The expanding footprint of CRISPR/Cas9 in the plant sciences

Plant Cell Reports

Volumn 35, Issue 7, 2016, Pages 1451-1468

  Schaeffer, Scott M ^a   Nakata, Paul A ^a  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

Cas9; CRISPR; Crop improvement; Functional genomics; Gene editing; Gene knock in

Indexed keywords

BIOLOGICAL MODEL; CRISPR CAS SYSTEM; FORECASTING; GENE EDITING; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; PLANT; PLANT GENE; PROCEDURES; SITE DIRECTED MUTAGENESIS; TRANSGENIC PLANT; TRENDS;

CRISPR-CAS SYSTEMS; FORECASTING; GENE EDITING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ENGINEERING; MODELS, GENETIC; MUTAGENESIS, SITE-DIRECTED; PLANTS; PLANTS, GENETICALLY MODIFIED;

EID: 84965054211     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-016-1987-x     Document Type: Review

References (157)

1. Ahloowalia BS, Maluszynski M (2001) Induced mutations—a new paradigm in plant breeding. Euphytica 118:167–173
2. Ali Z, Abul-faraj A, Li L, Ghosh N, Piatek M, Mahjoub A, Aouida M, Piatek A, Baltes NJ, Voytas DF et al (2015a) Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant 8:1288–1291
3. Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz MM (2015b) CRISPR/Cas9-mediated viral interference in plants. Genome Biol 16:238
4. Anton T, Bultmann S, Leonhardt H, Markaki Y (2014) Visualization of specific DNA sequences in living mouse embryonic stem cells with a programmable fluorescent CRISPR/Cas system. Nucleus 5:163–172
5. Auer TO, Duroure K, Cian AD, Concordet JP, Bene FD (2014) Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res 24:142–153
6. Bains GS, Howard HW (1950) Haploid plants of Solanum demissum. Nature 166:795
7. Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF (2014) DNA replicons for plant genome engineering. Plant Cell 26:151–163
8. Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN, Bisaro DM, Voytas DF (2015) Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat Plants 1:15145
9. Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39
10. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84
11. Benitez-Alfonso Y, Faulkner C, Ritzenthaler C, Maule AJ (2010) Plasmodesmata: gateways to local and systemic virus infection. Mol Plant Microbe Interact 23:1403–1412
12. Bikard D, Jiang W, Samai P, Hochschild A, Zhang F, Marraffini LA (2013) Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res 41:7429–7437
13. Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA targeting. Science 333:1843–1846
14. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiol Read Engl 151:2551–2561
15. Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52
16. Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72
17. Brooks C, Nekrasov V, Lippman ZB, 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
18. Cardi T (2016) Cisgenesis and genome editing: combining concepts and efforts for a smarter use of genetic resources in crop breeding. Plant Breed 135:139–147
19. Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol. doi:10.1111/mpp.12375
20. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406
21. Chen K, Gao C (2013) Targeted genome modification technologies and their applications in crop improvements. Plant Cell Rep 33:575–583
22. Chen C, Fenk LA, de Bono M (2013) Efficient genome editing in Caenorhabditis elegans by CRISPR-targeted homologous recombination. Nucleic Acids Res 41:e193
23. Chen X, Li M, Feng X, Guang S (2015) Targeted Chromosomal Translocations And Essential Gene Knockout Using CRISPR/Cas9 technology in Caenorhabditis elegans. Genetics 201:1295–1306
24. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761
25. Chu VT, Weber T, Wefers B, Wurst W, Sander S, Rajewsky K, Kühn R (2015) Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat Biotechnol 33:543–548
26. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161
27. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–607
28. Ding Q, Strong A, Patel KM, Ng SL, Gosis BS, Regan SN, Cowan CA, Rader DJ, Musunuru K (2014) Permanent alteration of PCSK9 with in vivo CRISPR-Cas9 genome editing. Circ Res 115:488–492
29. Dominguez AA, Lim WA, Qi LS (2016) Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation. Nat Rev Mol Cell Biol 17:5–15
