Application of genome editing tools in plants
Author affiliations
DOI:
https://doi.org/10.15625/1811-4989/15464Abstract
Genome editing technology is the genome modification techniques, such as targeted mutagenesis or insert/delete/replacement at specific locations in the genome of living organisms. Genome editing is based on the creation of double sequence break (DSB) in a specific location and DNA repair via nonhomologous end joining (NHEJ) or homology direct repair (HDR). The development of sequence-specific nuclease (SSN) allows precise editing of the target gene. These SSNs include: meganuclease (MN), zinc finger nuclease (ZFN), transcription activator-like effector nuclease (TALEN) and CRISPR-associated nuclease (Cas) including CRISPR/Cas9 (from Streptococcus pyogenes) and CRISPR/Cpf1 (from Prevoltella and Francisella1). These are the genome editing tools used to create DSBs at specific locations of the genome. Recently, the base editing (BE) and prime editing (PE) tools have been reported. This review will cover the basics of these tools and their application in genome editing in plants, especially providing the most up-to-date information on their application in crop improvement.
Downloads
References
TAÌ LIỆU THAM KHẢO
• Ainley WM, Sastry-Dent L, Welter ME, Murray MG, Zeitler B, Amora R, Corbin DR, Miles RR, Arnold NL, Strange TL, Simpson MA, Cao Z, Carroll C, Pawelczak KS, Blue R, West K, Rowland LM, Perkins D, Samuel P, Dewes CM, Shen L, Sriram S, Evans SL, Rebar EJ, Zhang L, Gregory PD, Urnov FD, Webb SR, Petolino JF (2013) Trait stacking via targeted genome editing. Plant Biotechnol J 11(9): 1126-1134
• Ali Z, Abul-faraj A, Li L, Ghosh N, Piatek M, Mahjoub A, Aouida M, Piatek A, Baltes NJ, Voytas DF, Dinesh-Kumar S, Mahfouz MM (2015) Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant 8: 1288-1291
• Andersson M, Turesson H, Nicolia A, Fält AS, Samuelsson M, Hofvander P (2017) Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Rep 36: 117-128
• Andersson M, Turesson, H, Olsson N, Fält AS, Ohlsson P, Gonzalez MN, Samuelsson M, Hofvander P (2018) Genome editing in potato via CRISPR-Cas9 ribonucleoprotein delivery. Physiol Plant 164: 378-384
• Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen PJ, Wilson C, Newby GA, Raguram A, Liu DR (2019) Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576: 149-157
• Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF (2014) DNA replicons for plant genome engineering. Plant Cell 26: 151-163
• Bernabe-Orts JM, Casas-Rodrigo I, Minguet EG, Landolfi V, Garcia-Carpintero V, Gianoglio S, Vazquez-Vilar M, Granell A, Orzaez D (2019) Assessment of Cas12a-mediated gene editing efficiency in plants. Plant Biotech J 17: 1971-1984
• Bertier LD, Ron M, Huo H, Bradford K J, Britt A B, Michelmore RW (2018) High-resolution analysis of the efficiency, heritability, and editing outcomes of CRISPR-Cas9 -induced modifications of NCED4 in lettuce (Lactuca sativa). G3 8: 1513-1521
• Bhaya D, Davison M, and Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: Versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 45: 273-279
• Bibikova M, Beumer K, Trautman JK, Carroll D (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300: 764, doi: 10.1126/science.1079512
• Blanvillain-Baufume S, Reschke M, Sole M, Auguy F, Doucoure H, Szurek B, Meynard D, Portefaix M, Cunnac S, Guiderdoni E, Boch J,Koebnik R (2017) Targeted promoter editing for rice resistance to Xanthomonas oryzae pv Oryzae reveals differential activities for SWEET14-inducing TAL efectors. Plant Biotechnol J 15(3): 306-317
• Bogdanove AJ, Voytas DF (2011) TAL effectors: Customizable proteins for DNA targeting. Science 333: 1843-1846
• 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: 1509-1512
• Bonawitz ND , Ainley WM, Itaya A, Chennareddy SR, Cicak T, Effinger K, Jiang K, Mall TK, Marri PR, Samuel JP, Sardesai N, Simpson M, Folkerts O, Sarria R, Webb SR, Delkin, Gonzalez DO, Simmonds DH, Dayakar R, Pareddy DR (2019) Zinc finger nuclease-mediated targeting of multiple transgenes to an endogenous soybean genomic locus via non-homologous end joining. Plant Biotech J 17: 750-761
• Braatz, J, Harloff HJ, Mascher M, Stein N, Himmelbach A, Junget C (2017) CRISPR-Cas9 targeted mutagenesis leads to simultaneous modification of different homoeologous gene copies in polyploidy oilseed rape (Brassica napus). Plant Physiol 174: 935-942
• Brinkman EK, Chen T, Amendola M, van Steensel B (2014) Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res 42 (22): e168
• Brooks C, Nekrasov V, Lippman Z B, and 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
• Budhagatapalli N, Rutten T, Gurushidze M, Kumlehn J, Hensel G (2015) Targeted modifcation of gene function exploiting homologydirected repair of TALEN-mediated double-strand breaks in barley. G3 (Bethesda) 5(9): 1857-63
• Butler NM, Baltes NJ, Voytas DF, Douches DS (2016) Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence specific nucleases. Front Plant Sci 7: 1045
• Butt H, Eid A, Ali Z, Atia MAM, Mokhtar MM, Hassan N, Lee CM, Bao G, Mahfouz MM (2017) Efficient CRISPR/Cas9-mediated genome editing using a chimeric single-guide RNA molecule. Front Plant Sci 8: 1441
• Butt H, Rao GS, Sedeek K, Aman R, Kamel R, Mahfouz M (2020) Engineering herbicide resistance via prime editing in rice. Plant Biotech J: 1-3, doi: 10.1111/pbi.13399
• Cai CQ, Doyon Y, Ainley WM, Miller JC, Dekelver RC, Moehle EA, Rock JM, Lee YL, Garrison R, Schulenberg L, Blue R, Worden A, Baker L, Faraji F, Zhang L, Holmes MC, Rebar EJ, Collingwood TN, Rubin-Wilson B, Gregory PD, Urnov FD, Petolino JF (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol 69: 699-709
