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Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi

Year 2017, Volume: 3 Issue: 1, 52 - 60, 31.01.2017

Abstract

Helicoverpa armigera, the pod borer is a major constraint to global chickpea production. Genetic improvement of chickpea
for insect resistance by traditional methods has been hampered by narrow genetic diversity in the elite gene pool.
Bacillus thuringiensis (Bt) chickpea plants expressing Bt genes as well as pyramids also have been developed already
and many are in field trials. But, already available Bt crops like cotton have increased the insect resistance to transgenic
plants in H. armigera. Although Bt chickpeas have yet to be commercialized, but the sustainability of Btcrops is vulnerable
to the insect resistance in Helicoverpa. The next generation approach for crop protection against Helicoverpa is to
knock down the crucial physiology-related genes of insect pests using transgenic plants, which is called Plant-mediated
RNAinterference (RNAi). Common small interfering RNAs (siRNAs) for the target genes of H. armigera, designed in
silico could be used to study the lethal effect of down-regulating crucial target genes in chickpea. This review describes
the progress of developing resistance to H. armigera in chickpea using Bt toxin genes and the future prospects of using
plant-mediated RNAi for H. armigera resistance. The plant-mediated RNAi approach holds great promise for future
development but further studies will be required to optimize RNAi-based strategies for chickpea protection against
H. armigera using integrated pest management strategies.

