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Advances in Accurate Microbial Genome-Editing CRISPR Technologies

  • Lee, Ho Joung (Department of Systems Biotechnology, Chung-Ang University) ;
  • Lee, Sang Jun (Department of Systems Biotechnology, Chung-Ang University)
  • Received : 2021.06.20
  • Accepted : 2021.07.07
  • Published : 2021.07.28

Abstract

Previous studies have modified microbial genomes by introducing gene cassettes containing selectable markers and homologous DNA fragments. However, this requires several steps including homologous recombination and excision of unnecessary DNA regions, such as selectable markers from the modified genome. Further, genomic manipulation often leaves scars and traces that interfere with downstream iterative genome engineering. A decade ago, the CRISPR/Cas system (also known as the bacterial adaptive immune system) revolutionized genome editing technology. Among the various CRISPR nucleases of numerous bacteria and archaea, the Cas9 and Cas12a (Cpf1) systems have been largely adopted for genome editing in all living organisms due to their simplicity, as they consist of a single polypeptide nuclease with a target-recognizing RNA. However, accurate and fine-tuned genome editing remains challenging due to mismatch tolerance and protospacer adjacent motif (PAM)-dependent target recognition. Therefore, this review describes how to overcome the aforementioned hurdles, which especially affect genome editing in higher organisms. Additionally, the biological significance of CRISPR-mediated microbial genome editing is discussed, and future research and development directions are also proposed.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF-2021R1A2C1013606), Republic of Korea. This study was also supported by Rural Development Administration (Project No. PJ015001032021), Republic of Korea.

References

  1. 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. https://doi.org/10.1128/jb.169.12.5429-5433.1987
  2. Mojica FJ, Diez-Villasenor C, Soria E, Juez G. 2000. Biological significance of a family of regularly spaced repeats in the genomes of archaea, bacteria and mitochondria. Mol. Microbiol. 36: 244-246. https://doi.org/10.1046/j.1365-2958.2000.01838.x
  3. Jansen R, Embden JD, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43: 1565-1575. https://doi.org/10.1046/j.1365-2958.2002.02839.x
  4. Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Soria E. 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60: 174-182. https://doi.org/10.1007/s00239-004-0046-3
  5. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712. https://doi.org/10.1126/science.1138140
  6. Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170. https://doi.org/10.1126/science.1179555
  7. 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. https://doi.org/10.1126/science.1225829
  8. Adli M. 2018. The CRISPR tool kit for genome editing and beyond. Nat. Commun. 9: 1911. https://doi.org/10.1038/s41467-018-04252-2
  9. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. 2011. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res. 39: 9275-9282. https://doi.org/10.1093/nar/gkr606
  10. Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS, Kriz AJ, et al. 2015. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520: 186-191. https://doi.org/10.1038/nature14299
  11. Esvelt KM, Mali P, Braff JL, Moosburner M, Yaung SJ, Church GM. 2013. Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat. Methods 10: 1116-1121. https://doi.org/10.1038/nmeth.2681
  12. Hou Z, Zhang Y, Propson NE, Howden SE, Chu LF, Sontheimer EJ, et al. 2013. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 110: 15644-15649. https://doi.org/10.1073/pnas.1313587110
  13. Hirano H, Gootenberg JS, Horii T, Abudayyeh OO, Kimura M, Hsu PD, et al. 2016. Structure and engineering of Francisella novicida Cas9. Cell 164: 950-961. https://doi.org/10.1016/j.cell.2016.01.039
