Skip to main content
SpringerLink
Log in
Book cover

Biosafety of Forest Transgenic Trees pp 31–66Cite as

New Transformation Technologies for Trees

  • Chapter
  • First Online:

Part of the book series: Forestry Sciences ((FOSC,volume 82))

Abstract

Application of transgenic techniques to trees has emerged as a powerful tool for their genetic improvement. However, for some recalcitrant or transformation time-consuming species transgenic research should be strengthened and further efforts will be necessary to improve regeneration and transformation efficiencies. This review focuses on the recent advances and techniques for genetic manipulation that can be applied to obtain transgenic trees with enhanced biosafety. After selection of transformed plants, marker genes presence becomes useless and undesirable. For generation of marker-free transgenic plants or resolving complex transgene integration structures, several methodologies based on site-specific recombination have been developed. Precise homologous recombination-mediated integration of a DNA sequence of interest at a particular site within a genome is the ultimate tool for genetic engineering. Genome editing allows a much more precise manipulation of tree genomes. Expression of multiple transgenes is often required for engineering metabolic pathways. Recent progress has made powerful techniques available and gene stacking can be achieved in trees by two methodologies: co-transformation and serial transformation. The application of technologies based on small RNAs allowing silencing target genes (RNA interference, artificial microRNAs, and artificial trans-acting siRNAs) is of particular interest to produce directed down-regulation of target genes in tree species. Mixing of genetic materials between species that cannot hybridize by natural means is one of the major criticisms to transgenic crops. Cisgenesis and intragenesis were developed as alternatives to transgenesis.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Agrawal PK, Kohli A, Twyman RM, Christou P (2005) Transformation of plants with multiple cassettes generates simple transgene integration patterns and high expression levels. Mol Breed 16:247–260

    Article  CAS  Google Scholar 

  • Ainley WM, Sastry-Dent L, Welter ME, Murray MG, Zeitler B, Amora R, Corbin DR, Miles RR, Arnold NL, Strange TL, Simpson MA, Cao Z, Carroll C, Pawelczak KS, Blue R, West K, Rowland LM, Perkins D, Samuel P, Dewes CM, Shen L, Sriram S, Evans SL, Rebar EJ, Zhang L, Gregory PD, Urnov FD, Webb SR, Petolino JF (2013) Trait stacking via targeted genome editing. Plant Biotechnol J 11:1126–1134

    Article  CAS  PubMed  Google Scholar 

  • Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ballester A, Cervera M, Peña L (2007) Efficient production of transgenic Citrus plants using isopentenyl transferase positive selection and removal of the marker gene by site-specific recombination. Plant Cell Rep 26:39–45

    Article  CAS  PubMed  Google Scholar 

  • Ballester A, Cervera M, Peña L (2008) Evaluation of selection strategies alternative to nptII in genetic transformation of citrus. Plant Cell Rep 27:1005–1015

    Article  CAS  PubMed  Google Scholar 

  • Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436

    Article  CAS  PubMed  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 

  • 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, Shendure J, Stoddard BL, Certo MT, Baker D, Scharenberg AM (2014) megaTALs: a rare-cleaving nuclease architecture for therapeutic genome engineering. Nucleic Acids Res 42:2591–2601

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:28.1–28.31

    Google Scholar 

  • Breyer D, Kopertekh L, Dirk R (2014) Alternatives to antibiotic resistance marker genes for in vitro selection of genetically modified plants. Scientific developments, current use, operational access and biosafety considerations. Critical Rev Plant Sci 33(4):286–330

    Article  CAS  Google Scholar 

  • Brunet E, Simsek D, Tomishima M, DeKelver R, Choi VM, Gregory P, Urnov F, Weinstock DM, Jasin M (2009) Chromosomal translocations induced at specified loci in human stem cells. Proc Natl Acad Sci USA 106:10620–12625

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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, Petolino JF (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol 69:699–709

    Article  CAS  PubMed  Google Scholar 

  • Carbonell A, Takeda A, Fahlgren N, Johnson SC, Cuperus JT, Carrington JC (2014) New generation of artificial microRNA and synthetic trans-acting small interfering RNA vectors for efficient gene silencing in Arabidopsis. Plant Physiol. doi:10.1104/pp.113.234989

    PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed Central  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 39:e82

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen K, Shan Q, Gao C (2014) An efficient TALEN mutagenesis system in rice. Methods. doi:10.1016/j.ymeth.2014.02.013

