Molecular identification of insecticide degradation by gut bacteria isolated from Helicoverpa armigera of Cotton plants
Article Main
Abstract
The cotton bollworm Helicoverpa armigera occurs as a major pest in many economically important crops, including cotton, pigeon pea, chickpea, pea, cowpea, sunflower, tomato, sorghum, pearl millet and other crops. Intestinal microorganisms play important role in the degradation of diet components of insects. In order to know the role of gut bacteria in insecticide resistance five insecticides Chlorpyriphos (20% EC), Cypermethrin (25% EC), Malathion (50% EC), Quinalphos (25% EC), Triazophos (40% EC), were selected for the insecticide degradation studies. All the bacterial isolates from the gut of lab and field populations of H. armigera were identified using 16S rRNA gene-based identification and tested for their growth on minimal salt medium (MSM) along with the selected insecticides. A total of 11 bacterial isolates were tested and among them, isolate CL4 (Rhodococcus sp.) was found to grow on minimal salt medium (MSM) and with chlorpyriphos and isolate CL2 (Enterococcus casseliflavus) was able to grow in MSM with chloropyriphos (C22H19Cl2NO3) and malathion (C10H19O6PS2) and no growth was seen in MSM without insecticide (control). Gas Chromatography analysis of the positive bacterial isolate cultures in MSM showed that the isolate CL4 (Rhodococcus sp.) was able to utilize 43.9% of chlorpyriphos and isolate CL2 (E.casseliflavus) was able to utilize 26% of chlorpyriphos and 57.1% of malathion in MSM broth cultures with comparison with the respective control cultures. Findings of the current work suggested that gut bacteria in the field populations of H. armigera plays a role in insecticide resistance
Article Details
Article Details
Keywords
Cotton plants, Gut bacteria, Helicoverpa armigera, Insecticide degradation, Molecular identification
References
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Bai, L.S., Zhao, C.X., Xu, J.J., Feng, C., Li, Y.Q., Dong, Y. L. & Ma, Zhi-qing (2019). Identification and biochemical characterization of carboxylesterase 001G associated with insecticide detoxification in Helicoverpa armigera. Pest. Biochem. Physiol. 157, 69–79. DOI: 10.1016/j.pestbp.20 19.03.009
Broderick, N.A., Raffa, K.F., Goodman, R.M & Handelsman, J. (2004). Census of bacterial community of gypsy moth larval mid gut by using culturing and culture independent methods. Applied Environmental Microbiology. 70, 290-300.DOI: 10.1128/AEM.70.1.293-300.2004
Carol, R.L., Sarah, E.P & Ronald, J.P. (2003). Degradation and detoxification of the dihydrochalcone phloridzin by Enterobacter agglomerans, a bacterium associated with the apple pest, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae. Environmental Entomology. 32, 953-962.DOI: 10.1603/0046-225X-32.5.953
Dar, M.A., Shaikh, A.F., Pawar, K.D., Xie, R., Sun, J., Kandasamy, S., &Pandit, R.S. (2021). Evaluation of cellulose degrading bacteria isolated from the gut-system of cotton bollworm, Helicoverpa armigera and their potential values in biomass conversion. PeerJ 9: e11254. DOI: 10.7717/peerj.11254
