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Molecular Biotechnology

, Volume 60, Issue 8, pp 651–663 | Cite as

An Update on Genetic Modification of Chickpea for Increased Yield and Stress Tolerance

  • Manoj Kumar
  • Mohd Aslam Yusuf
  • Manisha Nigam
  • Manoj Kumar
Review

Abstract

Chickpea is a highly nutritious grain legume crop, widely appreciated as a health food, especially in the Indian subcontinent. The major constraints on chickpea production are biotic (Helicoverpa, bruchid, aphid, ascochyta) and abiotic (drought, heat, salt, cold) stresses, which reduce the yield by up to 90%. Various strategies like conventional breeding, molecular breeding, and modern plant breeding have been used to overcome these problems. Conventionally, breeding programs aim at development of varieties that combine maximum number of traits through inter-specific hybridization, wide hybridization, and hybridization involving more than two parents. Breeding is difficult in this crop because of its self-pollinating nature and limited genetic variation. Recent advances in in vitro culture and gene technologies offer unique opportunities to realize the full potential of chickpea production. However, as of date, no transgenic chickpea variety has been approved for cultivation in the world. In this review, we provide an update on the development of genetically modified chickpea plants, including those resistant to Helicoverpa armigera, Callosobruchus maculatus, Aphis craccivora, as well as to drought and salt stress. The genes utilized for development of resistance against pod borer, bruchid, aphid, drought, and salt tolerance, namely, Bt, alpha amylase inhibitor, ASAL, P5CSF129A, and P5CS, respectively, are discussed.

Keywords

Chickpea Transgenics Agrobacterium Abiotic stress Biotic stress 

Abbreviations

ASAL

Allium sativum leaf lectin

Bt

Bacillus thuringiensis

CaMV35S

Cauliflower Mosaic Virus 35S promoter

CSIRO

Commonwealth Scientific and Industrial Research Organisation

GM

Genetically modified

ICRISAT

International Crop Research Institute for Semi-Arid Tropics

IARI

Indian Agricultural Research Institute

IIPR

Indian Institute of Pulses Research

MAS

Marker-assisted selection

Mbps

Mega base pairs

MT

Million tons

mha

Million hectares

P5CS

Δ1-Pyrroline-5-carboxylate synthetase

Notes

Acknowledgements

The study was supported by the New Initiative (as a Cross Flow Technology project) “Root Biology and its Correlation to Sustainable Plant Development and Soil Fertility” from Council of Scientific and Industrial Research (CSIR), and project titled “Characterization of gene(s) responsible for tyloses formation in chickpea during Fusarium oxysporum infection” from Science & Engineering Research Board (SERB), New Delhi, India. The manuscript communication number assigned to this manuscript by the Dean, R&D, Integral University, Lucknow, is IU/R&D/2018-MCN000228.

