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Genome Editing: Advances and Prospects

  • Jaykumar Patel
  • Avinash MishraEmail author
Chapter

Abstract

There is an urgent need to develop quality crop with improved productivity and wider tolerance to the environmental (biotic and abiotic) stresses for addressing different issues including global water crisis, food security, and climate change effect on agriculture. Traditional lengthy procedures for crop improvement including classical breeding and random mutagenesis will not be able to fulfill growing crop demand in near future. Gene targeting technology is a powerful transformative procedure that permits accurate genetic modification in any genome which relies on a variety of molecular editors. Formation of directed DNA cleavage by ZFNs, TALENs, and CRISPR/Cas9, followed by restoration via the DNA repair system either by NHEJ (non-homologous end joining) or by HDR (homology directed recombination), provides a useful insight of gene function and trait modification. In this chapter, we have described the four available types of genome editing tools; meganucleases, ZFNs, TALENs, and CRISPR systems, and discussed their revolutionary applications in precision molecular breeding and functional genomics research of crops. Furthermore, specific challenges in the plant genome editing and prospects were also reviewed.

Keywords

Genome editing Meganuclease ZFNs TALENs CRISPR ABEs 

Notes

Acknowledgments

CSIR-CSMCRI Communication No.: PRIS- 140/2018. CSIR-Young Scientist (YSP-02/2016-17) and SERB-DST (EMR/2016/000538) projects are thankfully acknowledged. Author JP is thankful to UGC, Govt. of India for Junior Research Fellowship.

References

  1. Abdallah, N. A., Prakash, C. S., & McHughen, A. G. (2015). Genome editing for crop improvement: Challenges and opportunities. GM Crops & Food, 6(4), 183–205.  https://doi.org/10.1080/21645698.2015.1129937.CrossRefGoogle Scholar
  2. Abudayyeh, O. O., Gootenberg, J. S., Konermann, S., Joung, J., Slaymaker, I. M., Cox, D. B. T., Shmakov, S., Makarova, K. S., Semenova, E., Minakhin, L., Severinov, K., Regev, A., Lander, E. S., Koonin, E. V., & Zhang, F. (2016). C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science, 353(6299), aaf5573–aaf5573.  https://doi.org/10.1126/science.aaf5573.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Adli, M. (2018). The CRISPR tool kit for genome editing and beyond. Nature Communications, 9(1), 1911.  https://doi.org/10.1038/s41467-018-04252-2.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Agnieszka, P., Zahir, A., Hatoon, B., Lixin, L., Aala, A., Sahar, A.-S., Mustapha, A., & M, M. M. (2015). RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnology Journal, 13(4), 578–589.  https://doi.org/10.1111/pbi.12284.CrossRefGoogle Scholar
  5. Alagoz, Y., Gurkok, T., Zhang, B., & 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. Scientific Reports, 6, 30910.  https://doi.org/10.1038/srep30910.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ali, Z., Abulfaraj, A., Idris, A., Ali, S., Tashkandi, M., & Mahfouz, M. M. (2015). CRISPR/Cas9-mediated viral interference in plants. Genome Biology, 16(1), 238.  https://doi.org/10.1186/s13059-015-0799-6.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Andersson, M., Turesson, H., Nicolia, A., Fält, A.-S., Samuelsson, M., & Hofvander, P. (2017). Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Reports, 36(1), 117–128.  https://doi.org/10.1007/s00299-016-2062-3.CrossRefPubMedGoogle Scholar
  8. Armin, S., Felix, W., Jacqueline, B., Holger, P., & David, E. (2017). Towards CRISPR/Cas crops – bringing together genomics and genome editing. The New Phytologist, 216(3), 682–698.  https://doi.org/10.1111/nph.14702.CrossRefGoogle Scholar
  9. Bae, S., Park, J., & Kim, J.-S. (2014). Cas-OFFinder: A fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases. Bioinformatics, 30(10), 1473–1475.  https://doi.org/10.1093/bioinformatics/btu048.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Baltes, N. J., Hummel, A. W., Konecna, E., Cegan, R., Bruns, A. N., Bisaro, D. M., & Voytas, D. F. (2015). Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nature Plants, 1, 15145.  https://doi.org/10.1038/nplants.2015.145.CrossRefGoogle Scholar
  11. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A., & Horvath, P. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315(5819), 1709–1712.  https://doi.org/10.1126/science.1138140.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Begemann, M. B., Gray, B. N., January, E., Gordon, G. C., He, Y., Liu, H., Wu, X., Brutnell, T. P., Mockler, T. C., & Oufattole, M. (2017). Precise insertion and guided editing of higher plant genomes using Cpf1 CRISPR nucleases. Scientific Reports, 7(1), 11606.  https://doi.org/10.1038/s41598-017-11760-6.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bibikova, M., Carroll, D., Segal, D. J., Trautman, J. K., Smith, J., Kim, Y.-G., & Chandrasegaran, S. (2001). Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Molecular and Cellular Biology, 21(1), 289–297.CrossRefGoogle Scholar
  14. Bland, C., Ramsey, T. L., Sabree, F., Lowe, M., Brown, K., Kyrpides, N. C., & Hugenholtz, P. (2007). CRISPR recognition tool (CRT): A tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics, 8(1), 209.  https://doi.org/10.1186/1471-2105-8-209.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A., & Bonas, U. (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science, 326(5959), 1509–1512.  https://doi.org/10.1126/science.1178811.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bolotin, A., Quinquis, B., Sorokin, A., & Ehrlich, S. D. (2005). Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 151(8), 2551–2561.  https://doi.org/10.1099/mic.0.28048-0.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bortesi, L., & Fischer, R. (2015). The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnology Advances, 33(1), 41–52.  https://doi.org/10.1016/j.biotechadv.2014.12.006.CrossRefPubMedGoogle Scholar
  18. Breitler, J.-C., Dechamp, E., Campa, C., Zebral Rodrigues, L. A., Guyot, R., Marraccini, P., & Etienne, H. (2018). CRISPR/Cas9-mediated efficient targeted mutagenesis has the potential to accelerate the domestication of Coffea canephora. Plant Cell, Tissue and Organ Culture (PCTOC).  https://doi.org/10.1007/s11240-018-1429-2.
  19. Brooks, C., Nekrasov, V., Lippman, Z. B., & 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 Physiology, 166(3), 1292–1297.  https://doi.org/10.1104/pp.114.247577.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Brouns, S. J. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J. H., Snijders, A. P. L., Dickman, M. J., Makarova, K. S., Koonin, E. V., & van der Oost, J. (2008). Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321(5891), 960–964.  https://doi.org/10.1126/science.1159689.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Cai, C. Q., Doyon, Y., Ainley, W. M., Miller, J. C., DeKelver, R. C., Moehle, E. A., Rock, J. M., Lee, Y.-L., Garrison, R., Schulenberg, L., Blue, R., Worden, A., Baker, L., Faraji, F., Zhang, L., Holmes, M. C., Rebar, E. J., Collingwood, T. N., Rubin-Wilson, B., Gregory, P. D., Urnov, F. D., & Petolino, J. F. (2009). Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Molecular Biology, 69(6), 699–709.  https://doi.org/10.1007/s11103-008-9449-7.CrossRefPubMedGoogle Scholar
  22. Carpenter, J. E. (2010). Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nature Biotechnology, 28, 319–321.  https://doi.org/10.1038/nbt0410-319.
