ORIGINAL ARTICLE
Larvicidal activity of Bacillus thuringiensis Colombian native strains against Bemisia tabaci (Hemiptera: Aleyrodidae)
1
Department of Sciences and Agricultural Sciences, Faculty of Science of Agricultural, Juan de Castellanos University Foundation, Tunja, Colombia
2
Department of Natural Science and Environmental, Faculty of Science and Engineering, Jorge Tadeo Lozano University, Bogotá, Colombia
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Submission date: 2018-11-07
Acceptance date: 2019-06-14
Online publication date: 2020-01-22
Corresponding author
Javier Adolfo Hernandez Fernandez
Department of Natural Science and Environmental, Faculty of Science and Engineering, Jorge Tadeo Lozano University, Bogotá, Colombia
Department of Natural Science and Environmental, Faculty of Science and Engineering, Jorge Tadeo Lozano University, Bogotá, Colombia
Journal of Plant Protection Research 2019;59(4):503-511
KEYWORDS
TOPICS
ABSTRACT
The whitefly, Bemisia tabaci, an insect of the order Hemiptera which attacks more than 600 species of plants, is one of the most important agricultural pests around the world. The insecticidal Cry proteins from Bacillus thuringiensis (Bt) are useful biological pesticides, and some are toxic to Hemipteran insects. In this study, Colombian native isolates of Bt were functionally characterized at molecular and biological levels. The strains contained between one and five different crystal shapes: round, triangular, amorphous, bipyramidal and squared. The strains presented between three to seven bands of proteins in their electrophoretic pattern that were organized into six groups according to their possible biological activity on insect pests. Cry1Aa, cry1Ab, cry1Ac, cry1B and cry1C genes were identified for PCR in the different Bt isolates. Bioassays were performed on tomato leaves whose surface was spread with 3 μg · ml−1 crude extract of Bt toxins. Second instar larvae of whitefly, which were placed on top of leaves and exposed to the toxins for 7 days, exhibited mortalities from 18 to 69%. The lethal concentration 50 (LC50) of ZBUJTL39, Bt kurstaki HD1 and ZCUJTL9 strains were 1.83, 1.85 and 2.16 μg · ml−1, respectively (p < 0.05). These results
show that the native Bt strain ZBUJTL39, which contained the genes cry1Aa, cry1Ab, cryCa and cryBa could eventually be used for the development of an integrated management program together with other tools for the control of B. tabaci.
ACKNOWLEDGEMENTS
This work was supported by the Office of Research, Creation and Extension of the Universidad Jorge Tadeo Lozano.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (59)
1.
Al-Shayji Y., Shaheen N. 2008. Isolation of Bacillus thuringiensis strain from Kuwait’s soil effective against whitefly nymphs. Journal of Insect Science 8 (4): 53–59.
2.
Arango J., Romero A.M., Orduz S. 2002. Diversity of Bacillus thuringiensis strains from Colombia with insecticidal activity against Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal Applied Microbiology 92 (3): 466−474. DOI: https://doi.org/10.1046/j.1365....
3.
Asokan R., Swamy H.M., Thimmegowda G.G., Mahmood R. 2014. Diversity analysis and characterization of Coleoptera, Hemiptera and Nematode-active cry genes in native isolates of Bacillus thuringiensis. Annals of Microbiology 64 (1): 85−98. DOI: https://doi.org/10.1007/s13213....
4.
Bargen H., Saudhof K., Poehling H.M. 1998. Prey finding by larvae and adult females of Episyrphus balteatus. Entomologia Experimentalis et Applicata 87 (3): 245−254. DOI: https://doi.org/10.1046/j.1570....
5.
Barloy F., Delécluse A., Nicolas L., Lecadet M.M. 1996. Cloning and expression of the first anaerobic toxin gene from Clostridium bifermentans subsp. malaysia, encoding a new mosquitocidal protein with homologies to Bacillus thuringiensis delta-endotoxins. Journal of Bacteriology 178 (11): 3099−3105. DOI: 10.1128/jb.178.11.3099-3105.1996.
6.
Basit M., Saeed S., Saleem M.A., Denholm I., Shah M. 2013. Detection of resistance, cross-resistance, and stability of resistance to new chemistry insecticides in Bemisia tabaci (Hemiptera: Aleyroridae). Journal of Economic Entomology 106 (3): 1414−1422. DOI: https://doi.org/10.1603/EC1241....
7.
Baum J.A., Sukuru U.R., Penn S.R., Meyer S.E., Subbarao S., Shi X., Clark T.L. 2012. Cotton plants expressing a hemipteran-active Bacillus thuringiensis crystal protein impact the development and survival of Lygus hesperus (Hemiptera: Miridae) nymphs. Journal of Economic Entomology 105 (2): 616−624. DOI: https://doi.org/10.1603/EC1120....