References

  1. 1.
    Rao, P. P., Birthal, P. S., Bhagavatula, S., & Bantilan, M. C. S. (2010). Chickpea and pigeonpea economies in Asia: Facts, trends and outlook. Patancheru: International Crops Research Institute for the Semi-Arid Tropics.Google Scholar
  2. 2.
    Varshney, R. K., et al. (2013). Draft genome sequence of chickpea (Cicer arietinum L.). Nature Biotechnology, 31, 3.  https://doi.org/10.1038/nbt.2491.CrossRefGoogle Scholar
  3. 3.
    Gaur, P. M., Thudi, M., Samineni, S., & Varshney, R. K. (2014). Advances in chickpea genomics. In N. Gupta, N. Nadarajan & D. Sen Gupta (Eds.), Legumes in the omic era (pp. 73–94). New York: Springer.CrossRefGoogle Scholar
  4. 4.
    Garg, R., Shankar, R., Thakkar, B., et al. (2016). Transcriptome analyses reveal genotype and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Scientific Reports.  https://doi.org/10.1038/srep19228.Google Scholar
  5. 5.
    Ali, Q., Ahsan, M., Farooq, J., & Saleem, M. (2010). Genetic variability and trait association in chickpea (Cicer arietinum L.). Electronic Journal of Plant Breeding, 1, 328–333.Google Scholar
  6. 6.
    Singh, R., Sharma, P., Varshney, R. K., Sharma, S. K., & Singh, N. K. (2008). Chickpea improvement: Role of wild species and genetic markers. Biotechnology and Genetic Engineering Reviews, 25, 267–313.CrossRefGoogle Scholar
  7. 7.
    Gaikwad, A. R., Desai, N. C., Langhi, A. M., & Jadhav, S. D. (2011). Studies on genetic variability in chickpea (Cicer arietinum L.). Ecology, Environment and Conservation, 17, 585–588.Google Scholar
  8. 8.
    Jain, M., Misra, G., Patel, R. K., et al. (2013). A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). The Plant Journal, 74, 715–729.CrossRefGoogle Scholar
  9. 9.
    Gupta, S., Nawaz, K., Parween, S., Roy, R., Sahu, K., Pole, A. K., et al. (2016). Draft genome sequence of Cicer reticulatum L., the wild progenitor of chickpea provides a resource for agronomic trait improvement. DNA Research.  https://doi.org/10.1093/dnares/dsw042.Google Scholar
  10. 10.
    Acharjee, S., & Sarmah, B. K. (2013). Biotechnlogically generating super chickpea for food and national security. Plant Science, 207, 108–116.CrossRefGoogle Scholar
  11. 11.
    Kar, S., et al. (1996). Expression of cry1Ac gene of Bacillus thuringiensis in transgenic chickpea plants inhibits development of borer (Heliothis armigera) larvae. Transgenic Research, 15, 473–497.Google Scholar
  12. 12.
    Sanyal, I., Singh, A. K., 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 Science, 168, 1135–1146.CrossRefGoogle Scholar
  13. 13.
    Biradar, S. S., Sridevi, O., & Salimath, P. M. (2009). Genetic enhancement of chickpea for pod borer resistance through expression of Cry1Ac protein. Karnataka Journal of Agricultural Science, 22, 467–470.Google Scholar
  14. 14.
    Acharjee, S., Sarmah, B. K., Kumar, P. A., Olsen, K., Mahon, R., Moar, W. J., et al. (2010). Transgenic chickpea (Cicer arietinum L.) expressing a sequence-modified cry2Aa gene. Plant Science, 178, 333–339.CrossRefGoogle Scholar
  15. 15.
    Das, A., Datta, S., Thakur, S., Shukla, A., Ansari, J., Sujayanand, G. K., et al. (2017). Expression of a chimeric gene encoding insecticidal crystal protein cry1Aabc of Bacillus thuringiensis in chickpea (Cicer arietinum L.) confers resistance to gram pod borer (Helicoverpa armigera Hubner). Frontiers in Plant Science, 8, 1423.  https://doi.org/10.3389/fpls.2017.01423.CrossRefGoogle Scholar
  16. 16.
    Chakraborty, J., Sen, S., Ghosh, P., Sengupta, A., Basu, D., & Das, S. (2016). Homologous promoter derived constitutive and chloroplast targeted expression of synthetic cry1Ac in transgenic chickpea confers resistance against Helicoverpa armigera. Plant Cell, Tissue and Organ Culture, 125, 521–535.  https://doi.org/10.1007/s11240-016-0968-7.CrossRefGoogle Scholar
  17. 17.
