Precision Targeted Mutagenesis via Cas9 Paired Nickases in Rice

Plant and Cell Physiology

Volumn 57, Issue 5, 2016, Pages 1058-1068

  Mikami, Masafumi ^a,b   Toki, Seiichi ^a,b   Endo, Masaki ^b  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

CRISPR Cas9; Genome editing; Off target; Rice; Targeted mutagenesis

Indexed keywords

DEOXYRIBONUCLEASE I; GUIDE RNA; PLANT PROTEIN;

CRISPR CAS SYSTEM; ENZYMOLOGY; GENE EDITING; GENE TARGETING; GENETICS; METABOLISM; MUTAGENESIS; MUTATION; ORYZA;

CRISPR-CAS SYSTEMS; DEOXYRIBONUCLEASE I; GENE EDITING; GENE TARGETING; MUTAGENESIS; MUTATION; ORYZA; PLANT PROTEINS; RNA, GUIDE;

EID: 84971507156     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcw049     Document Type: Article

References (47)

1. Brooks, C., Nekrasov, V., Lippman, Z.B. and Van, Eck. J. (2015) 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.
2. Cho, S.W., Kim, S., Kim, J.M. and Kim, J.S. (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31: 230-232.
3. Cho, S.W., Kim, S., Kim, Y., Kweon, J., Kim, H.S., et al. (2014) Analysis of offtarget effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 24: 132-141.
4. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823.
5. Endo, M., Mikami, M. and Toki, S. (2015) Multigene knockout utilizing offtarget mutations of the CRISPR/Cas9 system in rice. Plant Cell Physiol. 56: 41-47.
6. Fan, D., Liu, T., Li, C., Jiao, B., Li, S., Hou, Y., et al. (2015) Efficient CRISPR/ Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci. Rep. 5: 12217.
7. Fauser, F., Schiml, S. and Puchta, H. (2014) Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 79: 348-359.
8. Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D.L., Wei, P., et al. (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23: 1229-1232.
9. Fu, Y., Foden, J.A., Khayter, C., Maeder, M.L., Reyon, D., Joung, J.K., et al. (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31: 822-826.
10. Heyer, W.D., Ehmsen, K.T. and Liu, J. (2010) Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44: 113-139.
11. Hsu, P.D., Scott, D.A., Weinstein, J.A., Ran, F.A., Konermann, S., Agarwala, V., et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31: 827-832.
12. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., et al. (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31: 227-229.
13. International Rice Genome Sequencing Project. (2005) The map-based sequence of the rice genome. Nature 436: 793-800.
14. Ito, Y., Nishizawa-Yokoi, A., Endo, M., Mikami, M. and Toki, S. (2015) CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem. Biophys. Res. Commun. 467: 76-82.
15. Jiang, W., Bikard, D., Cox, D., Zhang, F. and Marraffini, L.A. (2013a) RNAguided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31: 233-239.
16. Jiang, W., Yang, B. and Weeks, D.P. (2014) Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS One 9: e99225.
17. Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B. and Weeks, D.P. (2013b) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41: e188.
18. 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.
19. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E. and Doudna, J. (2013) RNAprogrammed genome editing in human cells. Elife 2: e00471.
20. Kuscu, C., Arslan, S., Singh, R., Thorpe, J. and Adli, M. (2014) Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat. Biotechnol. 32: 677-683.
21. Li, J.F., Norville, J.E., Aach, J., McCormack, M., Zhang, D., Bush, J., et al. (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 31: 688-691.
22. Mali, P., Aach, J., Stranges, P.B., Esvelt, K.M., Moosburner, M., et al. (2013b) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31: 833-838.
23. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., et al. (2013a) RNA-guided human genome engineering via Cas9. Science 339: 823-826.
24. Miao, J., Guo, D., Zhang, J., Huang, Q., Qin, G., Zhang, X., et al. (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res. 23: 1233-1236.
25. 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.
26. 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.
27. Pattanayak, V., Lin, S., Guilinger, J.P., Ma, E., Doudna, J.A. and Liu, D.R. (2013) Highthroughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31: 839-843.
28. Ran, F.A., Hsu, P.D., Lin, C.Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., et al. (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389.
29. Sakane, I., Kamataki, C., Takizawa, Y., Nakashima, M., Toki, S., Ichikawa, H., et al. (2008) Filament formation and robust strand exchange activities of the rice DMC1A and DMC1B proteins. Nucleic Acids Res. 36: 4266-4276.
30. 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.
31. Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., et al. (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31: 686-688.
32. Shen, B., Zhang, W., Zhang, J., Zhou, J., Wang, J., Chen, L., et al. (2013) Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat. Methods 11: 399-402.
33. Smith, C., Gore, A., Yan, W., Abalde-Atristain, L., Li, Z., He, C., et al. (2014) Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 15: 12-13.
34. Sternberg, S.H., Redding, S., Jinek, M., Greene, E.C. and Doudna, J.A. (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507: 62-67.
35. Sun, X., Hu, Z., Chen, R., Jiang, Q., Song, G., Zhang, H., et al. (2015) Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci. Rep. 5: 10342.
36. 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: 931-45.
37. Symington, L.S. and Gautier, J. (2011) Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45: 247-271.
38. Takimoto, I., Christensen, A.H., Quail, P.H., Uchimiya, H. and Toki, S. (1994) Non-systemic expression of a stress-responsive maize polyubiquitin gene (Ubi-1) in transgenic rice plants. Plant Mol. Biol. 26: 1007-1012.
39. Toki, S. (1997) Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol. Biol. Rep. 15: 16-21.
40. Toki, S., Hara, N., Ono, K., Onodera, H., Tagiri, A., et al. (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J. 47: 969-976.
41. Upadhyay, S.K., Kumar, J., Alok, A. and Tuli, R. (2013) RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda) 3: 2233-2238.
42. Veres, A., Gosis, B.S., Ding, Q., Collins, R., Ragavendran, A., Brand, H., et al. (2014) Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by wholegenome sequencing. Cell Stem Cell 15: 27-30.
43. Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., et al. (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32: 947-951.
44. Woo, J.W., Kim, J., Kwon, S.I., Corvalan, C., Cho, S.W., Kim, H., et al. (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33: 1162-1164.
45. Xu, R., Li, H., Qin, R., Wang, L., Li, L., Wei, P., et al. (2014) Gene targeting using Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice 7: 923-926.
46. Zhang, H., Zhang, J., Wei, P., Zhang, B., Gou, F., Feng, Z., et al. (2014) The CRISPR/Cas9 system produced specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol. J. 12: 797-807.
47. Zhou, H., Liu, B., Weeks, D.P., Spalding, M.H. and Yang, B. (2014) Large chromosomal deletions heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res. 42: 10903-10914.