Advertisement

Applications of Genome Engineering/Editing Tools in Plants

  • Chakravarthi Mohan
  • Priscila Yumi Tanaka Shibao
  • Flavio Henrique SilvaEmail author
Chapter
First Online:

Abstract

The advent of engineered nucleases such as zinc finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs) and clustered regularly interspaced short palindromic repeats/Cas9 (CRISPR/Cas9) has revolutionized targeted genome editing. CRISPR/Cas9-based editing system has surpassed its predecessors owing to its simplicity, versatility and efficiency. Therefore, it has become the most promising genome-editing tool in recent years which is evident through the increasing number of publications and in several organisms. This technology has profound applications in areas of functional genomics and crop improvement. Recent studies have proved that multiplex genome editing is possible not only in model crops but in major crops too. Unlike transgenic crops which yield random insertions of target genes, genome-editing tools enable targeted gene insertion at a specified locus (knock-in), deletion of desired genes from the genome (knockout) and also genome modification (replacement). In this context, this chapter describes in detail the various applications of genome-editing technologies in crop improvement and highlights how this tool has outwitted transgenic technology in recent times.

Keywords

Base editing CRISPR/Cas9 Genome editing Knock-in Knockout TALENs ZFNs 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

CM and PYTS gratefully acknowledge the São Paulo Research Foundation (FAPESP) for the postdoctoral research grant (Proc. 2015/10855-9) and doctoral grant (Proc. No. 2017/16118-1), respectively. FHS is a recipient of a Research Productivity Scholarship from the National Council for Research and Development (CNPq #311745/2013-0).

