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Use of TALEs and TALEN Technology for Genetic Improvement of Plants

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Abstract

Genome editing with engineered nucleases has become a powerful tool of targeted genome modifications providing unprecedented control over animal and plant genetic material for precise, robust and highly specific genome engineering. Precise genome editing has been a long standing goal in the field of biology which has been achieved with the help of engineered nucleases like zinc finger nucleases, transcription activator-like effector nucleases (TALENs), and the Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR-associated system. These engineered nucleases consist of a binding and a nuclease domain which are generally used in the form of a pair. The binding domain binds specifically to a DNA sequence whilst the nuclease domain creates double-strand breaks (DSBs) which are further used for non-homologous end joining or homologous recombination repair. Creation of DSBs is the principle of this technology which can be further used for gene addition, deletion and modification in the targeted DNA. Besides nuclease activity, TALE (transcription activator-like effector) proteins have also been used along with other effector domains for different purposes like gene activation, gene repression, epigenetic modifications, etc. The use of TALEs and TALENs for precise genome modifications of plants is now a common practice. So far, tens of crop plants have been modified using engineered nucleases like rice, wheat, tomato, potato, tobacco, maize, barley, cotton, etc. The TALE and TALEN technology is being used for development of biotic and abiotic stress-resistant plants as well as yield and quality improvement. In this article, we will briefly review and discuss TALEs and TALENs, their discovery, binding specificity, designing, functional domains, delivery and use for genome editing specifically in plants.

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References

  • Arazoe T, Ogawa T, Miyoshi K, Yamato T, Ohsato S, Sakuma T (2015) Tailor‐made TALEN system for highly efficient targeted gene replacement in the rice blast fungus. Biotechnol Bioeng 112(7):1335–1342

    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(1):151–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bibikova M, Golic M, Golic KG, Carroll D (2002) Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161:1169–1175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bloom K, Ely A, Mussolino C, Cathomen T, Arbuthnot P (2013) Inactivation of hepatitis B virus replication in cultured cells and in vivo with engineered transcription activator-like effector nucleases. Mol Ther 21(10):1889–1897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloom K, Mussolino C, Arbuthnot P (2015) Transcription activator-like effector (TALE) nucleases and repressor TALEs for antiviral gene therapy. Curr Stem Cell Rep 1:1–8

    Article  CAS  Google Scholar 

  • Blount BA, Weenink T, Vasylechko S, Ellis T (2012) Rational diversification of a promoter providing fine-tuned expression and orthogonal regulation for synthetic biology. PLoS ONE 7(3):e33279–e33279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boch J (2011) TALEs of genome targeting. Nat Biotechnol 29:135–136

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Scholze H, Schornack S et al (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509–1512

    Article  CAS  PubMed  Google Scholar 

  • Bodnar AM, Bernal A, Szurek B, López CE (2013) Tell me a tale of TALEs. Mol Biotechnol 53:228–235

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13:394–401

    Article  CAS  PubMed  Google Scholar 

  • Boissel S, Jarjour J, Astrakhan A, Adey A, Gouble A, Duchateau P (2013) megaTALs: a rare-cleaving nuclease architecture for therapeutic genome engineering. Nucleic Acids Res 42(4):2591–2601

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonas U, Stall RE, Staskawicz B (1989) Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet 218:127–136

    Article  CAS  PubMed  Google Scholar 

  • Briggs AW, Rios X, Chari R, Yang L, Zhang F, Mali P, Church GM (2012) Iterative capped assembly: rapid and scalable synthesis of repeat-module DNA such as TAL effectors from individual monomers. Nucleic Acids Res gks624

  • Büttner D, Bonas U (2002) Getting across-bacterial type III effector proteins on their way to the plant cell. EMBO J 21:5313–5322

    Article  PubMed  PubMed Central  Google Scholar 

  • Castiblanco LF, Gil J, Rojas A, Osorio D, Gutiérrez S, Muñoz‐Bodnar A, Alvaro LP, Bernal AJ (2012) TALE1 from Xanthomonas axonopodis pv. manihotis acts as a transcriptional activator in plant cells and is important for pathogenicity in cassava plants. Mol Plant Pathol 14:84–95

