Genome Editing and Abiotic Stress Tolerance in Crop Plants

  • Giridara Kumar Surabhi
  • Bijayalaxmi Badajena
  • Santosh Kumar Sahoo


Abiotic stresses such as drought, salinity, high temperature, chilling, and heavy metals have caused alterations in plant growth and development, threatening crop yield and quality, and leading to global food insecurity. In this aspect, plant breeders have developed many genetic engineering approaches to enhance crop productivity, which are not able to meet the demand of food production as the inheritance of abiotic stress tolerance is so complex. To overcome the limitations of genetic engineering techniques, plant breeders are now focusing on recent availability of genome editing because of its simplicity, high efficiency, and precise target modification at genomic loci for developing abiotic stress-tolerant crops. Advancements in genome editing technologies such as zinc finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs), and clustered regularly interspaced short palindromic repeats (CRISPR/Cas9) have made it possible for molecular biologists to more precisely target any gene of interest. However, ZFNs and TALENs are costly and protracted as they involve intricate steps that require protein engineering. Among these techniques, CRISPR/Cas9 is widely used for reasons of its simplicity, low cost, and ease of genome editing. This chapter focuses on the application of recent genome editing tools in advancing abiotic stress tolerance in different crop plants.


Abiotic stress ZFN CRISPR TALEN Drought Salinity Cold Heavy metals 



CRISPR-associated protein 9


Clustered regularly interspaced short palindromic repeats


Double-strand breaks


Genome editing/Genetic engineering


Germination percentage


Germination rate


Homology directed repair


Homologous recombination


Mitogen-activated protein kinase


Nonhomologous end-joining


Transcription activator-like


Transcription activation-like effector nucleases


Truncated RNA


Zinc finger nucleases



Work in the laboratory of GKS is supported by the Forest and Environment Department, Government of Odisha, India, and is gratefully acknowledged. The authors apologize for being unable to cite all relevant papers.