  14. Kim E, Koo T, Park SW, Kim D, Kim K, Cho HY, et al. 2017. In vivo genome editing with a small Cas9 orthologue derived from Campylobacter jejuni. Nat. Commun. 8: 14500. https://doi.org/10.1038/ncomms14500
  15. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. 2013. RNA-guided human genome engineering via Cas9. Science 339: 823-826. https://doi.org/10.1126/science.1232033
  16. Cong L, Ran FA, Cox D, Lin SL, Barretto R, Habib N, et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823. https://doi.org/10.1126/science.1231143
  17. 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. 41: e188. https://doi.org/10.1093/nar/gkt780
  18. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, et al. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153: 910-918. https://doi.org/10.1016/j.cell.2013.04.025
  19. Cho SW, Kim S, Kim JM, Kim JS. 2013. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31: 230-232. https://doi.org/10.1038/nbt.2507
  20. Gonzalez MN, Massa GA, Andersson M, Turesson H, Olsson N, Falt AS, et al. 2019. Reduced enzymatic browning in potato tubers by specific editing of a polyphenol oxidase gene via ribonucleoprotein complexes delivery of the CRISPR/Cas9 system. Front. Plant Sci. 10: 1649. https://doi.org/10.3389/fpls.2019.01649
  21. Cyranoski D. 2016. CRISPR gene-editing tested in a person for the first time. Nature 539: 479. https://doi.org/10.1038/nature.2016.20988
  22. Reyrat JM, Pelicic V, Gicquel B, Rappuoli R. 1998. Counterselectable markers: untapped tools for bacterial genetics and pathogenesis. Infect. Immun. 66: 4011-4017. https://doi.org/10.1128/IAI.66.9.4011-4017.1998
  23. Jager W, Schafer A, Puhler A, Labes G, Wohlleben W. 1992. Expression of the Bacillus subtilis sacB gene leads to sucrose sensitivity in the gram-positive bacterium Corynebacterium glutamicum but not in Streptomyces lividans. J. Bacteriol. 174: 5462-5465. https://doi.org/10.1128/jb.174.16.5462-5465.1992
  24. Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69-73. https://doi.org/10.1016/0378-1119(94)90324-7
  25. Kolisnychenko V, Plunkett G, 3rd, Herring CD, Feher T, Posfai J, Blattner FR, et al. 2002. Engineering a reduced Escherichia coli genome. Genome Res. 12: 640-647. https://doi.org/10.1101/gr.217202
  26. Pyne ME, Moo-Young M, Chung DA, Chou CP. 2015. Coupling the CRISPR/Cas9 system with lambda red recombineering enables simplified chromosomal gene replacement in Escherichia coli. Appl. Environ. Microbiol. 81: 5103-5114. https://doi.org/10.1128/AEM.01248-15
  27. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645. https://doi.org/10.1073/pnas.120163297
  28. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2: 2006.0008.
  29. Swingle B, Markel E, Costantino N, Bubunenko MG, Cartinhour S, Court DL. 2010. Oligonucleotide recombination in Gram-negative bacteria. Mol. Microbiol. 75: 138-148. https://doi.org/10.1111/j.1365-2958.2009.06976.x
  30. Fabret C, Ehrlich SD, Noirot P. 2002. A new mutation delivery system for genome-scale approaches in Bacillus subtilis. Mol. Microbiol. 46: 25-36. https://doi.org/10.1046/j.1365-2958.2002.03140.x
  31. Fedoryshyn M, Welle E, Bechthold A, Luzhetskyy A. 2008. Functional expression of the Cre recombinase in actinomycetes. Appl. Microbiol. Biotechnol. 78: 1065-1070. https://doi.org/10.1007/s00253-008-1382-9
  32. Lee SH, Kim HJ, Shin YA, Kim KH, Lee SJ. 2016. Single crossover-mediated markerless genome engineering in Clostridium acetobutylicum. J. Microbiol. Biotechnol. 26: 725-729. https://doi.org/10.4014/jmb.1512.12012
  33. Wyman C, Kanaar R. 2006. DNA double-strand break repair: All's well that ends well. Annu. Rev. Genet. 40: 363-383. https://doi.org/10.1146/annurev.genet.40.110405.090451
  34. Jin H, Lee B, Luo Y, Choi Y, Choi EH, Jin H, et al. 2020. FOXL2 directs DNA double-strand break repair pathways by differentially interacting with Ku. Nat. Commun. 11: 2010. https://doi.org/10.1038/s41467-020-15748-1
