Skip to main content
Log in

Genome editing for targeted improvement of plants

  • Review Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Recent advances in gene/genome editing technologies, such as engineered meganucleases (EMNs), zinc finger nucleases (ZFNs), transcription activator-like effector nuclease (TALENs) and clustered regularly interspaced palindromic repeats (CRISPR/Cas9) allowed researchers to precisely modify or mutate genes. These genome editing tools make double-strand breaks (DSB) in DNA and then repair it by employing error-prone non-homologous end joining (NHEJ) or homology directed repair (HDR) mechanism which leads to mutation in specific location in genome. Since these editing techniques are simple to use, highly efficient and specific as compared to earlier mutation methods, their use in plant biology research is increasing rapidly to enhance biotic and abiotic stress tolerance, increased nutritional value and new trait development. Here, we review the applications of EMNs, ZFNs, TALENs and CRISPR/Cas9 in various plants (cereals, vegetable, oil crops and fruits), comparison of genome editing methods and their biosafety regulations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ainley WM, Sastry-Dent L, Welter ME, Murray MG, Zeitler B, Amora R et al (2013) Trait stacking via targeted genome editing. Plant Biotech J 11:1126–1134

    Article  CAS  Google Scholar 

  • Albert H, Dale EC, Lee E, Ow DW (1995) Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7:649–659

    Article  CAS  PubMed  Google Scholar 

  • Ali Z, Abul-faraj A, Piatek M, Mahfouz M (2015a) Activity and specificity of TRV-mediated gene editing in plants. Plant Signal Behav. doi:10.1080/15592324.2015.1044191

    PubMed  PubMed Central  Google Scholar 

  • Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz MM (2015b) CRISPR/Cas9- mediated viral interference in plants. Genome Biol 16:238. doi:10.1186/s13059-015-0799-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aouida M, Piatek MJ, Bangarusamy DK, Mahfouz MM (2014) Activities and specificities of homodimeric TALENs in Saccharomyces cerevisiae. Curr Genet 60:61–74

    Article  CAS  PubMed  Google Scholar 

  • Araki M, Ishii T (2015) Towards social acceptance of plant breeding by genome editing. Trends Plant Sci 20(3):145–149

    Article  CAS  PubMed  Google Scholar 

  • Araki M, Nojima K, Ishii T (2014) Caution required for handling genome editing technology. Trends Biotechnol 32(5):234–237

    Article  CAS  PubMed  Google Scholar 

  • Arnould S, Perez C, Cabaniols JP, Smith J, Gouble A, Grizot S, Epinat JC, Duclert A, Duchateau P, Paques F (2007) Engineered I-CreI derivatives cleaving sequences from the human XPC gene can induce highly efficient gene correction in mammalian cells. J Mol Biol 371:49–65

    Article  CAS  PubMed  Google Scholar 

  • Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF (2014) DNA replicons for plant genome engineering. Plant Cell 26:151–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN, Bisaro DM et al (2015) Conferring resistance to geminiviruses with the CRISPR-Cas prokaryotic immune system. Nat Plants. doi:10.1038/nplants.2015.145

    Google Scholar 

  • Barrangou R (2012) RNA-mediated programmable DNA cleavage. Nat Biotechnol 30:836–838

    Article  CAS  PubMed  Google Scholar 

  • Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712

    Article  CAS  PubMed  Google Scholar 

  • Becker M (2012) Method of the year 2011. Nat Methods. doi:10.1038/nmeth.1852

    Google Scholar 

  • Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA-binding specificity of TAL-type III effectors. Science 326:1509–1512

    Article  CAS  PubMed  Google Scholar 

  • Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA targeting. Science 333:1843–1846