  1. Akhtar I, Nazir N (2013) Effect of water logging and drought stress in plants. Int J Water Resour Environ Sci 22:34–40Google Scholar
  2. Anderssona M, Turessona H, Olssona N, Fälta A-S, Ohlssona P, Gonzalezb MN, Samuelssond M, Hofvandera P (2018) Genome editing in potato via CRISPR-Cas9 ribonucleoprotein delivery. Physiol Plant 164:1–8CrossRefGoogle Scholar
  3. Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell. Scholar
  4. Ashraf MA, Akbar A, Askari SH, Iqbal M, Rasheed R, Hussain I (2018) Recent advances in abiotic stress tolerance of plants through chemical priming: an overview. In: Advances in seed priming, pp 51–79CrossRefGoogle Scholar
  5. Bechtold U, Field B (2018) Molecular mechanisms controlling plant growth during abiotic stress. J Exp Bot 69:2753–2758PubMedPubMedCentralCrossRefGoogle Scholar
  6. Belhaj K, Garcia AC, Kamoun S, Nekrasov V (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39PubMedPubMedCentralCrossRefGoogle Scholar
  7. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84PubMedCrossRefGoogle Scholar
  8. Bo W, Zhaohui Z, Huanhuan Z, Xia W, Binglin L, Lijia Y, Xiangyan H, Deshui Y, Xuelian Z, Chunguo W, Wenqin S, Chengbin C, Yong Z (2019) Targeted mutagenesis of NAC transcription factor gene, OsNAC041, leading to salt sensitivity in rice. Rice Sci 26:98–108CrossRefGoogle Scholar
  9. Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52PubMedCrossRefGoogle Scholar
  10. Brooks C, Nekrasov V, Lippman ZB, Eck JV (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-Associated9 system. Plant Physiol 166:1292–1297PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cai Y, Chen L, Liu X, Guo C, Sun S, Wu C, Jiang B, Han T, Hou W (2018) CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnol J 16:176–185PubMedCrossRefGoogle Scholar
  12. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39:e82–e82PubMedPubMedCentralCrossRefGoogle Scholar
  13. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761PubMedPubMedCentralCrossRefGoogle Scholar
  14. Christian M, Qi Y, Zhang Y, Voytas DF (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 3:1697–1705PubMedCrossRefGoogle Scholar
  15. Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, Daulhac A, Coffman A, Yabandith A, Retterath A, Haun W, Baltes NJ, Mathis L, Voytas DF, Zhang F (2015) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14(1):169–176PubMedCrossRefGoogle Scholar
  16. Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99PubMedCrossRefGoogle Scholar
  17. Cordones MN, Mohamed S, Tanoi K, Natsuko Kobayashi NI, Takagi K, Vernet A (2017) Production of low-Cs C rice plants by inactivation of the K C transporter OsHAK1 with the CRISPR-Cas system. Plant J 92:43–56CrossRefGoogle Scholar
  18. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163PubMedPubMedCentralCrossRefGoogle Scholar
  19. Curtin SJ, Anderson JE, Starker CG, Baltes NJ, Mani D (2013) Targeted mutagenesis for functional analysis of gene duplication in legumes. Methods Mol Biol 1069:25–42PubMedCrossRefPubMedCentralGoogle Scholar
  20. Daryanto S, Wang L, Jacinthe P-A (2016) Global synthesis of drought effects on maize and wheat production. PlosOne 11:e0156362CrossRefGoogle Scholar
  21. Du H, Zeng X, Zhao M, Cui X, Wang Q, Yang H, Cheng H (2016) Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol 217:90–97PubMedCrossRefPubMedCentralGoogle Scholar
  22. Duan J, Kai W (2012) OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS One 7:e45117PubMedPubMedCentralCrossRefGoogle Scholar
  23. Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan AZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147PubMedPubMedCentralCrossRefGoogle Scholar
  24. FAOSTAT (2016) FAOSTAT Database. Accessed 8 Feb 2018
  25. Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS et al (2017) Drought stress in grain legumes during reproduction and grain filling. J Agron Crop Sci 203:81–102CrossRefGoogle Scholar