• Cai Y, Chen L, Zhang Y, Yuan S, Su Q, Sun S, Wu C, Yao W, Han T, Hou W (2020) Target base editing in soybean using a modified CRISPR/Cas9 system. Plant Biotech J 1-3, doi: 10.1111/pbi.13386
• Cantos C, Francisco P, Trijatmiko KR, Slamet-Loedin I, Chadha-Mohanty PK (2014) Identification of “safe harbor” loci in indica rice genome by harnessing the property of zinc-finger nucleases to induce DNA damage and repair. Front Plant Sci 5: 302
• Cebrian-Serrano A, Davies B (2017) CRISPR-Cas orthologues and variants: optimizing the repertoire, specificity and delivery of genome engineering tools. Mamm Genome 28: 247-261
• 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 Res 39(12): e82
• Cermak T, Baltes NJ, Cegan R, Zhang Y, Voytas DF (2015) High-frequency, precise modifcation of the tomato genome. Genome Biol 16(1): 232
• 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 17: 1140-1153
• Chao S, Cai, Feng B, Jiao G, Sheng Z, Luo J, Tang S, Wang J, Hu P, Wei X (2019) Editing of rice isoamylase gene ISA1 provides insights into its function in starch formation. ScienceDirect, Rice Sci 26(2): 77-87
• Char SN, Unger-Wallace E, Frame B, Briggs SA, Main M, Spalding MH, Vollbrecht E, Wang K, Yang B (2015) Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J 13(7): 1002-1010
• Char SN, Neelakandan AK, Nahampun H, Frame B, Main M, Spalding MH, Becraft PW, Meyers BC, Walbot V, Wang K, Yang B (2017) An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol J 15: 257-268
• Char SN, Wei J, Mu Q, Li X, Zhang ZJ, Yu J, Yan B (2020) An Agrobacterium-delivered CRISPR/Cas9 system for targeted mutagenesis in sorghum. Plant Biotech J 18: 319-321
• Che P, Anand A, Wu E, Sander JD, Simon MK, Zhu W, Sigmund AL, Zastrow‐Hayes G, Miller M, Liu D, Shai Lawit SJ, Zhao ZY, Albertsen MC, Joneset TJ (2018) Developing a flexible, high efficiency Agrobacterium-mediated sorghum transformation system with broad application. Plant Biotechnol J 16: 1388-1395
• 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. Sci Rep 7: 44304
• 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
• Christian M, Y Qi, Y Zhang, and D F Voytas, 2013. Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3: Genes Genomes Genet 3(9): 1697-1705
• Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, Daulhac A, Coffman A, Yabandith A, Retterath A, Haun W, Nicholas J, Baltes DS, Mathis L, Voytas DF, Zhang F (2016) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14(1):169-176
• Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini L A, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823
• Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C, Baltes NJ, Reyon D, Dahlborg EJ, Goodwin MJ, Coffman AP, Dobbs D, Joung JK, Voytas DF, Stupar RM (2011) Targeted mutagenesis of duplicated genes in soybean with zinc finger nucleases. Plant Physiol 156: 466-473
• Curtin SJ, Xiong Y, Michno JM, Campbell BW, Stec AO, Cermak T, Starker C, Voytas DF, Eamens AL, Stupar RM (2018) CRISPR/Cas9 and TALENs generate heritable mutations for genes involved in small RNA processing of Glycine max and Medicago truncatula. Plant Biotechnol J 16 : 1125-1137
• Dahlem TJ, Hoshijima K, Jurynec MJ, Gunther D, Starker CG, Locke AS, Weis AM, Voytas DF, Grunwald DJ (2012) Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet 8(8): e1002861
• de Lange O, Schreiber T, Schandry N, Radeck J, Braun KH, Koszinowski J, Heuer H, Strauß A, Lahaye T (2013) Breaking the DNA-binding code of Ralstonia solanacearum TAL effectors provides new possibilities to generate plant resistance genes against bacterial wilt disease. New Phytol 199: 773-786
• de Pater S, Neuteboom LW, Pinas JE, Hooykaas PJ, van der Zaal BJ (2009) ZFN-induced mutagenesis and gene-targeting in Arabidopsis through Agrobacterium-mediated floral dip transformation. Plant Biotechnol J 7: 821-835
• de Pater S, Pinas JE, Hooykaas PJJ, van der Zaal BJ (2013) ZFN-mediated gene targeting of the Arabidopsis protoporphyrinogen oxidase gene through Agrobacterium-mediated floral dip transformation. Plant Biotechnology J 11: 510-515
• Demorest ZL, Cofman A, Baltes NJ, Stoddard TJ, Clasen BM, Luo S, Retterath A, Yabandith A, Gamo ME, Bissen J, Mathis L, Voytas DF, Zhang F (2016) Direct stacking of sequence-specifc nuclease-induced mutations to produce high oleic and low linolenic soybean oil. BMC Plant Biol 16(1): 225, doi: 10.1186/s12870-016-0906-1
• D’Halluin K, Vanderstraeten C, Van Hulle J, Rosolowska J, Van Den Brande I, 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
• Djukanovic V, Smith J, Lowe K, Yang M, Gao H, Jones S, Nicholson MG, West A, Lape J, Bidney D, Falco SC, Jantz D, Lyznik LA (2013) Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. The Plant J 76: 888-899
• Dong D, Ren K, Qiu X, Zheng J, Guo M, Guan X, Liu H, Li N, Zhang B, Yang D, Ma C, Wang S, Wu D, Ma Y, Fan S, Wang J, Gao N, Huang Z (2016) The crystal structure of Cpf1 in complex with CRISPR RNA. Nature 532: 522-526
• 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
• Endo M, Mikami M, Toki S (2016) Biallelic gene targeting in rice. Plant Physiol 170: 667–677
• Endo A, Masafumi M, Kaya H, Toki S (2016a) Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Sci Rep 6: 38169
• 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, doi: 10.1038/srep12217
• Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu JK (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23: 1229-1232
• Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, Zeng L, Liu X, Zhu JK (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA 111(12): 4632-4637
• Fonfara I, Richter H, Bratovic M, Rhun A L, Charpentier E (2016) The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA.