    PubMed Central  Google Scholar 

  • Chilton MDM, Que Q (2003) Targeted integration of T-DNA into the tobacco genome at double-stranded breaks: new insights on the mechanism of T-DNA integration. Plant Physiol 133:956–965

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chong-Pérez B, Reyes M, Rojas L, Ocaña B, Ramos A, Kosky RG, Angenon G (2013) Excision of a selectable marker gene in transgenic banana using a Cre/lox system controlled by an embryo specific promoter. Plant Mol Biol 83:143–152

    Article  PubMed  CAS  Google Scholar 

  • Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chuang CF, Meyerowitz EM (2000) Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:4985–4990

    Article  PubMed Central  CAS  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Cuellar W, Gaudin A, Solórzano D, Casas A, Ñopo L, Chudalayandi P, Medrano G, Kreuze J, Ghislain M (2006) Self-excision of the antibiotic resistance gene nptII using a heat inducible Cre-loxP system from transgenic potato. Plant Mol Biol 62:71–83

    Article  CAS  PubMed  Google Scholar 

  • Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C, Baltes NJ, Reyon D, Dahlborg EJ, Goodwin MJ, Coffman AP, Dobbs D, Joung JK, Voytas DF, Supar RM (2011) Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol 156:466–473

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • D’Halluin K, Ruiter R (2013) Directed genome engineering for genome optimization. Int J Dev Biol 57:621–627

    Article  PubMed  CAS  Google Scholar 

  • D’Halluin K, Vanderstraeten C, Stals E, Cornelissen M, Ruiter R (2008) Homologous recombination: a basis for targeted genome optimization in crop species such as maize. Plant Biotechnol J 6:93–102

    PubMed  Google Scholar 

  • Dale EC, Ow DW (1991) Gene-transfer with subsequent removal of the selection gene from the host genome. P Natl Acad Sci USA 88:10558–10562

    Article  CAS  Google Scholar 

  • Davis L, Maizels N (2011) DNA nicks promote efficient and safe targeted gene correction. PLoS ONE 6:e23981

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Day CD, Lee E, Kobayashi J, Holappa LD, Albert H, Ow DW (2000) Transgene integration into the same chromosome location can produce alleles that express at a predictable level, or alleles that are differentially silenced. Gene Dev 14:2869–2880

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Felippes FF, Wang JW, Weigel D (2012) MIGS: miRNA-induced gene silencing. Plant J 70:541–547

    Article  PubMed  CAS  Google Scholar 

  • De Lange O, Binder A, Lahaye T (2014) From dead leaf, to new life: TAL effectors as tools for synthetic biology. Plant J 78(5):753–771

    Article  PubMed  CAS  Google Scholar 

  • De Pater S, Neuteboom LW, Pinas JE, Hooykaas PJJ, van der Zaal BJ (2009) ZFN-induced mutagenesis and gene-targeting in Arabidopsis through Agrobacterium-mediated floral dip transformation. Plant Biotechnol J 7:821–835

    Article  PubMed  CAS  Google Scholar 

  • Dhekney SA, Li ZT, Gray DJ (2011) Grapevines engineered to express cisgenic Vitis vinifera thaumatin-like protein exhibit fungal disease resistance. In Vitro Cell Dev Plant 47:458–466

    Article  CAS  Google Scholar 

  • Djukanovic V, Smith J, Lowe K, Yang M, Gao H, Jones S, Nicholson MG, West A, Lape J, Bidney D, Falco SC, Jantz D, Lyznik LA (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 

  • Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC (2011) Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Methods 8:74–79

    Article  CAS  PubMed  Google Scholar 

  • Du J, Mansfield SD, Groover AT (2009) The Populus homeobox gene ARBORKNOX2 regulates cell differentiation during secondary growth. Plant J 60:1000–1014

    Article  CAS  PubMed  Google Scholar 

  • Dutt M, Li ZT, Dhekney SA, Gray DJ (2008) A co-transformation system to produce transgenic grapevines free of marker genes. Plant Sci 175:423–430

    Article  CAS  Google Scholar 

  • EFSA Panel on GMO (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

    Google Scholar 

  • Erikson O, Hertzberg M, Näsholm T (2004) A conditional marker gene allowing both positive and negative selection in plants. Nat Biotechnol 22:455–458

    Article  CAS  PubMed  Google Scholar 

  • Even-Faitelson L, Samach A, Melamed-Bessudo C, Avivi-Ragolsky N, Levy A (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 

  • 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) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA 111:4632–4637

