logo

SCIENCE CHINA Life Sciences, Volume 60, Issue 5: 490-505(2017) https://doi.org/10.1007/s11427-017-9022-1

Current and future editing reagent delivery systems for plant genome editing

More info
  • ReceivedFeb 28, 2017
  • AcceptedMar 22, 2017
  • PublishedMay 1, 2017

Abstract

Many genome editing tools have been developed and new ones are anticipated; some have been extensively applied in plant genetics, biotechnology and breeding, especially the CRISPR/Cas9 system. These technologies have opened up a new era for crop improvement due to their precise editing of user-specified sequences related to agronomic traits. In this review, we will focus on an update of recent developments in the methodologies of editing reagent delivery, and consider the pros and cons of current delivery systems. Finally, we will reflect on possible future directions.


Interest statement

The author(s) declare that they have no conflict of interest.


References

[1] Alagoz Y., Gurkok T., Zhang B., Unver T.. Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci Rep, 2016, 6: 30910 CrossRef PubMed ADS Google Scholar

[2] Ainley W.M., Sastry-Dent L., Welter M.E., Murray M.G., Zeitler B., Amora R., Corbin D.R., Miles R.R., Arnold N.L., Strange T.L., Simpson M.A., Cao Z., Carroll C., Pawelczak K.S., Blue R., West K., Rowland L.M., Perkins D., Samuel P., Dewes C.M., Shen L., Sriram S., Evans S.L., Rebar E.J., Zhang L., Gregory P.D., Urnov F.D., Webb S.R., Petolino J.F.. Trait stacking via targeted genome editing. Plant Biotechnol J, 2013, 11: 1126-1134 CrossRef PubMed Google Scholar

[3] Ali Z., Abul-faraj A., Li L., Ghosh N., Piatek M., Mahjoub A., Aouida M., Piatek A., Baltes N.J., Voytas D.F., Dinesh-Kumar S., Mahfouz M.M.. Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant, 2015, 8: 1288-1291 CrossRef PubMed Google Scholar

[4] Altpeter F., Springer N.M., Bartley L.E., Blechl A.E., Brutnell T.P., Citovsky V., Conrad L.J., Gelvin S.B., Jackson D.P., Kausch A.P., Lemaux P.G., Medford J.I., Orozco-Cárdenas M.L., Tricoli D.M., Van Eck J., Voytas D.F., Walbot V., Wang K., Zhang Z.J., Stewart C.N.. Advancing crop transformation in the era of genome editing. Plant Cell, 2016, 28: 1510-1520 CrossRef PubMed Google Scholar

[5] Andersson M., Turesson H., Nicolia A., Fält A.S., Samuelsson M., Hofvander P.. Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Rep, 2017, 36: 117-128 CrossRef PubMed Google Scholar

[6] Baltes N.J., Gil-Humanes J., Cermak T., Atkins P.A., Voytas D.F.. DNA replicons for plant genome engineering. Plant Cell, 2014, 26: 151-163 CrossRef PubMed Google Scholar

[7] Belhaj K., Chaparro-Garcia A., Kamoun S., Nekrasov V.. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods, 2013, 9: 39 CrossRef PubMed Google Scholar

[8] Beetham P.R., Kipp P.B., Sawycky X.L., Arntzen C.J., May G.D.. A tool for functional plant genomics: chimeric RNA/DNA oligonucleotides cause in vivo gene-specific mutations. Proc Natl Acad Sci USA, 1999, 96: 8774-8778 CrossRef Google Scholar

[9] Bortesi L., Fischer R.. The CRISPR/Cas9 system for plant genome editing and beyond. Biotech Adv, 2015, 33: 41-52 CrossRef PubMed Google Scholar

[10] Brooks C., Nekrasov V., Lippman Z.B., Van Eck J.. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol, 2014, 166: 1292-1297 CrossRef PubMed Google Scholar

[11] Butler N.M., Atkins P.A., Voytas D.F., Douches D.S.. Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) using the CRISPR/Cas system. PLoS ONE, 2015, 10: e0144591 CrossRef PubMed ADS Google Scholar

[12] Cai Y., Chen L., Liu X., Sun S., Wu C., Jiang B., Han T., Hou W.. CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS ONE, 2015, 10: e0136064 CrossRef PubMed ADS Google Scholar

[13] Cai C.Q., Doyon Y., Ainley W.M., Miller J.C., Dekelver R.C., Moehle E.A., Rock J.M., Lee Y.L., Garrison R., Schulenberg L., Blue R., Worden A., Baker L., Faraji F., Zhang L., Holmes M.C., Rebar E.J., Collingwood T.N., Rubin-Wilson B., Gregory P.D., Urnov F.D., Petolino J.F.. Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol, 2009, 69: 699-709 CrossRef PubMed Google Scholar

[14] Cao M.X., Huang J.Q., Yao Q.H., Liu S.J., Wang C.L., Wei Z.M.. Site-specific DNA excision in transgenic rice with a cell-permeable cre recombinase. Mol Biotechnol, 2006, 32: 055-064 CrossRef Google Scholar

[15] Čermák T., Baltes N.J., Čegan R., Zhang Y., Voytas D.F.. High-frequency, precise modification of the tomato genome. Genome Biol, 2015, 16: 232 CrossRef PubMed Google Scholar

[16] Chandrasekaran J., Brumin M., Wolf D., Leibman D., Klap C., Pearlsman M., Sherman A., Arazi T., Gal-On A.. Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol, 2016, 17: 1140-1153 CrossRef PubMed Google Scholar

[17] Char S.N., Unger-Wallace E., Frame B., Briggs S.A., Main M., Spalding M.H., Vollbrecht E., Wang K., Yang B.. Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J, 2015, 13: 1002-1010 CrossRef PubMed Google Scholar

[18] Chugh A., Eudes F., Shim Y.S.. Cell-penetrating peptides: nanocarrier for macromolecule delivery in living cells. IUBMB Life, 2010, 62: 183-193 CrossRef PubMed Google Scholar

[19] Clasen B.M., Stoddard T.J., Luo S., Demorest Z.L., Li J., Cedrone F., Tibebu R., Davison S., Ray E.E., Daulhac A., Coffman A., Yabandith A., Retterath A., Haun W., Baltes N.J., Mathis L., Voytas D.F., Zhang F.. Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J, 2016, 14: 169-176 CrossRef PubMed Google Scholar

[20] Cole-Strauss A., Yoon K., Xiang Y., Byrne B.C., Rice M.C., Gryn J., Holloman W.K., Kmiec E.B.. Correction of the mutation responsible for sickle cell anemia by an RNA-DNA oligonucleotide. Science, 1996, 273: 1386-1389 CrossRef ADS Google Scholar