  23. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J. A., Somia, N. V., Bogdanove, A. J., & Voytas, D. F. (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Research, 39(12), e82–e82.  https://doi.org/10.1093/nar/gkr218.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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. (2013). Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 155(7), 1479–1491.  https://doi.org/10.1016/j.cell.2013.12.001.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Chen, X., Lu, X., Shu, N., Wang, S., Wang, J., Wang, D., Guo, L., & Ye, W. (2017). Targeted mutagenesis in cotton (Gossypium hirsutum L.) using the CRISPR/Cas9 system. Scientific Reports, 7, 44304.  https://doi.org/10.1038/srep44304.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Christian, M., Cermak, T., Doyle, E. L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A. J., & Voytas, D. F. (2010). Targeting DNA double-Strand breaks with TAL effector nucleases. Genetics, 186(2), 757–761.  https://doi.org/10.1534/genetics.110.120717.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Christian, J., Gina, C. G., Janina, B., Niharika, S., & Siegbert, M. (2018). Recent developments in genome editing and applications in plant breeding. Plant Breeding, 137(1), 1–9.  https://doi.org/10.1111/pbr.12526.CrossRefGoogle Scholar
  28. Clasen, B. M., Stoddard, T. J., Song, L., Demorest, Z. L., Jin, L., Frederic, C., Redeat, T., Shawn, D., RE, E., Aurelie, D., Andrew, C., Ann, Y., Adam, R., William, H., BN, J., Luc, M., Voytas, D. F., & Feng, Z. (2016). Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnology Journal, 14(1), 169–176.  https://doi.org/10.1111/pbi.12370.CrossRefPubMedGoogle Scholar
  29. Cong, L., Zhou, R., Y-c, K., Cunniff, M., & Zhang, F. (2012). Comprehensive interrogation of natural TALE DNA-binding modules and transcriptional repressor domains. Nature Communications, 3, 968.  https://doi.org/10.1038/ncomms1962.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L., & Zhang, F. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science.  https://doi.org/10.1126/science.1231143.
  31. Cradick, T. J., Qiu, P., Lee, C. M., Fine, E. J., & Bao, G. (2014). COSMID: A web-based tool for identifying and validating CRISPR/Cas off-target sites. Molecular Therapy Nucleic Acids, 3(12), e214.  https://doi.org/10.1038/mtna.2014.64.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Crawley, A. B., Henriksen, J. R., & Barrangou, R. (2018). CRISPRdisco: An automated pipeline for the discovery and analysis of CRISPR-Cas systems. The CRISPR Journal, 1(2), 171–181.  https://doi.org/10.1089/crispr.2017.0022.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Curtin, S. J., Zhang, F., Sander, J. D., Haun, W. J., Starker, C., Baltes, N. J., Reyon, D., Dahlborg, E. J., Goodwin, M. J., Coffman, A. P., Dobbs, D., Joung, J. K., Voytas, D. F., & Stupar, R. M. (2011). Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiology, 156(2), 466–473.  https://doi.org/10.1104/pp.111.172981.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Curtin, S. J., Voytas, D. F., & Stupar, R. M. (2012). Genome engineering of crops with designer nucleases. The Plant Genome, 5(2), 42–50.CrossRefGoogle Scholar
  35. de Toledo Thomazella, D. P., Brail, Q., Dahlbeck, D., & Staskawicz, B. J. (2016). CRISPR-Cas9 mediated mutagenesis of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. bioRxiv.  https://doi.org/10.1101/064824.
  36. Demorest, Z. L., Coffman, A., Baltes, N. J., Stoddard, T. J., Clasen, B. M., Luo, S., Retterath, A., Yabandith, A., Gamo, M. E., Bissen, J., Mathis, L., Voytas, D. F., & Zhang, F. (2016). Direct stacking of sequence-specific nuclease-induced mutations to produce high oleic and low linolenic soybean oil. BMC Plant Biology, 16(1), 225.  https://doi.org/10.1186/s12870-016-0906-1.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Deng, D., Yan, C., Pan, X., Mahfouz, M., Wang, J., Zhu, J.-K., Shi, Y., & Yan, N. (2012). Structural basis for sequence-specific recognition of DNA by TAL effectors. Science, 335(6069), 720–723.  https://doi.org/10.1126/science.1215670.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Deng, W., Rupon, J. W., Krivega, I., Breda, L., Motta, I., Jahn, K. S., Reik, A., Gregory, P. D., Rivella, S., Dean, A., & Blobel, G. A. (2014). Reactivation of developmentally silenced globin genes by forced chromatin looping. Cell, 158(4), 849–860.  https://doi.org/10.1016/j.cell.2014.05.050.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Deng, W., Shi, X., Tjian, R., Lionnet, T., & Singer, R. H. (2015). CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proceedings of the National Academy of Sciences, 112(38), 11870–11875.  https://doi.org/10.1073/pnas.1515692112.CrossRefGoogle Scholar
  40. Durr, J., Papareddy, R., Nakajima, K., & Gutierrez-Marcos, J. (2018). Highly efficient heritable targeted deletions of gene clusters and non-coding regulatory regions in Arabidopsis using CRISPR/Cas9. Scientific Reports, 8(1), 4443.  https://doi.org/10.1038/s41598-018-22667-1.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Engler, C., Gruetzner, R., Kandzia, R., & Marillonnet, S. (2009). Golden gate shuffling: A one-pot DNA shuffling method based on type IIs restriction enzymes. PLoS One, 4(5), e5553.CrossRefGoogle Scholar
  42. Fan, D., Liu, T., Li, C., Jiao, B., Li, S., Hou, Y., & Luo, K. (2015). Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Scientific Reports, 5, 12217.  https://doi.org/10.1038/srep12217.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D.-L., Wei, P., Cao, F., Zhu, S., Zhang, F., Mao, Y., & Zhu, J.-K. (2013). Efficient genome editing in plants using a CRISPR/Cas system. Cell Research, 23, 1229.  https://doi.org/10.1038/cr.2013.114.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Feng, Z., Mao, Y., Xu, N., Zhang, B., Wei, P., Yang, D.-L., Wang, Z., Zhang, Z., Zheng, R., Yang, L., Zeng, L., Liu, X., & Zhu, J.-K. (2014). Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in <em>Arabidopsis</em>. Proceedings of the National Academy of Sciences.  https://doi.org/10.1073/pnas.1400822111.