Nature 532: 517-521
• Forner J, Pfeifer A, Langenecker T, Manavella PA, Lohmann JU (2015) Germline-transmitted genome editing in Arabidopsis thaliana using TAL-efector-nucleases. PLoS One 10(3): e0121056
• Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nature Biotech 31: 822-826
• Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D, Lyznik A (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. The Plant J 61: 176-187
• Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR (2017) Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage. Nature 551(7681): 464-471
• Gomez MA, Z Lin D, Mol T, Chauhan RD, Hayden L, Renninger K, Beyene G, Taylor NJ, Carrington JC, Staskawicz BJ, Bart RS (2019) Simultaneous CRISPR/Cas9-mediated editing of cassava eIF4E isoforms nCBP-1 and nCBP-2 reduces cassava brown
streak disease symptom severity and incidence. Plant Biotech J 17: 421-434
• Güell M, Yang L, Church GM (2014) Genome editing assessment using CRISPR Genome Analyzer (CRISPR-GA). Bioinformatics 30 (20): 2968-2970
• Gurushidze M, Hensel G, Hiekel S, Schedel S, Valkov V, Kumlehn J (2014) True-breeding targeted gene knock-out in barley using designer TALE nuclease in haploid cells. PLoS One 9(3): e92046
• Haun W, Cofman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF, Zhang F (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 12(7): 934-940
• Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170
• Hua K, Tao X, Yuan F, Wang D, Zhu J (2018) Precise A-T to G-C base editing in the rice genome. Mol Plant 11: 627-630
• Hua K, Jiang Y, Tao X, Zhu JK (2020) Precision genome engineering in rice using prime editing system. Plant Biotech J 1-3, doi: 10.1111/pbI13395
• Huang J, Li J, Zhou J, Wang L, Yang S, Hurst LD, Li WH, Tian D (2018) Identifying a large number of high-yield genes in rice by pedigree analysis, whole-genome sequencing, and CRISPR-Cas9 gene knockout. Proc Natl Acad Sci USA 115: E7559-E7567
• Huang L, Li Q, Zhang C, Chu R, Gu Z, Tan H, Zhao D, Fan X, Liu Q (2020) Creating novel Wx alleles with fine-tuned amylose levels and improved grain quality in rice by promoter editing using CRISPR/Cas9 system. Plant Biotech J 1-3, doi: 10.1111/pbI13391
• Hummel AW, Chauhan RD, Cermak T, Mutka AM, Vijayaraghavan A, Boyher A, Starker CG, Bart R, Voytas DF, Taylor NJ (2018) Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. Plant Biotechnol J 16(7): 1275-1282
• Iaffaldano B, Zhang Y, Cornish K (2016) CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection. Ind Crops Products 89: 356-362
• 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
• Jansing J, Sack M, Augustine SM, Fischer R, Bortesi L (2019) CRISPR/Cas9-mediated knockout of six glycosyltransferase genes in Nicotiana benthamiana for the production of
recombinant proteins lacking -1,2-xylose and core -1,3-fucose. Plant Biotech J 17: 350-361
• Jia HG, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PloS One 9: e93806
• Jia H, Zhang Y, Orbovic V, Xu J, White F, Jones J, Wang N (2016) Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15: 817-823
• Jia H, Orbovic V, Wang N (2019) CRISPR-LbCas12a-mediated modification of citrus. Plant Biotech J 17: 1928-1937
• 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, doi:10.1093/nar/ gkt780
• Jiang WZ, Henry IM, Lynagh PG, Comai L, Cahoon EB, Weeks DP (2017) Significant enhancement of fatty acid composition in seeds of the allohexaploid, Camelina sativa, using CRISPR/Cas9 gene editing. Plant Biotechnol J 15:648-57
• Jin S, Zong Y, Gao Q, Zhu Z, Wang Y, Qin P, Liang C, Wang D, Qiu JL, Zhang F, Gao C (2019) Cytosine, but not adenine, base editors induce genome-wide off-target mutations in rice. Science 364: 292-295
• 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
• Jung JH, 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 Mol Biol 92: 131-142
• Kannan B, Jung JH, Moxley GW, Lee SM, Altpeter F (2018) TALEN-mediated targeted mutagenesis of more than 100 COMT copies/alleles in highly polyploid sugarcane improves saccharification efficiency without compromising biomass yield. Plant Biotechnol J 16: 856-866
• Kim JM, Kim D, Kim S, Kim JS (2014) Genotyping with CRISPR-Cas derived RNA-guided endonucleases. Nat Commun DOI: 10.1038/ncomms4157
• Kim H, Kim S T, Ryu J, Kang B C, Kim J S, Kim SG (2017) CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat Commun 8: 14406
• Kim D, Kim D, Alptekin B, Budak H (2017) CRISPR/Cas9 genome editing in wheat Funct Integr Genomics 18: 31–41
• Kim YA, Moon H, Park CI (2019) CRISPR/Cas9-targeted mutagenesis of Os8N3 in rice to confer resistance to Xanthomonas oryzae pV Oryzae. Rice 12: 67 doiorg/10.1186/s12284-019-0325-7
• Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc fnger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA 93: 1156-1160