References

  1. Alagoz Y, Gurkok T, Zhang B, Unver T (2016) Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci Rep 6:309–310CrossRefGoogle Scholar
  2. Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz MM (2015) CRISPR/Cas9-mediated viral interference in plants. Genome Biol 16:238–249PubMedPubMedCentralCrossRefGoogle Scholar
  3. Anand P, Schug A, Wenzel W (2013) Structure based design of protein linkers for zinc finger nuclease. FEBS Lett 587(19):3231–3235PubMedCrossRefGoogle Scholar
  4. Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN, Bisaro DM, Voytas DF (2015) Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat Plants 1:15145CrossRefGoogle Scholar
  5. Barrangou R, Horvath P (2012) CRISPR: new horizons in phage resistance and strain identification. Annu Rev Food Sci Technol 3:143–162PubMedCrossRefGoogle Scholar
  6. Bartel DP (2009) MicroRNAs: Target recognition and regulatory functions. Cell 136(2):215–233PubMedPubMedCentralCrossRefGoogle Scholar
  7. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326(5959):1509–1152PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bortesi L, Fischer R (2014) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33(1):41–52PubMedCrossRefGoogle Scholar
  9. Butler NM, Atkins PA, Voytas DF, Douches DS (2015) Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) using the CRISPR/Cas System. PLoS One 10:e0144591PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cai C, Doyon Y, Ainley W, Miller J, DeKelver R et al (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol 69:699–709PubMedCrossRefGoogle Scholar
  11. Cathomen T, Keith Joung J (2008) Zinc-finger Nucleases: The Next Generation Emerges. Mol Ther 16(7):1200–1207PubMedCrossRefGoogle Scholar
  12. Cermak T, Doyle EC, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39(12):e82PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M et al (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153PubMedPubMedCentralCrossRefGoogle Scholar
  14. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA Double-Strand Breaks with TAL Effector Nucleases. Genetics 186(2):757–761PubMedPubMedCentralCrossRefGoogle Scholar
  15. Christian M, Qi Y, Zhang Y, Voytas DF (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL Effector Nucleases (TALENs). G3 (Bethesda) 3:1697–1705CrossRefGoogle Scholar
  16. 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 (2016) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169–176PubMedCrossRefGoogle Scholar
  17. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819–823PubMedPubMedCentralCrossRefGoogle Scholar
  18. Courtier-Orgogoz V, Morizot B, Boete C (2017) Agricultural pest control with CRISPR based gene drive: time for public debate: Should we use gene drive for pest control? EMBO Rep 18:878–880CrossRefGoogle Scholar
  19. Dreissig S, Schiml S, Schindele P, Weiss O, Rutten T, Schubert V, Gladilin E, Mette MF, Puchta H, Houben A (2017) Live-cell CRISPR imaging in plants reveals dynamic telomere movements. Plant J 91(4):565–573PubMedPubMedCentralCrossRefGoogle Scholar
  20. Du H, Zeng X, Zhao M, Cui X, Wang Q, Yang H, Cheng H, Yu D (2016) Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol 217:90–97PubMedCrossRefPubMedCentralGoogle Scholar
  21. Engler C, Kandzia R, Marillonnet S (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS One 3(11):e3647PubMedPubMedCentralCrossRefGoogle Scholar
  22. Esvelt KM, Smidler AL, Catteruccia F, Church GM (2014) Concerning RNA-guided gene drives for the alteration of wild populations. elife 3:e03401PubMedPubMedCentralCrossRefGoogle Scholar
  23. Gantz VM, Jasinskiene N, Tatarenkova O, Fazekas A, Macias VM, Bier E, James AA (2015) Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc Natl Acad Sci U S A 112:6736–6743CrossRefGoogle Scholar
  24. Georges F, Ray H (2017) Genome editing of crops: a renewed opportunity for food security. In: (Ed.). GM Crops Food 8(1):1–12PubMedPubMedCentralCrossRefGoogle Scholar
  25. Gilbert LA, Horlbeck MA, Adamson B (2014) Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159(3):647–661PubMedPubMedCentralCrossRefGoogle Scholar
  26. Greisman HA, Pabo CO (1997) A general strategy for selecting high-affinity zinc finger proteins for diverse DNA target sites. Science 275(5300):657–661PubMedCrossRefGoogle Scholar
