Progress in genome editing technology and its application in plants

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Zhang, Kai ^a,b   Raboanatahiry, Nadia ^a   Zhu, Bin ^a   Li, Maoteng ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUANGGANG NORMAL UNIVERSITY   (China)

Author keywords

CRISPR C2c1; CRISPR C2c2; CRISPR Cas9; CRISPR Cpf1; Genome editing technology; RNAi; TALEN; ZFN

Indexed keywords

EID: 85012981989     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.00177     Document Type: Article

References (131)

1. Abudayyeh, O. O., Gootenberg, J. S., Konermann, S., Joung, J., Slaymaker, I. M., Cox, D. B. T., et al. (2016). C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573. doi: 10.1126/science.aaf5573
2. Ahmed, M. M. S., Bian, S., Wang, M., Zhao, J., Zhang, B., Liu, Q., et al. (2016). RNAi-mediated resistance to rice black-streaked dwarf virus in transgenic rice. Transgenic Res. doi: 10.1007/s11248-016-9999-4. [Epub ahead of print].
3. Ammara, U. E., Mansoor, S., Saeed, M., Amin, I., Briddon, R. W., and Al-Sadi, A. M. (2015). RNA interference-based resistance in transgenic tomato plants against Tomato yellow leaf curl virus-Oman (TYLCV-OM) and its associated beta satellite. Virol. J. 12:38. doi: 10.1186/s12985-015-0263-y
4. Anantharaman, V., Makarova, K. S., Burroughs, A. M., Koonin, E. V., and Aravind, L. (2013). Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing. Biol. Direct 8:15. doi: 10.1186/1745-6150-8-15
5. Arazoe, T., Miyoshi, K., Yamato, T., Ogawa, T., Ohsato, S., and Arie, T. (2015). Tailor-made CRISPR/Cas system for highly efficient targeted gene replacement in the rice blast fungus. Biotechnol. Bioeng. 112, 2543-2549. doi: 10.1002/bit.25662
6. Austin, E. A., and Huber, B. E. (1993). A first step in the development of gene therapy for colorectal carcinoma: cloning, sequencing, and expression of Escherichia coli cytosine deaminase. Mol. Pharmacol. 43, 380-387.
7. Beerli, R. R., and Barbas, C. R. (2002). Engineering polydactyl zinc-finger transcription factors. Nat. Biotechnol. 20, 135-141. doi: 10.1038/nbt0202-135
8. Boch, J., and Bonas, U. (2010). Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 48, 419-436. doi: 10.1146/annurev-phyto-080508-081936
9. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., and Kay, S. (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512. doi: 10.1126/science.1178811
10. Brooks, C., Nekrasov, V., Lippman, Z. B., and Van Eck, J. (2014). Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 166, 1292-1297. doi: 10.1104/pp.114.247577
11. Brummelkamp, T. R., Bernards, R., and Agami, R. (2002). A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553. doi: 10.1126/science.1068999
12. Brunet, E., Simsek, D., Tomishima, M., DeKelver, R., Choi, V. M., and Gregory, P. (2009). Chromosomal translocations induced at specified loci in human stem cells. Proc. Natl. Acad. Sci. U.S.A. 106, 10620-10625. doi: 10.1073/pnas.0902076106
13. Cai, C. Q., Doyon, Y., Ainley, W. M., Miller, J. C., Dekelver, R. C., and Moehle, E. A. (2009). Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol. Biol. 69, 699-709. doi: 10.1007/s11103-008-9449-7
14. Cencic, R., Miura, H., Malina, A., Robert, F., Ethier, S., and Schmeing, T. M. (2014). Protospacer adjacent motif (PAM)-distal sequences engage CRISPR Cas9 DNA target cleavage. PLoS ONE 9:e109213. doi: 10.1371/journal.pone. 0109213
15. Chen, B., Gilbert, L. A., Cimini, B. A., Schnitzbauer, J., Zhang, W., and Li, G. (2013). Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155, 1479-1491. doi: 10.1016/j.cell.2013. 12.001
16. Chen, X., Chen, G., Truksa, M., Snyder, C. L., Shah, S., and Weselake, R. J. (2014). Glycerol-3-phosphate acyltransferase 4 is essential for the normal development of reproductive organs and the embryo in Brassica napus. J. Exp. Bot. 65, 4201-4215. doi: 10.1093/jxb/eru199
