CRISPR/Cas9: A gene targeting technology and its application in the study of plant genetic function

doi:10.11686/cyxb2016430

Abstract

Abstract: CRISPR/Cas (clustered regularly interspaced short palindromic repeats) was derived from the adaptive immune system of bacteria and archaea to resist attacks from invasive viruses and exogenous DNA. Comparing zinc finger nuclease (ZFN) and transcription activator-like effector nuclease (TALENs), the type II CRISPR/Cas9 system mediated by RNA breaks new ground for gene editing due to its efficiency, low cost and ease of operation for the study of genetic function. This review summarizes recent research and progress of the structure, mechanisms and application of CRISPR/Cas9 for the study of genetic function and crop breeding. We also investigate the potential future development of CRISPR/Cas9.

BAO Ai-Ke, BAI Tian-Hui, ZHAO Tian-Xuan, SU Jia-Hao. CRISPR/Cas9: A gene targeting technology and its application in the study of plant genetic function[J]. Acta Prataculturae Sinica, 2017, 26(7): 190-200.

References

[1] Nadiya O, Anzhela K, Holger P. Different pathways of homologous recombination are used for the repair of double-strand breaks within tandemly arranged sequences in the plant genome. Plant Journal, 2003, 35(5): 604-612.
[2] Mladenov E, Magin S, Soni A, et al . DNA double-strand break repair as determinant of cellular radiosensitivity to killing and target in radiation therapy. Frontiers in Oncology, 2013, 3: 113.
[3] Hsu P, Lander E, Zhang F. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 2014, 157(6): 1262-1278.
[4] Voytas D F. Plant genome engineering with sequence-specific nucleases. Annual Review of Plant Biology, 2013, 64: 327-350.
[5] Puchta H, Fauser F. Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant Journal, 2014, 78(5): 727-741.
[6] Epinat J C, Arnould S, Chames P, et al . A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucleic Acids Research, 2003, 31(11): 2952-2962.
[7] Chevalier B S, Stoddard B L. Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucleic Acids Research, 2001, 29(18): 3757-3774.
[8] Zhang D B, Shi P, Pang X N. Research progress in engineered nucleases for genome site-specific editing. Basic & Clinical Medicine, 2013, 33(12): 1634-1637.
张殿宝, 施萍, 庞希宁. 人工核酸酶用于基因组定点编辑的研究进展. 基础医学与临床, 2013, 33(12): 1634-1637.
[9] Urnov F D, Rebar E J, Holmes M C, et al . Genome editing with engineered zinc finger nucleases. Nature Reviews Genetics, 2010, 11(9): 636-646.
[10] Éva Scheuring Vanamee, Santagata S, Aggarwal A K. FokⅠ requires two specific DNA sites for cleavage. Journal of Molecular Biology, 2001, 309: 69-78.
[11] Zeng M H, Jiang M B, Cai L H. Comparison of ZFNs and TALENs in the application of genetic modification. International Journal of Genetics, 2013, 36(6): 257-260.
曾敏慧, 蒋满波, 蔡柳洪. ZFNs和TALENs在基因修饰中的应用比较. 国际遗传学杂志, 2013, 36(6): 257-260.
[12] Ramirez C L, Foley J E, Wright D A, et al . Unexpected failure rates for modular assembly of engineered zinc fingers. Nature Methods, 2008, 5(5): 374-375.
[13] He L X Z, Chen H D, Xiao L. Molecular “scissors”—TALENs mediated site—specific gene. Chinese Journal of Cell Biology, 2013, 35(8): 1205-1210.
何丽夏子, 陈海德, 肖磊. 分子“剪刀”——TALENs介导的定点基因修饰技术. 中国细胞生物学学报, 2013, 35(8): 1205-1210.
[14] Bogdanove A J, Voytas D F. TAL effectors: customizable proteins for DNA targeting. Science, 2011, 333(6051): 1843-1846.
[15] Mussolino C, Cathomen T. RNA guides genome engineering. Nature Biotechnology, 2013, 31(3): 208-209.
[16] Ishino Y, Shinagawa H, Makino K, et al . Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli , and identification of the gene product. Journal of Bacteriology, 1987, 169(12): 5429-5433.
[17] Mojica V C, Soria E, Juez G. Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria (letter). Molecular Microbiology, 2000, 36(1): 244-246.
[18] Jansen R, Embden J D A V, Gaastra W, et al . Identification of genes that are associated with DNA repeats in prokaryotes. Molecular Microbiology, 2002, 43(6): 1565-1575.
[19] Gupta S K, John S, Naik R, et al . A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. Plos Computational Biology, 2005, 1(6): e60.
[20] Makarova K S, Haft D H, Barrangou R, et al . Evolution and classification of the CRISPR-Cas systems. Nature Reviews Microbiology, 2011, 9(6): 467-477.
[21] Mojica F J M, Chcsar Díez-Villaseñor, García-Martínez J, et al . Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. Journal of Molecular Evolution, 2005, 60(2): 174-182.
[22] Pourcel C, Salvignol G, Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology, 2005, 151(3): 653-663.
