CRISPR/Cas9: A powerful tool for crop genome editing

Crop Journal

Volumn 4, Issue 2, 2016, Pages 75-82

  Song, Gaoyuan ^a   Jia, Meiling ^a   Chen, Kai ^a   Kong, Xingchen ^a   Khattak, Bushra ^a   Xie, Chuanxiao ^a   Li, Aili ^a   Mao, Long ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

CRISPR Cas9; Double strand break; Genome editing; TALENs; ZFNs

Indexed keywords

EID: 85009135352     PISSN: 20955421     EISSN: 22145141     Source Type: Journal    
DOI: 10.1016/j.cj.2015.12.002     Document Type: Review

References (75)

1. [1] Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., Nakata, A., Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169 (1987), 5429–5433.
2. [2] Horvath, P., Barrangou, R., CRISPR/Cas, the immune system of bacteria and archaea. Science 327 (2010), 167–170.
3. [3] Jansen, R., Embden, J.D., Gaastra, W., Schouls, L.M., Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43 (2002), 1565–1575.
4. [4] Bolotin, A., Quinquis, B., Sorokin, A., Ehrlich, S.D., Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151 (2005), 2551–2561.
5. [5] Mojica, F.J., Díez-Villasen, C., García-Martínez, J., Soria, E., Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60 (2005), 174–182.
6. [6] Pourcel, C., Salvignol, G., Vergnaud, G., CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151 (2005), 653–663.
7. [7] Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J., Charpentier, E., CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471 (2011), 602–607.
8. [8] Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821.
9. [9] Belhaj, K., Chaparro-Garcia, A., Kamoun, S., Patron, N.J., Nekrasov, V., Editing plant genomes with CRISPR/Cas9. Curr. Opin. Biotechnol. 32 (2015), 76–78.
10. [10] Nishimasu, H., Ran, F.A., Hsu, P.D., Konermann, S., Shehata, S.I., Dohmae, N., Ishitani, R., Zhang, F., Nureki, O., Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156 (2014), 935–949.
11. [11] Jinek, M., Jiang, F., Taylor, D.W., Sternberg, S.H., Kaya, E., Ma, E., Anders, C., Hauer, M., Zhou, K., Lin, S., Kaplan, M., Iavarone, A.T., Charpentier, E., Nogales, E., Doudna, J.A., Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science, 343, 2014, 1247997.
12. [12] Anders, C., Niewoehner, O., Duerst, A., Jinek, M., Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513 (2014), 569–573.
13. [13] Puchta, H., The repair of double stranded DNA breaks in plants. J. Exp. Bot. 56 (2005), 1–14.
14. [14] Shukla, V.K., Doyon, Y., Miller, J.C., Dekelver, R.C., Moehle, E.A., Worden, S.E., Mitchell, J.C., Arnold, N.L., Gopalan, S., Meng, X.D., Choi, V.M., Rock, J.M., Wu, Y.Y., Katibah, G.E., Gao, Z.F., McCaskill, D., Simpson, M.A., Blakeslee, B., Greenwalt, S.A., Butler, H.J., Hinkley, S.J., Zhang, L., Rebar, E.J., Gregory, P.D., Uronv, F.D., Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459 (2009), 437–441.
15. [15] Schiml, S., Fauser, F., Puchta, H., The CRISPR/Cas9 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 (2014), 1139–1150.
16. [16] Porteus, M.H., Caroll, D., Gene targeting using zing finger nucleases. Nat. Biotechnol. 23 (2005), 967–973.
17. [17] Christian, M., Cermak, T., Doyle, E.L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A.J., Voytas, D.F., Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186 (2010), 757–761.
18. [18] Miller, J.C., Tan, S., Qiao, G., Barlow, K.A., Wang, J., Xia, D.F., Meng, X., Paschon, D.E., Leung, E., Hinkley, S.J., Dulay, G.P., Hua, K.L., Ankoudinova, I., Cost, G.J., Urnov, F.D., Zhang, H.S., Holmes, M.C., Zhang, L., Gregory, P.D., Rebar, E.J., A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29 (2011), 143–148.