[21] Curtin S.J., Zhang F., Sander J.D., Haun W.J., Starker C., Baltes N.J., Reyon D., Dahlborg E.J., Goodwin M.J., Coffman A.P., Dobbs D., Joung J.K., Voytas D.F., Stupar R.M.. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol, 2011, 156: 466-473 CrossRef PubMed Google Scholar

[22] de Pater S., Neuteboom L.W., Pinas J.E., Hooykaas P.J.J., van der Zaal B.J.. ZFN-induced mutagenesis and gene-targeting in Arabidopsis through Agrobacterium-mediated floral dip transformation. Plant Biotech J, 2009, 7: 821-835 CrossRef PubMed Google Scholar

[23] de Pater S., Pinas J.E., Hooykaas P.J.J., van der Zaal B.J.. ZFN-mediated gene targeting of the Arabidopsis protoporphyrinogen oxidase gene through Agrobacterium-mediated floral dip transformation. Plant Biotechnol J, 2013, 11: 510-515 CrossRef PubMed Google Scholar

[24] Dinesh-Kumar, S.P., Anandalakshmi, R., Marathe, R., Schiff, M., and Liu, Y. (2003). Virus-induced gene silencing. Methods Mol Biol 236, 287–294. Google Scholar

[25] Dong C., Beetham P., Vincent K., Sharp P.. Oligonucleotide-directed gene repair in wheat using a transient plasmid gene repair assay system. Plant Cell Rep, 2006, 25: 457-465 CrossRef PubMed Google Scholar

[26] Du J., Jin J., Yan M., Lu Y.. Synthetic nanocarriers for intracellular protein delivery. Curr Drug Metab, 2012, 13: 82-92 CrossRef Google Scholar

[27] Du H., Zeng X., Zhao M., Cui X., Wang Q., Yang H., Cheng H., Yu D.. Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotech, 2016, 217: 90-97 CrossRef PubMed Google Scholar

[28] English J., Davenport G., Elmayan T., Vaucheret H., Baulcombe D.. Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J, 1997, 12: 597-603 CrossRef Google Scholar

[29] Fan D., Liu T., Li C., Jiao B., Li S., Hou Y., Luo K.. Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep, 2015, 5: 12217 CrossRef PubMed ADS Google Scholar

[30] Fauser F., Schiml S., Puchta H.. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J, 2014, 79: 348-359 CrossRef PubMed Google Scholar

[31] Feng Z., Zhang B., Ding W., Liu X., Yang D.L., Wei P., Cao F., Zhu S., Zhang F., Mao Y., Zhu J.K.. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res, 2013, 23: 1229-1232 CrossRef PubMed Google Scholar

[32] Feng Z., Mao Y., Xu N., Zhang B., Wei P., Yang D.L., Wang Z., Zhang Z., Zheng R., Yang L., Zeng L., Liu X., Zhu J.K.. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA, 2014, 111: 4632-4637 CrossRef PubMed ADS Google Scholar

[33] Forner J., Pfeiffer A., Langenecker T., Manavella P.A., Manavella P., Lohmann J.U.. Germline-transmitted genome editing in Arabidopsis thaliana using TAL-effector-nucleases. PLoS ONE, 2015, 10: e0121056 CrossRef PubMed ADS Google Scholar

[34] Forsyth A., Weeks T., Richael C., Duan H.. Transcription activator-like effector nucleases (TALEN)-mediated targeted DNA insertion in potato plants. Front Plant Sci, 2016, 7: 1572 CrossRef PubMed Google Scholar

[35] Gao J., Wang G., Ma S., Xie X., Wu X., Zhang X., Wu Y., Zhao P., Xia Q.. CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol, 2015, 87: 99-110 CrossRef PubMed Google Scholar

[36] Gelvin S.B.. Agrobacterium-mediated plant transformation: the biology behind the “Gene-Jockeying” tool. Microbiol Mol Biol Rev, 2003, 67: 16-37 CrossRef Google Scholar

[37] Gil-Humanes J., Wang Y., Liang Z., Shan Q., Ozuna C.V., Sánchez-León S., Baltes N.J., Starker C., Barro F., Gao C., Voytas D.F.. High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J, 2017, 89: 1251-1262 CrossRef PubMed Google Scholar

[38] Gupta M., DeKelver R.C., Palta A., Clifford C., Gopalan S., Miller J.C., Novak S., Desloover D., Gachotte D., Connell J., Flook J., Patterson T., Robbins K., Rebar E.J., Gregory P.D., Urnov F.D., Petolino J.F.. Transcriptional activation of Brassica napus β-ketoacyl-ACP synthase II with an engineered zinc finger protein transcription factor. Plant Biotech J, 2012, 10: 783-791 CrossRef PubMed Google Scholar

[39] Gurushidze M., Hensel G., Hiekel S., Schedel S., Valkov V., Kumlehn J.. True-breeding targeted gene knock-out in barley using designer TALE-nuclease in haploid cells. PLoS ONE, 2014, 9: e92046 CrossRef PubMed ADS Google Scholar

[40] Hartung F., Schiemann J.. Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J, 2014, 78: 742-752 CrossRef PubMed Google Scholar

[41] Haun W., Coffman A., Clasen B.M., Demorest Z.L., Lowy A., Ray E., Retterath A., Stoddard T., Juillerat A., Cedrone F., Mathis L., Voytas D.F., Zhang F.. Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J, 2014, 12: 934-940 CrossRef PubMed Google Scholar

[42] Huang Y.W., Lee H.J., Tolliver L.M., Aronstam R.S.. Delivery of nucleic acids and nanomaterials by cell-penetrating peptides: opportunities and challenges. BioMed Res Int, 2015, 2015: 1-16 CrossRef PubMed Google Scholar

[43] Ito Y., Nishizawa-Yokoi A., Endo M., Mikami M., Toki S.. CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem Biophys Res Commun, 2015, 467: 76-82 CrossRef PubMed Google Scholar

[44] Jacobs T.B., LaFayette P.R., Schmitz R.J., Parrott W.A.. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol, 2015, 15: 16 CrossRef PubMed Google Scholar

[45] Jensen, S.P., Febres, V.J., and Moore, G.A. (2014). Cell penetrating peptides as an alternative transformation method in citrus. J Citrus Pathol 1, 10.15. Google Scholar

[46] Jia H., Wang N.. Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE, 2014a, 9: e93806 CrossRef PubMed ADS Google Scholar

[47] Jia H., Wang N.. Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves. Plant Cell Rep, 2014b, 33: 1993-2001 CrossRef PubMed Google Scholar

[48] Jia H., Orbovic V., Jones J.B., Wang N.. Modification of the PthA4 effector binding elements in Type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4:dCsLOB1.3 infection. Plant Biotechnol J, 2016, 14: 1291-1301 CrossRef PubMed Google Scholar

