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CRISPR/Cas Plant Genome Editing Systems and Their Applications in Maize |
YANG Meng-bing1,2,JIANG Yi-lin1,2,ZHU Lei1,2,AN Xue-li1,2,3,**(),WAN Xiang-yuan1,2,3,**() |
1 Research Center of Biology and Agriculture, Shunde Graduate School, School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing 100083, China 2 Zhongzhi International Institute of Agricultural Biosciences, Beijing 100192, China 3 Beijing Engineering Laboratory of Main Crop Bio-Tech Breeding, Beijing International Science and Technology Cooperation Base of Bio-Tech Breeding, Beijing Solidwill Sci-Tech Co., Ltd., Beijing 100192, China |
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Abstract Due to their simplicity and high efficiency, CRISPR/Cas systems provide efficient tools for functional genomics and crop molecular breeding. In this review, we summarize the current developments of CRISPR/Cas genomic editing systems in plants and compare the differences between these systems and their derivative technologies. We review the applications of CRISPR/Cas9 editing technology in maize improvement focusing on yield, quality, disease resistance, abiotic stress resistance, male sterile line development and haploid induction. Finally, we discuss the future improvement of CRISPR/Cas systems and provide perspectives on prospect genome editing technologies.
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Received: 02 November 2021
Published: 13 January 2022
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Corresponding Authors:
Xue-li AN,Xiang-yuan WAN
E-mail: xuelian@ustb.edu.cn;wanxiangyuan@ustb.edu.cn
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|
|
[1] |
Maximiano M R, Távora F T P K, Prado G S, et al. CRISPR genome editing technology: a powerful tool applied to developing agribusiness. Journal of Agricultural and Food Chemistry, 2021, 69(23): 6379-6395.
doi: 10.1021/acs.jafc.1c01062
pmid: 34097395
|
|
|
[2] |
Christian M, Cermak T, Doyle E L, et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics, 2010, 186(2): 757-761.
doi: 10.1534/genetics.110.120717
pmid: 20660643
|
|
|
[3] |
Urnov F D, Rebar E J, Holmes M C, et al. Genome editing with engineered zinc finger nucleases. Nature Reviews Genetics, 2010, 11(9): 636-646.
doi: 10.1038/nrg2842
|
|
|
[4] |
González Castro N G, Bjelic J, Malhotra G, et al. Comparison of the feasibility, efficiency, and safety of genome editing technologies. International Journal of Molecular Sciences, 2021, 22(19): 10355.
doi: 10.3390/ijms221910355
|
|
|
[5] |
Zhu H C, Li C, Gao C X. Applications of CRISPR-Cas in agriculture and plant biotechnology. Nature Reviews Molecular Cell Biology, 2020, 21(11): 661-677.
doi: 10.1038/s41580-020-00288-9
|
|
|
[6] |
Barrangou R, Marraffini L A. CRISPR-cas systems: prokaryotes upgrade to adaptive immunity. Molecular Cell, 2014, 54(2): 234-244.
doi: 10.1016/j.molcel.2014.03.011
pmid: 24766887
|
|
|
[7] |
Makarova K S, Wolf Y I, Alkhnbashi O S, et al. An updated evolutionary classification of CRISPR-Cas systems. Nature Reviews Microbiology, 2015, 13(11): 722-736.
doi: 10.1038/nrmicro3569
pmid: 26411297
|
|
|
[8] |
Makarova K S, Wolf Y I, Iranzo J, et al. Evolutionary classification of CRISPR-Cas systems: a burst of class 2 and derived variants. Nature Reviews Microbiology, 2020, 18(2): 67-83.
doi: 10.1038/s41579-019-0299-x
pmid: 31857715
|
|
|
[9] |
Biswas S, Zhang D B, Shi J X. CRISPR/Cas systems: opportunities and challenges for crop breeding. Plant Cell Reports, 2021, 40(6): 979-998.
doi: 10.1007/s00299-021-02708-2
|
|
|
[10] |
Jinek M, Jiang F G, Taylor D W, et al. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science, 2014, 343(6176): 1247997.
doi: 10.1126/science.1247997
|
|
|
[11] |
Jinek M, Chylinski K, Fonfara I, et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 2012, 337(6096): 816-821.