  27. Hahn F, Mantegazza O, Greiner A, Hegemann P, Eisenhut M, Weber APM (2017) An efficient visual screen for CRISPR/Cas9 activity in Arabidopsis thaliana. Front Plant Sci 8:39PubMedPubMedCentralCrossRefGoogle Scholar
  28. Hanania U, Ariel T, Tekoah Y, Fux L, Sheva M, Gubbay Y, Weiss M, Oz D, Azulay Y, Turbovski A, Forster Y, Shaaltiel Y (2017) Establishment of a tobacco BY2 cell line devoid of plant-specific xylose and fucose as a platform for the production of biotherapeutic proteins. Plant Biotechnol J 15:1120–1129PubMedPubMedCentralCrossRefGoogle Scholar
  29. Hilton IB, D’Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE et al (2015) Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 33:510–517PubMedPubMedCentralCrossRefGoogle Scholar
  30. Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327(5962):167–170CrossRefPubMedGoogle Scholar
  31. Hu Y, Zhang J, Jia H, Sosso D, Li T, Frommer WB, Yang B, White FF, Wang N, Jones JB (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci U S A 111:521–529CrossRefGoogle Scholar
  32. Huang S, Weigel D, Beachy RN, Li J (2016) A proposed regulatory framework for genome-edited crops. Nat Genet 48(2):109–111PubMedCrossRefGoogle Scholar
  33. Hurt JA, Thibodeau SA, Hirsh AS, Pabo CO, Joung JK (2003) Highly specific zinc finger proteins obtained by directed domain shuffling and cell-based selection. Proc Natl Acad Sci U S A 14;100(21):12271–12276CrossRefGoogle Scholar
  34. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:16PubMedPubMedCentralCrossRefGoogle Scholar
  35. Jacobs TB, Zhang N, Patel D, Martin GB (2017) Generation of a collection of mutant tomato lines using pooled CRISPR libraries. Plant Physiol 174:2033–2037CrossRefGoogle Scholar
  36. Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9(4):e93806PubMedPubMedCentralCrossRefGoogle Scholar
  37. Jia H, Zhang Y, Orbovic V, Xu J, White F, Jones J, Wang N (2017) Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15:817–823PubMedPubMedCentralCrossRefGoogle Scholar
  38. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucl Acids Res 41:e188PubMedCrossRefGoogle Scholar
  39. Jiang WZ, Henry IM, Lynagh PG, Comai L, Cahoon EB, Weeks DP (2017) Significant enhancement of fatty acid composition in seeds of the allohexaploid, Camelina sativa, using CRISPR/Cas9 gene editing. Plant Biotechnol J 15:648–657PubMedPubMedCentralCrossRefGoogle Scholar
  40. Karvelis T, Gasiunas G, Siksnys V (2013) Programmable DNA cleavage in vitro by Cas9. Biochem Soc Trans 41(6):1401–1406PubMedCrossRefGoogle Scholar
  41. Kaur N, Alok A, Shivani KN, Pandey P, Awasthi P, Tiwari S (2018) CRISPR/Cas9-mediated efficient editing in phytoene desaturase (PDS) demonstrates precise manipulation in banana cv. Rasthali genome. Func Int Genomics 18(1):89–99CrossRefGoogle Scholar
  42. Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 93(3):1156–1160PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kim H, Kim S-T, Ryu J, Kang B-C, Kim J-S, Kim S-G (2017) CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat Commun 8:14406PubMedPubMedCentralCrossRefGoogle Scholar
  44. Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 33:420–424CrossRefGoogle Scholar
  45. Larson MH, Gilbert LA, Wang X, Lim WA, Weis JS (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat Protoc 8:2180–2196PubMedPubMedCentralCrossRefGoogle Scholar
  46. 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
  47. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, 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
  48. Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP, Huang L et al (2015) Cas9-guide RNA directed genome editing in soybean. Plant Physiol 169(2):960–970PubMedPubMedCentralCrossRefGoogle Scholar
  49. 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 2:16139PubMedCrossRefGoogle Scholar
  50. Li X, Zhou W, Ren Y, Tian X, Lv T, Wang Z, Fang J, Chu C, Yang J, Bu Q (2017) High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing. J Genet Genomics 44(3):175–178PubMedCrossRefGoogle Scholar
  51. Li C, Chen C, Chen H, Wang S, Chen X, Cui Y (2018a) Verification of DNA motifs in Arabidopsis using CRISPR/Cas9-mediated mutagenesis. Plant Biotechnol J 8:1446–1451CrossRefGoogle Scholar
  52. Li R, Fu D, Zhu B, Luo Y, Zhu H (2018b) CRISPR/Cas9-mediated mutagenesis of lncRNA1459 alters tomato fruit ripening. Plant J. (in press)Google Scholar