[23] Bolotin A, Quinquis B, Sorokin A, et al . Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 2005, 151: 2551-2561.
[24] Barrangou R, Fremaux C, Deveau H, et al . CRISPR provides acquired resistance against viruses in prokaryotes. Science, 2007, 315(5819): 1709-1712.
[25] Jinek M, Chylinski K, Fonfara I, et al . A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 2012, 337(6096): 816-821.
[26] Mandal P, Ferreira L M R, Collins R, et al . Efficient ablation of genes in human hematopoietic stem and effector cells using CRISPR/Cas9. Cell Stem Cell, 2014, 15(5): 643-652.
[27] Chen X, Xu F, Zhu C, et al . Dual sgRNA-directed gene knockout using CRISPR/Cas9 technology in Caenorhabditis elegans . Scientific Reports, 2014, 4: 7581.
[28] Auer T O, Duroure K, Concordet J P, et al . CRISPR/Cas9-mediated conversion of eGFP- into Gal4-transgenic lines in zebrafish. Nature Protocols, 2014, 9(12): 2823-2840.
[29] Zhu S, Rong Z, Lu X, et al . Gene targeting through homologous recombination in monkey embryonic stem cells using CRISPR/Cas9 system. Stem Cells & Development, 2015, 24(10): 1147-1149.
[30] Seeger C, Ji A S. Targeting hepatitis B virus with CRISPR/Cas9. Molecular Therapy Nucleic Acids, 2014, 3: e216.
[31] Yuen K S, Chan C P, Wong N H, et al . CRISPR/Cas9-mediated genome editing of Epstein-Barr virus in human cells. Journal of General Virology, 2015, 96: 626-636.
[32] Osborn M J, Gabriel R, Webber B R, et al . Fanconi anemia gene editing by the CRISPR/Cas9 system. Human Gene Therapy, 2015, 26(2): 114-126.
[33] Grissa I, Vergnaud G, Pourcel C. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics, 2007, 8: 172.
[34] Karginov F V, Hannon G J. The CRISPR system: small RNA-guided defense in bacteria and archaea. Molecular Cell, 2010, 37(1): 7-19.
[35] Feng Z, Zhang B, Ding W, et al . Efficient genome editing in plants using a CRISPR/Cas system. Cell Research, 2013, 23(10): 1229-1232.
[36] Wei C, Liu J, Yu Z, et al . TALEN or Cas9-rapid, efficient and specific choices for genome modifications. Journal of Genetics & Genomics, 2013, 40(6): 281-289.
[37] Li J, Zhang Y, Chen K L, et al . CRISPR/Cas: a novel way of RNA-guided genome editing. Hereditas, 2013, 35(11): 1265-1273.
李君, 张毅, 陈坤玲, 等. CRISPR/Cas系统: RNA靶向的基因组定向编辑新技术. 遗传, 2013, 35(11): 1265-1273.
[38] Wang T, Birsoy K, Hughes N W, et al . Identification and characterization of essential genes in the human genome. Science, 2015, 350(6264): 1096-1101.
[39] Lillestøl R K, Redder P, Garrett R A, et al . A putative viral defence mechanism in archaeal cells. Archaea, 2006, 2(1): 59-72.
[40] Deltcheva E, Chylinski K, Sharma C M, et al . CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 2011, 471(7340): 602-607.
[41] Li T M, Du B. CRISPR-Cas system and coevolution of bacteria and phages. Hereditas, 2011, 33(3): 213-218.
李铁民, 杜波. CRISPR-Cas系统与细菌和噬菌体的共进化. 遗传, 2011, 33(3): 213-218.
[42] Mojica F J M, Díezvillaseñor C, Garcíamartínez J, et al . Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology, 2009, 155(3): 733-740.
[43] Sternberg S H, Redding S, Jinek M, et al . DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, 2014, 507(7490): 62-67.
[44] Jinek M, Jiang F, Taylor D W, et al . Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science, 2014, 343(6176): 1247997.
[45] Nishimasu H, Ran F A, Hsu P, et al . Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell, 2014, 156(5): 935-949.
[46] Bhaya D, Davison M, Barrangou R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annual Review of Genetics, 2011, 45: 273-297.
[47] Beloglazova N, Brown G, Zimmerman M D, et al . A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. Journal of Biological Chemistry, 2008, 283(29): 20361-20371.
[48] Pougach K, Semenova E E, Datsenko K A, et al . Transcription, processing and function of CRISPR cassettes in Escherichia coli . Molecular Microbiology, 2010, 77(6): 1367-1379.
[49] Brouns S J J, Jore M M, Lundgren M, et al . Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 2008, 321(5891): 960-964.
[50] Garneau J E, Dupuis M É, Villion M, et al . The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 2010, 468(7320): 67-71.
[51] Cong L, Ran F A, Cox D, et al . Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339(6121): 819-823.
[52] Mali P, Church G M. RNA-guided human genome engineering via Cas9. Science, 2013, 339(6121): 823-826.
[53] Xu R, Li H, Qin R, et al . Gene targeting using the Agrobacterium tumefaciens -mediated CRISPR-Cas system in rice. Rice(N Y), 2014, 7(1): 5.
[54] Li J F, Norville J E, Aach J, et al . Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology, 2013, 31(8): 688-691.