doi: 10.1126/science.1225829
|
|
|
[12] |
Mali P, Yang L H, Esvelt K M, et al. RNA-guided human genome engineering via Cas9. Science, 2013, 339(6121): 823-826.
doi: 10.1126/science.1232033
|
|
|
[13] |
Cong L, Ran F A, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339(6121): 819-823.
doi: 10.1126/science.1231143
pmid: 23287718
|
|
|
[14] |
Shan Q W, Wang Y P, Li J, et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology, 2013, 31(8): 686-688.
doi: 10.1038/nbt.2650
|
|
|
[15] |
Li J F, Norville J E, Aach J, et al. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology, 2013, 31(8): 688-691.
doi: 10.1038/nbt.2654
|
|
|
[16] |
Nekrasov V, Staskawicz B, Weigel D, et al. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nature Biotechnology, 2013, 31(8): 691-693.
doi: 10.1038/nbt.2655
|
|
|
[17] |
Hille F, Richter H, Wong S P, et al. The biology of CRISPR-Cas: backward and forward. Cell, 2018, 172(6): 1239-1259.
doi: 10.1016/j.cell.2017.11.032
|
|
|
[18] |
Butiuc-Keul A, Farkas A, Carpa R, et al. CRISPR-Cas system: the powerful modulator of accessory genomes in prokaryotes. Microbial Physiology, 2021: 1-16.
|
|
|
[19] |
Mladenov E, Iliakis G. Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutation Research, 2011, 711(1-2): 61-72.
doi: 10.1016/j.mrfmmm.2011.02.005
|
|
|
[20] |
Siebert R, Puchta H. Efficient repair of genomic double-strand breaks by homologous recombination between directly repeated sequences in the plant genome. The Plant Cell, 2002, 14(5): 1121-1131.
doi: 10.1105/tpc.001727
|
|
|
[21] |
Char S N, Neelakandan A K, Nahampun H, et al. An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnology Journal, 2017, 15(2): 257-268.
doi: 10.1111/pbi.2017.15.issue-2
|
|
|
[22] |
Zetsche B, Gootenberg J S, Abudayyeh O O, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 2015, 163(3): 759-771.
doi: 10.1016/j.cell.2015.09.038
pmid: 26422227
|
|
|
[23] |
Shmakov S, Abudayyeh O O, Makarova K S, et al. Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Molecular Cell, 2015, 60(3): 385-397.
doi: 10.1016/j.molcel.2015.10.008
pmid: 26593719
|
|
|
[24] |
Bandyopadhyay A, Kancharla N, Javalkote V S, et al. CRISPR-Cas12a (Cpf1): a versatile tool in the plant genome editing tool box for agricultural advancement. Frontiers in Plant Science, 2020, 11: 584151.
doi: 10.3389/fpls.2020.584151
|
|
|
[25] |
Banakar R, Schubert M, Collingwood M, et al. Comparison of CRISPR-Cas9/Cas12a ribonucleoprotein complexes for genome editing efficiency in the rice phytoene desaturase (OsPDS) gene. Rice, 2020, 13(1): 1-7.
doi: 10.1186/s12284-019-0361-3
|
|
|
[26] |
Lee K, Zhang Y X, Kleinstiver B P, et al. Activities and specificities of CRISPR/Cas9 and Cas12a nucleases for targeted mutagenesis in maize. Plant Biotechnology Journal, 2019, 17(2): 362-372.
doi: 10.1111/pbi.2019.17.issue-2
|
|
|
[27] |
Kim H, Kim S T, Ryu J, et al. CRISPR/Cpf1-mediated DNA-free plant genome editing. Nature Communications, 2017, 8: 14406.
doi: 10.1038/ncomms14406
|
|
|
[28] |
Schindele A, Dorn A, Puchta H. CRISPR/Cas brings plant biology and breeding into the fast lane. Current Opinion in Biotechnology, 2020, 61: 7-14.
doi: S0958-1669(19)30060-6
pmid: 31557657
|
|
|
[29] |
Endo A, Masafumi M, Kaya H, et al. Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Scientific Reports, 2016, 6: 38169.
doi: 10.1038/srep38169
|
|
|
[30] |
Li C X, Liu C L, Qi X T, et al. RNA-guided Cas9 as an in vivo desired-target mutator in maize. Plant Biotechnology Journal, 2017, 15(12): 1566-1576.