• Kirchner TW, Niehaus M, Debener T, Schenk MK, Herde M (2017) Efficient generation of mutations mediated by CRISPR/Cas9 in the hairy root transformation system of Brassica carinata. PLoS One 12(9): e0185429 https://doIorg/10.1371/journaLponE0185429
• Kleinstiver BP, Prew MS, Tsai SQ, Topkar V, Nguyen NT, Zheng Z, Gonzales APW, Li Z, Peterson RT, Yeh J-RJ, Martin J. Arye MJ, Joung JK (2015) Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 23: 523(7561): 481-485
• Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533(7603): 420-424
• Komor AC, Badran AH, Liu, DR (2017) CRISPR-Based technologies for the manipulation of eukaryotic genomes. Cell 168(1-2): 20-36
• Koonin EV, Makarova KS, Zhang F (2017) Diversity, classification and evolution of CRISPR-Cas systems. Curr Opin Microbiol 37: 67-78
• Lawrenson T, Shorinola O, Stacey N, Li C, Ostergaard L, Patron N, Uauy C, Harwood W (2015) Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol 16: 258
• Lee K, Zhang Y, Kleinstiver BP, Guo JA, Aryee MJ, Miller J, Malzahn A, Zarecor S, Lawrence-Dill CJ, Joung JK, Qi Y, Wang K (2019) Activities and specificities of CRISPR/Cas9 and Cas12a nucleases for targeted mutagenesis in maize. Plant Biotech J 17: 362-372
• Li B, Rui H, Li Y, Wang Q, Alariqi M, Qin L, Sun L, Ding X, Wang F, Zou J, Wang Y, Yuan D, Zhang X, Jin S (2019) Robust CRISPR/Cpf1 (Cas12a)-mediated genome editing in allotetraploid cotton (Gossypium hirsutum). Plant Biotech J 17: 1862-1864
• Li C, Zong Y, Wang Y, Jin S, Zhang D, Song Q, Zhang R, Gao C (2018) Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion. Genome Biol 19(1): 59
• Li C, Li W, Zhou Z, Chen H, Xie C, Lin Y (2020) A new rice breeding method: CRISPR/Cas9 system editing of the Xa13 promoter to cultivate transgene-free bacterial
blight-resistant rice. Plant Biotech J 18: 313-315
• Li H, Qin R, Liu X, Liao S, Xu R, Yang J, Wei P (2019) CRISPR/Cas9-mediated adenine Base editing in rice genome. ScienceDirect, Rice Sci 26(2): 125-128
• Li H, Li J Chen J, Yan L, Xia L (2020) Precise modifications of both exogenous and endogenous genes in rice by prime editing. Mol Plant 13: 671–674
• 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
• Li J, Stoddard TJ, Demorest ZL, Lavoie PO, Luo S, Clasen BM, Cedrone F, Ray EE, Cofman AP, Daulhac A, Yabandith A, Retterath AJ, Mathis L, Voytas DF, D'Aoust MA, Zhang F (2016) Multiplexed, targeted gene editing in Nicotiana benthamiana for glyco-engineering and monoclonal antibody production. Plant Biotechnol J 14(2): 533-542
• Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, Li J, Gao C (2016a) Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plants 2: 16139
• Li J, Zhang H, Si X, Tian Y, Chen K, Liu J, Chen H, Gao C (2017) Generation of thermosensitive male-sterile maize by targeted knockout of the ZmTMS5 gene. J Genet Genomics 44(9): 465-468
• Li J, Sun Y, Du J, Zhao Y, Xia L (2017a) Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol Plant 10: 526-529
• Li J, Manghwar H, Sun L, Wang P, Wang G, Sheng H, Zhang J, Liu H, Qin L, Rui H, Li B, Lindsey K, Daniell H, Jin S, Zhang X (2019) Whole genome sequencing reveals rare off-target mutations and considerable inherent genetic or/and somaclonal variations in CRISPR/Cas9-edited cotton plants. Plant Biotechnol J 17: 858-868
• Li L, Piatek MJ, Atef A, Piatek A, Wibowo A, Fang X, Sabir JSM, Zhu JK, Mahfouz MM (2012) Rapid and highly efficient construction of TALE-based transcriptional regulators and nucleases for genome modification. Plant Mol Biol 78(4-5): 407-416
• Li L, Atef A, Piatek A, Ali Z, Piatek M, Aouida M, Sharakou A, Mahjoub A, Wang G, Khan S, Fedoroff NV, Zhu JK, Mahfouz, M (2013) Characterization and DNA-binding specificities of Ralstonia TAL-like effectors. Mol Plant 6: 1318-1330
• 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 7: 377- doi: 10.3389/fplS2016.00377
• Li R, Fu D, Zhu B, Luo Y, Zhu H (2018) CRISPR/Cas9-mediated mutagenesis of lncRNA1459 alters tomato fruit ripening. Plant J 94: 513-524
• Li R, Li R, Li X, Fu D, Zhu B, Tian H, Luo Y, Zhu H (2018a) Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol J 16(2): 415-427
• Li S, Zhang Y, Xia L, Yiping Qi Y (2020) CRISPR-Cas12a enables efficient biallelic gene targeting in rice. Plant Biotech J 18: 1351-1353
• Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-effciency TALEN-based gene editing produces disease-resistant rice. Nat Biotech 30: 390-392
• Li T, Liu B, Chen CY, Yang B (2016) TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J Genet Genom 43(5): 297–305
• Li T, Yang X, Yu Y, Si X, Zhai X, Zhang H, Dong W, Gao C, Xu C (2018) Domestication of wild tomato is accelerated by genome editing. Nat Biotechnol doi:https:// doIorg/10.1038/nbT4273.
