CRISPR/Cas9: a promising way to exploit genetic variation in plants

Biotechnology Letters

Volumn 38, Issue 12, 2016, Pages 1991-2006

  Rani, Reema ^a   Yadav, Prashant ^a   Barbadikar, Kalyani M ^b   Baliyan, Nikita ^c   Malhotra, Era Vaidya ^d   Singh, Binay Kumar ^e   Kumar, Arun ^a   Singh, Dhiraj ^a  

^a ICAR DIRECTORATE OF RAPESEED MUSTARD RESEARCH   (India)

^b DIRECTORATE OF RICE RESEARCH   (India)

^c INDIAN AGRICULTURAL RESEARCH INSTITUTE   (India)

^d NATIONAL RESEARCH CENTRE ON PLANT BIOTECHNOLOGY   (India)

^e ICAR INDIAN INSTITUTE OF AGRICULTURAL BIOTECHNOLOGY   (India)

Author keywords

CRISPR Cas9; Crop improvement; Genome editing; Mutagenesis

Indexed keywords

CROPS; MUTAGENESIS; NUCLEIC ACIDS;

CRISPR/CAS9; CROP IMPROVEMENT; GENE MODIFICATION; GENETIC RESOURCES; GENETIC VARIATION; INTERFERENCE PATHWAY; NONHOMOLOGOUS END JOINING; REPAIR MECHANISM;

GENES;

PLANT PROTEIN;

CRISPR CAS SYSTEM; CROP; GENETIC VARIATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANT GENOME;

CRISPR-CAS SYSTEMS; CROPS, AGRICULTURAL; GENETIC VARIATION; GENOME, PLANT; PLANT PROTEINS;

EID: 84984655358     PISSN: 01415492     EISSN: 15736776     Source Type: Journal    
DOI: 10.1007/s10529-016-2195-z     Document Type: Review

References (84)