  45. Fonfara, I., Richter, H., Bratovič, M., Le Rhun, A., & Charpentier, E. (2016). The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature, 532, 517.  https://doi.org/10.1038/nature17945.CrossRefPubMedGoogle Scholar
  46. Frederic, P., & Philippe, D. (2007). Meganucleases and DNA double-strand break-induced recombination: Perspectives for gene therapy. Current Gene Therapy, 7(1), 49–66.  https://doi.org/10.2174/156652307779940216.CrossRefGoogle Scholar
  47. Gao, R., Feyissa, B. A., Croft, M., & Hannoufa, A. (2018). Gene editing by CRISPR/Cas9 in the obligatory outcrossing Medicago sativa. Planta, 247(4), 1043–1050.  https://doi.org/10.1007/s00425-018-2866-1.CrossRefPubMedGoogle Scholar
  48. Garneau, J. E., Dupuis, M.-È., Villion, M., Romero, D. A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A. H., & Moineau, S. (2010). The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 468, 67.  https://doi.org/10.1038/nature09523.CrossRefGoogle Scholar
  49. Gasiunas, G., Barrangou, R., Horvath, P., & Siksnys, V. (2012). Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proceedings of the National Academy of Sciences, 109(39), E2579–E2586.  https://doi.org/10.1073/pnas.1208507109.CrossRefGoogle Scholar
  50. Haft, D. H., Selengut, J., Mongodin, E. F., & Nelson, K. E. (2005). A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Computational Biology, 1(6), e60.  https://doi.org/10.1371/journal.pcbi.0010060.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hao, N., Shearwin, K. E., & Dodd, I. B. (2017). Programmable DNA looping using engineered bivalent dCas9 complexes. Nature Communications, 8(1), 1628.  https://doi.org/10.1038/s41467-017-01873-x.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hess, G. T., Frésard, L., Han, K., Lee, C. H., Li, A., Cimprich, K. A., Montgomery, S. B., & Bassik, M. C. (2016). Directed evolution using dCas9-targeted somatic hypermutation in mammalian cells. Nature Methods, 13, 1036.  https://doi.org/10.1038/nmeth.4038.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Hilton, I. B., D’Ippolito, A. M., Vockley, C. M., Thakore, P. I., Crawford, G. E., Reddy, T. E., & Gersbach, C. A. (2015). Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nature Biotechnology, 33, 510.  https://doi.org/10.1038/nbt.3199.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Hochstrasser, M. L., Taylor, D. W., Bhat, P., Guegler, C. K., Sternberg, S. H., Nogales, E., & Doudna, J. A. (2014). CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. Proceedings of the National Academy of Sciences, 111(18), 6618–6623.  https://doi.org/10.1073/pnas.1405079111.CrossRefGoogle Scholar
  55. Hongge, J., Yunzeng, Z., Vladimir, O., Jin, X., White, F. F., Jones, J. B., & Nian, W. (2017). Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnology Journal, 15(7), 817–823.  https://doi.org/10.1111/pbi.12677.CrossRefGoogle Scholar
  56. Hua, K., Tao, X., Yuan, F., Wang, D., & Zhu, J.-K. (2018). Precise A·T to G·C base editing in the rice genome. Molecular Plant, 11(4), 627–630.  https://doi.org/10.1016/j.molp.2018.02.007.CrossRefPubMedGoogle Scholar
  57. Iaffaldano, B., Zhang, Y., & Cornish, K. (2016). CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection. Industrial Crops and Products, 89, 356–362.  https://doi.org/10.1016/j.indcrop.2016.05.029.CrossRefGoogle Scholar
  58. Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., & Nakata, A. (1987). Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. Journal of Bacteriology, 169(12), 5429–5433.CrossRefGoogle Scholar
  59. Ito, Y., Nishizawa-Yokoi, A., Endo, M., Mikami, M., & Toki, S. (2015). CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochemical and Biophysical Research Communications, 467(1), 76–82.  https://doi.org/10.1016/j.bbrc.2015.09.117.CrossRefPubMedGoogle Scholar
  60. Jacquier, A., & Dujon, B. (1985). An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell, 41(2), 383–394.  https://doi.org/10.1016/S0092-8674(85)80011-8.CrossRefPubMedGoogle Scholar
  61. Jeyabharathy, C., Marina, B., Dalia, W., Diana, L., Chen, K., Mali, P., Amir, S., Tzahi, A., & Amit, G.-O. (2016). Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Molecular Plant Pathology, 17(7), 1140–1153.  https://doi.org/10.1111/mpp.12375.CrossRefGoogle Scholar
  62. Ji, X., Zhang, H., Zhang, Y., Wang, Y., & Gao, C. (2015). Establishing a CRISPR–Cas-like immune system conferring DNA virus resistance in plants. Nature Plants, 1, 15144.  https://doi.org/10.1038/nplants.2015.144.CrossRefPubMedGoogle Scholar
  63. Jia, H., & Wang, N. (2017). Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One, 9(4), e93806.  https://doi.org/10.1371/journal.pone.0093806.CrossRefGoogle Scholar
  64. Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B., & Weeks, D. P. (2013). Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Research, 41(20), e188–e188.  https://doi.org/10.1093/nar/gkt780.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012). A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science.  https://doi.org/10.1126/science.1225829.
  66. Jinrui, S., Huirong, G., Hongyu, W., Renee, L. H., AR, L., Meizhu, Y., HS, M., Hua, M., & HJ, E. (2017). ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnology Journal, 15(2), 207–216.  https://doi.org/10.1111/pbi.12603.CrossRefGoogle Scholar
  67. Jung, J. H., & Altpeter, F. (2016). TALEN mediated targeted mutagenesis of the caffeic acid O-methyltransferase in highly polyploid sugarcane improves cell wall composition for production of bioethanol. Plant Molecular Biology, 92(1), 131–142.  https://doi.org/10.1007/s11103-016-0499-y.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Junhui, Z., Guoming, W., & Zhongchi, L. (2018). Efficient genome editing of wild strawberry genes, vector development and validation. Plant Biotechnology Journal, 0(0).  https://doi.org/10.1111/pbi.12922.
  69. Kang, B.-C., Yun, J.-Y., Kim, S.-T., Shin, Y., Ryu, J., Choi, M., Woo, J. W., & Kim, J.-S. (2018). Precision genome engineering through adenine base editing in plants. Nature Plants, 4(7), 427–431.  https://doi.org/10.1038/s41477-018-0178-x.CrossRefPubMedGoogle Scholar
  70. Kaur, N., Alok, A., Shivani, K. N., Pandey, P., Awasthi, P., & Tiwari, S. (2018). CRISPR/Cas9-mediated efficient editing in phytoene desaturase (PDS) demonstrates precise manipulation in banana cv. Rasthali genome. Functional & Integrative Genomics, 18(1), 89–99.  https://doi.org/10.1007/s10142-017-0577-5.CrossRefGoogle Scholar
  71. Kay, S., & Bonas, U. (2009). How Xanthomonas type III effectors manipulate the host plant. Current Opinion in Microbiology, 12(1), 37–43.  https://doi.org/10.1016/j.mib.2008.12.006.CrossRefPubMedGoogle Scholar
  72. Kay, S., Hahn, S., Marois, E., Hause, G., & Bonas, U. (2007). A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science, 318(5850), 648–651.  https://doi.org/10.1126/science.1144956.CrossRefPubMedGoogle Scholar
  73. Kelliher, T., Starr, D., Richbourg, L., Chintamanani, S., Delzer, B., Nuccio, M. L., Green, J., Chen, Z., McCuiston, J., Wang, W., Liebler, T., Bullock, P., & Martin, B. (2017). MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature, 542, 105.  https://doi.org/10.1038/nature20827.CrossRefPubMedGoogle Scholar
  74. Kim, D., Kim, J., Hur, J. K., Been, K. W., S-h, Y., & Kim, J.-S. (2016a). Genome-wide analysis reveals specificities of Cpf1 endonucleases in human cells. Nature Biotechnology, 34, 863.  https://doi.org/10.1038/nbt.3609.CrossRefPubMedGoogle Scholar
  75. Kim, H. K., Song, M., Lee, J., Menon, A. V., Jung, S., Kang, Y.-M., Choi, J. W., Woo, E., Koh, H. C., Nam, J.-W., & Kim, H. (2016b). In vivo high-throughput profiling of CRISPR–Cpf1 activity. Nature Methods, 14, 153.  https://doi.org/10.1038/nmeth.4104.CrossRefPubMedGoogle Scholar
  76. Kim, H., Kim, S.-T., Ryu, J., Kang, B.-C., Kim, J.-S., & Kim, S.-G. (2017a). CRISPR/Cpf1-mediated DNA-free plant genome editing. Nature Communications, 8, 14406.  https://doi.org/10.1038/ncomms14406.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Kim, Y. B., Komor, A. C., Levy, J. M., Packer, M. S., Zhao, K. T., & Liu, D. R. (2017b). Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nature Biotechnology, 35, 371.  https://doi.org/10.1038/nbt.3803.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Klimek-Chodacka, M., Oleszkiewicz, T., Lowder, L. G., Qi, Y., & Baranski, R. (2018). Efficient CRISPR/Cas9-based genome editing in carrot cells. Plant Cell Reports, 37(4), 575–586.  https://doi.org/10.1007/s00299-018-2252-2.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Klug, A., & Rhodes, D. (1987). ‘Zinc fingers’: A novel protein motif for nucleic acid recognition. Trends in Biochemical Sciences, 12, 464–469.  https://doi.org/10.1016/0968-0004(87)90231-3.CrossRefGoogle Scholar
  80. Komor, A. C., Kim, Y. B., Packer, M. S., Zuris, J. A., & Liu, D. R. (2016). Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature, 533, 420.  https://doi.org/10.1038/nature17946.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Labun, K., Montague, T. G., Gagnon, J. A., Thyme, S. B., & Valen, E. (2016). CHOPCHOP v2: A web tool for the next generation of CRISPR genome engineering. Nucleic Acids Research, 44(W1), W272–W276.  https://doi.org/10.1093/nar/gkw398.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Labun, K., Guo, X., Chavez, A., Church, G., Gagnon, J. A., & Valen, E. (2018). Accurate analysis of genuine CRISPR editing events with ampliCan. bioRxiv.  https://doi.org/10.1101/249474.