    Article  CAS  PubMed  Google Scholar 

  • Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotech Adv 33:41–52

    Article  CAS  Google Scholar 

  • Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166:1292–1297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bultmann S, Morbitzer R, Schmidt CS, Thanisch K, Spada F, Elsaesser J, Lahaye T, Leonhardt H (2012) Targeted transcriptional activation of silent oct4 pluripotency gene by combining designer TALEs and inhibition of epigenetic modifiers. Nucleic Acids Res 40:5368–5377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai CQ, Doyon Y, Ainley WM, Miller JC, Dekelver RC, Moehle EA, Rock JM et al (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol 69:699–709

    Article  CAS  PubMed  Google Scholar 

  • Cai Y, Chen L, Liu X, Sun S, Wu C, Jiang B et al (2015) CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS One. doi:10.1371/journal.pone.0136064

    Google Scholar 

  • Caldwell D, McCallum N, Shaw P, Muehlbauer GJ, Marshall DF, Waugh R (2004) A structured mutant population for forward and reverse genetics in Barley (Hordeum vulgare L.). Plant J 40:143–150

    Article  CAS  PubMed  Google Scholar 

  • Cantos C, Francisco P, Trijatmiko KR, Slamet-Loedin I, Chadha-Mohanty PK (2014) Identification of “safe harbor” loci in indica rice genome by harnessing the property of zinc-finger nucleases to induce DNA damage and repair. Front Plant Sci. doi:10.3389/fpls.2014.00302

    PubMed  PubMed Central  Google Scholar 

  • Carroll D (2011) Genome engineering with zinc-finger nucleases. Genetics 188:773–782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll D, Morton JJ, Beumer KJ, Segal DJ (2006) Design, construction and in vitro testing of zinc finger nucleases. Nat Protoc 1(3):1329–1341

    Article  CAS  PubMed  Google Scholar 

  • Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. doi:10.1093/nar/gkr218

    PubMed  Google Scholar 

  • Cermak T, Baltes NJ, Čegan R, Zhang Y, Voytas DF (2015) High-frequency, precise modification of the tomato genome. Genome Biol. doi:10.1186/s13059-015-0796-9

    PubMed  PubMed Central  Google Scholar 

  • Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol. doi:10.1111/mpp.12375

    PubMed  Google Scholar 

  • Chaparro-Garcia A, Kamoun S, Nekrasov V (2015) Boosting plant immunity with CRISPR/Cas. Genome Biol. doi:10.1186/s13059-015-0829-4

    PubMed  PubMed Central  Google Scholar 

  • Char SN, Unger-Wallace E, Frame B, Briggs SA, Main M, Spalding MH, Vollbrecht E, Wang K, Yang B (2015) Heritable site-specific mutagenesis using TALENs in maize. Plant Biotech J. doi:10.1111/pbi.12344

    Google Scholar 

  • Chawla R, Shakya R, Rommens CM (2012) Tuber-specific silencing of asparagine synthetase-1 reduces the acrylamide-forming potential of potatoes grown in the field without affecting tuber shape and yield. Plant Biotech J 10:913–924

    Article  CAS  Google Scholar 

  • Chen K, Shan Q, Gao C (2014) An efficient TALEN mutagenesis system in rice. Methods 69:2–8

    Article  CAS  PubMed  Google Scholar 

  • Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, Kim JS (2014) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24:132–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christian M, Qi Y, Zhang Y, Voytas DF (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 (Bethesda) 3:1697–1705

    Article  CAS  Google Scholar 

  • Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R et al (2016) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotech J. doi:10.1111/pbi.12370

    Google Scholar 

  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cristea S, Freyvert Y, Santiago Y, Holmes MC, Urnov FD, Gregory PD et al (2013) In vivo cleavage of transgene donors promotes nuclease-mediated targeted integration. Biotechnol Bioeng 110:871–880

    Article  CAS  PubMed  Google Scholar 

  • Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C, Baltes NJ et al (2011) Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol 156:466–473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curtin SJ, Anderson JE, Starker CG, Baltes NJ, Mani D, Voytas DF, Stupar RM (2013) Targeted mutagenesis for functional analysis of gene duplication in legumes. Methods Mol Biol 1069:25–42