    Article  PubMed Central  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Fladung M, Becker D (2010) Targeted integration and removal of transgenes in hybrid aspen (Populus tremula L. x P. tremuloides Michx.) using site-specific recombination systems. Plant Biol 12:334–340

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:822–826

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK (2014) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32:279–284

    Article  PubMed Central  CAS  PubMed  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 

  • Gambley RL, Ford R, Smith GR (1993) Microprojectile transformation of sugarcane meristems and regeneration of shoots expressing B-Glucuronidase. Plant Cell Rep 12:343–346

    Article  CAS  PubMed  Google Scholar 

  • García-Almodovar RC, Petri C, Padilla IMG, Burgos L (2014) Combination of site-specific recombination and a conditional selective marker gene allows for the production of marker-free tobacco plants. Plant Cell Tiss Organ Cult 116:205–215

    Article  CAS  Google Scholar 

  • Ghosh Z, Mallick B (2012) Renaissance of the regulatory RNAs. In: Mallick B (ed) Regulatory RNAs. Springer, Berlin. doi:10.1007/978-3-642-22517-8_1

    Google Scholar 

  • Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, Lim WA, Weissman JS, Qi LS (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gottfried P, Lotan O, Kolot M, Maslenin L, Bendov R, Gorovits R, Yesodi V, Yagil E, Rosner A (2005) Site-specific recombination in Arabidopsis plants promoted by the Integrase protein of coliphage HK022. Plant Mol Biol 57:435–444

    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 

  • Grindley NDF, Whiteson KL, Rice PA (2006) Mechanisms of site-specific recombination. Annu Rev Biochem 75:567–605

    Article  CAS  PubMed  Google Scholar 

  • Guilinger JP, Pattanayak V, Reyon D, Tsai SQ, Sander JD, Joung JK, Liu DR (2014a) Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity. Nat Methods 11:429–435

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guilinger JP, Thompson DB, Liu DR (2014b) Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32:577–582

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guo J, Morrell-Falvey JL, Labbé JL, Muchero W, Kalluri UC, Tuskan GA, Chen JG (2012) Highly efficient isolation of Populus mesophyll protoplasts and its application in transient expression assays. PLoS ONE 7:e44908

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gutiérrez-Nava ML, Aukerman MJ, Sakai H, Tingey S, Williams RW (2008) Artificial trans-acting siRNAs confer consistent and effective gene silencing. Plant Physiol 147:543–551

    Article  CAS  Google Scholar 

  • Hafez M, Hausner G (2012) Homing endonucleases: DNA scissors on a mission. Genome 55:553–569

    Article  CAS  PubMed  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    Article  CAS  PubMed  Google Scholar 

  • Han KH, Wilbert S, Perkins EJ, Gordon MP (1992) Development of transgenic trees for use in removal and detoxification of chemical wastes. In: Proceedings of IUFRO working party S2.04.06 workshop “Molecular Biology of Forest Trees”, Carcans-Maubuisson, France

    Google Scholar 

  • Hanin M, Paszkowski J (2003) Plant genome modification by homologous recombination. Curr Opin Plant Biol 6:157–162

    Article  CAS  PubMed  Google Scholar 

  • Hare PD, Chua NH (2002) Excision of selectable marker genes from transgenic plants. Nat Biotechnol 20:575–580

    Article  CAS  PubMed  Google Scholar 

  • Hartung F, Schiemann J (2013) Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J 78:742–752

    Article  CAS  Google Scholar 

  • Hauser F, Chen W, Deinlein U, Chang K, Ossowski S, Fitz J, Hannon GJ, Schroeder JI (2013) A genomic-scale artificial microRNA library as a tool to investigate the functionally redundant gene space in Arabidopsis. Plant Cell 25:2848–2863

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Herzog K, Flachowsky H, Deising HB, Hanke MV (2012) Heat-shock-mediated elimination of the nptII marker gene in transgenic apple (Malus × domestica Borkh). Gene 498:41–49

    Article  CAS  PubMed  Google Scholar 

  • Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31:827–832

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jia H, Pang Y, Chen X, Fang R (2006) Removal of the selectable marker gene from transgenic tobacco plants by expression of Cre recombinase from a tobacco mosaic virus vector through agroinfection. Transgenic Res 15:375–384

    Article  CAS  PubMed  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 41:e188

    Article  PubMed Central  CAS  PubMed  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 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  CAS  PubMed  Google Scholar 

  • Joshi SG, Schaart JG, Groenwold R, Jacobsen E, Schouten HJ, Krens FA (2011) Functional analysis and expression profiling of HcrVf1 and HcrVf2 for development of scab resistant cisgenic and intragenic apples. Plant Mol Biol 75:579–591

