Scientific opinion addressing the safety assessment of plants developed using Zinc Finger Nuclease 3 and other Site‐Directed Nucleases with similar function
2012; Wiley; Volume: 10; Issue: 10 Linguagem: Inglês
10.2903/j.efsa.2012.2943
ISSN1831-4732
Tópico(s)Insect Resistance and Genetics
ResumoEFSA JournalVolume 10, Issue 10 2943 OpinionOpen Access Scientific opinion addressing the safety assessment of plants developed using Zinc Finger Nuclease 3 and other Site-Directed Nucleases with similar function EFSA Panel on Genetically Modified Organisms (GMO), EFSA Panel on Genetically Modified Organisms (GMO)Search for more papers by this author EFSA Panel on Genetically Modified Organisms (GMO), EFSA Panel on Genetically Modified Organisms (GMO)Search for more papers by this author First published: 25 October 2012 https://doi.org/10.2903/j.efsa.2012.2943Citations: 68 Panel members: Salvatore Arpaia, Andrew Nicholas Edmund Birch, Andrew Chesson, Patrick du Jardin, Achim Gathmann, Jürgen Gropp, Lieve Herman, Hilde-Gunn Hoen-Sorteberg, Huw Jones, Jozsef Kiss, Gijs Kleter, Pagona Lagiou, Martinus Lovik, Antoine Messéan, Hanspeter Naegeli, Kaare Magne Nielsen, Jaroslava Ovesna, Joe Perry, Nils Rostoks, Christoph Tebbe Correspondence: GMO@efsa.europa.eu Acknowledgement: The Panel wishes to thank the members of the Working Group on risk assessment of plants developed through new techniques: John Bradshaw, Josep Casacuberta, Andrew Chesson, Howard Davies, Frank Hartung, Sirpa Kärenlampi, Gijs Kleter, Harry Kuiper, Michele Morgante, Kaare Nielsen, Fabien Nogué, Annette Pöting, Pere Puigdomenech and Jeremy Sweet for the preparatory work on this scientific opinion; and EFSA staff: Andrea Gennaro, Yi Liu and Nancy Podevin for the scientific support provided to this scientific opinion and Nancy Podevin also for the preparation of the figures and coordination of the work. Adoption date: 18 October 2012 Published date: 25 October 2012 Question number: EFSA-Q-2012-00241 On request from: European Commission AboutPDF ToolsExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Abstract The European Commission requested that the EFSA Panel on Genetically Modified Organisms deliver a scientific opinion related to risk assessment of plants developed using the zinc finger nuclease 3 technique (ZFN-3) which allows the integration of gene(s) in a predefined insertion site in the genome of the recipient species. Since other nucleases with a similar function to ZFN are considered in this opinion the term site-directed nuclease 3 (SDN-3) is used to describe the technique rather than ZFN-3 specifically. The EFSA GMO Panel considers that its guidance documents are applicable for the evaluation of food and feed products derived from plants developed using the SDN-3 technique and for performing an environmental risk assessment. However, on a case-by-case basis lesser amounts of event specific data may be needed for the risk assessment of plants developed using the SDN-3 technique. The EFSA GMO Panel compared the hazards associated with plants produced by the SDN-3 technique with those obtained by conventional plant breeding techniques and by currently used transgenesis. With respect to the genes introduced, the SDN-3 technique does not differ from transgenesis or from the other genetic modification techniques currently used, and can be used to introduce transgenes, intragenes or cisgenes. The main difference between the SDN-3 technique and transgenesis is that the insertion of DNA is targeted to a predefined region of the genome. Therefore, the SDN-3 technique