  83. Lawrenson, T., Shorinola, O., Stacey, N., Li, C., Østergaard, L., Patron, N., Uauy, C., & Harwood, W. (2015). Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biology, 16(1), 258.  https://doi.org/10.1186/s13059-015-0826-7.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Li, T., Liu, B., Spalding, M. H., Weeks, D. P., & Yang, B. (2012). High-efficiency TALEN-based gene editing produces disease-resistant rice. Nature Biotechnology, 30, 390.  https://doi.org/10.1038/nbt.2199.CrossRefPubMedGoogle Scholar
  85. Li, J.-F., Norville, J. E., Aach, J., McCormack, M., Zhang, D., Bush, J., Church, G. M., & Sheen, J. (2013). Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology, 31(8), 688.CrossRefGoogle Scholar
  86. Li, Z., Liu, Z.-B., Xing, A., Moon, B. P., Koellhoffer, J. P., Huang, L., Ward, R. T., Clifton, E., Falco, S. C., & Cigan, A. M. (2015). Cas9-guide RNA directed genome editing in soybean. Plant Physiology.  https://doi.org/10.1104/pp.15.00783.
  87. Li, J., Sun, Y., Du, J., Zhao, Y., & Xia, L. (2017). Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Molecular Plant, 10(3), 526–529.  https://doi.org/10.1016/j.molp.2016.12.001.CrossRefPubMedGoogle Scholar
  88. Li, S., Zhang, X., Wang, W., Guo, X., Wu, Z., Du, W., Zhao, Y., & Xia, L. (2018). Expanding the scope of CRISPR/Cpf1-mediated genome editing in rice. Molecular Plant, 11(7), 995–998.  https://doi.org/10.1016/j.molp.2018.03.009.CrossRefPubMedGoogle Scholar
  89. Liang, F.-S., Ho, W. Q., & Crabtree, G. R. (2011). Engineering the ABA plant stress pathway for regulation of induced proximity. Science Signaling, 4(164), rs2–rs2.  https://doi.org/10.1126/scisignal.2001449.CrossRefPubMedPubMedCentralGoogle Scholar
  90. Liang, Z., Chen, K., Li, T., Zhang, Y., Wang, Y., Zhao, Q., Liu, J., Zhang, H., Liu, C., Ran, Y., & Gao, C. (2017). Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nature Communications, 8, 14261.  https://doi.org/10.1038/ncomms14261.CrossRefPubMedPubMedCentralGoogle Scholar
  91. Liang, Z., Chen, K., Zhang, Y., Liu, J., Yin, K., Qiu, J.-L., & Gao, C. (2018). Genome editing of bread wheat using biolistic delivery of CRISPR/Cas9 in vitro transcripts or ribonucleoproteins. Nature Protocols, 13, 413.  https://doi.org/10.1038/nprot.2017.145.CrossRefPubMedGoogle Scholar
  92. Lopez-Obando, M., Hoffmann, B., Géry, C., Guyon-Debast, A., Téoulé, E., Rameau, C., Bonhomme, S., & Nogué, F. (2016). Simple and efficient targeting of multiple genes through CRISPR-Cas9 in <em>Physcomitrella patens</em>. G3: Genes|Genomes|Genetics, 6(11), 3647–3653.  https://doi.org/10.1534/g3.116.033266.CrossRefPubMedPubMedCentralGoogle Scholar
  93. Lowder, L. G., Paul, J. W., Baltes, N. J., Voytas, D. F., Zhang, Y., Zhang, D., Tang, X., Zheng, X., Hsieh, T.-F., & Qi, Y. (2015). A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiology.  https://doi.org/10.1104/pp.15.00636.
  94. Lu, Y., & Zhu, J.-K. (2017). Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Molecular Plant, 10(3), 523–525.  https://doi.org/10.1016/j.molp.2016.11.013.CrossRefPubMedGoogle Scholar
  95. Ma, H., Naseri, A., Reyes-Gutierrez, P., Wolfe, S. A., Zhang, S., & Pederson, T. (2015). Multicolor CRISPR labeling of chromosomal loci in human cells. Proceedings of the National Academy of Sciences.  https://doi.org/10.1073/pnas.1420024112.
  96. Ma, J., Köster, J., Qin, Q., Hu, S., Li, W., Chen, C., Cao, Q., Wang, J., Mei, S., Liu, Q., Xu, H., & Liu, X. S. (2016a). CRISPR-DO for genome-wide CRISPR design and optimization. Bioinformatics, 32(21), 3336–3338.  https://doi.org/10.1093/bioinformatics/btw476.CrossRefPubMedPubMedCentralGoogle Scholar
  97. Ma, Y., Zhang, J., Yin, W., Zhang, Z., Song, Y., & Chang, X. (2016b). Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nature Methods, 13, 1029.  https://doi.org/10.1038/nmeth.4027.CrossRefPubMedGoogle Scholar
  98. Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F. J. M., Wolf, Y. I., Yakunin, A. F., van der Oost, J., & Koonin, E. V. (2011). Evolution and classification of the CRISPR–Cas systems. Nature Reviews Microbiology, 9, 467.  https://doi.org/10.1038/nrmicro2577.CrossRefPubMedGoogle Scholar
  99. Makarova, K. S., Wolf, Y. I., Alkhnbashi, O. S., Costa, F., Shah, S. A., Saunders, S. J., Barrangou, R., Brouns, S. J. J., Charpentier, E., Haft, D. H., Horvath, P., Moineau, S., Mojica, F. J. M., Terns, R. M., Terns, M. P., White, M. F., Yakunin, A. F., Garrett, R. A., van der Oost, J., Backofen, R., & Koonin, E. V. (2015). An updated evolutionary classification of CRISPR–Cas systems. Nature Reviews Microbiology, 13, 722.  https://doi.org/10.1038/nrmicro3569.CrossRefPubMedPubMedCentralGoogle Scholar
  100. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., & Church, G. M. (2013). RNA-guided human genome engineering via Cas9. Science, 339(6121), 823–826.  https://doi.org/10.1126/science.1232033.CrossRefPubMedPubMedCentralGoogle Scholar
  101. Mao, Y., Zhang, H., Xu, N., Zhang, B., Gou, F., & Zhu, J.-K. (2013). Application of the CRISPR–Cas system for efficient genome engineering in plants. Molecular Plant, 6(6), 2008–2011.  https://doi.org/10.1093/mp/sst121.CrossRefPubMedPubMedCentralGoogle Scholar
  102. Marraffini, L. A., & Sontheimer, E. J. (2008). CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science, 322(5909), 1843–1845.  https://doi.org/10.1126/science.1165771.CrossRefPubMedPubMedCentralGoogle Scholar
  103. Mercx, S., Tollet, J., Magy, B., Navarre, C., & Boutry, M. (2016). Gene inactivation by CRISPR-Cas9 in Nicotiana tabacum BY-2 suspension cells. Frontiers in Plant Science, 7(40).  https://doi.org/10.3389/fpls.2016.00040.
