Current advances on CRISPR/Cas genome editing technologies in plants

LIU Yaoguang; LI Gousi; ZHANG Yaling; CHEN Letian

doi:10.7671/j.issn.1001-411X.201905058

Journal of South China Agricultural University > 2019 > 40(5): 38-49. > DOI: 10.7671/j.issn.1001-411X.201905058

LIU Yaoguang, LI Gousi, ZHANG Yaling, et al. Current advances on CRISPR/Cas genome editing technologies in plants[J]. Journal of South China Agricultural University, 2019, 40(5): 38-49. DOI: 10.7671/j.issn.1001-411X.201905058

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Current advances on CRISPR/Cas genome editing technologies in plants

State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources/College of Life Sciences, South China Agricultural University, Guangzhou 510642, China

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Received Date: May 04, 2019
Available Online: May 17, 2023

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Abstract

Abstract

Development of genome editing technologies provides efficient tools for functional genomics and crop molecular breeding. Owing to its simplicity and high efficiency, CRISPR/Cas systems, including CRISPR/Cas9 and CRISPR/Cas12a, have been widely used for genome editing in many organisms. In this review, we summarize the recent advances on improvements and applications of CRISPR/Cas systems in plants, as well as the methods for analyzing targeted mutations in edited plants. Finally, we discuss current problems of CRISPR/Cas systems and give a prospect of genome editing technologies.
- CRISPR,
- plant,
- genome editing,
- targeted-mutation analysis

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References (125)