17. Cheng, A. W., Wang, H., Yang, H., Shi, L., Katz, Y., and Theunissen, T. W. (2013). Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res. 23, 1163-1171. doi: 10.1038/cr.2013.122
18. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., and Habib, N. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823. doi: 10.1126/science.1231143
19. Conticello, S. G. (2008). The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9:229. doi: 10.1186/gb-2008-9-6-229
20. Curtin, S. J., Zhang, F., Sander, J. D., Haun, W. J., Starker, C., and Baltes, N. J. (2011). Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol. 156, 466-473. doi: 10.1104/pp.111.172981
21. de Pater, S., Pinas, J. E., Hooykaas, P. J., and van der Zaal, B. J. (2013). ZFN-mediated gene targeting of the Arabidopsis protoporphyrinogen oxidase gene through Agrobacterium-mediated floral dip transformation. Plant Biotechnol. J. 11, 510-515. doi: 10.1111/pbi.12040
22. Dong, D., Ren, K., Qiu, X., Zheng, J., Guo, M., and Guan, X. (2016). The crystal structure of Cpf1 in complex with CRISPR RNA. Nature 532:522. doi: 10.1038/nature17944
23. Duan, J., Lu, G., Xie, Z., Lou, M., Luo, J., and Guo, L. (2014). Genome-wide identification of CRISPR/Cas9 off-targets in human genome. Cell Res. 24, 1009-1012. doi: 10.1038/cr.2014.87
24. Dzitoyeva, S., Dimitrijevic, N., and Manev, H. (2001). Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Mol Psychiatry 6, 665-670. doi: 10.1038/sj.mp.4000955
25. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498. doi: 10.1038/350 78107
26. Fang, Y., and Tyler, B. M. (2016). Efficient disruption and replacement of an effector gene in the oomycete Phytophthora sojae using CRISPR/Cas9. Mol. Plant Pathol. 17, 127-139. doi: 10.1111/mpp.12318
27. Fattah, F., Lee, E. H., Weisensel, N., Wang, Y., Lichter, N., and Hendrickson, E. A. (2010). Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet. 6:e1000855. doi: 10.1371/journal.pgen.1000855
28. Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D. L., and Wei, P. (2013). Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23, 1229-1232. doi: 10.1038/cr.2013.114
29. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811. doi: 10.1038/35888
30. Fonfara, I., Richter, H., Bratovic, M., Le Rhun, A., and Charpentier, E. (2016). The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature 532, 517. doi: 10.1038/nature17945
31. Friedland, A. E., Tzur, Y. B., Esvelt, K. M., Colaiácovo, M. P., Church, G. M., and Calarco, J. A. (2013). Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat. Methods 10, 741-743. doi: 10.1038/nmeth.2532
32. Fu, Y., Sander, J. D., Reyon, D., Cascio, V. M., and Joung, J. K. (2014). Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32, 279-284. doi: 10.1038/nbt.2808
33. Gao, F., Shen, X. Z., Jiang, F., Wu, Y., and Han, C. (2016). DNA-guided genome editing using the Natronobacterium gregoryi Argonaute. Nat. Biotechnol. 34, 768-773. doi: 10.1038/nbt.3547
34. Garneau, J. E., Dupuis, M. È., Villion, M., Romero, D. A., Barrangou, R., and Boyaval, P. (2010). The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468, 67-71. doi: 10.1038/nature09523
35. Gilbert, L. A., Larson, M. H., Morsut, L., Liu, Z., Brar, G. A., and Torres, S. E. (2013). CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154, 442-451. doi: 10.1016/j.cell.2013.06.044
36. Gorbunova, V. V., and Levy, A. A. (1999). How plants make ends meet: DNA double-strand break repair. Trends Plant Sci. 4, 263-269. doi: 10.1016/S1360-1385(99)01430-2
37. Grynberg, M., Erlandsen, H., and Godzik, A. (2003). HEPN: a common domain in bacterial drug resistance and human neurodegenerative proteins. Trends Biochem. Sci. 28, 224-226. doi: 10.1016/S0968-0004(03)00060-4