References

  • Acharjee S, Sarmah BK (2013a) Biotechnologically generating “super chickpea” for food and nutritional security. Plant Sci 207:108–16. doi: 10.1016/j.plantsci.2013.02.003 Acharjee S, Sarmah BK (2013b) Transgenic Bacillus thuringiensis (Bt) chickpea: India’ s most wanted genetically modified (GM) pulse crop. African J Biotechnol 12:5709-5713. doi: 10.5897/ AJB12.2439 Acharjee S, Sarmah BK, Kumar PA, et al., (2010) Transgenic chickpeas (Cicer arietinum L.) expressing a sequence-modified cry2Aa gene. Plant Sci 178:333–339. doi: 10.1016/j. plantsci.2010.02.001 Alvi AHK, Sayyed AH, Naeem M, Ali M (2012) Field-Evolved Resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis Toxin Cry1Ac in Pakistan. PLoS One 7: e47309. Armes NJ, Jadav DR, Bond GS, et al., (1992) Insecticide resistance in the pod borer Helicoverpa armigera in South India. Pest Science 34: 355-364 Asharani, B. M (2011) Transformation of chickpea lines with Cry1X using in planta transformation and characterization of putative transformants T1 lines for molecular and biochemical characters. J Plant Breed Crop Sci 3:413-423. doi: 10.5897/JPBCS11.074 Asokan R, Chandra GS, Manamohan M, Kumar NKK (2013) Effect of diet delivered various concentrations of double-stranded RNA in silencing a midgut and a non-midgut gene of Helicoverpa armigera. Bull Entomol Res 103: 555–63. doi: 10.1017/S0007485313000138 Asokan R, Nagesha SN, Manamohan M, et al., (2012) Common siRNAs for various target genes of the fruit borer, Helicoverpa armigera Hubner (Lepidoptera: Noctuidae). Current Science 102: 1692-1699 Asokan R, Sharath Chandra G, Manamohan M, et al., (2014) Response of various target genes to diet-delivered dsRNA mediated RNA interference in the cotton bollworm, Helicoverpa armigera. J Pest Sci 87: 163–172. doi: 10.1007/ s10340-013-0541-7 BANR (Board on Agriculture and Natural Resources) (2000) Genetically modified pest-protected plant: science and regulation. p. 292. Barton KA, Whiteley HR, Yang NS (1987) Bacillus thuringiensis δ-endotoxin expressed in transgenic Nicotiana tabacum provides resistance to Lepidopteran insects. Plant Physiology 85: 1103-1109 Biradar SS, Sridevi O, Salimath PM (2009) Genetic enhancement of chickpea for pod borer resistance through expression of CryIAc protein. Karnataka J Agric Sci 22: 467-470. Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49: 423-435 Carrière Y, Crickmore N, Tabashnik BE (2015) Optimizing pyramided transgenic Bt crops for sustainable pest management. Nat Biotechnol 33:161-168. doi: 10.1038/nbt.3099 Choudhary M, Sahi S (2011) In silico designing of insecticidal small interfering RNA (siRNA) for Helicoverpa armigera control. Indian Journal of Experimental Biology 49:469-474. Cohen BM, Gould F, Bentur JC (2000) Bt rice: practical steps to sustainable use. International Rice Research 25: 4-10 Devi VS, Sharma HC, Rao PA (2011) Interaction between host plant resistance and biological activity of Bacillus thuringiensis in managing the pod borer Helicoverpa armigera in chickpea. Crop Protection 30: 962-969 FAOSTAT (2013). Agricultural Data. http://faostat3. fao.org/faostat-gateway/go/to/download/Q/QC/E Ganguly M, Molla KA, Karmakar S, et al., (2014) Development of pod borer-resistant transgenic chickpea using a pod-specific and a constitutive promoter-driven fused cry1Ab/Ac gene. Theor Appl Genet 127:2555–2565. doi: 10.1007/ s00122-014-2397-5 Gassmann AJ, Petzold-Maxwell JL, Clifton EH, et al., (2014) Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. Proc Natl Acad Sci U S A 111:5141–6. doi: 10.1073/ pnas.1317179111 Gaur PM, Jukanti AK, Varshney RK (2012) Impact of Genomic Technologies on Chickpea Breeding Strategies. Agronomy 2:199–221. doi: 10.3390/ agronomy2030199 Giri AP, Harsulkar AM, Deshpande VV, et al., (1998) Chickpea defensive proteinase inhibitors can be inactivated by podborers gut proteinases. Plant Physiol 116: 393–401 © Plant Breeders Union of Turkey (BİSAB) 59 Gordon KHJ, Waterhouse PM (2007) RNAi for insect-proof plants. Nat Biotechnol 25:1231-2. doi: 10.1038/nbt1107-1231 Hegedus D, Erlandson M, Gillott C, et al., (2009) New insights into peritrophic matrix synthesis, architecture, and function.Annu Rev Entomol 54: 285-302 Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol 56: 227-235 ICRISAT (1992). The medium term plan. International Crops Research Institute for Semi-Arid Tropics. Patancheru. India. Indurker S, Misra HS, Eapen S (2007) Genetic transformation of chickpea (Cicer arietinum L.) with insecticidal crystal protein gene using particle gun bombardment. Plant Cell Rep 26:755-763. doi: 10.1007/s00299-006-0283-6 James C (2014) Global status of commercialized Biotech/GM crops: 2012. ISAAA Brief No. 47 ISAAA: Ithaca, NY Jukanti AK, Gaur PM, Gowda CL, et al., (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. British Journal of Nutrition 108: S11-S26. Kar S, Basu D, Das S, et al., (1997) Expression of cryIA(c) gene of Bacillus thurigenesis in transgenic