    Kambrekar, D. N. (2016). Management of legume podborer, Helicoverpa armigera with host plant resistance. Legume Genomics and Genetics.  https://doi.org/10.5376/lgg.2016.07.0005.Google Scholar
  18. 18.
    Sarmah, B. K., et al. (2004). Transgenic chickpea seeds expressing high levels of a bean alfa-amylase inhibitor. Molecular Breeding, 14, 73–82.CrossRefGoogle Scholar
  19. 19.
    Chakraborti, D., Sarkar, A., Mondal, H. A., & Das, S. (2009). Tissue specific expression of potent insecticidal, Allium sativum leaf agglutinin (ASAL) in important pulse crop, chickpea (Cicer arietinum L.) to resist the phloem feeding Aphis craccivora. Transgenic Research, 18, 529–544.CrossRefGoogle Scholar
  20. 20.
    Bhatnagar-Mathur, P., Vadez, V., Devi, M. J., Lavanya, M., Vani, G., & Sharma, K. K. (2009). Genetic engineering of chickpea (Cicer arietinum L.) with the P5CSF129A gene for osmoregulation with implications on drought tolerance. Molecular Breeding, 23, 591–606.  https://doi.org/10.1007/s11032-009-9258-y.CrossRefGoogle Scholar
  21. 21.
    Anbanzhagan, K., Bhatnagar-Mathur, P., Vadez, V., Reddy, D. S., Kishore, P. B. K., & Sharma, K. K. (2015). DREB1A overexpression in transgenic chickpea alters key traits influencing plant water budget across water regimes. Plant Cell Reports, 34, 199–210.CrossRefGoogle Scholar
  22. 22.
    Ghanti, K. K., Sujata, S., Vijay, K. G., Kumar, B. M., et al. (2011). Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. Biologia Plantarum, 55, 634.  https://doi.org/10.1007/s10535-011-0161-0.CrossRefGoogle Scholar
  23. 23.
    Jukanti, A. K., Gaur, P. M., Gowda, C. L. L., & Chibbar, R. N. (2012). Nutritional quality and health benefits of chickpea (Cicer arietinum L.): A review. British Journal of Nutrition, 108, S11–S26.CrossRefGoogle Scholar
  24. 24.
    Wang, N., Hatcher, D. W., Tyler, R. T., Toews, R., Gawalko, E. J. (2010). Effect of cooking on the composition of beans (Phaseolus vulgaris L.) and chickpeas (Cicer arietinum L.). Food Research International, 43, 589–594.CrossRefGoogle Scholar
  25. 25.
    Chau, C. F., Cheung, P. C., & Wong, Y. S. (1997). Effect of cooking on content of amino acids and antinutrients in three Chinese indigenous legume seeds. Journal of the Science of Food and Agriculture, 75, 447–452.CrossRefGoogle Scholar
  26. 26.
    Wang, N., Lewis, M. J., Brennan, J. G., & Westby, A. (1997). Effect of processing methods on nutrients and anti-nutritional factors in cowpea. Food Chemistry, 58, 59–68.CrossRefGoogle Scholar
  27. 27.
    El-Adawy, T. A. (2002). Nutritional composition and antinutritional factors of chickpeas (Cicer arietinum L.) undergoing different cooking methods and germination. Plant Foods for Human Nutrition, 57, 83–97.CrossRefGoogle Scholar
  28. 28.
    Singh, P. K., Shrivastava, N., Sharma, B., & Bhagyawant, S. S. (2015). Effect of domestic processes on chickpea seeds for antinutritional contents and their divergence. American Journal of Food Science and Technology, 3(4), 111–117.Google Scholar
  29. 29.
    Gupta, N., Shrivastava, N., & Bhagyawant, S. S. (2017). Multivariate analysis based on nutritional value, antinutritional profile and antioxidant capacity of forty chickpea genotypes grown in India. Journal of Nutrition and Food Sciences.  https://doi.org/10.4172/2155-9600.1000600.Google Scholar
  30. 30.
    Patil, S. P., Niphadkar, P. V., & Bapat, M. M. (2001). Chickpea: A major food allergen in the Indian subcontinent and its clinical and immunochemical correlation. Annals of Allergy, Asthma & Immunology, 87(2), 140–145.  https://doi.org/10.1016/S1081-1206(10)62209-0.CrossRefGoogle Scholar
  31. 31.
    India’s trade destination of chickpea (2015–2016). Retrieved November 11, 2017 from http://agricoop.nic.in/sites/default/files/Pulses.pdf.
  32. 32.
    Muehlbauer, F. J., & Sarker, A. (2017). Economic importance of chickpea: Production, value, and world trade. In R. K. Varshney et al. (Eds.), The chickpea genome, compendium of plant genomes.  https://doi.org/10.1007/978-3-319-66117-9_2.
