Targeting non-coding RNAs in plants with the CRISPR-cas technology is a challenge yet worth accepting

Frontiers in Plant Science

Volumn 6, Issue NOVEMBER, 2015, Pages

  Basak, Jolly ^a   Nithin, Chandran ^b  

^a VISVA BHARATI UNIVERSITY   (India)

^b INDIAN INSTITUTE OF TECHNOLOGY   (India)

Author keywords

CRISPR Cas; Homologous recombination; LncRNA; miRNA; NHEJ; Off target mutation

Indexed keywords

EID: 84947605598     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.01001     Document Type: Review

References (78)

1. Ambros, V. (2001). microRNAs: tiny regulators with great potential. Cell 107, 823-826. doi: 10.1016/S0092-8674(01)00616-X
2. Anders, C., Niewoehner, O., Duerst, A., and Jinek, M. (2014). Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513, 569-573. doi: 10.1038/nature13579
3. Baltes, N. J., Gil-Humanes, J., Cermak, T., Atkins, P. A., and Voytas, D. F. (2014). DNA replicons for plant genome engineering. Plant Cell 26, 151-163. doi: 10.1105/tpc.113.119792
4. Barrangou, R., Birmingham, A., Wiemann, S., Beijersbergen, R. L., Hornung, V., and Smith, A. (2015). Advances in CRISPR-Cas9 genome engineering: lessons learned from RNA interference. Nucleic Acids Res. 43, 3407-3419. doi: 10.1093/nar/gkv226
5. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., et al. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science315, 1709-1712. doi: 10.1126/science.1138140
6. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell116, 281-297. doi: 10.1016/S0092-8674(04)00045-5
7. Bassett, A. R., Azzam, G., Wheatley, L., Tibbit, C., Rajakumar, T., Mcgowan, S., et al. (2014). Understanding functional miRNA-target interactions in vivo by site-specific genome engineering. Nat. Commun. 5:4640. doi: 10.1038/ncomms5640
8. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., Patron, N. J., and Nekrasov, V. (2015). Editing plant genomes with CRISPR/Cas9. Curr. Opin. Biotechnol. 32, 76-84. doi: 10.1016/j.copbio.2014.11.007
9. Bibikova, M., Beumer, K., Trautman, J. K., and Carroll, D. (2003). Enhancing gene targeting with designed zinc finger nucleases. Science 300:764. doi: 10.1126/science.1079512
10. Bortesi, L., and Fischer, R. (2015). The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33, 41-52. doi: 10.1016/j.biotechadv.2014.12.006
11. 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
12. Bushati, N., and Cohen, S. M. (2007). microRNA Functions. Annu. Rev. Cell. Dev. Biol. 23, 175-205. doi: 10.1146/annurev.cellbio.23.090506.123406
13. Carrington, J. C., and Ambros, V. (2003). Role of microRNAs in plant and animal development. Science 301, 336-338. doi: 10.1126/science.1085242
14. Carroll, D. (2011). Genome engineering with zinc-finger nucleases. Genetics 188, 773-782. doi: 10.1534/genetics.111.131433
15. Cho, S. W., Kim, S., Kim, Y., Kweon, J., Kim, H. S., Bae, S., et al. (2014). Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases.Genome Res. 24, 132-141. doi: 10.1101/gr.162339.113
16. Christian, M., Cermak, T., Doyle, E. L., Schmidt, C., Zhang, F., Hummel, A., et al. (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics186, 757-761. doi: 10.1534/genetics.110.120717
17. 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. doi: 10.1126/science.1231143
18. Consortium, T. F., Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M. C., et al. (2005). The transcriptional landscape of the mammalian genome. Science 309, 1559-1563. doi: 10.1126/science.1112014
19. Derrien, T., Johnson, R., Bussotti, G., Tanzer, A., Djebali, S., Tilgner, H., et al. (2012). The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 22, 1775-1789. doi: 10.1101/gr.132159.111
20. Dieci, G., Fiorino, G., Castelnuovo, M., Teichmann, M., and Pagano, A. (2007). The expanding RNA polymerase III transcriptome. Trends Genet. 23, 614-622. doi: 10.1016/j.tig.2007.09.001
21. Djuranovic, S., Nahvi, A., and Green, R. (2011). A parsimonious model for gene regulation by miRNAs. Science 331, 550-553. doi: 10.1126/science.1191138
22. Doench, J. G., Hartenian, E., Graham, D. B., Tothova, Z., Hegde, M., Smith, I., et al. (2014). Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol. 32, 1262-1267. doi: 10.1038/nbt.3026
23. Fatica, A., and Bozzoni, I. (2014). Long non-coding RNAs: new players in cell differentiation and development. Nat. Rev. Genet. 15, 7-21. doi: 10.1038/nrg3606
24. Feng, Z., Mao, Y., Xu, N., Zhang, B., Wei, P., Yang, D. L., et al. (2014). Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111, 4632-4637. doi: 10.1073/pnas.1400822111
25. 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