38. Guilinger, J. P., Thompson, D. B., and Liu, D. R. (2014). Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat. Biotechnol. 32, 577-582. doi: 10.1038/nbt.2909
39. Hess, G. T., Frésard, L., Han, K., Lee, C. H., Li, A., Cimprich, K. A., et al. (2016). Directed evolution using dCas9-targeted somatic hypermutation in mammalian cells. Nat. Methods. 13, 1036-1042. doi: 10.1038/nmeth.4038
40. Hille, F., and Charpentier, E. (2016). CRISPR-Cas: biology, mechanisms and relevance. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 371:20150496. doi: 10.1098/rstb.2015.0496
41. Hou, D. X., Kai, K., Li, J. J., Lin, S., Terahara, N., and Wakamatsu, M. (2004). Anthocyanidins inhibit activator protein 1 activity and cell transformation: structure-activity relationship and molecular mechanisms. Carcinogenesis 25, 29-36. doi: 10.1093/carcin/bgg184
42. Hsu, P. D., Scott, D. A., Weinstein, J. A., Ran, F. A., Konermann, S., and Agarwala, V. (2013). DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832. doi: 10.1038/nbt.2647
43. Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., and Nakata, A. (1987). Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169, 5429-5433. doi: 10.1128/jb.169.12.5429-5433.1987
44. Jiang, W., Bikard, D., Cox, D., Zhang, F., and Marraffini, L. A. (2013). RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31, 233-239. doi: 10.1038/nbt.2508
45. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821. doi: 10.1126/science.1225829
46. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E., and Doudna, J. (2013). RNA-programmed genome editing in human cells. eLife 2:e471. doi: 10.7554/eLife.00471
47. Kao, K. N., andMichayluk, M. R. (1974). Amethodfor high-frequency intergeneric fusion of plant protoplasts. Planta 115, 355-367. doi: 10.1007/BF00388618
48. Kim, D., Kim, J., Hur, J. K., Been, K. W., Yoon, S., and Kim, J. (2016). Genome-wide analysis reveals specificities of Cpf1 endonucleases in human cells. Nat. Biotechnol. 34:863. doi: 10.1038/nbt.3609
49. Kim, Y. G., and Chandrasegaran, S. (1994). Chimeric restriction endonuclease. Proc. Natl. Acad. Sci. U.S.A. 91, 883-887. doi: 10.1073/pnas.91.3.883
50. Kim, Y. G., Cha, J., and Chandrasegaran, S. (1996). Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl. Acad. Sci. U.S.A. 93, 1156-1160. doi: 10.1073/pnas.93.3.1156
51. Kleinstiver, B. P., Tsai, S. Q., Prew, M. S., Nguyen, N. T., Welch, M. M., and Lopez, J. M. (2016). Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat. Biotechnol. 34:869. doi: 10.1038/nbt.3620
52. Komor, A. C., Kim, Y. B., Packer, M. S., Zuris, J. A., and Liu, D. R. (2016). Programmable editing of a target base in genomic DNA without double-stranded DNAcleavage. Nature 533:420. doi: 10.1038/nature17946
53. Kwon, D. N., Lee, K., Kang, M. J., Choi, Y. J., Park, C., and Whyte, J. J. (2013). Production of biallelic CMP-Neu5Ac hydroxylase knock-out pigs. Sci Rep 3:1981. doi: 10.1038/srep01981
54. Lawhorn, I. E., Ferreira, J. P., and Wang, C. L. (2014). Evaluation of sgRNA target sites for CRISPR-mediated repression of TP53. PLoS ONE 9:e113232. doi: 10.1371/journal.pone.0113232
55. Lee, H. J., Kim, E., and Kim, J. S. (2010). Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res. 20, 81-89. doi: 10.1101/gr.099747.109
56. Lee, H. J., Kweon, J., Kim, E., Kim, S., and Kim, J. S. (2012). Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res. 22, 539-548. doi: 10.1101/gr.129635.111
57. Li, J. F., Norville, J. E., Aach, J., McCormack, M., Zhang, D., and Bush, J. (2013). Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 31, 688-691. doi: 10.1038/nbt.2654
58. Li, T., Liu, B., Chen, C. Y., and Yang, B. (2016). TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J. Genet. Genomics 43, 297-305. doi: 10.1016/j.jgg.2016.03.005