References

[1]	ZHANG Y, MA X, XIE X, et al. CRISPR/Cas9-based genome editing in plants [M]. Prog Mol Biol Transl, 2017, 149: 133-150.
[2]	李希陶, 刘耀光. 基因组编辑技术在水稻功能基因组和遗传改良中的应用[J]. 生命科学, 2016, 28(10): 1243-1249.
[3]	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[J]. J Bacteriol, 1987, 169(12): 5429-5433. doi: 10.1128/jb.169.12.5429-5433.1987
[4]	MOJICA F J, DIEZ-VILLASENOR C, SORIA E, et al. Biological significance of a family of regularly spaced repeats in the genomes of archaea, bacteria and mitochondria[J]. Mol Microbiol, 2000, 36(1): 244-246. doi: 10.1046/j.1365-2958.2000.01838.x
[5]	MOJICA F J, FERRER C, JUEZ G, et al. Long stretches of short tandem repeats are present in the largest replicons of the archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning[J]. Mol Microbiol, 1995, 17(1): 85-93. doi: 10.1111/mmi.1995.17.issue-1
[6]	JANSEN R, EMBDEN J D A V, GAASTRA W, et al. Identification of genes that are associated with DNA repeats in prokaryotes[J]. Mol Microbiol, 2002, 43(6): 1565-1575. doi: 10.1046/j.1365-2958.2002.02839.x
[7]	MOJICA F J M, DÍEZ-VILLASEÑOR C, GARCÍA-MARTÍNEZ J, et al. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements[J]. J Mol Evol, 2005, 60(2): 174-182. doi: 10.1007/s00239-004-0046-3
[8]	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[J]. Microbiology, 2005, 151(3): 653-663. doi: 10.1099/mic.0.27437-0
[9]	BOLOTIN A, OUINQUIS B, SOROKIN A, et al. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin[J]. Microbiology, 2005, 151(8): 2551-2561. doi: 10.1099/mic.0.28048-0
[10]	BARRANGOU R, FREMAUX C, DEVEAU H, et al. CRISPR provides acquired resistance against viruses in prokaryotes[J]. Science, 2007, 315(5819): 1709-1712. doi: 10.1126/science.1138140
[11]	SOREK R, KUNIN V, HUGENHOLTZ P. CRISPR: A widespread system that provides acquired resistance against phages in bacteria and archaea[J]. Nat Rev Microbiol, 2008, 6(3): 181-186. doi: 10.1038/nrmicro1793
[12]	MARRAFFINI L A, SONTHEIMER E J. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA[J]. Science, 2008, 322(5909): 1843-1845. doi: 10.1126/science.1165771
[13]	DEVEAU H, BARRANGOU R, GARNEAU J E, et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus[J]. J Bacteriol, 2008, 190(4): 1390-1400. doi: 10.1128/JB.01412-07
[14]	GARNEAU J E, DUPUIS M E, VILLION M, et al. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA[J]. Nature, 2010, 468(7320): 67-71. doi: 10.1038/nature09523
[15]	JINEK M, CHYLINSKI K, FONFARA I, et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity[J]. Science, 2012, 337(6096): 816-821. doi: 10.1126/science.1225829
[16]	GRISSA I, VERGNAUD G, POURCEL C. CRISPRFinder: A web tool to identify clustered regularly interspaced short palindromic repeats[J]. Nucleic Acids Res, 2007, 35(Web server issue): W52-W57. doi: 10.1093/nar/gkm360
[17]	MAKAROVA K S, HAFT D H, BARRANGOU R, et al. Evolution and classification of the CRISPR-Cas systems[J]. Nat Rev Microbiol, 2011, 9(6): 467-477. doi: 10.1038/nrmicro2577
[18]	CONG L, RAN F A, COR D, et al. Multiplex genome engineering using CRISPR/Cas systems[J]. Science, 2013, 339(6121): 819-823. doi: 10.1126/science.1231143
[19]	MAKAROVA K S, KOONIN E V. Annotation and classification of CRISPR-Cas systems[J]. Methods Mol Biol, 2015, 1311: 47-75. doi: 10.1007/978-1-4939-2687-9
[20]	SHMAKOV S, ABUDAYYEH O O, MAKAROVA K S, et al. Discovery and functional characterization of diverse class 2 CRISPR-Cas systems[J]. Mol Cell, 2015, 60(3): 385-397. doi: 10.1016/j.molcel.2015.10.008