[49] Jiang W., Zhou H., Bi H., Fromm M., Yang B., Weeks D.P.. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res, 2013, 41: e188 CrossRef PubMed Google Scholar

[50] Jiang W.Z., Yang B., Weeks D.P.. Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS ONE, 2014, 9: e99225 CrossRef PubMed ADS Google Scholar

[51] Jung J.H., Altpeter F.. 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, 2016, 92: 131-142 CrossRef PubMed Google Scholar

[52] Kapila J., De Rycke R., Van Montagu M., Angenon G.. An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci, 1997, 122: 101-108 CrossRef Google Scholar

[53] Kelley M.L., Strezoska , He K., Vermeulen A., Smith A.B.. Versatility of chemically synthesized guide RNAs for CRISPR-Cas9 genome editing. J Biotech, 2016, 233: 74-83 CrossRef PubMed Google Scholar

[54] Kumagai M.H., Donson J., della-Cioppa G., Harvey D., Hanley K., Grill L.K.. Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc Natl Acad Sci USA, 1995, 92: 1679-1683 CrossRef ADS Google Scholar

[55] Lawrenson T., Shorinola O., Stacey N., Li C., Østergaard L., Patron N., Uauy C., Harwood W.. Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol, 2015, 16: 258 CrossRef PubMed Google Scholar

[56] Li J.F., Norville J.E., Aach J., McCormack M., Zhang D., Bush J., Church G.M., Sheen J.. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol, 2013, 31: 688-691 CrossRef PubMed Google Scholar

[57] Li J., Stoddard T.J., Demorest Z.L., Lavoie P.O., Luo S., Clasen B.M., Cedrone F., Ray E.E., Coffman A.P., Daulhac A., Yabandith A., Retterath A.J., Mathis L., Voytas D.F., D’Aoust M.A., Zhang F.. Multiplexed, targeted gene editing in Nicotiana benthamiana for glyco-engineering and monoclonal antibody production. Plant Biotechnol J, 2016, 14: 533-542 CrossRef PubMed Google Scholar

[58] Li T., Liu B., Spalding M.H., Weeks D.P., Yang B.. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol, 2012, 30: 390-392 CrossRef PubMed Google Scholar

[59] Li T., Liu B., Chen C.Y., Yang B.. TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J Genet Genomics, 2016, 43: 297-305 CrossRef PubMed Google Scholar

[60] Li Z., Liu Z.B., Xing A., Moon B.P., Koellhoffer J.P., Huang L., Ward R.T., Clifton E., Falco S.C., Cigan A.M.. Cas9-guide RNA directed genome editing in soybean. Plant Physiol, 2015, 169: 960-970 CrossRef PubMed Google Scholar

[61] Liang Z., Zhang K., Chen K., Gao C.. Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genomics, 2014, 41: 63-68 CrossRef PubMed Google Scholar

[62] Liang Z., Chen K., Li T., Zhang Y., Wang Y., Zhao Q., Liu J., Zhang H., Liu C., Ran Y., Gao C.. Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun, 2017, 8: 14261 CrossRef PubMed ADS Google Scholar

[63] Lloyd A., Plaisier C.L., Carroll D., Drews G.N.. Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci USA, 2005, 102: 2232-2237 CrossRef PubMed ADS Google Scholar

[64] Lor V.S., Starker C.G., Voytas D.F., Weiss D., Olszewski N.E.. Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol, 2014, 166: 1288-1291 CrossRef PubMed Google Scholar

[65] Lowe K., Wu E., Wang N., Hoerster G., Hastings C., Cho M.J., Scelonge C., Lenderts B., Chamberlin M., Cushatt J., Wang L., Ryan L., Khan T., Chow-Yiu J., Hua W., Yu M., Banh J., Bao Z., Brink K., Igo E., Rudrappa B., Shamseer P.M., Bruce W., Newman L., Shen B., Zheng P., Bidney D., Falco S.C., RegisterIII J.C., Zhao Z.Y., Xu D., Jones T.J., Gordon-Kamm W.J.. Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell, 2016, 28: 1998-2015 CrossRef PubMed Google Scholar

[66] Luo S., Li J., Stoddard T.J., Baltes N.J., Demorest Z.L., Clasen B.M., Coffman A., Retterath A., Mathis L., Voytas D.F., Zhang F.. Non-transgenic plant genome editing using purified sequence-specific nucleases. Mol Plant, 2015, 8: 1425-1427 CrossRef PubMed Google Scholar

[67] Ma X., Zhang Q., Zhu Q., Liu W., Chen Y., Qiu R., Wang B., Yang Z., Li H., Lin Y., Xie Y., Shen R., Chen S., Wang Z., Chen Y., Guo J., Chen L., Zhao X., Dong Z., Liu Y.G.. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicotplants. Mol Plant, 2015, 8: 1274-1284 CrossRef PubMed Google Scholar

[68] Mahfouz M.M., Li L., Shamimuzzaman M., Wibowo A., Fang X., Zhu J.K.. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci USA, 2011, 108: 2623-2628 CrossRef PubMed ADS Google Scholar

[69] Malnoy M., Viola R., Jung M.H., Koo O.J., Kim S., Kim J.S., Velasco R., Nagamangala Kanchiswamy C.. DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci, 2016, 7: 1904 CrossRef PubMed Google Scholar

[70] Mao Y., Zhang H., Xu N., Zhang B., Gou F., Zhu J.K.. Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant, 2013, 6: 2008-2011 CrossRef PubMed Google Scholar

[71] Martin-Ortigosa S., Valenstein J.S., Lin V.S.Y., Trewyn B.G., Wang K.. Gold functionalized mesoporous silica nanoparticle mediated protein and DNA codelivery to plant cells via the biolistic method. Adv Funct Mater, 2012, 22: 3576-3582 CrossRef Google Scholar

[72] Martin-Ortigosa S., Peterson D.J., Valenstein J.S., Lin V.S.Y., Trewyn B.G., Lyznik L.A., Wang K.. Mesoporous silica nanoparticle-mediated intracellular Cre protein delivery for maize genome editing via loxP site excision. Plant Physiol, 2014, 164: 537-547 CrossRef PubMed Google Scholar

[73] Marton I., Zuker A., Shklarman E., Zeevi V., Tovkach A., Roffe S., Ovadis M., Tzfira T., Vainstein A.. Nontransgenic genome modification in plant cells. Plant Physiol, 2010, 154: 1079-1087 CrossRef PubMed Google Scholar

[74] Miao J., Guo D., Zhang J., Huang Q., Qin G., Zhang X., Wan J., Gu H., Qu L.J.. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res, 2013, 23: 1233-1236 CrossRef PubMed Google Scholar

