Gene targeting and editing in crop plants: a new era of precision opportunities

Molecular Breeding

Volumn 35, Issue 1, 2015, Pages 1-15

  Rinaldo, Amy R ^a   Ayliffe, Michael ^a  

^a CSIRO   (Australia)

Author keywords

CRISPR; Homologous; NHEJ; Nuclease; Recombination; TALEN

Indexed keywords

CROPS; CULTIVATION; PLANTS (BOTANY); TRANSCRIPTION;

CRISPR; CROP IMPROVEMENT; CROP PLANTS; FOOD DEMAND; GENE TARGETING; HOMOLOGOUS; NHEJ; NUCLEASE; RECOMBINATION; TALEN;

MOLECULES;

EID: 84921900348     PISSN: 13803743     EISSN: 15729788     Source Type: Journal    
DOI: 10.1007/s11032-015-0210-z     Document Type: Review

References (137)

1. Ainley WM, Sastry-Dent L, Welter ME, Murray MG, Zeitler B, Amora R, Corbin R, Miles RR, Arnold NL, Strange TL, Simpson MA, Cao Z, Carroll C, Pawelczak KS, Blue R, West K, Rowland LM, Perkins D, Samuel P, Dewes CM, Shen L, Sriram S, Evand SL, Rebar EJ, Zhang L, Gregory PD, Urnov FD, Webb SR, Petolino JF (2013) Trait stacking via targeted genome editing. Plant Biotechnol J 11:1126–1134
2. Akbudak MA, More AB, Nandy S, Srivastava V (2010) Dosage-dependent gene expression from direct repeat locus in rice developed by site-specific gene integration. Mol Biotechnol 45:15–23
3. Albert H, Dale EC, Lee E, Ow DW (1995) Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7:649–659
4. Arnould S, Delenda C, Grizot S, Desseaux C, Paques F, Silva GH, Smith J (2011) The I-CreI meganuclease and its engineered derivatives: applications from cell modification to gene therapy. Protein Eng Des Sel 24:27–31
5. Baszczynski CL, Gordon-Kamm WJ, Lyznik LA, Peterson DJ, Zhao ZY (2003) Site-specific recombinases and their uses for targeted gene manipulation in plant systems. In: Stewart CN Jr (ed) Transgenic plants: current innovations and future trends. Horizon, Wymondham, pp 157–178
6. Beetham PR, Kipp PB, Sawycky XL, Arntzen CJ, May GD (1999) A tool for functional plant genomics: chimeric RNA/DNA oligonucleotides cause in vivo gene-specific mutations. Proc Natl Acad Sci USA 96:8774–8778
7. Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39–49
8. Bibikova M, Golic M, Golic KG, Carroll D (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300:764
9. 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 326:1509–1512
10. Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13:394–401
11. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705
12. Cai CQ, Doyon Y, Ainley WH et al (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol 69:699–1709
13. Cermak T, Doyle EL, 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:e82
14. Chan SH, Stoddard BL, Xu SY (2011) Natural and engineered nicking endonucleases—from cleavage mechanism to engineering of strand-specificity. Nucleic Acids Res 239:1–18
15. Chawla R, Ariza-Nieto M, Wilson AJ, Moore SK, Srivastava V (2006) Transgene expression produced by biolistic-mediated, site-specific gene integration is consistently inherited by the subsequent generations. Plant Biotechnol J 4:209–218
16. Choi S, Begum D, Koshinsky H, Ow DW, Wing RA (2000) A new approach for the identification and cloning of genes: the pBACwich system using Cre/lox-site specific recombination. Nucleic Acids Res 28:e19
17. 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. Genet 186:757–761
18. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jian W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using the CRISPR/Cas systems. Sci 339:819–823
19. Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C, Baltes NJ, Reyon D, Dalborg EJ, Goodwin MJ, Coffman AP, Dobbs D, Joung JK, Voytas DF, Stupar RM (2011) Targeted mutagenesis of duplicated genes in soybean with zinc finger nucleases. Plant Physiol 156:466–473
20. D’Halluin K, Vandderstraeten C, Stals E, Cornelissen M, Ruiter R (2008) Homologous recombination: a basis for targeted genome optimisation in crop species such as maize. Plant Biotechnol J 6:93–102
21. Day CD, Lee E, Kobayashi J, Holappa LD, Albert H, Ow DW (2000) Transgene integration into the same chromosomal location can produce alleles that are differentially silenced. Genes Dev 14:2869–2880
22. de Pater S, Neuteboom LW, Pinas JE, Hooykaas PJ, van der Zaal BJ (2009) ZFN-induced mutagenesis and gene-targeting in Arabidopsis through agrobacterium-mediated floral dip transformation. Plant Biotechnol J 7:821–835