  35. Della M, Palmbos PL, Tseng HM, Tonkin LM, Daley JM, Topper LM, et al. 2004. Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine. Science 306: 683-685. https://doi.org/10.1126/science.1099824
  36. Stephanou NC, Gao F, Bongiorno P, Ehrt S, Schnappinger D, Shuman S, et al. 2007. Mycobacterial nonhomologous end joining mediates mutagenic repair of chromosomal double-strand DNA breaks. J. Bacteriol. 189: 5237-5246. https://doi.org/10.1128/JB.00332-07
  37. Zhu H, Shuman S. 2010. Gap filling activities of Pseudomonas DNA Ligase D (LigD) polymerase and functional interactions of LigD with the DNA end-binding Ku protein. J. Biol. Chem. 285: 4815-4825. https://doi.org/10.1074/jbc.M109.073874
  38. de Vega M. 2013. The minimal Bacillus subtilis nonhomologous end joining repair machinery. PLoS One 8: e64232. https://doi.org/10.1371/journal.pone.0064232
  39. Bertrand C, Thibessard A, Bruand C, Lecointe F, Leblond P. 2019. Bacterial NHEJ: a never ending story. Mol. Microbiol. 111: 1139-1151. https://doi.org/10.1111/mmi.14218
  40. Selle K, Barrangou R. 2015. Harnessing CRISPR-Cas systems for bacterial genome editing. Trends Microbiol. 23: 225-232. https://doi.org/10.1016/j.tim.2015.01.008
  41. Cobb RE, Wang Y, Zhao H. 2015. High-efficiency multiplex genome editing of Streptomyces species using an engineered CRISPR/Cas system. ACS Synth. Biol. 4: 723-728. https://doi.org/10.1021/sb500351f
  42. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31: 233-239. https://doi.org/10.1038/nbt.2508
  43. Huang H, Zheng G, Jiang W, Hu H, Lu Y. 2015. One-step high-efficiency CRISPR/Cas9-mediated genome editing in Streptomyces. Acta Biochim. Biophys. Sin. (Shanghai) 47: 231-243. https://doi.org/10.1093/abbs/gmv007
  44. Lee N, Hwang S, Lee Y, Cho S, Palsson B, Cho BK. 2019. Synthetic biology tools for novel secondary metabolite discovery in Streptomyces. J. Microbiol. Biotechnol. 29: 667-686. https://doi.org/10.4014/jmb.1904.04015
  45. Guo T, Xin Y, Zhang Y, Gu X, Kong J. 2019. A rapid and versatile tool for genomic engineering in Lactococcus lactis. Microb. Cell Fact. 18: 22. https://doi.org/10.1186/s12934-019-1075-3
  46. Wirth NT, Kozaeva E, Nikel PI. 2020. Accelerated genome engineering of Pseudomonas putida by I-SceI-mediated recombination and CRISPR-Cas9 counterselection. Microb. Biotechnol. 13: 233-249. https://doi.org/10.1111/1751-7915.13396
  47. Zhang J, Zhang D, Zhu J, Liu H, Liang S, Luo Y. 2020. Efficient multiplex genome editing in Streptomyces via engineered CRISPR-Cas12a systems. Front. Bioeng. Biotechnol. 8: 726. https://doi.org/10.3389/fbioe.2020.00726
  48. Feng X, Zhao D, Zhang X, Ding X, Bi C. 2018. CRISPR/Cas9 assisted multiplex genome editing technique in Escherichia coli. Biotechnol. J. 13: e1700604.
  49. Choe D, Lee JH, Yoo M, Hwang S, Sung BH, Cho S, et al. 2019. Adaptive laboratory evolution of a genome-reduced Escherichia coli. Nat. Commun. 10: 935. https://doi.org/10.1038/s41467-019-08888-6
  50. Darmon E, Leach DR. 2014. Bacterial genome instability. Microbiol. Mol. Biol. Rev. 78: 1-39. https://doi.org/10.1128/MMBR.00035-13
  51. Liu J, Wang Y, Lu Y, Zheng P, Sun J, Ma Y. 2017. Development of a CRISPR/Cas9 genome editing toolbox for Corynebacterium glutamicum. Microb. Cell. Fact. 16: 205. https://doi.org/10.1186/s12934-017-0815-5
  52. Ungerer J, Pakrasi HB. 2016. Cpf1 is a versatile tool for CRISPR genome editing across diverse species of cyanobacteria. Sci. Rep. 6: 39681. https://doi.org/10.1038/srep39681
  53. Altenbuchner J. 2016. Editing of the Bacillus subtilis genome by the CRISPR-Cas9 system. Appl. Environ. Microbiol. 82: 5421-5427. https://doi.org/10.1128/AEM.01453-16
  54. Oh JH, van Pijkeren JP. 2014. CRISPR-Cas9-assisted recombineering in Lactobacillus reuteri. Nucleic Acids Res. 42: e131. https://doi.org/10.1093/nar/gku623
  55. Yan MY, Yan HQ, Ren GX, Zhao JP, Guo XP, Sun YC. 2017. CRISPR-Cas12a-assisted recombineering in bacteria. Appl. Environ. Microbiol. 83: e00947-00917.