  33. 33.
    Leport, L., Turner, N. C., French, R. J., Barr, M. D., Duda, R., et al. (1999). Physiological responses of chickpea genotypes to terminal drought in a Mediterranean-type environment. European Journal of Agronomy, 11, 279–291.CrossRefGoogle Scholar
  34. 34.
    Worldwide chickpea production scenario in 1980 and 2016 (2017). Retrieved May 19, 2018 from http://www.fao.org/faostat/en/#compare.
  35. 35.
    Alexandratos, N., & Bruinsma, J. (2012). World agriculture towards 2030/2050: The 2012 revision. Rome: Food and Agriculture Organization of The United Nations.Google Scholar
  36. 36.
    State wise share to total production and area of chickpea in India (2015–2016). Retrieved November 10, 2017 from http://www.commoditiescontrol.com/eagritrader/common/newsdetail.php?type=SPR&itemid=8204&comid=,2,&frm=admin.
  37. 37.
    Ryan, J. (1997). A global perspective on pigeonpea and chickpea sustainable production system: Present status and future potential. In A. Asthana, & A. M. Kapur (Eds.), Recent advances in pulses research in India (pp. 1–31). Kalyanpur: Indian Society for Pulses Research and Development.Google Scholar
  38. 38.
    Millan, T., Clarke, H. J., Siddique, K. H. M., Bhuriwalla, H. K., Gaur, P. M., Kumar, J., et al. (2006). Chickpea molecular breeding: New tools and concepts. Euphytica, 147, 81–103.CrossRefGoogle Scholar
  39. 39.
    Chaturvedi, S. K., & Nadarajan, N. (2010). Genetic enhancement for grain yield in chickpea accomplishments and resetting research agenda. Electronic Journal of Plant Breeding, 1(4), 611–615.Google Scholar
  40. 40.
    Levitt, J. (1972). Responses of plants to environmental stresses. New York: Academic Press.Google Scholar
  41. 41.
    Turner, N. C. (1986). Crop water deficit: A decade of progress. Advances in Agronomy, 39, 1–51.CrossRefGoogle Scholar
  42. 42.
    Loomis, R. S., & Connor, D. J. (1992). Crop ecology: Productivity and management in agricultural systems (pp. 224–256). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  43. 43.
    Bent, A. F. (1996). Plant disease resistance genes: Function meets structure. The Plant Cell, 8, 1757–1771.CrossRefGoogle Scholar
  44. 44.
    Hulbert, S. H., Webb, C. A., Smith, S. M., & Sun, Q. (2001). Resistance gene complexes: Evolution and utilization. Annual Review of Phytopathology, 39, 285–312.CrossRefGoogle Scholar
  45. 45.
    Tameling, W. I. L., Elzinga, S. D. J., Darmin, P. S., Vossen, J. H., Takken, F. L. W., et al. (2002). The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. The Plant Cell, 14, 2929–2939.CrossRefGoogle Scholar
  46. 46.
    Kobe, B., & Deisenhofer, J. (1995). A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature, 374, 183–186.CrossRefGoogle Scholar
  47. 47.
    Lesiter, R. T., & Katagiri, F. (2000). A resistance gene product of the nucleotide binding site-leucine rich repeats class can form a complex with bacterial avirulence proteins in vivo. The Plant Journal, 22, 345–354.CrossRefGoogle Scholar
  48. 48.
    Dangl, J. L., & Jones, J. D. G. (2001). Plant pathogens and integrated defence responses to infection. Nature, 411, 826–833.CrossRefGoogle Scholar
  49. 49.
    Meyers, B. C., Kozik, A., Griego, A., Kuang, H., & Michelmore, R. W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. The Plant Cell, 15, 809–834.CrossRefGoogle Scholar
  50. 50.
    Monosi, B., Wisser, R. J., Pennill, L., & Hulbert, S. H. (2004). Full-genome analysis of resistance gene homologues in rice. Theoretical and Applied Genetics, 109, 1434–1447.CrossRefGoogle Scholar
  51. 51.
    Ameline-Torregrosa, C., Wang, B. B., O’bleness, M. S., Deshpande, S., Zhu, H., et al. (2008). Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiology, 146, 5–21.CrossRefGoogle Scholar
  52. 52.
    Radwan, O., Gandhi, S., Heesacker, A., Whitaker, B., Taylor, C., et al. (2008). Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Molecular Genetics and Genomics, 280, 111–125.CrossRefGoogle Scholar