[55] Nekrasov V, Staskawicz B, Weigel D, et al . Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nature Biotechnology, 2013, 31(8): 691-693.
[56] Shan Q, Wang Y, Li J, et al . Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology, 2013, 31(8): 686-688.
[57] Mao Y, Zhang H, Xu N, et al . Application of the CRISPR-Cas system for efficient genome engineering in plants. Molecular Plant, 2013, 6(6): 2008-2011.
[58] Upadhyay S K, Kumar J, Alok A, et al . RNA-guided genome editing for target gene mutations in wheat. G3-Genes Genomes Genetics, 2013, 3(12): 2233-2238.
[59] Zhang H, Zhang J, Wei P, et al . The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnology Journal, 2014, 12: 797-807.
[60] Kabin, Yinong, Yang. RNA-Guided genome editing in plants using a CRISPR-Cas system. Molecular Plant, 2013, 6(6): 1975-1983.
[61] Belhaj K, Chaparro-Garcia A, Kamoun S, et al . Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods, 2013, 9(1): 39.
[62] Yin K, Han T, Liu G, et al . A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Scientific Reports, 2015, 5: 14926.
[63] Jiang W, Zhou H, Bi H, et al . Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis , tobacco, sorghum and rice. Nucleic Acids Research, 2013, 41(20): e188.
[64] Jia H, Wang N. Targeted genome editing of sweet orange using Cas9/sgRNA. Plos One, 2014, 9(4): e93806.
[65] Fan D, Liu T, Li C, et al . Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Scientific Reports, 2015, 5: 12217.
[66] Meng Y, Hou Y, Wang H, et al . Targeted mutagenesis by CRISPR/Cas9 system in the model legume Medicago truncatula . Plant Cell Reports, 2017, 36(2): 371-374.
[67] Lozano-Juste J, Cutler S R. Plant genome engineering in full bloom. Trends in Plant Science, 2014, 19(5): 284-287.
[68] Qi L S, Larson M H, Gilbert L A, et al . Repurposing CRISPR as an RNA-Guided platform for sequence-specific control of gene expression. Cell, 2013, 152(5): 1173-1183.
[69] Zhang D W, Zhang C F, Dong F, et al . Application of CRISPR/Cas9 system in breeding of new antiviral plant germplasm. Hereditas, 2016, 38(9): 811-820.
张道微, 张超凡, 董芳, 等. CRISPR/Cas9系统在培育抗病毒植物新种质中的应用. 遗传, 2016, 38(9): 811-820.
[70] Ji X, Zhang H, Zhang Y, et al . Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nature Plants, 2015, 1(10): 15144.
[71] Baltes N J, Hummel A W, Konecna E, et al . Conferring resistance to geminiviruses with the CRISPR-Cas prokaryotic immune system. Nature Plants, 2015, 1(10): 15145.
[72] Zhang Y, Liang Z, Zong Y, et al . Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nature Communications, 2016, 7: 12617.
[73] Wiles M V, Qin W, Cheng A W, et al . CRISPR-Cas9-mediated genome editing and guide RNA. Mammalian Genome, 2015, 26(9/10): 501-510.
[74] Fu Y, Foden J A, Khayter C, et al . High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nature Biotechnology, 2013, 31(9): 822-826.
[75] Hsu P D, Scott D A, Weinstein J A, et al . DNA targeting specificity of RNA-guided Cas9 nucleases. Nature Biotechnology, 2013, 31(9): 827-832.
[76] Fu Y, Sander J D, Reyon D, et al . Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nature Biotechnology, 2014, 32(3): 279-284.
[77] Ran F A, Hsu P, Lin C Y, et al . Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 2013, 154(6): 1380-1389.
[78] Shen B, Zhang W, Zhang J, et al . Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nature Methods, 2014, 11(4): 399-402.
[79] Guilinger J P, Thompson D B, Liu D R. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nature Biotechnology, 2014, 32(6): 577-582.
[80] Tsai S Q, Wyvekens N, Khayter C, et al . Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nature Biotechnology, 2014, 32(6): 569-576.
[81] Miao J, Guo D, Zhang J, et al . Targeted mutagenesis in rice using CRISPR-Cas system. Cell Research, 2013, 23(10): 1233-1236.
[82] Brooks C, Nekrasov V, Lippman Z B, et al . Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiology, 2014, 166(3): 1292-1297.
[83] Sugano S S, Shirakawa M, Takagi J, et al . CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant & Cell Physiology, 2014, 55(3): 475-481.
[84] Zhou H, Bo L, Weeks D P, et al . Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Research, 2014, 42(17): 10903-10914.
[85] Jacobs T B, Lafayette P R, Schmitz R J, et al . Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnology, 2015, 15: 16.
[86] 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 Journal, 2014, 80(6): 1139-1150.
[87] Xing H L, Dong L, Wang Z P, et al . A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biology, 2014, 14: 327.