26. Fujii, W., Kawasaki, K., Sugiura, K., and Naito, K. (2013). Efficient generation of large-scale genome-modified mice using gRNA and CAS9 endonuclease. Nucleic Acids Res.41, e187. doi: 10.1093/nar/gkt772
27. Gao, J., Wang, G., Ma, S., Xie, X., Wu, X., Zhang, X., et al. (2015). CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol. Biol. 87, 99-110. doi: 10.1007/s11103-014-0263-0
28. Gilbert, L. A., Larson, M. H., Morsut, L., Liu, Z., Brar, G. A., Torres, S. E., et al. (2013). CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes.Cell 154, 442-451. doi: 10.1016/j.cell.2013.06.044
29. 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
30. Han, J., Zhang, J., Chen, L., Shen, B., Zhou, J., Hu, B., et al. (2014). Efficient in vivo deletion of a large imprinted lncRNA by CRISPR/Cas9. RNA Biol. 11, 829-835. doi: 10.4161/rna.29624
31. Hirota, K., Miyoshi, T., Kugou, K., Hoffman, C. S., Shibata, T., and Ohta, K. (2008). Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs. Nature 456, 130-134. doi: 10.1038/nature07348
32. Ho, T. T., Zhou, N., Huang, J., Koirala, P., Xu, M., Fung, R., et al. (2015). Targeting non-coding RNAs with the CRISPR/Cas9 system in human cell lines. Nucleic Acids Res. 43, e17. doi: 10.1093/nar/gku1198
33. Horvath, P., and Barrangou, R. (2010). CRISPR/Cas, the immune system of bacteria and archaea. Science 327, 167-170. doi: 10.1126/science.1179555
34. Hsu, P. D., Lander, E. S., and Zhang, F. (2014). Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262-1278. doi: 10.1016/j.cell.2014.05.010
35. 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. doi: 10.1038/nbt.2647
36. Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Kaini, P., Sander, J. D., et al. (2013a). Heritable and precise zebrafish genome editing using a CRISPR-Cas system. PLoS ONE 8:e68708. doi: 10.1371/journal.pone.0068708
37. Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., et al. (2013b). Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31, 227-229. doi: 10.1038/nbt.2501
38. Jia, H., and Wang, N. (2014). Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE 9:e93806. doi: 10.1371/journal.pone.0093806
39. Jiang, Q., Meng, X., Meng, L., Chang, N., Xiong, J., Cao, H., et al. (2014a). Small indels induced by CRISPR/Cas9 in the 5' region of microRNA lead to its depletion and Drosha processing retardance. RNA Biol. 11, 1243-1249. doi: 10.1080/15476286.2014.996067
40. Jiang, W., Yang, B., and Weeks, D. P. (2014b). Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS ONE 9:e99225. doi: 10.1371/journal.pone.0099225
41. Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B., and Weeks, D. P. (2013). Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification inArabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41, e188. doi: 10.1093/nar/gkt780
42. Jones-Rhoades, M. W., Bartel, D. P., and Bartel, B. (2006). MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19-53. doi: 10.1146/annurev.arplant.57.032905.105218
43. Joung, J. K., and Sander, J. D. (2013). TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 14, 49-55. doi: 10.1038/nrm3486
44. Jung, J.-H., Seo, P., and Park, C.-M. (2009). MicroRNA biogenesis and function in higher plants. Plant Biotechnol. Rep. 3, 111-126. doi: 10.1007/s11816-009-0085-8
45. Kidner, C. A., and Martienssen, R. A. (2005). The developmental role of microRNA in plants. Curr. Opin. Plant Biol. 8, 38-44. doi: 10.1016/j.pbi.2004.11.008
46. 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
47. Lipshitz, H., Peattie, D., and Hogness, D. (1987). Novel transcripts from the Ultrabithorax domain of the bithorax complex. Genes Dev. 1, 307-322. doi: 10.1101/gad.1.3.307
48. Lloyd, A., Plaisier, C. L., Carroll, D., and Drews, G. N. (2005). Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 102, 2232-2237. doi: 10.1073/pnas.0409339102
49. Louro, R., El-Jundi, T., Nakaya, H. I., Reis, E. M., and Verjovski-Almeida, S. (2008). Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics 92, 18-25. doi: 10.1016/j.ygeno.2008.03.013
50. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., Dicarlo, J. E., et al. (2013). RNA-guided human genome engineering via Cas9. Science 339, 823-826. doi: 10.1126/science.1232033
51. Mallory, A. C., and Vaucheret, H. (2006). Functions of microRNAs and related small RNAs in plants. Nat. Genet. 38(Suppl.), S31-S36. doi: 10.1038/ng0706-850b
52. Mariner, P. D., Walters, R. D., Espinoza, C. A., Drullinger, L. F., Wagner, S. D., Kugel, J. F., et al. (2008). Human alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol. Cell 29, 499-509. doi: 10.1016/j.molcel.2007.12.013