    Article  CAS  PubMed  Google Scholar 

  • D’Halluin K, Vanderstraeten C, Van Hulle J, Rosolowska J, Van Den Brande I, Pennewaert A, D’Hont K, Bossut M, Jantz D, Ruiter R, Broadhvest J (2013) Targeted molecular trait stacking in cotton through targeted double-strand break induction. Plant Biotech J 11:933–941

    Article  CAS  Google Scholar 

  • De Buck S, Jacobs A, Van Montagu M, Depicker A (1999) The DNA sequences of T-DNA junctions suggest that complex T-DNA loci are formed by a recombination process resembling T-DNA integration. Plant J 20:295–304

    Article  PubMed  Google Scholar 

  • de Pater S, Pinas JE, Hooykaas PJ, Van der Zaal BJ (2013) ZFN mediated gene targeting of the Arabidopsis protoporphyrinogen oxidase gene through Agrobacterium-mediated floral dip transformation. Plant Biotech J 11:510–515

    Article  CAS  Google Scholar 

  • Djukanovic V, Smith J, Lowe K, Yang M, Gao H, Jones S, Nicholson MG, West A, Lape J, Bidney D, Carl Falco S, Jantz D, Alexander L (2013) Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J 76:888–899

    Article  CAS  PubMed  Google Scholar 

  • Du H, Zeng X, Zhao M, Cui X, Wang Q, Yang H, Cheng H, Yu D (2015) Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotech. doi:10.1016/j.jbiotec.2015.11.005

    Google Scholar 

  • EFSA Panel on Genetically Modified Organisms (2012) Scientific opinion addressing the safety assessment of plants developed using zinc finger nuclease 3 and other site-directed nucleases with similar function. EFSA J 10:2943

    Article  CAS  Google Scholar 

  • Endo M, Mikami M, Toki S (2015) Multi gene knockout utilizing off-target mutations of the CRISPR/Cas9 system in rice. Plant Cell Physiol 56:41–47

    Article  CAS  PubMed  Google Scholar 

  • Endo M, Mikami M, Toki S (2016) Bi-allelic gene targeting in rice. Plant Physiol. doi:10.1104/pp.15.01663

    PubMed  Google Scholar 

  • Even-Faitelson L, Samach A, Melamed-Bessudo C, Avivi-Ragolsky N, Levy AA (2011) Localized egg-cell expression of effector proteins for targeted modification of the Arabidopsis genome. Plant J 68:929–937

    Article  CAS  PubMed  Google Scholar 

  • Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep. doi:10.1038/srep12217

    Google Scholar 

  • Fauser F, Schiml S, Puchta H (2014) Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J 79:348–359. doi:10.1111/tpj.12554

    Article  CAS  PubMed  Google Scholar 

  • 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/Cas system. Cell Res 23:1229–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, Zeng L, Liu X, Zhu JK (2014) Multi-generation analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas induced gene modifications in Arabidopsis. PNAS 111:4632–4637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng C, Yuan J, Wang R, Liu Y, Birchler JA, Han F (2016) Efficient targeted genome modification in maize using CRISPR/Cas9 system. J Genet Genomics 43:37–43

    Article  PubMed  Google Scholar 

  • Forner J, Pfeiffer A, Langenecker T, Manavella P, Lohmann JU (2015) Germline- transmitted genome editing in Arabidopsis thaliana using TAL-Effector-Nucleases. PLoS One. doi:10.1371/journal.pone.0121056

    Google Scholar 

  • Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D, Lyznik LA (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J 61:176–187

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Wang G, Ma S, Xie X, Wu X, Zhang X, Wu Y, Zhao P, Xia Q (2015a) CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol 87:99–110