  26. Forsyth A, Weeks T, Richael C, Duan H (2016) Transcription activator-like effector nucleases (TALEN)-mediated targeted DNA insertion in potato plants. Front Plant Sci 17:1572Google Scholar
  27. Gabaldón-Leal C, Webber H, Otegui ME, Slafer GA, Ordónez R, Gaiser T, Loritea IJ, Ruiz-Ramos M, Ewert F (2016) Modelling the impact of heat stress on maize yield formation. Field Crops Res 198:226–237CrossRefGoogle Scholar
  28. Gall HL, Philippe F, Domon J-M, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plan Theory 4:112–166Google Scholar
  29. Gao C (2015) Genome editing in crops: from bench to field. Natl Sci Rev 2:13–15CrossRefGoogle Scholar
  30. Gao W, Long L, Tian X, Xu F, Liu J, Singh PK, Botella JR, Song C (2017) Genome editing in cotton with the CRISPR/Cas9 system. Front Plant Sci 8:1364PubMedPubMedCentralCrossRefGoogle Scholar
  31. Grissa I, Vergnaud G, Pourcel C (2007) CRISPR Finder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:52–57CrossRefGoogle Scholar
  32. Guo M, Liu J-H, Ma X, Luo D-X, Gang Z-H, Lu M-H (2016) The plant heat transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 7:1–13Google Scholar
  33. Gupta A, Gopal M, Thomas GV, Manikandan V, Gajewski J, Thomas G, Seshagiri S, Schuster SC, Rajesh P, Gupta R (2015) Whole genome sequencing and analysis of plant growth promoting bacteria isolated from the rhizosphere of plantation crops coconut, cocoa and arecanut. PLoS One 9:e104259CrossRefGoogle Scholar
  34. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical and molecular characterization. Int J Genomics 2014(701596):1–18CrossRefGoogle Scholar
  35. Howells RM, Craze M, Bowden S, Wallington EJ (2018) Efficient generation of stable, heritable gene edits in wheat using CRISPR/Cas9. BMC Plant Biol 18:215PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hryhorowicz M, Ski DL, Zeyland J, Słomski R (2017) CRISPR/Cas9 immune system as a tool for genome engineering. Arch Immunol Ther Exp 65:233–240CrossRefGoogle Scholar
  37. Hu C, Quan C, Zhou J, Yu Q, Bai Z, Xu Z, Gao X, Li L, Zhu J, Chen R (2018) Identification and characterization of a novel abiotic stress responsive OsTHIC gene from rice. Biotechnol Biotechnol Equip 32:874–880CrossRefGoogle Scholar
  38. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169:5429–5433PubMedPubMedCentralCrossRefGoogle Scholar
  39. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:1–10CrossRefGoogle Scholar
  40. Jaganathan D, Ramasamy K, Sellamuthu G, Jayabalan S, Venkataraman G (2018) CRISPR for crop improvement: an update review. Front Plant Sci 9:985PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jain M (2015) Functional genomica of abiotic stress tolerance in plants: a CRISPR approach. Front Plant Sci 6:1–4CrossRefGoogle Scholar
  42. Jallad KN (2015) Heavy metal exposure from ingesting rice and its related potential hazardous health risks to humans. Environ Sci Pollut Res Int 22:15449–15458PubMedCrossRefGoogle Scholar
  43. Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9:e93806PubMedPubMedCentralCrossRefGoogle Scholar
  44. Jiang W, Zhou H, Bi H, Fromm M, Yang B (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41:e188PubMedPubMedCentralCrossRefGoogle Scholar
  45. Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55PubMedCrossRefGoogle Scholar
  46. Kamburova VS, Nikitina EV, Shermatov SE, Buriev ZT, Kumpatla SP, Emani C, Abdurakhmonov IY (2017) Genome editing in plants: an overview of tools and applications. Int J Agron 2017:1–15CrossRefGoogle Scholar
  47. Kamthan A, Chaudhury A, Kamthan M, Datta A (2016) Genetically modified (GM) crops: milestones and new advances in crop improvement. Theor Appl Genet 129:1639–1655PubMedCrossRefGoogle Scholar
  48. Kim D, Alptekin B, Budak H (2018) CRISPR/Cas9 genome editing in wheat. Funct Integr Genomics 18:31–41PubMedCrossRefGoogle Scholar
