a novel related gene, commonly occurring in Lepidoptera-specific Bacillus thuringiensis Japanese isolates that produce spherical parasporal inclusions. Curr. Microbiol. 42:2001;129-133.
68. Porcar M., Iriarte J., Dumanoir V.C., Ferrandis M.D., Lecadet M.M., Ferré J., Caballero P. Identification and characterization of the new Bacillus thuringiensis serovars pirenaica (serotype H57) and iberica (serotype H59). J. Appl. Microbiol. 87:1999;640-648.
69. Rang, C. (1996) Etude des relations structure - Fonction chez les endotoxins de Bacillus thuringiensis. University of Montpellier II, Montpellier, 145 pp.
70. Barloy F., Lecadet M.M., Delécluse A. Distribution of clostridial cry-like genes among Bacillus thuringiensis and Clostridium strains. Curr. Microbiol. 36:1998;232-237.