chickpea plants inhibits development of pod borer (Heliothis armigera) larvae. Transgenic Research6: 177-185 Khatodia S, Kharb P, Batra P, Chowdhury VK (2014a) Development and characterization of transgenic chickpea (Cicer arietinum L.) plants with cry1Ac gene using tissue culture independent protocol. International J Adv Res 2: 323-331 Khatodia, S., Kharb, P., Batra, P., & Chowdhury, V. K. (2014b). Real time PCR based detection of transgene copy number in transgenic chickpea lines expressing Cry1Aa 3 and Cry1Ac, 2(4), Int J Pure App Biosci 100-105. Khatodia, S., Bhatotia, K., Passricha, N., Khurana, S. M. P., & Tuteja, N. (2016). The CRISPR/Cas Genome-Editing Tool: Application in Improvement of Crops. Frontiers in Plant Science, 7, 1-13. https://doi.org/10.3389/fpls.2016.00506 Li H, Rodda M, Gnanasambandam A, et al., (2015) Breeding for biotic stress resistance in chickpea: progress and prospects. Euphytica. doi: 10.1007/ s10681-015-1462-8 Mallikarjuna N (2001). Prospects of using Cicer canariense for chickpea improvement. International Chickpea and Pigeonpea Newsletter8: 23-24 Mao Y-B, Cai W-J, Wang J-W, et al., (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–13. doi: 10.1038/nbt1352 Mao Y-B, Tao X-Y, Xue X-Y, et al., (2011) Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Res 20:665–73. doi: 10.1007/ s11248-010-9450-1 Mao Y-B, Xue X-Y, Tao X-Y, et al., (2013) Cysteine protease enhances plant-mediated bollworm RNA interference. Plant Mol Biol 83:119–29. doi: 10.1007/s11103-013-0030-7 Mehrotra M, Sanyal I, Amla D V. (2011) High-efficiency Agrobacterium-mediated transformation of chickpea (Cicer arietinum L.) and regeneration of insect-resistant transgenic plants. Plant Cell Rep 30:1603-1616. doi: 10.1007/ s00299-011-1071-5 Neelima MG, Ramu SV, Sreevathsa R, et al., (2008) In planta transformation strategy to generate transgenic plants in chickpea: Proof of concept with a cry gene. Journal of Plant Biology 35: 201-206 Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26: 393-400 Rao PP, Birthal PS, Bhagavatula S, et al., (2010) Chickpea and pigeonpea economies in Asia: facts, trends and outlook. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, Andhra Pradesh, India. pp. 1-76 Rawat P, Singh AK, Ray K, et al., (2011) Detrimental effect of expression of Bt endotoxin Cry1Ac on in vitro regeneration, in vivo growth and development of tobacco and cotton transgenics. Journal of Biosciences36: 363-376 Rocher EJD, Vargo-Gogola TC, Diehn SH, et al., (1998) Direct evidence for rapid degradation of Bacillus thuringiensis toxin mRNA as a cause of poor expression in plants. Plant Physiology 117: 1445-1461 Romeis J, Sharma HC, Sharman KK, et al., (2004) The potential of transgenic chickpeas for pest control and possible effects on non-target arthropods. Crop Prot 23:923-938 3(1):52-60, 2017 60 bitki ıslahçıları alt birliği www.bisab.org.tr Ekin Journal Sanyal I, Singh AK, Kaushik M, Amla D V (2005) Agrobacterium-mediated transformation of chickpea (Cicer arietinum L.) with Bacillus thuringiensis cry1Ac gene for resistance against pod borer insect Helicoverpa armigera. Plant Sci 168:1135-1146. doi: 10.1016/j.plantsci. 2004.12.015 Schnepf E, Crickmore N, Van Rie J, et al., (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews 62: 775-806 Sharma HC, Crouch JH, Sharma KK, et al., (2002) Applications of biotechnology for crop improvement: prospects and constraints. Plant Science 163: 381-395 Sharma HC, Pampapathy G, Lanka SK, et al., (2005) Antibiosis mechanism of resistance to legume pod borer, Helicoverpa armigera in wild relatives of chickpea. Euphytica 142: 107-117 Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521. doi: 10.1038/ nbt.2597 Tabashnik BE, Carrière Y, Dennehy TJ, et al., (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J Econ Entomol 96: 1031-1038 Tabashnik BE, Gassmann AJ, Crowder DW, et al., (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26: 199–202 Tabashnik BE, Van Rensburg JBJ, Carriere Y (2009) Field- evolved insect resistance to Bt crops: Definition, theory, and data. J Econ Entomol 102: 2011–2025 Varshney RK, Thudi M, May GD, et al., (2010) Legume genomics and breeding. Plant Breeding Rev 33: 257-304 Xiong Y, Zeng H, Zhang Y, et al., (2013) Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. Int J Biol Sci 9:370–81. doi: 10.7150/ijbs.5929 Yadav SS, Kumar J, Yadav SK, et al., (2006) Evaluation of Helicoverpa and drought resistance in desi and kabuli chickpea. Plant Genetic Resources: Characterization and Utilization 4: 198-203. Zhang X, Liu X, Ma J, Zhao J (2013) Silencing of cytochrome P450 CYP6B6 gene of cotton bollworm (Helicoverpa armigera) by RNAi. Bulletin of Entomological Research 584-591. Zhu J-Q, Liu S, Ma Y, et al., (2012) Improvement of pest resistance in transgenic tobacco plants expressing dsRNA of an insect-associated gene EcR. PLoS One 7:e38572. doi: 10.1371/journal.pone.0038572
Year 2017, Volume: 3 Issue: 1, 52 - 60, 31.01.2017