  53. Li R, Li R, Li X, Fu D, Zhu B, Tian H, Luo Y, Zhu H (2018c) Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol J 16:415–427PubMedCrossRefGoogle Scholar
  54. Liang Z, Chen K, Li T, Yi Zhang Y, Wang Y, Zhao Q, Liu J, Zhang H, Liu C, Ran Y, Gao C (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8:14261PubMedPubMedCentralCrossRefGoogle Scholar
  55. Liu C, Zhang L, Liu H, Cheng K (2017) Delivery strategies of the CRISPR-Cas9 gene-editing system for therapeutic applications. J Control Release 266:17–26PubMedPubMedCentralCrossRefGoogle Scholar
  56. Liu P, Chen M, Liu Y, Qi LS, Ding S (2018) CRISPR-based chromatin remodeling of the endogenous Oct4 or Sox2 locus enables reprogramming to pluripotency cell. Stem Cell 22(2):252–261Google Scholar
  57. Lu Y, Zhu JK (2017) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 System. Mol Plant 10:523–525PubMedCrossRefPubMedCentralGoogle Scholar
  58. Ma X, Liu YG (2016) CRISPR/Cas9-based multiplex genome editing in monocot and dicot plants. Curr Protoc Mol Biol 115:31.6.1–31.6.21CrossRefGoogle Scholar
  59. Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, Xie Y, Shen R, Chen S, Wang Z, Chen Y, Guo J, Chen L, Zhao X, Dong Z, Liu YG (2015) A Robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8(8):1274–1284PubMedCrossRefGoogle Scholar
  60. Ma H, Tu LC, Naseri A, Huisman M, Zhang S, Grunwald D, Pederson T (2016a) Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISP Rainbow. Nat Biotechnol 34(5):528–531PubMedPubMedCentralCrossRefGoogle Scholar
  61. Ma X, Zhu Q, Chen Y, Liu YG (2016b) CRISPR/Cas9 platforms for genome editing in plants: developments and applications. Mol Plant 9(7):961–974PubMedCrossRefGoogle Scholar
  62. Mahfouz MM, Li L, Piatek M, Fang X, Mansour H, Bangarusamy DK, Zhu J-K (2012) Targeted transcriptional repression using a chimeric TALE-SRDX repressor protein. Plant Mol Biol 78(3):311–321PubMedCrossRefGoogle Scholar
  63. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339(6121):823–826PubMedPubMedCentralCrossRefGoogle Scholar
  64. Malnoy M, Viola R, Jung MH, Koo OJ, Kim S, Kim JS et al (2016) DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci 7:1904PubMedPubMedCentralCrossRefGoogle Scholar
  65. Mani M, Kandavelou K, Dy FJ, Durai S, Chandrasegaran S (2005) Design, engineering, and characterization of zinc finger nucleases. Biochem Biophys Res Commun 335(2):447–457PubMedCrossRefGoogle Scholar
  66. Mazier M, Flamain F, Nicolaï M, Sarnette V, Caranta C (2011) Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against Potyviruses in Tomato. PLoS One 6(12):e29595PubMedPubMedCentralCrossRefGoogle Scholar
  67. Meng X, Yu H, Zhang Y, Zhuang F, Song X, Gao S, Gao C, Li J (2017) Construction of a genome-wide mutant library in rice using CRISPR/Cas9. Mol Plant 10(9):1238–1241PubMedCrossRefGoogle Scholar
  68. Moore M, Klug A, Choo Y (2001) Improved DNA binding specificity from polyzinc finger peptides by using strings of two-finger units. Proc Natl Acad Sci U S A 98(4):1437–1441PubMedPubMedCentralCrossRefGoogle Scholar
  69. Morgan SL, Mariano NC, Bermudez A, Arruda NL, Wu F, Luo Y, Shankar G, Jia L, Chen H, Hu JF, Hoffman AR, Huang CC, Pitteri SJ, Wang KC (2017) Manipulation of nuclear architecture through CRISPR-mediated chromosomal looping. Nat Commun 8:15993PubMedPubMedCentralCrossRefGoogle Scholar
  70. Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326:1501PubMedPubMedCentralCrossRefGoogle Scholar
  71. Nakajima I, Ban Y, Azuma A, Onoue N, Moriguchi T, Yamamoto T et al (2017) CRISPR/Cas9-mediated targeted mutagenesis in grape. PLoS One 12(5):e0177966PubMedPubMedCentralCrossRefGoogle Scholar
  72. Nekrasov V, Staskawicz B, Weigel D, Jones JDG, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31:691–693PubMedCrossRefGoogle Scholar
  73. Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S (2017) Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep 7:482PubMedPubMedCentralCrossRefGoogle Scholar
  74. Nishitani C, Hirai N, Komori S, Wada M, Okada K, Osakabe K, Yamamoto T, Osakabe Y (2016) Efficient genome editing in apple using a CRISPR/Cas9 system. Sci Rep 6:31481PubMedPubMedCentralCrossRefGoogle Scholar
  75. Odipio J, Alicai T, Ingelbrecht I, Nusinow DA, Bart R, Taylor NJ (2017) Efficient CRISPR/Cas9 genome editing of phytoene desaturase in cassava. Front Plant Sci 8:1780PubMedPubMedCentralCrossRefGoogle Scholar