  53. 53.
    Glynn, N. C., Comstock, J. C., Sood, S. G., Dang, P. M., & Chaparro, J. X. (2008). Isolation of nucleotide binding site-leucine rich repeat and kinase resistance gene analogues from sugarcane Saccharum spp. Pest Management Science, 64, 48–56.CrossRefGoogle Scholar
  54. 54.
    Kumar, M., Mishra, S., Dixit, V. K., Kumar, M., Agrawal, L., Chauhan, P. S., et al. (2015). Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea. Plant Signaling & Behavior.  https://doi.org/10.1080/15592324.2015.1071004.Google Scholar
  55. 55.
    Dua, R. P., & Sharma, P. C. (1995). Salinity tolerance of kabuli and desi chickpea genotypes. International Chickpea and Pigeonpea Newsletter, 2, 19–22.Google Scholar
  56. 56.
    Dua, R. P., Chaturvedi, S. K., & Shiv, S. (2001). Reference varieties of chickpea for IPR regime. Kanpur: Indian Institute of Pulses Research.Google Scholar
  57. 57.
    Shanower, T. G., Kelley, T. G., & Cowgill, S. E. (1998). Development of effective and environmentally sound strategies to control Helicoverpa armigera in pigeonpea and chickpea production systems. In R. K. Saini (Ed.), Tropical entomology. Proceedings of the 3rd international conference on tropical entomology (pp. 239–260). Nairobi: lClPE Science Press.Google Scholar
  58. 58.
    Sharma, H. C., Gowda, C. L. L., Stevenson, P. C., Ridsdill-Smith, T. J., Clement, S. L., Ranga Rao, G. V., et al. (2007). Host plant resistance and insect pest management in chickpea. In S. S. Yadav, R. R. Redden, W. Chen & B. Sharma (Eds.), Chickpea breeding and management (pp. 520–537). Wallingford: CAB International.CrossRefGoogle Scholar
  59. 59.
    Forrester, N. W., Cahill, M., Bird, L., & Layland, J. K. (1993). Management of pyrethoid and endosulfan resistance in Helicoverpu urmigeru (Lepidoptera: Noctuidae) in Australia. Bulletin of Entomological Research, 1, 1–132.Google Scholar
  60. 60.
    Kranthi, K. R., Jadhav, D. R., Kranthi, S., Wanjari, R. R., Ali, S. S., & Russcll, D. A. (2002). Insecticide resistance in five major insect pests of cotton in India. Crop Protection, 21, 449–460.CrossRefGoogle Scholar
  61. 61.
    Fontana, G. S., Santini, L., Caretto, S., Frugis, G., & Mariotti, D. (1993). Genetic transformation in the grain legume (Cicer arietinum L.). Plant Cell Reports, 12, 194–198.CrossRefGoogle Scholar
  62. 62.
    Ganguly, M., Molla, K. A., Karmakar, S., Datta, K., & Datta, S. K. (2014). Development of pod borer-resistant transgenic chickpea using a pod-specific and a constitutive promoter-driven fused cry1Ab/Ac gene. Theoretical and Applied Genetics, 127, 2555–2565.  https://doi.org/10.1007/s00122-014-2397-5.CrossRefGoogle Scholar
  63. 63.
    Sharma, H. C., Sharma, K. K., & Crouch, J. H. (2004). Genetic transformation of crops for insect resistance: Potential and limitations. Critical Reviews in Plant Sciences, 23, 47–72.CrossRefGoogle Scholar
  64. 64.
    Singh, K. B., Malhotra, R. S., Halila, H. M., Knights, E. J., & Verma, M. M. (1994). Current status and future strategy in breeding chickpea for resistance to biotic and abiotic stresses. Euphytica, 73, 137–149.CrossRefGoogle Scholar
  65. 65.
    Dayal, S., Lavanya, M., Devi, P., & Sharma, K. K. (2003). An efficient protocol for shoot regeneration and genetic transformation of pigeon pea (Cajanus cajan L. Millsp.) using leaf explants. Plant Cell Reports, 21, 1072–1079.CrossRefGoogle Scholar
  66. 66.
    Boulter, D. (1993). Insect pest control by copying nature using genetically engineered crops. Phytochemistry, 34, 1453–1466.CrossRefGoogle Scholar
  67. 67.
    Ussuf, K. K., Laxmi, N. H., & Mita, R. (2001). Protease inhibitors: Plant derived genes of insecticidal protein for developing insect resistant transgenic plants. Current Science, 80, 847–853.Google Scholar
  68. 68.