Dar, M.A., Shaikh, A.A., Pawar, K.D., & Pandit, R.S. (2018). Exploring the gut of Helicoverpa armigera for cellulose degrading bacteria and evaluation of a potential strain for lignocellulosic biomass deconstruction. Process Biochemistry. DOI: 10.1016/j.procbio.2018.08.001
Dick, R.E., Quinn, J.P. (1995). Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Applied Microbial Biocontrol. 43(8): 545-550.DOI: 10.1007/BF00218464
Dillon, R.J and Dillon, V.M. (2004). The gut bacteria of insects: non-pathogenic interactions. Annual Review of Entomology. 49, 71-92. DOI: 10.1146/annurev.e nto.49.061802.123416
Gavriel, S., Jurkevitch, E., Gazit, Y. & Yuval, B. (2010). Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies. Journal of Applied Entomology. 10, 439-444. DOI: 10.1111/j.1439-0418.201 0.01605.x
Gebbardi, K., Schimana, J., Muller, J., Krantal, P., Zeeck, A & Vater, I. (2001). Screening for biologically active metabolites with endosymbiotic bacilli isolated from arthropods. FEMS Microbiology. 217, 199-205.DOI: 10.1111/j.1574-6968.2002.tb11475.x
Genta, A.F., Dillon, R.J., Terra, R.W & Ferreira, C. (2006). Potential role for gut microbiota in cell wall digestion and glucoside detoxification in Tenebrio molitor larvae. Journal of Insect Physiology. 52, 593-601. DOI: 10.1016/j.jinsphy s.2006.02.007
Hao, O.J., Kim, M.H., Seagren, E.A & Kim, H. (2002). Kinetics of phenols and chlorophenol utilization by Acinetobacter species. Chemosphere. 46, 797-807.DOI: 10.1016/S0045-6535(01)00182-5
Hayashi, A., Aoyagi, H., Yoshimura, T & Hideo Tanaka, H. (2007). Development of novel method for screening microorganisms using symbiotic association between insect and intestinal microorganisms. Journal of Bioscience and Bioengineering. 103, 358-367. DOI: 10.1263/jbb.103.358
Hoffman, C.S & Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 57, 267-272. DOI: 10.1016/0378-1119(87)90131-4
Jilani, S and Khan, A.M. (2004). Isolation, characterization and growth response of pesticide degrading bacteria. Journal of Biological Science. 4, 15-20. DOI: 10.3923/jbs.2004.15.20
Jing, T.Z., Qi, F.H. & Wang, Z.Y. (2020). Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision? Microbiome 8, 38. DOI: 10.1186/s40168-020-00823-y
Kanekar, P.P., Bhadbhade, B.J., Deshpande, N.M & Sarnaik, S.S. (2004). Biodegradation of Organophosphates. Biological Sciences. 70, 57-70
Kranthi, K.R., Jadhav, D., Wanjari, R., Kranthi, S. & Russell, D. (2001). Pyrethroid resistance and mechanism of resistance in field strains of Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology. 94, 254-263. DOI: 10.1603/0022-0493-94.1.253
Lee, K.S., Metcalf, W.W. &Wanner, B.L. (1992). Evidence for two phosphonate degradative pathways in Enterobacter aerogenes. Journal of Bacteriology. 174, 2501-2510. DOI: 10.1128/jb.174.8.2501-2510.1992
Lei, P., Nie, M.Q., Wen, X.M., Ge, B.Z. &Zang, Z.J. (2004). Study of degradation characters of preponderant Flavobacterial strains in a mixture of anthracene, phenantherene and pyrene. Journal of Xi’an Jiaotong University.38, 657–658.
Mishra, P.K. and Tandon, S.M. (2003). Gut bacterial flora of Helicoverpa armigera (Hub.) (Lepidoptera: Noctuidae). Indian Journal of Microbiology. 43, 55-56.
Nagarkatti, S. and Satyaprakash, S. (1974). Rearing Helicoverpa armigera (Hubn.) on an artificial diet. Technical Bulletin Commonwealth Institute of Biological Control. 17, 169-173.