8.
Bradford M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1): 248−254. DOI: https://doi.org/10.1016/0003-2....
9.
Bravo A., Hendrickx K., Jansens S., Peferoen M. 1992. Immunocytochemical analysis of specific binding of Bacillus thuringiensis insecticidal crystal proteins to lepidopteran and coleopteran mudgut membranes. Journal of Invertebrate Pathology 60 (3): 247−253. DOI: https://doi.org/10.1016/0022-2....
10.
Bravo A., Sarabia S., López L., Ontiveros H., Abarca C., Ortiz A., Quintero R. 1998. Characterization of cry genes in a Mexican Bacillus thuringiensis strain collection. Applied and Environmental Microbiology 64 (12): 4965−4972.
11.
Cerón J., Covarrubias L., Quintero R., Ortiz A., Ortiz M., Aranda E., Bravo A. 1994. PCR analysis of the cryI insecticidal crystal family genes from Bacillus thuringiensis. Applied and Environmental Microbiology 60 (1): 353−356.
12.
Cerón J., Ortíz A., Quintero R., Güereca L. Bravo A. 1995. Specific PCR primers directed to identify cryI and cryIII genes within a Bacillus thuringiensis strain collection. Applied and Environmental Microbiology 61 (11): 3826−3831.
13.
Chougule N.P., Li H., Liu S., Linz L.B., Narva K.E., Meade T., Bonning B.C. 2013. Retargeting of the Bacillus thuringiensis toxin Cyt2Aa against hemipteran insect pests. Proceedings of the National Academy of Sciences 110 (21): 8465−8470. DOI: https://doi.org/10.1073/pnas.1....
14.
Crickmore N. 2019. Bacillus thuringiensis toxin nomenclature. Available on: http://www.lifesci.sussex.ac.u... [Accessed: 25 July 2018].
15.
Crickmore N., Zeigler D.R., Feitelson J., Schnepf E., Van Rie J., Lereclus D., Dean D.H. 1998. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiology and Molecular Biology Reviews 62 (3): 807−813.
16.
Davidson E.W., Patron R.B., Lacey L.A., Frutos R., Vey A., Hendrix D.L.1996. Activity of natural toxins against the silver leaf whitefly, Bemisia argentifolii, using a novel feeding bioassay system. Entomologia Experimentalis et Applicata 79 (1): 25−32. DOI: https://doi.org/10.1111/j.1570....
17.
El-Assal S.E.D., Youssef N.A., Amin G.A. 2013. Isolation and identification of locally isolated bacterial strains effective against whitefly Bemisia tabaci. Archives of Agronomy and Soil Science 59 (6): 779−790. DOI: https://doi.org/10.1080/036503....
18.
Espinel C., Torres L., Grijalba E., Villamizar L., Cotes A.M. 2008. Preformulados para control de la mosca blanca Bemisia tabaci (Hemiptera: Aleyrodidae) en condiciones de laboratorio. Revista Colombiana de Entomología 34 (1): 22−28.
19.
Feiltelson J.S., Payne J., Kim L. 1992. Bacillus thuringiensis: insects and beyond. Nature Biotechnology 10 (3): 271−275. DOI: https://doi.org/10.1038/nbt039....
20.
Garcia-Robles I., Sánchez J., Gruppe A., Martínez-Ramí-rez A.C., Rausell- Real M.D., Bravo A. 2001. Mode of action of Bacillus thuringiensis PS86Q3 strain in hymenopteran forest pests. Insect Biochemistry and Molecular Biology 31 (9): 849−856. DOI: https://doi.org/10.1016/S0965-....
21.
González A. 2011. Evaluation of entomopathogens for the control of whitefly (Bemisia tabaci Genn.) in tomato (Lycopersicon esculentum Mill.). (No. SB951. G661 2011). Magister Thesis, Saltillo, Coahuila, México.
22.
González Z.J.E., Gallardo J.M. 1999. Desarrollo y capacidad reproductiva de Bemisia tabaci (Gennadius) (Homoptera; Aleyrodidae) en pimiento a tres temperaturas. Boletín de Sanidad Vegetal Plagas 25: 3−11.
23.
Gough J.M., Kemp D.H., Akhurst R.J., Pearson R.D., Kongsuwan K. 2005. Identification and characterization of proteins from Bacillus thuringiensis with high toxic activity against the sheep blowfly, Lucilia cuprina. Journal of Invertebrate Pathology 90 (1): 39–46.
24.
Henderson C.F., Tilton E.W. 1955. Tests with acaricides against the brown wheat mite. Journal of Economic Entomology 48 (2): 157−161.
25.