[21]	GRATZ S J, CUMMINGS A M, NGUYEN J N, et al. Genome engineering of Drosophila with the CRISPR RNA-Guided cas9 nuclease[J]. Genetics, 2013, 194(4): 1029-1035. doi: 10.1534/genetics.113.152710
[22]	JINEK M, EAST A, CHENG A, et al. RNA-programmed genome editing in human cells[J]. eLife, 2013, 2: e00471.
[23]	CHO S W, KIM S, KIM J M, et al. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease[J]. Nat Biotechnol, 2013, 31(3): 230-232. doi: 10.1038/nbt.2507
[24]	HWANG W Y, FU Y, REYON D, et al. Efficient genome editing in zebrafish using a CRISPR-Cas system[J]. Nat Biotechnol, 2013, 31(3): 227-229. doi: 10.1038/nbt.2501
[25]	MALI P, YANG L, ESVELT K M, et al. RNA-guided human genome engineering via Cas9[J]. Science, 2013, 339(6121): 823-826. doi: 10.1126/science.1232033
[26]	FENG Z, ZHANG B, DING W, et al. Efficient genome editing in plants using a CRISPR/Cas system[J]. Cell Res, 2013, 23(10): 1229-1232. doi: 10.1038/cr.2013.114
[27]	MAO Y, ZHANG H, XU N, et al. Application of the CRISPR-Cas system for efficient genome engineering in plants[J]. Mol Plant, 2013, 6(6): 2008-2011. doi: 10.1093/mp/sst121
[28]	XIE K, YANG Y. RNA-guided genome editing in plants using a CRISPR-Cas system[J]. Mol Plant, 2013, 6(6): 1975-1983. doi: 10.1093/mp/sst119
[29]	FU Y, FODEN J A, KHAYTER C, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells[J]. Nat Biotechnol, 2013, 31(9): 822-826. doi: 10.1038/nbt.2623
[30]	SHAN Q, WANG Y, LI J, et al. Targeted genome modification of crop plants using a CRISPR-Cas system[J]. Nat Biotechnol, 2013, 31(8): 686-688. doi: 10.1038/nbt.2650
[31]	YIN K, GAO C, QIU J. Progress and prospects in plant genome editing[J]. Nat Plants, 2017, 3(8): 17107. doi: 10.1038/nplants.2017.107
[32]	LIU X, XIE C, SI H, et al. CRISPR/Cas9-mediated genome editing in plants[J]. Methods, 2017, 121/122: 94-102. doi: 10.1016/j.ymeth.2017.03.009
[33]	SOYARS C L, PETERSON B A, BURR C A, et al. Cutting edge genetics: CRISPR/Cas9 editing of plant genomes[J]. Plant Cell Physiol, 2018, 59(8): 1608-1620. doi: 10.1093/pcp/pcy079
[34]	SONG G, JIA M, CHEN K, et al. CRISPR/Cas9: A powerful tool for crop genome editing[J]. Crop J, 2016, 4(2): 75-82. doi: 10.1016/j.cj.2015.12.002
[35]	SCHAEFFER S M, NAKATA P A. CRISPR/Cas9-mediated genome editing and gene replacement in plants: Transitioning from lab to field[J]. Plant Sci, 2015, 240: 130-142. doi: 10.1016/j.plantsci.2015.09.011
[36]	ZETSCHE B, GOOTENBERG J S, ABUDAYYEH O O, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system[J]. Cell, 2015, 163(3): 759-771. doi: 10.1016/j.cell.2015.09.038
[37]	MAHFOUZ M M. Genome editing: The efficient tool CRISPR-Cpf1[J]. Nat Plants, 2017, 3: 17028. doi: 10.1038/nplants.2017.28
[38]	ZAIDI S S, MAHFOUZ M M, MANSOOR S. CRISPR-Cpf1: A new tool for plant genome editing[J]. Trends Plant Sci, 2017, 22(7): 550-553. doi: 10.1016/j.tplants.2017.05.001
[39]	ENDO A, MASAFUMI M, KAYA H, et al. Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida[J]. Sci Rep, 2016, 6: 38169.
[40]	HU X, WANG C, LIU Q, et al. Targeted mutagenesis in rice using CRISPR-Cpf1 system[J]. J Genet Genomics, 2017, 44(1): 71-73. doi: 10.1016/j.jgg.2016.12.001
[41]	WANG M, MAO Y, LU Y, et al. Multiplex gene editing in rice using the CRISPR-Cpf1 system[J]. Mol Plant, 2017, 10(7): 1011-1013. doi: 10.1016/j.molp.2017.03.001
[42]	TANG X, LOWDER L G, ZHANG T, et al. A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants[J]. Nat Plants, 2017, 3: 17018.
