Plant genome editing with TALEN and CRISPR

Cell and Bioscience

Volumn 7, Issue 1, 2017, Pages

  Malzahn, Aimee ^a   Lowder, Levi ^b   Qi, Yiping ^a,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Cas9; Cpf1; CRISPR; HDR; NHEJ; Plant genome editing; TALEN

Indexed keywords

EID: 85018575555     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/s13578-017-0148-4     Document Type: Review

References (231)

1. Ray DK, Mueller ND, West PC, Foley JA. Yield trends are insufficient to double global crop production by 2050. PLoS ONE. 2013;8(6):e66428.
2. Wolt JD, Wang K, Yang B. The Regulatory status of genome-edited crops. Plant Biotechnol J. 2016;14(2):510-8.
3. Kanaar R, Hoeijmakers JH, van Gent DC. Molecular mechanisms of DNA double strand break repair. Trends Cell Biol. 1998;8(12):483-9.
4. Steinert J, Schiml S, Puchta H. Homology-based double-strand break-induced genome engineering in plants. Plant Cell Rep. 2016;35(7):1429-38.
5. Hartlerode AJ, Scully R. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem J. 2009;423(2):157-68.
6. Pastwa E, Blasiak J. Non-homologous DNA end joining. Acta Biochim Pol. 2003;50(4):891-908.
7. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol. 2014;32(9):947-51.
8. Puchta H. The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot. 2005;56(409):1-14.
9. Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature. 2009;459(7245):442-5.
10. Paques F, Duchateau P. Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gene Ther. 2007;7(1):49-66.
11. Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D, et al. Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J. 2010;61(1):176-87.
12. Kim YG, Cha J, Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA. 1996;93(3):1156-60.
13. Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J, Kim YG, Chandrasegaran S. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol. 2001;21(1):289-97.
14. Beerli RR, Barbas CF 3rd. Engineering polydactyl zinc-finger transcription factors. Nat Biotechnol. 2002;20(2):135-41.
15. Segal DJ, Beerli RR, Blancafort P, Dreier B, Effertz K, Huber A, Koksch B, Lund CV, Magnenat L, Valente D, et al. Evaluation of a modular strategy for the construction of novel polydactyl zinc finger DNA-binding proteins. Biochemistry. 2003;42(7):2137-48.
16. Ramirez CL, Foley JE, Wright DA, Muller-Lerch F, Rahman SH, Cornu TI, Winfrey RJ, Sander JD, Fu F, Townsend JA, et al. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat Methods. 2008;5(5):374-5.
17. Cornu TI, Thibodeau-Beganny S, Guhl E, Alwin S, Eichtinger M, Joung JK, Cathomen T. DNA-binding specificity is a major determinant of the activity and toxicity of zinc-finger nucleases. Mol Ther. 2008;16(2):352-8.
18. Doyon Y, McCammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, Amora R, Hocking TD, Zhang L, Rebar EJ, et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol. 2008;26(6):702-8.
19. Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM, Eichtinger M, Jiang T, Foley JE, Winfrey RJ, Townsend JA, et al. Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell. 2008;31(2):294-301.
20. Sander JD, Dahlborg EJ, Goodwin MJ, Cade L, Zhang F, Cifuentes D, Curtin SJ, Blackburn JS, Thibodeau-Beganny S, Qi Y, et al. Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat Methods. 2011;8(1):67-9.
21. Zhang F, Maeder ML, Unger-Wallace E, Hoshaw JP, Reyon D, Christian M, Li X, Pierick CJ, Dobbs D, Peterson T, et al. High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci USA. 2010;107(26):12028-33.
22. Qi Y, Zhang Y, Zhang F, Baller JA, Cleland SC, Ryu Y, Starker CG, Voytas DF. Increasing frequencies of site-specific mutagenesis and gene targeting in Arabidopsis by manipulating DNA repair pathways. Genome Res. 2013;23(3):547-54.
23. Qi Y, Zhang Y, Baller JA, Voytas DF. Histone H2AX and the small RNA pathway modulate both non-homologous end-joining and homologous recombination in plants. Mutat Res. 2016;783:9-14.
24. Moscou MJ, Bogdanove AJ. A simple cipher governs DNA recognition by TAL effectors. Science. 2009;326(5959):1501.
25. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U. Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009;326(5959):1509-12.
26. Boch J, Bonas U. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol. 2010;48:419-36.
27. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics. 2010;186(2):757-61.
28. Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B. TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res. 2011;39(1):359-72.
29. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol. 2011;29(2):143-8.
30. Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu JK. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci USA. 2011;108(6):2623-8.
31. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 2011;39(12):e82.
32. Li T, Huang S, Zhao X, Wright DA, Carpenter S, Spalding MH, Weeks DP, Yang B. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res. 2011;39(14):6315-25.