Hernández F.J., Ramírez L., Ramirez N., Fuentes L.S., Jiménez J. 2011. Molecular and biological characterization of native Bacillus thuringiensis strains for controlling tomato leafminer (Tuta absoluta Meyrick) (Lepidoptera: Gelechiidae) in Colombia. World Journal of Microbiology and Biotechnology 27 (3): 579−590. DOI: https://doi.org/10.1007/s11274... (in Spanish).
26.
Hernández J. 2016. Bacillus thuringiensis: a natural tool in Insect Pest Control. In: Gupta et al. (ed.). The Handbook of Microbial Bioresources. CABI publishers, UK.
27.
Hernández-Fernández J., and López-Pazos, S.A. 2011. Bacillus thuringiensis: soil microbial insecticide, diversity and their relationship with the entomopathogenic activity. In: Soil Microbes and Environmental Health. Nova Science Publishers, Bogotá, Colombia, pp 59-80.
28.
Hill B.G. 1969. A morphological comparison between two species of whitefly, Trialeurodes vaporariorum (Westw.) and Bemisia tabaci (Genn.) (Homoptera: Aleurodidae) which occur on tobacco in the Transvaal. Phytophylactica 1 (3−4): 127−146.
29.
Höfte H., Whiteley H.R. 1989. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiological reviews 53 (2): 242−255.
30.
ICA. 2004. Integrated management of white flies Bemisia tabaco (Gennadius) and Aleurotrachelus socialis Bondar. Ministry of agriculture and rural development. Instituto Agropecuario Colombia ICA. Bulletin of plant health 41 ed. Bogotá, Colombia, 60 pp. (in Spanish).
31.
Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 15: 227 (5259): 680−685.
32.
Lapidot M., Friedmann M. 2002. Breeding for resistance to whitefly-transmitted geminiviruses. Annals of Applied Biology 140 (2): 09−127. DOI: https://doi.org/10.1111/j.1744....
33.
Leroy P.D., Wathelet B., Sabri A., Francis F., Verheggen F.J., Capella Q., Haubruge E. 2011. Aphid-host plant interactions: does aphid honeydew exactly reflect the host plant amino acid composition? Arthropod-Plant Interactions 5 (3): 193−199. DOI: https://doi.org/10.1007/s11829....
34.
Li H., Chougule N.P., Bonning B.C. 2011. Interaction of the Bacillus thuringiensis delta endotoxins Cry1Ac and Cry3Aa with the gut of the pea aphid, Acyrthosiphon pisum (Harris). Journal of Invertebrate Pathology 107 (1): 69−78. DOI: https://doi.org/10.1016/j.jip.....
35.
Lonc E., Doroszkiewicz W., Klowden M.J., Rydzanicz K., Galgan A. 2001. Entomopathogenic activities of environmental isolates of Bacillus thuringiensis against dipteran larvae. Journal of Vector Ecology 26: 15−20.
36.
López-Meza J.E., Ibarra J.E. 1996. Characterization of a novel strain of Bacillus thuringiensis. Applied and Environmental Microbiology 62 (4): 1306−1310.
37.
Ohba M., Aizawa K. 1986. Insect toxicity of Bacillus thuringiensis isolated from soils of Japan Journal of Invertebrate Patholog 47: 12−20.
38.
Oliveira M., Amancio E., Laumann R., Gomes L. 2003. Natural enemies of Bemisia tabaci (Gennadius) B biotype and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) in Brasilia, DF. Neotropical Entomology 32: 151–154. DOI: http://dx.doi.org/10.1590/S151....
39.
Pitre L., Hernandez J., Bernal J. 2008. Toxicity of recombinant delta-endotoxins of Bacillus thuringiensis on Guatemalan moth larvae (Tecia solanivora) (Lepidoptera: Gelechiidae). Revista Colombiana de Biotecnología 10 (2): 85–96. DOI: https://doi.org/10.15446/rev.c... (in Spanish).
40.
Porcar M., Grenier A.M., Federici B., Rahbé Y. 2009. Effects of Bacillus thuringiensis δ-endotoxins on the pea aphid (Acyrthosiphon pisum). Applied and Environmental Microbiology 75 (14): 4897−4900. DOI: 10.1128/AEM.00686-09.
41.
Quesada-Moraga E., García-Tóvar E., Valverde-Garcıa P., Santiago-Alvarez C. 2004. Isolation, geographical diversity and insecticidal activity of Bacillus thuringiensis from soils in Spain. Microbiological Research 159 (1): 59−71. DOI: https://doi.org/10.1016/j.micr....
42.
Ramalakshmi A., Udayasuriyan V. 2010. Diversity of Bacillus thuringiensis isolated from western ghats of Tamil Nadu state, India. Current Microbiology 61 (1): 13−18. DOI: https://doi.org/10.1007/s00284....
43.