  76. Ordon J, Gantner J, Kemna J, Schwalgun L, Reschke M, Streubel J, Boch J, Stuttmann J (2017) Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit. Plant J 89(1):155–168PubMedCrossRefGoogle Scholar
  77. 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
  78. Pabo C, Peisach E, Grant R (2001) Design and selection of novel Cys2 His2 zinc finger proteins. Annu Rev Biochem 70:313–340PubMedCrossRefGoogle Scholar
  79. Pan C, Ye L, Qin L, Liu X, He Y, Wang J, Chen L et al (2016) CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6:24765PubMedPubMedCentralCrossRefGoogle Scholar
  80. Peng A, Chen S, Lei T, Xu L, He Y, Wu L et al (2017) Engineering canker resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J 15(12):1509–1519PubMedPubMedCentralCrossRefGoogle Scholar
  81. Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S (2015) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13:578–589PubMedCrossRefGoogle Scholar
  82. Porteus MH, Carroll D (2005) Gene targeting using zinc finger nucleases. Nat Biotechnol 23(8):967–973PubMedCrossRefGoogle Scholar
  83. Pyott DE, Sheehan E, Molnar A (2016) Engineering of CRISPR/ Cas9- mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol Plant Path 17:1276–1288CrossRefGoogle Scholar
  84. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP et al (2013) Repurposing CRISPR as an RNA-guided platform for sequence specific control of gene expression. Cell 152:1173–1183PubMedPubMedCentralCrossRefGoogle Scholar
  85. Ren B, Yan F, Kuang Y, Li N, Zhang D, Zhou X, Lin H, Zhou H (2018) Improved base editor for efficiently inducing genetic variations in rice with CRISPR/Cas9-guided hyperactive hAID mutant. Mol Plant doi 11:623.  https://doi.org/10.1016/j.molp.2018.01.005 CrossRefGoogle Scholar
  86. Rodríguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell 171(2):470–480PubMedCrossRefGoogle Scholar
  87. Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32(4):347–355PubMedPubMedCentralCrossRefGoogle Scholar
  88. Schiml S, Fauser F, Puchta H (2014) The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J 80:1139–1150PubMedCrossRefGoogle Scholar
  89. Scholze H, Boch J (2010) TAL effector-DNA specificity. Virulence 1(5):428–432PubMedCrossRefGoogle Scholar
  90. Scott MJ, Gould F, Lorenzen MD, Grubbs N, Edwards OR, O’Brochta DA (2017) Agricultural production: assessment of the potential use of Cas9-mediated gene drive systems for agricultural pest control. J Respon Innov 5:98–120CrossRefGoogle Scholar
  91. Shalem O, Sanjana NE, Zhang F (2015) High-throughput functional genomics using CRISPR-Cas9. Nat Rev Genet 16:299–311PubMedPubMedCentralCrossRefGoogle Scholar
  92. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31(8):686–688PubMedCrossRefGoogle Scholar
  93. Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800PubMedCrossRefPubMedCentralGoogle Scholar
  94. Shen C, Que Z, Xia Y, Tang N, Li D, He R, Cao M (2017) Knock out of the annexin gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. J Plant Biol 60(6):539–547CrossRefGoogle Scholar
  95. Shi J, Habben JE, 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
  96. 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
  97. Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K (2017) Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol 35:441PubMedCrossRefGoogle Scholar
  98. Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC et al (2009) Precise genome modification in the crop Zea mays using zinc finger nucleases. Nature 459:437–441PubMedCrossRefGoogle Scholar
  99. Sonoda E, Hochegger H, Saberi A, Taniguchi Y, Takeda S (2006) Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst) 5(9–10):1021–1029CrossRefGoogle Scholar
  100. Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X et al (2016) Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol Plant 9:628–631PubMedCrossRefPubMedCentralGoogle Scholar
  101. Sun Y, Jiao G, Liu Z, Zhang X, Li J, Guo X, Du W, Du J, Francis F, Zhao Y et al (2017) Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci 8:298PubMedPubMedCentralGoogle Scholar
  102. Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM (2015) Targeted mutagenesis, precise gene editing and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 169:931–945PubMedPubMedCentralCrossRefGoogle Scholar