    Article  PubMed  CAS  Google Scholar 

  • Cathomen T, Joung KL (2008) Zinc-finger nucleases: the next generation emerges. Mol Ther 16:1200–1207

    Article  CAS  PubMed  Google Scholar 

  • Cermak T, Doyle EL, Christian M et al (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39:82

    Article  CAS  Google Scholar 

  • Cermak T, Starker CG, Voytas DF (2015) Efficient design and assembly of custom TALENs using the golden gate platform. In: Chromosomal Mutagenesis. Springer, New York, pp 133–159

  • Char SN, Unger‐Wallace E, Frame B et al (2015) Heritable site‐specific mutagenesis using TALENs in maize. Plant Biotechnol J 13:1002–1010

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Oikonomou G, Chi, CN et al. (2013) A large-scale in vivo analysis reveals that TALENs are significantly more mutagenic than ZFNs generated using context-dependent assembly. Nucleic Acids Res gks1356

  • Chen J, Zhang W, Lin J et al (2014) An efficient antiviral strategy for targeting hepatitis B virus genome using transcription activator-like effector nucleases. Mol Ther 22:303–311

    Article  PubMed  CAS  Google Scholar 

  • Cheng Z, Yi P, Wang X et al (2013) Conditional targeted genome editing using somatically expressed TALENs in C. elegans. Nat Biotechnol 31:934–937

    Article  CAS  PubMed  Google Scholar 

  • Cheng X, Li F, Cai J et al (2015) Artificial TALE as a convenient protein platform for engineering broad-spectrum resistance to begomoviruses. Viruses 7:4772–4782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho HS, Kang JG, Lee JH et al (2015) Direct regulation of E-cadherin by targeted histone methylation of TALE-SET fusion protein in cancer cells. Oncotarget 6:23837

    Article  PubMed  PubMed Central  Google Scholar 

  • Choi SM, Kim Y, Shim JS et al (2013) Efficient drug screening and gene correction for treating liver disease using patient‐specific stem cells. Hepatology 57:2458–2468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christian M, Cermak T, Doyle EL et al (2010) Targeting DNA double-strand mobreaks with TAL effector nucleases. Genetics 186:757–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clasen BM, Stoddard TJ, Luo S et al (2015) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J. doi:10.1111/12370

    Google Scholar 

  • Cong L, Zhou R, Kuo YC, Cunniff M, Zhang F (2012) Comprehensive interrogation of natural TALE DNA-binding modules and transcriptional repressor domains. Nat Commun 3:968

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conrads-Strauch J, Balbo I, Bonas, U (1993) Repetitive motifs in the avrBs3 avirulence gene family determine specificity of resistance to Xanthomonas campestris pv. vesicatoria. In: Mechanisms of Plant Defense Responses. Springer, Dordrecht, pp 37–40

  • Davies B, Davies G, Preece C, Puliyadi R, Szumska D, Bhattacharya S (2013) Site specific mutation of the Zic2 locus by microinjection of TALEN mRNA in mouse CD1, C3H and C57BL/6J oocytes. PLoS ONE 8:e60216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Lange O, Wolf C, Dietze J, Elsaesser J, Morbitzer R, Lahaye T (2014) Programmable DNA-binding proteins from Burkholderia provide a fresh perspective on the TALE-like repeat domain. Nucleic Acids Res 42:7436–7449

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deng D, Yan C, Pan X et al (2012) Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335:720–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Halluin K, Vanderstraeten C, Hulle J et al (2013) Targeted molecular trait stacking in cotton through targeted double‐strand break induction. Plant Biotechnol J 11:933–941

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ding Q, Lee YK, Schaefer EA et al (2013) A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell 12:238–251

    Article  CAS  PubMed  Google Scholar 

  • Doyle EL, Booher NJ, Standage DS, Voytas DF, Brendel VP, VanDyk JK, Bogdanove AJ (2012) TAL effector-nucleotide targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res. doi:10.1093/nar/gks608

    Google Scholar 

  • Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ (2013) TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol 23:390–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dreyer AK, Hoffmann D, Lachmann N et al (2015) TALEN-mediated functional correction of X-linked chronic granulomatous disease in patient-derived induced pluripotent stem cells. Biomaterials 69:191–200