33. Morbitzer R, Elsaesser J, Hausner J, Lahaye T. Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res. 2011;39(13):5790-9.
34. Wiedenheft B, Sternberg SH, Doudna JA. RNA-guided genetic silencing systems in bacteria and archaea. Nature. 2012;482(7385):331-8.
35. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315(5819):1709-12.
36. Marraffini LA, Sontheimer EJ. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science. 2008;322(5909):1843-5.
37. Makarova KS, Zhang F, Koonin EV. SnapShot: Class 2 CRISPR-Cas systems. Cell. 2017;168(1-2):328.
38. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816-21.
39. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819-23.
40. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823-6.
41. Paul JW 3rd, Qi Y. CRISPR/Cas9 for plant genome editing: accomplishments, problems and prospects. Plant Cell Rep. 2016;35(7):1417-27.
42. Lowder L, Malzahn A, Qi Y. Rapid evolution of manifold CRISPR systems for plant genome editing. Front Plant Sci. 2016;7:1683.
43. Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG, Bogdanove AJ, Voytas DF. Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol. 2013;161(1):20-7.
44. Christian M, Qi Y, Zhang Y, Voytas DF. Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 (Bethesda). 2013;3(10):1697-705.
45. Lor VS, Starker CG, Voytas DF, Weiss D, Olszewski NE. Targeted mutagenesis of the tomato PROCERA gene using TALENs. Plant Physiol. 2014;166:1288-91.
46. Shan Q, Wang Y, Chen K, Liang Z, Li J, Zhang Y, Zhang K, Liu J, Voytas DF, Zheng X, et al. Rapid and efficient gene modification in rice and Brachypodium using TALENs. Mol Plant. 2013;6(4):1365-8.
47. Zhang H, Gou F, Zhang J, Liu W, Li Q, Mao Y, Botella JR, Zhu JK. TALEN-mediated targeted mutagenesis produces a large variety of heritable mutations in rice. Plant Biotechnol J. 2016;14(1):186-94.
48. Li T, Liu B, Spalding MH, Weeks DP, Yang B. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol. 2012;30(5):390-2.
49. Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, et al. Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J. 2014;12(7):934-40.
50. Shan Q, Zhang Y, Chen K, Zhang K, Gao C. Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J. 2015;13(6):791-800.
51. Ma L, Zhu F, Li Z, Zhang J, Li X, Dong J, Wang T. TALEN-based mutagenesis of lipoxygenase LOX3 enhances the storage tolerance of rice (Oryza sativa) seeds. PLoS ONE. 2015;10(12):e0143877.
52. Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, Daulhac A, et al. Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J. 2016;14(1):169-76.
53. Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, Lin Q, Luo W, Wu G, Li H. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front Plant Sci. 2016;7:377.
54. Li Q, Zhang D, Chen M, Liang W, Wei J, Qi Y, Yuan Z. Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. J Genet Genom. 2016;43:415-9.
55. Zhou H, He M, Li J, Chen L, Huang Z, Zheng S, Zhu L, Ni E, Jiang D, Zhao B, et al. Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci Rep. 2016;6:37395.
56. Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu YG, Zhao K. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE. 2016;11(4):e0154027.
57. Pyott DE, Sheehan E, Molnar A. Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol Plant Pathol. 2016;17:1276-88.
58. Baltes N. Conferring resistance to geminiviruses with the CRISPR-Cas prokaryotic immune system. Nat Plants. 2015;1:15145.
59. Gutierrez C. Geminivirus DNA replication. Cell Mol Life Sci. 1999;56(3-4):313-29.
60. Ali Z, Abul-faraj A, Li L, Ghosh N, Piatek M, Mahjoub A, Aouida M, Piatek A, Baltes NJ, Voytas DF, et al. Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant. 2015;8(8):1288-91.
61. Ji X, Zhang H, Zhang Y, Wang Y, Gao C. Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nat Plants. 2015;1:15144.
62. Zhang Y, Rajan R, Seifert HS, Mondragon A, Sontheimer EJ. DNase H activity of Neisseria meningitidis Cas9. Mol Cell. 2015;60(2):242-55.
63. Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu JK. Mutational evidence for the critical role of CBF genes in cold acclimation in Arabidopsis. Plant Physiol. 2016;171:2744-59.
64. Zhou X, Jacobs TB, Xue LJ, Harding SA, Tsai CJ. Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy. New Phytol. 2015;208(2):298-301.
65. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol. 2013;31(8):686-8.
66. Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu JL, Gao C. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun. 2016;7:12617.
67. Li C, Unver T, Zhang B. A high-efficiency CRISPR/Cas9 system for targeted mutagenesis in cotton (Gossypium hirsutum L.). Sci Rep. 2017;7:43902.
68. Chen X, Lu X, Shu N, Wang S, Wang J, Wang D, Guo L, Ye W. Targeted mutagenesis in cotton (Gossypium hirsutum L.) using the CRISPR/Cas9 system. Sci Rep. 2017;7:44304.