  104. Miao, J., Guo, D., Zhang, J., Huang, Q., Qin, G., Zhang, X., Wan, J., Gu, H., & Qu, L.-J. (2013). Targeted mutagenesis in rice using CRISPR-Cas system. Cell Research, 23, 1233.  https://doi.org/10.1038/cr.2013.123.CrossRefPubMedPubMedCentralGoogle Scholar
  105. Michno, J.-M., Wang, X., Liu, J., Curtin, S. J., Kono, T. J. Y., & Stupar, R. M. (2015). CRISPR/Cas mutagenesis of soybean and Medicago truncatula using a new web-tool and a modified Cas9 enzyme. GM Crops & Food, 6(4), 243–252.  https://doi.org/10.1080/21645698.2015.1106063.CrossRefGoogle Scholar
  106. Miller, J. C., Holmes, M. C., Wang, J., Guschin, D. Y., Lee, Y.-L., Rupniewski, I., Beausejour, C. M., Waite, A. J., Wang, N. S., Kim, K. A., Gregory, P. D., Pabo, C. O., & Rebar, E. J. (2007). An improved zinc-finger nuclease architecture for highly specific genome editing. Nature Biotechnology, 25, 778.  https://doi.org/10.1038/nbt1319.CrossRefPubMedGoogle Scholar
  107. 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. (2010). A TALE nuclease architecture for efficient genome editing. Nature Biotechnology, 29, 143.  https://doi.org/10.1038/nbt.1755.CrossRefPubMedGoogle Scholar
  108. Miller, J. C., Zhang, L., Xia, D. F., Campo, J. J., Ankoudinova, I. V., Guschin, D. Y., Babiarz, J. E., Meng, X., Hinkley, S. J., Lam, S. C., Paschon, D. E., Vincent, A. I., Dulay, G. P., Barlow, K. A., Shivak, D. A., Leung, E., Kim, J. D., Amora, R., Urnov, F. D., Gregory, P. D., & Rebar, E. J. (2015). Improved specificity of TALE-based genome editing using an expanded RVD repertoire. Nature Methods, 12, 465.  https://doi.org/10.1038/nmeth.3330.CrossRefPubMedGoogle Scholar
  109. Mojica, F. J., Ferrer, C., Juez, G., & Rodríguez-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. Molecular Microbiology, 17(1), 85–93.  https://doi.org/10.1111/j.1365-2958.1995.mmi_17010085.x.CrossRefPubMedGoogle Scholar
  110. Mojica, F. J. M., Díez-Villaseñor, C. S., García-Martínez, J., & Soria, E. (2005). Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. Journal of Molecular Evolution, 60(2), 174–182.  https://doi.org/10.1007/s00239-004-0046-3.CrossRefPubMedGoogle Scholar
  111. Mojica, F. J. M., Díez-Villaseñor, C., García-Martínez, J., & Almendros, C. (2009). Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology, 155(3), 733–740.  https://doi.org/10.1099/mic.0.023960-0.CrossRefPubMedGoogle Scholar
  112. Montague, T. G., Cruz, J. M., Gagnon, J. A., Church, G. M., & Valen, E. (2014). CHOPCHOP: A CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Research, 42(W1), W401–W407.  https://doi.org/10.1093/nar/gku410.CrossRefPubMedPubMedCentralGoogle Scholar
  113. Morgan, S. L., Mariano, N. C., Bermudez, A., Arruda, N. L., Wu, F., Luo, Y., Shankar, G., Jia, L., Chen, H., Hu, J.-F., Hoffman, A. R., Huang, C.-C., Pitteri, S. J., & Wang, K. C. (2017). Manipulation of nuclear architecture through CRISPR-mediated chromosomal looping. Nature Communications, 8, 15993.  https://doi.org/10.1038/ncomms15993.CrossRefPubMedPubMedCentralGoogle Scholar
  114. Moscou, M. J., & Bogdanove, A. J. (2009). A simple cipher governs DNA recognition by TAL effectors. Science, 326(5959), 1501–1501.  https://doi.org/10.1126/science.1178817.CrossRefPubMedPubMedCentralGoogle Scholar
  115. Nekrasov, V., Staskawicz, B., Weigel, D., Jones, J. D., & Kamoun, S. (2013). Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nature Biotechnology, 31(8), 691.CrossRefGoogle Scholar
  116. Nishida, K., Arazoe, T., Yachie, N., Banno, S., Kakimoto, M., Tabata, M., Mochizuki, M., Miyabe, A., Araki, M., Hara, K. Y., Shimatani, Z., & Kondo, A. (2016). Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science, 353(6305), aaf8729.  https://doi.org/10.1126/science.aaf8729.CrossRefPubMedGoogle Scholar
  117. Nishitani, C., Hirai, N., Komori, S., Wada, M., Okada, K., Osakabe, K., Yamamoto, T., & Osakabe, Y. (2016). Efficient genome editing in apple using a CRISPR/Cas9 system. Scientific Reports, 6, 31481.  https://doi.org/10.1038/srep31481.CrossRefPubMedPubMedCentralGoogle Scholar
  118. Ochiai, H., Sugawara, T., & Yamamoto, T. (2015). Simultaneous live imaging of the transcription and nuclear position of specific genes. Nucleic Acids Research, 43(19), e127–e127.  https://doi.org/10.1093/nar/gkv624.CrossRefPubMedPubMedCentralGoogle Scholar
  119. Okuzaki, A., Ogawa, T., Koizuka, C., Kaneko, K., Inaba, M., Imamura, J., & Koizuka, N. (2018). CRISPR/Cas9-mediated genome editing of the fatty acid desaturase 2 gene in Brassica napus. Plant Physiology and Biochemistry.  https://doi.org/10.1016/j.plaphy.2018.04.025.