[75] Mikami M., Toki S., Endo M.. Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice. Plant Mol Biol, 2015, 88: 561-572 CrossRef PubMed Google Scholar

[76] Mikami M., Toki S., Endo M.. Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant Cell Physiol, 2016, 57: 1058-1068 CrossRef PubMed Google Scholar

[77] Nekrasov V., Staskawicz B., Weigel D., Jones J.D.G., Kamoun S.. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol, 2013, 31: 691-693 CrossRef PubMed Google Scholar

[78] Nicolia A., Proux-Wéra E., Åhman I., Onkokesung N., Andersson M., Andreasson E., Zhu L.H.. Targeted gene mutation in tetraploid potato through transient TALEN expression in protoplasts. J Biotech, 2015, 204: 17-24 CrossRef PubMed Google Scholar

[79] Okuzaki A., Toriyama K.. Chimeric RNA/DNA oligonucleotide-directed gene targeting in rice. Plant Cell Rep, 2004, 22: 509-512 CrossRef PubMed Google Scholar

[80] Osakabe K., Osakabe Y., Toki S.. Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc Natl Acad Sci USA, 2010, 107: 12034-12039 CrossRef PubMed ADS Google Scholar

[81] Paul J.W., Qi Y.. CRISPR/Cas9 for plant genome editing: accomplishments, problems and prospects. Plant Cell Rep, 2016, 35: 1417-1427 CrossRef PubMed Google Scholar

[82] Peer R., Rivlin G., Golobovitch S., Lapidot M., Gal-On A., Vainstein A., Tzfira T., Flaishman M.A.. Targeted mutagenesis using zinc-finger nucleases in perennial fruit trees. Planta, 2015, 241: 941-951 CrossRef PubMed Google Scholar

[83] Petolino J.F.. Genome editing in plants via designed zinc finger nucleases. Cell Dev Biol-Plant, 2015, 51: 1-8 CrossRef PubMed Google Scholar

[84] Piatek A., Ali Z., Baazim H., Li L., Abulfaraj A., Al-Shareef S., Aouida M., Mahfouz M.M.. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J, 2015, 13: 578-589 CrossRef PubMed Google Scholar

[85] Popat A., Hartono S.B., Stahr F., Liu J., Qiao S.Z., Qing (Max) Lu G.. Mesoporous silica nanoparticles for bioadsorption, enzyme immobilisation, and delivery carriers. Nanoscale, 2011, 3: 2801-2818 CrossRef PubMed ADS Google Scholar

[86] Pratt, S. Growers to see new HT canola in 2016. The Western Producer. 2012-05-28. http://www.producer.com/2014/03/growers-to-see-new-ht-canola-in-2016/. Google Scholar

[87] Qi Y., Zhang Y., Zhang F., Baller J.A., Cleland S.C., Ryu Y., Starker C.G., Voytas D.F.. Increasing frequencies of site-specific mutagenesis and gene targeting in Arabidopsis by manipulating DNA repair pathways. Genome Res, 2013a, 23: 547-554 CrossRef PubMed Google Scholar

[88] Qi Y., Li X., Zhang Y., Starker C.G., Baltes N.J., Zhang F., Sander J.D., Reyon D., Joung J.K., Voytas D.F.. Targeted deletion and inversion of tandemly arrayed genes in Arabidopsis thaliana using zinc finger nucleases. G3, 2013b, 3: 1707-1715 CrossRef PubMed Google Scholar

[89] Raitskin O., Patron N.J.. Multi-gene engineering in plants with RNA-guided Cas9 nuclease. Curr Opin Biotech, 2016, 37: 69-75 CrossRef PubMed Google Scholar

[90] Rakoczy-Trojanowska, M. (2002). Alternative methods of plant transformation: a short review. Cell Mol Biol Lett 7, 849–858. Google Scholar

[91] Ren C., Liu X., Zhang Z., Wang Y., Duan W., Li S., Liang Z.. CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.). Sci Rep, 2016, 6: 32289 CrossRef PubMed ADS Google Scholar

[92] Rinaldo A.R., Ayliffe M.. Gene targeting and editing in crop plants: a new era of precision opportunities. Mol Breeding, 2015, 35: 40 CrossRef Google Scholar

[93] Sauer N.J., Narváez-Vásquez J., Mozoruk J., Miller R.B., Warburg Z.J., Woodward M.J., Mihiret Y.A., Lincoln T.A., Segami R.E., Sanders S.L., Walker K.A., Beetham P.R., Schöpke C.R., Gocal G.F.W.. Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol, 2016, 170: 1917-1928 CrossRef PubMed Google Scholar

[94] Schaeffer S.M., Nakata P.A.. CRISPR/Cas9-mediated genome editing and gene replacement in plants: transitioning from lab to field. Plant Sci, 2015, 240: 130-142 CrossRef PubMed Google Scholar

[95] Schiml S., Fauser F., Puchta H.. The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J, 2014, 80: 1139-1150 CrossRef PubMed Google Scholar

[96] Shan Q., Wang Y., Chen K., Liang Z., Li J., Zhang Y., Zhang K., Liu J., Voytas D.F., Zheng X., Zhang Y., Gao C.. Rapid and efficient gene modification in rice and Brachypodium using TALENs. Mol Plant, 2013a, 6: 1365-1368 CrossRef PubMed Google Scholar

[97] Shan Q., Wang Y., Li J., Zhang Y., Chen K., Liang Z., Zhang K., Liu J., Xi J.J., Qiu J.L., Gao C.. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol, 2013b, 31: 686-688 CrossRef PubMed Google Scholar

[98] Shan Q., Zhang Y., Chen K., Zhang K., Gao C.. Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J, 2015, 13: 791-800 CrossRef PubMed Google Scholar

[99] Shi J., Gao H., Wang H., Lafitte H.R., Archibald R.L., Yang M., Hakimi S.M., Mo H., Habben J.E.. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J, 2017, 15: 207-216 CrossRef PubMed Google Scholar

[100] Shukla V.K., Doyon Y., Miller J.C., DeKelver R.C., Moehle E.A., Worden S.E., Mitchell J.C., Arnold N.L., Gopalan S., Meng X., Choi V.M., Rock J.M., Wu Y.Y., Katibah G.E., Zhifang G., McCaskill D., Simpson M.A., Blakeslee B., Greenwalt S.A., Butler H.J., Hinkley S.J., Zhang L., Rebar E.J., Gregory P.D., Urnov F.D.. Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature, 2009, 459: 437-441 CrossRef PubMed ADS Google Scholar

[101] Stoddard T.J., Clasen B.M., Baltes N.J., Demorest Z.L., Voytas D.F., Zhang F., Luo S.. Targeted mutagenesis in plant cells through transformation of sequence-specific nuclease mRNA. PLoS ONE, 2016, 11: e0154634 CrossRef PubMed ADS Google Scholar