59. Li, T., Liu, B., Spalding, M. H., Weeks, D. P., and Yang, B. (2012). High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 30, 390-392. doi: 10.1038/nbt.2199
60. Li, X., Song, Y., Century, K., Straight, S., Ronald, P., and Dong, X. (2001). A fast neutron deletion mutagenesis-based reverse genetics systemfor plants. Plant J. 27, 235-242. doi: 10.1046/j.1365-313x.2001.01084.x
61. Li, Z., Liu, Z. B., Xing, A., Moon, B. P., Koellhoffer, J. P., and Huang, L. (2015). Cas9-guide RNA directed genome editing in soybean. Plant Physiol. 169:960. doi: 10.1104/pp.15.00783
62. Liang, Z., Zhang, K., Chen, K., and Gao, C. (2014). Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J. Genet. Genomics 41, 63-68. doi: 10.1016/j.jgg.2013.12.001
63. Liu, L., Chen, P., Wang, M., Li, X., Wang, J., Yin, M., et al. (2017). C2c1-sgRNA complex structure reveals RNA-guided DNA cleavage mechanism. Mol. Cell. 65, 310-322. doi: 10.1016/j.molcel.2016.11.040
64. Lor, V. S., Starker, C. G., Voytas, D. F., Weiss, D., and Olszewski, N. E. (2014). Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol. 166, 1288-1291. doi: 10.1104/pp.114.247593
65. Ma, Y., Zhang, J., Yin, W., Zhang, Z., Song, Y., and Chang, X. (2016). Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat. Methods. 13, 1029-1035. doi: 10.1038/nmeth.4027
66. Maeder, M. L., Thibodeau-Beganny, S., Osiak, A., Wright, D. A., Anthony, R. M., and Eichtinger, M. (2008). Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol. Cell 31, 294-301. doi: 10.1016/j.molcel.2008.06.016
67. Mahfouz, M. M., Li, L., Shamimuzzaman, M., Wibowo, A., Fang, X., and Zhu, J. K. (2011). De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc. Natl. Acad. Sci. U.S.A. 108, 2623-2628. doi: 10.1073/pnas.1019533108
68. Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., and Horvath, P. (2011). Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9, 467-477. doi: 10.1038/nrmicro2577
69. Makarova, K. S., Wolf, Y. I., Alkhnbashi, O. S., Costa, F., Shah, S. A., and Saunders, S. J. (2015). Anupdatedevolutionary classificationof CRISPR-Cas systems. Nat. Rev. Microbiol. 13, 722-736. doi: 10.1038/nrmicro3569
70. Mali, P., Aach, J., Stranges, P. B., Esvelt, K. M., Moosburner, M., and Kosuri, S. (2013c). CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833-838. doi: 10.1038/nbt.2675
71. Mali, P., Esvelt, K. M., and Church, G. M. (2013a). Cas9 as a versatile tool for engineering biology. Nat. Methods 10, 957-963. doi: 10.1038/nmeth.2649
72. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., and DiCarlo, J. E. (2013b). RNA-guided human genome engineering via Cas9. Science 339, 823-826. doi: 10.1126/science.1232033
73. Marine, S., Bahl, A., Ferrer, M., and Buehler, E. (2012). Common seed analysis to identify off-target effects in siRNA screens. J. Biomol. Screen. 17, 370-378. doi: 10.1177/1087057111427348
74. Miao, J., Guo, D., Zhang, J., Huang, Q., Qin, G., and Zhang, X. (2013). Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res. 23, 1233-1236. doi: 10.1038/cr.2013.123
75. Mikami, M., Toki, S., and Endo, M. (2015). Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice. Plant Mol. Biol. 88, 561-572. doi: 10.1007/s11103-015-0342-x
76. Mojica, F. J., Díez-Villasenor, C., García-Martinez, J., and Soria, E. (2005). Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60, 174-182. doi: 10.1007/s00239-004-0046-3
77. Moscou, M. J., and Bogdanove, A. J. (2009). A simple cipher governs DNA recognition by TAL effectors. Science 326:1501. doi: 10.1126/science.1178817
78. Muramatsu, M., Sankaranand, V. S., Anant, S., Sugai, M., Kinoshita, K., and Davidson, N. O. (1999). Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274, 18470-18476. doi: 10.1074/jbc.274.26.18470