[43]	XU R, QIN R, LI H, et al. Generation of targeted mutant rice using a CRISPR-Cpf1 system[J]. Plant Biotechnol J, 2017, 15(6): 713-717. doi: 10.1111/pbi.2017.15.issue-6
[44]	BEGEMANN M B, GRAY B N, JANUARY E, et al. Precise insertion and guided editing of higher plant genomes using Cpf1 CRISPR nucleases[J]. Sci Rep, 2017, 7: 11606.
[45]	LI S, ZHANG X, WANG W, et al. Expanding the scope of CRISPR/Cpf1-mediated genome editing in rice[J]. Mol Plant, 2018, 11(7): 995-998. doi: 10.1016/j.molp.2018.03.009
[46]	MALZAHN A A, TANG X, LEE K, et al. Application of CRISPR-Cas12a temperature sensitivity for improved genome editing in rice, maize, and Arabidopsis[J]. BMC Biol, 2019, 17(1): 9.
[47]	KIM H, KIM S, RYU J, et al. CRISPR/Cpf1-mediated DNA-free plant genome editing[J]. Nat Commun, 2017, 8: 14406. doi: 10.1038/ncomms14406
[48]	FENG Z, MAO Y, XU N, et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis[J]. Proc Natl Acad Sci USA, 2014, 111(12): 4632-4637. doi: 10.1073/pnas.1400822111
[49]	MA X, ZHANG Q, ZHU Q, et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants[J]. Mol Plant, 2015, 8(8): 1274-1284. doi: 10.1016/j.molp.2015.04.007
[50]	马兴亮, 刘耀光. 植物CRISPR/Cas9基因组编辑系统与突变分析[J]. 遗传, 2016(2): 118-125.
[51]	ANDERSSON M, TURESSON H, NICOLIA A, et al. Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts[J]. Plant Cell Rep, 2017, 36(1): 117-128. doi: 10.1007/s00299-016-2062-3
[52]	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[J]. Nat Commun, 2016, 7: 12617.
[53]	ZHOU H, LIU B, WEEKS D P, et al. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice[J]. Nucleic Acids Res, 2014, 42(17): 10903-10914. doi: 10.1093/nar/gku806
[54]	ORDON J, GANTNER J, KEMNA J, et al. Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit[J]. Plant J, 2017, 89(1): 155-168. doi: 10.1111/tpj.2017.89.issue-1
[55]	CHO S, YU S, PARK J, et al. Accession-dependent CBF gene deletion by CRISPR/Cas system in arabidopsis[J]. Front Plant Sci, 2017, 8: 1910.
[56]	WANG F, WANG C, LIU P, et al. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922[J]. PLoS One, 2016, 11(4): e154027.
[57]	ZHOU J, PENG Z, LONG J, et al. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice[J]. Plant J, 2015, 82(4): 632-643. doi: 10.1111/tpj.12838
[58]	TANG L, MAO B, LI Y, et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield[J]. Sci Rep, 2017, 7: 14438.
[59]	XIE Y, NIU B, LONG Y, et al. Suppression or knockout of SaF/SaM overcomes the Sa-mediated hybrid male sterility in rice[J]. J Integr Plant Biol, 2017, 59(9): 669-679. doi: 10.1111/jipb.12564
[60]	SHEN R, WANG L, LIU X, et al. Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice[J]. Nat Commun, 2017, 8: 1310.
[61]	XIE Y, XU P, HUANG J, et al. Interspecific hybrid sterility in rice is mediated by OgTPR1 at the S1 locus encoding a peptidase-like protein[J]. Mol Plant, 2017, 10(8): 1137-1140. doi: 10.1016/j.molp.2017.05.005
[62]	XIE Y, TANG J, XIE X, et al. An asymmetric allelic interaction drives allele transmission bias in interspecific rice hybrids[J]. Nat Commun, 2019, 10(1): 2501.
[63]	LI Q, ZHANG D, CHEN M, et al. Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9[J]. J Genet Genomics, 2016, 43(6): 415-419. doi: 10.1016/j.jgg.2016.04.011
[64]	ZHOU H, HE M, LI J, et al. Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system[J]. Sci Rep, 2016, 6: 37395.
[65]	LI X, ZHOU W, REN Y, et al. High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing[J]. J Genet Genomics, 2017, 44(3): 175-178. doi: 10.1016/j.jgg.2017.02.001
