New variants of CRISPR RNA-guided genome editing enzymes

Plant Biotechnology Journal

Volumn 15, Issue 8, 2017, Pages 917-926

  Murovec, Jana ^a   Pirc, Žan ^a   Yang, Bing ^b  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Cpf1; CRISPR effector C2c2; CRISPR Cas9; genome editing; plant biotechnology; variants of Streptococcus pyogenes Cas9

Indexed keywords

BIOLOGICAL MODEL; BIOTECHNOLOGY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; ENZYMOLOGY; GENE EDITING; GENETICS; PROCEDURES; STREPTOCOCCUS PYOGENES; TRANSGENIC PLANT;

BIOTECHNOLOGY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; GENE EDITING; MODELS, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED; STREPTOCOCCUS PYOGENES;

EID: 85019022155     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12736     Document Type: Review

References (82)

1. Abudayyeh, O.O., Gootenberg, J.S., Konermann, S., Joung, J., Slaymaker, I.M., Cox, D.B.T., Shmakov, S. et al. (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science, 353, aaf5573.
2. Alagoz, Y., Gurkok, T., Zhang, B. and Unver, T. (2016) Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci. Rep. 6, 30910.
3. Ali, Z., Abulfaraj, A., Idris, A., Ali, S., Tashkandi, M. and Mahfouz, M.M. (2015a) CRISPR/Cas9-mediated viral interference in plants. Genome Biol. 16, 238.
4. Ali, Z., Abulfaraj, A., Li, L., Ghosh, N., Piatek, M., Mahjoub, A., Aouida, M. et al. (2015b) Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol. Plant, 8, 1288–1291.
5. Ali, Z., Ali, S., Tashkandi, M., Zaidi, S.S.-E.-A. and Mahfouz, M.M. (2016) CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci. Rep. 6, 26912.
6. Baltes, N.J., Hummel, A.W., Konecna, E., Cegan, R., Bruns, A.N., Bisaro, D.M. and Voytas, D.F. (2015) Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat. Plants, 1, 15145.
7. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A. et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315, 1709–1712.
8. Burstein, D., Harrington, L.B., Strutt, S.C. and Probst, A.J. (2017) New CRISPR-Cas systems from uncultivated microbes. Nature, 542, 237–241.
9. Chandrasekaran, J., Brumin, M., Wolf, D., Leibman, D., Klap, C., Pearlsman, M., Sherman, A. et al. (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol. Plant Pathol. 17, 1140–1153.
10. Chew, W.L., Tabebordbar, M., Cheng, J.K.W., Mali, P., Wu, E.Y., Ng, A.H.M., Zhu, K. et al. (2016) A multifunctional AAV-CRISPR-Cas9 and its host response. Nat. Methods, 13, 868–874.
11. 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.
12. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D. et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819–823.
13. East-Seletsky, A., O'Connell, M.R., Knight, S.C., Burstein, D., Cate, J.H.D., Tjian, R. and Doudna, J.A. (2016) Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature, 538, 270–273.
14. Endo, A., Masafumi, M., Kaya, H. and Toki, S. (2016) Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Sci. Rep. 6, 38169.
15. 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.
16. Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D.-L., Wei, P., Cao, F. et al. (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23, 1229–1232.
17. Garneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C. et al. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 468, 67–71.
18. Gasiunas, G., Barrangou, R., Horvath, P. and Siksnys, V. (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl Acad. Sci. USA, 109, E2579–E2586.
19. 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.
20. Hou, Z., Zhang, Y., Propson, N.E., Howden, S.E., Chu, L., Sontheimer, E.J. and Thomson, J.A. (2013) Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl Acad. Sci. USA, 110, 15644–15649.
21. Hu, X., Wang, C., Liu, Q., Fu, Y. and Wang, K. (2016) Targeted mutagenesis in rice using CRISPR-Cpf1 system. J. Genet. Genomics, 44, 2016–2018.
22. 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.
23. Jansen, R., van Embden, J.D.A., Gaastra, W. and Schouls, L.M. (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43, 1565–1575.
24. Ji, X., Zhang, H., Zhang, Y., Wang, Y. and Gao, C. (2015) Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nat. Plants, 1, 15144.
25. Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B. and Weeks, D.P. (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41, e188.
26. 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, 816–822.
27. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E. and Doudna, J.A. (2013) RNA-programmed genome editing in human cells. eLife, e00471.
28. Kaya, H., Mikami, M., Endo, A., Endo, M. and Toki, S. (2016) Highly specific targeted mutagenesis in plants using Staphylococcus aureus Cas9. Sci. Rep. 6, 26871.
29. Kim, H., Kim, S.-T., Ryu, J., Kang, B.-C., Kim, J.-S. and Kim, S.-G. (2017) CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat. Commun. 8, 14406.
30. Kleinstiver, B.P., Prew, M.S., Tsai, S.Q., Nguyen, N.T., Topkar, V.V., Zheng, Z. and Joung, J.K. (2015a) Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat. Biotechnol. 33, 1293–1298.
31. Kleinstiver, B.P., Prew, M.S., Tsai, S.Q., Topkar, V.V., Nguyen, N.T., Zheng, Z., Gonzales, A.P.W. et al. (2015b) Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature, 523, 481–485.
32. 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 DNA cleavage. Nature, 533, 420–424.
33. Law, J.A. and Jacobsen, S.E. (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204–220.
34. Li, J.-F., Norville, J.E., Aach, J., McCormack, M., Zhang, D., Bush, J., Church, G.M. 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.
35. Li, J., Sun, Y., Du, J., Zhao, Y. and Xia, L. (2016) Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol. Plant, 10, 526–529.
36. Liang, Z., Chen, K., Li, T., Zhang, Y., Wang, Y., Zhao, Q., Liu, J. et al. (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat. Commun. 8, 14261.
37. Liu, X.S., Wu, H., Ji, X., Stelzer, Y., Wu, X., Czauderna, S., Shu, J. et al. (2016) Editing DNA methylation in the mammalian genome. Cell, 167, 233–247.
38. Lowder, L.G., Zhang, D., Baltes, N.J., Paul, J.W., Tang, X., Zheng, X., Voytas, D.F. et al. (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol. 169, 971–985.
39. Lu, Y. and Zhu, J. (2016) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant, 10, 523–525.
40. Makarova, K.S., Grishin, N.V., Shabalina, S.A., Wolf, Y.I. and Koonin, E.V. (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct, 1, 7.
41. Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S., Costa, F., Shah, S.A., Saunders, S.J., Barrangou, R. et al. (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13, 722–736.
42. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E. et al. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823–826.
43. Malnoy, M., Viola, R., Jung, M.-H., Koo, O.-J., Kim, S., Kim, J.-S., Velasco, R. et al. (2016) DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front. Plant Sci. 7, 1904.
44. Marton, I., Zuker, A., Shklarman, E., Zeevi, V., Tovkach, A., Roffe, S., Ovadis, M. et al. (2010) Nontransgenic genome modification in plant cells. Plant Physiol. 154, 1079–1087.
45. Mei, Y., Wang, Y., Chen, H., Sun, Z.S. and Ju, X.D. (2016) Recent progress in CRISPR/Cas9 technology. J. Genet. Genom. 43, 63–75.
46. Miao, J., Guo, D., Zhang, J., Huang, Q., Qin, G., Zhang, X., Wan, J. et al. (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res. 23, 1233–1236.
47. Mikami, M., Toki, S. and Endo, M. (2016) Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant Cell Physiol. 57, 1058–1068.
48. Mojica, F.J.M., Ferrer, C., Juez, G. and Rodriguez-Valera, F. (1995) Long stretches of short tandem repeats are present in the largest replicons of the Archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning. Mol. Microbiol. 17, 85–93.
49. Mojica, F.J.M., Díez-Villaseñor, C., Soria, E. and Juez, G. (2000) Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol. Microbiol. 36, 244–246.
50. Nekrasov, V., Staskawicz, B., Weigel, D., Jones, J.D.G. and Kamoun, S. (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 691–693.
51. Nishida, K., Arazoe, T., Yachie, N., Banno, S., Kakimoto, M., Tabata, M., Mochizuki, M. et al. (2016) Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science, 353, aaf8729.
52. Perez-Pinera, P., Kocak, D.D., Vockley, C.M., Adler, A.F., Kabadi, A.M., Polstein, L.R., Thakore, P.I. et al. (2013) RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat. Methods, 10, 973–976.
53. Piatek, A., Ali, Z., Baazim, H., Li, L., Abulfaraj, A., Al-Shareef, S., Aouida, M. et al. (2015) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol. J. 13, 578–589.
54. Price, A.A., Sampson, T.R., Ratner, H.K., Grakoui, A. and Weiss, D.S. (2015) Cas9-mediated targeting of viral RNA in eukaryotic cells. Proc. Natl Acad. Sci. USA, 112, 6164–6169.