79. Nekrasov, V., Staskawicz, B., Weigel, D., Jones, J. D., and Kamoun, S. (2013). Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 691-693. doi: 10.1038/nbt.2655
80. Osakabe, K., Osakabe, Y., and Toki, S. (2010). Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc. Natl. Acad. Sci. U.S.A. 107, 12034-12039. doi: 10.1073/pnas.1000234107
81. Pabo, C. O., Peisach, E., and Grant, R. A. (2001). Design and selection of novel Cys2His2 zinc finger proteins. Annu. Rev. Biochem. 70, 313-340. doi: 10.1146/annurev.biochem.70.1.313
82. Page, D. R., and Grossniklaus, U. (2002). The art and design of genetic screens: Arabidopsis thaliana. Nat. Rev. Genet. 3, 124-136. doi: 10.1038/nrg730
83. Pawluk, A., Amrani, N., Zhang, Y., Garcia, B., Hidalgo-Reyes, Y., and Lee, J. (2016b). Naturally occurring off-switches for CRISPR-Cas9. Cell 167, 1829-1838. doi: 10.1016/j.cell.2016.11.017
84. Pawluk, A., Staals, R. H. J., Taylor, C., Watson, B. N. J., Saha, S., Fineran, P. C., et al. (2016a). Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat. Microbiol. 1:16085. doi: 10.1038/nmicrobiol.2016.85
85. Perez-Pinera, P., Kocak, D. D., Vockley, C. M., Adler, A. F., Kabadi, A. M., Polstein, L. R., et al. (2013). RNA-guided gene activation by CRISPR-Cas9-basedtranscriptionfactors. Nat. Methods 10, 973-976. doi: 10.1038/nmeth.2600
86. Rada, C., and Di Noia, J. M. (2004). Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol. Cell 16, 163-171. doi: 10.1016/j.molcel.2004.10.011
87. Ran, F. A., Hsu, P. D., Lin, C. Y., Gootenberg, J. S., Konermann, S., and Trevino, A. E. (2013). Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389. doi: 10.1016/j.cell.2013.08.021
88. Sachse, C., Krausz, E., Krönke, A., Hannus, M., Walsh, A., and Grabner, A. (2005). High-throughput RNA interference strategies for target discovery and validation by using synthetic short interfering RNAs: functional genomics investigations of biological pathways. Methods Enzymol. 392, 242-277. doi: 10.1016/S0076-6879(04)92015-0
89. Salts, Y., Beckmann, J. S., Loyter, A., and Lavi, U. (1985). Interactions of sendai virus with plant protoplasts. Plant Sci. 41, 141-149. doi: 10.1016/0168-9452(85)90116-5
90. Sander, J. D., Cade, L., Khayter, C., Reyon, D., Peterson, R. T., and Joung, J. K. (2011). Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat. Biotechnol. 29, 697-698. doi: 10.1038/nbt.1934
91. Schiml, S., Fauser, F., and 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, 1139-1150. doi: 10.1111/tpj.12704
92. Schunder, E., Rydzewski, K., Grunow, R., and Heuner, K. (2013). First indication for a functional CRISPR/Cas system in Francisella tularensis. Int. J. Med. Microbiol. 303, 51-60. doi: 10.1016/j.ijmm.2012.11.004
93. Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., and Liang, Z. (2013). Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31, 686-688. doi: 10.1038/nbt.2650
94. Shan, Q., Zhang, Y., Chen, K., Zhang, K., and Gao, C. (2015). Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol. J. 13, 791-800. doi: 10.1111/pbi.12312
95. Shmakov, S., Abudayyeh, O. O., Makarova, K. S., Wolf, Y. I., Gootenberg, J. S., and Semenova, E. (2015). Discovery and functional characterization of diverse class 2 CRISPR-cas systems. Mol. Cell 60, 385-397. doi: 10.1016/j.molcel.2015. 10.008
96. Shukla, V. K., Doyon, Y., Miller, J. C., DeKelver, R. C., Moehle, E. A., and Worden, S. E. (2009). Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459, 437-441. doi: 10.1038/nature07992
97. Sonoda, E., Hochegger, H., Saberi, A., Taniguchi, Y., and Takeda, S. (2006). Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair. 5, 1021-1029. doi: 10.1016/j.dnarep.2006.05.022
98. Soyk, S., Müller, N. A., Park, S. J., Schmalenbach, I., Jiang, K., Hayama, R., et al. (2016). Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat. Genet. 49, 162-168. doi: 10.1038/ng.3733