    Article  CAS  PubMed  Google Scholar 

  • Durai S, Mani M, Kandavelou K, Wu J, Porteus MH, Chandrasegaran S (2005) Zinc finger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res 33:5978–5990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engler C, Kandzia R, Marillonnet S (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3:3647

    Article  CAS  Google Scholar 

  • Fadel HJ, Morrison JH, Saenz DT et al (2014) TALEN knockout of the PSIP1 gene in human cells: analyses of HIV-1 replication and allosteric integrase inhibitor mechanism. J Virol 88:9704–9717

    Article  PubMed  PubMed Central  CAS  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 10:e0121056

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK (2013) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32(3):279–284

    Article  CAS  Google Scholar 

  • Gallie DR (1993) Posttranscriptional regulation of gene expression in plants. Annu Rev Plant Biol 44(1):77–105

    Article  CAS  Google Scholar 

  • Gan Q, Bai H, Zhao X et al (2011) Transcriptional characteristics of Xa21‐mediated defense responses in rice. J Integr Plant Biol 53:300–311

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Tsang JC, Gaba F, Wu D, Lu L, Liu P (2014) Comparison of TALE designer transcription factors and the CRISPR/dCas9 in regulation of gene expression by targeting enhancers. Nucleic Acids Res 42:e155–e155

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao F, Shen XZ, Jiang F, Wu Y, Han C (2016) DNA-guided genome editing using the Natronobacterium gregoryi Argonaute. Nat Biotechnol. doi:10.1038/nbt.3547

    PubMed Central  Google Scholar 

  • Garg A, Lohmueller JJ, Silver PA, Armel TZ (2012) Engineering synthetic TAL effectors with orthogonal target sites. Nucleic Acids Res gks404

  • Geissler R, Scholze H, Hahn S et al (2011) Transcriptional activators of human genes with programmable DNA-specificity. PLoS ONE 6:e19509

    Article  CAS  PubMed  Google Scholar 

  • Grau J, Boch J, Posch S (2013) TALENoffer: genome-wide TALEN off-target prediction. Bioinformatics 29:2931–2932

    Article  CAS  PubMed  Google Scholar 

  • Greco R, Ouwerkerk PB, Sallaud C et al (2001) Transposon insertional mutagenesis in rice. Plant Physiol 125:1175–1177

    Article  CAS  PubMed  PubMed Central  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 9(3):e92046

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haun W, Coffman A, Clasen BM et al (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 2:934–940

    Article  CAS  Google Scholar 

  • Heigwer F, Kerr G, Walther N et al (2013) E-TALEN: a web tool to design TALENs for genome engineering. Nucleic Acids Res 41:e190–e190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heuer H, Yin YN, Xue QY, Smalla K, Guo JH (2007) Repeat domain diversity of avrBs3-like genes in Ralstonia solanacearum strains and association with host preferences in the field. Appl Environ Microbiol 73:4379–4384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilton IB, D’Ippolito AM, Vockley CM et al (2015) Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 33:510–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hockemeyer D, Wang H, Kiani S et al (2011) Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 29:731–734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hopkins CM, White FF, Choi SH, Guo A, Leach JE (1992) Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact 5:451–459

    Article  CAS  PubMed  Google Scholar 

  • Huang P, Xiao A, Zhou M, Zhu Z, Lin S, Zhang B (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29:699–700

    Article  PubMed  CAS  Google Scholar 

  • Jia J, Jin Y, Bian T et al (2014) Bacterial delivery of TALEN proteins for human genome editing. PLoS ONE. doi:10.1371/0091547

    Google Scholar 

  • Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. 2014

  • Joung JK, Mendenhall EM, Bernstein BE, Reyon D (2013) Transcription activator-like effector (TALE)-lysine-specific demethylase 1 (LSD1) fusion proteins. U.S. Patent Application 14/435,065

  • Juillerat A, Dubois G, Valton J et al. (2014) Comprehensive analysis of the specificity of transcription activator-like effector nucleases. Nucleic Acids Res gku155

  • Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648

    Article  CAS  PubMed  Google Scholar 

  • Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 93:1156–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim Y, Schumaker KS, Zhu JK (2006) EMS mutagenesis of Arabidopsis. In: Arabidopsis Protocols. Humana Press, New York, pp 101–103

  • Konermann S, Brigham MD, Trevino AE et al (2013) Optical control of mammalian endogenous transcription and epigenetic states. Nature 500:472–476

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuscu C, Arslan S, Singh R, Thorpe J, Adli M (2014) Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat Biotechnol 32(7):677–683

    Article  CAS  PubMed  Google Scholar 

  • Lamb BM, Mercer AC, Barbas CF (2013) Directed evolution of the TALE N-terminal domain for recognition of all 5′ bases. Nucleic Acids Res gkt754

  • Li T, Huang S, Zhao, X et al. (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res gkr188

  • 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 L, Atef A, Piatek A et al (2013) Characterization and DNA-binding specificities of Ralstonia TAL-like effectors. Mol Plant 6:1318–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Stoddard TJ, Demorest ZL, Lavoie PO, Luo S, Clasen BM et al (2015) Multiplexed, targeted gene editing in Nicotiana benthamiana for glyco‐engineering and monoclonal antibody production. Plant Biotechnol J 14(2):533–42

    Article  PubMed  CAS  Google Scholar 

  • Li T, Liu B, Chen CY, Yang B (2016) TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J Genet Genomics. doi:10.1016/j.jgg.2016.03.005

    Google Scholar 

  • Lieber MR (2010) NHEJ and its backup pathways in chromosomal translocations. Nat Struct Mol Biol 17:393–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin Y, Fine EJ, Zheng Z et al (2014) SAPTA: a new design tool for improving TALE nuclease activity. Nucleic Acids Res 42:e47–e47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W, Yuan JS, Stewart JCN (2013) Advanced genetic tools for plant biotechnology. Nat Rev Genet 14:781–793

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Gaj T, Patterson JT, Sirk SJ, Barbas LCF (2014) Cell-penetrating peptide-mediated delivery of TALEN proteins via bioconjugation for genome engineering. PLoS ONE 9:e85755

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lombardo A, Genovese P, Beausejour CM et al (2007) Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 25:1298–1306

    Article  CAS  PubMed  Google Scholar 

  • Luo S, Li J, Stoddard TJ et al (2015) Non-transgenic plant genome editing using purified sequence-specific nucleases. Mol Plant. doi:10.1016/j.molp.2015.05.012

    Google Scholar 

  • Maeder ML, Angstman JF, Richardson ME et al (2013) Targeted DNA demethylation and activation of endogenous genes using programmable TALE-TET1 fusion proteins. Nat Biotechnol 31:1137–1142

    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. Proc Natl Acad Sci U S A 108:2623–2628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahfouz MM, Li L, Piatek M et al (2012) Targeted transcriptional repression using a chimeric TALE-SRDX repressor protein. Plant Mol Biol 78:311–321

    Article  CAS  PubMed  Google Scholar 

  • Mak ANS, Bradley P, Cernadas RA, Bogdanove AJ, Stoddard BL (2012) The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335:716–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S et al (2013) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31(9):833–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maresca M, Lin VG, Guo N, Yang Y (2013) Obligate ligation-gated recombination (ObLiGaRe): custom-designed nuclease-mediated targeted integration through non homologous end joining. Genome Res 23(3):539–546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marois E, Van den Ackerveken G, Bonas U (2002) The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant-Microbe Interact 15:637–646

    Article  CAS  PubMed  Google Scholar 

  • Mendenhall EM, Williamson KE, Reyon D et al (2013) Locus-specific editing of histone modifications at endogenous enhancers. Nat Biotechnol 31:1133–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mercer AC, Gaj T, Fuller RP, Barbas CF (2012) Chimeric TALE recombinases with programmable DNA sequence specificity. Nucleic Acids Res 40:11163–11172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller JC, Tan S, Qiao G et al (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29:143–148