    Shade, R. E., Schroeder, R. E., Poueyo, J. J., Tabe, L. M., Murdock, L. I., Higgins, T. J. V., et al. (1994). Transgenic pea seeds expressing the α-amylase inhibitor of the common bean are resistant to bruchid beetles. Nature Biotechnology, 12, 793–796.CrossRefGoogle Scholar
  69. 69.
    Schroeder, H. E., Gollash, S., & Moore, A. (1995). Bean α-amylase inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L.). Plant Physiology, 107, 1233–1239.CrossRefGoogle Scholar
  70. 70.
    Ryan, C. A. (1990). Protease inhibitors in plants: Genes for improving defense against insects and pathogens. Annual Review of Phytopathology, 28, 25–45.CrossRefGoogle Scholar
  71. 71.
    Ishimoto, M., & Chrispeels, M. J. (1996). Protective mechanism of the Mexican bean weevil against high levels of α-amylase inhibitor in the common bean. Plant Physiology, 111, 393–401.CrossRefGoogle Scholar
  72. 72.
    Ignacimuthu, S., & Prakash, S. (2006). Agrobacterium-mediated transformation of chickpea with alpha-amylase inhibitor gene for insect resistance. Journal of Biosciences, 31(3), 339–345.CrossRefGoogle Scholar
  73. 73.
    Chokshi, D. (2006). Toxicity studies of Blockal, a dietary supplement containing phase 2 starch neutralizer (Phase 2), a standardized extract of the common white kidney bean (Phaseolus vulgaris). International Journal of Toxicology, 25(5), 361–371.CrossRefGoogle Scholar
  74. 74.
    Barrett, M. L., & Udani, J. K. (2011). A proprietary alpha-amylase inhibitor from white bean (Phaseolus vulgaris): A review of clinical studies on weight loss and glycemic control. Nutrition Journal, 10, 24. http://www.nutritionj.com/content/10/1/24.
  75. 75.
    Lee, R. Y., Reiner, D., Dekan, G., Moore, A. E., Higgins, T. J., & Epstein, M. M. (2013). Genetically modified α-amylase inhibitor peas are not specifically allergenic in mice. PLoS ONE, 8, e52972.  https://doi.org/10.1371/journal.pone.0052972.CrossRefGoogle Scholar
  76. 76.
    Dutta, I., Saha, P., Majumder, P., Sarkar, A., Chakraborti, D., Banerjee, S., et al. (2005). The efficacy of a novel insecticidal protein, Allium sativum leaf lectin (ASAL), against homopteran insects monitored in transgenic tobacco. Plant Biotechnology Journal, 3(6), 601–611.CrossRefGoogle Scholar
  77. 77.
    Dutta, I., Majumder, P., Saha, P., Ray, K., & Das, S. (2005). Constitutive and phloem specific expression of Allium sativum leaf agglutinin (ASAL) to engineer aphid (Lipaphis erysimi) resistance in transgenic Indian mustard (Brassica juncea). Plant Science.  https://doi.org/10.1016/j.plantsci.2005.05.016.Google Scholar
  78. 78.
    Yarasi, B., Sadumpati, V., Immanni, C. P., Vudem, D. R., & Khareedu, V. R. (2008). Transgenic rice expressing Allium sativum leaf agglutinin (ASAL) exhibits high level resistance against major sap-sucking pests. BMC Plant Biology, 8, 102–115.CrossRefGoogle Scholar
  79. 79.
    Shukla, A. K., Upadhyay, S. K., Mishra, M., Saurabh, S., Singh, R., Singh, H., et al. (2016). Expression of an insecticidal fern protein in cotton protects against whitefly. Nature Biotechnology, 34, 1046–1051.CrossRefGoogle Scholar
  80. 80.
    Chickpea improved varieties. Retrieved November 10, 2017 from http://www.dpd.gov.in/VARIETIES-Web%20site.pdf.
  81. 81.
    Haware, M. P., & Nene, Y. L. (1982). Races of Fusarium oxysporum. Plant Disease, 66, 809–810.CrossRefGoogle Scholar
  82. 82.
    Pratap, A., Chaturvedi, S. K., Tomar, R., Rajan, N., Malviya, N., Thudi, M., et al. (2017). Marker-assisted introgression of resistance to fusarium wilt race 2 in Pusa 256, an elite cultivar of desi chickpea. Molecular Genetics and Genomics, 292, 1237–1245.  https://doi.org/10.1007/s00438-017-1343-z.CrossRefGoogle Scholar
  83. 83.
    Gil, J., Castro, J. P., Millan, T., Madrid, E., & Rubio, J. (2017). Development of new kabuli large-seeded chickpea materials with resistance to Ascochyta blight. Crop and Pasture Science, 68(11), 967–972.  https://doi.org/10.1071/CP17055.CrossRefGoogle Scholar
  84. 84.