53. Martianov, I., Ramadass, A., Serra Barros, A., Chow, N., and Akoulitchev, A. (2007). Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445, 666-670. doi: 10.1038/nature05519
54. Mercer, T. R., Dinger, M. E., Sunkin, S. M., Mehler, M. F., and Mattick, J. S. (2008). Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. U.S.A. 105, 716-721. doi: 10.1073/pnas.0706729105
55. Mercer, T. R., and Mattick, J. S. (2013). Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 20, 300-307. doi: 10.1038/nsmb.2480
56. 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. doi: 10.1038/cr.2013.123
57. Miller, J. C., Tan, S., Qiao, G., Barlow, K. A., Wang, J., Xia, D. F., et al. (2011). A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148. doi: 10.1038/nbt.1755
58. Nguyen, V. T., Kiss, T., Michels, A. A., and Bensaude, O. (2001). 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414, 322-325. doi: 10.1038/35104581
59. Nie, L., Wu, H.-J., Hsu, J.-M., Chang, S.-S., Labaff, A. M., Li, C.-W., et al. (2012). Long non-coding RNAs: versatile master regulators of gene expression and crucial players in cancer. Am. J. Transl. Res. 4, 127-150.
60. Nithin, C., Patwa, N., Thomas, A., Bahadur, R. P., and Basak, J. (2015). Computational prediction of miRNAs and their targets in Phaseolus vulgaris using simple sequence repeat signatures. BMC Plant Biol. 15:140. doi: 10.1186/s12870-015-0516-3
61. Nodine, M. D., and Bartel, D. P. (2010). MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev. 24, 2678-2692. doi: 10.1101/gad.1986710
62. Pattanayak, V., Lin, S., Guilinger, J. P., Ma, E., Doudna, J. A., and Liu, D. R. (2013). High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843. doi: 10.1038/nbt.2673
63. Pefanis, E., Wang, J., Rothschild, G., Lim, J., Kazadi, D., Sun, J., et al. (2015). RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity. Cell 161, 774-789. doi: 10.1016/j.cell.2015.04.034
64. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., et al. (2013). Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152, 1173-1183. doi: 10.1016/j.cell.2013.02.022
65. Reyon, D., Tsai, S. Q., Khayter, C., Foden, J. A., Sander, J. D., and Joung, J. K. (2012). FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol.30, 460-465. doi: 10.1038/nbt.2170
66. Sander, J. D., and Joung, J. K. (2014). CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347-355. doi: 10.1038/nbt.2842
67. Shan, Q., Wang, Y., Li, J., and Gao, C. (2014). Genome editing in rice and wheat using the CRISPR/Cas system. Nat. Protoc. 9, 2395-2410. doi: 10.1038/nprot.2014.157
68. Shukla, V. K., Doyon, Y., Miller, J. C., Dekelver, R. C., Moehle, E. A., Worden, S. E., et al. (2009). Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459, 437-441. doi: 10.1038/nature07992
69. Tsai, S. Q., Wyvekens, N., Khayter, C., Foden, J. A., Thapar, V., Reyon, D., et al. (2014). Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32, 569-576. doi: 10.1038/nbt.2908
70. Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S., and Gregory, P. D. (2010). Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646. doi: 10.1038/nrg2842
71. Willingham, A. T., Orth, A. P., Batalov, S., Peters, E. C., Wen, B. G., Aza-Blanc, P., et al. (2005). A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 309, 1570-1573. doi: 10.1126/science.1115901
72. Wu, X.-M., Liu, M.-Y., Ge, X.-X., Xu, Q., and Guo, W.-W. (2011). Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta 233, 495-505. doi: 10.1007/s00425-010-1312-9
73. Xiao, A., Wang, Z., Hu, Y., Wu, Y., Luo, Z., Yang, Z., et al. (2013). Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res. 41, e141. doi: 10.1093/nar/gkt464
74. Yang, L., Conway, S. R., and Poethig, R. S. (2011). Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156.Development 138, 245-249. doi: 10.1242/dev.058578
75. Zhang, F., Maeder, M. L., Unger-Wallace, E., Hoshaw, J. P., Reyon, D., Christian, M., et al. (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
76. Zhao, Y., Dai, Z., Liang, Y., Yin, M., Ma, K., He, M., et al. (2014). Sequence-specific inhibition of microRNA via CRISPR/CRISPRi system. Sci. Rep. 4:3943. doi: 10.1038/srep03943
77. Zhou, H., Liu, B., Weeks, D. P., Spalding, M. H., and Yang, B. (2014). Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res. 42, 10903-10914. doi: 10.1093/nar/gku806
78. Zhu, Q. H., and Wang, M. B. (2012). Molecular functions of long non-coding RNAs in plants. Genes (Basel) 3, 176-190. doi: 10.3390/genes3010176