[66]	LI M, LI X, ZHOU Z, et al. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system[J]. Front Plant Sci, 2016, 7: 377.
[67]	SHEN L, HUA Y, FU Y, et al. Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice[J]. Sci China Life Sci, 2017, 60(5): 506-515. doi: 10.1007/s11427-017-9008-8
[68]	XU R, YANG Y, QIN R, et al. Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice[J]. J Genet Genomics, 2016, 43(8): 529-532. doi: 10.1016/j.jgg.2016.07.003
[69]	SUN Y, JIAO G, LIU Z, et al. Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes[J]. Front Plant Sci, 2017, 8: 298.
[70]	ZHANG J, ZHANG H, BOTELLA J R, et al. Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties[J]. J Integr Plant Biol, 2018, 60(5): 369-375. doi: 10.1111/jipb.v60.5
[71]	SUN Y, ZHANG X, WU C, et al. Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase[J]. Mol Plant, 2016, 9(4): 628-631. doi: 10.1016/j.molp.2016.01.001
[72]	LI J, MENG X, ZONG Y, et al. Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9[J]. Nat Plants, 2016, 2: 16139.
[73]	LI C, ZONG Y, WANG Y, et al. Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion[J]. Genome Biol, 2018, 19: 59.
[74]	LU Y, ZHU J. Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system[J]. Mol Plant, 2017, 10(3): 523-525. doi: 10.1016/j.molp.2016.11.013
[75]	LUO M, GILBERT B, AYLIFFE M. Applications of CRISPR/Cas9 technology for targeted mutagenesis, gene replacement and stacking of genes in higher plants[J]. Plant Cell Rep, 2016, 35(7): 1439-1450. doi: 10.1007/s00299-016-1989-8
[76]	WANG M, LU Y, BOTELLA J R, et al. Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system[J]. Mol Plant, 2017, 10(7): 1007-1010. doi: 10.1016/j.molp.2017.03.002
[77]	MIKI D, ZHANG W, ZENG W, et al. CRISPR/Cas9-mediated gene targeting in Arabidopsis using sequential transformation[J]. Nat Commun, 2018, 9: 1967.
[78]	KOMOR A C, KIM Y B, PACKER M S, et al. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage[J]. Nature, 2016, 533(7603): 420-424. doi: 10.1038/nature17946
[79]	GAUDELLI N M, KOMOR A C, REES H A, et al. Programmable base editing of A·T to G·C in genomic DNA without DNA cleavage[J]. Nature, 2017, 551(7681): 464-471. doi: 10.1038/nature24644
[80]	LI J, SUN Y, DU J, et al. Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system[J]. Mol Plant, 2017, 10(3): 526-529. doi: 10.1016/j.molp.2016.12.001
[81]	SHIMATANI Z, KASHOJIYA S, TAKAYAMA M, et al. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion[J]. Nat Biotechnol, 2017, 35(5): 441-443. doi: 10.1038/nbt.3833
[82]	ZONG Y, WANG Y, LI C, et al. Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion[J]. Nat Biotechnol, 2017, 35(5): 438-440. doi: 10.1038/nbt.3811
[83]	CHEN Y, WANG Z, NI H, et al. CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis[J]. Sci China Life Sci, 2017, 60(5): 520-523. doi: 10.1007/s11427-017-9021-5
[84]	HUA K, TAO X, YUAN F, et al. Precise A·T to G·C base editing in the rice genome[J]. Mol Plant, 2018, 11(4): 627-630. doi: 10.1016/j.molp.2018.02.007
[85]	YAN F, KUANG Y, REN B, et al. Highly efficient A·T to G·C base editing by Cas9n-guided tRNA adenosine deaminase in rice[J]. Mol Plant, 2018, 11(4): 631-634. doi: 10.1016/j.molp.2018.02.008
[86]	KANG B, YUN J, KIM S, et al. Precision genome engineering through adenine base editing in plants[J]. Nat Plants, 2018, 4(7): 427-431. doi: 10.1038/s41477-018-0178-x