30. Dong ZQ, Chen TT, Zhang J, Hu N, Cao MY, Dong FF, Jiang YM, Chen P, Lu C, Pan MH (2016). Establishment of a highly efficient virus-inducible CRISPR/Cas9 system in insect cells. Antiviral Res 130:50–57
31. Dunwell JM (2010) Haploids in flowering plants: origins and exploitation. Plant Biotechnol J 8:377–424
32. 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. Sci Rep 5:12217
33. Fauser F, Schiml S, 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
34. Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y et al (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232
35. Feng C, Yuan J, Wang R, Liu Y, Birchler JA, Han F (2016) Efficient targeted genome modification in maize using CRISPR/Cas9 system. J Genet Genomics 43:37–43
36. Fichtner F, Castellanos RU, Ülker B (2014) Precision genetic modifications: a new era in molecular biology and crop improvement. Planta 239:921–939
37. Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405
38. Gamper HB, Parekh H, Rice MC, Bruner M, Youkey H, Kmiec EB (2000) The DNA strand of chimeric RNA/DNA oligonucleotides can direct gene repair/conversion activity in mammalian and plant cell-free extracts. Nucleic Acids Res 28:4332–4339
39. Gao J, Wang G, Ma S, Xie X, Wu X, Zhang X, Wu Y, Zhao P, Xia Q (2015) CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol 87:99–110
40. Garneau JE, Dupuis MÈ, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadán AH, Moineau S (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71
41. Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci 109:E2579–E2586
42. Geisinger JM, Turan S, Hernandez S, Spector LP, Calos MP (2016) In vivo blunt-end cloning through CRISPR/Cas9-facilitated non-homologous end-joining. Nucleic Acids Res. doi:10.1093/nar/gkv1542
43. Gergerich RC, Welliver RA, Gettys S, Osterbauer NK, Kamenidou S, Martin RR, Golino DA, Eastwell K, Fuchs M, Vidalakis G et al (2015) Safeguarding fruit crops in the age of agricultural globalization. Plant Dis 99:176–187
44. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA et al (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–451
45. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, Guimaraes C, Panning B, Ploegh HL, Bassik MC, Qi LS (2014) Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159:647–661
46. Guha S, Maheshwari SC (1964) In vitro production of embryos from anthers of Datura. Nature 204:497
47. Guilinger JP, Thompson DB, Liu DR (2014) Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32:577–582
48. Hafez M, Hausner G (2012) Homing endonucleases: DNA scissors on a mission. Genome 55:553–569
49. Harper G, Hull R, Lockhart B, Olszewski N (2002) Viral sequences integrated into plant genomes. Annu Rev Phytopathol 40:119–136
50. Hilton IB, D’Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA (2015) Epigenome editing by a CRISPR/Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 33:510–517
51. Hnatuszko-Konka K, Kowalczyk T, Gerszberg A, Wiktorek-Smagug A, Kononowicz A (2014) Phaseolus vulgaris—recalcitrant potential. Biotechnol Adv 32:1205–1215
52. Hou Z, Zhang Y, Propson NE, Howden SE, Chu LF, Sontheimer EJ, Thomson JA (2013) Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc Natl Acad Sci 110:15644–15649
53. Hou H, Atlihan N, Lu ZX (2014) New biotechnology enhances the application of cisgenesis in plant breeding. Front Plant Sci 5:389
54. Houten JG, Quak F, van der Meer FA (1968) Heat treatment and meristem culture for the production of virus-free plant material. Neth J Plant Pathol 74:17–24
55. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O et al (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31:827–832
56. Hu W, Kaminski R, Yang F, Zhang Y, Cosentino L, Li F, Luo B, Alvarez-Carbonell D, Garcia-Mesa Y, Karn J et al (2014) RNA-directed gene editing specifically eradicates latent and prevents new HIV-1 infection. Proc Natl Acad Sci 111:11461–11466
57. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21:635–637
58. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:16
59. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254
60. Jain M (2015) Function genomics of abiotic stress tolerance in plants: a CRISPR approach. Front Plant Sci 6:375
61. Ji X, Zhang H, Zhang Y, Wang Y, Gao C (2015) Establishing a CRISPR–Cas-like immune system conferring DNA virus resistance in plants. Nat Plants 1:15144