23. de Pater S, Pinas JE, Hooykaas PJJ, van der Zaal BJ (2013) ZFN-mediated gene targeting of the Arabidopsis protoporhyrinogen oxidase gene through Agrobacterium-mediated floral dip transformation. Plant Biotechnol J 11:510–515
24. DeFrancesco L (2011) Move over ZFNs. Nat Biotechnol 29:681–684
25. Dhalluin K, Vanderstraeten C, Van Hulle J, Rosolowska J, Van Den Brande I, Pennewaert A, Dhont K, Bossut M, Jantz D, Ruiter R, Broadvest J (2013) Targeted molecular trait stacking in cotton through targeted double-strand break induction. Plant Biotechnol J 11:933–941
26. Djukanovic V, Smith J, Lowe K, Yang M, Gao H, Jones S, Nicholson MG, West A, Lape J, Bidney D, Falco SC, Jantz D, Lyznik LA (2013) Male-sterile plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J 76:888–899
27. Dong C, Beetham P, Vincent K, Sharp P (2006) Oligonucleotide-directed gene repair in wheat using a transient plasmid gene repair assay system. Plant Cell Rep 25:457–465
28. Fauser F, Schiml S, Puchta H (2014) Both CRISPR/Cas-based nuclease and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J 79:348–359
29. Feng Z, Zhang B, Ding W, Liu X, Yang D-L, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu J-K (2013) Efficient genome editing in plants using a CSRIPR/Cas system. Cell Res 23:1229–1232
30. Fladung M, Becker D (2010) Targeted integration and removal of transgenes in hybrid aspen (Populus termula L. × P. tremuloides Michx.) using site-specific recombination systems. Plant Biol 12:334–340
31. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD (2013) High frequency off-target mutagenesis induced CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:8
32. Gaj T, Gerbach CA, Barbas CF III (2013) ZFN, TALEN and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405
33. Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D, Lyznik LA (2010) Heritable targeted mutagenesis in maize using designed endonucleases. Plant J 61:176–187
34. Gasser CS, Fraley RT (1989) Genetically engineering plants for crop improvement. Science 244:1293–1299
35. Gupta M, DeKelver RC, Palta A, Clifford C, Gopalan S, Miller JC, Novak S, Desloover D, Gachotte D, Connell J, Flook J, Patterson T, Robbins K, Rebar EJ, Gregory PD, Urnov FD, Petolino JF (2012) Transcriptional activation of Brassica napus B-ketoacyl-ACP synthase II with an engineered zinc finger protein transcription factor. Plant Biotechnol J10:783–791
36. Gupta A, Hall VL, Kok FO, Shin M, McNulty JC, Lawson ND, Wolfe SA (2014) Targeted chromosomal deletions and inversions in zebrafish. Genome Res 23:1008–1017
37. Gurushidze M, Henesel G, Hiekel S, Schedel S, Valkov V, Kumlehn J (2014) True-breeding targeted gene knock-out in barley using designer TALE-nuclease in haploid cells. PLoS. doi:10.1371/journal.pone.0092046
38. Hannin M, Volrath S, Bogucki A, Briker M, Ward E, Paszkowski J (2001) Gene targeting in Arabidopsis. Plant J 28:671–677
39. Hartung F, Schiemann J (2014) Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J 78:742–752
40. Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF, Zhang F (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J. doi:10.1111/pbi.12201
41. Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170
42. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31:827–832
43. Iida S, Terada R (2005) Modification of endogenous natural genes by gene targeting in rice and other higher plants. Plant Mol Biol 59:205–219
44. Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE 9:e93806
45. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRIPSR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. doi:10.1093/nar/gkt780
46. Jiang W, Yang B, Weeks DP (2014) Efficient CRISPR/Ca9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS ONE 9:e99225
47. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Sci 337:816–821
48. Johnson RA, Gurevich V, Levy AA (2013) A rapid assay to quantify the cleavage efficiency of custom-designed nucleases in planta. Plant Mol Biol 82:207–221
49. Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55
50. Kerbach S, Lorz H, Becker D (2005) Site specific recombination in Zea mays. Theor Appl Genet 111:1608–1616
51. Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA 93:1156–1160
52. Klug A (2005) Towards therapeutic applications of engineered zinc finger proteins. FEBS Lett 579:892–894
53. Kochevenko A, Willmitzer L (2003) Chimeric RNA/DNA oligonucleotide-based site-specific modification of the tobacco acetolactate synthase gene. Plant Physiol 132:174–184
54. Kuzma J, Kokotovich A (2011) Renegotiating GM crop regulation. EMBO Reps 12:883–888
55. Lee HJ, Kim E, Kim J-S (2010) Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res 20:81–89
56. Li Z, Xing A, Moon BP, McCardell RP, Mills K, Falco SC (2009) Site-specific integration of transgene cassettes in soybean via recombinase-mediated DNA cassette exchange. Plant Physiol 151:1087–1095
57. Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B (2011) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39:359–372
58. Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392
59. Li J-F, 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 31:688–691
60. Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genomics 41:63–68
61. Lloyd A, Plasier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci USA 102:2232–2237
62. Louwerse JD, van Lier MCM, van der Steen DM, de Vlaam CMT, Hooykaas PJJ, Vergunst AC (2007) Stable recombinase-mediated cassette exchange in Arabidopsis using Agrobacterium tumefaciens. Plant Physiol 145:1282–1293
63. Lozano-Juste J, Cutler SR (2014) Plant genome engineering in full bloom. Trends Plant Sci. doi:10.1016/j.tplants.2014.02.014
64. Lusser M, Davies HV (2013) Comparative regulatory approaches for groups of new plant breeding techniques. New Biotechnol 30:437–4456
65. Maeder ML, Linder SJ, Cascio VM, Fu Y, Ho QH, Joung KJ (2013) CRISPR RNA-guided activation of endogenous human genes. Nat Methods 10:977–979
66. 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 USA 108:2623–2628
67. Mahfouz MM, Li L, Piatek M, Fang X, Mansour H, Bangarusamy DK, Zhu JK (2012) Targeted transcriptional repression using chimeric TALE-SRDX repressor protein. Plant Mol Biol 78:311–321
68. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Sci 339:823–826
69. Mani M, Smith J, Kandavelou K, Berg JM, Chandrasegaran S (2005) Binding of two zinc finger nuclease monomers to two specific sites is required for effective double-strand DNA cleavage. Biochem Biophys Res Commun 334:1191–1197
70. Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu J-K (2013) Application of the CRIPSR-Cas system for efficient genome engineering in plants. Mol Plant 6:2008–2011
71. Marra MC, Piggott NE, Goodwin BK (2010) The anticipated value of SmartStax™ for US corn growers. AgBioForum 13:1–12
72. Marton I, Zuker A, Shklarman E, Zeevi V, Tovkach A, Roffe S, Ovadis M, Tzfira T, Vanstein A (2010) Non-transgenic genome modification in plant cells. Plant Physiol 154:1079–1087
73. McConnell-Smith A, Takeuchi R, Pellenz S, Davis L, Maizels N, Monnat RJ, Stoddard BL (2009) Generation of a nicking enzyme that stimulates site-specific gene conversion from the I-Anil LAGLIDADG homing endonuclease. Proc Natl Acad Sci 106:5099–5104
74. Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL et al (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25:778–785
75. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, Dulay GP, Hua KL, Ankoudinova I, Cost GJ, Urnov FD, Zhang HS, Holmes MC, Zhang L, Gregory PD, Rebar EJ (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29:143–148
76. Morbitzer R, Romer P, Boch J, Lahaye T (2010) Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. Proc Natl Acad Sci USA 107:21617–21622
77. Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Sci 326:1501
78. Nandy S, Srivastava V (2011) Site-specific gene integration in rice genome mediated by the FLP–FRT recombination system. Plant Biotechnol J 9:713–721
79. Nanto K, Ebinuma H (2008) Marker-free site-specific integration plants. Transgenic Res 17:337–344
80. Nanto K, Yamada-Watanabe K, Ebinuma H (2005) Agrobacterium-mediated RMCE approach for gene replacement. Plant Biotechnol J 3:203–214
81. Nanto K, Sato K, Katayama Y, Ebinuma H (2009) Expression of a transgene exchanged by the recombinase mediated cassette (RMCE) method in plants. Plant Cell Rep 28:777–785
82. 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 31:691–693