[87]	REN B, YAN F, KUANG Y, et al. Improved base editor for efficiently inducing genetic variations in rice with CRISPR/Cas9-guided hyperactive hAID mutant[J]. Mol Plant, 2018, 11(4): 623-626. doi: 10.1016/j.molp.2018.01.005
[88]	LI X, XIE Y, ZHU Q, et al. Targeted genome editing in genes and cis-regulatory regions improves qualitative and quantitative traits in crops[J]. Mol Plant, 2017, 10(11): 1368-1370. doi: 10.1016/j.molp.2017.10.009
[89]	RODRIGUEZ-LEAL D, LEMMON Z H, MAN J, et al. Engineering quantitative trait variation for crop improvement by genome editing[J]. Cell, 2017, 171(2): 470. doi: 10.1016/j.cell.2017.08.030
[90]	PUCHTA H. Using CRISPR/Cas in three dimensions: Towards synthetic plant genomes, transcriptomes and epigenomes[J]. Plant J, 2016, 87(1): 5-15. doi: 10.1111/tpj.2016.87.issue-1
[91]	PIATEK A, ALI Z, BAAZIM H, et al. RNA-guided transcriptional regulation[J]. Plant Biotechnol J, 2015, 13(4): 578-589. doi: 10.1111/pbi.12284
[92]	LOWDER L G, ZHANG D, BALTES N J, et al. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation[J]. Plant Physiol, 2015, 169(2): 971-985. doi: 10.1104/pp.15.00636
[93]	LI Z, ZHANG D, XIONG X, et al. A potent Cas9-derived gene activator for plant and mammalian cells[J]. Nat Plants, 2017, 3(12): 930-936. doi: 10.1038/s41477-017-0046-0
[94]	MA X, CHEN L, ZHU Q, et al. Rapid decoding of sequence-specific nuclease-induced heterozygous and biallelic mutations by direct sequencing of PCR products[J]. Mol Plant, 2015, 8(8): 1285-1287. doi: 10.1016/j.molp.2015.02.012
[95]	LIU W, XIE X, MA X, et al. DSDecode: A web-based tool for decoding of sequencing chromatograms for genotyping of targeted mutations[J]. Mol Plant, 2015, 8(9): 1431-1433. doi: 10.1016/j.molp.2015.05.009
[96]	XIE X, MA X, ZHU Q, et al. CRISPR-GE: A convenient software toolkit for CRISPR-based genome editing[J]. Mol Plant, 2017, 10(9): 1246-1249. doi: 10.1016/j.molp.2017.06.004
[97]	XUE L J, TSAI C J. AGEseq: Analysis of genome editing by sequencing[J]. Mol Plant, 2015, 8(9): 1428-1430. doi: 10.1016/j.molp.2015.06.001
[98]	PARK J, LIM K, KIM J, et al. Cas-analyzer: An online tool for assessing genome editing results using NGS data[J]. Bioinformatics, 2017, 33(2): 286-288. doi: 10.1093/bioinformatics/btw561
[99]	GUELL M, YANG L, CHURCH G M. Genome editing assessment using CRISPR genome analyzer (CRISPR-GA)[J]. Bioinformatics, 2014, 30(20): 2968-2970. doi: 10.1093/bioinformatics/btu427
[100]	PINELLO L, CANVER M C, HOBAN M D, et al. Analyzing CRISPR genome-editing experiments with CRISPResso[J]. Nat Biotechnol, 2016, 34(7): 695-697. doi: 10.1038/nbt.3583
[101]	LIU Q, WANG C, JIAO X, et al. Hi-TOM: A platform for high-throughput tracking of mutations induced by CRISPR/Cas systems[J]. Sci China Life Sci, 2019, 62(1): 1-7. doi: 10.1007/s11427-018-9402-9
[102]	LLOYD A, PLAISIER C L, CARROLL D, et al. Targeted mutagenesis using zinc-finger nucleases in Arabidopsis[J]. Proc Natl Acad Sci USA, 2005, 102(6): 2232-2237. doi: 10.1073/pnas.0409339102
[103]	VOYTAS D F. Plant genome engineering with sequence-specific nucleases [M]. Annu Rev Plant Biol, 2013: 64, 327-350.
[104]	GUSCHIN D Y, WAITE A J, KATIBAH G E, et al. A rapid and general assay for monitoring endogenous gene modification [M]. Method Mol Biol, 2010, 649: 247-256.
[105]	ZHENG X, YANG S, ZHANG D, et al. Effective screen of CRISPR/Cas9-induced mutants in rice by single-strand conformation polymorphism[J]. Plant Cell Rep, 2016, 35(7): 1545-1554. doi: 10.1007/s00299-016-1967-1
[106]	HSU P D, SCOTT D A, WEINSTEIN J A, et al. DNA targeting specificity of RNA-guided Cas9 nucleases[J]. Nat Biotechnol, 2013, 31(9): 827-832. doi: 10.1038/nbt.2647