1. Ainley WM, Sastry-Dent L, Welter ME, Murray MG, Zeitler B, Amora R et al (2013) Trait stacking via targeted genome editing. Plant Biotechnol 11:1126–1134
2. Anders C, Niewoehner O, Duerst A, Jinek M (2014) Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513:69–73
3. Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T (2010) Control fruit patterning in Arabidopsis thaliana. Genes Dev 24:2127–2132
4. Barrangou R, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712
5. 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 Method 9:39
6. Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P (2007) CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinform 8:209
7. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR (2013) Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493:429–432
8. Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52
9. Brooks C, Nekrasov V, Lippman ZB, Van EJ (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
10. Brouns SJ, Jore MM, Lundgren M, Westra ER, Silikhuis RJ, Snijders AP, Dickmen MJ, Makarova KS, Koonin EV, Vander OJ (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 32:960–964
11. Carroll D (2011) Genome engineering with zinc-finger nucleases. Genetics 188:773–782
12. Cermak T, Baltes NJ, Cegan R, Zhang Y, Daniel F (2015) High-frequency, precise modification of the tomato genome. Genome Biol 16:232
13. Changtian P, Ye L, Qin L, Liu X, He Y, Wang J, Chen L, Lu G (2016) CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6:24765
14. Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, Kim JS (2014) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24:132–141
15. Chylinski K, Le Rhun A, Charpentier E (2013) The tracr RNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol 10:726–737
16. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823
17. Cooper HD, Spillane C, Hodgkin T (2001) Broadening the genetic base of crop production. CAB International, Wallingford
18. D’Halluin K, Vanderstraeten C, Van HJ, Rosolowska J, Van DBI, Pennewaert A, D’Hont K, Bossut M, Jantz D, Ruiter R, Broadhvest J (2013) Targeted molecular trait stacking in cotton through targeted double-strand break induction. Plant Biotechnol J 11:933–941
19. 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
20. Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096
21. Du H, Zeng X, Zhao M, Cui X, Wang Q, Yang H, Cheng H, Yu D (2016) Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol 217:90–97
22. Esvelt KM, Smidler AL, Catteruccia F, Church GM (2014) Concerning RNA-guided gene drives for the alteration of wild populations. Elife 3:e03401. doi:10.7554/eLife.03401
23. 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
24. Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P et al (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232
25. Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK (2014) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32:279–284
26. Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405
27. Gantz VM, Bier E (2015) Genome editing: the mutagenic chain reaction, a method for converting heterozygous to homozygous mutations. Science 348:442–444
28. Gao J, Wang G, Ma S, Xie X, Wu X, Zhang X, Wu Y, Zhao P, Xia Q et al (2014) CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol 10:127–139
29. Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R, Boyaval R, Fremaux C, Horvath P, Magadan AH, Moieau S (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71
30. Grissa I, Vergnaud G, Pourcel C (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinform 8:172
31. Heler R, Samai P, Modell JW, Weiner C, Goldberg GW, Bikard D, Marraffini LA (2014) Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature 519(7542):199–202
32. Hyun Y, Kim J, Cho SW, Choi Y, Kim J, Coupland G (2015) Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles. Planta 241:271–284
33. 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. J Bacteriol 169:5429–5433
34. Ito Y, Yokoi AN, Endo M, Mikami M, Toki S (2015) CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem Biophys Res Commun 467:76–82
35. Jain M (2015) Function genomics of abiotic stress tolerance in plants: a CRISPR approach. Front Plant Sci 6:375
36. Jansen R, Embden JDAV, Gaastra W, Schouls LM (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43:1565–1575
37. Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE 9(4):93806
38. 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 Acid Res 41:188
39. 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(6096):816–821
40. Jinek M, Jiang F, Taylor DW, Sternberg SH, Kaya E, Ma E, Anders C, Hauer M, Zhou K, Lin S, Kaplan M, Iavarone AT, Charpentier E, Nogales E, Doudna JA (2014) Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science 343:1247997
41. Kim JM, Kim D, Kim S, Kim JS (2014) Genotyping with CRISPR-Cas-derived RNA-guided endonucleases. Nat Commun 5:3157
42. Kolata G (2015) Chinese scientists edit genes of human embryos, raising concerns. The New York Times 23
43. Larson MH, Gilbert LA, Wang X, Lim WA, Weissman JS, Qi LS (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat Protoc 8:2180–2196
44. 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
45. Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP, Huang L et al (2015) Cas9-Guide RNA directed genome-editing in soybean. Plant Physiol 169:960–970
46. Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, Lin Q, Luo W, Wu G, Li H (2016) Reassessment of the four yield related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front Plant Sci. doi:10.3389/fpls.2016.00377
47. 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
48. Liu Z, Hirani AH, McVetty PB, Daayf F, Quiros CF, Li G (2012) Reducing progoitrin and enriching glucoraphanin in Brassica napus seeds through silencing of the GSL-ALK gene family. Plant Mol Biol 79:179–189
49. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826
50. Mao Y, Zhang H, Xu N, Zhang B, Gao F, Zhu JK (2013) Application of the CRISPR/Cas system for efficient genome engineering in plants. Mol Plant 6:2008–2011
51. Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845
52. Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23:1233
53. Mojica FJ, 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
54. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Almendros C (2009) Short motif sequences determines the targets of the prokaryotic CRISPR defence system. Microbiology 155:733–740
55. Nejat N, Rookes J, Mantri NL, Cahill DM (2016) Plant–pathogen interactions: toward development of next-generation disease-resistant plants. Crit Rev Biotechnol. Early Online:1–9
56. Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31:691–693
57. Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI, Dohmae N, Ishitani R, Zhang F, Nureki O (2014) Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156(5):935–949
58. Osakabe K, Osakabe Y, Toki S (2010) Site directed mutagenesis in Arabidopsis using custom designed zinc finger nucleases. Proc Natl Acad Sci USA 107:12034–12039
59. Peng R, Lin G, Li J (2016) Potential pitfalls of CRISPR/Cas9-mediated genome editing. FEBS J 283:1218–1231
60. Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S, Aouida M, Mahfouz MM (2014) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13(4):578–589
61. 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 151:653–663
62. Puchta H, Fauser F (2013) Gene targeting in plants: 25 years later. Int J Dev Biol 57:629–637
63. Ramirez CL, Foley JE, Wright DA, Müller-Lerch F, Rahman SH, Cornu TI, Winfrey RJ, Sander JD, Fu F, Townsend JA, Cathomen T, Voytas DF, Joung JK (2008) Unexpected failure rates for modular assembly of engineered zinc fingers. Nat Method 5:374–375
64. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380–1389
65. Sander JD, Joung JK (2014) CRISPR-cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32:347–355
66. 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 12:12704
67. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688
68. Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I (2014) CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant Cell Physiol 55:475–481
69. 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
70. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D et al (2014) Dimeric CRISPR RNA guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32:569–576
71. Tsz K, Martin T, Hong L (2015) Structure principles of CRISPR-Cas surveillance and effector complexes. Annu Rev Biophys 44:229–255
72. Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3 Genes 3:2233–2238
73. Voytas DF (2013) Plant genome engineering with sequence-specific nucleases. Annu Rev Plant Biol 64:327–350
74. Waltz E (2016) Gene-edited CRISPR mushroom escapes US regulation. Nature 532:293
75. 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
76. Wathelet JP, Marlier M, Severing M, Boenke A, Wagstaffe PJ (2006) Measurement of glucosinolates in rapeseeds. Nat Toxins 3:299–304
77. Wyman C, Kanaar R (2006) DNA double-strand break repair: all’s well that ends well. Annu Rev Genet 40:363–381
78. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14(14):327
79. 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 5:114
80. Zala NH, Bosamia CT, Shukla YM, Kumar S, Kulkarni KS (2016) Genome modifications in crops employing engineered nucleases. Agric Rev 37:154–159
81. Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N, Zhu JK (2014) The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 12:797–807
82. Zhang B, Yang X, Yang C, Li M, Guo Y (2016) Exploiting the CRISPR/Cas9 system for targeted genome mutagenesis in petunia. Sci Rep 6:20315
83. 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 Acid Res 42:10903–10914
84. 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