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kanwar K, Bhardwaj A, Agarwal S, Sharma DR (2003) Genetic transformation of Robinia pseudoacacia by Agrobacterium tumefaciens. Indian J Exp Biol 41:149–153

    CAS  PubMed  Google Scholar 

  • Katz SS, Gimble FS, Storici F (2014) To nick or not to nick: comparison of I-SceI single- and double-strand break-induced recombination in yeast and human cells. PLoS ONE 9:e88840

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kilby NJ, Davies GJ, Snaith MR, Murray JAH (1995) FLP recombinase in transgenic plants: constitutive activity in stably transformed tobacco and generation of marked cell clones in Arabidopsis. Plant J 8:637–652

    Article  CAS  PubMed  Google Scholar 

  • Kleinstiver BP, Wolfs JM, Kolaczyk T, Roberts AK, Hu SX, Edgell DR (2012) Monomeric site-specific nucleases for genome editing. Proc Natl Acad Sci USA 109:8061–8066

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klevebring D, Street NR, Fahlgren N, Kasschau KD, Carrington JC, Lundeberg J, Jansson S (2009) Genome-wide profiling of populus small RNAs. BMC Genom 10:620

    Article  CAS  Google Scholar 

  • Kopertekh L, Schiemann J (2005) Agroinfiltration as a tool for transient expression of cre recombinase in vivo. Transgenic Res 14:793–798

    Article  CAS  PubMed  Google Scholar 

  • Kopertekh L, Schulze K, Frolov A, Strack D, Broer I, Schiemann J (2010) Cre-mediated seed-specific transgene excision in tobacco. Plant Mol Biol 72:597–605

    Article  CAS  PubMed  Google Scholar 

  • Le Roux JJ, Staden JV (1991) Micropropagation and tissue culture of Eucalyptus-a review. Tree Physiol 9:435–477

    Article  PubMed  Google Scholar 

  • Lee HJ, Kweon J, Kim E, Kim S, Kim J (2012) Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res 22:539–548

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li ZS, Xing AQ, Moon BP, Burgoyne SA, Guida AD, Liang HL, Lee C, Caster CS, Barton JE, Klein TM, Falco SC (2007) A Cre/loxP-mediated self-activating gene excision system to produce marker gene free transgenic soybean plants. Plant Mol Biol 65:329–341

    Article  CAS  PubMed  Google Scholar 

  • Li J, Brunner AM, Shevchenco O, Meilan R, Ma C, Skinner JS, Strauss SH (2008) Efficient and stable transgene suppression via RNAi in field-grown poplars. Transgenic Res 17:679–694

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Li JF, Zhang D, Sheen J (2014a) Epitope-tagged protein-based artificial miRNA screens for optimized gene silencing in plants. Nat Protoc 9:939–949

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    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 

  • Lippman Z, Martienssen R (2004) The role of RNA interference in heterochromatic silencing. Nature 431:364–370

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Chen YQ (2010) A new mechanism in plant engineering: The potential roles of microRNAs in molecular breeding for crop improvement. Biotechnol Adv 28:301–307

    Article  CAS  PubMed  Google Scholar 

  • Liu HK, Yang C, Wei ZM (2005) Heat shock-regulated site-specific excision of extraneous DNA in transgenic plants. Plant Sci 168:997–1003

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • López-Noguera S, Petri C, Burgos L (2009) Combining a regeneration-promoting gene and site-specific recombination allows a more efficient apricot transformation and the elimination of marker genes. Plant Cell Rep 28:1781–1790

    Article  PubMed  CAS  Google Scholar 

  • Lusser M, Davies HV (2013) Comparative regulatory approaches for groups of new plant breeding techniques. Nat Biotechnol 30:437–446

    CAS  Google Scholar 

  • Lusser M, Parisi C, Plan D, Rodríguez-Cerezo E (2012) Deployment of new biotechnologies in plant breeding. Nat Biotechnol 30:231–239

    Article  CAS  PubMed  Google Scholar 

  • 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, Müller-Lerch F, Fu F, Pearlberg J, Göbel C, Dassie JP, Pruett-Miller SM, Porteus MH, Sgroi DC, Iafrate AJ, Dobbs D, McCray PB Jr, Cathomen T, Voytas DF, Joung JK (2008) Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 31:294–301