can minimise hazards associated with the disruption of genes and/or regulatory elements in the recipient genome. Whilst the SDN-3 technique can induce off-target changes in the genome of the recipient plant these would be fewer than those occurring with most mutagenesis techniques. Furthermore, where such changes occur they would be of the same types as those produced by conventional breeding techniques. References Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC and Ecker JR, 2003. Genome-wide Insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653– 657. Bai YL, Pavan S, Zheng Z, Zappel NF, Reinstadler A, Lotti C, De Giovanni C, Ricciardi L, Lindhout P, Visser R, Theres K and Panstruga R, 2008. Naturally occurring broad-spectrum powdery mildew resistance in a central American tomato accession is caused by loss of Mlo function. Molecular Plant-Microbe Interactions, 21, 30– 39. Bitinaite J, Wah DA, Aggarwal AK and Schildkraut I, 1998. FokI dimerization is required for DNA cleavage. Proceedings of the National Academy of Sciences of the United States of America, 95, 10570– 10575. Boch J and Bonas U, 2010. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual Review of Phytopathology, 48, 419– 436. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A and Bonas U, 2009. Breaking the Code of DNA Binding Specificity of TAL-Type III Effectors. Science, 326, 1509– 1512. Bogdanove AJ, Schornack S and Lahaye T, 2010. TAL effectors: finding plant genes for disease and defense. Current Opinion in Plant Biology, 13, 394– 401. Cai CQ, Doyon Y, Ainley WM, Miller JC, DeKelver RC, Moehle EA, Rock JM, Lee YL, Garrison R, Schulenberg L, Blue R, Worden A, Baker L, Faraji F, Zhang L, Holmes MC, Rebar EJ, Collingwood TN, Rubin-Wilson B, Gregory PD, Urnov FD and Petolino JF, 2009. Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Molecular Biology, 69, 699– 709. Cecchini E, Mulligan BJ, Covey SN and Milner JJ, 1998. Characterization of gamma irradiation-induced deletion mutations at a selectable locus in Arabidopsis. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 401, 199– 206. Ceoloni C, Forte P, Gennaro A, Micali S, Carozza R and Bitti A, 2005. Recent developments in durum wheat chromosome engineering. Cytogenetic and Genome Research, 109, 328– 334. Cornu TI, Thibodeau-Beganny S, Guhl E, Alwin S, Eichtinger M, Joung JK and Cathomen T, 2008. DNA-binding specificity is a major determinant of the activity and toxicity of zinc-finger nucleases. Molecular Therapy, 16, 352– 358. Curtin SJ, Voytas DF and Stupar RM, 2012. Genome Engineering of Crops with Designer Nucleases. Plant Genome, 5, 42– 50. D'Halluin K, Vanderstraeten C, Stals E, Cornelissen M and Ruiter R, 2008. Homologous recombination: a basis for targeted genome optimization in crop species such as maize. Plant Biotechnology Journal, 6, 93– 102. Dahmani-Mardas F, Troadec C, Boualem A, Leveque S, Alsadon AA, Aldoss AA, Dogimont C and Bendahmane A, 2010. Engineering melon plants with improved fruit shelf life using the TILLING approach. PloS one, 5, e15776. Dalmais M, Schmidt J, Le Signor C, Moussy F, Burstin J, Savois V, Aubert G, Brunaud V, de Oliveira Y, Guichard C, Thompson R and Bendahmane A, 2008. UTILLdb, a Pisum sativum in silico forward and reverse genetics tool. Genome Biology, 9. Davis L and Maizels N, 2011. DNA Nicks Promote Efficient and Safe Targeted Gene Correction. PloS one, 6, e23981. de Pater S, Neuteboom LW, Pinas JE, Hooykaas PJJ and van der Zaal BJ, 2009. UN-induced mutagenesis and gene-targeting in Arabidopsis through Agrobacterium-mediated floral dip transformation. Plant Biotechnology Journal, 7, 821– 835. Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD and Holmes MC, 2011. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nature Methods, 8, 74– 79. EFSA, 2010. Guidance on the environmental risk assessment of genetically modified plants. EFSA Journal, 8, 1879. EFSA, 2011. Guidance for risk assessment of food and feed from genetically modified plants. EFSA Journal, 9, 2150. EFSA, 2012. Scientific opinion addressing the safety assessment of plants developed through cisgenesis and intragenesis. The EFSA Journal, 10, 2561. Evans DA, 1983. Agricultural applications of plant protoplast fusion. Bio-Technology, 1, 253– 261. Evans DA, 1989. Somaclonal variation - genetic-basis and breeding applications. Trends in Genetics, 5, 46– 50. Fajardo-Sanchez E, Stricher F, Paques F, Isalan M and Serrano L, 2008. Computer design of obligate heterodimer meganucleases allows efficient cutting of custom DNA sequences. Nucleic Acids Research, 36, 2163– 2173. Fauser F, Roth N, Pacher M, Ilg G, Sanchez-Fernandez R, Biesgen C and Puchta H, 2012. In planta gene targeting. Proceedings of the National Academy of Sciences of the United States of America, 109, 7535– 7540. Fedak G, 1999. Molecular aids for integration of alien chromatin through wide crosses. Genome, 42, 584– 591. Fonfara I, Curth U, Pingoud A and Wende W, 2012. Creating highly specific nucleases by fusion of active restriction endonucleases and catalytically inactive homing endonucleases. Nucleic Acids Research, 40, 847– 860. Friedburg EC, Walker GC, Siede W, Wood RD, Schultz RA and Ellenberger T, 2006. DNA repair and mutagenesis ( 2nd ed.). ASM Press, Washington, DC, 1118 pp. Gabriel R, Lombardo A, Arens A, Miller JC, Genovese P, Kaeppel C, Nowrouzi A, Wang J, Friedman G, Holmes MC, Gregory PD, Glimm H, Schmidt M, Naldini L and von Kalle C, 2011. Genome-Wide Determination of Double-Strand Breaks reveals High Specificity of Zinc Finger Nucleases. Human Gene Therapy, 21, 1371– 1371. Gennaro A, Forte P, Carozza R, Sardaro MLS, Ferri D, Bitti A, Borrelli GM, D'Egidio MG and Ceoloni C, 2007. Pyramiding different alien chromosome segments in durum wheat: Feasibility and breeding potential. Israel Journal of Plant Sciences, 55, 267– 276. Glick BR and Pasternak JJ, 2003. Molecular biotechnology: principles and applications of recombinant DNA. Ed BRPJJ Glick. 1000 pp. Glimelius K, Fahlesson J, Landgren M, Sjodin C and Sundberg E, 1991. Gene-transfer via somatic hybridization in plants. Trends in Biotechnology, 9, 24– 30. Gonçalves MAFV, van Nierop GP, Holkers M and de Vries AAF, 2012. Concerted nicking of donor and chromosomal acceptor DNA promotes homology-directed gene targeting in human cells. Nucleic Acids Research, 40, 3443– 3455. Gorbunova V and Levy AA, 1999. How plants make ends meet: DNA double-strand break repair. Trends in Plant Science, 4, 263– 269. Greene EA, Codomo CA, Taylor NE, Henikoff JG, Till BJ, Reynolds SH, Enns LC, Burtner C, Johnson JE, Odden AR, Comai L and Henikoff S, 2003. Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics, 164, 731– 740. Grizot S, Epinat JC, Thomas S, Duclert A, Rolland S, Pâques F and Duchateau P, 2010. Generation of redesigned homing endonucleases comprising DNA-binding domains derived from two different scaffolds. Nucleic Acids Research, 38, 2006– 2018. Händel EM, Alwin S and Cathomen T, 2009. Expanding or Restricting the Target Site Repertoire of Zinc-finger Nucleases: The Inter-domain Linker as a Major Determinant of Target Site Selectivity. Molecular Therapy, 17, 104– 111. Heacock M, Spangler E, Riha K, Puizina J and Shippen DE, 2004. Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO Journal, 23, 2304– 2313. Huang P, Xiao A, Zhou M, Zhu Z, Lin S and Zhang B, 2011. Heritable gene targeting in zebrafish using customized TALENs. Nature Biotechnology, 29, 699– 700. Isalan M and Choo Y, 2001. Rapid, high-throughput engineering of sequence-specific zinc finger DNA-binding proteins. Methods in Enzymology, 340, 593– 609. Janick J, 2004. Genetic alterations associated with the origins of fruit culture. In: Acta Horticulturae. Eds F Laurens, K Evans, 683– 691. Jiang C, Mithani A, Gan X, Belfield EJ, Klingler JP, Zhu J-K, Ragoussis J, Mott R and Harberd NP, 2011. Regenerant Arabidopsis Lineages Display a Distinct Genome-Wide Spectrum of Mutations Conferring Variant Phenotypes. Current Biology, 21, 1385– 1390. Kay S, Hahn S, Marois E, Hause G and Bonas U, 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science, 318, 648– 651. Kazama Y, Hirano T, Saito H, Liu Y, Ohbu S, Hayashi Y and Abe T, 2011. Characterization of highly efficient heavy-ion mutagenesis in Arabidopsis thaliana. BMC Plant Biology, 11, 161. Khrustaleva LI and Kik C, 2000. Introgression of Allium fistulosum into A-cepa mediated by A-roylei. Theoretical and Applied Genetics, 100, 17– 26. Kim JS, Lee HJ and Carroll D, 2010. Genome editing with modularly assembled zinc-finger nucleases. Nature Methods, 7, 91– 91. Kim YG, Cha J and Chandrasegaran S, 1996. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proceedings of the National Academy of Sciences of the United States of America, 93, 1156– 1160. Knoll JE, Ramos ML, Yajuan Z, Holbrook CC, Chow M, Sixue C, Maleki S, Anjanabha B and Ozias-Akins P, 2011. TILLING for allergen reduction and improvement of quality traits in peanut (Arachis hypogaea L.). BMC Plant Biology, 11. Krieg DR, 1963. Ethyl methanesulfonate-induced reversion of bacteriophage T4rII mutants. Genetics, 48, 561– 580. Krieger U, Lippman ZB and Zamir D, 2010. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nature Genetics, 42, 459– U138. Laity JH, Lee BM and Wright PE, 2001. Zinc finger proteins: new insights into structural and functional diversity. Current Opinion in Structural Biology, 11, 39– 46. Larkin PJ and Scowcroft WR, 1981. Somaclonal variation - a novel source of variability from cell-cultures for plant improvement. Theoretical and Applied Genetics, 60, 197– 214. Lawrence E, 1995. Henderson's Dictionary of Biological Terms. 11th Edition, Wiley-Liss, Li X, Song Y, Century K, Straight S, Ronald P, Dong X, Lassner M and Zhang Y, 2001. A fast neutron deletion mutagenesis-based reverse genetics system for plants. The Plant Journal, 27, 235– 242. Liu JH, Xu XY and Deng XX, 2005. Intergeneric somatic hybridization and its application to crop genetic improvement. Plant Cell Tissue and Organ Culture, 82, 19– 44. Lukaszewski AJ, 2000. Manipulation of the 1RS.1BL translocation in wheat by induced homoeologous recombination. CropScience, 40, 216– 225. Lynch PT, Davey MR and Power JB, 1993. Plant protoplast fusion and somatic hybridization. Methods in Enzymology, 221, 379– 393. Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM, Eichtinger M, Jiang T, Foley JE, Winfrey RJ, Townsend JA, Unger-Wallace E, Sander JD, Muller-Lerch F, Fu FL, Pearlberg J, Gobel C, Dassie JP, Pruett-Miller SM, Porteus MH, Sgroi DC, Iafrate AJ, Dobbs D, McCray PB, Cathomen T, Voytas DF and Joung JK, 2008. Rapid "Open-Source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Molecular Cell, 31, 294– 301. Mandell JG and Barbas CF, 2006. Zinc Finger Tools: custom DNA-binding domains for transcription factors and nucleases. Nucleic Acids Research, 34, W516 - 523. Mathias R, Espinosa S and Robbelen G, 1990. A new embryo rescue procedure for interspecific hybridization. Plant Breeding, 104, 258– 261. Mauseth J, 1991. Botany, An introduction to Plant Biology. Ed SC Publishing. 