83. Okuzaki A, Toriyama K (2004) Chimeric RNA/DNA oligonucelotide-directed gene targeting in rice. Plant Cell Rep 22:509–512
84. Osakabe K, Osakabe Y, Toki S (2010) Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc Natl Acad Sci USA 107:12034–12039
85. Ow D (2007) GM maize from site-specific recombination technology, what next? Curr Opin Biotechnol 18:115–120
86. Paques F, Duchateau P (2007) Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gene Therapy 7:49–66
87. Parry MAJ, Madgwick PJ, Bayon C, Tearall K, Hernandez-Lopez A, Baudo M, Rakszegi M, Hamada W, Al-Yassin A, Ouabbou H, Labhilili M, Phillips AL (2009) Mutation discovery for crop improvement. J Exp Bot 60:2817–2825
88. Perez-Pinera P, Kocak DD, Vockley CM, Adler AF, Kabadi AM, Polstein LR, Thakore PI, Glass KA, Ousterout DG, Leong KW, Guilak F, Crawford GE, Reddy TE, Gersbach CA (2013) RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods 10:973–976
89. Petolino JF, Worden A, Curlee K, Connell J, Strange Moynahan TL, Larsen C, Russell S (2010) Zinc finger nuclease-mediated transgene deletion. Plant Mol Biol 73:617–628
90. Porteus MH, Carroll D (2005) Gene targeting using zinc finger nucleases. Nat Biotechnol 23:967–973
91. Pruett-Miller SM, Reading DW, Porter SN, Porteus MH (2009) Attenuation of zinc finger nuclease toxicity by small-molecule regulation of protein levels. PLoS Genet 5(2):e1000376. doi:10.1371/journal.pgen.1000376
92. Puchta H (2002) Gene replacement by homologous recombination in plants. Plant Mol Biol 48:173–182
93. Puchta H (2005) The repair of double stranded DNA breaks in plants. J Exp Bot 56:1–14
94. Puchta H, Dujon B, Hohn B (1996) Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc Natl Acad Sci USA 93:5055–5060
95. Qi Y, Li X, Zhang Y, Starker CG, Baltes NJ, Zhang F, Sander JD, Reyon D, Joung JK, Voytas DF (2013a) Targeted deletion and inversion of tandemly arrayed genes in Arabidopsis thaliana using zinc finger nucleases. G3 3:1707–1715
96. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weismann JS, Arkin AP, Lim WA (2013b) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183
97. Que Q, Chilton M-D, de Fontes CM, He C, Nuccio M, Zhu T, Wu Y, Chen JS, Shi L (2010) Trait stacking in transgenic crops. GM Crop 1:220–229
98. Ramalingam S, Kandavelou K, Rajenderan R, Chandrasegaran S (2011) Creating designed zinc-finger nucleases with minimal cytotoxicity. J Mol Biol 405:630–641
99. Sanchez JP, Ullman C, Moore M, Choo Y, Chua NH (2006) Regulation of Arabidopsis thaliana 4-coumarate: coenzyme-A ligase-1 expression by artificial zinc finger chimeras. Plant Biotechnol J 4:103–114
100. Schornack S, Moscou MJ, Ward ER, Horvath DM (2013) Engineering plant disease resistance based on TAL effectors. Ann Rev Phytopathol 51:383–406
101. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root D, Doench JG, Zhang F (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Sci 343:84–87
102. Shan Q, Wang Y, Chen K, Liang Z, Li J, Zhang Y, Zhang K, Liu J, Voytas DF, Zheng X, Zhang Y, Gao C (2013a) Rapid and efficient gene modifications in rice and Brachypodium using TALENs. Mol Plant. doi:10.1093/mp/ss162
103. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu J-L, Gao C (2013b) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688
104. Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu YY, Katibah GE, Zhifang G, McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregory PD, Urnov FD (2009) Precise genome modification in the crop species Zea mays using zinc finger nucleases. Nat 259:442–445
105. Small I (2007) RNAi for revealing and engineering plant gene functions. Curr Opin Biotechnol 18:148–153
106. Srivastava V (2013) Site specific gene integration in rice. In: Rice protocols, methods in molecular biology. vol. 958, Humana Press, Pennsylvania, USA, pp 83–93
107. Srivastava V, Ow DW (2002) Biolistic site-specific integration in rice. Mol Breeding 8:345–350
108. Srivastava V, Anderson OD, Ow DW (1999) Single-copy transgenic wheat generated through the resolution of complex integration patterns. Proc Natl Acad Sci USA 96:11117–11121
109. Srivastava V, Ariza-Nieto M, Wilson AJ (2004) Cre-mediated site-specific gene integration for consistent transgene expression in rice. Plant Biotechnol J 2:169–179