    Article  CAS  PubMed  Google Scholar 

  • Mino T, Mori T, Aoyama Y, Sera T (2014) Inhibition of DNA replication of human papillomavirus by using zinc finger–single-chain foki dimer hybrid. Mol Biotechnol 56:731–737

    Article  CAS  PubMed  Google Scholar 

  • Mock U, Machowicz R, Hauber I, Horn S, Abramowski P, Berdien B (2015) mRNA transfection of a novel TAL effector nuclease (TALEN) facilitates efficient knockout of HIV co-receptor CCR5. Nucleic Acids Res 43(11):5560–5571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moehle EA, Rock JM, Lee YL et al (2007) Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc Natl Acad Sci U S A 104:3055–3060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montague TG, Cruz JM, Gagnon JA, Church GM, Valen E (2014) CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res 42:W401–W407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morbitzer R, Elsaesser J, Hausner J, Lahaye T (2011a) Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res 39:5790–5799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morbitzer R, Römer P, Boch J, Lahaye T (2011b) Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. Proc Natl Acad Sci U S A 107:21617–21622

    Article  Google Scholar 

  • Mori T, Takenaka K, Domoto F, Aoyama Y, Sera T (2013) Inhibition of binding of tomato yellow leaf curl virus Rep to its replication origin by artificial zinc-finger protein. Mol Biotechnol 54:198–203

    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 

  • Muller HJ (1927) X-ray induced mutation of Drosophila virilis. Science 66:84–87

    Article  CAS  PubMed  Google Scholar 

  • Mussolino C, Morbitzer R, Lütge F, Dannemann N, Lahaye T, Cathomen T (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39:9283–9293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakatsukasa T, Shiraishi Y, Negi S, Imanishi M, Futaki S, Sugiura Y (2005) Site-specific DNA cleavage by artificial zinc finger-type nuclease with cerium-binding peptide. Biochem Biophys Res Commun 330:247–252

    Article  CAS  PubMed  Google Scholar 

  • Neff KL, Argue DP, Ma AC, Lee HB, Clark KJ, Ekker SC (2013) Mojo Hand, a TALEN design tool for genome editing applications. BMC Bioinforma 14:1

    Article  CAS  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 

  • Rai N, Ferreiro A, Neckelmann A (2014) RiboTALE: a modular, inducible system for accurate gene expression control. Scientific Reports 5

  • Ramalingam S, Annaluru N, Kandavelou K, Chandrasegaran S (2014) TALEN-mediated generation and genetic correction of disease-specific human induced pluripotent stem cells. Curr Gene Ther 14:461–472

    Article  CAS  PubMed  Google Scholar 

  • Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE et al (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154(6):1380–1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rémy S, Tesson L, Ménoret S, U S Al C, Scharenberg AM, Anegon I (2010) Zinc-finger nucleases: a powerful tool for genetic engineering of animals. Transgenic Res 19:363–371

    Article  PubMed  CAS  Google Scholar 

  • Reyon D, Khayter C, Regan MR, Joung JK, Sander JD (2012) Engineering designer transcription activator‐‐like effector nucleases (TALENs) by REAL or REAL‐fast assembly. Curr Protoc Mol Biol. doi:10.1002/0471142727

    PubMed  PubMed Central  Google Scholar 

  • Richard GF, Viterbo D, Khanna V, Mosbach V, Castelain L, Dujon B (2014) Highly specific contractions of a single CAG/CTG trinucleotide repeat by TALEN in yeast. PLoS ONE. doi:10.1371/0095611

    Google Scholar 

  • Römer P, Hahn S, Jordan T, Strauß T, Bonas U, Lahaye T (2007) Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:645–648

    Article  PubMed  CAS  Google Scholar 

  • Römer P, Recht S, Lahaye T (2009) A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc Natl Acad Sci U S A 106:20526–20531

    Article  PubMed  PubMed Central  Google Scholar 

  • Rouet P, Smih F, Jasin M (1994) Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol 14:8096–8106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saijo Y, Schulze-Lefert P (2008) Manipulation of the eukaryotic transcriptional machinery by bacterial pathogens. Cell Host Microbe 4:96–99

    Article  CAS  PubMed  Google Scholar 

  • Sakuma T, Hosoi S, Woltjen K et al (2013) Efficient TALEN construction and evaluation methods for human cell and animal applications. Genes Cells 18:315–326