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y (2015b) Auxin binding protein 1 (ABP1) is not required for either auxin signalling or Arabidopsis development. PNAS 112:2275–2280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta M, DeKelver RC, Palta A, Clifford C, Gopalan S, Miller JC, Novak S, Desloover D et al (2012) Transcriptional activation of Brassica napus beta-ketoacyl-ACP synthase II with an engineered zinc finger protein transcription factor. Plant Biotech J 10:783–791

    Article  CAS  Google Scholar 

  • Gurushidze M, Hensel G, Hiekel S, Schedel S, Valkov V, Kumlehn J (2014) True-breeding targeted gene knock-out in barley using designer TALE nuclease in haploid cells. PLoS One. doi:10.1371/journal.pone.0092046

    PubMed  PubMed Central  Google Scholar 

  • Hartung F, Schiemann J (2014) Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J 78:742–752

    Article  CAS  PubMed  Google Scholar 

  • Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF, Zhang F (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotech J 12:934–940

    Article  CAS  Google Scholar 

  • Hinge V, Patil H, Nadaf AB (2015) Comparative characterization of aroma volatiles and related gene expression analysis at vegetative and mature stages in basmati and non-basmati rice (Oryza sativa L.) cultivars. Appl. Biochem. doi:10.1007/s12010-015-1898-2

    Google Scholar 

  • Hyun Y, Kim J, Cho SW, Choi Y, Kim JS, Coupland G (2015) Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles. Planta 241:271–284. doi:10.1007/s00425-014-2180-5

    Article  CAS  PubMed  Google Scholar 

  • Iqbal Z, Sattar MN, Shafiq M (2016) CRISPR/Cas9: A tool to circumscribe cotton leaf curl disease. Front Plant Sci. doi:10.3389/fpls.2016.00475

    Google Scholar 

  • Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in E coli and identification of the gene product. J Bacteriol 169:5429–5433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Toki S (2015) CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem Biophys Res Commun. doi:10.1016/j.bbrc.2015.09.117

    Google Scholar 

  • Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol. doi:10.1186/s12896-015-0131-2

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ji X, Zhang H, Zhang Y, Wang Y, Gao C (2015) Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nat Plants. doi:10.1038/nplants.2015.144

    PubMed  Google Scholar 

  • Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One. doi:10.1371/journal.pone.0093806

    Google Scholar 

  • 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. doi:10.1093/nar/gkt780

    Google Scholar 

  • Jiang W, Yang B, Weeks DP (2014) Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS One. doi:10.1371/journal.pone.0099225

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Johnson RA, Gurevich V, Filler S, Samach A, Levy AA (2015) Comparative assessments of CRISPR-Cas nucleases’ cleavage efficiency in planta. Plant Mol Biol 87:143–156

    Article  CAS  PubMed  Google Scholar 

  • Kanchiswamy CN (2016) DNA-free genome editing methods for targeted crop improvement. Plant Cell Rep. doi:10.1007/s00299-016-1982-2

    PubMed  Google Scholar 

  • Kanchiswamy CN, Sargent DJ, Velasco R, Maffei ME, Malnoy M (2015) Looking forward to genetically edited fruit crops. Trends Biotechnol 33(2):62–63

    Article  CAS  Google Scholar 

  • Khandagale KS, Zanan RL, Nadaf AB (2016) RNA interference and targeted genome editing for improvement of rice (Oryza sativa L.). Israel J Plant Sci (communicated)

  • Khatodia S, Bhatotia K, Passricha N, Khurana SMP, Tuteja N (2016) The CRISPR/Cas genome-editing tool: application in improvement of crops. Front Plant Sci. doi:10.3389/fpls.2016.00506

    PubMed  PubMed Central  Google Scholar 

  • Kirik A, Salomon S, Puchta H (2000) Species-specific double-strand break repair and genome evolution in plants. EMBO J 19:5562–5566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawrenson T, Shorinola O, Stacey N, Li C, Østergaard L, Patron N, Uauy C, Harwood W (2015) Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol. doi:10.1186/s13059-015-0826-7