Paramasiva, I., Shouche, Y., Kulkarni, G. J., Krishnayya, P. V., Akbar, S. M., & Sharma, H. C. (2014). Diversity in gut microflora of Helicoverpa armigera populations from different regions in relation to biological activity of Bacillus thuringiensis ?-endotoxin Cry1Ac. Archives of Insect Biochemistry and Physiology, 87, 201–213. DOi: 10.1002/arch.21190
Priya, N.G., Ojha, A., Kajla, M.K., Raj, A. & Rajagopal, R. (2012). Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS One. 7, e30768.DOI: 10.1371/journal.pone.0030768
Rajagopal, R., Sivakumar, S., Agrawal, N., Malhotra, P & Bhatnagar, R.K. (2002). Silencing of midgut aminopeptidase N of Spodoptera litura by dsRNA establishes its role as Bacillus thuringiensis toxin receptor. Journal of Biological Chemistry.277, 46849-46851. DOI: 10.1074/jbc.C200 523200
Rajendran, L., Samiyappan, R., Raguchander, T. & Saravanakumar, D. (2007). Endophytic bacteria mediate plant resistance against cotton bollworm. Journal of Plant Interactions. 2, 1–10.DOI: 10.1080/17429140701420003
Rani, A., Sharma, A., Rajagopal, R., Adak, T.& Bhatnagar, R.K. (2009). Bacterial diversity analysis of larvae and adult midgut micro-flora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiology. 9, 96.DOI: 10.1186/1471-2180-9-96
Ranjith, M.T., Chellappan, M., Harish, E.R., Girija, D. & Nazeem, P.A. (2016). Bacterial communities associated with the gut of tomato fruit borer, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) based on Illumina Next-Generation Sequencing. Journal of Asia-Pacific Entomology. 19, 333–340. DOI: 10.1016/j.aspen.20 16.03.007
Regode, V., Kuruba, S., Mohammad, A.S., & Sharma, H.C. (2016). Isolation and characterization of gut bacterial proteases involved in inducing pathogenicity of Bacillus thuringiensis toxin in cotton bollworm, Helicoverpa armigera. Frontiers in Microbiology, 7, 1567. DOI: 10.3389/fmicb.2016.01567
Sambrook, J., Fritsch, E.F. & Maniatis, T. (2001). Molecular Cloning, A Laboratory Manual, 3rdedn (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY).
Sharon, G., Segal, D., Ringo, J.M., Hefetz, A. & Rosenberg, I.Z. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of National Academy of Sciences. 107, 20051–20056.DOI: 10.1073/pnas.1009906107
Shinde, A. A., Shaikh, F. K., Gadge, P. P., Padul, M. V., Govindwar, S. P., & Kachole, M. S. (2017). Conserved nature of Helicoverpa armigera gut bacterial flora on different host plants and in vitro interactions with PI proteins advocates role in host digestive physiology. Journal of the Saudi Society of Agricultural Sciences. 18: 141-149. DOI:10.1016/j.jssas.2017.03.004
Singh, K., Brajesh, K., Walker, A., Alum, J., Morgan, W & Wright, D.J. (2004). Biodegradation of chlorpyrifos by Enterobacter strain B-14 and its use in biodegradation of contaminated soils. Applied Environmental Microbiology. 70, 4855-4863.DOI: 10.1128/AEM.70.8.4855-4863.2004
Thakur, D., Bhuyan, M., Majumdar, S., Yadav, A., Hazarika, L.K., Harman, N., Baruah, A.A.L.H., & Bora, T.C. (2005). Isolation, characterization, in-vitro antibiotic susceptibility and pesticide tolerance of gut bacteria from rice hispa, Dicladispa armigera (Olivier). Indian Journal of Microbiology. 45, 217-221.
Verma, K., Agarwal, M., Farooq, M., Misra, R.B & Hans, R.K. (2006). Endosulfan degradation by a Rhodococcus strain isolated from the earthworm gut. Ecotoxicology and Environmental Safety. 64, 377-381.DOI: 10.1016/j.ecoe nv.2005.05.014
Vesta, S.A., Sandra, R & Virmantas, S. (2006). Myrcene resistant bacteria isolated from the gut of phytophagous insects Ips typographus. Ekologia. 4, 1-6.
Visotto, L.E., Oliveira, M.G.A., Guedes, R.N.C., Ribon, A.O.B & Good-God, P.I.V. (2009). Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis. Journal of Insect Physiology. 55, 185-191.DOI: 10.1016/j.jinsphys.2008.10.017
Whalon, M.E., Mota-Sanchez, D. & Hollingsworth, R. (2008). Global Pesticide Resistance in Arthropods. (CAB International, Oxfordshire, UK).