    Li, Y., Ruperao, P., Batley, J., Edwards, D., Davidson, J., Hobson, K., et al. (2017). Genome analysis identified novel candidate genes for Ascochyta blight resistance in chickpea using whole genome re-sequencing data. Frontiers in Plant Science, 8, 359.  https://doi.org/10.3389/fpls.2017.00359.Google Scholar
  85. 85.
    Garg, T., Mallikarjuna, B. P., Thudi, M., Samineni, S., Singh, S., Sandhu, J. S., et al. (2018). Identification of QTLs for resistance to Fusarium wilt and Ascochyta blight in a recombinant inbred population of chickpea (Cicer arietinum L.). Euphytica, 214, 45.  https://doi.org/10.1007/s10681-018-2125-3.CrossRefGoogle Scholar
  86. 86.
    Indurker, S., Misra, H. S., & Eapen, S. (2007). Genetic transformation of chickpea (Cicer arietinum L.) with insecticidal crystal protein gene using particle gun bombardment. Plant Cell Reports, 26, 755–763.  https://doi.org/10.1007/s00299-006-0283-6.CrossRefGoogle Scholar
  87. 87.
    Asharani, B. M., Ganeshaiah, K. N., Raja, A., Kumar, V., & Makarla, U. K. (2011). Transformation of chickpea lines with Cry1X using in planta transformation and characterization of putative transformants T1 lines for molecular and biochemical characters. Journal of Plant Breeding and Crop Science, 3(16), 413–423.CrossRefGoogle Scholar
  88. 88.
    Mehrotra, M., Singh, A. K., Sanyal, I., et al. (2011). Pyramiding of modified cry1Ab and cry1Ac genes of Bacillus thuringiensis in transgenic chickpea (Cicer arietinum L.) for improved resistance to pod borer insect Helicoverpa armigera. Euphytica, 182, 87.  https://doi.org/10.1007/s10681-011-0501-3.CrossRefGoogle Scholar
  89. 89.
    Chiaiese, P., Ohkama-Ohtsu, N., Molvig, L., Godfree, R., Dove, H., Hocart, C., et al. (2004). Sulphur and nitrogen nutrition influence the response of chickpea seeds to an added, transgenic sink for organic sulphur. Journal of Experimental Botany, 55, 1889–1901.  https://doi.org/10.1093/jxb/erh198.CrossRefGoogle Scholar
  90. 90.
    Nester, E. W., Altosaar, I., & Stotzky, G. (2002). 100 years of Bacillus thuringiensis: A critical scientific assessment. Ithaca: American Academy of Microbiology Colloquium Report. Based on Colloquium.Google Scholar
  91. 91.
    Collard, B. C. Y., & Mackill, D. J. (2008). Marker-assisted selection: An approach for precision plant breeding in the twenty-first century. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 557–572.CrossRefGoogle Scholar
  92. 92.
    Gao, L., et al. (2013). Do transgenesis and marker-assisted backcross breeding produce substantially equivalent plants?—A comparative study of transgenic and backcross rice carrying bacterial blight resistant gene Xa21. BMC Genomics, 14, 738.CrossRefGoogle Scholar
  93. 93.
    Sheoran, S., Singh, R. K., & Tripathi, S. (2018). Marker assisted backcross breeding in chickpea (Cicer arietinum L.) for drought tolerance. International Journal of Chemical Studies, 6(1), 1046–1050.Google Scholar
  94. 94.
    Khan, A., Sovero, V., & Gemenet, D. (2016). Genome-assisted breeding for drought resistance. Current Genomics, 17(4), 330–342.  https://doi.org/10.2174/1389202917999160211101417.CrossRefGoogle Scholar
  95. 95.
    Ahmad, Z., Mumtaz, A. S., Ghafoor, A., Ali, A., & Nisar, M. (2014). Marker Assisted Selection (MAS) for chickpea Fusarium oxysporum wilt resistant genotypes using PCR based molecular markers. Molecular Biology Reports, 41, 6755–6762.  https://doi.org/10.1007/s11033-014-3561-3.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Manoj Kumar
    • 1
    • 2
  • Mohd Aslam Yusuf
    • 3
  • Manisha Nigam
    • 4
  • Manoj Kumar
    • 2
  1. 1.Department of BiosciencesIntegral UniversityLucknowIndia
  2. 2.Division of Plant Microbe InteractionsCSIR-National Botanical Research InstituteLucknowIndia
  3. 3.Department of BioengineeringIntegral UniversityLucknowIndia
  4. 4.Department of BiochemistryHemvati Nandan Bahuguna, Garhwal University, SrinagarGarhwalIndia

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