69. Morineau C, Bellec Y, Tellier F, Gissot L, Kelemen Z, Nogue F, Faure JD. Selective gene dosage by CRISPR-Cas9 genome editing in hexaploid Camelina sativa. Plant Biotechnol J. 2016. doi: 10.1111/pbi.12671.
70. Jiang WZ, Henry IM, Lynagh PG, Comai L, Cahoon EB, Weeks DP. Significant enhancement of fatty acid composition in seeds of the allohexaploid, Camelina sativa, using CRISPR/Cas9 gene editing. Plant Biotechnol J. 2016. doi: 10.1111/pbi.12663.
71. Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y. Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci USA. 2015;112(7):2275-80.
72. Tang F, Yang S, Liu J, Zhu H. Rj4, a gene controlling nodulation specificity in soybeans, encodes a thaumatin-like protein but not the one previously reported. Plant Physiol. 2016;170(1):26-32.
73. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D. Specific effects of microRNAs on the plant transcriptome. Dev Cell. 2005;8(4):517-27.
74. Liu X, Hao L, Li D, Zhu L, Hu S. Long non-coding RNAs and their biological roles in plants. Genom Proteom Bioinform. 2015;13(3):137-47.
75. Basak J, Nithin C. Targeting non-coding RNAs in plants with the CRISPR-Cas technology is a challenge yet worth accepting. Front Plant Sci. 1001;2015:6.
76. Zhou H, Liu B, Weeks DP, Spalding MH, Yang B. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res. 2014;42(17):10903-14.
77. Zhao Y, Zhang C, Liu W, Gao W, Liu C, Song G, Li WX, Mao L, Chen B, Xu Y, et al. An alternative strategy for targeted gene replacement in plants using a dual-sgRNA/Cas9 design. Sci Rep. 2016;6:23890.
78. Duan YB, Li J, Qin RY, Xu RF, Li H, Yang YC, Ma H, Li L, Wei PC, Yang JB. Identification of a regulatory element responsible for salt induction of rice OsRAV2 through ex situ and in situ promoter analysis. Plant Mol Biol. 2016;90(1-2):49-62.
79. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014;14:327.
80. Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant. 2015;8(8):1274-84.
81. Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X, Zheng X, Voytas DF, Hsieh TF, Zhang Y, Qi Y. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol. 2015;169:971-85.
82. Zhang Z, Mao Y, Ha S, Liu W, Botella JR, Zhu JK. A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep. 2016;35(7):1519-33.
83. Wang C, Shen L, Fu Y, Yan C, Wang K. A simple CRISPR/Cas9 system for multiplex genome editing in rice. J Genet Genom. 2015;42(12):703-6.
84. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154(6):1380-9.
85. Fauser F, Schiml S, Puchta H. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 2014;79(2):348-59.
86. Schiml S, Fauser F, Puchta H. 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. 2014;80(6):1139-50.
87. Mikami M, Toki S, Endo M. Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant Cell Physiol. 2016;57(5):1058-68.
88. Tang X, Zheng X, Qi Y, Zhang D, Cheng Y, Tang A, Voytas DF, Zhang Y. A single transcript CRISPR-Cas9 system for efficient genome editing in plants. Mol Plant. 2016;9(7):1088-91.
89. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ, Joung JK. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol. 2014;32(6):569-76.
90. Guilinger JP, Thompson DB, Liu DR. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol. 2014;32(6):577-82.
91. Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol. 2011;29(8):731-4.
92. Budhagatapalli N, Rutten T, Gurushidze M, Kumlehn J, Hensel G. Targeted modification of gene function exploiting homology-directed repair of TALEN-mediated double-strand breaks in barley. G3 (Bethesda). 2015;5(9):1857-63.
93. Li T, Liu B, Chen CY, Yang B. TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J Genet Genom. 2016;43(5):297-305.
94. Cermak T, Baltes NJ, Cegan R, Zhang Y, Voytas DF. High-frequency, precise modification of the tomato genome. Genome Biol. 2015;16(1):232.
95. Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF. DNA replicons for plant genome engineering. Plant Cell. 2014;26(1):151-63.
96. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol. 2013;31(8):688-91.
97. Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X, Du W, Zhao Y, Xia L. Engineering herbicide resistant rice plants through CRISPR/Cas9-mediated homologous recombination of the acetolactate synthase. Mol Plant. 2016;9(4):628-31.
98. Endo M, Mikami M, Toki S. Biallelic gene targeting in rice. Plant Physiol. 2016;170(2):667-77.
99. Wang M, Lu Y, Botella J, Mao Y, Hua K, Zhu JK. Gene Targeting by Homology-directed Repair in Rice using a Geminivirus-based CRISPR/Cas9 System. Mol Plant. 2017. doi: 10.1016/j.molp.2017.03.002.