    PubMed  PubMed Central  Google Scholar 

  • Li T, Huang S, Zhao X, Wright DA, Carpenter S, Spalding MH, Yang B (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 39(14):6315–6325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392

    Article  CAS  PubMed  Google Scholar 

  • Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J (2013) Multiplex and homologous recombination mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31:688–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Liu B, Chen CY, Yang B (2014) TALEN utilization in rice genome modifications. Methods 69:9–16

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP, Huang L, Ward RT, Clifton E, Falco SC, Cigan AM (2015) Cas9-guide RNA directed genome editing in Soybean. Plant Physiol. doi:10.1104/pp.15.00783

    Google Scholar 

  • Li Q, Zhang D, Chen M, Liang W, Wei J, Qi Y, Yuan Z (2016) Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. J Genet Genomics. doi:10.1016/j.jgg.2016.04.011

    PubMed Central  Google Scholar 

  • Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genomics 41:63–68

    Article  CAS  PubMed  Google Scholar 

  • Liang G, Zhang H, Lou D, Yu D (2016) Selection of highly efficient sgRNAs for CRISPR/Cas9 based plant genome editing. Sci Rep. doi:10.1038/srep21451

    Google Scholar 

  • Lloyd A, Plaisier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. PNAS 102:2232–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lor VS, Starker CG, Voytas DF, Weiss D, Olszewski NE (2014) Targeted mutagenesis of the tomato PROCERA gene using TALENs. Plant Physiol 166:1288–1291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X, Zheng X, Voytas DF, Hsieh TF, Zhang Y, Qi Y (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol. doi:10.1104/pp.15.00636

    PubMed  PubMed Central  Google Scholar 

  • Ma XL, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R et al (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant. doi:10.1016/j.molp.2015.04.007

    Google Scholar 

  • Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM et al (2008) Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 31:294–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu JK (2011) De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA-binding specificity creates double-strand breaks. PNAS 108:2623–2628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahfouz MM, Piatek A, Stewart CN Jr (2014) Genome engineering via TALENs and CRISPR/Cas9 systems: challenges and perspectives. Plant Biotech J 12:1006–1014

    Article  CAS  Google Scholar 

  • Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marta V, Joan MB, Asun F, Pello Z, Jose B, Antonio G, Diego O (2016) A modular toolbox for gRNA–Cas9 genome engineering in plants based on the GoldenBraid standard. Plant Methods. doi:10.1186/s13007-016-0101-2

    Google Scholar 

  • Martin-Ortigosa S, Peterson DJ, Valenstein JS, Lin VS, Trewyn BG, Lyznik LA, Wang K (2014) Mesoporous silica nanoparticle-mediated intracellular cre protein delivery for maize genome editing via lox-P site excision. Plant Physiol 164:537–547

    Article  CAS  PubMed  Google Scholar 

  • McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeted screening for induced mutations. Nat Biotechnol 18:455–457

    Article  CAS  PubMed  Google Scholar 

  • Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, Wan J, Gu H, Qu LJ (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23:1233–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikami M, Toki S, Endo M (2015a) Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice. Plant Mol Biol. doi:10.1007/s11103-015-0342-x

    PubMed  PubMed Central  Google Scholar 

  • Mikami M, Toki S, Endo M (2015b) Parameters affecting frequency of CRISPR/Cas9 mediated targeted mutagenesis in rice. Plant Cell Rep. doi:10.1007/s00299-015-1826-5

    PubMed  Google Scholar 

  • Mojica FJM, Ferrer C, Juez G, Rodrı´guez-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

    Article  CAS  PubMed  Google Scholar 

  • Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326:1501

    Article  CAS  PubMed  Google Scholar 

  • Nanto K, Sato K, Katayama Y, Ebinuma H (2009) Expression of a transgene exchanged by the recombinase-mediated cassette exchange (RMCE) method in plants. Plant Cell Rep 28:777–785