19. [19] Voytas, D.F., Plant genome engineering with sequence-specific nuclease. Annu. Rev. Plant Biol. 64 (2013), 327–350.
20. [20] Li, J.F., Norville, J.E., Aach, J., McCormack, M., Zhang, D., Bush, J., Church, G.M., Sheen, J., Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 31 (2013), 688–691.
21. [21] Jiang, W.Z., Zhou, H.B., Bi, H.H., Fromm, M., Yang, B., Weeks, D.P., Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41 (2013), 1–12.
22. [22] 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. 79 (2014), 348–359.
23. [23] Feng, Z.Y., Zhang, B.T., Ding, W.N., Liu, X.D., Yang, D.L., Wei, P.L., Cao, F.Q., Zhu, S.H., Zhang, F., Mao, Y.F., Zhu, J.K., Efficient genome editing in plants using a CSRIPR/Cas system. Cell Res. 23 (2013), 1229–1232.
24. [24] Hyun, Y.B., Kim, J., Cho, S.W., Choi, Y., Kim, J.S., Coupland, G., Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted REGN of the CRISPR/Cas9 system to generate heritable null alleles. Planta 241 (2015), 271–284.
25. [25] Feng, Z.Y., Mao, Y.F., Xu, N.F., Zhang, B.T., Wei, P.L., Yang, D.L., Wang, Z., Zhang, Z.J., Zheng, R., Yang, L., Liu, X.D., Zhu, J.K., Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 4632–4637.
26. [26] Mao, Y.F., Zhang, H., Xu, N.F., Zhang, B.T., Gou, F., Zhu, J.K., Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol. Plant 6 (2013), 2008–2011.
27. [27] Ali, Z., Abul-faraj, A., Li, L., Ghosh, N., Piatek, M., Mahjoub, A., Aouida, M., Piatek, A., Baltes, N.J., Voytas, D.F., Dinesh-Kumar, S., Mahfouz, M.M., Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol. Plant 8 (2015), 1288–1291.
28. [28] Gao, J.P., Wang, G.H., Ma, S.Y., Xie, X.D., Wu, X.W., Zhang, X.T., Wu, Y.Q., Zhao, P., Xia, Q.Y., CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol. Biol. 87 (2015), 99–110.
29. [29] Nekrasov, V., Staskawicz, B., Weigel, D., Jones, J.D., Kamoun, S., Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31 (2013), 691–693.
30. [30] Brooks, C., Nekrasov, V., Lippman, Z.B., Eck, J.V., Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 166 (2014), 1292–1297.
31. [31] Shan, Q.W., Wang, Y.P., Li, J., Zhang, Y., Chen, K.L., Liang, Z., Zhang, K., Liu, J.X., Xi, J.J., Qiu, J.L., Gao, C.X., Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31 (2013), 686–688.
32. [32] Miao, J., Guo, D.S., Zhang, J.Z., Huang, Q.P., Qin, G.J., Zhang, X., Wan, J.M., Gu, H.Y., Qu, L.J., Targeted mutagenesis in rice using CRISPR-Cas9 system. Cell Res. 23 (2013), 1233–1236.
33. [33] Zhang, H., Zhang, J.S., Wei, P.L., Zhang, B.T., Gou, F., Feng, Z.Y., Mao, Y.F., Yang, L., Zhang, H., Xu, N.F., Zhu, J.K., The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol. J. 12 (2014), 797–807.
34. [34] Xie, K.B., Yang, Y.N., RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant 6 (2013), 1975–1983.
35. [35] Xu, R.F., Li, H., Qin, R.Y., Wang, L., Li, L., Wei, P.C., Yang, J.B., Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice, 7, 2014, 5.
36. [36] Xie, K.B., Minkenberg, B., Yang, Y.N., Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 3570–3575.
37. [37] Ma, X.L., Zhang, Q.Y., Zhu, Q.L., Liu, W., Chen, Y., Qiu, R., Wang, B., Yang, Z.F., Li, H.Y., Lin, Y.R., Xie, Y.Y., Shen, R.X., Chen, S.F., Wang, Z., Chen, Y.L., Guo, J.L., Chen, L., Zhao, X.C., Dong, Z.C., Liu, Y.G., A robust CRISPR/Cas9 system for convenient high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant, 2015, 10.1016/j.molp.
38. [38] Zhou, H.B., Liu, B., Weeks, D.P., Spalding, M.H., Yang, B., Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res. 42 (2014), 10903–10914.