Abstract

References

  • Acharjee S, Sarmah BK (2013a) Biotechnologically generating “super chickpea” for food and nutritional security. Plant Sci 207:108–16. doi: 10.1016/j.plantsci.2013.02.003 Acharjee S, Sarmah BK (2013b) Transgenic Bacillus thuringiensis (Bt) chickpea: India’ s most wanted genetically modified (GM) pulse crop. African J Biotechnol 12:5709-5713. doi: 10.5897/ AJB12.2439 Acharjee S, Sarmah BK, Kumar PA, et al., (2010) Transgenic chickpeas (Cicer arietinum L.) expressing a sequence-modified cry2Aa gene. Plant Sci 178:333–339. doi: 10.1016/j. plantsci.2010.02.001 Alvi AHK, Sayyed AH, Naeem M, Ali M (2012) Field-Evolved Resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis Toxin Cry1Ac in Pakistan. PLoS One 7: e47309. Armes NJ, Jadav DR, Bond GS, et al., (1992) Insecticide resistance in the pod borer Helicoverpa armigera in South India. Pest Science 34: 355-364 Asharani, B. M (2011) Transformation of chickpea lines with Cry1X using in planta transformation and characterization of putative transformants T1 lines for molecular and biochemical characters. J Plant Breed Crop Sci 3:413-423. doi: 10.5897/JPBCS11.074 Asokan R, Chandra GS, Manamohan M, Kumar NKK (2013) Effect of diet delivered various concentrations of double-stranded RNA in silencing a midgut and a non-midgut gene of Helicoverpa armigera. Bull Entomol Res 103: 555–63. doi: 10.1017/S0007485313000138 Asokan R, Nagesha SN, Manamohan M, et al., (2012) Common siRNAs for various target genes of the fruit borer, Helicoverpa armigera Hubner (Lepidoptera: Noctuidae). Current Science 102: 1692-1699 Asokan R, Sharath Chandra G, Manamohan M, et al., (2014) Response of various target genes to diet-delivered dsRNA mediated RNA interference in the cotton bollworm, Helicoverpa armigera. J Pest Sci 87: 163–172. doi: 10.1007/ s10340-013-0541-7 BANR (Board on Agriculture and Natural Resources) (2000) Genetically modified pest-protected plant: science and regulation. p. 292. Barton KA, Whiteley HR, Yang NS (1987) Bacillus thuringiensis δ-endotoxin expressed in transgenic Nicotiana tabacum provides resistance to Lepidopteran insects. Plant Physiology 85: 1103-1109 Biradar SS, Sridevi O, Salimath PM (2009) Genetic enhancement of chickpea for pod borer resistance through expression of CryIAc protein. Karnataka J Agric Sci 22: 467-470. Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49: 423-435 Carrière Y, Crickmore N, Tabashnik BE (2015) Optimizing pyramided transgenic Bt crops for sustainable pest management. Nat Biotechnol 33:161-168. doi: 10.1038/nbt.3099 Choudhary M, Sahi S (2011) In silico designing of insecticidal small interfering RNA (siRNA) for Helicoverpa armigera control. Indian Journal of Experimental Biology 49:469-474. Cohen BM, Gould F, Bentur JC (2000) Bt rice: practical steps to sustainable use. International Rice Research 25: 4-10 Devi VS, Sharma HC, Rao PA (2011) Interaction between host plant resistance and biological activity of Bacillus thuringiensis in managing the pod borer Helicoverpa armigera in chickpea. Crop Protection 30: 962-969 FAOSTAT (2013). Agricultural Data. http://faostat3. fao.org/faostat-gateway/go/to/download/Q/QC/E Ganguly M, Molla KA, Karmakar S, et al., (2014) Development of pod borer-resistant transgenic chickpea using a pod-specific and a constitutive promoter-driven fused cry1Ab/Ac gene. Theor Appl Genet 127:2555–2565. doi: 10.1007/ s00122-014-2397-5 Gassmann AJ, Petzold-Maxwell JL, Clifton EH, et al., (2014) Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. Proc Natl Acad Sci U S A 111:5141–6. doi: 10.1073/ pnas.1317179111 Gaur PM, Jukanti AK, Varshney RK (2012) Impact of Genomic Technologies on Chickpea Breeding Strategies. Agronomy 2:199–221. doi: 10.3390/ agronomy2030199 Giri AP, Harsulkar AM, Deshpande VV, et al., (1998) Chickpea defensive proteinase inhibitors can be inactivated by podborers gut proteinases. Plant Physiol 116: 393–401 © Plant Breeders Union of Turkey (BİSAB) 59 Gordon KHJ, Waterhouse PM (2007) RNAi for insect-proof plants. Nat Biotechnol 25:1231-2. doi: 10.1038/nbt1107-1231 Hegedus D, Erlandson M, Gillott C, et al., (2009) New insights into peritrophic matrix synthesis, architecture, and function.Annu Rev Entomol 54: 285-302 Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol 56: 227-235 ICRISAT (1992). The medium term plan. International Crops Research Institute for Semi-Arid Tropics. Patancheru. India. Indurker S, Misra HS, Eapen S (2007) Genetic transformation of chickpea (Cicer arietinum L.) with insecticidal crystal protein gene using particle gun bombardment. Plant Cell Rep 26:755-763. doi: 10.1007/s00299-006-0283-6 James C (2014) Global status of commercialized Biotech/GM crops: 2012. ISAAA Brief No. 47 ISAAA: Ithaca, NY Jukanti AK, Gaur PM, Gowda CL, et al., (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. British Journal of Nutrition 108: S11-S26. Kar S, Basu D, Das S, et al., (1997) Expression of cryIA(c) gene of Bacillus thurigenesis in transgenic chickpea