    Article  CAS  PubMed  Google Scholar 

  • Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31:691–693

    Article  CAS  PubMed  Google Scholar 

  • Nicolia A, Proux-Wera E, Ahman I, Onkokesung N, Andersson M, Andreasson E, Zhu LH (2015) Targeted gene mutation in tetraploid potato through transient TALEN expression in protoplasts. J Biotechnol 204:17–24

    Article  CAS  PubMed  Google Scholar 

  • Ning YQ, Ma ZY, Huang HW, Mo H, Zhao TT, Li L, Cai T, Chen S, Ma L, He XJ (2015) Two novel NAC transcription factors regulate gene expression and flowering time by associating with the histone demethylase JMJ14. Nucleic Acids Res 43:1469–1484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishitani C, Hirai N, Komori S, Wada M, Okada K, Osakabe K, Yamamoto T, Osakabe Y (2016) Efficient Genome Editing in Apple Using a CRISPR/Cas9 system. Sci Rep 6:31481. doi:10.1038/srep31481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osakabe K, Osakabe Y, Toki S (2010) Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. PNAS 107:12034–12039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peer R, Rivlin G, Golobovitch S, Lapidot M, Gal-On A, Vainstein A, Tzfira T, Flaishman MA (2015) Targeted mutagenesis using zinc-finger nucleases in perennial fruit trees. Planta 241:941–951

    Article  CAS  PubMed  Google Scholar 

  • Petolino JF, Worden A, Curlee K, Connell J, Moynahan TL, Larsen C, Russell S (2010) Zinc finger nuclease-mediated transgene deletion. Plant Mol Biol 73:617–628

    Article  CAS  PubMed  Google Scholar 

  • Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S, Aouida M, Mahfouz MM (2015) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13:578–589

    Article  CAS  PubMed  Google Scholar 

  • Porteus MH, Carroll D (2005) Gene targeting using zinc finger nucleases. Nat Biotechnol 23:967–973

    Article  CAS  PubMed  Google Scholar 

  • Puchta H, Dujon B, Hohn B (1993) Homologous recombination in plant-cells is enhanced by in vivo induction of double-strand breaks into DNA by a site-specific endonuclease. Nucleic Acids Res 21:5034–5040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013a) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183. doi:10.1016/j.cell.2013.02.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi Y, Li X, Zhang Y, Starker CG, Baltes NJ, Zhang F, Sander JD, Reyon D, Joung JK, Voytas DF (2013b) Targeted deletion and inversion of tandomly arrayed genes in Arabidopsis thaliana using zinc finger nucleases. G3 (Bethesda) 3:1707–1715

    Article  PubMed Central  CAS  Google Scholar 

  • Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281–2308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy DCL, Radhika V, Bharadwaj A, Khandagale KS, Aswath C (2012) miRNAs in brinjal (Solanum melongena) mined through an in silico approach. J Hort Sci Biotechnol 87(2):186–192

    CAS  Google Scholar 

  • Ren C, Liu X, Zhang Z, Wang Y, Duan W, Li S, Liang Z (2016) CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.). Sci Rep 6:32289. doi:10.1038/srep32289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ron M, Kajala K, Pauluzzi G, Wang D, Reynoso MA, Zumstein K, Garcha J, Winte S, Masson H, Inagaki S, Federici F, Sinha N, Deal RB, Bailey-Serres J, Brady SM (2014) Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol 166:455–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roth N, Klimesch J, Dukowic-Schulze S, Pacher M, Mannuss A, Puchta H (2012) The requirement for recombination factors differs considerably between different pathways of homologous double-strand break repair in somatic plant cells. Plant J 72:781–790

    Article  CAS  PubMed  Google Scholar 

  • Russell SH, Hoopes JL, Odell JT (1992) Directed excision of a transgene from the plant genome. Mol Gen Genet 234:49–59