Wilson, G.R. and Benoit, T.G. (1993). Alkaline pH activated Bacillus thuringiensis spores. Journal of Invertebrate Pathology. 62, 87–89.DOI: 10.1006/jipa.1993.1079
Xiang, H., Wei, G. F., Jia, S., Huang, J. & Miao, X.X. (2006). Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Canadian Journal of Microbiology. 52, 1085–1092.DOI: 10.1139/w06-064
Yang, X., Xu, P., Yuan, H., Graham, R.I., Wilson, K., & Wu, K. (2019). Discovery and characterization of a novel picorna-like RNA virus in the cotton bollworm Helicoverpa armigera. Journal of Invertebrate Pathology, 160, 1–7. DOI: 10.1016/j.jip.2018.11.003
Yuan, H., Xu, P., Yang, X., Graham, R.I., Wilson, K., & Wu, K. (2017). Characterization of a novel member of genus Iflavirus in Helicoverpa armigera. Journal of Invertebrate Pathology, 144, 65–73. DOI:10.1016/j.jip.20 17.0 1.011
Ahlawat, S., Singh, D., Yadav, A., Singh, A.K., Virdi, J. S., & Sharma, K.K. (2020). Proteomic analysis reveals the damaging role of low redox laccase from Yersinia enterocolitica strain 8081 in the midgut of Helicoverpa armigera. Biotechnology letters, 42, 2189–2210. DOI: 10.1007/s10529-020-02925-x
Bai, L.S., Zhao, C.X., Xu, J.J., Feng, C., Li, Y.Q., Dong, Y. L. & Ma, Zhi-qing (2019). Identification and biochemical characterization of carboxylesterase 001G associated with insecticide detoxification in Helicoverpa armigera. Pest. Biochem. Physiol. 157, 69–79. DOI: 10.1016/j.pestbp.20 19.03.009
Broderick, N.A., Raffa, K.F., Goodman, R.M & Handelsman, J. (2004). Census of bacterial community of gypsy moth larval mid gut by using culturing and culture independent methods. Applied Environmental Microbiology. 70, 290-300.DOI: 10.1128/AEM.70.1.293-300.2004
Carol, R.L., Sarah, E.P & Ronald, J.P. (2003). Degradation and detoxification of the dihydrochalcone phloridzin by Enterobacter agglomerans, a bacterium associated with the apple pest, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae. Environmental Entomology. 32, 953-962.DOI: 10.1603/0046-225X-32.5.953
Dar, M.A., Shaikh, A.F., Pawar, K.D., Xie, R., Sun, J., Kandasamy, S., &Pandit, R.S. (2021). Evaluation of cellulose degrading bacteria isolated from the gut-system of cotton bollworm, Helicoverpa armigera and their potential values in biomass conversion. PeerJ 9: e11254. DOI: 10.7717/peerj.11254
Dar, M.A., Shaikh, A.A., Pawar, K.D., & Pandit, R.S. (2018). Exploring the gut of Helicoverpa armigera for cellulose degrading bacteria and evaluation of a potential strain for lignocellulosic biomass deconstruction. Process Biochemistry. DOI: 10.1016/j.procbio.2018.08.001
Dick, R.E., Quinn, J.P. (1995). Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Applied Microbial Biocontrol. 43(8): 545-550.DOI: 10.1007/BF00218464
Dillon, R.J and Dillon, V.M. (2004). The gut bacteria of insects: non-pathogenic interactions. Annual Review of Entomology. 49, 71-92. DOI: 10.1146/annurev.e nto.49.061802.123416
Gavriel, S., Jurkevitch, E., Gazit, Y. & Yuval, B. (2010). Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies. Journal of Applied Entomology. 10, 439-444. DOI: 10.1111/j.1439-0418.201 0.01605.x
Gebbardi, K., Schimana, J., Muller, J., Krantal, P., Zeeck, A & Vater, I. (2001). Screening for biologically active metabolites with endosymbiotic bacilli isolated from arthropods. FEMS Microbiology. 217, 199-205.DOI: 10.1111/j.1574-6968.2002.tb11475.x
Genta, A.F., Dillon, R.J., Terra, R.W & Ferreira, C. (2006). Potential role for gut microbiota in cell wall digestion and glucoside detoxification in Tenebrio molitor larvae. Journal of Insect Physiology. 52, 593-601. DOI: 10.1016/j.jinsphy s.2006.02.007
Hao, O.J., Kim, M.H., Seagren, E.A & Kim, H. (2002). Kinetics of phenols and chlorophenol utilization by Acinetobacter species. Chemosphere. 46, 797-807.DOI: 10.1016/S0045-6535(01)00182-5