100. Gil-Humanes J, Wang Y, Liang Z, Shan Q, Ozuna CV, Sanchez-Leon S, Baltes NJ, Starker C, Barro F, Gao C, et al. High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J. 2017;89(6):1251-62.
101. Fauser F, Roth N, Pacher M, Ilg G, Sanchez-Fernandez R, Biesgen C, Puchta H. In planta gene targeting. Proc Natl Acad Sci USA. 2012;109(19):7535-40.
102. Beerli RR, Segal DJ, Dreier B, Barbas CF 3rd. Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc Natl Acad Sci USA. 1998;95(25):14628-33.
103. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M. Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 2003;34(5):733-9.
104. Kay S, Hahn S, Marois E, Hause G, Bonas U. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science. 2007;318(5850):648-51.
105. Romer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science. 2007;318(5850):645-8.
106. Mahfouz MM, Li L, Piatek M, Fang X, Mansour H, Bangarusamy DK, Zhu JK. Targeted transcriptional repression using a chimeric TALE-SRDX repressor protein. Plant Mol Biol. 2012;78(3):311-21.
107. Lin S, Zhao Y, Zhu Y, Gosney M, Deng X, Wang X, Lin J. An effective and inducible system of TAL effector-mediated transcriptional repression in Arabidopsis. Mol Plant. 2016;9(11):1546-9.
108. Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S, Aouida M, Mahfouz MM. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J. 2015;13(4):578-89. doi: 10.1111/pbi.12284.
109. Valton J, Dupuy A, Daboussi F, Thomas S, Marechal A, Macmaster R, Melliand K, Juillerat A, Duchateau P. Overcoming transcription activator-like effector (TALE) DNA binding domain sensitivity to cytosine methylation. J Biol Chem. 2012;287(46):38427-32.
110. Esvelt KM, Mali P, Braff JL, Moosburner M, Yaung SJ, Church GM. Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods. 2013;10(11):1116-21.
111. Steinert J, Schiml S, Fauser F, Puchta H. Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus. Plant J. 2015;84(6):1295-305.
112. Kaya H, Mikami M, Endo A, Endo M, Toki S. Highly specific targeted mutagenesis in plants using Staphylococcus aureus Cas9. Sci Rep. 2016;6:26871.
113. Zhang HY, Wang XH, Dong L, Wang ZP, Liu B, Lv J, Xing HL, Han CY, Wang XC, Chen QJ. MISSA 2.0: an updated synthetic biology toolbox for assembly of orthogonal CRISPR/Cas systems. Sci Rep. 2017;7:41993.
114. Kaya H, Ishibashi K, Toki S. A split Staphylococcus aureus Cas9 as a compact genome editing tool in plants. Plant Cell Physiol. 2017. doi: 10.1093/pcp/pcx034.
115. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163(3):759-71.
116. Yin X, Biswal AK, Dionora J, Perdigon KM, Balahadia CP, Mazumdar S, Chater C, Lin HC, Coe RA, Kretzschmar T et al. CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant Cell Rep. 2017. doi: 10.1007/s00299-017-2118-z.
117. Xu R, Qin R, Li H, Li D, Li L, Wei P, Yang J. Generation of targeted mutant rice using a CRISPR-Cpf1 system. Plant Biotechnol J. 2016. doi: 10.1111/pbi.12669.
118. Endo A, Masafumi M, Kaya H, Toki S. Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Sci Rep. 2016;6:38169. doi: 10.1038/srep38169
119. Tang X, Lowder LG, Zhang T, Malzahn AA, Zheng X, Voytas DF, Zhong Z, Chen Y, Ren Q, Li Q, et al. A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants. 2017;3:17018.
120. Kim H, Kim ST, Ryu J, Kang BC, Kim JS, Kim SG. CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat Commun. 2017;8:14406. doi: 10.1038/ncomms14406.
121. Wang M, Mao Y, Lu Y, Tao X, Zhu JK. Multiplex gene editing in rice using the CRISPR-Cpf1 System. Mol Plant. 2017. doi: 10.1016/j.molp.2017.03.001.
122. Luo S, Li J, Stoddard TJ, Baltes NJ, Demorest ZL, Clasen BM, Coffman A, Retterath A, Mathis L, Voytas DF, et al. Non-transgenic plant genome editing using purified sequence-specific nucleases. Mol Plant. 2015;8(9):1425-7.
123. Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol. 2015;33(11):1162-4.
124. Liang Z, Chen K, Li T, Zhang Y, Wang Y, Zhao Q, Liu J, Zhang H, Liu C, Ran Y, et al. Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun. 2017;8:14261.
125. Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature. 2016;533(7603):420-4.
126. Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M, Tabata M, Mochizuki M, Miyabe A, Araki M, Hara KY, et al. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science. 2016;353(6305):8729.