55. Pyott, D.E., Sheehan, E. and Molnar, A. (2016) Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol. Plant Pathol. 4, 1–13.
56. Qi, L.S., Larson, M.H., Gilbert, L.A., Doudna, J.A., Weissman, J.S., Arkin, A.P. and Lim, W.A. (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152, 1173–1183.
57. Ran, F.A., Hsu, P.D., Lin, C.Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., Scott, D.A. et al. (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 154, 1380–1389.
58. Ran, F.A., Cong, L., Yan, W.X., Scott, D.A., Gootenberg, J.S., Kriz, A.J., Zetsche, B. et al. (2015) In vivo genome editing using Staphylococcus aureus Cas9. Nature, 520, 186–190.
59. Rau, K. and Rentmeister, A. (2016) CRISPR/Cas9: a new tool for RNA imaging in live cells. ChemBioChem, 17, 1682–1684.
60. Sampson, T.R., Saroj, S.D., Llewellyn, A.C., Tzeng, Y. and Weiss, D.S. (2013) A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature, 497, 254–257.
61. 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.
62. Schiml, S., Fauser, F. and Puchta, H. (2016) Repair of adjacent single-strand breaks is often accompanied by the formation of tandem sequence duplications in plant genomes. Proc. Natl Acad. Sci. USA, 113, 7266–7271.
63. Shan, Q.W., Wang, Y.P., Li, J., Zhang, Y., Chen, K.L., Liang, Z., Zhang, K. et al. (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31, 686–688.
64. Shmakov, S., Abudayyeh, O.O., Makarova, K.S., Wolf, Y.I., Gootenberg, J.S., Semenova, E., Minakhin, L. et al. (2015) Discovery and functional characterization of diverse Class 2 CRISPR-Cas systems. Mol. Cell, 60, 385–397.
65. Slaymaker, I.M., Gao, L., Zetsche, B., Scott, D.A., Yan, W.X. and Zhang, F. (2016) Rationally engineered Cas9 nucleases with improved specificity. Science, 351, 84–88.
66. Song, G., Jia, M., Chen, K., Kong, X., Khattak, B., Xie, C., Li, A. et al. (2016) CRISPR/Cas9: a powerful tool for crop genome editing. Crop J. 4, 75–82.
67. Steinert, J., Schiml, S., Fauser, F. and Puchta, H. (2015) Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus. Plant J. 84, 1295–1305.
68. Subburaj, S., Chung, S.J., Lee, C., Ryu, S.M., Kim, D.H., Kim, J.S., Bae, S. et al. (2016) Site-directed mutagenesis in Petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep. 35, 1535–1544.
69. Sun, Y., Li, J. and Xia, L. (2016) Precise genome modification via sequence-specific nucleases-mediated gene targeting for crop improvement. Front. Plant Sci. 7, 1928.
70. Svitashev, S., Schwartz, C., Lenderts, B., Young, J.K. and Cigan, A.M. (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat. Commun. 7, 13274.
71. Tsai, S.Q., Wyvekens, N., Khayter, C., Foden, J.A., Thapar, V., Reyon, D., Goodwin, M.J. et al. (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32, 569–576.
72. 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.
73. Vojta, A., Dobrinic, P., Tadic, V., Bockor, L., Korac, P., Julg, B., Klasic, M. et al. (2016) Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res. 44, 5615–5628.
74. Weeks, D.P., Spalding, M.H. and Yang, B. (2016) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol. J. 14, 483–495.
75. Wiedenheft, B., Sternberg, S.H. and Doudna, J.A. (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature, 482, 331–338.
76. Wolt, J.D., Wang, K. and Yang, B. (2016) The regulatory status of genome-edited crops. Plant Biotechnol. J. 14, 510–518.
77. Woo, J.W., Kim, J., Kwon, S.I., Corvalan, C., Cho, S.W., Kim, H., Kim, S.-G. et al. (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33, 1162–1164.
78. Wright, A.V., Sternberg, S.H., Taylor, D.W., Staahl, B.T., Bardales, J.A., Kornfeld, J.E. and Doudna, J.A. (2015) Rational design of a split-Cas9 enzyme complex. Proc. Natl Acad. Sci. USA, 112, 2984–2989.
79. Xie, K. and Yang, Y. (2013) RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant, 6, 1975–1983.
80. Xu, R., Qin, R., Li, H., Li, D., Li, L., Wei, P. and Yang, J. (2016) Generation of targeted mutant rice using a CRISPR-Cpf1 system. Plant Biotechnol. J. doi: 10.1111/pbi.12669
81. Zetsche, B., Gootenberg, J.S., Abudayyeh, O.O., Slaymaker, I.M., Makarova, K.S., Essletzbichler, P., Volz, S.E. et al. (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 163, 759–771.
82. Zhang, K., Raboanatahiry, N., Zhu, B. and Li, M. (2017) Progress in genome editing technology and its application in plants. Front. Plant Sci. 8, 177.