Multi-gene engineering in plants with RNA-guided Cas9 nuclease

Current Opinion in Biotechnology

Volumn 37, Issue , 2016, Pages 69-75

  Raitskin, Oleg ^a   Patron, Nicola J ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONCURRENT ENGINEERING; GENES; RNA;

DNA TARGETS; ENDONUCLEASES; GENE ENGINEERING; MONOMERIC PROTEINS; MULTIPLE GENES; PLANT SPECIES; SIMULTANEOUS EDITING; TRANSCRIPTIONAL REGULATION;

NUCLEIC ACIDS;

CAS9 ENDONUCLEASE; CRISPR ASSOCIATED PROTEIN; DNA DIRECTED RNA POLYMERASE III; DNA FRAGMENT; ENDONUCLEASE; RNA; RNA POLYMERASE II; SINGLE GUIDE RNA; UNCLASSIFIED DRUG; GUIDE RNA;

DNA SEQUENCE; GENE EXPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC ENGINEERING; MOLECULAR CLONING; PLANT GENE; PLANT GENOME; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; RNA GUIDED CAS9 NUCLEASE MEDIATED GENE EDITING; TRANSCRIPTION REGULATION; ANIMAL; GENETICS; HUMAN; METABOLISM; PLANT;

ANIMALS; ENDONUCLEASES; GENE EXPRESSION; GENETIC ENGINEERING; HUMANS; PLANTS; RNA, GUIDE;

EID: 84949964421     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2015.11.008     Document Type: Review

References (73)