[102] Sugano S.S., Shirakawa M., Takagi J., Matsuda Y., Shimada T., Hara-Nishimura I., Kohchi T.. CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L.. Plant Cell Physiol, 2014, 55: 475-481 CrossRef PubMed Google Scholar

[103] Sun X., Hu Z., Chen R., Jiang Q., Song G., Zhang H., Xi Y.. Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci Rep, 2015, 5: 10342 CrossRef PubMed ADS Google Scholar

[104] Svitashev S., Young J.K., Schwartz C., Gao H., Falco S.C., Cigan A.M.. Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol, 2015, 169: 931-945 CrossRef PubMed Google Scholar

[105] Svitashev S., Schwartz C., Lenderts B., Young J.K., Mark Cigan A.. Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat Commun, 2016, 7: 13274 CrossRef PubMed ADS Google Scholar

[106] Torney F., Trewyn B.G., Lin V.S.Y., Wang K.. Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotech, 2007, 2: 295-300 CrossRef PubMed ADS Google Scholar

[107] Tovkach A., Zeevi V., Tzfira T.. A toolbox and procedural notes for characterizing novel zinc finger nucleases for genome editing in plant cells. Plant J, 2009, 57: 747-757 CrossRef PubMed Google Scholar

[108] Townsend J.A., Wright D.A., Winfrey R.J., Fu F., Maeder M.L., Joung J.K., Voytas D.F.. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature, 2009, 459: 442-445 CrossRef PubMed ADS Google Scholar

[109] Upadhyay S.K., Kumar J., Alok A., Tuli R.. RNA-guided genome editing for target gene mutations in wheat. G3, 2013, 3: 2233-2238 CrossRef PubMed Google Scholar

[110] Vainstein A., Marton I., Zuker A., Danziger M., Tzfira T.. Permanent genome modifications in plant cells by transient viral vectors. Trends Biotech, 2011, 29: 363-369 CrossRef PubMed Google Scholar

[111] Voytas D.F., Gao C.. Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol, 2014, 12: e1001877 CrossRef PubMed Google Scholar

[112] Wang S., Zhang S., Wang W., Xiong X., Meng F., Cui X.. Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Rep, 2015, 34: 1473-1476 CrossRef PubMed Google Scholar

[113] Wang L., Li F., Dang L., Liang C., Wang C., He B., Liu J., Li D., Wu X., Xu X., Lu A., Zhang G.. In vivo delivery systems for therapeutic genome editing. Int J Mol Sci, 2016, 17: 626 CrossRef PubMed Google Scholar

[114] Wang M., Liu Y., Zhang C., Liu J., Liu X., Wang L., Wang W., Chen H., Wei C., Ye X., Li X., Tu J.. Gene editing by co-transformation of TALEN and chimeric RNA/DNA oligonucleotides on the rice OsEPSPS gene and the inheritance of mutations. PLoS ONE, 2015, 10: e0122755 CrossRef PubMed ADS Google Scholar

[115] Wang Y., Cheng X., Shan Q., Zhang Y., Liu J., Gao C., Qiu J.L.. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol, 2014, 32: 947-951 CrossRef PubMed Google Scholar

[116] Wang Z.P., Xing H.L., Dong L., Zhang H.Y., Han C.Y., Wang X.C., Chen Q.J.. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol, 2015, 16: 144 CrossRef PubMed Google Scholar

[117] Weeks D.P., Spalding M.H., Yang B.. Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J, 2016, 14: 483-495 CrossRef PubMed Google Scholar

[118] Wendt T., Holm P.B., Starker C.G., Christian M., Voytas D.F., Brinch-Pedersen H., Holme I.B.. TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol, 2013, 83: 279-285 CrossRef PubMed Google Scholar

[119] Weinthal D., Tovkach A., Zeevi V., Tzfira T.. Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci, 2010, 15: 308-321 CrossRef PubMed Google Scholar

[120] Woo J.W., Kim J., Kwon S.I., Corvalán C., Cho S.W., Kim H., Kim S.G., Kim S.T., Choe S., Kim J.S.. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol, 2015, 33: 1162-1164 CrossRef PubMed Google Scholar

[121] Wright D.A., Townsend J.A., Winfrey Jr R.J., Irwin P.A., Rajagopal J., Lonosky P.M., Hall B.D., Jondle M.D., Voytas D.F.. High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J, 2005, 44: 693-705 CrossRef PubMed Google Scholar

[122] Xie K., Yang Y.. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant, 2013, 6: 1975-1983 CrossRef PubMed Google Scholar

[123] Xie K., Minkenberg B., Yang Y.. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci USA, 2015, 112: 3570-3575 CrossRef PubMed ADS Google Scholar

[124] Xing H.L., Dong L., Wang Z.P., Zhang H.Y., Han C.Y., Liu B., Wang X.C., Chen Q.J.. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol, 2014, 14: 327 CrossRef PubMed Google Scholar

[125] Xu R., Li H., Qin R., Wang L., Li L., Wei P., Yang J.. Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice, 2014, 7: 5 CrossRef PubMed Google Scholar

[126] Yan L., Wei S., Wu Y., Hu R., Li H., Yang W., Xie Q.. High-efficiency genome editing in Arabidopsis using YAO promoter-driven CRISPR/Cas9 system. Mol Plant, 2015, 8: 1820-1823 CrossRef PubMed Google Scholar

[127] Yin K., Han T., Liu G., Chen T., Wang Y., Yu A.Y.L., Liu Y.. A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Sci Rep, 2015, 5: 14926 CrossRef PubMed ADS Google Scholar

[128] Yoon K., Cole-Strauss A., Kmiec E.B.. Targeted gene correction of episomal DNA in mammalian cells mediated by a chimeric RNA.DNA oligonucleotide. Proc Natl Acad Sci USA, 1996, 93: 2071-2076 CrossRef Google Scholar

[129] Zhang F., Maeder M.L., Unger-Wallace E., Hoshaw J.P., Reyon D., Christian M., Li X., Pierick C.J., Dobbs D., Peterson T., Joung J.K., Voytas D.F.. High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci USA, 2010, 107: 12028-12033 CrossRef PubMed ADS Google Scholar

[130] Zhang H., Zhang J., Wei P., Zhang B., Gou F., Feng Z., Mao Y., Yang L., Zhang H., Xu N., Zhu J.K.. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J, 2014, 12: 797-807 CrossRef PubMed Google Scholar

[131] Zhang H., Gou F., Zhang J., Liu W., Li Q., Mao Y., Botella J.R., Zhu J.K.. TALEN-mediated targeted mutagenesis produces a large variety of heritable mutations in rice. Plant Biotechnol J, 2016, 14: 186-194 CrossRef PubMed Google Scholar