    CAS  PubMed  Google Scholar 

  • Salomon S, Puchta H (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J 17:6086–6095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sander SD, Joung JK (2014) CRISPR-Cas systems for genome editing, regulation and targeting. Nat Biotechnol 32(4):347–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sander JD, Zaback P, Joung JK, Voytas DF, Dobbs D (2007) Zinc Finger Targeter (ZiFiT): an engineered zinc finger/target site design tool. Nucleic Acids Res 35:599–605

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schiml S, Fauser F, Puchta H (2014) 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 80:1139–1150

    Article  CAS  PubMed  Google Scholar 

  • Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG et al (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87

    Article  CAS  PubMed  Google Scholar 

  • Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688

    Article  CAS  PubMed  Google Scholar 

  • Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotech J 13:791–800

    Article  CAS  Google Scholar 

  • Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE et al (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441

    Article  CAS  PubMed  Google Scholar 

  • Silva G, Poirot L, Galetto R, Smith J, Montoya G, Duchateau P, Pâques F (2011) Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr Gene Ther 11:11–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinert J, Schiml S, Fauser F, Puchta H (2015) Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophiles and Staphylococcus aureus. Plant J 84(6):1295–1305

    Article  CAS  PubMed  Google Scholar 

  • Stoddard BL (2011) Homing endonucleases: From microbial genetic invaders to reagents for targeted DNA modification. Structure 19:7–15. doi:10.1016/j.str.2010.12.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM (2015) Targeted mutagenesis, precise gene editing and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 2:931–945

    Article  CAS  Google Scholar 

  • Swedish Board of Agriculture (2015) Green light in the tunnel”! Swedish Board of Agriculture: a CRISPR-Cas9-mutant but not a GMO. http://www.upsc.se/about-upsc/news/4815-green-light-in-the-tunnel-swedish-board-of-agriculture-a-crispr-cas9-mutant-but-not-a-gmo.html. Accessed 10 Sept 2016

  • Tax FE, Vernon DM (2001) T-DNA-associated duplication/translocations in Arabidopsis implications for mutant analysis and functional genomics. Plant Physiol 126:1527–1538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor G, Petrucci L, Lambert A, Baxter S, Jarjour J, Stoddard B (2012) LAHEDES: the LAGLIDADG homing endonuclease database and engineering server. Nucleic Acids Res 40:110–116

    Article  CAS  Google Scholar 

  • The McGuinness Institute (2013) An Overview of Genetic Modification in New Zealand 1973–2013: The First Forty Years, Auckland Council. http://www.aucklandcouncil.govt.nz/EN/planspoliciesprojects/plansstrategies/unitaryplan/Documents/Section32report/Appendices/Appendix%203.49.16.pdf. Accessed 8 Sept 2016

  • Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai C, Xue L (2015) CRISPRing into the woods. GM Crops Food. doi:10.1080/21645698.2015.1091553

    PubMed  PubMed Central  Google Scholar 

  • Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda) 3:2233–2238

    Article  CAS  Google Scholar 

  • USDA (2012) http://www.aphis.usda.gov/biotechnology/downloads/reg_loi/APHIS_response_DO W_ZFN_PK1_030812.pdf]

  • Waltz E (2016) Gene-edited CRISPR mushroom escapes US regulation. Nature 532:293. doi:10.1038/nature.2016.19754

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Liu Y, Zhang C, Liu J, Liu X, Wang L et al (2015) Gene editing by co-transformation of TALEN and chimeric RNA/DNA oligonucleotides on the rice OsEPSPS gene and the inheritance of mutations. PLoS One. doi:10.1371/journal.pone.0122755

    Google Scholar 

  • Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu YG, Zhao K (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One. doi:10.1371/journal.pone.0154027

    Google Scholar 

  • Weeks DP, Spalding MH, Yang B (2015) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotech J. doi:10.1111/pbi.12448

    Google Scholar 

  • Weinthal D, Tovkach A, Zeevi V, Tzfira T (2010) Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci 15(6):308–321

    Article  CAS  PubMed  Google Scholar 

  • Wendt T, Holm PB, Starker CG, Christian M, Voytas DF, Brinch- Pedersen H, Holme IB (2013) TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol 83:279–285