  56. Ao X, Yao Y, Li T, Yang TT, Dong X, Zheng ZT, et al. 2018. A multiplex genome editing method for Escherichia coli based on CRISPR-Cas12a. Front. Microbiol. 9: 2307. https://doi.org/10.3389/fmicb.2018.02307
  57. Reisch CR, Prather KL. 2015. The no-SCAR (Scarless Cas9 Assisted Recombineering) system for genome editing in Escherichia coli. Sci. Rep. 5: 15096. https://doi.org/10.1038/srep15096
  58. Leenay RT, Vento JM, Shah M, Martino ME, Leulier F, Beisel CL. 2019. Genome editing with CRISPR-Cas9 in Lactobacillus plantarum revealed that editing outcomes can vary across strains and between methods. Biotechnol. J. 14: e1700583.
  59. Li J, Sun J, Gao X, Wu Z, Shang G. 2019. Coupling ssDNA recombineering with CRISPR-Cas9 for Escherichia coli DnaG mutations. Appl. Microbiol. Biotechnol. 103: 3559-3570. https://doi.org/10.1007/s00253-019-09744-9
  60. Wang Y, Zhang ZT, Seo SO, Lynn P, Lu T, Jin YS, et al. 2016. Bacterial genome editing with CRISPR-Cas9: Deletion, integration, single nucleotide modification, and desirable "Clean" mutant selection in Clostridium beijerinckii as an example. ACS Synth. Biol. 5: 721-732. https://doi.org/10.1021/acssynbio.6b00060
  61. Wang X, He J, Le K. 2018. Making point mutations in Escherichia coli BL21 genome using the CRISPR-Cas9 system. FEMS Microbiol. Lett. 365. doi: 10.1093/femsle/fny060.
  62. Yao R, Liu D, Jia X, Zheng Y, Liu W, Xiao Y. 2018. CRISPR-Cas9/Cas12a biotechnology and application in bacteria. Synth. Syst. Biotechnol. 3: 135-149. https://doi.org/10.1016/j.synbio.2018.09.004
  63. Jiang Y, Qian F, Yang J, Liu Y, Dong F, Xu C, et al. 2017. CRISPR-Cpf1 assisted genome editing of Corynebacterium glutamicum. Nat. Commun. 8: 15179. https://doi.org/10.1038/ncomms15179
  64. Deveau H, Barrangou R, Garneau JE, Labonte J, Fremaux C, Boyaval P, et al. 2008. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190: 1390-1400. https://doi.org/10.1128/JB.01412-07
  65. Mojica FJM, Diez-Villasenor C, Garcia-Martinez J, Almendros C. 2009. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology (Reading) 155: 733-740. https://doi.org/10.1099/mic.0.023960-0
  66. Gasiunas G, Young JK, Karvelis T, Kazlauskas D, Urbaitis T, Jasnauskaite M, et al. 2020. A catalogue of biochemically diverse CRISPR-Cas9 orthologs. Nat. Commun. 11: 5512. https://doi.org/10.1038/s41467-020-19344-1
  67. Wang J, Li J, Zhao H, Sheng G, Wang M, Yin M, et al. 2015. Structural and mechanistic basis of PAM-dependent spacer acquisition in CRISPR-Cas systems. Cell 163: 840-853. https://doi.org/10.1016/j.cell.2015.10.008
  68. Collias D, Beisel CL. 2021. CRISPR technologies and the search for the PAM-free nuclease. Nat. Commun. 12: 555. https://doi.org/10.1038/s41467-020-20633-y
  69. Karvelis T, Gasiunas G, Siksnys V. 2017. Harnessing the natural diversity and in vitro evolution of Cas9 to expand the genome editing toolbox. Curr. Opin. Microbiol. 37: 88-94. https://doi.org/10.1016/j.mib.2017.05.009
  70. Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI, Dohmae N, et al. 2014. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156: 935-949. https://doi.org/10.1016/j.cell.2014.02.001
  71. Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng Z, et al. 2015. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523: 481-485. https://doi.org/10.1038/nature14592
  72. Gao L, Cox DBT, Yan WX, Manteiga JC, Schneider MW, Yamano T, et al. 2017. Engineered Cpf1 variants with altered PAM specificities. Nat. Biotechnol. 35: 789-792. https://doi.org/10.1038/nbt.3900