• Li X, Wang Y, Chen S, Tian H, Fu D, Zhu B, Luo Y, Zhu H (2018) Lycopene is enriched in tomato fruit by CRISPR/Cas9-mediated multiplex genome editing. Front Plant Sci 9: 559, doi: 10.3389/fplS2018.00559
• Li Z, Liu Z B, Xing A, Moon BP, Koellhoffer J P, Huang L, Ward R T, Clifton E, Falco SC, Cigan AM (2015) Cas9-guide RNA directed genome editing in soybean. Plant Physiol 169: 960-970
• 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(2): 63-68
• 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. Nat Commun 8: e14261
• Liang Z, Chen K, Yan Y, Zhang Y, Gao C (2018) Genotyping genome-edited mutations in plants using CRISPR ribonucleoprotein complexes. Plant Biotech J 16: 2053-2062
• Liang Z, Chen K, Zhang Y, Liu J, Yin K, Qiu JL, Gao C (2018b) Genome editing of bread wheat using biolistic delivery of CRISPR/Cas9 in vitro transcripts or ribonucleoproteins. Nat Protoc 13: 413-430
• Lin Q, Zong Y, Xue C, Wang S, Jin S, Zhu Z, Wang Y, Anzalone AV, Raguram A, Doman JL, Liu DR, Caixia Gao C (2020) Prime genome editing in rice and wheat. Nat Biotechnol 38(5): 582-585
• Liu W, Xie X, Ma X, Li J, Chen J, Liu YG (2015) DSDecode: a web-based tool for decoding of sequencing chromatograms for genotyping of targeted mutations. Mol Plant 8 (9): 1431-1433
• Liu HJ, Jian L, Xu J, Zhang Q, Zhang M, Jin M, Peng Y, Yan J, Han B, Liu J, Gao F, Liu X, Huang L, Wei W, Ding Y, Yang X, Li Z, Zhang M, Sun J, Bai M, Song W, Chen H, Sun X, Li W, Lu Y, Liu Y, Zhao J, Qian Y, Jackson D, Fernie AR, Yan J (2020) High-throughput CRISPR/Cas9 mutagenesis streamlines trait gene identification in maize. The Plant Cell 32: 1397-1413
• Lloyd A, Plaisier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natt Acad Sci USA 102: 2232-2237
• Lor VS, Starker CG, Voytas DF, Weiss D, Olszewski NE (2014) Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol 166: 1288-1291
• Lopez-Obando M, Hoffmann B, Gery C, Guyon-Debast A, Teoule E, Rameau C, Bonhomme S, Nogue F (2016) Simple and efficient targeting of multiple genes through CRISPR-Cas9 in Physcomitrella patens. G3 6: 3647-3653
• Lu Y, Zhu J K (2017) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol Plant 10: 523-525
• Lu K, Wu B, Wang J, Zhu W, Nie H, Qian J, Huang W, Fang Z (2018) Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnol J 16: 1710-1722
• Ma L, Zhu F, Li Z, Zhang J, Li X, Dong J, Wang T (2015) TALEN-based mutagenesis of lipoxygenase LOX3 enhances the storage tolerance of rice (Oryza sativa) seeds. PLoS One 10(12): e0143877
• Mahfouz M M, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu J K (2011) De novo-engineered transcription activator-like effector TALE hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci USA 108: 2623-2628
• Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJM, Tern RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV (2015) An updated evolutionary classification of CRISPR–Cas systems. Nat Rev Microbiol 13(11): 722-736
• Mali P, Yang L, Esvelt KM, Aach J, Guell M, Dicarlo JE, Norville J E, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339: 823
• Malnoy M, Viola R, Jung MH, Koo OJ, Kim S, Kim JS, Velasco R, Nagamangala Kanchiswamy C (2016) DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins, Front Plant Sci 7: e01904, https://doIorg/10.3389/fplS2016.01904
• Mao Y, Zhang H, Xu N, Zhang B, Gao F, Zhu JK (2013) Application of the CRISPRCas system for efficient genome engineering in plants. Mol Plant doi:10.1093/mp/sst121
• 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
• Michno JM, Wang X, Liu J, Curtin SJ, Kono TJY, Stupar RM (2015) CRISPR/Cas mutagenesis of soybean and Medicago truncatula using a new web-tool and a modified Cas9 enzyme. GM Crops Food 6: 243-252
• Morbitzer R, Römer P, Boch J, Lahaye T (2010) Regulation of selected genome loci using de novo-engineered transcription activatorlike effector (TALE)-type transcription factors. Proc Natl Acad Sci USA 107: 21617-21622
• 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
• Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S (2017) Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep 7: 482
• Nicolia A, Proux-Wera E, Ahman I, Onkokesung N, Andersson M, Andreasson E, Zhu LH (2015) Targeted gene mutation in tetraploid potato through transient TALEN expression in protoplasts. J Biotechnol 204:17-24
• Nishimasu H, Shi X, Ishiguro S, Gao L, Hirano S, Okazaki S, Noda T, Abudayyeh OO, Gootenberg JS, Mori H, Oura S, Holmes B, Tanaka M, Seki M, Hirano H, Aburatani H, Ishitani R, Ikawa M, Yachie N, Zhang F, Nureki O (2018) Engineered CRISPR-Cas9 nuclease with expanded targeting space. Science 361: 1259-1262