plants inhibits development of pod borer (Heliothis armigera) larvae. Transgenic Research6: 177-185 Khatodia S, Kharb P, Batra P, Chowdhury VK (2014a) Development and characterization of transgenic chickpea (Cicer arietinum L.) plants with cry1Ac gene using tissue culture independent protocol. International J Adv Res 2: 323-331 Khatodia, S., Kharb, P., Batra, P., & Chowdhury, V. K. (2014b). Real time PCR based detection of transgene copy number in transgenic chickpea lines expressing Cry1Aa 3 and Cry1Ac, 2(4), Int J Pure App Biosci 100-105. Khatodia, S., Bhatotia, K., Passricha, N., Khurana, S. M. P., & Tuteja, N. (2016). The CRISPR/Cas Genome-Editing Tool: Application in Improvement of Crops. Frontiers in Plant Science, 7, 1-13. https://doi.org/10.3389/fpls.2016.00506 Li H, Rodda M, Gnanasambandam A, et al., (2015) Breeding for biotic stress resistance in chickpea: progress and prospects. Euphytica. doi: 10.1007/ s10681-015-1462-8 Mallikarjuna N (2001). Prospects of using Cicer canariense for chickpea improvement. International Chickpea and Pigeonpea Newsletter8: 23-24 Mao Y-B, Cai W-J, Wang J-W, et al., (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–13. doi: 10.1038/nbt1352 Mao Y-B, Tao X-Y, Xue X-Y, et al., (2011) Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Res 20:665–73. doi: 10.1007/ s11248-010-9450-1 Mao Y-B, Xue X-Y, Tao X-Y, et al., (2013) Cysteine protease enhances plant-mediated bollworm RNA interference. Plant Mol Biol 83:119–29. doi: 10.1007/s11103-013-0030-7 Mehrotra M, Sanyal I, Amla D V. (2011) High-efficiency Agrobacterium-mediated transformation of chickpea (Cicer arietinum L.) and regeneration of insect-resistant transgenic plants. Plant Cell Rep 30:1603-1616. doi: 10.1007/ s00299-011-1071-5 Neelima MG, Ramu SV, Sreevathsa R, et al., (2008) In planta transformation strategy to generate transgenic plants in chickpea: Proof of concept with a cry gene. Journal of Plant Biology 35: 201-206 Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26: 393-400 Rao PP, Birthal PS, Bhagavatula S, et al., (2010) Chickpea and pigeonpea economies in Asia: facts, trends and outlook. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, Andhra Pradesh, India. pp. 1-76 Rawat P, Singh AK, Ray K, et al., (2011) Detrimental effect of expression of Bt endotoxin Cry1Ac on in vitro regeneration, in vivo growth and development of tobacco and cotton transgenics. Journal of Biosciences36: 363-376 Rocher EJD, Vargo-Gogola TC, Diehn SH, et al., (1998) Direct evidence for rapid degradation of Bacillus thuringiensis toxin mRNA as a cause of poor expression in plants. Plant Physiology 117: 1445-1461 Romeis J, Sharma HC, Sharman KK, et al., (2004) The potential of transgenic chickpeas for pest control and possible effects on non-target arthropods. Crop Prot 23:923-938 3(1):52-60, 2017 60 bitki ıslahçıları alt birliği www.bisab.org.tr Ekin Journal Sanyal I, Singh AK, Kaushik M, Amla D V (2005) Agrobacterium-mediated transformation of chickpea (Cicer arietinum L.) with Bacillus thuringiensis cry1Ac gene for resistance against pod borer insect Helicoverpa armigera. Plant Sci 168:1135-1146. doi: 10.1016/j.plantsci. 2004.12.015 Schnepf E, Crickmore N, Van Rie J, et al., (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews 62: 775-806 Sharma HC, Crouch JH, Sharma KK, et al., (2002) Applications of biotechnology for crop improvement: prospects and constraints. Plant Science 163: 381-395 Sharma HC, Pampapathy G, Lanka SK, et al., (2005) Antibiosis mechanism of resistance to legume pod borer, Helicoverpa armigera in wild relatives of chickpea. Euphytica 142: 107-117 Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521. doi: 10.1038/ nbt.2597 Tabashnik BE, Carrière Y, Dennehy TJ, et al., (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J Econ Entomol 96: 1031-1038 Tabashnik BE, Gassmann AJ, Crowder DW, et al., (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26: 199–202 Tabashnik BE, Van Rensburg JBJ, Carriere Y (2009) Field- evolved insect resistance to Bt crops: Definition, theory, and data. J Econ Entomol 102: 2011–2025 Varshney RK, Thudi M, May GD, et al., (2010) Legume genomics and breeding. Plant Breeding Rev 33: 257-304 Xiong Y, Zeng H, Zhang Y, et al., (2013) Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. Int J Biol Sci 9:370–81. doi: 10.7150/ijbs.5929 Yadav SS, Kumar J, Yadav SK, et al., (2006) Evaluation of Helicoverpa and drought resistance in desi and kabuli chickpea. Plant Genetic Resources: Characterization and Utilization 4: 198-203. Zhang X, Liu X, Ma J, Zhao J (2013) Silencing of cytochrome P450 CYP6B6 gene of cotton bollworm (Helicoverpa armigera) by RNAi. Bulletin of Entomological Research 584-591. Zhu J-Q, Liu S, Ma Y, et al., (2012) Improvement of pest resistance in transgenic tobacco plants expressing dsRNA of an insect-associated gene EcR. PLoS One 7:e38572. doi: 10.1371/journal.pone.0038572
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Journal Section Articles
Authors