doi: 10.1111/pbi.2017.15.issue-12
|
|
|
[31] |
Liu L, Gallagher J, Arevalo E D, et al. Enhancing grain-yield-related traits by CRISPR-Cas9 promoter editing of maize CLE genes. Nature Plants, 2021, 7(3): 287-294.
doi: 10.1038/s41477-021-00858-5
|
|
|
[32] |
Qi X T, Wu H, Jiang H Y, et al. Conversion of a normal maize hybrid into a waxy version using in vivo CRISPR/Cas9 targeted mutation activity. The Crop Journal, 2020, 8(3): 440-448.
doi: 10.1016/j.cj.2020.01.006
|
|
|
[33] |
Wilson L M, Whitt S R, Ibáñez A M, et al. Dissection of maize kernel composition and starch production by candidate gene association. The Plant Cell, 2004, 16(10): 2719-2733.
doi: 10.1105/tpc.104.025700
|
|
|
[34] |
Shi J R, Gao H R, Wang H Y, et al. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnology Journal, 2017, 15(2): 207-216.
doi: 10.1111/pbi.2017.15.issue-2
|
|
|
[35] |
Svitashev S, Schwartz C, Lenderts B, et al. Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nature Communications, 2016, 7: 13274.
doi: 10.1038/ncomms13274
pmid: 27848933
|
|
|
[36] |
Li Y M, Zhu J J, Wu H, et al. Precise base editing of non-allelic acetolactate synthase genes confers sulfonylurea herbicide resistance in maize. The Crop Journal, 2020, 8(3): 449-456.
doi: 10.1016/j.cj.2019.10.001
|
|
|
[37] |
Zhang Z H, Zhang X, Lin Z L, et al. A large transposon insertion in the stiff1 promoter increases stalk strength in maize. The Plant Cell, 2020, 32(1): 152-165.
doi: 10.1105/tpc.19.00486
|
|
|
[38] |
Zhang J J, Zhang X F, Chen R R, et al. Generation of transgene-free semidwarf maize plants by gene editing of Gibberellin-Oxidase20-3 using CRISPR/Cas9. Frontiers in Plant Science, 2020, 11: 1048.
doi: 10.3389/fpls.2020.01048
|
|
|
[39] |
Pathi K M, Rink P, Budhagatapalli N, et al. Engineering smut resistance in maize by site-directed mutagenesis of LIPOXYGENASE 3. Frontiers in Plant Science, 2020, 11: 543895.
doi: 10.3389/fpls.2020.543895
|
|
|
[40] |
Li Q Q, Wu G X, Zhao Y P, et al. CRISPR/Cas9-mediated knockout and overexpression studies reveal a role of maize phytochrome C in regulating flowering time and plant height. Plant Biotechnology Journal, 2020, 18(12): 2520-2532.
doi: 10.1111/pbi.v18.12
|
|
|
[41] |
Huang C, Sun H Y, Xu D Y, et al. ZmCCT9 enhances maize adaptation to higher latitudes. PNAS, 2018, 115(2): E334-E341.
doi: 10.1073/pnas.1718058115
|
|
|
[42] |
Li J, Zhang H W, Si X M, et al. Generation of thermosensitive male-sterile maize by targeted knockout of the ZmTMS5 gene. Journal of Genetics and Genomics, 2017, 44(9): 465-468.
doi: 10.1016/j.jgg.2017.02.002
|
|
|
[43] |
Chen R R, Xu Q L, Liu Y, et al. Generation of transgene-free maize male sterile lines using the CRISPR/Cas9 system. Frontiers in Plant Science, 2018, 9: 1180.
doi: 10.3389/fpls.2018.01180
|
|
|
[44] |
Teng C, Zhang H, Hammond R, et al. Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nature Communications, 2020, 11: 2912.
doi: 10.1038/s41467-020-16634-6
|
|
|
[45] |
Zhong Y, Liu C X, Qi X L, et al. Mutation of ZmDMP enhances haploid induction in maize. Nature Plants, 2019, 5(6): 575-580.
doi: 10.1038/s41477-019-0443-7
pmid: 31182848
|
|
|
[46] |
Liu C X, Li X, Meng D X, et al. A 4-bp insertion at ZmPLA1 encoding a putative phospholipase A generates haploid induction in maize. Molecular Plant, 2017, 10(3): 520-522.