62. Jia H, Wang N (2014a) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE 9:e93806
63. Jia H, Wang N (2014b) Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves. Plant Cell Rep 33:1993–2001
64. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41(20):e188
65. Jiang W, Brueggeman AJ, Horken KM, Plucinak TM, Weeks DP (2014) Successful transient expression of Cas9 and single guide RNA genes in Chlamydomonas reinhardtii. Eukaryot Cell 13:1465–1469
66. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA—guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821
67. Kabadi AM, Gersbach CA (2014) Engineering synthetic TALE and CRISPR/Cas9 transcription factors for regulating gene expression. Methods 69:188–197
68. Karimi-Ashtiyani R, Ishii T, Niessen M, Stein N, Heckmann S, Gurushidze M, Banaei-Moghaddam AM, Fuchs J, Schubert V, Koch K et al (2015) Point mutation impairs centromeric CENH3 loading and induces haploid plants. Proc Natl Acad Sci 112:11211–11216
69. Kearns NA, Pham H, Tabak B, Genga RM, Silverstein NJ, Garber M, Maehr R (2015) Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat Methods 12:401–403
70. Kim S, Kim D, Cho SW, Kim J, Kim JS (2014) Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res 24:1012–1019
71. Kimura Y, Hisano Y, Kawahara A, Higashijima S (2014) Efficient generation of knock-in transgenic zebrafish carrying reporter/driver genes by CRISPR/Cas9-mediated genome engineering. Sci Rep 4:6545
72. Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng Z, Gonzales APW, Li Z, Peterson RT, Yeh JRJ et al (2015) Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523:481–485
73. Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Keith Joung J (2016) High-fidelity CRISPR–Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529:490–495
74. Koike-Yusa H, Li Y, Tan EP, Velasco-Herrera MDC, Yusa K (2014) Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat Biotechnol 32:267–273
75. Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, Hsu PD, Habib N, Gootenberg JS, Nishimasu H et al (2015) Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517:583–588
76. Korkmaz G, Lopes R, Ugalde AP, Nevedomskaya E, Han R, Myacheva K, Zwart W, Elkon R, Agami R (2016) Functional genetic screens for enhancer elements in the human genome using CRISPR-Cas9. Nat Biotechnol 34:192–198
77. Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11:2283–2290
78. Kumar V, Jain M (2015) The CRISPR–Cas system for plant genome editing: advances and opportunities. J Exp Bot 66:47–57
79. Lee CM, Cradick TJ, Bao G (2016) The Neisseria meningitidis CRISPR-Cas9 system enables specific genome editing in mammalian cells. Mol Ther J Am Soc Gene Ther 24:645–654
80. Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B (2011) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39:359–372
81. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31:688–691
82. Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genom 41:63–68
83. Lin PC, Corn JE (2015) Co-opting CRISPR to deliver functional RNAs. Nat Methods 12:613–614
84. Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66
85. Liu X, Hao L, Li D, Zhu L, Hu S (2015) Long non-coding RNAs and their biological roles in plants. Genom Proteom Bioinform 13:137–147
86. Lowder L, Zhang Y, Baltes N, Paul J, Tang X, Zheng X, Voytas D, Hsieh TF, Zhang D, Qi Y (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Phys 169:971–985
87. Lozano-Juste J, Cutler SR (2014) Plant genome engineering in full bloom. Trends Plant Sci 19:284–287
88. Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y et al (2015) A Robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8:1274–1284
89. Maeder ML, Linder SJ, Cascio VM, Fu Y, Ho QH, Joung JK (2013) CRISPR RNA-guided activation of endogenous human genes. Nat Methods 10:977–979
90. Mahfouz MM, Piatek A, Stewart CN (2014) Genome engineering via TALENs and CRISPR/Cas9 systems: challenges and perspectives. Plant Biotechnol J 12:1006–1014
91. Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, Yang L, Church GM (2013) Cas9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31:833–838
92. Maruyama T, Dougan SK, Truttmann MC, Bilate AM, Ingram JR, Ploegh HL (2015) Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat Biotechnol 33:538–542
93. Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, Wan J, Gu H, Qu LJ (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23:1233–1236