39. [39] Liang, Z., Zhang, K., Chen, K.L., Gao, C.X., Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J. Genet. Genomics 41 (2014), 63–68.
40. [40] Svitashev, S., Young, J.K., Schwartz, C., Gao, H.R., Falco, S.C., Cigan, A.M., Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol. 169 (2015), 931–945.
41. [41] Jia, H.G., Wang, N., Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One, 9, 2014, e93806.
42. [42] Fan, D., Liu, T.T., Li, C.F., Jiao, B., Li, S., Hou, Y.S., Luo, K.M., Efficient CRISPR/Cas9-mediated targeted mutagenesis in populous in the first generation. Sci. Rep., 2015, 10.1038/srep12217.
43. [43] Jacoobs, T.B., LaFayette, P.R., Schmitz, R.J., Parrott, W.A., Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol., 15, 2015, 16.
44. [44] Li, Z.S., Liu, Z.B., Xing, A.Q., Moon, B.P., Koellhoffer, J.P., Huang, L.X., Ward, R.T., Clifton, E., Falco, S.C., Cigan, A.M., Cas9-guide RNA directed genome editing in soybean. Plant Physiol. 169 (2015), 960–970.
45. [45] Wang, Y.P., Cheng, X., Shan, Q.W., Zhang, Y., Liu, J.X., Gao, C.X., Qiu, J.L., Simultaneous editing of three homoealleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32 (2014), 937–951.
46. [46] Shan, Q.W., Wang, Y.P., Li, J., Gao, C.X., Genome editing in rice and wheat using the CRISPR/Cas9 system. Nat. Protoc. 9 (2014), 2395–2410.
47. [47] Slade, A.J., Fuerstenberg, S.I., Loeffler, D., Steine, M.N., Facciotti, D., A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat. Biotechnol. 23 (2005), 75–81.
48. [48] Muehlbauer, G.J., Feuillet, C., Genetics and Genomics of the Triticeae. Jorgensen, R.A., (eds.) Plant Genetics and Genomics: Crops and Models, vol. 7, 2009, Springer-Verlag, New York, 685–711.
49. [49] Hsu, P.D., Scott, D.A., Weinstein, J.A., Ran, F.A., Konermann, S., Agarwala, V., Li, Y.Q., Fine, E.J., Wu, X.B., Shalem, O., Cradick, T.J., Marraffini, L.A., Bao, G., Zhang, F., DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31 (2013), 827–832.
50. [50] Pattanayak, V., Lin, S., Guilinger, J.P., Ma, E., Doudna, J.A., Liu, D.R., High-throughput profiling of off-target DNA cleavage reveals RNA programmed Cas9 nuclease specificity. Nat. Biotechnol. 31 (2013), 839–843.
51. [51] Sternberg, S.H., Redding, S., Jinek, M., Greene, E.C., Doudna, J.A., DNA interrogation by the CRISPR RNA-guide endonuclease Cas9. Nature 6 (2014), 62–67.
52. [52] Xie, K.B., Zhang, J.W., Yang, Y.N., Genome-wide prediction of highly specific guide RNA spacers for CRISPR-Cas9-mediated genome editing in model plants and major crops. Mol. Plant 5 (2014), 023–926.
53. [53] Xie, S.S., Shen, B., Zhang, C.B., Huang, X.X., Zhang, Y.L., sgRNAcas9: a software package for designing CRISPR sgRNA and evaluation potential off-target cleavage sites. PLoS One, 9, 2015, e100448.
54. [54] Yan, M., Zhou, S.R., Xue, H.W., CRISPR primer designer: design primers for knockout and chromosome imaging CRISPR-Cas system. J. Integr. Plant Biol. 7 (2015), 613–617.
55. [55] Cradick, T.J., Qiu, P., Lee, C.M., Fine, E.J., G Bao, COSMID: a web-based tool for identifying and validating CRISPR/Cas off-target sites. Mol. Ther. Nucl. Acids, 3, 2014, e214.
56. [56] Heigwer, F., Kerr, G., Boutros, M., E-CRISPR: fast CRISPR target site identification. Nat. Methods 11 (2014), 122–123.
57. [57] Montague, T.G., Cruz, J.M., Gagnon, J.A., Church, G.M., Valen, E., CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 42 (2014), W401–W407.
58. [58] Xiao, A., Cheng, Z.C., Kong, L., Zhu, Z.Y., Lin, S., Gao, G., Zhang, B., CasOT: a genome-wide Cas9/gRNA off-target searching tool. Bioinformatics 30 (2014), 1180–1182.