doi: 10.1016/j.molp.2017.01.011
|
|
|
[47] |
Gao H R, Mutti J, Young J K, et al. Complex trait loci in maize enabled by CRISPR-Cas9 mediated gene insertion. Frontiers in Plant Science, 2020, 11: 535.
doi: 10.3389/fpls.2020.00535
|
|
|
[48] |
Schoof H, Lenhard M, Haecker A, et al. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell, 2000, 100(6): 635-644.
pmid: 10761929
|
|
|
[49] |
Moreno M A, Harper L C, Krueger R W, et al. liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes & Development, 1997, 11(5): 616-628.
doi: 10.1101/gad.11.5.616
|
|
|
[50] |
Nelson O E, Rines H W. The enzymatic deficiency in the waxy mutant of maize. Biochemical and Biophysical Research Communications, 1962, 9(4): 297-300.
doi: 10.1016/0006-291X(62)90043-8
|
|
|
[51] |
Gao H R, Gadlage M J, Lafitte H R, et al. Superior field performance of waxy corn engineered using CRISPR-Cas9. Nature Biotechnology, 2020, 38(5): 579-581.
doi: 10.1038/s41587-020-0444-0
|
|
|
[52] |
Dong L, Qi X T, Zhu J J, et al. Supersweet and waxy: meeting the diverse demands for specialty maize by genome editing. Plant Biotechnology Journal, 2019, 17(10): 1853-1855.
doi: 10.1111/pbi.13144
pmid: 31050154
|
|
|
[53] |
Sharma P, Gayen D. Plant protease as regulator and signaling molecule for enhancing environmental stress-tolerance. Plant Cell Reports, 2021, 40(11): 2081-2095.
doi: 10.1007/s00299-021-02739-9
|
|
|
[54] |
Matres J M, Hilscher J, Datta A, et al. Genome editing in cereal crops: an overview. Transgenic Research, 2021, 30(4): 461-498.
doi: 10.1007/s11248-021-00259-6
|
|
|
[55] |
Buckler E S, Holland J B, Bradbury P J, et al. The genetic architecture of maize flowering time. Science, 2009, 325(5941): 714-718.
doi: 10.1126/science.1174276
pmid: 19661422
|
|
|
[56] |
Jiang Y L, Li Z W, Liu X Z, et al. ZmFAR1 and ZmABCG26 regulated by microRNA are essential for lipid metabolism in maize anther. International Journal of Molecular Sciences, 2021, 22(15): 7916.
doi: 10.3390/ijms22157916
|
|
|
[57] |
Jiang Y L, An X L, Li Z W, et al. CRISPR/Cas9-based discovery of maize transcription factors regulating male sterility and their functional conservation in plants. Plant Biotechnology Journal, 2021, 19(9): 1769-1784.
doi: 10.1111/pbi.v19.9
|
|
|
[58] |
Seguí-Simarro J M, Jacquier N M A, Widiez T. Overview of in vitro and in vivo doubled haploid technologies. Doubled Haploid Technology, 2021. DOI: 10.1007/978-1-0716-1315-3_1.
doi: 10.1007/978-1-0716-1315-3_1
|
|
|
[59] |
Kelliher T, Starr D, Su X J, et al. One-step genome editing of elite crop germplasm during haploid induction. Nature Biotechnology, 2019, 37(3): 287-292.
doi: 10.1038/s41587-019-0038-x
pmid: 30833776
|
|
|
[60] |
Wang B B, Zhu L, Zhao B B, et al. Development of a haploid-inducer mediated genome editing system for accelerating maize breeding. Molecular Plant, 2019, 12(4): 597-602.
doi: 10.1016/j.molp.2019.03.006
|
|
|
[61] |
Cho S W, Kim S, Kim Y, et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Research, 2014, 24(1): 132-141.
doi: 10.1101/gr.162339.113
|
|
|
[62] |
Ledford H. US regulation misses some GM crops. Nature, 2013, 500(7463): 389-390.
doi: 10.1038/500389a
|
|
|
[63] |
Jones H D. Regulatory uncertainty over genome editing. Nature Plants, 2015, 1: 14011.
doi: 10.1038/nplants.2014.11
pmid: 27246057
|
|
|
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