127. Li J, Sun Y, Du J, Zhao Y, Xia L. Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol Plant. 2016;10(3):526-9.
128. Lu Y, Zhu JK. Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 System. Mol Plant. 2016;10(3):523-5.
129. Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C. Precise base editing in rice, wheat and maize with a Cas9- cytidine deaminase fusion. Nat Biotechnol. 2017. doi: 10.1038/nbt.3811.
130. Ren B, Yan F, Kuang Y, Li N, Zhang D, Lin H, Zhou H. A CRISPR/Cas9 toolkit for efficient targeted base editing to induce genetic variations in rice. Sci China Life Sci. 2017. doi: 10.1007/s11427-016-0406-x.
131. Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K et al. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol. 2017. doi: 10.1038/nbt.3833.
132. Chen Y, Wang Z, Ni H, Xu Y, Chen Q, Jiang L. CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. Sci China Life Sci. 2017. doi: 10.1007/s11427-017-9021-5.
133. Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho MJ, Scelonge C, Lenderts B, Chamberlin M, Cushatt J et al. Morphogenic regulators baby boom and wuschel improve monocot transformation. Plant Cell. 2016. doi: 10.1105/tpc.16.00124.
134. Forner J, Pfeiffer A, Langenecker T, Manavella PA, Lohmann JU. Germline-transmitted genome editing in Arabidopsis thaliana using TAL-effector-nucleases. PLoS ONE. 2015;10(3):e0121056.
135. Johnson RA, Gurevich V, Levy AA. A rapid assay to quantify the cleavage efficiency of custom-designed nucleases in planta. Plant Mol Biol. 2013;82(3):207-21.
136. Wendt T, Holm PB, Starker CG, Christian M, Voytas DF, Brinch-Pedersen H, Holme IB. TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol. 2013;83(3):279-85.
137. Gurushidze M, Hensel G, Hiekel S, Schedel S, Valkov V, Kumlehn J. True-breeding targeted gene knock-out in barley using designer TALE-nuclease in haploid cells. PLoS ONE. 2014;9(3):e92046.
138. Char SN, Unger-Wallace E, Frame B, Briggs SA, Main M, Spalding MH, Vollbrecht E, Wang K, Yang B. Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J. 2015;13(7):1002-10.
139. Liang Z, Zhang K, Chen K, Gao C. Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genom. 2014;41(2):63-8.
140. Li J, Stoddard TJ, Demorest ZL, Lavoie PO, Luo S, Clasen BM, Cedrone F, Ray EE, Coffman AP, Daulhac A, et al. Multiplexed, targeted gene editing in Nicotiana benthamiana for glyco-engineering and monoclonal antibody production. Plant Biotechnol J. 2016;14(2):533-42.
141. Nicolia A, Proux-Wera E, Ahman I, Onkokesung N, Andersson M, Andreasson E, Zhu LH. Targeted gene mutation in tetraploid potato through transient TALEN expression in protoplasts. J Biotechnol. 2015;204:17-24.
142. Butler NM, Baltes NJ, Voytas DF, Douches DS. Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases. Front Plant Sci. 1045;2016:7.
143. Wang M, Liu Y, Zhang C, Liu J, Liu X, Wang L, Wang W, Chen H, Wei C, Ye X, et al. Gene editing by co-transformation of TALEN and chimeric RNA/DNA oligonucleotides on the rice OsEPSPS gene and the inheritance of mutations. PLoS ONE. 2015;10(4):e0122755.
144. Blanvillain-Baufume S, Reschke M, Sole M, Auguy F, Doucoure H, Szurek B, Meynard D, Portefaix M, Cunnac S, Guiderdoni E et al. Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant Biotechnol J. 2017;15(3):306-17. doi: 10.1111/pbi.12613.
145. Nishizawa-Yokoi A, Cermak T, Hoshino T, Sugimoto K, Saika H, Mori A, Osakabe K, Hamada M, Katayose Y, Starker C, et al. A defect in DNA Ligase4 enhances the frequency of TALEN-mediated targeted mutagenesis in rice. Plant Physiol. 2016;170(2):653-66.
146. Demorest ZL, Coffman A, Baltes NJ, Stoddard TJ, Clasen BM, Luo S, Retterath A, Yabandith A, Gamo ME, Bissen J, et al. Direct stacking of sequence-specific nuclease-induced mutations to produce high oleic and low linolenic soybean oil. BMC Plant Biol. 2016;16(1):225.
147. Du H, Zeng X, Zhao M, Cui X, Wang Q, Yang H, Cheng H, Yu D. Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol. 2016;217:90-7.
148. Jung JH, Altpeter F. TALEN mediated targeted mutagenesis of the caffeic acid O-methyltransferase in highly polyploid sugarcane improves cell wall composition for production of bioethanol. Plant Mol Biol. 2016;92(1-2):131-42.
149. Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y, et al. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 2013;23(10):1229-32.
150. Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA. 2014;111(12):4632-7.
151. Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu JK. Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant. 2013;6(6):2008-11.
152. Mao Y, Zhang Z, Feng Z, Wei P, Zhang H, Botella JR, Zhu JK. Development of germ-line-specific CRISPR-Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant Biotechnol J. 2015;14(2):519-32.
153. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 2013;41(20):e188.
154. Jiang W, Yang B, Weeks DP. Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS ONE. 2014;9(6):e99225.
155. Hyun Y, Kim J, Cho SW, Choi Y, Kim JS, Coupland G. Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles. Planta. 2015;241(1):271-84.
156. Johnson RA, Gurevich V, Filler S, Samach A, Levy AA. Comparative assessments of CRISPR-Cas nucleases' cleavage efficiency in planta. Plant Mol Biol. 2015;87(1-2):143-56.
157. Wang ZP, Xing HL, Dong L, Zhang HY, Han CY, Wang XC, Chen QJ. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 2015;16:144.
158. Yan L, Wei S, Wu Y, Hu R, Li H, Yang W, Xie Q. High-efficiency genome editing in Arabidopsis using YAO promoter-driven CRISPR/Cas9 system. Mol Plant. 2015;8(12):1820-3.
159. Kim H, Kim ST, Ryu J, Choi MK, Kweon J, Kang BC, Ahn HM, Bae S, Kim JS, Kim SG. A simple, flexible and high-throughput cloning system for plant genome editing via CRISPR-Cas system. J Integr Plant Biol. 2016;58:705-12.
160. Jia Y, Ding Y, Shi Y, Zhang X, Gong Z, Yang S. The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol. 2016;212(2):345-53.
161. Ordon J, Gantner J, Kemna J, Schwalgun L, Reschke M, Streubel J, Boch J, Stuttmann J. Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit. Plant J. 2017;89(1):155-68.
162. Li P, Li YJ, Zhang FJ, Zhang GZ, Jiang XY, Yu HM, Hou BK. The Arabidopsis UDP-glycosyltransferases UGT79B2 and 79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J. 2017;89(1):85-103.
163. Veillet F, Gaillard C, Coutos-Thevenot P, La Camera S. Targeting the AtCWIN1 Gene to explore the role of invertases in sucrose transport in roots and during Botrytis cinerea infection. Front Plant Sci. 1899;2016:7.
164. Ryder P, McHale M, Fort A, Spillane C. Generation of stable nulliplex autopolyploid lines of Arabidopsis thaliana using CRISPR/Cas9 genome editing. Plant Cell Rep. 2017. doi: 10.1007/s00299-017-2125-0.
165. Lawrenson T, Shorinola O, Stacey N, Li C, Ostergaard L, Patron N, Uauy C, Harwood W. Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol. 2015;16:258.
166. Baek K, Kim DH, Jeong J, Sim SJ, Melis A, Kim JS, Jin E, Bae S. DNA-free two-gene knockout in Chlamydomonas reinhardtii via CRISPR-Cas9 ribonucleoproteins. Sci Rep. 2016;6:30620.
167. Janga MR, Campbell LM, Rathore KS. CRISPR/Cas9-mediated targeted mutagenesis in upland cotton (Gossypium hirsutum L.). Plant Mol Biol. 2017. doi: 10.1007/s11103-017-0599-3.
168. Iaffaldano B, Zhang Y, Cornish K. CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection. Ind Crops Prod. 2016;89:356-62.
169. Sauer NJ, Narvaez-Vasquez J, Mozoruk J, Miller RB, Warburg ZJ, Woodward MJ, Mihiret YA, Lincoln TA, Segami RE, Sanders SL, et al. Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol. 2016;170(4):1917-28.
170. Ren C, Liu X, Zhang Z, Wang Y, Duan W, Li S, Liang Z. CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.). Sci Rep. 2016;6:32289.
171. Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I, Kohchi T. CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant Cell Physiol. 2014;55(3):475-81.
172. Wang L, Wang L, Tan Q, Fan Q, Zhu H, Hong Z, Zhang Z, Duanmu D. Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus using CRISPR-Cas9. Front Plant Sci. 2016;7:1333.
173. Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM. Targeted Mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol. 2015;169(2):931-45.
174. Zhu J, Song N, Sun S, Yang W, Zhao H, Song W, Lai J. Efficiency and inheritance of targeted mutagenesis in maize using CRISPR-Cas9. J Genet Genom. 2016;43(1):25-36.
175. Feng C, Yuan J, Wang R, Liu Y, Birchler JA, Han F. Efficient targeted genome modification in maize using CRISPR/Cas9 system. J Genet Genom. 2016;43(1):37-43.
176. Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J. 2017;15(2):207-16.