Hayashi, A., Aoyagi, H., Yoshimura, T & Hideo Tanaka, H. (2007). Development of novel method for screening microorganisms using symbiotic association between insect and intestinal microorganisms. Journal of Bioscience and Bioengineering. 103, 358-367. DOI: 10.1263/jbb.103.358
Hoffman, C.S & Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 57, 267-272. DOI: 10.1016/0378-1119(87)90131-4
Jilani, S and Khan, A.M. (2004). Isolation, characterization and growth response of pesticide degrading bacteria. Journal of Biological Science. 4, 15-20. DOI: 10.3923/jbs.2004.15.20
Jing, T.Z., Qi, F.H. & Wang, Z.Y. (2020). Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision? Microbiome 8, 38. DOI: 10.1186/s40168-020-00823-y
Kanekar, P.P., Bhadbhade, B.J., Deshpande, N.M & Sarnaik, S.S. (2004). Biodegradation of Organophosphates. Biological Sciences. 70, 57-70
Kranthi, K.R., Jadhav, D., Wanjari, R., Kranthi, S. & Russell, D. (2001). Pyrethroid resistance and mechanism of resistance in field strains of Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology. 94, 254-263. DOI: 10.1603/0022-0493-94.1.253
Lee, K.S., Metcalf, W.W. &Wanner, B.L. (1992). Evidence for two phosphonate degradative pathways in Enterobacter aerogenes. Journal of Bacteriology. 174, 2501-2510. DOI: 10.1128/jb.174.8.2501-2510.1992
Lei, P., Nie, M.Q., Wen, X.M., Ge, B.Z. &Zang, Z.J. (2004). Study of degradation characters of preponderant Flavobacterial strains in a mixture of anthracene, phenantherene and pyrene. Journal of Xi’an Jiaotong University.38, 657–658.
Mishra, P.K. and Tandon, S.M. (2003). Gut bacterial flora of Helicoverpa armigera (Hub.) (Lepidoptera: Noctuidae). Indian Journal of Microbiology. 43, 55-56.
Nagarkatti, S. and Satyaprakash, S. (1974). Rearing Helicoverpa armigera (Hubn.) on an artificial diet. Technical Bulletin Commonwealth Institute of Biological Control. 17, 169-173.
Paramasiva, I., Shouche, Y., Kulkarni, G. J., Krishnayya, P. V., Akbar, S. M., & Sharma, H. C. (2014). Diversity in gut microflora of Helicoverpa armigera populations from different regions in relation to biological activity of Bacillus thuringiensis ?-endotoxin Cry1Ac. Archives of Insect Biochemistry and Physiology, 87, 201–213. DOi: 10.1002/arch.21190
Priya, N.G., Ojha, A., Kajla, M.K., Raj, A. & Rajagopal, R. (2012). Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS One. 7, e30768.DOI: 10.1371/journal.pone.0030768
Rajagopal, R., Sivakumar, S., Agrawal, N., Malhotra, P & Bhatnagar, R.K. (2002). Silencing of midgut aminopeptidase N of Spodoptera litura by dsRNA establishes its role as Bacillus thuringiensis toxin receptor. Journal of Biological Chemistry.277, 46849-46851. DOI: 10.1074/jbc.C200 523200
Rajendran, L., Samiyappan, R., Raguchander, T. & Saravanakumar, D. (2007). Endophytic bacteria mediate plant resistance against cotton bollworm. Journal of Plant Interactions. 2, 1–10.DOI: 10.1080/17429140701420003
Rani, A., Sharma, A., Rajagopal, R., Adak, T.& Bhatnagar, R.K. (2009). Bacterial diversity analysis of larvae and adult midgut micro-flora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiology. 9, 96.DOI: 10.1186/1471-2180-9-96
Ranjith, M.T., Chellappan, M., Harish, E.R., Girija, D. & Nazeem, P.A. (2016). Bacterial communities associated with the gut of tomato fruit borer, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) based on Illumina Next-Generation Sequencing. Journal of Asia-Pacific Entomology. 19, 333–340. DOI: 10.1016/j.aspen.20 16.03.007
Regode, V., Kuruba, S., Mohammad, A.S., & Sharma, H.C. (2016). Isolation and characterization of gut bacterial proteases involved in inducing pathogenicity of Bacillus thuringiensis toxin in cotton bollworm, Helicoverpa armigera. Frontiers in Microbiology, 7, 1567. DOI: 10.3389/fmicb.2016.01567
Sambrook, J., Fritsch, E.F. & Maniatis, T. (2001). Molecular Cloning, A Laboratory Manual, 3rdedn (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY).