  103. Svitashev S, Schwartz C, Lenderts B, Young JK, Cigan AM (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat Commun 7:13274PubMedPubMedCentralCrossRefGoogle Scholar
  104. Thompson DB, Aboulhouda S, Hysolli E, Smith CJ, Wang S, Castanon O, Church GM (2017) The future of multiplexed eukaryotic genome engineering. ACS Chem Biol 13(2):313–325PubMedPubMedCentralCrossRefGoogle Scholar
  105. Tian S, Jiang L, Gao Q, Zhang J, Zong M, Zhang H, Ren Y, Guo S, Gong G, Liu F, Xu Y (2017) Efficient CRISPR/Cas9-based gene knockout in watermelon. Plant Cell Rep 36(3):399–406PubMedCrossRefGoogle Scholar
  106. Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445PubMedPubMedCentralCrossRefGoogle Scholar
  107. Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-Guided Genome Editing for Target Gene Mutations in Wheat. G3: Genes, Genomes. Genetics 3(12):2233–2238Google Scholar
  109. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153(4):910–918PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951PubMedCrossRefGoogle Scholar
  111. Wang S, Zhang S, Wang W, Xiong X, Meng F, Cui X (2015) Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Rep 34(9):1473–1476PubMedCrossRefGoogle Scholar
  112. Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu YG, Zhao K (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One 11:e0154027PubMedPubMedCentralCrossRefGoogle Scholar
  113. Weinthal D, Tovkach A, Zeevi V, Tzfira T (2010) Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci 15(6):308–321PubMedCrossRefGoogle Scholar
  114. Weinthal DM, Taylor RA, Tzfira T (2013) Non homologous end joining-mediated gene replacement in plant cells. Plant Physiol 162:390–400PubMedPubMedCentralCrossRefGoogle Scholar
  115. Woo JW, Kim J, Kwon SI, Corvalán C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33(11):1162–1164CrossRefGoogle Scholar
  116. Xie K, Minkenberg B, Yang Y (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci U S A 112(11):3570–3575PubMedPubMedCentralCrossRefGoogle Scholar
  117. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327PubMedPubMedCentralCrossRefGoogle Scholar
  118. Xu R, Yang Y, Qin R, Hao L, 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
  119. Zaidi SS, Mansoor S (2017) Viral vectors for plant genome engineering. Front Plant Sci 11(8):539Google Scholar
  120. Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG, Bogdanove AJ, Voytas DF (2013) TALENs enable efficient plant genome engineering. Plant Physiol 161(1):20–27PubMedCrossRefGoogle Scholar
  121. Zhang Z, Mao Y, Ha S, Liu W, Botella JR, Zhu JK (2015) A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep 35(7):1519–1533PubMedPubMedCentralCrossRefGoogle Scholar
  122. Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K et al (2016a) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617PubMedPubMedCentralCrossRefGoogle Scholar
  123. Zhang B, Yang X, Yang C, Li M, Guo Y (2016b) Exploiting the CRISPR/Cas9 System for targeted genome mutagenesis in Petunia. Sci Rep 6:20315PubMedPubMedCentralCrossRefGoogle Scholar
  124. Zhao Y, Zhang C, Liu W, Gao W, Liu C, Song G, Li WX et al (2016a) An alternative strategy for targeted gene replacement in plants using a dual-sgRNA/Cas9 design. Sci Rep 6:23890PubMedPubMedCentralCrossRefGoogle Scholar
  125. Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu JK (2016b) Mutational evidence for the critical role of CBF genes in cold acclimation in Arabidopsis. Plant Physiol 171:2744–2759PubMedPubMedCentralGoogle Scholar
  126. Zhou H, Liu B, Weeks DP, Spalding MH, Yang B (2014) Large chromosomal deletions heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res 42:10903–10914PubMedPubMedCentralCrossRefGoogle Scholar
  127. Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X, Tang A, Zheng X, Zhang T, Qi Y, Zhang Y (2017) CRISPR-Cas9 based genome editing reveals new insights into MicroRNA function and regulation in rice. Front Plant Sci 8:1598PubMedPubMedCentralCrossRefGoogle Scholar
  128. Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9- cytidine deaminase fusion. Nat Biotechnol 35:438–440PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Chakravarthi Mohan
    • 1
  • Priscila Yumi Tanaka Shibao
    • 1
  • Flavio Henrique Silva
    • 1
    Email author
  1. 1.Molecular Biology Laboratory, Department of Genetics and EvolutionFederal University of São CarlosSão CarlosBrazil

Personalised recommendations

Cite chapter

Buy options