Ramírez L., Ramírez N., Fuentes L.S., Jiménez J., Hernández-Fernández J. 2010. Standardization of a bioassay and preliminary evaluation of three commercial formulations of Bacillus thuringiensis against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Revista Colombiana de Biotecnología 12 (1): 12−21. (in Spanish).
44.
Salazar-Magallon J.A., Hernandez-Velazquez V.M., Alvear-Garcia I., Arenas-Sosa A., Pena-Chora G. 2015. Evaluation of industrial by-products for the production of Bacillus thuringiensis strain GP139 and the pathogenicity when applied to Bemisia tabaci nymphs. Bulletin of Insectology 68 (1): 103−109.
45.
Sambrook J., Russell D.W. 2001. In vitro mutagenesis using double-stranded DNA templates: selection of mutants with DpnI. Vol. 2. p. 13−19. In: “Molecular Cloning. A Laboratory Manual” (M.R. Green, J. Sambrook, eds.). Cold Spring Habour Laboratory Press, New York.
46.
Sansinenea E. 2012. Discovery and description of Bacillus thuringiensis. p. 3−18. In: “Bacillus thuringiensis Biotechnology” (E. Sansinenea, ed.). Springer, Dordrecht. DOI: https://doi.org/10.1007/978-94....
47.
Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Dean D.H. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews 62 (3): 775−806.
48.
Schünemann R., Knaak N., Fiuza L.M. 2014. Mode of action and specificity of Bacillus thuringiensis toxins in the control of caterpillars and stink bugs in soybean culture. International Scholarly Research Notices: Microbiology 2014: 135675. DOI: http://dx.doi.org/10.1155/2014....
49.
Shao E., Liu S., Lin L., Guan X. 2013. Proteolytic processing of Bacillus thuringiensis toxin Cry1AB in rice brown planthopper, Nilaparvata lugens (Stal). Journal of Invertebrate Pathology 114 (3): 255−257. DOI: https://doi.org/10.1016/j.jip.....
50.
Sims S.R. 1997. Host activity spectrum of the CryIIA Bacillus thuringiensis subsp. kurstaki protein: effects on Lepidoptera, Diptera, and non-target arthropods. Southwestern Entomologist. Available on: http://agris.fao.org/agris-sea... [Accessed: 28 July 2018].
51.
Travers R.S., Martin P.A., Reichelderfer C.F. 1987. Selective process for efficient isolation of soil Bacillus spp. Applied Environmental of Microbiology 53 (6): 1263–1266.
52.
Somoza-Vargas C.E., Hernández-Velázquez V.M., Peña--Chora G., Torres-Garcia G., Huerta-de la Peña A., Ortega--Martínez L.D., Antonio J. 2018. Interaction of Beauveria bassiana strain HPI-019/14 and Bacillus thuringiensis strain GP139 for the biological control of Bemisia tabaci in strawberry Bulletin of Insectology 71 (2): 201−209.
53.
Van Frankenhuyzen K.V. 2009. Insecticidal activity of Bacillus thuringiensis crystal proteins. Journal of Invertebrate Pathology 101 (1): 1−16. DOI: https://doi.org/10.1016/j.jip.....
54.
Van Frankenhuyzen K.V. 2013. Cross-order and cross-phylum activity of Bacillus thuringiensis pesticidal proteins. Journal of Invertebrate Pathology 114 (1): 76−85. DOI: http://dx.doi.org/10.1016/j.ji....
55.
Vassiliou V., Emmanouilidou M., Perrakis A., Morou E., Vontas J., Tsagkarakou A., Roditakis E. 2011. Insecticide resistance in Bemisia tabaci from Cyprus. Insect Science 18 (1): 30−39. DOI: https://doi.org/10.1111/j.1744....
56.
Vázquez L.L., Murguido C., Elizondo A.I., Elosegui O., Morales F.J. 2007. Biological control of the whitefly Bemisia tabaci CIAT. 355 ed. Bogotá, Colombia 36 pp. (in Spanish).
57.
Walters F.S., English L.H. 1995. Toxicity of Bacillus thuringiensis δ-endotoxins toward the potato aphid in an artificial diet bioassay. Entomologia Experimentalis et Applicata 77: 211–216. DOI: https://doi.org/10.1111/j.1570....
58.
Xu Z., Yao B., Sun M., Yu. Z. 2004. Protection of mice infected with Plasmodium berghei by Bacillus thuringiensis crystal proteins. Parasitology Research 92 (1): 53−57. DOI: https://doi.org/10.1007/s00436....
59.
Zhang J., Hodgman T.C., Krieger L., Schnetter W., Schairer H.U. 1997. Cloning and analysis of the first cry gene from Bacillus popilliae. Journal of Bacteriology 179 (13): 4336−4341. DOI: https://doi.org/10.1128/jb.179....
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