[107]	ANDERSON K R, HAEUSSLER M, WATANABE C, et al. CRISPR off-target analysis in genetically engineered rats and mice[J]. Nat Methods, 2018, 15(7): 512-514. doi: 10.1038/s41592-018-0011-5
[108]	ZHANG H, ZHANG J, WEI P, et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation[J]. Plant Biotechnol J, 2014, 12(6): 797-807. doi: 10.1111/pbi.2014.12.issue-6
[109]	TANG X, LIU G, ZHOU J, et al. A large-scale whole-genome sequencing analysis reveals highly specific genome editing by both Cas9 and Cpf1 (Cas12a) nucleases in rice[J]. Genome Biol, 2018, 19: 84.
[110]	NEKRASOV V, WANG C, WIN J, et al. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion[J]. Sci Rep, 2017, 7: 482.
[111]	LI J, MANGHWAR H, SUN L, et al. Whole genome sequencing reveals rare off-target mutations and considerable inherent genetic or/and somaclonal variations in CRISPR/Cas9-edited cotton plants[J]. Plant Biotechnol J, 2019, 17(5): 858-868. doi: 10.1111/pbi.2019.17.issue-5
[112]	ZUO E, SUN Y, WEI W, et al. Cytosine base editor generates substantial off-target single-nucleotide variants in mouse embryos[J]. Science, 2019, 364(6437): 289-292.
[113]	JIN S, ZONG Y, GAO Q, et al. Cytosine, but not adenine, base editors induce genome-wide off-target mutations in rice[J]. Science, 2019, 364(6437): 292-295.
[114]	FU Y, SANDER J D, REYON D, et al. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs[J]. Nat Biotechnol, 2014, 32(3): 279-284. doi: 10.1038/nbt.2808
[115]	CHO S W, KIM S, KIM Y, et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases[J]. Genome Res, 2014, 24(1): 132-141. doi: 10.1101/gr.162339.113
[116]	PATTANAYAK V, LIN S, GUILINGER J P, et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity[J]. Nat Biotechnol, 2013, 31(9): 839-843. doi: 10.1038/nbt.2673
[117]	ZHANG D, ZHANG H, LI T, et al. Perfectly matched 20-nucleotide guide RNA sequences enable robust genome editing using high-fidelity SpCas9 nucleases[J]. Genome Biol, 2017, 18: 191.
[118]	SVITASHEV S, SCHWARTZ C, LENDERTS B, et al. Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes[J]. Nat Commun, 2016, 7: 13274.
[119]	MIRCETIC J, STEINEBRUNNER I, DING L, et al. Purified Cas9 fusion proteins for advanced genome manipulation[J]. Small Methods, 2017, 1: 1600052. doi: 10.1002/smtd.v1.4
[120]	SLAYMAKER I M, GAO L, ZETSCHE B, et al. Rationally engineered Cas9 nucleases with improved specificity[J]. Science, 2015, 351(6268): 84-88.
[121]	KLEINSTIVER B P, PATTANAYAK V, PREW M S, et al. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects[J]. Nature, 2016, 529(7587): 490-495. doi: 10.1038/nature16526
[122]	TANG J, CHEN L, LIU Y. Off-target effects and the solution[J]. Nat Plants, 2019, 5(4): 341-342. doi: 10.1038/s41477-019-0406-z
[123]	AKCAKAYA P, BOBBIN M L, GUO J A, et al. In vivo CRISPR editing with no detectable genome-wide off-target mutations[J]. Nature, 2018, 561: 416-419. doi: 10.1038/s41586-018-0500-9
[124]	WIENERT B, WYMAN S K, RICHARDSON C D, et al. Unbiased detection of CRISPR off-targets in vivo using DISCOVER-Seq[J]. Science, 2019, 364(6437): 286.
[125]	JUN R, XIXUN H, KEJIAN W, et al. Development and application of CRISPR/Cas system in rice[J]. Rice Sci, 2019, 26(2): 69-76. doi: 10.1016/j.rsci.2019.01.001

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Current advances on CRISPR/Cas genome editing technologies in plants

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