Sharon, G., Segal, D., Ringo, J.M., Hefetz, A. & Rosenberg, I.Z. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of National Academy of Sciences. 107, 20051–20056.DOI: 10.1073/pnas.1009906107
Shinde, A. A., Shaikh, F. K., Gadge, P. P., Padul, M. V., Govindwar, S. P., & Kachole, M. S. (2017). Conserved nature of Helicoverpa armigera gut bacterial flora on different host plants and in vitro interactions with PI proteins advocates role in host digestive physiology. Journal of the Saudi Society of Agricultural Sciences. 18: 141-149. DOI:10.1016/j.jssas.2017.03.004
Singh, K., Brajesh, K., Walker, A., Alum, J., Morgan, W & Wright, D.J. (2004). Biodegradation of chlorpyrifos by Enterobacter strain B-14 and its use in biodegradation of contaminated soils. Applied Environmental Microbiology. 70, 4855-4863.DOI: 10.1128/AEM.70.8.4855-4863.2004
Thakur, D., Bhuyan, M., Majumdar, S., Yadav, A., Hazarika, L.K., Harman, N., Baruah, A.A.L.H., & Bora, T.C. (2005). Isolation, characterization, in-vitro antibiotic susceptibility and pesticide tolerance of gut bacteria from rice hispa, Dicladispa armigera (Olivier). Indian Journal of Microbiology. 45, 217-221.
Verma, K., Agarwal, M., Farooq, M., Misra, R.B & Hans, R.K. (2006). Endosulfan degradation by a Rhodococcus strain isolated from the earthworm gut. Ecotoxicology and Environmental Safety. 64, 377-381.DOI: 10.1016/j.ecoe nv.2005.05.014
Vesta, S.A., Sandra, R & Virmantas, S. (2006). Myrcene resistant bacteria isolated from the gut of phytophagous insects Ips typographus. Ekologia. 4, 1-6.
Visotto, L.E., Oliveira, M.G.A., Guedes, R.N.C., Ribon, A.O.B & Good-God, P.I.V. (2009). Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis. Journal of Insect Physiology. 55, 185-191.DOI: 10.1016/j.jinsphys.2008.10.017
Whalon, M.E., Mota-Sanchez, D. & Hollingsworth, R. (2008). Global Pesticide Resistance in Arthropods. (CAB International, Oxfordshire, UK).
Wilson, G.R. and Benoit, T.G. (1993). Alkaline pH activated Bacillus thuringiensis spores. Journal of Invertebrate Pathology. 62, 87–89.DOI: 10.1006/jipa.1993.1079
Xiang, H., Wei, G. F., Jia, S., Huang, J. & Miao, X.X. (2006). Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Canadian Journal of Microbiology. 52, 1085–1092.DOI: 10.1139/w06-064
Yang, X., Xu, P., Yuan, H., Graham, R.I., Wilson, K., & Wu, K. (2019). Discovery and characterization of a novel picorna-like RNA virus in the cotton bollworm Helicoverpa armigera. Journal of Invertebrate Pathology, 160, 1–7. DOI: 10.1016/j.jip.2018.11.003
Yuan, H., Xu, P., Yang, X., Graham, R.I., Wilson, K., & Wu, K. (2017). Characterization of a novel member of genus Iflavirus in Helicoverpa armigera. Journal of Invertebrate Pathology, 144, 65–73. DOI:10.1016/j.jip.20 17.0 1.011
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Molecular identification of insecticide degradation by gut bacteria isolated from Helicoverpa armigera of Cotton plants. (2021). Journal of Applied and Natural Science, 13(2), 641-653. https://doi.org/10.31018/jans.v13i2.2678