• 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. Sci Rep 6: 31481
• Nishizawa-Yokoi A, Cermak T, Hoshino T, Sugimoto K, Saika H, Mori A, Osakabe K, Hamada M, Katayose Y, Starker C, Voytas DF, Toki S (2016) A defect in DNA Ligase4 enhances the frequency of TALEN-mediated targeted mutagenesis in rice. Plant Physiol 170(2): 653-666
• Odipio J, Alicai T, Ingelbrecht I, Nusinow DA, Bart R, Taylor NJ (2017) Efficient CRISPR/Cas9 genome editing of phytoene desaturase in cassava. Front Plant Sci 8: 1780, doi: 10.3389/fplS2017.01780
• 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 Physiol Biochem 131: 63-69
• Ortigosa A, Gimenez-Ibanez S, Leonhardt N, Solano R (2019) Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of SlJAZ2. Plant Biotechnol J 17: 665-673
• Osakabe K, Osakabe Y, Toki S (2010) Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc Nat Acad Sci USA 107(26): 12034-12039
• Petolino JF, Worden A, Curlee K, Connell J, Tonya L, Moynahan S, Larsen C, Russell S (2010) Zinc finger nucleasemediated transgene deletion. Plant Mol Biol 73(6): 617-628
• Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56(409): 1-14
• Qi W, Zhu T, Tian Z, Li C, Zhang W, Song R (2016) High-efficiency CRISPR/Cas9 multiplex gene editing using the glycine tRNA-processing system-based strategy in maize. BMC Biotechnol 16: 58
• Qin L, Li J, Wang Q, Xu Z, Sun L, Alariqi M, Manghwar H, Wang G, Li B, Ding X, Rui H, Huang H, Lu T, Lindsey K, Daniell H , Zhang X, Jin S (2020). High-efficient and precise base editing of C•G to T•A in the allotetraploid cotton (Gossypium hirsutum) genome using a modified CRISPR/Cas9 system. Plant Biotech J 18: 45-56
• Ramlee MK, Yan T, Cheung AM, Chuah CT, Li S (2015) High throughput genotyping of CRISPR/Cas9-mediated mutants using fluorescent PCR-capillary gel electrophoresis. Sci Rep 5: 15587
• Ramlee MK, Wang J, Cheung AM, Li S (2017) Using a fluorescent PCR-capillary gel electrophoresis technique to genotype CRISPR/ Cas9-mediated knockout mutants in a high-throughput format. J Vis Exp 122: e55586, doi:10.3791/55586
• 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. Sci Rep 6: 32289
• Ren B, Yan F, Kuang Y, Li N, Zhang D, Zhou X, Lin H, Zhou H (2018) Improved base editor for efficiently inducing genetic variations in rice with CRISPR/Cas9-guided hyperactive hAID mutant. Mol Plant 11(4): 623-626
• Sanchez-Leon S, Gil-Humanes J, Ozuna CV, Gimenez MJ, Sousa C, Voytas DF, Barro F (2018) Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J 16(4): 902-910
• Sander JD, Dahlborg EJ, Goodwin MJ, Cade L, Zhang F, Cifuentes D, Curtin SJ, Blackburn JS, ThibodeauBeganny S, Qi Y, Pierick CJ, Hoffman E, Maeder ML, Khayter C, Reyon D, Dobbs D, Langenau M, Stupar RM, Giraldez AJ, Voytas DF, Peterson RT, Yeh JR, Joung, JK (2011) Selection-free zinc-fingernuclease engineering by context-dependent assembly CoDAa. Nat Methods 8: 67-69
• Sauer NJ, Narvaez-Vasquez J, Mozoruk J, Miller RB, Warburg ZJ, Woodward MJ, Mihiret YA, Lincoln TA, Segami RE, Sanders SL (2016) Oligonucleotide mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol 170: 1917-1928
• Sawai S, Ohyama K, Yasumoto S, Seki H, Sakuma T, Yamamoto T, Takebayashi Y, Kojima M, Sakakibara H, Aoki T, Muranaka T, Saito K, Umemoto N (2014) Sterol side chain reductase 2 is a key enzyme in the biosynthesis of cholesterol, the common precursor of toxic steroidal glycoalkaloids in potato. Plant cell 26(9): 3763-3774
• 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
• Shan Q, Wang Y, Chen K, Liang Z, Li J, Zhang Y, Zhang K, Liu J, Voytas DF, Zheng X, Zhang Y, Gao C (2013a) Rapid and efcient gene modifcation in rice and Brachypodium using TALENs. Mol Plant 6(4):1365-1368
• Shan Q, Wang Y, Li J, Gao C (2014) Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc 9: 2395-2410
• Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791-800
• Shao X , Wu S, Dou T, Zhu H, Hu C, Huo H, He W, Deng G, Sheng O, Bi F, Gao H, Dong T, Li C, Yang Q, Yi G (2020) Using CRISPR/Cas9 genome editing system to create MaGA20ox2 gene-modified semi-dwarf banana. Plant Biotech J 18: 17-19
• Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15(2): 207-216
• 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. Nat Biotechnol 35(5): 441-443
• Smith J, Grizot S, Arnould S, Duclert A, Epinat JC, Chames P, Prieto J, Redondo P, Blanco F, Bravo J, Montoya G, Paques F, Duchateau P (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res 34, e149. doi:10.1093/nar/gkl720.
