Abstract
Gene editing is a new genetic engineering technology that uses sequence-specific nucleases to insert, delete, or replace nucleic acid base(s) of the target gene, or introduce exogenous DNA sequences at a specific site in the genome of an organism to achieve the desired modification. Currently, the CRISPR/Cas system is the most widely used genome editing technology because it is relatively simple with high editing efficiency. In this review, we discuss the CRISPR/Cas system’s application and its current limitations in rice breeding. Also, we elaborate on possible improved methods regarding its mechanism and development history.
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References
Baysal C, Bortesi L, Zhu CF, Farré G, Schillberg S, Christou P (2016) CRISPR/Cas9 activity in the rice OsBEIIb gene does not induce off-target effects in the closely related paralog OsBEIIa. Mol Breed 36. https://doi.org/10.1007/s11032-016-0533-4
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. https://doi.org/10.3389/fpls.2017.01441
Cong L, Ran FA, Cor D, Lin SL, Barretto R, Habib N, Hsu PD, Wu XB, Jiang WY, Marraffini LA, Zheng F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823
Cui Y, Zhu MM, Xu ZJ, Xu Q (2019) Assessment of the effect of ten heading time genes on reproductive transition and yield components in rice using a CRISPR/Cas9 system. Theor Appl Genet 132:1887–1896
Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao YJ, Pirzada ZA, Eckert MR, Vogel J, Charpentier E (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–607
Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, Boyaval P, Romero DA, Horvath P, Moineau S (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. Bacterio l190:1390–1400
Duan YB, Li J, Qin RY, Xu RF, Li H, Yang YC, Ma H, Li L, Wei PC, Yang JB (2016) Identification of a regulatory element responsible for salt induction of rice OsRAV2 through ex situ and in situ promoter analysis. Plant Mol Biol l90:49–62
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/Cassystem. Cell Res 23:1229–1232
Giedrius G, Rodolphe B, Philippe H, Virginijus S (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 109:E2579–E2586
Gu S, Zheng WJ, Ma DR (2020) Research progress of CRISPR/Cas9 gene-editing system in rice breeding. Mol Plant Breed http://kns.cnki.net/kcms/detail/46.1068.S.20200605.1609.008.html
Hao W, Ji ZY, Zheng KL, Sun HD, Wang FJ, Tang YC, Zhang MW, Zhao KJ, Wang CL (2018) Enhancing rice resistance to bacterial blight by genome editing, Zhiwu Yichuan Xuebao. J Plant Genet Resource 19:523–530
Hu XJ, Yang J, Cheng C, Zhou JH, Niu FA, Wang XQ, Zhang ML, Cao LM, Chu HW (2018) Targeted editing of rice SD1gene using CRISPR/Cas9 system. Zhongguo Shuidao Kexue. Chin J Rice Sci 32:219–225
Huang LH, Li QF, Zhang CQ, Chu R, Gu ZW, Tan HY, Zhao DS, Fan XL, Liu QQ (2020) Creating novel Wx alleles with fine-tuned amylose levels and improved grain quality in rice by promoter editing using CRISPR/Cas9 system. Plant Biotechnol J 18:2164–2166. https://doi.org/10.1111/pbi.13391
Ikeda T, Tanaka W, Mikami M, Endo M, Hirano HY (2015) Generation of artificial drooping leaf mutants by CRISPR-Cas9 technology in rice. Gene Genet Syst 90:231–235
Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata T (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
Jansen R, Embden JDAV, Gaastra W, Schouls LM (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43:1565–1575
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
Khanday SD, Yang B, Mercier R, Sundaresan V (2019) A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565:91–95
Komatsu A, Ohtake M, Shimatani Z, Nishida K (2020) Production of herbicide-sensitive strain to prevent volunteer rice infestation using a CRISPR-Cas9 cytidine deaminase fusion. Front Plant Sci 11. https://doi.org/10.3389/fpls.2020.00925
Kuang YJ, Li SF, Ren B, Yan F, Spetz C, Li XJ, Zhou XP, Zhou HB (2020) Base-editing-mediated artificial evolution of OsALS1in planta to develop novel herbicide-tolerant rice germplasms. Mol Plant 13:565–572
Li CY, Li W, W H, Chen H, Xie CH, Lin YJ (2020) A new rice breeding method: CRISPR/Cas9 system editing of the Xa13 promoter to cultivate transgene-free bacterial blight-resistant rice. Plant Biotechnol J 18:313–315. https://doi.org/10.1111/pbi.13217