99. Stadler, L. J. (1928a). Mutations in barley induced by X-rays and radium. Science 68, 186-187.
100. Stadler, L. J. (1928b). Genetic effects of x-rays in maize. Proc. Natl. Acad. Sci. U.S.A. 14, 69-75.
101. Stroud, D. A., Surgenor, E. E., Formosa, L. E., Reljic, B., Frazier, A. E., and Dibley, M. G. (2016). Accessory subunits are integral for assembly and function of human mitochondrial complex I. Nature 538, 123-126. doi: 10.1038/nature19754
102. Suzuki, T., Eiguchi, M., Kumamaru, T., Satoh, H., Matsusaka, H., and Moriguchi, K. (2008). MNU-induced mutant pools and high performance TILLINGenable finding of any gene mutation in rice. Mol. Genet. Genomics 279, 213-223. doi: 10.1007/s00438-007-0293-2
103. Svitashev, S., Young, J. K., Schwartz, C., Gao, H., Falco, S. C., and Cigan, A. M. (2015). Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol. 169, 931-945. doi: 10.1104/pp.15.00793
104. Symington, L. S., and Gautier, J. (2011). Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271. doi: 10.1146/annurev-genet-110410-132435
105. Takahashi, J. S., Pinto, L. H., and Vitaterna, M. H. (1994). Forward and reverse genetic approaches to behavior in the mouse. Science 264, 1724-1733. doi: 10.1126/science.8209253
106. Talamè, V., Bovina, R., Sanguineti, M. C., Tuberosa, R., Lundqvist, U., and Salvi, S. (2008). TILLMore, a resource for the discovery of chemically induced mutants in barley. Plant Biotechnol. J. 6, 477-485. doi: 10.1111/j.1467-7652.2008.00341.x
107. Townsend, J. A., Wright, D. A., Winfrey, R. J., Fu, F., Maeder, M. L., and Joung, J. K. (2009). High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459, 442-445. doi: 10.1038/nature 07845
108. Travella, S., Klimm, T. E., and Keller, B. (2006). RNA interference-based gene silencing as an efficient tool for functional genomics in hexaploid bread wheat. Plant Physiol. 142, 6-20. doi: 10.1104/pp.106.084517
109. Tsai, S. Q., Wyvekens, N., Khayter, C., Foden, J. A., Thapar, V., and Reyon, D. (2014). Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32, 569-576. doi: 10.1038/nbt.2908
110. Tsutsui, H., and Higashiyama, T. (2017). pKAMA-ITACHI vectors for highly efficient CRISPR/Cas9-mediated gene knockout in Arabidopsis thaliana. Plant Cell Physiol. 58, 46-56. doi: 10.1093/pcp/pcw191
111. Upadhyay, S. K., Kumar, J., Alok, A., and Tuli, R. (2013). RNA-guided genome editing for target gene mutations in wheat. G3 3, 2233-2238. doi: 10.1534/g3.113.008847
112. Vestergaard, G., Garrett, R. A., and Shah, S. A. (2014). CRISPR adaptive immune systems of Archaea. RNA Biol. 11, 156-167. doi: 10.4161/rna.27990
113. Wang, N., Wang, Y., Tian, F., King, G. J., Zhang, C., and Long, Y. (2008). A functional genomics resource for Brassica napus: development of an EMS mutagenized population and discovery of FAE1 point mutations by TILLING. New Phytol. 180, 751-765. doi: 10.1111/j.1469-8137.2008.02619.x
114. Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., and Gao, C. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32, 947-951. doi: 10.1038/nbt.2969
115. Wei, C., Liu, J., Yu, Z., Zhang, B., Gao, G., and Jiao, R. (2013). TALEN or Cas9 - rapid, efficient and specific choices for genome modifications. J. Genet. Genomics 40, 281-289. doi: 10.1016/j.jgg.2013.03.013