  73. Hu JH, Miller SM, Geurts MH, Tang W, Chen L, Sun N, et al. 2018. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature 556: 57-63. https://doi.org/10.1038/nature26155
  74. Nishimasu H, Shi X, Ishiguro S, Gao L, Hirano S, Okazaki S, et al. 2018. Engineered CRISPR-Cas9 nuclease with expanded targeting space. Science 361: 1259-1262. https://doi.org/10.1126/science.aas9129
  75. Kim B, Kim HJ, Lee SJ. 2020. Regulation of microbial metabolic rates using CRISPR interference with expanded PAM sequences. Front. Microbiol. 11: 282. https://doi.org/10.3389/fmicb.2020.00282
  76. Kim B, Kim HJ, Lee SJ. 2020. Effective blocking of microbial transcriptional initiation by dCas9-NG-mediated CRISPR interference. J. Microbiol. Biotechnol. 30: 1919-1926. https://doi.org/10.4014/jmb.2008.08058
  77. Li D, Zhou H, Zeng X. 2019. Battling CRISPR-Cas9 off-target genome editing. Cell. Biol. Toxicol. 35: 403-406. https://doi.org/10.1007/s10565-019-09485-5
  78. Fu BX, St Onge RP, Fire AZ, Smith JD. 2016. Distinct patterns of Cas9 mismatch tolerance in vitro and in vivo. Nucleic Acids Res. 44: 5365-5377. https://doi.org/10.1093/nar/gkw417
  79. Lin YN, Cradick TJ, Brown MT, Deshmukh H, Ranjan P, Sarode N, et al. 2014. CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res. 42: 7473-7485. https://doi.org/10.1093/nar/gku402
  80. Chen SJ. 2019. Minimizing off-target effects in CRISPR-Cas9 genome editing. Cell. Biol. Toxicol. 35: 399-401. https://doi.org/10.1007/s10565-019-09486-4
  81. Chapman JR, Taylor MR, Boulton SJ. 2012. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell. 47: 497-510. https://doi.org/10.1016/j.molcel.2012.07.029
  82. 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: 420-424. https://doi.org/10.1038/nature17946
  83. Kim D, Lim K, Kim DE, Kim JS. 2020. Genome-wide specificity of dCpf1 cytidine base editors. Nat. Commun. 11: 4072. https://doi.org/10.1038/s41467-020-17889-9
  84. Grunewald J, Zhou R, Iyer S, Lareau CA, Garcia SP, Aryee MJ, et al. 2019. CRISPR DNA base editors with reduced RNA off-target and self-editing activities. Nat. Biotechnol. 37: 1041-1048. https://doi.org/10.1038/s41587-019-0236-6
  85. Jeong YK, Song B, Bae S. 2020. Current status and challenges of DNA base editing tools. Mol. Ther. 28: 1938-1952. https://doi.org/10.1016/j.ymthe.2020.07.021
  86. Lee SS, Ding N, Sun YD, Yuan TL, Li J, Yuan QC, et al. 2020. Single C-to-T substitution using engineered APOBEC3G-nCas9 base editors with minimum genome- and transcriptome-wide off-target effects. Sci. Adv. 6: eaba1773. https://doi.org/10.1126/sciadv.aba1773
  87. Sun J, Lu LB, Liang TX, Yang LR, Wu JP. 2020. CRISPR-assisted multiplex base editing system in Pseudomonas putida KT2440. Front. Bioeng. Biotechnol. 8: 905. https://doi.org/10.3389/fbioe.2020.00905
  88. Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, et al. 2019. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576: 149-157. https://doi.org/10.1038/s41586-019-1711-4
  89. Yang L, Chen J. 2020. A tale of two moieties: Rapidly evolving CRISPR/Cas-based genome editing. Trends Biochem. Sci. 45: 874-888. https://doi.org/10.1016/j.tibs.2020.06.003
  90. Arroyo-Olarte RD, Bravo Rodriguez R, Morales-Rios E. 2021. Genome editing in bacteria: CRISPR-Cas and beyond. Microorganisms 9: 844. https://doi.org/10.3390/microorganisms9040844
  91. Fu YF, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32: 279-284. https://doi.org/10.1038/nbt.2808
  92. Li P, Kleinstiver BP, Leon MY, Prew MS, Navarro-Gomez D, Greenwald SH, et al. 2018. Allele-specific CRISPR-Cas9 genome editing of the single-base P23H mutation for rhodopsin-associated dominant retinitis pigmentosa. CRISPR J. 1: 55-64. https://doi.org/10.1089/crispr.2017.0009