  49. Lamaoui M, Jemo M, Datla R, Bekkaoui F (2018) Heat and drought stresses in crops and approaches for their mitigation. Front Chem 6:26PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lee DK, Chung PJ, Jeong JS, Jang G, Bang SW, Jung H, Kim YS, Ha SH, Choi YD, Kim JK (2017) The rice OsNAC6 transcription factor orchestrates multiple molecular mechanisms involving root structural adaptions and nicotianamine biosynthesis for drought tolerance. Plant Biotechnol J 15:754–764PubMedPubMedCentralCrossRefGoogle Scholar
  51. Lei M, Tie BQ, Song ZG, Liao BH, Lepo JE, Huang YZ (2015) Heavy metal pollution and potential health risk assessment of white rice around mine areas in Hunan Province, China. Food Secur 7:45–54CrossRefGoogle Scholar
  52. Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87PubMedCrossRefGoogle Scholar
  53. Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B (2010) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39:359–372PubMedPubMedCentralCrossRefGoogle Scholar
  54. Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392PubMedCrossRefGoogle Scholar
  55. Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, Li J, Gao C (2016) Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9. Nat Plants 2(10)Google Scholar
  56. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Sheen J (2013) Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31:688–691PubMedPubMedCentralCrossRefGoogle Scholar
  57. Li JF, Zhang D, Sheen J (2014) Cas9-Based genome editing in Arabidopsis and tobacco. Methods Enzymol 546:459–472PubMedCrossRefGoogle Scholar
  58. Li Y, Cai H, Liu P, Wang C, Gao H, Wu C et al (2017) Arabidopsis MAPKKK18 positively regulates drought stress resistance via downstream MAPKK3. Biochem Biophys Res Commun 484:292–297PubMedCrossRefGoogle Scholar
  59. Li S, Zhang X, Wang W, Guo X, Wu Z, Du W, Zhao Y, Xia L (2018) Expanding the scope of CRISPR/Cpf1-mediated genome editing in rice. Mol Plant 11(7):995–998PubMedCrossRefGoogle Scholar
  60. Li J, Yu D, Qanmber G, Lu L, Wang L, Zheng L, Liu Z, Wu H, Liu X, Chen Q, Li F, Yang Z (2019a) GhKLCR1, a kinesin light chain-related gene, induces drought-stress sensitivity in Arabidopsis. Sci China Life Sci 62:63–75PubMedCrossRefGoogle Scholar
  61. Li R, Liu C, Zhao R, Wang L, Chen L, Yu W, Zhang S, Sheng J, Shen L (2019b) CRISPR/Cas9-mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol 19:38PubMedPubMedCentralCrossRefGoogle Scholar
  62. Liang D, Nia Z, Xia H, Xie Y, Lv X, Wang J, Lin L, Deng Q, Luo X (2019) Exogenous melatonin promotes biomass accumulation and photosynthesis of kiwifruit seedlings under drought stress. Sci Horticult 246:34–43CrossRefGoogle Scholar
  63. Liu L, Ji H, An J, Shi K, Ma J, Liu B, Tang L, Cao W, Zhu Y (2019) Response of biomass accumulation in wheat to low-temperature stress at jointing and booting stages. Environ Exp Bot 157:46–57CrossRefGoogle Scholar
  64. Lloyd A, Plaisier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci U S A 102:2232–2237PubMedPubMedCentralCrossRefGoogle Scholar
  65. Long L, Guo D-D, Gao W, Yang W-W, Hou L-P, Ma X-N, Miao Y-C, Botella JR, Song C-P (2018) Optimization of CRISPR/Cas9 genome editing in cotton by improved sgRNA expression. Plant Methods 14:85PubMedPubMedCentralCrossRefGoogle Scholar
  66. Lou D, Wang H, Liang G, Yu D (2017) OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Front Plant Sci 8Google Scholar
  67. Ma X, Zhu Q, Chen Y, Liu YG (2016) Crispr/cas9 platforms for genome editing in plants: developments and applications. Mol Plant 9:961–974PubMedCrossRefGoogle Scholar
  68. Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM, Eichtinger M, Unger-Wallace E (2008) Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 31:294–301PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu JK (2011) De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci U S A 108:2623–2628PubMedPubMedCentralCrossRefGoogle Scholar
  70. Mao X, Zheng Y, Xiao K, Wei Y, Zhu Y, Cai Q (2018) OsPRX2 contributes to stomatal closure and improves potassium deficiency tolerance in rice. Biochem Biophys Res Commun 495:461–467PubMedCrossRefGoogle Scholar