    Article  CAS  PubMed  Google Scholar 

  • Salanoubat M, Genin S, Artiguenave F et al (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497–502

    Article  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 JD, Maeder ML, Reyon D, Voytas DF, Joung JK, Dobbs D (2010) ZiFiT (Zinc Finger Targeter): an updated zinc finger engineering tool. Nucleic Acids Res gkq319

  • Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, Yeh JR (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29:697–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanjana NE, Cong L, Zhou Y, Cunniff MM, Feng G, Zhang F (2012) A transcription activator-like effector toolbox for genome engineering. Nat Protoc 7:171–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid-Burgk JL, Schmidt T, Kaiser V, Höning K, Hornung V (2013) A ligation-independent cloning technique for high-throughput assembly of transcription activator-like effector genes. Nat Biotechnol 31:76–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholze H, Boch J (2010) TAL effector-DNA specificity. Virulence 1:428–432

    Article  PubMed  Google Scholar 

  • Scholze H, Boch J (2011) TAL effectors are remote controls for gene activation. Curr Opin Microbiol 14:47–53

    Article  CAS  PubMed  Google Scholar 

  • Sera T (2005) Inhibition of virus DNA replication by artificial zinc finger proteins. J Virol 79:2614–2619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan Q, Wang Y, Chen K et al (2013) Rapid and efficient gene modification in rice and Brachypodium using TALENs. Mol Plant 6:1365–1368

    Article  CAS  PubMed  PubMed Central  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 Biotechnol J 13:791–800

    Article  CAS  PubMed  Google Scholar 

  • Shen B, Zhang W, Zhang J, Zhou J, Wang J, Chen L et al (2014) Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Methods 11(4):399–402

    Article  CAS  PubMed  Google Scholar 

  • Soldner F, Laganière J, Cheng AW et al (2011) Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146:318–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stadler LJ (1928) Mutations in barley induced by X-rays and radium. Science 68:186–187

    Article  CAS  PubMed  Google Scholar 

  • Stolzenburg S (2014) Epigenetic editing using programmable zinc ginger proteins: inherited silencing of endogenous gene expression by targeted DNA methylation. Dissertation, University of Groningen

  • Streubel J, Blücher C, Landgraf A, Boch J (2012) TAL effector RVD specificities and efficiencies. Nat Biotechnol 30:593–595

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Li N, Huang G et al (2013) Site‐specific gene targeting using transcription activator‐like effector (TALE)‐based nuclease in Brassica oleracea. J Integr Plant Biol 55:1092–1103

    Article  CAS  PubMed  Google Scholar 

  • Takada S, Sato T, Ito Y (2013) Targeted gene deletion of miRNAs in mice by TALEN system. PLoS ONE 8

  • Takenaka K, Koshino-Kimura Y, Aoyama Y, Sera T (2007). Inhibition of tomato yellow leaf curl virus replication by artificial zinc-finger proteins. In: Nucleic Acids Symposium Series (vol. 51, no. 1). Oxford University Press, pp 429–430

  • Tesson L, U S Al C, Ménoret S et al (2011) Knockout rats generated by embryo microinjection of TALENs. Nat Biotechnol 29:695–696

    Article  CAS  PubMed  Google Scholar 

  • Tong C, Huang G, Ashton C, Wu H, Yan H, Ying QL (2012) Rapid and cost-effective gene targeting in rat embryonic stem cells by TALENs. J Genet Genomics 39:275–280

    Article  CAS  PubMed  Google Scholar 

  • Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D et al (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32(6):569–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uhde-Stone C, Cheung E, Lu B (2014) TALE activators regulate gene expression in a position-and strand-dependent manner in mammalian cells. Biochem Biophys Res Commun 443:1189–1194

    Article  CAS  PubMed  Google Scholar 

  • Voytas DF (2013) Plant genome engineering with sequence-specific nucleases. Annu Rev Plant Biol 64:327–350

    Article  CAS  PubMed  Google Scholar 

  • Waltz E (2012) Tiptoeing around transgenics. Nat Biotechnol 30:215–217

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Li J, Huang H (2012) An integrated chip for the high‐throughput synthesis of transcription activator‐like effectors. Angew Chem Int Ed 124:8633–8636