110. Stege JT, Guan X, Ho T, Beachy RN, Barbas CF III (2002) Controlling gene expression in plants using zinc finger transcription factor. Plant J 32:1077–1086
111. Straub A, LaHaye T (2013) Zinc fingers, TAL effectors or Cas9-based DNA binding proteins: What’s best for targeting desired genome loci? Mol Plant 6:1384–1387
112. Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ et al (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25:786–793
113. Tester M, Langridge P (2010) Breeding Technologies to increase crop production in a changing world. Sci 327:818–822
114. Thomas Scott C (2005) The zinc finger nuclease monopoly. Nat Biotechnol 23:915–918
115. Tovkach A, Zeevi V, Tzfira T (2009) A toolbox and procedural notes for characterising novel zinc finger nucleases for genome editing in plant cells. Plant J 57:747–757
116. 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. Nat 459:442–445
117. Tzfira T, Frankmen L, Vaidya M, Citovsky V (2003) Site-specific integration of Agrobacterium tumefacians T-DNA via double-stranded intermediates. Plant Physiol 133:1011–1023
118. Tzfira T, Weinthal D, Marton I, Zeevi V, Zuker A, Vainstein A (2012) Genome modification in plant cells by custom-made restriction enzymes. Plant Biotechnol J 10:373–389
119. Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3 3:2233–2238
120. van Nierop GP, de Vries AA, Holkers M, Vrijsen KR, Goncalves MA (2009) Stimulation of homology-directed gene targeting at an endogenous human locus by a nicking endonuclease. Nucleic Acids Res 37:5725–5736
121. Vergunst AC, Hooykaas PJJ (1998) Cre/lox-mediated site specific integration of Agrobacterium T-DNA in Arabidopsis thaliana by transient expression of Cre. Plant Mol Biol 38:393–406
122. Vergunst AC, Jansen LET, Hooykaas PJJ (1998) Site-specific integration of Agrobacterium T-DNA in Arabidosis thaliana mediated by Cre recombinase. Nucleic Acids Res 26:2729–2734
123. Waltz E (2012) Tiptoeing around transgenics. Nat Biotechnol 30:215–217
124. Wang Y, Yau Y-Y, Perkins-Balding D, Thomson JG (2011) Recombinase technology: applications and possibilities. Plant Cell Rep 30:267–285
125. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu J-L (2014) Simultaneous editing of three homoealleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol. doi:10.1038/nbt.2969
126. Weinthal DM, Taylor RA, Tzfira T (2013) Nonhomologous end joining-mediated gene replacement in plant cells. Plant Physiol 162:390–400
127. Wendt T, Holm PB, Starker CG, Christian M, Voytas DF, Brinch-Pedersen H, Holme IB (2013) TAL effector nuclease induced mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol 83:279–285
128. Wright DA, Townsend JA, Winfrey RJ, Irwin PA, Rajagopal J, Lonosky PM, Hall BD, Jondle MD, Voytas DF (2005) High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J 44:693–705
129. Xie K, Yang Y (2013) RNA-guided genome editing plants using a CRISPR-Cas system. Mol Plant 6:1975–1983
130. Xie K, Zhang J, Yang Y (2014) Genome-wide prediction of highly specific guide RNA spacers for CRISPR-Cas9-mediated genome editing in model plants and major crops. Mol Plant 7:923–926
131. 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 7:5
132. Yang M, Djukanovic V, Stagg J, Lenderts B, Bidney D, Falco SC, Lyznik LA (2009) Targeted mutagenesis in the progeny of maize transgenics. Plant Mol Biol 70:669–779
133. Zhang F (2014) CRISPR-Cas systems and methods for altering expression of gene products. US Patent No. 8,697,359
134. Zhang F, Maeder ML, Unger-Wallace E, Hoshaw JP, Reyon D, Christian M, Li X, Pierick CJ, Dobbs D, Peterson T, Joung KJ, Voytas DF (2010) High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci USA 107:12028–12033
135. Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG, Bogdanove AJ, Voytas DF (2013) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol 161:20–27
136. Zhang H, Zhang J, Wei O, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N, Zhu J-K (2014) The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J12:797–807
137. Zhu T, Peterson DJ, Tagliani L, Clair G, Baszczynski CL, Bowen B (1999) Targeted manipulation of maize genes in vivo using chimeric RNA/DNA oligonucleotides. Proc Natl Acad Sci USA 96:8768–8773