  71. Marco F, Bitrián CP, Venkat Rajam M, Alcázar R, Tiburcio AF (2015) Genetic engineering strategies for abiotic stress tolerance in plants. Plant Biol Biotechnol 2:579–609CrossRefGoogle Scholar
  72. Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23:1233–1236PubMedPubMedCentralCrossRefGoogle Scholar
  73. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Dulay GP (2010) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29:143PubMedCrossRefGoogle Scholar
  74. Minkenberg B, Xie K, Yang Y (2016) Discovery of rice essential genes by characterizing a CRISPR-edited mutation of closely related rice MAP kinasegenes. Plant J 89:636–648CrossRefGoogle Scholar
  75. Mishra R, Joshi RK, Zhao K (2018) Genome editing in rice: recent advances, challenges, and future implications. Front Plant Sci 9Google Scholar
  76. Mishra AK (2014) Climate change and challenges of water and food security. Int J Sustain Built Environ 3:153–165CrossRefGoogle Scholar
  77. Moonmoon S, Islam MT (2017) Effect of drought stress at different growth stages on yield and yield components of six rice (Oryza sativa L.) genotypes. Fundam Appl Agric 2:285–289CrossRefGoogle Scholar
  78. Muler AL, Oliveira RS, Lambers H, Veneklaas EJ (2014) Does cluster-root activity benefit nutrient uptake and growth of co-existing species? Oecologia (Berl) 174:23–31CrossRefGoogle Scholar
  79. Müller M, Munné-Bosch S (2015) Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol 169:32–41PubMedPubMedCentralCrossRefGoogle Scholar
  80. Mushtaq M, Bhat JA, Mir ZA, Sakina A, Ali S, Singh AK, Tyagi A, Salgotra RK, Dar AA, Bhat R (2018) CRISPR/Cas approach: a new way of looking at plant–abiotic interactions. J Plant Physiol 224–225:156–162PubMedCrossRefPubMedCentralGoogle Scholar
  81. Nemudryi AA, Valetdinova KR, Medvedev SP, Zakian SM (2014) TALEN and CRISPR/Cas Genome Editing Systems: tools of discovery. Acta Nat 6:19–40CrossRefGoogle Scholar
  82. Nezhadahmadi A, Hossain Prodhan Z, Faruq G (2013) Drought tolerance in wheat. Sci World J 610721:1–12CrossRefGoogle Scholar
  83. Osakabe K, Osakabe Y, Toki S (2010) Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc Natl Acad Sci U S A 107:12034–12039PubMedPubMedCentralCrossRefGoogle Scholar
  84. Osakabe Y, Watanabe T, Sugano SS, Ueta R, Ishihara R, Shinozaki K, Osakabe K (2016) Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci Rep 6:26685PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017) Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci 8:1–13PubMedPubMedCentralGoogle Scholar
  86. Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22(6):4056–4075CrossRefGoogle Scholar
  87. Petolino JF (2015) Genome editing in plants via designed zinc finger nucleases. In Vitro Cell Dev Biol 51:1–8CrossRefGoogle Scholar
  88. Podevin N, Davies HV, Hartung F, Nogue F, Casacuberta JM (2012) Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding. Trends Biotechnol 1063:1–9Google Scholar
  89. Qi Y, Li X, Zhang Y, Starker CG, Baltes NJ (2013) Targeted deletion and inversion of tandemly arrayed genes in Arabidopsis thaliana using zinc finger nucleases. G3 (Bethesda) 3(10):1707–1715PubMedCentralCrossRefGoogle Scholar
  90. Rai AC, Singh M, Shah K (2013) Engineering drought tolerant tomato plants over-expressing BcZAT12 gene encoding a C2H2 zinc finger transcription factor. Phytochemistry 85:44–50PubMedCrossRefGoogle Scholar
  91. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181PubMedCrossRefPubMedCentralGoogle Scholar
  92. Rath D, Amlinger L, Rath A, Lundgren M (2015) The CRISPR-Cas immune system: biology, mechanisms and applications. Biochimie (Paris) 117:119e–128eCrossRefGoogle Scholar
  93. Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571PubMedPubMedCentralCrossRefGoogle Scholar
  94. Salehi-Lisar SY, Bakhshayeshan-Agdam H (2016) Drought stress in plants: causes, consequences, and tolerance. In: Hossain M, Wani S, Bhattacharjee S, Burritt D, Tran LS (eds) Drought stress tolerance in plants, vol 1. Springer, Cham, pp 1–16Google Scholar