Li J, Meng XB, Zong Y, Chen KL, Zhang HW, Liu JX, Li JY, Gao CX (2016a) Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plant 2:16139
Li QL, Zhang DB, Chen MJ, Liang WQ, Wei JJ, Qi YP, Yuan Z (2016b) Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. Genet Genomic 43:415–419
Li XF, Zhou WJ, Ren YK, Tian XJ, Lv TX, Wang ZY, Fang J, Chu CC, Yang J, Bu QY (2017) High-efficiency breeding of early-maturing rice ultivars via CRISPR/Cas9-mediated genome editing. Genet Genom 44:175–178
Liu YG, Li GS, Zhang YL, Chen LT (2019) Current advances on CRISPR/Cas genome editing technologies in plants. J S China Agr Univ 40:38–49
Lu Y, Zhu JK (2016) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol Plant 10:523–525
Ma XS, Feng FJ, Zhang Y, Elesawi IE, Xu K, Li TF, Mei HW, Liu HY, Gao NN, Chen CL, Luo LJ, Yu SW (2019) A novel rice grain size gene OsSNB was identified by genome-wide association study in natural population. PLoS Genet 15:e1008191
Macovei A, Sevilla NR, Cantos C, Jonson GB, Loedin IS, Tomáš Č, Voytas DF, Choi IR, Mohanty PC (2018) Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to Rice tungro spherical virus. Plant Biotechnol J:12927. https://doi.org/10.1111/pbicompany
Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826
Mao YF, Botella JR, Liu YG, Zhu JK (2019) Gene editing in plants: progress and challenges. Natl Sci Rev 6:421–437. https://doi.org/10.1093/nsr/nwz005
Meng H, Xu P, Zhang YX, Wang H, Cao L, Cheng SH, Shen XH (2018) CRISPR/Cas9-mediated editing of GS3 to improve flowering time in japonica rice. Chin J Rice Sci 32:119–127
Miao J, Guo DS, Zhang JZ, Huang QP, Qin GJ, Zhang X, Wan JM, Gu HY, Qu LJ (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23:1233–1236
Mikami I, Uwatoko N, IkedaY YJ, Hirano HY, Suzuki Y, Sano Y (2008) Allelic diversification at the wx locus in landraces of Asian rice. Theor Appl Genet 116:979–989
Mojica FJ, Cesar DV, Elena S, Guadalupe J (2000) Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol 36:244–246
Mojica FJ, Ferrer C, Juez G, Rodríguez-Valera F (1995) 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. Mol Microbiol 17:85–93
Oliva R, Ji CH, Atienza-Grande G, Huguet-Tapia JC, Perez-Quintero A, Li T, Eom JS, Li CH, Nguyen H, Liu B, Auguy F, Sciallano C, Luu VT, Dossa GS, Cunnac S, Schmidt SM, Slamet-Loedin IH, Cruz CV, Szurek B, Frommer WB, White FF, Yang B (2019) Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol 37:1344–1350
Pource C, Salvignol G, Vergnaud G (2005) CRISPR elements in Versinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiol 151:653–663
Qi YB, Zhang LX, Wang LY, Song J, Wang JJ (2020) CRISPR/Cas9 targeted editing for the fragrant gene Badh2 in rice. Scientia Agr Sinica 53:1501–1509
Rodolphe B, Christophe F, Hélène D, Melissa R, Patrick B, Sylvain M, Dennis AR, Philippe H (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712
Santoso TJ, Trijatmiko KR, Char SN, Yang B, Wang K (2020) Targeted mutation of GA20ox-2 gene using CRISPR/Cas9 system generated semi-dwarf phenotype in rice. Front Plant Sci 482. https://doi.org/10.1088/1755-1315/482/1/012027
Shan QW, Wang YP, Li J, Zhang Y, Chen KL, Liang Z, Zhang K, Liu JX, Xi JZ, Qiu JL, Gao CX (2013) Targeted genome modification of crop plants using a CRISPR/Cas system. Nat Biotechnol 31:686–688
Shen L, HuaYF FYP, Li J, Liu Q, Jiao XZ, Xin GW, Wang JJ, Wang XH, Yan C, Wang K (2017) Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice. Sci China Life Sci 60:506–515
Sufia F, Neha J, Nisha S, Rohini S, Prasanta KD, Rhitu R, Sandeep Y, Pramod K, Ananda KS, Ajay J, Nagendra KS, Vandna R (2019) CRISPR-Cas9 directed genome engineering for enhancing salt stress tolerance in rice. Semin Cell Dev Biol 96:91–99
Sun YW, Jiao GA, Liu ZP, Zhang X, Li JY, Guo XP, Du WM, Du JL, Francis F, Zhao YD, Xia LQ (2017) Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00298
Tang L, Mao BG, Li YK, Lv QM, Zhang LP, Chen CY, He HJ, Wang WP, Zeng XF, Shao Y, Pan YL, Hu YY, Peng Y, Fu XQ, Li HQ, Xia ST, Zhao BG (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7:14438