[132] Zhang Y., Zhang F., Li X., Baller J.A., Qi Y., Starker C.G., Bogdanove A.J., Voytas D.F.. Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol, 2013, 161: 20-27 CrossRef PubMed Google Scholar

[133] Zhang Y., Liang Z., Zong Y., Wang Y., Liu J., Chen K., Qiu J.L., Gao C.. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun, 2016, 7: 12617 CrossRef PubMed ADS Google Scholar

[134] Zhou H., Liu B., Weeks D.P., Spalding M.H., Yang B.. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res, 2014, 42: 10903-10914 CrossRef PubMed Google Scholar

[135] Zhu T., Peterson D.J., Tagliani L., St. Clair G., Baszczynski C.L., Bowen B.. Targeted manipulation of maize genes in vivo using chimeric RNA/DNA oligonucleotides. Proc Natl Acad Sci USA, 1999, 96: 8768-8773 CrossRef Google Scholar

[136] Zhu T., Mettenburg K., Peterson D.J., Tagliani L., Baszczynski C.L.. Engineering herbicide-resistant maize using chimeric RNA/DNA oligonucleotides. Nat Biotechnol, 2000, 18: 555-558 CrossRef PubMed Google Scholar

  • Figure 1

    General procedure for genome editing in plants.

  • Figure 2

    Construct design for ZFNs, TALENs and CRISPR/Cas9 when Agrobacterium is used as the delivery method.

  • Table 1   Summary of reports of plant genome editing using ZFNs, TALENs and Crispr/Cas9 technology

    Plant species/Editor/Targeted gene(s)

    Targeted outcome

    Delivery method for transient assay or stable edited cells

    Delivery method for stable events

    Reference

    At/C/PDS3, FLS2, RACK1b, 1c

    Deletion, replacement and insertion (Multiplex)

    Protoplast transfection, Agroinfiltration

    Li et al., 2013

    At/C/-GFP

    Deletion and insertion

    Agroinfiltration

    Jiang et al., 2013

    At/C/-GFP

    Deletion and insertion

    Floral dipping

    Jiang et al., 2014

    At/C/-BRI1, JAZ1, GAI, YFP

    Deletion and insertion

    Protoplast transfection

    A. tumefaciens

    Feng et al., 2013

    At/C/-BRI1, JAZ1, GAI, CHL1, AP1, TT4, GUUS

    Deletion and insertion

    A. tumefaciens

    Feng et al., 2014

    At/C/-CHL1, CHL2, TT4i

    Deletion, replacement (HDR, NHEJ) and insertion (Multiplex)

    Protoplast transfection

    A. tumefaciens

    Mao et al., 2013

    At/C/-ADH1

    Replacement (HDR)

    Floral dipping

    Schiml et al., 2014

    At/C/-TRY, CPC, ETC2

    Deletion and insertion

    Floral dipping

    Xing et al., 2014

    At/C/-5g55580 with 3 targets sets

    Deletion and insertion

    Floral dipping

    Ma et al., 2015

    At/C/-ADH1, TT4, RTEL1, Guus

    Deletion and insertion. (HR-GUS gene)

    Floral dipping

    Fauser et al., 2014

    At/C/-ETC2, TRY, CPC

    Deletion and insertion (Multiplex)

    Floral dipping

    Wang et al., 2015

    At/C/-BRI1

    Deletion and insertion

    Floral dipping

    Yan et al., 2015

    Nb/C/-PDS3

    Deletion, replacement (HDR, NHEJ) and insertion

    Protoplast transfection, Agroinfiltration

    Li et al., 2013

    Nb/C/-PDS

    Deletion

    Agroinfiltration

    Belhaj et al., 2013

    Nb/C/-PDS

    Deletion

    Agroinfiltration

    A. tumefaciens

    Nekrasov et al., 2013

    Nb/C/-PDS

    Deletion

    Agroinfiltration

    Upadhyay et al., 2013

    Nb/C/-Transcriptional activation-EDLL domain, dHax3 TAD of phytopathogenic Xanthomonas spp. Repression-SRDX repression domain

    Regulation

    Agroinfiltration

    Piatek et al., 2015

    Nb/C/-PCNA, PDS

    Deletion and insertion

    TRV-mediated transformation

    Ali et al., 2015

    GFP

    Deletion and insertion (NHEJ)

    Agroinfiltration

    Jiang et al., 2013

    Nb/C/-PDS, IspH, fsGUS

    Deletion and insertion

    Agro-geminivirus

    Yin et al., 2015

    Nt/C/-PDS, PDR6

    Deletion and insertion

    Protoplast transfection

    Gao et al., 2015

    Nt/C/-SurA, SurB

    Deletion and insertion

    Agro-geminivirus

    Baltes et al., 2014

    Os/C/-ROC5, SPP, YSA

    Deletion and insertion

    A. tumefaciens

    Feng et al., 2013

    Os/C/-SWEET11, SWEET14, dsRED

    Deletion and insertion (NHEJ)

    Protoplast transfection

    Jiang et al., 2013

    Os/C/-NbPDS

    Deletion and insertion

    Agoinfiltration

    Belhaj et al., 2013

    Os/C/-PDS-SP1, BADH2, 02g23823, MPK2

    Deletion, replacement (HDR, NHEJ) and insertion

    Protoplast transfection

    Biolistic delivery

    Shan et al., 2013b

    Os/C/-MYB1

    Deletion and insertion

    Protoplast transfection

    A. tumefaciens

    Mao et al., 2013

    Os/C/-MPK5

    Deletion and insertion

    Protoplast transfection

    Xie and Yang, 2013

    Os/C/-CAO, LAZY1

    Deletion

    A. tumefaciens

    Miao et al., 2013

    Os/C/-PTG1, 2, 3, 4, 5, 6, 7, 8, 9

    Deletion and insertion

    (individual and multiplex)

    A. tumefaciens

    Xie et al., 2015

    Os/C/-BEL

    Replacement

    A. tumefaciens

    Xu et al., 2014

    Os/C/-11 FTL genes, GSTU, MRP15, AnP Waxy

    Deletion, substitution (HDR, NHEJ) and insertion

    A. tumefaciens

    Ma et al., 2015

    Os/C/-SWEET1a, 1b, 11 and 13; P450; 10 diterpenoid genes

    Deletion and insertion -large deletion (245 kb)

    Protoplast transfection

    A. tumefaciens

    Zhou et al., 2014

    Os/C/-PDS, PMS3, EPSPS, DERF1, MSH1, MYB5, MYB1, ROC5, SPP, YSA

    Deletion, substitution (HDR, NHEJ) and insertion

    A. tumefaciens

    Zhang et al., 2014

    (To be continued on the next page)