Surender Khatodıa This is me

Publication Date January 31, 2017
Published in Issue Year 2017 Volume: 3 Issue: 1

Cite

APA Khatodıa, S. (2017). Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi. Ekin Journal of Crop Breeding and Genetics, 3(1), 52-60.
AMA Khatodıa S. Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi. Ekin Journal. January 2017;3(1):52-60.
Chicago Khatodıa, Surender. “Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi”. Ekin Journal of Crop Breeding and Genetics 3, no. 1 (January 2017): 52-60.
EndNote Khatodıa S (January 1, 2017) Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi. Ekin Journal of Crop Breeding and Genetics 3 1 52–60.
IEEE S. Khatodıa, “Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi”, Ekin Journal, vol. 3, no. 1, pp. 52–60, 2017.
ISNAD Khatodıa, Surender. “Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi”. Ekin Journal of Crop Breeding and Genetics 3/1 (January 2017), 52-60.
JAMA Khatodıa S. Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi. Ekin Journal. 2017;3:52–60.
MLA Khatodıa, Surender. “Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi”. Ekin Journal of Crop Breeding and Genetics, vol. 3, no. 1, 2017, pp. 52-60.
Vancouver Khatodıa S. Helicoverpa Resistant Chickpea Plants: From Bt Toxins to Plant-Mediated RNAi. Ekin Journal. 2017;3(1):52-60.