• Subburaj, S, Chung, SJ, Lee, C, Ryu, SM, Kim, DH, Kim, JS, Bae, S, and Lee, GJ (2016) Site-d-irected mutagenesis in Petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins, Plant Cell Rep 35: 1535-1544
• 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
• Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu YY, Katiba, GE, Zhifang G McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregor PD, Urnov FD (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459: 4370-441
• Stoddard BL (2011) Homing endonucleases: From microbial genetic invaders to reagents for targeted DNA modification. Structure 19: 7-15
• Sun Z, Li N, Huang G, Xu J, Pan Y, Wang Z, Tang Q, Song M, Wang X (2013) Site-specific gene targeting using transcription activator-like effector (TALE)-based nuclease in Brassica oleracea. J Integr Plant Biol 55:1092-1103
• Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X, Du W, Zhao Y, Xia L (2016) Engineering herbicide resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol Plant 9: 628-631
• 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. Front Plant Sci 8: 1298
• Svitashev S, Young J K, Schwartz C, Gao H, Falco S C, 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
• Svitashev S, Schwartz C, Lenderts B, Young JK, Mark Cigan A (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexe. Nat Commun 7: e13274. https://doIorg/10.1038/ncomms13274
• Tang X, Lowder LG, Zhang T, Malzahn AA, Zheng X, Voytas DF, Zhong Z, Chen Y, Ren Q, Li Q (2017) A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants 3: 17018
• Tang X, Liu G, Zhou J, Ren Q, You Q, Tian L, Xin X, Zhong Z, Liu B, Zheng X, Zhang D, Malzahn A, Gong Z, Qi Y, Zhang T, Zhang Y(2018) A large-scale whole-genome sequencing analysis reveals highly specific genome editing by both Cas9 and Cpf1 (Cas12a) nucleases in rice. Genome Biol 19: 84
• Tang X, Ren Q, Yang L, Bao Y, Zhong Z, He Y, Liu S, Qi C, Liu B, Wang Y, Sretenovic S, Zhang Y, Zheng X, Zhang T, Qi Y, Zhang Y (2019) Single transcript unit CRISPR 2.0 systems for robust Cas9 and Cas12a mediated plant genome editing. Plant Biotechnol J 17(7): 1431-1445
• Tang X, Sretenovic S, Ren Q, Jia X, Li M, Fan T, Yin D, Xiang S, Guo Y, Liu L, Zheng X, Qi Y, Zhang Y (2020) Plant prime editors enable precise gene editing in rice cells. Mol Plant 13(5): 667-670
• Tian S, Jiang L, Gao Q, Zhang J, Zong M, Zhang H, Ren Y, Guo S, Gong G, Liu F (2017) Efficient CRISPR/Cas9-based gene knockout in watermelon. Plant Cell Rep 36: 399-406
• Tian S, Jiang L, Cui X, Zhang J, Guo S, Li M, Zhang H, Ren Y, Gong G, Zong M, Liu F, Chen Q, Xu Y (2018) Engineering herbicide-resistant watermelon variety through CRISPR/ Cas9-mediated base editing. Plant Cell Rep 37: 1353-1356
• 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
• Tsai S Q, Zheng Z L, Nguyen N T, Liebers M, Topkar V V, Thapar V, Wyvekens N, Khayter C, Iafrate A J, Le L P, Aryee M J, Joung J K. 2015. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol
(2): 187-197.
• Tuncel A, Corbin KR, Ahn-Jarvis J, Harris S, Hawkins E, Smedley MA, Harwood W, Warren FJ, Patron NJ, Smith AM (2019) Cas9-mediated mutagenesis of potato starch-branching enzymes generates a range of tuber starch phenotypes. Plant Biotech J 1-13, doi: 10.1111/pbI13137
• Ueta R, Abe C, Watanabe T, Sugano SS, Ishihara R, Ezura H, Osakabe Y, Osakabe K (2017) Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Sci Rep 7: 507 , DOI:10.1038/s41598-017-00501-4
• Veillet F, Perrot L, Chauvin L, Kermarrec MP, Guyon-Debast A, Chauvin JE, Nogué F, Mazier M (2019) Transgene-free genome editing in tomato and potato plants using Agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int J Mol Sci 20(2), pii-E402. https://doIorg/10.2290/ijms20020402
• Veillet F, Kermarrec MP, Chauvin L, Guyon-Debast A, Chauvin J, Gallois JL, Nogué F (2020) Prime editing is achievable in the tetraploid potato, but needs improvement. bioRxiv preprint doi: https://doi.org/10.1101/2020.06.18.159111.
• Vouillot L, Thelie A, Pollet N (2015) Comparison of T7E1 and surveyor mismatch cleavage assays to detect mutations triggered by engineered nucleases. G3: (Bethesda) 5: 407-415
• Waltz E (2016) CRISPR-edited crops free to enter market, skip regulation. Nat Biotechnol 34: 582
• Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu YG, Zhao K (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One 11: e0154027
• Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013) Onestep generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153: 910-918
• Wang L, Wang L, Tan Q, Fan Q, Zhu H, Hong Z, Zhang Z, Duanmu, D (2016) Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicas using CRISPR-Cas9. Front Plant Sci 7: 1333
• Wang L, Chen L, Li R, Zhao R, Yang M, Sheng J, Shen L (2017) Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J Agric Food Chem 65: 8674-8682
• Wang M, Liu Y, Zhang C, Liu J, Liu X, Wang L, Wang W, Chen H, Wei C, Ye X, Li X,
Tu J (2015) Gene editing by co-transformation of TALEN and chimeric RNA/DNA oligonucleotides on the rice OsEPSPS gene and the inheritance of mutations. PLoS One 10(4): e0122755
• Wang M, Mao Y, Lu Y, Tao X, Zhu, JK (2017a) Multiplex gene editing in rice using the CRISPR-Cpf1 system. Mol Plant 10: 1011-1013
• Wang M, Lu Y, Botella JR, Mao Y, Hua K, Zhu JK (2017b) Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system. Mol Plant 10: 1007-1010
• 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
• 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 Biotech 32: 947-951
• Wendt T, Holm P, Starker C, Christian M, Voytas D, Brinch-Pedersen H, Holme I (2013) TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol 83: 279-285
• 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, DOI: 10.1038/nbT3389
• Wright DA, Townsend JA, Winfrey RJ Jr, Irwin PA, Rajagopal J, Lonosky PM, Hall BD, Jondle MD, Voytas DF (2005) High frequency homologous recombination in plants mediated by zinc finger nucleases. Plant J 44: 693-705
• Wu J, Chen C, Xian G, Liu D, Lin L, Yin S, Sun Q, Fang Y, Zhang H, Wang Y (2020) Engineering herbicide-resistant oilseed rape by CRISPR/Cas9-mediated cytosine base-editing. Plant Biotech J : 1-3
• Xie K, Yang Y (2013) RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant 6: 1975-1983
• Xiong J, Ding J, Li Y (2015) Genome-editing technologies and their potential application in horticultural crop breeding. Horticul Res 2: 15019, doi:10.1038/hortres.2015.19
• Xu R, Yang Y, Qin R, Li H, Qiu C, Li L, Wei P, Yang J (2016) Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J Genet Genomics 43: 529-532
• Xu R, Qin R, Li H, Li D, Li L, Wei P, Yang J (2017) Generation of targeted mutant rice using a CRISPR-Cpf1 system. Plant Biotechnol J 15: 713-717.