116. Weinthal, D. M., Taylor, R. A., and Tzfira, T. (2013). Nonhomologous end joining-mediated gene replacement in plant cells. Plant Physiol. 162, 390-400. doi: 10.1104/pp.112.212910
117. Wiedenheft, B., Sternberg, S. H., and Doudna, J. A. (2012). RNA-guided genetic silencing systems in bacteria and archaea. Nature 482, 331-338. doi: 10.1038/nature10886
118. Wright, A. V., Nuñez, J. K., and Doudna, J. A. (2016). Biology and applications of CRISPR Systems: Harnessing nature’s toolbox for genome engineering. Cell 164, 29-44. doi: 10.1016/j.cell.2015.12.035
119. Wu, J. L., Wu, C., Lei, C., Baraoidan, M., Bordeos, A., and Madamba, M. R. (2005). Chemical- and irradiation-induced mutants of indica rice IR64 for forward and reverse genetics. Plant Mol. Biol. 59, 85-97. doi: 10.1007/s11103-004-5112-0
120. Wu, X., Scott, D. A., Kriz, A. J., Chiu, A. C., Hsu, P. D., and Dadon, D. B. (2014). Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat. Biotechnol. 32, 670-676. doi: 10.1038/nbt.2889
121. Xiao, A., Wang, Z., Hu, Y., Wu, Y., Luo, Z., and Yang, Z. (2013). Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res. 41:e141. doi: 10.1093/nar/gkt464
122. Xie, K., Zhang, J., and Yang, Y. (2014). Genome-wide prediction of highly specific guide RNAspacers for CRISPR-Cas9-mediated genome editing in model plants and major crops. Mol. Plant 7, 923-926. doi: 10.1093/mp/ssu009
123. Xing, H. L., Dong, L., Wang, Z. P., Zhang, H. Y., Han, C. Y., and Liu, B. (2014). A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14:327. doi: 10.1186/s12870-014-0327-y
124. Xu, R., Qin, R., Li, H., Li, D., Li, L., Wei, P., et al. (2016). Generation of targeted mutant rice using a CRISPR-Cpf1 system. Plant Biotechnol. J. doi: 10.1111/pbi.12669. [Epub ahead of print].
125. Yang, H., Gao, P., Rajashankar, K. R., and Patel, D. J. (2016). PAM-dependent target DNA recognition and cleavage by C2c1 CRISPR-Cas endonuclease. Cell 167, 1814-1828. doi: 10.1016/j.cell.2016.11.053
126. Yang, L., Briggs, A. W., Chew, W. L., Mali, P., Guell, M., Aach, J., et al. (2016). Engineering and optimising deaminase fusions for genome editing. Nat. Commun. 7:13330. doi: 10.1038/ncomms13330
127. Zamore, P. D., Tuschl, T., Sharp, P. A., and Bartel, D. P. (2000). RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101, 25-33. doi: 10.1016/S0092-8674(00)80620-0
128. Zetsche, B., Gootenberg, J. S., Abudayyeh, O. O., Slaymaker, I. M., Makarova, K. S., and Essletzbichler, P. (2015). Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163, 759-771. doi: 10.1016/j.cell.2015.09.038
129. Zhang, F., Maeder, M. L., Unger-Wallace, E., Hoshaw, J. P., Reyon, D., and Christian, M. (2010). High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc. Natl. Acad. Sci. U.S.A. 107, 12028-12033. doi: 10.1073/pnas.0914991107
130. Zhang, Y., Zhang, F., Li, X., Baller, J. A., Qi, Y., and Starker, C. G. (2013). Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol. 161, 20-27. doi: 10.1104/pp.112.205179
131. Zhao, Y., Zhang, C., Liu, W., Gao, W., Liu, C., and Song, G. (2016). An alternative strategy for targeted gene replacement in plants using a dual-sgRNA/Cas9 design. Sci Rep 6:23890. doi: 10.1038/srep23890