    (Continued)

    Plant species/Editor/Targeted gene(s)

    Targeted outcome

    Delivery method for transient assay or stable edited cells

    Delivery method for stable events

    Reference

    Pre-integrated DsRED

    Deletion and insertion

    A. tumefaciens

    Mikami et al., 2015

    Os/C/-DMC1A

    Deletion and insertion

    Mikami et al., 2016

    Ta/C/-MLO

    Deletion and insertion (NHEJ)

    Protoplast transfection

    Shan et al., 2013b; Wang et al., 2014

    Ta/C/-GW2(RNP)

    Deletion and insertion

    Protoplast transfection

    Biolistic delivery

    Liang et al., 2017

    Ta/C/Inox, PDS

    Deletion

    Agroinfiltration

    Upadhyay et al., 2013

    Hv/C/-PM19

    Deletion and replacement

    A. tumefaciens

    Lawrenson et al., 2015

    Ds/C/-RED2

    Deletion and insertion

    A. tumefaciens

    Jiang et al., 2013

    Mp/C/-ARF1

    Deletion

    A. tumefaciens

    Sugano et al., 2014

    Zm/C/-IPK

    Deletion and insertion

    Protoplast transfection

    Liang et al., 2014

    Zm/C/-HKT1

    Deletion and insertion (multiplex)

    Protoplast transfection

    A. tumefaciens

    Xing et al., 2014

    Zm/C/LIG1, MS26, MS45, ALS1, ALS2

    Deletion, replacement and gene insertion

    Biolistic delivery

    Svitashev et al., 2015

    Zm/C/-LIG, MS26, MS45, ALS2

    Deletion and insertion

    Biolistic delivery

    Svitashev et al., 2016

    Zm/C/-ARGOS8

    Deletion , insertion and swap

    Biolistic delivery

    Shi et al., 2017

    Gm/C/-preintegrated gfp5a’, gfp3a’ 07g14530, 01gDDM1, 11gDDM1, 01g+11gDDM1-Chr-1,01g+11gDDM1-Chr11, Met1-04g, Met1-06g, miR1514, miR1509

    Deletion, insertion and replacement

    A. rhizogenes

    Jacobs et al., 2015

    Gm/C/-DD20, DD43, ALS1

    Deletion, insertion, replacement (HDR) and editing

    Biolistic delivery

    Li et al., 2015

    Gm/C/-06g14180, 08g02290, Glyma12g37050

    Deletion and insertion

    A. rhizogenes

    Sun et al., 2015

    Gm/C/-Transgene BAR, FEI, FEI2, SHR

    Deletion and insertion

    A. rhizogenes

    Cai et al., 2015

    Gm/C/-PDS11, GlymaPDS18

    Deletion and insertion

    A. rhizogenes

    A. tumefaciens

    Du et al., 2016

    Cs/C/PDS

    Deletion and replacement

    Agroinfiltration

    Jia and Wang, 2014a

    Cp/C/CsPDS

    Deletion and replacement

    Agroinfiltration

    A. tumefaciens

    Jia and Wang, 2014b

    Cp/C/CsLOB1 promoter

    Regulation

    Jia et al., 2016

    Sl/C/-AGO7

    Deletion and replacement

    A. tumefaciens

    Brooks et al., 2014

    Sl/C/-Ant1

    Insertion

    Agro-germinivirus

    Čermák et al., 2015

    Sl/C/-RIN

    Deletion and insertion

    A. tumefaciens

    Ito et al., 2015

    St/C/-IAA2

    Deletion and replacement

    A. tumefaciens

    Wang et al., 2015

    St/C/-ALS1

    Deletion and insertion

    A. tumefaciens

    Butler et al., 2015

    St/C/-GBSS

    Deletion and insertion

    Potoplast transfection

    Andersson et al., 2017

    Pt/C/-PDS

    Deletion and replacement

    A. tumefaciens

    Fan et al., 2015

    Bo/C/-C.GA4.a

    Deletion and replacement

    A. tumefaciens

    Lawrenson et al., 2015

    Ps/C/-4OMT2

    Deletion

    Agroinfiltration

    TRV-mediated

    Alagoz et al., 2016

    Cs/C/-eIF4E

    Deletion and insertion

    A. tumefaciens

    Chandrasekaran et al., 2016

    Vv/C/-IdnDH

    Deletion and insertion

    A. tumefaciens

    Ren et al., 2016

    Vv/C/-MLO-7

    Deletion and insertion

    Protoplast transfection

    Malnoy et al., 2016

    Md/C/-DIPM-1, DIPM-2, DIPM-4

    Deletion and insertion

    Protoplast transfection

    Malnoy et al., 2016

    At/Z/-Pre-integrated QQR

    Deletion and insertion

    Floral dipping

    Lloyd et al., 2005

    At/Z/-Incomplete GUS gene

    Deletion and insertion

    A. tumefaciens

    Tovkach et al., 2009

    (To be continued on the next page)

    At/C/-ADH1, TT4

    Deletion and insertion

    Protoplast transfection

    Floral dipping

    Zhang et al., 2010

    At/Z/-ABI4

    Deletion and substitution

    Floral dipping

    Osakabe et al., 2010

    At/Z/-Pre-integrated target sequence

    Deletion and insertion

    Floral dipping

    de Pater et al., 2009

    At/Z/-PPO

    Replacement (HDR)

    Floral dipping

    de Pater et al., 2013

    At/Z/-Pre-integrated GUS gene

    Deletions and substitutions

    viral vectors

    Vainstein et al., 2011

    At/Z/-Pre-integrated GFP

    Replacement with hph (HDR)

    A. tumefaciens

    Weinthal et al., 2010

    At/Z/-ADH1

    Replacement (HDR) (in the absence of

    DNA repair proteins KU70 and LIG4)

    Floral dipping

    Qi et al., 2013a

    At/Z/-3 RLK gene clusters, 1 large R gene cluster

    Deletion, inversion and duplications

    Floral dipping

    Qi et al., 2013b

    At/Z/-ADH1

    Replacement

    Biolistic delivery -geminivirus

    Baltes et al., 2014

    Petunia/Z/-Pre-integrated target GUS sequence

    Deletion and insertion

    A. tumefaciens

    Marton et al., 2010

    Gm/Z/-DCL1(DCL1a/DCL1b), DCL4 (DCL4a/DCL4b), DCL2a, DCL2b, RDR6a, RDR6b, HEN1a

    Deletion and insertion

    A. rhizogenes

    A.rhizogenes

    Curtin et al., 2011

    Nt/Z/-gus:nptII

    Replacement (HDR)