Usman B, Nawaz G, Zhao N, Liao SY, Qin BX, Liu F, Liu YG, Li RB (2020) Programmed editing of rice (Oryza sativa L.) OsSPL16gene using CRISPR/Cas9 improves grain yield by modulating the expression of pyruvate enzymes and cell cycle proteins. Int J Mol Sci 22. https://doi.org/10.3390/ijms22010249
Wang C, Liu Q, Shen Y, Hua YF, Wang JJ, Lin JN, Wu MG, Sun TT, Cheng ZK, Mercier R, Wang KJ (2019) Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat Biotechnol 37:283–286
Wang FJ, Wang CL, Liu PQ, Lei CL, Hao W, Gao Y, Liu YG, Zhao KJ (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One 11:e154027
Wang G, Wang C, Lu G, Wang W, Greene TW (2020) Knockouts of a late flowering gene via CRISPR-Cas9 confer early maturity in rice at multiple field locations. Plant Biotechnol J 104:137–150. https://doi.org/10.1007/s11103-020-01031-w
Wu MJ, Liu HQ, Lin Y, Chen JM, Fu YP, Luo JM, Zhang ZJ, Liang KJ, Chen SB, Wang F (2020) In-frame and frame-shift editing of the Ehd1 gene to develop japonica rice with prolonged basic vegetative growth periods. Front Plant Sci 11. https://doi.org/10.3389/fpls.2020.00307
Xie YY, Niu BX, Long YM, Li GS, Tang JT, ZhangYL RD, Liu YG, Chen LT (2017) Suppression or knockout of SaFISaM overcomes the Sa-mediated hybrid male sterility in rice. Integr Plant Biol 59:669–679
Xie YY, Tang JT, Xie XR, Li XJ, Huang JL, Fei Y, Han JL, Chen SF, Tang HW, Zhao XC, Tao DY, Xu P, Liu YG, Chen L (2019) An asymmetric allelic interaction drives allele transmission bias in interspecific rice hybrids. Nat Commun 10:2501
Xu P, Wang H, Tu RR, Liu QE, Wu WQ, Fu XM, Cao LY, Shen XH (2019) Orientation improvement of blast resistance in rice via CRISPR/Cas9 system. Zhongguo Shuidao Kexue 33:313–322
Xu Y, Wang FQ, Chen ZH, Wang J, Li WQ, Fan FJ, Tao YJ, Zhao L, Zhong WG, Zhu QH, Yang J (2020) Intron-targeted gene insertion in rice using CRISPR/Cas9: A case study of the Pi-ta gene. Crop J 8:424–431. https://doi.org/10.1016/j.cj.2019.03.006
Xue WY, Xing YZ, Weng XY, Zhao Y, Tang WJ, Wang L, Zhou HJ, Yu SB, Xu CG, Li XH, Zhang QF (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767
Yang P, Chen CL, Yao XY, Xiong YH, Huang YP, Hu B, Yin JH (2020) Improvement of amylase and fragrance levels of rice by CRISPR/Cas9 system. Mol Plant Breed 18:915–923
Yu H, Lin T, Meng X, Du H, Zhang J, Liu G, Chen M, Jing Y, Kou L, Li X, Gao Q, Liang Y, Liu X, Fan Z, Liang Y, Cheng Z, Chen M, Tian Z, Wang Y, Chu C, Zuo J, Wan J, Qian Q, Han B, Zuccolo A, Wing RA, Gao C, Liang C, Li JY (2021) A route to de novo domestication of wild allotetraploid rice. Cell 184:1156–1170.e14. https://doi.org/10.1016/j.cell.2021.01.013
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 11. https://doi.org/10.3389/fpls.2020.00575
Zhang J, Fan X, Hu Y, Zhou X, He Q, Liang L, Xing Y (2020) Global analysis of CCT family knockout mutants identifies four genes involved in regulating heading date in rice. J Integr Plant Biol. https://doi.org/10.1111/jipb.13013
Zhang JS, Zhang H, Botella JR, Zhu JK (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
Zhou H, He M, Li J, Chen L, Huang ZF, Zheng SY, Zhu LY, Ni E, Jiang DG, Zhao BG, Zhuang CX (2016) Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci Rep 6:37395
Zhou JH, Peng Z, Long JY, Sosso D, Liu B, Eom JS, Huang S, Liu SZ, Cruz CV, Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant 82:632–643
Zhou JP, Xin XH, He Y, Chen HQ, Li Q, Tang X, Zhong ZH, Deng KJ, Zheng XL, Akher SA, Cai GZ, Qi YP, Zhang Y (2019) Multiplex QTL editing of grain-related genes improves yield in elite rice varieties. Plant Cell Rep 38:475–485
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This research project is supported by National Natural Science Foundation of China (31000703 and 31360329), Guangxi Science and Technology Projects (AA17204049, AA18221043 and AA17204050-2).
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Editor: Prakash Lakshmanan
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Ma, Z., Wei, M., Zhang, Y. et al. Development of CRISPR_Cas9 genome editing system and its application in rice molecular breeding. In Vitro Cell.Dev.Biol.-Plant 57, 700–708 (2021). https://doi.org/10.1007/s11627-021-10203-2
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DOI: https://doi.org/10.1007/s11627-021-10203-2