  95. Salehi-lisar SY, Motafakkerazad R, Hossain MM, Rahman IMM (2012) Water stress in plants: causes, effects and responses. InTech, CroatiaGoogle Scholar
  96. Selmar D, Kleinwachter M (2013) Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products. Plant Cell Physiol 54:817–826PubMedCrossRefGoogle Scholar
  97. Semiz G, Blande JD, Heijari J, Işık K, Niinemets Ü, Holopainen JK (2012) Manipulation of VOC emissions with methyl jasmonate and carrageenan in the evergreen conifer Pinus sylvestris and evergreen broadleaf Quercus ilex. Plant Biol 14:57–65PubMedCrossRefGoogle Scholar
  98. Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Dumat C (2016) Heavy metal stress and crop productivity. In: Hakeem KR (ed) Production and global environmental issues. Springer International, Cham, pp 1–25Google Scholar
  99. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688PubMedCrossRefGoogle Scholar
  100. Shan Q, Wang Y, Li J, Gao C (2014) Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc 9:2395–2410PubMedCrossRefGoogle Scholar
  101. Shanmugavadivel PS, Prakash C, Mithra SVA (2019) Molecular approaches for dissecting and improving drought and heat tolerance in rice. Adv Rice Res Abiotic Stress Tolerance 2019:839–867CrossRefGoogle Scholar
  102. Shen C, Que Z, Xia Y, Tang N, Li D, He R, Cao M (2017a) Knock out of the Annexin Gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. J Plant Biotechnol 60:539–547Google Scholar
  103. Shen JB, Lv B, Luo LQ, He JM, Mao CJ, Xi DD, Ming F (2017b) The NAC-type transcription factor OsNAC2 regulates ABA-dependent genes and abiotic stress tolerance in rice. Sci Rep 7:40641PubMedPubMedCentralCrossRefGoogle Scholar
  104. Shi J, Habben J, Archibald RL, Drummond BJ, Chamberlin MA, Williams RW, Lafitte HR et al (2015) Overexpression of ARGOS genes modifies plant sensitivity to ethylene, leading to improved drought tolerance in both Arabidopsis and maize. Plant Physiol 169:266–282PubMedPubMedCentralCrossRefGoogle Scholar
  105. Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216PubMedCrossRefGoogle Scholar
  106. Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441PubMedCrossRefGoogle Scholar
  107. Singh S, Prasad S, Yadav V, Kumar A, Jaiswal B, Kumar A, Khan NA, Dwivedi DK (2018) Effect of drought stress on yield and yield components of rice (Oryza sativa L.) genotypes. Int J Curr Microbiol Appl Sci 7:2752–2759CrossRefGoogle Scholar
  108. Stephens J, Barakate A (2017) Gene editing technologies – ZFNs, TALENs, and CRISPR/Cas9. In: Thomas B, Murray BG, Murphyp JB (eds) Encyclopedia of applied plant sciences, 2nd edn. Academic, Cambridge, MA, pp 157–161CrossRefGoogle Scholar
  109. Tamás MJ, Sharma SK, Ibstedt S, Jacobson T, Christen P (2014) Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomol Ther 4:252–267Google Scholar
  110. Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, He H, Wang W, Zeng X et al (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7:14438PubMedPubMedCentralCrossRefGoogle Scholar
  111. Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML (2009) High frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445PubMedPubMedCentralCrossRefGoogle Scholar
  112. Tzfira T, Weinthal D, Marton I, Zeevi V, Zuker A, Vainstein A (2012) Genome modifications in plant cells by custom made restriction enzymes. Plant Biotechnol J 10:373–389PubMedCrossRefGoogle Scholar
  113. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD (2010) Genome editing with engineered zinc finger nucleases. Nat Rev Genet 11:636–646PubMedCrossRefGoogle Scholar
  114. Waltz E (2018) With a free pass, CRISPR-edited plants reach market in record time. Nat Biotechnol 36:6–7PubMedCrossRefGoogle Scholar
  115. Wang C, Lu W, He X, Wang F, Zhou Y, Guo X (2016a) The cotton mitogen-activated protein kinase 3 functions in drought tolerance by regulating stomatal responses and root growth. Plant Cell Physiol 57:1629–1642PubMedCrossRefGoogle Scholar