  120. Osakabe, K., Osakabe, Y., & Toki, S. (2010). Site-directed mutagenesis in <em>Arabidopsis</em> using custom-designed zinc finger nucleases. Proceedings of the National Academy of Sciences, 107(26), 12034–12039.  https://doi.org/10.1073/pnas.1000234107.CrossRefGoogle Scholar
  121. Park, J., Bae, S., & Kim, J.-S. (2015). Cas-designer: A web-based tool for choice of CRISPR-Cas9 target sites. Bioinformatics, 31(24), 4014–4016.  https://doi.org/10.1093/bioinformatics/btv537.CrossRefPubMedGoogle Scholar
  122. Pengcheng, W., Jun, Z., Lin, S., Yizan, M., Jiao, X., Sijia, L., Jinwu, D., Jiafu, T., Qinghua, Z., Lili, T., Henry, D., Shuangxia, J., & Xianlong, Z. (2018). High efficient multisites genome editing in allotetraploid cotton (Gossypium hirsutum) using CRISPR/Cas9 system. Plant Biotechnology Journal, 16(1), 137–150.  https://doi.org/10.1111/pbi.12755.CrossRefGoogle Scholar
  123. Porteus, M. H., & Baltimore, D. (2003). Chimeric nucleases stimulate gene targeting in human cells. Science, 300(5620), 763–763.  https://doi.org/10.1126/science.1078395.CrossRefPubMedGoogle Scholar
  124. Pourcel, C., Salvignol, G., & Vergnaud, G. (2005). CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology, 151(3), 653–663.  https://doi.org/10.1099/mic.0.27437-0.CrossRefPubMedGoogle Scholar
  125. Puchta, H., & Fauser, F. (2013). Gene targeting in plants: 25 years later. The International Journal of Developmental Biology, 57(6-7-8), 629–637.CrossRefGoogle Scholar
  126. Puchta, H., Dujon, B., & Hohn, B. (1993). Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. Nucleic Acids Research, 21(22), 5034–5040.CrossRefGoogle Scholar
  127. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., & Lim, W. A. (2013). Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152(5), 1173–1183.  https://doi.org/10.1016/j.cell.2013.02.022.CrossRefPubMedPubMedCentralGoogle Scholar
  128. Qiwei, S., Yi, Z., Kunling, C., Kang, Z., & Caixia, G. (2015). Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnology Journal, 13(6), 791–800.  https://doi.org/10.1111/pbi.12312.CrossRefGoogle Scholar
  129. Ramirez, C. L., Foley, J. E., Wright, D. A., Müller-Lerch, F., Rahman, S. H., Cornu, T. I., Winfrey, R. J., Sander, J. D., Fu, F., Townsend, J. A., Cathomen, T., Voytas, D. F., & Joung, J. K. (2008). Unexpected failure rates for modular assembly of engineered zinc fingers. Nature Methods, 5, 374.  https://doi.org/10.1038/nmeth0508-374.CrossRefPubMedGoogle Scholar
  130. Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., & Zhang, F. (2013). Genome engineering using the CRISPR-Cas9 system. Nature Protocols, 8, 2281.  https://doi.org/10.1038/nprot.2013.143.CrossRefPubMedPubMedCentralGoogle Scholar
  131. Ren, C., Liu, X., Zhang, Z., Wang, Y., Duan, W., Li, S., & Liang, Z. (2016). CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.). Scientific Reports, 6, 32289.  https://doi.org/10.1038/srep32289.CrossRefPubMedPubMedCentralGoogle Scholar
  132. Ren, B., Yan, F., Kuang, Y., Li, N., Zhang, D., Lin, H., & Zhou, H. (2017). A CRISPR/Cas9 toolkit for efficient targeted base editing to induce genetic variations in rice. Science China Life Sciences, 60(5), 516–519.  https://doi.org/10.1007/s11427-016-0406-x.CrossRefPubMedGoogle Scholar
  133. Reyon, D., Tsai, S. Q., Khayter, C., Foden, J. A., Sander, J. D., & Joung, J. K. (2012). FLASH assembly of TALENs for high-throughput genome editing. Nature Biotechnology, 30, 460.  https://doi.org/10.1038/nbt.2170.CrossRefPubMedPubMedCentralGoogle Scholar
  134. Ruud, J., van Embden, J. D., Gaastra, W., & Schouls, L. M. (2002). Identification of genes that are associated with DNA repeats in prokaryotes. Molecular Microbiology, 43(6), 1565–1575.  https://doi.org/10.1046/j.1365-2958.2002.02839.x.CrossRefGoogle Scholar
  135. Sander, J. D., Dahlborg, E. J., Goodwin, M. J., Cade, L., Zhang, F., Cifuentes, D., Curtin, S. J., Blackburn, J. S., Thibodeau-Beganny, S., Qi, Y., Pierick, C. J., Hoffman, E., Maeder, M. L., Khayter, C., Reyon, D., Dobbs, D., Langenau, D. M., Stupar, R. M., Giraldez, A. J., Voytas, D. F., Peterson, R. T., Yeh, J.-R. J., & Joung, J. K. (2010). Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nature Methods, 8, 67.  https://doi.org/10.1038/nmeth.1542.CrossRefPubMedPubMedCentralGoogle Scholar
  136. Sander, J. D., Cade, L., Khayter, C., Reyon, D., Peterson, R. T., Joung, J. K., & Yeh, J.-R. J. (2011). Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nature Biotechnology, 29, 697.  https://doi.org/10.1038/nbt.1934.CrossRefPubMedPubMedCentralGoogle Scholar
  137. Sanjana, N. E., Cong, L., Zhou, Y., Cunniff, M. M., Feng, G., & Zhang, F. (2012). A transcription activator-like effector toolbox for genome engineering. Nature Protocols, 7, 171.  https://doi.org/10.1038/nprot.2011.431.CrossRefPubMedPubMedCentralGoogle Scholar
  138. Sauer, N. J., Narváez-Vásquez, J., Mozoruk, J., Miller, R. B., Warburg, Z. J., Woodward, M. J., Mihiret, Y. A., Lincoln, T. A., Segami, R. E., Sanders, S. L., Walker, K. A., Beetham, P. R., Schöpke, C. R., & Gocal, G. F. (2016). Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiology.  https://doi.org/10.1104/pp.15.01696.
  139. Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., Zhang, K., Liu, J., Xi, J. J., Qiu, J.-L., & Gao, C. (2013). Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology, 31, 686.  https://doi.org/10.1038/nbt.2650.CrossRefPubMedGoogle Scholar
  140. Shibuya, K., Watanabe, K., & Ono, M. (2018). CRISPR/Cas9-mediated mutagenesis of the EPHEMERAL1 locus that regulates petal senescence in Japanese morning glory. Plant Physiology and Biochemistry.  https://doi.org/10.1016/j.plaphy.2018.04.036.
  141. Shimatani, Z., Kashojiya, S., Takayama, M., Terada, R., Arazoe, T., Ishii, H., Teramura, H., Yamamoto, T., Komatsu, H., Miura, K., Ezura, H., Nishida, K., Ariizumi, T., & Kondo, A. (2017). Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nature Biotechnology, 35, 441.  https://doi.org/10.1038/nbt.3833.CrossRefPubMedGoogle Scholar
  142. Shmakov, S., Abudayyeh, O. O., Makarova, K. S., Wolf, Y. I., Gootenberg, J. S., Semenova, E., Minakhin, L., Joung, J., Konermann, S., Severinov, K., Zhang, F., & Koonin, E. V. (2015). Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Molecular Cell, 60(3), 385–397.  https://doi.org/10.1016/j.molcel.2015.10.008.CrossRefPubMedPubMedCentralGoogle Scholar
  143. Smargon, A. A., Cox, D. B. T., Pyzocha, N. K., Zheng, K., Slaymaker, I. M., Gootenberg, J. S., Abudayyeh, O. A., Essletzbichler, P., Shmakov, S., Makarova, K. S., Koonin, E. V., & Zhang, F. (2017). Cas13b is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Molecular Cell, 65(4), 618–630.e617.  https://doi.org/10.1016/j.molcel.2016.12.023.CrossRefPubMedPubMedCentralGoogle Scholar
  144. Smith, J., Grizot, S., Arnould, S., Duclert, A., Epinat, J.-C., Chames, P., Prieto, J., Redondo, P., Blanco, F. J., Bravo, J., Montoya, G., Pâques, F., & Duchateau, P. (2006). A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Research, 34(22), e149–e149.  https://doi.org/10.1093/nar/gkl720.CrossRefPubMedPubMedCentralGoogle Scholar
  145. Songstad, D. D., Petolino, J. F., Voytas, D. F., & Reichert, N. A. (2017). Genome editing of plants. Critical Reviews in Plant Sciences, 36(1), 1–23.  https://doi.org/10.1080/07352689.2017.1281663.CrossRefGoogle Scholar
  146. Stemmer, M., Thumberger, T., del Sol, K. M., Wittbrodt, J., & Mateo, J. L. (2015). CCTop: An intuitive, flexible and reliable CRISPR/Cas9 target prediction tool. PLoS One, 10(4), e0124633.  https://doi.org/10.1371/journal.pone.0124633.CrossRefPubMedPubMedCentralGoogle Scholar
  147. Stoddard, B. L. (2011). Homing endonucleases: From microbial genetic invaders to reagents for targeted DNA modification. Structure, 19(1), 7–15.  https://doi.org/10.1016/j.str.2010.12.003.CrossRefPubMedPubMedCentralGoogle Scholar
  148. Streubel, J., Blücher, C., Landgraf, A., & Boch, J. (2012). TAL effector RVD specificities and efficiencies. Nature Biotechnology, 30, 593.  https://doi.org/10.1038/nbt.2304.CrossRefPubMedGoogle Scholar
  149. Sugano, S. S., Shirakawa, M., Takagi, J., Matsuda, Y., Shimada, T., Hara-Nishimura, I., & Kohchi, T. (2014). CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant and Cell Physiology, 55(3), 475–481.  https://doi.org/10.1093/pcp/pcu014.CrossRefPubMedGoogle Scholar
  150. Sun, Y., Jiao, G., Liu, Z., Zhang, X., Li, J., Guo, X., Du, W., Du, J., Francis, F., Zhao, Y., & Xia, L. (2017). Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Frontiers in Plant Science, 8, 298.  https://doi.org/10.3389/fpls.2017.00298.CrossRefPubMedPubMedCentralGoogle Scholar
  151. Svitashev, S., Young, J., Schwartz, C., Gao, H., Falco, S. C., & Cigan, A. M. (2015). Targeted mutagenesis, precise gene editing and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiology.  https://doi.org/10.1104/pp.15.00793.