1. Mali P., Aach J., Stranges P.B., Esvelt K.M., Moosburner M., Kosuri S., Yang L., Church G.M. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 2013, 31:833-838.
2. Qi L.S., Larson M.H., Gilbert L.A., Doudna J.A., Weissman J.S., Arkin A.P., Lim W.A. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 2013, 152:1173-1183.
3. 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., et al. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 2013, 155:1479-1491.
4. Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315:1709-1712.
5. Bhaya D., Davison M., Barrangou R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 2011, 45:273-297.
6. Deltcheva E., Chylinski K., Sharma C.M., Gonzales K., Chao Y., Pirzada Z.A., Eckert M.R., Vogel J., Charpentier E. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 2011, 471:602-607.
7. Jansen R., Embden J.D., Gaastra W., Schouls L.M. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 2002, 43:1565-1575.
8. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
9. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
10. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337:816-821.
11. Sternberg S.H., Redding S., Jinek M., Greene E.C., Doudna J.A. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 2014, 507:62-67.
12. Fauser F., Schiml S., Puchta H. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J 2014, 79:348-359.
13. Feng Z., Mao Y., Xu N., Zhang B., Wei P., Yang D.L., Wang Z., Zhang Z., Zheng R., Yang L., et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci U S A 2014, 111:4632-4637.
14. Gao Y., Zhang Y., Zhang D., Dai X., Estelle M., Zhao Y. Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci U S A 2015, 112:2275-2280.
15. Gao Y., Zhao Y. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J Integr Plant Biol 2014, 56:343-349.
16. Jiang W., Zhou H., Bi H., Fromm M., Yang B., Weeks D.P. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 2013, 41:e188.
17. Schiml S., Fauser F., Puchta H. 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 2014, 80:1139-1150.
18. Xing H.L., Dong L., Wang Z.P., Zhang H.Y., Han C.Y., Liu B., Wang X.C., Chen Q.J. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 2014, 14:327.
19. Liang Z., Zhang K., Chen K., Gao C. Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genomics 2014, 41:63-68.
20. Ali Z., Abul-Faraj A., Piatek M., Mahfouz M.M. Activity and specificity of TRV-mediated gene editing in plants. Plant Signal Behav 2015.
21. Belhaj K., Chaparro-Garcia A., Kamoun S., Nekrasov V. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 2013, 9:39.
22. Gao J.P., Wang G.H., Ma S.Y., Xie X.D., Wu X.W., Zhang X.T., Wu Y.Q., Zhao P., Xia Q.Y. CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol 2015, 87:99-110.
23. Li J.F., Norville J.E., Aach J., McCormack M., Zhang D., Bush J., Church G.M., Sheen J. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 2013, 31:688-691.
24. Li J.F., Zhang D., Sheen J. Cas9-based genome editing in Arabidopsis and tobacco. Methods Enzymol 2014, 546:459-472.
25. Nekrasov V., Staskawicz B., Weigel D., Jones J.D., Kamoun S. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 2013, 31:691-693.
26. Ma X., Zhang Q., Zhu Q., Liu W., Chen Y., Qiu R., Wang B., Yang Z., Li H., Lin Y., et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 2015.
27. Mao Y., Zhang H., Xu N., Zhang B., Gou F., Zhu J.K. Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant 2013, 6:2008-2011.
28. Miao J., Guo D., Zhang J., Huang Q., Qin G., Zhang X., Wan J., Gu H., Qu L.J. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 2013, 23:1233-1236.
29. Shan Q., Wang Y., Li J., Gao C. Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc 2014, 9:2395-2410.
30. Shan Q., Wang Y., Li J., Zhang Y., Chen K., Liang Z., Zhang K., Liu J., Xi J.J., Qiu J.L., et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 2013, 31:686-688.
31. Xu R., Li H., Qin R., Wang L., Li L., Wei P., Yang J. Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice (N Y) 2014, 7:5.
32. Xu R.F., Li H., Qin R.Y., Li J., Qiu C.H., Yang Y.C., Ma H., Li L., Wei P.C., Yang J.B. Generation of inheritable and transgene clean targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep 2015, 5:11491.
33. Zhang H., Zhang J., Wei P., Zhang B., Gou F., Feng Z., Mao Y., Yang L., Zhang H., Xu N., et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 2014, 12:797-807.
34. Zhou H., Liu B., Weeks D.P., Spalding M.H., Yang B. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res 2014, 42:10903-10914.
35. Brooks C., Nekrasov V., Lippman Z.B., Van Eck J. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 2014, 166:1292-1297.
36. Ron M., Kajala K., Pauluzzi G., Wang D., Reynoso M.A., Zumstein K., Garcha J., Winte S., Masson H., Inagaki S., et al. Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol 2014, 166:455-469.
37. Upadhyay S.K., Kumar J., Alok A., Tuli R. RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda) 2013, 3:2233-2238.
38. Wang Y., Cheng X., Shan Q., Zhang Y., Liu J., Gao C., Qiu J.L. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 2014, 32:947-951.
39. Gaj T., Gersbach C.A., Barbas C.F. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 2013, 31:397-405.
40. Jiang W., Bikard D., Cox D., Zhang F., Marraffini L.A. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 2013, 31:233-239.