672 pp. McCallum CM, Comai L, Greene EA and Henikoff S, 2000. Targeting induced local lesions in genomes (TILLING) for plant functional genomics. Plant Physiology, 123, 439– 442. McConnell Smith A, Takeuchi R, Pellenz S, Davis L, Maizels N, Monnat RJ, Jr. and Stoddard BL, 2009. Generation of a nicking enzyme that stimulates site-specific gene conversion from the I-AniI LAGLIDADG homing endonuclease. Proceedings of the National Academy of Sciences of the United States of America, 106, 5099– 5104. Men AE, Laniya TS, Searle IR, Iturbe-Ormaetxe I, Gresshoff I, Jiang Q, Carroll BJ and Gresshoff PM, 2002. Fast Neutron Mutagenesis of Soybean (Glycine soja L.) Produces a Supernodulating Mutant Containing a Large Deletion in Linkage Group H. Genome Letters, 1, 147– 155. Metzger MJ, McConnell-Smith A, Stoddard BL and Miller AD, 2011. Single-strand nicks induce homologous recombination with less toxicity than double-strand breaks using an AAV vector template. Nucleic Acids Research, 39, 926– 935. Miller JC, Holmes MC, Wang JB, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA, Gregory PD, Pabo CO and Rebar EJ, 2007. An improved zinc-finger nuclease architecture for highly specific genome editing. Nature Biotechnology, 25, 778– 785. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E and Hinkley SJ, 2011. A TALE nuclease architecture for efficient genome editing. Nature Biotechnology, 29, 143 - 148. Minczuk M, Papworth MA, Miller JC, Murphy MP and Klug A, 2008. Development of a single-chain, quasi-dimeric zinc-finger nuclease for the selective degradation of mutated human mitochondrial DNA. Nucleic Acids Research, 36, 3926– 3938. Mino T, Aoyama Y and Sera T, 2009. Efficient double-stranded DNA cleavage by artificial zinc-finger nucleases composed of one zinc-finger protein and a single-chain FokI dimer. Journal of Biotechnology, 140, 156– 161. Miyajima D, 2006. Ovules that failed to form seeds in zinnia (Zinnia violacea Cav.). Scientia Horticulturae, 107, 176– 182. Miyao A, Nakagome M, Ohnuma T, Yamagata H, Kanamori H, Katayose Y, Takahashi A, Matsumoto T and Hirochika H, 2012. Molecular Spectrum of Somaclonal Variation in Regenerated Rice Revealed by Whole-Genome Sequencing. Plant and Cell Physiology, 53, 256– 264. Morbitzer R, Romer P, Boch J and Lahaye T, 2010. Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. Proceedings of the National Academy of Sciences of the United States of America, 107, 21617– 21622. Morgante M, De Paoli E and Radovic S, 2007. Transposable elements and the plant pan-genomes. Current Opinion in Plant Biology, 10, 149– 155. Morita R, Kusaba M, Iida S, Yamaguchi H, Nishio T and Nishimura M, 2009. Molecular characterization of mutations induced by gamma irradiation in rice. Genes & Genetic Systems, 84, 361– 370. Moscou MJ and Bogdanove AJ, 2009. A simple cipher governs DNA recognition by TAL effectors. Science, 326, 1501. Ossowski S, Schneeberger K, Lucas-Lledo JI, Warthmann N, Clark RM, Shaw RG, Weigel D and Lynch M, 2010. The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana. Science, 327, 92– 94. Pâques F and Duchateau P, 2007. Meganucleases and DNA double-strand break-induced recombination: Perspectives for gene therapy. Current Gene Therapy, 7, 49– 66. Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B and Grandbastien MA, 2010. Impact of transposable elements on the organization and function of allopolyploid genomes. The New phytologist, 186, 37– 45. Pattanayak V, Ramirez CL, Joung JK and Liu DR, 2011. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nature Methods, 8, 765– U115. Piron F, Nicolaï M, Minoïa S, Piednoir E, Moretti A, Salgues A, Zamir D, Caranta C and Bendahmane A, 2010. An Induced Mutation in Tomato eIF4E Leads to Immunity to Two Potyviruses. PloS one, 5, e11313. Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D and Lifschitz E, 1998. The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development, 125, 1979– 1989. Puchta H, 2003. Towards the ideal GMP: Homologous recombination and marker gene excision. Journal of Plant Physiology, 160, 743– 754. Puchta H, Dujon B and Hohn B, 1996. Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proceedings of the National Academy of Sciences, USA, 93, 5055– 5060. Rabinovich SV, 1998. Importance of wheat-rye translocations for breeding modern cultivars of Triticum aestivum L. (Reprinted from Wheat: Prospects for global improvement, 1998). Euphytica, 100, 323– 340. Ramirez CL, Certo MT, Mussolino C, Goodwin MJ, Cradick TJ, McCaffrey AP, Cathomen T, Scharenberg AM and Joung JK, 2012. Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects. Nucleic Acids Research, 40, 5560– 5568. Reed SM, 2005. Embryo rescue. Plant Development and Biotechnology, 235– 239. Rieger R, Michaelis A and Green MM, 1968. A glossary of genetics and cytogenetics. Classical and molecular. Springer, 652 pp. Römer P, Hahn S, Jordan T, Strauß T, Bonas U and Lahaye T, 2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science, 318, 645– 648. Rosen LE, Morrison HA, Masri S, Brown MJ, Springstubb B, Sussman D, Stoddard BL and Seligman LM, 2006. Homing endonuclease I-CreI derivatives with novel DNA target specificities. Nucleic Acids Research, 34, 4791– 4800. Salomon S and Puchta H, 1998. Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO Journal, 17, 6086– 6095. Schierling B, Dannemann N, Gabsalilow L, Wende W, Cathomen T and Pingoud A, 2012. A novel zinc-finger nuclease platform with a sequence-specific cleavage module. Nucleic Acids Research, 40, 2623– 2638. Sears ER, 1956. The transfer of leaf-rust resistance from Aegilops umbellulata to wheat. In: Genetics in plant breeding. Brook-haven Symposia in Biology 1956., 1– 22. Seligman LM, Chevalier BS, Chadsey MS, Edwards ST, Savage JH and Veillet AL, 2002. Mutations altering the cleavage specificity of a homing endonuclease. Nucleic Acids Research, 30, 3870– 3879. Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng XD, Choi VM, Rock JM, Wu YY, Katibah GE, Zhifang G, McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregory PD and Urnov FD, 2009. Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature, 459, 437– U156. Sikora P, Chawade A, Larsson M, Olsson J and Olsson O, 2011. Mutagenesis as a tool in plant genetics, functional genomics, and breeding. International Journal of Plant Genomics, 2011, 314829. Sollu C, Pars K, Cornu TI, Thibodeau-Beganny S, Maeder ML, Joung JK, Heilbronn R and Cathomen T, 2010. Autonomous zinc-finger nuclease pairs for targeted chromosomal deletion. Nucleic Acids Research, 38, 8269– 8276. Stewart JM, 1981. In vitro fertilization and embryo rescue. Environmental and Experimental Botany, 21, 301– 315. Stoddard BL, 2011. Homing Endonucleases: From Microbial Genetic Invaders to Reagents for Targeted DNA Modification. Structure, 19, 7– 15. Streubel J, Blucher C, Landgraf A and Boch J, 2012. TAL effector RVD specificities and efficiencies. Nature Biotechnology, 30, 593– 595. Suzuki T, Eiguchi M, Kumamaru T, Satoh H, Matsusaka H, Moriguchi K, Nagato Y and Kurata N, 2008. MNU-induced mutant pools and high performance TILLING enable finding of any gene mutation in rice. Molecular Genetics and Genomics, 279, 213– 223. Swanson-Wagner RA, Eichten SR, Kumari S, Tiffin P, Stein JC, Ware D and Springer NM, 2010. Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Research, 20, 1689– 1699. Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ and Cathomen T, 2007. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nature Biotechnology, 25, 786– 793. Szybalski W, Kim SC, Hasan N and Podhajska AJ, 1991. Class-IIS restriction enzymes-a review. Gene, 100, 13– 26. Tanaka S, Ishii C, Hatakeyama S and Inoue H, 2010. High efficient gene targeting on the AGAMOUS gene in an Arabidopsis AtLIG4 mutant. Biochemical and Biophysical Research Communications, 396, 289– 293. Tanksley SD and McCouch SR, 1997. Seed banks and molecular maps: unlocking genetic potential from the wild. Science, 277, 1063– 1066. Tzfira T, Frankman LR, Vaidya M and Citovsky V, 2003. Site-specific integration of Agrobacterium tumefaciens T-DNA via double-stranded intermediates. Plant Physiology, 133, 1011– 1023. Tzfira T, Weinthal D, Marton I, Zeevi V, Zuker A and Vainstein A, 2012. Genome modifications in plant cells by custom-made restriction enzymes. Plant Biotechnology Journal, 10, 373– 389. Urnov FD, Rebar EJ, Holmes MC, Zhang HS and Gregory PD, 2010. Genome editing with engineered zinc finger nucleases. Nature Reviews Genetics, 11, 636– 646. van der Wiel C, Schaart J, Niks R and Visser R (Wageningen UR Plant Breeding), 2010. Traditional plant breeding methods. Report 338, Available from edepot.wur.nl/141713. Van Eijk JP, Raamsdonk LWD, Eikenboom W and R.J. B, 1991. Interspecific crosses between Tulipa gesneriana cultivars and wild Tulipa species: a survey. Sexual Plant Reproduction, 4, 1– 5. Wang B and Chee PW, 2010. Application of advanced backcross quantitative trait locus (QTL) analysis in crop improvement. Journal of Plant Breeding and CropScience, 2, 221– 232. Wang J, Friedman G, Doyon Y, Wang NS, Li CJ, Miller JC, Hua KL, Yan JJ, Babiarz JE, Gregory PD and Holmes MC, 2012. Targeted gene addition to a predetermined site in the human genome using a ZFN-based nicking enzyme. Genome Research, 22, 1316– 1326. Waterworth WM, Drury GE, Bray CM and West CE, 2011. Repairing breaks in the plant genome: the importance of keeping it together. New Phytologist, 192, 805– 822. Wright DA, Townsend JA, Winfrey RJ, Irwin PA, Rajagopal J, Lonosky PM, Hall BD, Jondle MD and Voytas DF, 2005. High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant Journal, 44, 693– 705. Yaakov B and Kashkush K, 2011. Methylation, transcription, and rearrangements of transposable elements in synthetic allopolyploids. International Journal of Plant Genomics, 2011, 569826. Young JM, Kuykendall LD, Martinez-Romero E, Kerr A and Sawada H, 2001. A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R-rhizogenes, R-rubi, R-undicola and R-vitis. International Journal of Systematic and Evolutionary Microbiology, 51, 89– 103. Zhao H, Hiroi T, Hansen BS and Rade JJ, 2009. Cyclic stretch induces cyclooxygenase-2 gene expression in vascular endothelial cells via activation of nuclear factor kappa-beta. Biochemical and Biophysical Research Communications, 389, 599– 601. Citing Literature Volume10, Issue10October 20122943 ReferencesRelatedInformation
Referência(s)