  93. Park HM, Liu H, Wu J, Chong A, Mackley V, Fellmann C, et al. 2018. Extension of the crRNA enhances Cpf1 gene editing in vitro and in vivo. Nat. Commun. 9: 3313. https://doi.org/10.1038/s41467-018-05641-3
  94. McMahon MA, Prakash TP, Cleveland DW, Bennett CF, Rahdar M. 2018. Chemically modified Cpf1-CRISPR RNAs mediate efficient genome editing in mammalian cells. Mol. Ther. 26: 1228-1240. https://doi.org/10.1016/j.ymthe.2018.02.031
  95. Bin Moon S, Lee JM, Kang JG, Lee NE, Ha DI, Kim DY, et al. 2018. Highly efficient genome editing by CRISPR-Cpf1 using CRISPR RNA with a uridinylate-rich 3'-overhang. Nat. Commun. 9: 3651. https://doi.org/10.1038/s41467-018-06129-w
  96. Anderson EM, Haupt A, Schiel JA, Chou E, Machado HB, Strezoska Z, et al. 2015. Systematic analysis of CRISPR-Cas9 mismatch tolerance reveals low levels of off-target activity. J. Biotechnol. 211: 56-65. https://doi.org/10.1016/j.jbiotec.2015.06.427
  97. Lee HJ, Kim HJ, Lee SJ. 2020. CRISPR-Cas9-mediated pinpoint microbial genome editing aided by target-mismatched sgRNAs. Genome Res. 30: 768-775. https://doi.org/10.1101/gr.257493.119
  98. Kim HJ, Oh SY, and Lee SJ. 2020. Single-base genome editing in Corynebacterium glutamicum with the help of negative selection by target-mismatched CRISPR/Cpf1. J. Microbiol. Biotechnol. 30: 1583-1591. https://doi.org/10.4014/jmb.2006.06036
  99. Lee HJ, Kim HJ, Lee SJ. 2021. Mismatch intolerance of 5'-truncated sgRNAs in CRISPR/Cas9 enables efficient microbial single-base genome editing. Int. J. Mol. Sci. 22: 6457. https://doi.org/10.3390/ijms22126457
  100. Song B, Yang S, Hwang G-H, Yu J, Bae S. 2021. Analysis of NHEJ-based DNA repair after CRISPR-mediated DNA cleavage. Int. J. Mol. Sci. 22: 6397. https://doi.org/10.3390/ijms22126397
  101. Rodrigues SD, Karimi M, Impens L, Van Lerberge E, Coussens G, Aesaert S, et al. 2021. Efficient CRISPR-mediated base editing in Agrobacterium spp. Proc. Natl. Acad. Sci. USA 118: e2013338118. https://doi.org/10.1073/pnas.2013338118
  102. Hayashi A, Tanaka K. 2019. Short-homology-mediated CRISPR/Cas9-based method for genome editing in fission yeast. G3 (Bethesda) 9: 1153-1163. https://doi.org/10.1534/g3.118.200976
  103. Zhang J, Qian FH, Dong F, Wang QZ, Yang JJ, Jiang Y, et al. 2020. De Novo engineering of Corynebacterium glutamicum for L-proline production. ACS Synth. Biol. 9: 1897-1906. https://doi.org/10.1021/acssynbio.0c00249
  104. Shen W, Zhang J, Geng B, Qiu M, Hu M, Yang Q, et al. 2019. Establishment and application of a CRISPR-Cas12a assisted genome-editing system in Zymomonas mobilis. Microb. Cell Fact. 18: 162. https://doi.org/10.1186/s12934-019-1219-5
  105. Zhou D, Jiang Z, Pang Q, Zhu Y, Wang Q, Qi Q. 2019. CRISPR/Cas9-assisted seamless genome editing in Lactobacillus plantarum and its application in N-acetylglucosamine production. Appl. Environ. Microbiol. 85: e01367-01319.
  106. Krumbach K, Sonntag CK, Eggeling L, Marienhagen J. 2019. CRISPR/Cas12a mediated genome editing to introduce amino acid substitutions into the mechanosensitive channel MscCG of Corynebacterium glutamicum. ACS Synth. Biol. 8: 2726-2734. https://doi.org/10.1021/acssynbio.9b00361
  107. Wege SM, Gejer K, Becker F, Bolker M, Freitag J, Sandrock B. 2021. Versatile CRISPR/Cas9 systems for genome editing in Ustilago maydis. J. Fungi. 7: 149. https://doi.org/10.3390/jof7020149

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