177. Char SN, Neelakandan AK, Nahampun H, Frame B, Main M, Spalding MH, Becraft PW, Meyers BC, Walbot V, Wang K et al. An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol J. 2017;15(2):257-68.
178. Collonnier C, Epert A, Mara K, Maclot F, Guyon-Debast A, Charlot F, White C, Schaefer DG, Nogue F. CRISPR-Cas9-mediated efficient directed mutagenesis and RAD51-dependent and RAD51-independent gene targeting in the moss Physcomitrella patens. Plant Biotechnol J. 2017;15(1):122-31.
179. Lopez-Obando M, Hoffmann B, Gery C, Guyon-Debast A, Teoule E, Rameau C, Bonhomme S, Nogue F. Simple and efficient targeting of multiple genes through CRISPR-Cas9 in Physcomitrella patens. G3 (Bethesda). 2016;6(11):3647-53. doi: 10.1534/g3.116.033266.
180. Wang Q, Lu Y, Xin Y, Wei L, Huang S, Xu J. Genome editing of model oleaginous microalgae Nannochloropsis spp. by CRISPR/Cas9. Plant J. 2016;88(6):1071-81.
181. Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol. 2013;31(8):691-3.
182. Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods. 2013;9(1):39.
183. Upadhyay SK, Kumar J, Alok A, Tuli R. RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda). 2013;3(12):2233-8.
184. Yin K, Han T, Liu G, Chen T, Wang Y, Yu AY, Liu Y. A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Sci Rep. 2015;5:14926. doi: 10.1038/srep14926.
185. Vazquez-Vilar M, Bernabe-Orts JM, Fernandez-Del-Carmen A, Ziarsolo P, Blanca J, Granell A, Orzaez D. A modular toolbox for gRNA-Cas9 genome engineering in plants based on the GoldenBraid standard. Plant Methods. 2016;12:10.
186. Gao J, Wang G, Ma S, Xie X, Wu X, Zhang X, Wu Y, Zhao P, Xia Q. CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol. 2015;87(1-2):99-110.
187. Mercx S, Tollet J, Magy B, Navarre C, Boutry M. Gene inactivation by CRISPR-Cas9 in Nicotiana tabacum BY-2 suspension cells. Front Plant Sci. 2016;7:40.
188. Zhang B, Yang X, Yang C, Li M, Guo Y. Exploiting the CRISPR/Cas9 system for targeted genome mutagenesis in petunia. Sci Rep. 2016;6:20315.
189. Subburaj S, Chung SJ, Lee C, Ryu SM, Kim DH, Kim JS, Bae S, Lee GJ. Site-directed mutagenesis in Petunia x hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep. 2016;35(7):1535-44.
190. Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K. Efficient CRISPR/Cas9-mediated targeted mutagenesis in populus in the first generation. Sci Rep. 2015;5:12217.
191. Tingting L, Di F, Lingyu R, Yuanzhong J, Rui L, Keming L. Highly efficient CRISPR/Cas9-mediated targeted mutagenesis of multiple genes in Populus. Yi Chuan. 2015;37(10):1044-52.
192. Wang S, Zhang S, Wang W, Xiong X, Meng F, Cui X. Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Rep. 2015;34(9):1473-6.
193. Butler NM, Atkins PA, Voytas DF, Douches DS. Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) using the CRISPR/Cas System. PLoS ONE. 2015;10(12):e0144591.
194. Andersson M, Turesson H, Nicolia A, Falt AS, Samuelsson M, Hofvander P. Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Rep. 2017;36(1):117-28. doi: 10.1007/s00299-016-2062-3.
195. Zhou X, Zha M, Huang J, Li L, Imran M, Zhang C. StMYB44 negatively regulates phosphate transport by suppressing expression of PHOSPHATE1 in potato. J Exp Bot. 2017. doi: 10.1093/jxb/erx026.
196. Xie K, Yang Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant. 2013;6(6):1975-83.
197. Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N, et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J. 2014;12(6):797-807.
198. Ma L, Zhang D, Miao Q, Yang J, Xuan Y, Hu Y. Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol. 2017. doi: 10.1093/pcp/pcx040.
199. Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, Wan J, Gu H, Qu LJ. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res. 2013;23(10):1233-6.
200. Xu R, Li H, Qin R, Wang L, Li L, Wei P, Yang J. Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice (NY). 2014;7(1):5.
201. Endo M, Mikami M, Toki S. Multigene knockout utilizing off-target mutations of the CRISPR/Cas9 system in rice. Plant Cell Physiol. 2015;56(1):41-7.
202. Xie K, Minkenberg B, Yang Y. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci USA. 2015;112(11):3570-5.
203. Xu RF, Li H, Qin RY, Li J, Qiu CH, Yang YC, Ma H, Li L, Wei PC, Yang JB. Generation of inheritable and "transgene clean" targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep. 2015;5:11491.