94. Mojica FJM, Díez-Villaseñor C, García-Martínez J, Soria E (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60:174–182
95. Nagamangala Kanchiswamy C, Sargent DJ, Velasco R, Maffei ME, Malnoy M (2015) Looking forward to genetically edited fruit crops. Trends Biotechnol 33:62–64
96. Nekrasov V, Staskawicz B, Weigel D, Jones JDG, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31:691–693
97. Nelles DA, Fang MY, Aigner S, Yeo GW (2015) Applications of Cas9 as an RNA-programmed RNA-binding protein. BioEssays 37:732–739
98. Nelles DA, Fang MY, O’Connell MR, Xu JL, Markmiller SJ, Doudna JA, and Yeo GW (2016) Programmable RNA tracking in live cells with CRISPR/Cas9. Cell 165:488–496
99. Nuñez JK, Harrington LB, Kranzusch PJ, Engelman AN, Doudna JA (2015) Foreign DNA capture during CRISPR-Cas adaptive immunity. Nature 527:535–538
100. O’Connell MR, Oakes BL, Sternberg SH, East-Seletsky A, Kaplan M, Doudna JA (2014) Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516:263–266
101. Paszkowski J (2015) Controlled activation of retrotransposition for plant breeding. Curr Opin Biotechnol 32:200–206
102. Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S, Aouida M, Mahfouz MM (2015) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13:578–589
103. Podevin N, Davies HV, Hartung F, Nogué F, Casacuberta JM (2013) Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding. Trends Biotechnol 31:375–383
104. Porteus MH, Baltimore D (2003) Chimeric nucleases stimulate gene targeting in human cells. Science 300:763
105. Price AA, Sampson TR, Ratner HK, Grakoui A, Weiss DS (2015) Cas9-mediated targeting of viral RNA in eukaryotic cells. Proc Natl Acad Sci 112:6164–6169
106. Puchta H (2016) Using CRISPR/Cas in three dimensions: towards synthetic plant genomes, transcriptomes and epigenomes. Plant J. doi:10.1111/tpj.13100(in press)
107. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183
108. Raitskin O, Patron NJ (2016) Multi-gene engineering in plants with RNA-guided Cas9 nuclease. Curr Opin Biotechnol 37:69–75
109. Ramanan V, Shlomai A, Cox DBT, Schwartz RE, Michailidis E, Bhatta A, Scott DA, Zhang F, Rice CM, Bhatia SN (2015) CRISPR/Cas9 cleavage of viral DNA efficiently suppresses hepatitis B virus. Sci Rep 5:10833
110. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y et al (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380–1389
111. Ran FA, Cong L, Yan WX, Scott DA, Gootenburg JS, Kriz AJ, Zetsche B, Shalem O, Wu X, Makarova KS, Koonin EV, Sharp PA, Zhang F (2015) In vivo genome editing using Staphylococcus aureus Cas9. Nature 520:186–191
112. Ratz M, Testa I, Hell SW, Jakobs S (2015) CRISPR/Cas9-mediated endogenous protein tagging for RESOLFT super-resolution microscopy of living human cells. Sci Rep 5:9592
113. Rice JC, Allis CD (2001) Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr Opin Cell Biol 13:263–273
114. Ruan J, Li H, Xu K, Wu T, Wei J, Zhou R, Liu Z, Mu Y, Yang S, Ouyang H et al (2015) Highly efficient CRISPR/Cas9-mediated transgene knock-in at the H11 locus in pigs. Sci Rep 5:14253
115. Schaeffer SM, Nakata PA (2015) CRISPR/Cas9-mediated genome editing and gene replacement in plants: transitioning from lab to field. Plant Sci 240:130–142
116. Schiml S, Puchta H (2016) Revolutionizing plant biology: multiple ways of genome engineering by CRISPR/Cas. Plant Methods 12:8
117. Schiml S, Fauser F, 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
118. Schmidt T, Schmid-Burgk JL, Hornung V (2015) Synthesis of an arrayed sgRNA library targeting the human genome. Sci Rep 5:14987
119. Schouten HJ, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants. EMBO Rep 7:750–753
120. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG et al (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87
121. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688
122. Shechner DM, Hacisuleyman E, Younger ST, Rinn JL (2015) Multiplexable, locus-specific targeting of long RNAs with CRISPR-Display. Nat Methods 12:664–670
123. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F (2016) Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88
124. Small I (2007) RNAi for revealing and engineering plant gene functions. Curr Opin Biotechnol 18:148–153