• Xu R, Li J, Liu X, Shan T, Qin R, Wei P (2020). Development of Plant Prime-Editing Systems for Precise Genome Editing. Plant Comm 1: 100043
• Yan F, Kuang Y, Ren B, Wang J, Zhang D, Lin H, Yang B, Zhou X, Zhou H (2018) Highly efficient AT to GC base editing by Cas9n-guided tRNA adenosine deaminase in rice. Mol Plant 11: 631-634
• Yin K, Han T, Liu G, Chen T, Wang Y, Yu AYL, Liu Y (2015) A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Sci Rep 5:14926, DOi: 10.1038/srep14926
• Yu QH, Wang B, Li N, Tang Y, Yang S, Yang T, Xu J, Guo C, Yan P, Wang Q, Asmutola P (2017) CRISPR/Cas9-induced targeted mutagenesis and gene
replacement to generate longshelf life tomato lines. Sci Rep 7: 11874, DOI:10.1038/s41598-017-12262-1
• Zafar K, Khan MZ, Amin I, Mukhtar Z, Yasmin S, Arif M, Ejaz K, Mansoor S (2020) Precise CRISPR-Cas9 mediated genome editing in super Basmati rice for resistance against bacterial blight by targeting the major susceptibility gene. Front Plant Sci, doi: 10.3389/fplS2020.00575
• Zaidi SSA, Tashkandi M, Mansoor S, Mahfouz MM (2016) Engineering plant immunity: Using crispr/cas9 to generate virus resistance. Front Plant Sci 7: 1673
• Zeng D, Liu T, Ma X, Wang B, Zheng Z, Zhang Y, Xie X, Yang B, Zhao Z, Qinlong Zhu Q, Liu YG (2020) Quantitative regulation of Waxy expression by CRISPR/
Cas9-based promoter and 5’UTR-intron editing improves grain quality in rice. Plant Biotech J 1–3, doi: 10.1111/pbi.13427
• Zetsche B, Gootenberg J S, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 is a single RNA-guided endonuclease of a Class 2 CRISPRCas system. Cell 163: 759-771
• Zhang A, Liu Y, Wang F, Li T, Chen Z, Kong D, Bi J, Zhang F, Luo X, Wang J, Tang J, Yu X, Liu G,Luo L (2019) Enhanced rice salinity tolerance via CRISPR/Cas9-targeted mutagenesis of the OsRR22 gene. Mol Breed 39: 47, doIorg/10.1007/s11032-019-0954-y
• 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
• Zhang F, Maeder ML, Unger-Wallace E, Hoshaw JP, Reyon D, Christian M, Li X, Pierick CJ, Dobbs D, Peterson T, Joung JK, Voytas DF (2010) High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci USA 107: 12028-12033
• Zhang H, Gou F, Zhang J, Liu W, Li Q, Mao Y, Botella JR, Zhu JK (2016) TALEN-mediated targeted mutagenesis produces a large variety of heritable mutations in rice. Plant Biotech J 14(1): 186-194
• Zhang J, Zhang H, Botella JR, Zhu J (2018) Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J Integr Plant Biol 60: 369-375
• Zhang P, Du H, Wang J, Pu Y, Yang C, Yan R, Yang H, Cheng H, Yu D (2020) Multiplex CRISPR/Cas9-mediated metabolic engineering increases soya bean isoflavone content and resistance to soya bean mosaic virus. Plant Biotech 18: 1384-1395
• Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG, Bogdanove AJ, Voytas DF (2013) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol 161(1): 20-27
• Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu JL, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7: 12617
• Zhang Y, Bai Y, Wu G, Zou S, Chen Y, Gao C, Tang D (2017) Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J 91: 714-724
• Zhang Y, Li D, Zhang D, Zhao X, Cao X, Dong L,Liu J, Chen K, Zhang H, Gao C, Wang D (2018) Analysis of the functions of TaGW2 homoeologs in wheat grain weight and protein content traits. Plant J 94: 857-866
• Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom JS, Hoang S, Liu S, Vera Cruz C, Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82: 632-643
• Zhou Z, Tan H, Li Q, Chen J, Gao S, Wang Y, Chen W, Zhang L (2018) CRISPR/Cas9-mediated efficient targeted mutagenesis of RAS in Salvia miltiorrhiza. Phytochemistry 148: 63-70
• Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438-440
• Zong Y, Song Q, Li C, Jin S, Zhang D, Wang Y, Qiu JL, Gao C (2018) Effcient C-to-T base editing in plants using a fusion of nCas9 and human APOBEC3A. Nat Biotechnol 36: 950-953
Downloads
Published
How to Cite
Issue
Section