    Article  Google Scholar 

  • Wang Y, Cheng X, Shan Q (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 X, Wang Y, Wu X et al (2015) Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nat Biotechnol 33:175–178

    Article  CAS  PubMed  Google Scholar 

  • Weber E, Gruetzner R, Werner S, Engler C, Marillonnet S (2011) Assembly of designer TAL effectors by golden gate cloning. PLoS ONE 6:e19722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wefers B, Panda SK, Ortiz O et al (2013) Generation of targeted mouse mutants by embryo microinjection of TALEN mRNA. Nat Protoc 8:2355–2379

    Article  CAS  PubMed  Google Scholar 

  • Wendt T, Holm PB, Starker CG et al (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 

  • Werner J, Gossen M (2014) Modes of TAL effector-mediated repression. Nucleic Acids Res gku1124

  • White FF, Potnis N, Jones JB, Koebnik R (2009) The type III effectors of Xanthomonas. Mol Plant Pathol 10:749–766

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y, Bliss J, Gerbi SA (2015) Whole organism genome editing: targeted large DNA insertion via ObLiGaRe Non homologous End-joining in vivo capture. G3: Genes| Genome| Genet 5(9):1843–1847

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang B, Zhu W, Johnson LB, White FF (2000) The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc Natl Acad Sci U S A 97:9807–9812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Yuan P, Wen D et al (2013) ULtiMATE system for rapid assembly of customized TAL effectors. PLoS ONE. doi:10.1371/journal.pone.0075649

    Google Scholar 

  • Yang J, Zhang Y, Yuan P et al (2014) Complete decoding of TAL effectors for DNA recognition. Cell Res 24:628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye L, Wang J, Beyer AI (2014) Seamless modification of wild-type induced pluripotent stem cells to the natural CCR5Δ32 mutation confers resistance to HIV infection. Proc Natl Acad Sci U S A 111:9591–9596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Cong L, Lodato S, Kosuri S, Church GM, Arlotta P (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat Biotechnol 29:149–153

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Zhang F, Li X (2013a) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol 161:20–27

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Xiang D, Heriyanto F, Gao Y, Qian Z, Wu WS (2013b) Dissecting the roles of miR-302/367 cluster in cellular reprogramming using TALE-based repressor and TALEN. Stem Cell Rep 1:218–225

    Article  CAS  Google Scholar 

  • Zhang H, Gou F, Zhang J et al (2015) TALEN‐mediated targeted mutagenesis produces a large variety of heritable mutations in rice. Plant Biotechnol J. doi:10.1111/12372

    Google Scholar 

  • Zhao X, Ni W, Chen C, Sai W, Qiao J, Sheng J (2016) Targeted editing of myostatin gene in sheep by transcription activator-like effector nucleases. Asian Australas J Anim Sci 29(3):413–418

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We are grateful to Higher Education Commission (HEC) Pakistan for provision of funds to conduct this research work. Zulqurnain Khan was also supported by HEC to work on virus suppression in cotton through TALEN technology.

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Authors and Affiliations

  1. Center of Agricultural Biochemistry and Biotechnology (CABB), University of Agriculture, Faisalabad, 38040, Pakistan

    Zulqurnain Khan & Muhammad Salman Mubarik

  2. US-Pakistan Center for Advanced Studies in Agriculture and Food Security (USPCAS-AFS), University of Agriculture, Faisalabad, 38040, Pakistan

    Sultan Habibullah Khan, Bushra Sadia & Aftab Ahmad

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  1. Zulqurnain Khan
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  2. Sultan Habibullah Khan
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  3. Muhammad Salman Mubarik
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  4. Bushra Sadia
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  5. Aftab Ahmad
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Correspondence to Aftab Ahmad.

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Khan, Z., Khan, S.H., Mubarik, M.S. et al. Use of TALEs and TALEN Technology for Genetic Improvement of Plants. Plant Mol Biol Rep 35, 1–19 (2017). https://doi.org/10.1007/s11105-016-0997-8

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