125. Song J, Angel A, Howard M, Dean C (2012) Vernalization—a cold-induced epigenetic switch. J Cell Sci 125:3723–3731
126. Sprink T, Metje J, Hartung F (2015) Plant genome editing by novel tools: TALEN and other sequence specific nucleases. Curr Opin Biotechnol 32:47–53
127. Sugano SS, 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 Cell Physiol 55:475–481
128. Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM (2015) Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 169:931–945
129. Swiech L, Heidenreich M, Banerjee A, Habib N, Li Y, Trombetta J, Sur M, Zhang F (2015) In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat Biotechnol 33:102–106
130. Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, Cayrel A, Endre G, Zhao PX, Chabaud M et al (2008) Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J 54:335–347
131. Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445
132. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ, Joung JK (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32:569–576
133. Turck F, Coupland G (2014) Natural variation in epigenetic gene regulation and its effects on plant developmental traits. Evolution 68:620–631
134. Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol 12:e1001877
135. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951
136. 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 Rep 34:1473–1476
137. Wang G, Zhao N, Berkhout B, Das AT (2016) CRISPR-Cas9 can inhibit HIV-1 replication but NHEJ repair facilitates virus escape. Mol Ther J Am Soc Gene Ther 24:522–526
138. Watson JM, Fusaro AF, Wang M, Waterhouse PM (2005) RNA silencing platforms in plants. FEBS Lett 579:5982–5987
139. Weeks DP, Spalding MH, Yang B (2015) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J 14:483–495
140. Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–338
141. Woo JW, Kim J, Kwon SI, Corvalán C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33:1162–1164
142. Wright AV, Sternberg SH, Taylor DW, Staahl BT, Bardales JA, Kornfeld JE, Doudna JA (2015) Rational design of a split-Cas9 enzyme complex. Proc Natl Acad Sci 112:2984–2989
143. Wu Y, Liang D, Wang Y, Bai M, Tang W, Bao S, Yan Z, Li D, Li J (2013) Correction of a genetic disease in mouse via use of CRISPR-Cas9. Cell Stem Cell 13:659–662
144. Xiao A, Wang Z, Hu Y, Wu Y, Luo Z, Yang Z, Zu Y, Li W, Huang P, Tong X et al (2013) Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res 41:e141
145. Xu RF, Li H, Qin RY, Li J, Qiu CH, Yang YC, Ma H, Li L, Wei PC, Yang JB (2015) Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep 5:11491
146. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154:1370–1379
147. Yang L, Güell M, Niu D, George H, Lesha E, Grishin D, Aach J, Shrock E, Xu W, Poci J et al (2015) Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350:1101–1104
148. Yin H, Xue W, Chen S, Bogorad RL, Benedetti E, Grompe M, Koteliansky V, Sharp PA, Jacks T, Anderson DG (2014) Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat Biotechnol 32:551–553
149. Zaidi SS, Mansoor S, Ali Z, Tashkandi M, Mahfouz MM (2016) Engineering plants for Geminivirus resistance with CRISPR/Cas9 system. Trends Plant Sci 21:279–281
150. Zetsche B, Volz SE, Zhang F (2015a) A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat Biotechnol 33:139–142
151. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A et al (2015b) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771
152. Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N et al (2014) The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 12:797–807
153. Zhang L, Jia R, Palange NJ, Satheka AC, Togo J, An Y, Humphrey M, Ban L, Ji Y, Jin H et al (2015) Large genomic fragment deletions and insertions in mouse using CRISPR/Cas9. PLoS ONE 10:e0120396
154. Zhang D, Li Z, and Li JF (2016a) Targeted gene manipulation in plants using the CRISPR/Cas technology. J Genet Genomics. doi:10.1016/j.jgg.2016.03.001
155. Zhang B, Yang X, Yang C, Li M, Guo Y (2016b) Exploiting the CRISPR/Cas9 system for targeted genome mutagenesis in Petunia. Sci Rep 6:20315
156. Zhou H, Liu B, Weeks DP, Spalding MH, Yang B (2014) Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res 42:10903–10914
157. Zhou X, Jacobs TB, Xue LJ, Harding SA, Tsai CJ (2015) Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy. New Phytol 208:298–301