41. Xie K., Yang Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant 2013, 6:1975-1983.
42. Gao Y., Zhao Y. Specific and heritable gene editing in Arabidopsis. Proc Natl Acad Sci U S A 2014, 111:4357-4358.
43. Fan D., Liu T., Li C., Jiao B., Li S., Hou Y., Luo K. Efficient CRISPR/Cas9-mediated targeted mutagenesis in populus in the first generation. Sci Rep 2015, 5:12217.
44. Aida T., Chiyo K., Usami T., Ishikubo H., Imahashi R., Wada Y., Tanaka K.F., Sakuma T., Yamamoto T., Tanaka K. Cloning-free CRISPR/Cas system facilitates functional cassette knock-in in mice. Genome Biol 2015, 16:87.
45. Cho S.W., Lee J., Carroll D., Kim J.S., Lee J. Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 2013, 195:1177-1180.
46. Kim S., Kim D., Cho S.W., Kim J., Kim J.S. Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res 2014, 24:1012-1019.
47. Svitashev S., Young J.K., Schwartz C., Gao H., Falco S.C., Cigan A.M. Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 2015, 169:931-945.
48. Jia H., Wang N. Targeted genome editing of sweet orange using Cas9/sgRNA. PLOS ONE 2014, 9:e93806.
49. Jacobs T.B., LaFayette P.R., Schmitz R.J., Parrott W.A. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 2015, 15:16.
50. Ali Z., Abul-Faraj A., Li L., Ghosh N., Piatek M., Mahjoub A., Aouida M., Piatek A., Baltes N.J., Voytas D.F., et al. Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 System. Mol Plant 2015, 8:1288-1291.
51. Baltes N.J., Gil-Humanes J., Cermak T., Atkins P.A., Voytas D.F. DNA replicons for plant genome engineering. Plant Cell 2014, 26:151-163.
52. Lowder L.G., Zhang D., Baltes N.J., Paul J.W., Tang X., Zheng X., Voytas D.F., Hsieh T.F., Zhang Y., Qi Y. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 2015, 169:971-985.
53. Ma H., Wu Y., Dang Y., Choi J.G., Zhang J., Wu H. Pol III promoters to express small RNAs: delineation of transcription initiation. Mol Ther Nucleic Acids 2014, 3:e161.
54. Brummelkamp T.R., Bernards R., Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002, 296:550-553.
55. Miyagishi M., Taira K. U6 promoter-driven siRNAs with four uridine 3' overhangs efficiently suppress targeted gene expression in mammalian cells. Nat Biotechnol 2002, 20:497-500.
56. Xie K., Minkenberg B., Yang Y. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci U S A 2015, 112:3570-3575.
57. Engler C., Kandzia R., Marillonnet S. A one pot, one step, precision cloning method with high throughput capability. PLoS One 2008, 3:e3647.
58. Weber E., Gruetzner R., Werner S., Engler C., Marillonnet S. Assembly of designer TAL effectors by Golden Gate cloning. PLoS One 2011, 6:e19722.
59. Patron N., Orzaez D., Marillonnet S., Warzecha H., Matthewman C., Youles M., Raitskin O., Leveau A., Farré G., Rogers C., et al. Standards for plant synthetic biology: a common syntax for exchange of DNA parts. New Phytol 2015, 208:13-19.
60. Engler C., Youles M., Gruetzner R., Ehnert T.M., Werner S., Jones J.D., Patron N.J., Marillonnet S. A golden gate modular cloning toolbox for plants. ACS Synth Biol 2014, 3:839-843.
61. Werner S., Engler C., Weber E., Gruetzner R., Marillonnet S. Fast track assembly of multigene constructs using Golden Gate cloning and the MoClo system. Bioeng Bugs 2012, 3:38-43.
62. Gasiunas G., Barrangou R., Horvath P., Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 2012, 109:E2579-E2586.
63. Bikard D., Jiang W., Samai P., Hochschild A., Zhang F., Marraffini L.A. Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res 2013, 41:7429-7437.
64. Chavez A., Scheiman J., Vora S., Pruitt B.W., Tuttle M.E.P.R.I., Lin S., Kiani S., Guzman C.D., Wiegand D.J., et al. Highly efficient Cas9-mediated transcriptional programming. Nat Methods 2015, 12:326-328.
65. Esvelt K.M., Mali P., Braff J.L., Moosburner M., Yaung S.J., Church G.M. Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods 2013, 10:1116-1121.
66. Hilton I.B., D'Ippolito A.M., Vockley C.M., Thakore P.I., Crawford G.E., Reddy T.E., Gersbach C.A. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 2015, 33:510-517.
67. Kabadi A.M., Ousterout D.G., Hilton I.B., Gersbach C.A. Multiplex CRISPR/Cas9-based genome engineering from a single lentiviral vector. Nucleic Acids Res 2014, 42:e147.
68. Konermann S., Brigham M.D., Trevino A.E., Joung J., Abudayyeh O.O., Barcena C., Hsu P.D., Habib N., Gootenberg J.S., Nishimasu H., et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 2015, 517:583-588.
69. Tanenbaum M.E., Gilbert L.A., Qi L.S., Weissman J.S., Vale R.D. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 2014, 159:635-646.
70. Koike-Yusa H., Li Y., Tan E.P., Velasco-Herrera Mdel C., Yusa K. Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat Biotechnol 2014, 32:267-273.
71. Shalem O., Sanjana N.E., Hartenian E., Shi X., Scott D.A., Mikkelsen T.S., Heckl D., Ebert B.L., Root D.E., Doench J.G., et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014, 343:84-87.
72. Varshney G.K., Pei W., LaFave M.C., Idol J., Xu L., Gallardo V., Carrington B., Bishop K., Jones M., Li M., et al. High-throughput gene targeting and phenotyping in zebrafish using CRISPR/Cas9. Genome Res 2015.
73. Engler C., Gruetzner R., Werner S., Marillonnet S. A modular cloning system for standardized assembly of multigene constructs. PLoS One 2011, 6:e16765.