204. Mikami M, Toki S, Endo M. Parameters affecting frequency of CRISPR/Cas9 mediated targeted mutagenesis in rice. Plant Cell Rep. 2015;34(10):1807-15.
205. Mikami M, Toki S, Endo M. Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice. Plant Mol Biol. 2015;88(6):561-72.
206. Hu X, Wang C, Fu Y, Liu Q, Jiao X, Wang K. Expanding the range of CRISPR/Cas9 genome editing in rice. Mol Plant. 2016;9(6):943-5.
207. Zheng X, Yang S, Zhang D, Zhong Z, Tang X, Deng K, Zhou J, Qi Y, Zhang Y. Effective screen of CRISPR/Cas9-induced mutants in rice by single-strand conformation polymorphism. Plant Cell Rep. 2016;35:1545-54.
208. Osakabe Y, Watanabe T, Sugano SS, Ueta R, Ishihara R, Shinozaki K, Osakabe K. Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci Rep. 2016;6:26685.
209. Liu L, Zheng C, Kuang B, Wei L, Yan L, Wang T. Receptor-like kinase RUPO interacts with potassium transporters to regulate pollen tube growth and integrity in rice. PLoS Genet. 2016;12(7):e1006085.
210. Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, Li J, Gao C. Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plants. 2016;2:16139.
211. Liu Y, Xu Y, Ling S, Liu S, Yao J. Anther-preferential expressing gene PMR is essential for the mitosis of pollen development in rice. Plant Cell Rep. 2017. doi: 10.1007/s00299-017-2123-2.
212. Yuan J, Chen S, Jiao W, Wang L, Wang L, Ye W, Lu J, Hong D, You S, Cheng Z et al. Both maternally and paternally imprinted genes regulate seed development in rice. New Phytol. 2017. doi: 10.1111/nph.14510.
213. Li X, Zhou W, Ren Y, Tian X, Lv T, Wang Z, Fang J, Chu C, Yang J, Bu Q. High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing. J Genet Genom. 2017;44(3):175-8.
214. Sun Y, Jiao G, Liu Z, Zhang X, Li J, Guo X, Du W, Du J, Francis F, Zhao Y et al. Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci. 2017;8:298. doi: 10.3389/fpls.2017.00298.
215. Yamauchi T, Yoshioka M, Fukazawa A, Mori H, Nishizawa NK, Tsutsumi N, Yoshioka H, Nakazono M. An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell. 2017. doi: 10.1105/tpc.16.00976.
216. Li B, Cui G, Shen G, Zhan Z, Huang L, Chen J, Qi X. Targeted mutagenesis in the medicinal plant Salvia miltiorrhiza. Sci Rep. 2017;7:43320.
217. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol. 2015;15:16.
218. Sun X, Hu Z, Chen R, Jiang Q, Song G, Zhang H, Xi Y. Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci Rep. 2015;5:10342.
219. Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP, Huang L, Ward RT, Clifton E, Falco SC, Cigan AM. Cas9-guide RNA directed genome editing in soybean. Plant Physiol. 2015;169(2):960-70.
220. Cai Y, Chen L, Liu X, Sun S, Wu C, Jiang B, Han T, Hou W. CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS ONE. 2015;10(8):e0136064.
221. Jia H, Wang N. Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE. 2014;9(4):e93806.
222. Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J. 2017. doi: 10.1111/pbi.12733.
223. Ron M, Kajala K, Pauluzzi G, Wang D, Reynoso MA, Zumstein K, Garcha J, Winte S, Masson H, Inagaki S, et al. Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol. 2014;166(2):455-69.
224. Brooks C, Nekrasov V, Lippman ZB, Van Eck J. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 2014;166(3):1292-7.
225. Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Toki S. CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem Biophys Res Commun. 2015;467(1):76-82.
226. Pan C, Ye L, Qin L, Liu X, He Y, Wang J, Chen L, Lu G. CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep. 2016;6:24765.
227. Klap C, Yeshayahou E, Bolger AM, Arazi T, Gupta SK, Shabtai S, Usadel B, Salts Y, Barg R. Tomato facultative parthenocarpy results from SlAGAMOUS-LIKE 6 loss of function. Plant Biotechnol J. 2016. doi: 10.1111/pbi.12662.
228. Soyk S, Muller NA, Park SJ, Schmalenbach I, Jiang K, Hayama R, Zhang L, Van Eck J, Jimenez-Gomez JM, Lippman ZB. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet. 2017;49(1):162-8.
229. Xu C, Park SJ, Van Eck J, Lippman ZB. Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes Dev. 2016;30(18):2048-61.
230. Ueta R, Abe C, Watanabe T, Sugano SS, Ishihara R, Ezura H, Osakabe Y, Osakabe K. Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Sci Rep. 2017;7(1):507.
231. Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep. 2017;7(1):482.