  152. Tak, Y. G., & Farnham, P. J. (2015). Making sense of GWAS: Using epigenomics and genome engineering to understand the functional relevance of SNPs in non-coding regions of the human genome. Epigenetics & Chromatin, 8(1), 57.  https://doi.org/10.1186/s13072-015-0050-4.CrossRefGoogle Scholar
  153. Tanenbaum, M. E., Gilbert, L. A., Qi, L. S., Weissman, J. S., & Vale, R. D. (2014). A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell, 159(3), 635–646.  https://doi.org/10.1016/j.cell.2014.09.039.CrossRefPubMedPubMedCentralGoogle Scholar
  154. Tang, X., Lowder, L. G., Zhang, T., Malzahn, A. A., Zheng, X., Voytas, D. F., Zhong, Z., Chen, Y., Ren, Q., Li, Q., Kirkland, E. R., Zhang, Y., & Qi, Y. (2017). A CRISPR–Cpf1 system for efficient genome editing and transcriptional repression in plants. Nature Plants, 3, 17018.  https://doi.org/10.1038/nplants.2017.18.CrossRefPubMedGoogle Scholar
  155. Thakore, P. I., D’Ippolito, A. M., Song, L., Safi, A., Shivakumar, N. K., Kabadi, A. M., Reddy, T. E., Crawford, G. E., & Gersbach, C. A. (2015). Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nature Methods, 12, 1143.  https://doi.org/10.1038/nmeth.3630.CrossRefPubMedPubMedCentralGoogle Scholar
  156. Tian, S., Jiang, L., Gao, Q., Zhang, J., Zong, M., Zhang, H., Ren, Y., Guo, S., Gong, G., Liu, F., & Xu, Y. (2017). Efficient CRISPR/Cas9-based gene knockout in watermelon. Plant Cell Reports, 36(3), 399–406.  https://doi.org/10.1007/s00299-016-2089-5.CrossRefPubMedGoogle Scholar
  157. Townsend, J. A., Wright, D. A., Winfrey, R. J., Fu, F., Maeder, M. L., Joung, J. K., & Voytas, D. F. (2009). High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature, 459, 442.  https://doi.org/10.1038/nature07845.CrossRefPubMedPubMedCentralGoogle Scholar
  158. Urnov, F. D., Miller, J. C., Lee, Y.-L., Beausejour, C. M., Rock, J. M., Augustus, S., Jamieson, A. C., Porteus, M. H., Gregory, P. D., & Holmes, M. C. (2005). Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature, 435, 646.  https://doi.org/10.1038/nature03556.CrossRefPubMedGoogle Scholar
  159. Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S., & Gregory, P. D. (2010). Genome editing with engineered zinc finger nucleases. Nature Reviews Genetics, 11, 636.  https://doi.org/10.1038/nrg2842.CrossRefPubMedGoogle Scholar
  160. Vojta, A., Dobrinić, P., Tadić, V., Bočkor, L., Korać, P., Julg, B., Klasić, M., & Zoldoš, V. (2016). Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Research, 44(12), 5615–5628.  https://doi.org/10.1093/nar/gkw159.CrossRefPubMedPubMedCentralGoogle Scholar
  161. Voytas, D. F. (2013). Plant genome engineering with sequence-specific nucleases. Annual Review of Plant Biology, 64(1), 327–350.  https://doi.org/10.1146/annurev-arplant-042811-105552.CrossRefPubMedGoogle Scholar
  162. Waltz, E. (2016). CRISPR-edited crops free to enter market, skip regulation. Nature Biotechnology, 34, 582.  https://doi.org/10.1038/nbt0616-582.CrossRefPubMedGoogle Scholar
  163. Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., & Qiu, J.-L. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnology, 32, 947.  https://doi.org/10.1038/nbt.2969.CrossRefPubMedGoogle Scholar
  164. Wang, S., Zhang, S., Wang, W., Xiong, X., Meng, F., & Cui, X. (2015). Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Reports, 34(9), 1473–1476.  https://doi.org/10.1007/s00299-015-1816-7.CrossRefPubMedGoogle Scholar
  165. Wang, F., Wang, C., Liu, P., Lei, C., Hao, W., Gao, Y., Liu, Y.-G., & Zhao, K. (2016a). Enhanced Rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One, 11(4), e0154027.  https://doi.org/10.1371/journal.pone.0154027.CrossRefPubMedPubMedCentralGoogle Scholar
  166. Wang, L., Wang, L., Tan, Q., Fan, Q., Zhu, H., Hong, Z., Zhang, Z., & Duanmu, D. (2016b). Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus using CRISPR-Cas9. Frontiers in Plant Science, 7(1333).  https://doi.org/10.3389/fpls.2016.01333.