    Article  CAS  PubMed  Google Scholar 

  • Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–338. doi:10.1038/nature10886

    Article  CAS  PubMed  Google Scholar 

  • Wolt JD, Wang K, Yang B (2015) The Regulatory Status of Genome-edited Crops. Plant Biotech J. doi:10.1111/pbi.12444

    Google Scholar 

  • Woo JW, Kim J, Kwon S, Corvalán C, Cho SW, Kim H, Kim S, Kim S, Choe S, Kim J (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33:1162–1164. doi:10.1038/nbt.3389

    Article  CAS  PubMed  Google Scholar 

  • Wright DA, Townsend JA, Winfrey RJ, Irwin PA, Rajagopal J, Lonosky PM, Hall BD, Jondle MD, Voytas DF (2005) High frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J 44:693–705

    Article  CAS  PubMed  Google Scholar 

  • Wright DA, Li T, Yang B, Spalding MH (2014) TALEN-mediated genome editing: prospects and perspectives. Biochem J 462:15–24

    Article  CAS  PubMed  Google Scholar 

  • Xie K, Yang Y (2013) RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant 6:1975–1983

    Article  CAS  PubMed  Google Scholar 

  • Xiong JS, Ding J, Li Y (2015) Genome-editing technologies and their potential application in horticultural crop breeding. Hort Res. doi:10.1038/hortres.2015.19

    Google Scholar 

  • Xu R, Li H, Qin R, Wang L, Li L, Wei P, Yang J (2014) Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice (N Y) 7:5. doi:10.1186/s12284-014-0005-6

    Google Scholar 

  • Xu RF, Li H, Qin RY, Li J, Qiu CH, Yang YC, Ma H, Li L, Wei PC, Yang JB (2015) Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep. doi:10.1038/srep11491

    Google Scholar 

  • Yokoi AN, Cermak T, Hoshino T, Sugimoto K, Saika H, Mori A, Osakabe K, Hamada M, Katayose Y, Starker C, Voytas DF, Toki S (2015) A defect in DNA ligase 4 enhances the frequency of TALEN-mediated targeted mutagenesis in rice. Plant Physiol. doi:10.1104/pp.15.01542

    Google Scholar 

  • Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyl transferases to access H1-containing heterochromatin. Cell 153:193–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Maeder ML, Unger-Wallace E, Hoshaw JP, Reyon D, Christian M, Li X, Pierick CJ, Dobbs D, Peterson T, Joung JK, Voytas DF (2010) High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. PNAS 107:12028–12033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N, Zhu JK (2014) The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotech J 12:797–807

    Article  CAS  Google Scholar 

  • Zhang Z, Mao Y, Ha S, Liu W, Botella J, Zhu JK (2015) A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep. doi:10.1007/s00299-015-1900-z

    Google Scholar 

  • Zhou H, Liu B, Weeks DP, Spalding MH, Yang B (2014) Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res 42:10903–10914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom JS, Huang S, Liu S, Cruz CV, Frommer WB, White FF, Yang B (2015a) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–643

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Jacobs TB, Xue L, Harding SA, Tsai C (2015b) Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate: CoA ligase specificity and redundancy. New Phytol 208:298–301

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Song N, Sun S, Yang W, Zhao H, Song W, Lai J (2016) Efficiency and inheritance of targeted mutagenesis in maize using CRISPR–Cas9. J Genet Genomics 43:25–36

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

KK acknowledges Council of Scientific and Industrial Research (CSIR), New Delhi, India (Sanction No. 09/137/(0541)/2012-EMR-1) for the award of senior research fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Altafhusain Nadaf.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khandagale, K., Nadaf, A. Genome editing for targeted improvement of plants. Plant Biotechnol Rep 10, 327–343 (2016). https://doi.org/10.1007/s11816-016-0417-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-016-0417-4

Keywords

Navigation