  116. Wang W, Qin Q, Sun F, Wang Y, Xu D, Li Z (2016b) Genome-wide differences in DNA methylation changes in two contrasting rice genotypes in response to drought conditions. Front Plant Sci 7:1675PubMedPubMedCentralGoogle Scholar
  117. Wang L, Chen L, Li R, Zhao R, Yang M, Sheng J, Shen L (2017) Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J Agric Food Chem 65:8674–8682PubMedCrossRefGoogle Scholar
  118. Wei Y, Jin J, Jiang S, Ning S, Liu L (2018) Quantitative response of soybean development and yield to drought stress during different growth stages in the Huaibei Plain, China. Agronomy 8:1–16Google Scholar
  119. Xie K, Yang Y (2013) RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant 6:1975–1983PubMedCrossRefGoogle Scholar
  120. Xu ZY, Kim SY, Hyeon DY, Kim DH, Dong T, Park Y, Jin JB, Joo SH, Kim SK, Hong JC, Hwang D, Hwang I (2013) The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25:4708–4724PubMedPubMedCentralCrossRefGoogle Scholar
  121. Xu R, Li H, Qin R, Wang L, Li L, Wei P, Yang J (2014) Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice 7:5PubMedPubMedCentralCrossRefGoogle Scholar
  122. Xu H, Xiao T, Chen CH, Li W, Meyer CA, Wu Q (2015) Sequence determinants of improved CRISPR sgRNA design. Genome Res 25:1147–1157PubMedPubMedCentralCrossRefGoogle Scholar
  123. Xu R, Yang Y, Qin R, Li H, Qiu C, Li L, Wei P, Yang J (2016) Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J Genet Genomics 43:529–532PubMedCrossRefGoogle Scholar
  124. Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci U S A 103:10503–10508PubMedPubMedCentralCrossRefGoogle Scholar
  125. Ynet N, Yilancioglu K (2018) A CRISPR/Cas9 model of sunflower (Helianthus annuus L.) resistance for biotic and abiotic stresses. New Biotechnol 44:68–164Google Scholar
  126. Zaman QU, Li C, Cheng H, Hu Q (2018) Genome editing opens a new era of genetic improvement in polyploid crops. Crop J 7:141–150CrossRefGoogle Scholar
  127. Zhang F, Voytas DF (2011) Targeted mutagenesis in Arabidopsis using zinc finger nucleases. Methods Mol Biol 701:167–177PubMedCrossRefGoogle Scholar
  128. Zhang F, Maeder ML, Unger-Wallace E, Hoshawm JP, Reyon D, Christian M, Joung JK (2010) High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci U S A 107:12028–12033PubMedPubMedCentralCrossRefGoogle Scholar
  129. Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z (2014) TheCRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 12:797–807PubMedCrossRefGoogle Scholar
  130. Zhang H, Li D, Zhou Z, Zahoor R, Chen B, Meng Y (2017) Soil water and salt affect cotton (Gossypium hirsutum L.) photosynthesis, yield and fiber quality in coastal saline soil. Agric Water Manag 187:112–121CrossRefGoogle Scholar
  131. Zhang J, Zhang S, Cheng M, Jiang H, Zhang X, Peng C, Lu X, Zhang M, Jin J (2018a) Effect of drought on agronomic traits of rice and wheat: a meta-analysis. Int J Environ Res Public Health 15:1–14Google Scholar
  132. Zhang Y, Massel K, Godwin LD, Gao C (2018b) Application and potential of genome editing in crop improvement. Genome Biol 19:210PubMedPubMedCentralCrossRefGoogle Scholar
  133. Zhao Y, Zhang C, Liu W, Gao W, Liu C, Song G (2016) An alternative strategy for targeted gene replacement in plants using a dual-sgRNA/Cas9design. Sci Rep 6:23890PubMedPubMedCentralCrossRefGoogle Scholar
  134. Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X (2017) CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci 8:1598PubMedPubMedCentralCrossRefGoogle Scholar
  135. da Cruz RP et al (2013) Avoiding damage and achieving cold tolerance in rice plants. Food Energy Security 2(2):96–119CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Giridara Kumar Surabhi
    • 1
  • Bijayalaxmi Badajena
    • 1
  • Santosh Kumar Sahoo
    • 1
  1. 1.Plant Molecular Biology and ‘OMICS’ LaboratoryRegional Plant Resource CentreBhubaneswarIndia

Personalised recommendations