  167. Wang, M., Mao, Y., Lu, Y., Tao, X., & Zhu, J.-k. (2017). Multiplex gene editing in rice using the CRISPR-Cpf1 system. Molecular Plant, 10(7), 1011–1013.  https://doi.org/10.1016/j.molp.2017.03.001.CrossRefPubMedGoogle Scholar
  168. Westra, E. R., Buckling, A., & Fineran, P. C. (2014). CRISPR–Cas systems: Beyond adaptive immunity. Nature Reviews Microbiology, 12, 317.  https://doi.org/10.1038/nrmicro3241.CrossRefPubMedGoogle Scholar
  169. William, H., Andrew, C., CB, M., DZ, L., Anita, L., Erin, R., Adam, R., Thomas, S., Alexandre, J., Frederic, C., Luc, M., VD, F., & Feng, Z. (2014). Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnology Journal, 12(7), 934–940.  https://doi.org/10.1111/pbi.12201.CrossRefGoogle Scholar
  170. Woo, J. W., Kim, J., Kwon, S. I., Corvalán, C., Cho, S. W., Kim, H., Kim, S.-G., Kim, S.-T., Choe, S., & Kim, J.-S. (2015). DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nature Biotechnology, 33, 1162.  https://doi.org/10.1038/nbt.3389.CrossRefPubMedGoogle Scholar
  171. Wright, D. A., Thibodeau-Beganny, S., Sander, J. D., Winfrey, R. J., Hirsh, A. S., Eichtinger, M., Fu, F., Porteus, M. H., Dobbs, D., Voytas, D. F., & Joung, J. K. (2006). Standardized reagents and protocols for engineering zinc finger nucleases by modular assembly. Nature Protocols, 1, 1637.  https://doi.org/10.1038/nprot.2006.259.CrossRefPubMedGoogle Scholar
  172. Xiaohong, Z., Jacobs, T. B., Liang-Jiao, X., Harding, S. A., & Chung-Jui, T. (2015). Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy. The New Phytologist, 208(2), 298–301.  https://doi.org/10.1111/nph.13470.CrossRefGoogle Scholar
  173. Xie, K., & Yang, Y. (2013). RNA-guided genome editing in plants using a CRISPR–Cas system. Molecular Plant, 6(6), 1975–1983.  https://doi.org/10.1093/mp/sst119.CrossRefPubMedGoogle Scholar
  174. Xie, K., Zhang, J., & Yang, Y. (2014). Genome-wide prediction of highly specific guide RNA spacers for CRISPR-Cas9-mediated genome editing in model plants and major crops. Molecular Plant, 7(5), 923–926.  https://doi.org/10.1093/mp/ssu009.CrossRefPubMedGoogle Scholar
  175. Xiquan, G., Fangjun, L., Maoying, L., Kianinejad, A. S., Dever, J. K., Wheeler, T. A., Zhaohu, L., Ping, H., & Libo, S. (2013). Cotton GhBAK1 mediates Verticillium wilt resistance and cell death. Journal of Integrative Plant Biology, 55(7), 586–596.  https://doi.org/10.1111/jipb.12064.CrossRefGoogle Scholar
  176. Xixun, H., Xiangbing, M., Qing, L., Jiayang, L., & Kejian, W. (2018). Increasing the efficiency of CRISPR-Cas9-VQR precise genome editing in rice. Plant Biotechnology Journal, 16(1), 292–297.  https://doi.org/10.1111/pbi.12771.CrossRefGoogle Scholar
  177. Xu, R., Li, H., Qin, R., Wang, L., Li, L., Wei, P., & Yang, J. (2014). Gene targeting using the agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice, 7(1), 5.  https://doi.org/10.1186/s12284-014-0005-6.CrossRefPubMedPubMedCentralGoogle Scholar
  178. Yamano, T., Nishimasu, H., Zetsche, B., Hirano, H., Slaymaker, I. M., Li, Y., Fedorova, I., Nakane, T., Makarova, K. S., Koonin, E. V., Ishitani, R., Zhang, F., & Nureki, O. (2016). Crystal structure of Cpf1 in complex with guide RNA and target DNA. Cell, 165(4), 949–962.  https://doi.org/10.1016/j.cell.2016.04.003.CrossRefPubMedPubMedCentralGoogle Scholar
  179. Yang, L., Briggs, A. W., Chew, W. L., Mali, P., Guell, M., Aach, J., Goodman, D. B., Cox, D., Kan, Y., Lesha, E., Soundararajan, V., Zhang, F., & Church, G. (2016). Engineering and optimising deaminase fusions for genome editing. Nature Communications, 7, 13330.  https://doi.org/10.1038/ncomms13330.CrossRefPubMedPubMedCentralGoogle Scholar
  180. Yang, L., Paul, M., Zhengzhi, Z., Chonghui, J., Bing, Y., & Shui-zhang, F. (2018). Targeted mutagenesis in tetraploid switchgrass (Panicum virgatum L.) using CRISPR/Cas9. Plant Biotechnology Journal, 16(2), 381–393.  https://doi.org/10.1111/pbi.12778.CrossRefPubMedGoogle Scholar
  181. Yin, K., Han, T., Liu, G., Chen, T., Wang, Y., Yu, A. Y. L., & Liu, Y. (2015). A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Scientific Reports, 5, 14926.  https://doi.org/10.1038/srep14926.CrossRefPubMedPubMedCentralGoogle Scholar
  182. Zetsche, B., Gootenberg, J. S., Abudayyeh, O. O., Slaymaker, I. M., Makarova, K. S., Essletzbichler, P., Volz Sara, E., Joung, J., van der Oost, J., Regev, A., Koonin, E. V., & Zhang, F. (2015). Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 163(3), 759–771.  https://doi.org/10.1016/j.cell.2015.09.038.CrossRefPubMedPubMedCentralGoogle Scholar
  183. Zhang, F., Maeder, M. L., Unger-Wallace, E., Hoshaw, J. P., Reyon, D., Christian, M., Li, X., Pierick, C. J., Dobbs, D., Peterson, T., Joung, J. K., & Voytas, D. F. (2010). High frequency targeted mutagenesis in <em>Arabidopsis thaliana</em> using zinc finger nucleases. Proceedings of the National Academy of Sciences, 107(26), 12028–12033.  https://doi.org/10.1073/pnas.0914991107.CrossRefGoogle Scholar
  184. Zhang, F., Cong, L., Lodato, S., Kosuri, S., Church, G. M., & Arlotta, P. (2011). Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nature Biotechnology, 29, 149.  https://doi.org/10.1038/nbt.1775.CrossRefPubMedPubMedCentralGoogle Scholar
  185. Zhang, Y., Heidrich, N., Ampattu, B. J., Gunderson, C. W., Seifert, H. S., Schoen, C., Vogel, J., & Sontheimer, E. J. (2013). Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Molecular Cell, 50(4), 488–503.  https://doi.org/10.1016/j.molcel.2013.05.001.CrossRefPubMedPubMedCentralGoogle Scholar
  186. Zhang, B., Yang, X., Yang, C., Li, M., & Guo, Y. (2016). Exploiting the CRISPR/Cas9 system for targeted genome mutagenesis in Petunia. Scientific Reports, 6, 20315.  https://doi.org/10.1038/srep20315.CrossRefPubMedPubMedCentralGoogle Scholar
  187. Zhong, Z., Zhang, Y., You, Q., Tang, X., Ren, Q., Liu, S., Yang, L., Wang, Y., Liu, X., Liu, B., Zhang, T., Zheng, X., Le, Y., Zhang, Y., & Qi, Y. (2018). Plant genome editing using FnCpf1 and LbCpf1 nucleases at redefined and altered PAM sites. Molecular Plant, 11(7), 999–1002.  https://doi.org/10.1016/j.molp.2018.03.008.CrossRefPubMedGoogle Scholar
  188. Zong, Y., Wang, Y., Li, C., Zhang, R., Chen, K., Ran, Y., Qiu, J.-L., Wang, D., & Gao, C. (2017). Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nature Biotechnology, 35, 438.  https://doi.org/10.1038/nbt.3811.CrossRefPubMedGoogle Scholar
  189. Zupeng, W., Shuaibin, W., Dawei, L., Qiong, Z., Li, L., Caihong, Z., Yifei, L., & Hongwen, H. (2018). Optimized paired-sgRNA/Cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit. Plant Biotechnology Journal 0(0).  https://doi.org/10.1111/pbi.12884

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Division of Biotechnology and PhycologyCSIR-Central Salt and Marine Chemicals Research InstituteBhavnagarIndia
  2. 2.Academy of Scientific and Innovative ResearchCouncil of Scientific and Industrial ResearchGhaziabadIndia

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