59. [59] Mikami, M., Toki, S., Endo, M., Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice. Plant Mol. Biol. 88 (2015), 561–572.
60. [60] Ran, F.A., Hsu, P.D., Lin, C.Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., Scott, D.A., Inoue, A., Matoba, S., Zhang, Y., Zhang, F., Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154 (2014), 1380–1389.
61. [61] Shen, B., Zhang, W.S., Zhang, J., Zhou, J.K., Wang, J.Y., Chen, L., Wang, L., Hodgkins, A., Iyer, V., Huang, X.X., Skarens, W.C., Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat. Methods 11 (2014), 399–402.
62. [62] Qi, L.S., Larson, M.H., Gilbert, L.A., Doudna, J.A., Weismann, J.S., Arkin, A.P., Lim, W.A., Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152 (2013), 1173–1183.
63. [63] Gilbert, L.A., Horlbeck, M.A., Adamson, B., Villalta, J.E., Chen, Y.W., Whitehead, E.H., Guimaraes, C., Panning, B., Ploegh, H.L., Bassik, M.C., Qi, L.S., Kampmann, M., Weissman, J.S., Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159 (2014), 1–15.
64. [64] Rusk, N., CRISPRs and epigenome editing. Nat. Methods, 11, 2014, 28.
65. [65] Chen, B., Gilbert, L.A., Cimini, B.A., Schnitzbauer, J., Zhang, W., Li, G.W., Park, J., Blackburn, E.H., Weissman, J.S., Qi, L.S., Huang, B., Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155 (2013), 1479–1491.
66. [66] Polstein, L.R., Gersbach, C.A., A light-inducible CRISPR-Cas9 system for control of endogenous gene activation. Nat. Chem. Biol. 11 (2015), 198–200.
67. [67] Wang, Z.P., Xing, H.L., Dong, L., Zhang, H.Y., Han, C.Y., Wang, X.C., Chen, Q.J., Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol., 16, 2015, 144.
68. [68] Mao, Y.F., Zhang, Z.J., Feng, Z.G., Wei, P.L., Zhang, H., Botella, J.R., Zhu, J.K., Development of germ-line-specific CRISPR-Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant Biotechnol. J., 2015, 10.1111/pbi.12468.
69. [69] Deveau, H., Barrangou, R., Garneau, J.E., Labonté, J., Fremaux, C., Boyaval, P., Romero, D.A., Horvath, P., Moineau, S., Phage response to CRISPR-encoded resistance in Streptococcus thermophiles. J. Bacteriol. 190 (2008), 1390–1400.
70. [70] Ran, F.A., Cong, L., Yan, W.X., Scott, D.A., Gootenberg, J.S., Kriz, A.J., Zetsche, B., Shalem, O., Wu, X.B., Makarova, K.S., Koonin, E.V., Sharp, P.A., Zhang, F., In vivo genome editing using Staphylococcus aureus Cas9. Nature 520 (2015), 186–191.
71. [71] Kleisstiver, B.P., Prew, M.S., Tsai, S.Q., Topka, V.V., Nguyen, N.T., Zheng, Z.L., Gonzales, A.W., Li, Z.Y., Peterson, R.T., Yeh, J.J., Aryee, M.J., Joung, J.K., Engineering CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523 (2015), 481–485.
72. [72] Zetsche, B., Gootenberg, J.S., Abudayyeh, O.O., Slaymaker, I.M., Makarova, K.S., Essletzbichler, P., Volz, S.E., Joung, J.L., Oost, J.V.D., Regev, A., Koonin, E.V., Zhang, F., Cpf1 is a single RNA-guide endonuclease of a class 2 CRISPR-Cas system. Cell 163 (2015), 1–13.
73. [73] Kiani, S., Chavez, A., Tuttle, M., Hall, R.N., Chari, R., Ter-Ovanesyan, D., Qian, J., Pruitt, B.W., Beal, J., Vora, S., Buchthal, J., Kowal, E.J.K., Ebrahimkhani, M.R., Collins, J.J., Weiss, R., George Church, Cas9 gRNA engineering for genome editing, activation and repression. Nat. Methods 12 (2015), 1051–1054.
74. [74] Bortesi, L., Fischer, R., The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33 (2015), 41–52.
75. [75] Woo, J.W., Kim, J., Kwon, S.I., Corvalan, C., Cho, S.W., Kim, H., Kim, S.G., Kim, S.T., Choe, S., Kim, J.S., DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33 (2015), 1162–1164.