    Agro-geminivirus

    Baltes et al., 2014

    Nb/Z/-NtSuR, NtSuRB

    Deletion, replacement (HDR, NHEJ) and insertion

    Protoplast electroporation

    Townsend et al., 2009

    Nb/Z/-Preintegrated GUS:NPTII

    Replacement (HDR)

    Protoplast electroporation

    Wright et al., 2005

    Nb/Z/-Pre-integrated target sequence GFP

    Replacement (HDR)

    A. tumefaciens

    Cai et al., 2009

    Nt/Z/-CHN50

    Insertion of PAT gene

    A. tumefaciens

    Cai et al., 2009

    Nb/Z/-GFP and GUS

    Deletion and replacement (editing)

    Agro-geminivirus

    Agro-geminivirus

    Baltes et al., 2014

    Nb/Z/-Pre-integrated target sequence GFP

    Replacement with hph (HDR)

    A. tumefaciens

    Weinthal et al., 2010

    Nb/Z/-Pre-integrated target GUS sequence

    Deletion and insertion

    A. tumefaciens

    Marton et al., 2010

    Nb/Z/-Incomplete GUS gene

    Deletion and insertion

    A. tumefaciens

    Tovkach et al., 2009

    Zm/Z/-IPK

    Replacement and gene insertion (HDR)

    WHISKERSTM

    Shukla et al., 2009

    Zm/Z/-Pre-integrated target sequence PAT

    AAD1 gene insertion

    Biolistic method

    Ainley et al., 2013

    Bn/Z/-A ZFP-TF for KASII expression

    Gene regulation

    A. tumefaciens

    Gupta et al., 2012

    Md/Z/-Pre-integrated target sequence QQR–ZFN

    Deletion and insertion

    Agroinfiltration

    A. tumefaciens

    Peer et al., 2015

    Fc/Z/-Pre-integrated target sequence QQR–ZFN

    Deletion and insertion

    Agroinfiltration

    A. tumefaciens

    Peer et al., 2015

    At/T/-CLV3

    Deletion and insertion

    Floral dipping

    Forner et al., 2015

    Nt/T/-ALS (SurA, and SurB)

    Deletion, insertion and replacement (HDR)

    Protoplast transfection

    Zhang et al., 2013

    Nt/T/-SurA and SurB

    Deletion or insertion

    Agro-geminivirus

    Baltes et al., 2014

    Nb/T/-Effector binding element (EBE)

    Deletion or insertion

    A. tumefaciens

    Mahfouz et al., 2011

    Nb/T/-ALS

    Deletion

    Agro-geminivirus

    Baltes et al., 2014

    (To be continued on the next page)

    Nb/T/-ALS2

    Deletion

    Protoplast transfection-mRNA

    Stoddard et al., 2016

    Nb/T/-FucT and XylT

    Multiple deletion

    Protoplast transfection

    Li et al., 2016

    Os/T/-EPSPS

    Deletion and substitution

    Biolistic transformation

    Wang et al., 2015

    Os/T/-11N3 (also called SWEET14)

    Deletion and insertion

    A. tumefaciens

    Li et al., 2012

    Os/T/-DEP1, BADH2, CKX2, SD1

    Deletion, substitution and insertion

    Protoplast transfection

    Biolistic delivery

    Shan et al., 2013a

    Os/T/-BADH2, CKX2, DEP1

    Deletion and insertion

    A. tumefaciens

    Shan et al., 2015

    Os/T/-ALS

    Homologous recombination

    Biolistic delivery

    Li et al., 2016

    Os/T/-CSA, PMS3, DERF1, GN1a, TAD1, MST7, MST8

    Deletion, substitution and insertion

    A. tumefaciens

    Zhang et al., 2016

    Bd/T/-ABA1, CKX2, SMC6, SPL, SBP, COI, RHT, HTA1

    Deletion, substitution and insertion

    Protoplast transfection

    Biolistic delivery

    Shan et al., 2013a

    Hv/T/-Promoter of HvPAPhy_a

    Deletion

    A. tumefaciens

    Wendt et al., 2013

    Hv/T/-Pre-integrated target sequence GFP

    Deletion and insertion

    A. tumefaciens (Pollen)

    Gurushidze et al., 2014

    Ta/T/-MLO

    Deletion and insertion

    Protoplast transfection

    Biolistic delivery

    Wang et al., 2014

    Zm/T/PDS, IPK1A, IPK, MRP4

    Deletion

    Protoplast transfection

    A. tumefaciens

    Liang et al., 2014

    Zm/T/-glossy2

    Deletion

    Biolistic delivery

    A. tumefaciens

    Char et al., 2015

    Gm/T/-FAD2-1A, FAD2-1B

    Deletion and insertion

    A. rhizogenes

    A. rhizogenes

    Haun et al., 2014

    Gm/T/-PDS11, PDS18

    Deletion and insertion

    A. rhizogenes

    A. tumefaciens

    Du et al., 2016

    Sl/T/-PRO

    Deletion and insertion

    A. tumefaciens

    Lor et al., 2014

    Sl/T/-Ant1

    Insertion

    Agro-germinivirus

    Čermák et al., 2015

    St/T/-VInv

    Deletion and insertion

    Protoplast transfection

    Protoplast transfection

    Clasen et al., 2016

    St/T/-ALS

    Deletion and insertion

    Protoplast transfection

    Protoplast transfection

    Nicolia et al., 2015

    St/T/-Ubi7

    Insertion of a herbicide resisitsnt gene ASL

    Agroinfiltration

    A. tumefaciens

    Forsyth et al., 2016

    Ss/T/-COMT

    Deletion and insertion

    A. tumefaciens

    Jung and Altpeter, 2016

    At, A. thaliana (Arabidopsis); Nt, N. benthamiana; Nc, N. tobaccum (Tobacco); Os, O. sativa (Rice); Hv, H. vulgare (barley); Sb, S. bicolor (sorghum); Mp, M. polymorphal (liverwort); Zm, Z. mays (maize); Gm, G. max (soybean); Cs, C. sinensis (sweet orange); Cp, C. paradisi (grapefruit); Sl, S. lycopersicum (tomato); St, S. tuberosum (potato); Pt, P. tomentosa (populous); Bo, B. oleracea (oil rape); Ps, P. somniferum (opium poppy); Ca, C. sativus (cucumber); Vv, V. vinifera (grape); Md, M. domestica (Apple); Bn, B. napus (canola); Fc, F. carica (Fig), Bd, Brachypodium distachyon; Ss, Saccharum spp. Hybrids (sugarcane); C, Crispr/CAS 9; Z, Zinc-finger nucleases; T, Talen; Agro-germinivirus, Agrobacterium-mediated germinivirus delivery.

Copyright 2019 Science China Press Co., Ltd. 《中国科学》杂志社有限责任公司 版权所有

京ICP备18024590号-1