    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 USA 108:2623–2628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mali P, Esvelt KM, Church GM (2013) Cas9 as a versatile tool for engineering biology. Nat Methods 10:957–963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marton I, Zuker A, Shklarman E, Zeevi V, Tovkach A, Roffe S, Ovadis M, Tzfira T, Vainstein A (2010) Nontransgenic genome modification in plant cells. Plant Physiol 154:1079–1087

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matsunaga E, Sugita K, Ebinuma H (2002) Asexual production of selectable marker-free transgenic woody plants, vegetatively propagated species. Mol Breeding 10:95–106

    Article  CAS  Google Scholar 

  • McConnell Smith A, Takeuchi R, Pellenz S, Davis L, Maizels N, Monnat RJ, Stoddard BL (2009) Generation of a nicking enzyme that stimulates site-specific gene conversion from the I-AniI LAGLIDADG homing endonuclease. Proc Natl Acad Sci USA 106:5099–5104

    Article  PubMed Central  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Molesini B, Pii Y, Pandolfini T (2012) Fruit improvement using intragenesis and artificial microRNA. Trends Biotechnol 30:80–87

    Article  CAS  PubMed  Google Scholar 

  • Molnar A, Bassett A, Thuenemann E, Schwach F, Karkare S, Ossowski S, Weigel D, Baulcombe D (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J 58:165–174

    Article  CAS  PubMed  Google Scholar 

  • Montgomery TA, Yoo SJ, Fahlgren N, Gilbert SD, Howell MD, Sullivan CM, Alexander A, Nguyen G, Allen E, Ahn JH, Carrington JC (2008) AGO1-miR173 complex initiates phased siRNA formation in plants. Proc Natl Acad Sci USA 105:20055–20062

    Article  PubMed Central  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 

  • Mussolino C, Cathomen T (2011) On target? Tracing zinc-finger-nuclease specificity. Nat Methods 8:725–726

    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  PubMed Central  CAS  PubMed  Google Scholar 

  • Nekrasov V, Staskawicz B, Weigel D, Jones JDG, 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 

  • Onouchi H, Yokoi K, Machida C, Matsuzaki H, Oshima Y, Matsuoka K, Nakamura K, Machida Y (1991) Operation of an efficient site-specific recombination system of Zygosaccharomyces rouxii in tobacco cells. Nucleic Acids Res 19:6373–6378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690

    Article  CAS  PubMed  Google Scholar 

  • Pâques F, Duchateau P (2007) Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gene Ther 7:49–66

    Article  PubMed  Google Scholar 

  • Park YG, Son SH (1992) In vitro shoot regeneration from leaf mesophyll protoplasts of hybrid poplar (Populus nigra × P. maximowiczii). Plant Cell Rep 11:2–6

    Article  CAS  PubMed  Google Scholar 

  • Pattanayak V, Ramirez CL, Joung JK, Liu DR (2011) Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat Methods 8:765–770

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pauwels K, Podevin N, Breyer D, Carroll D, Herman P (2014) Engineering nucleases for gene targeting: safety and regulatory considerations. Nat Biotechnol 31:18–27

    CAS  Google Scholar 

  • Pérez-Quintero A, López C (2010) Artificial microRNAs and their applications in plant molecular biology. Agron Colomb 28:373–381

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Petri C, Burgos L (2005) Transformation of fruit trees. Useful breeding tool or continued future prospect? Transgenic Res 14:15–26

    Article  CAS  PubMed  Google Scholar 

  • Petri C, López-Noguera S, Wang H, García-Almodovar RC, Alburquerque N, Burgos L (2012) A chemical-inducible Cre-LoxP system allows for elimination of selection marker genes in transgenic apricot. Plant Cell Tiss Org 110:337–346

    Article  CAS  Google Scholar 

  • Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leplé JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat Biotechnol 20:607–612

    Article  CAS  PubMed  Google Scholar 

  • Podevin N, Davies HV, Hartung F, Nogué F, Casacuberta JM (2013) Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding. Trends Biotechnol 31:375–383

    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  PubMed Central  CAS  PubMed  Google Scholar 

  • Puchta H, Dujon B, Hohn B (1996) Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc Natl Acad Sci USA 93:5055–5060

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Puchta H (2003) Marker-free transgenic plants. Plant Cell Tiss Org 74:123–134

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ramirez CL, Foley JE, Wright DA, Müller-Lerch F, Rahman SH, Cornu TI, Winfrey RJ, Sander JD, Fu F, Townsend JA, Cathomen T, Voytas DF, Joung K (2008) Unexpected failure rates for modular assembly of engineered zinc fingers. Nat Methods 5:374–375

    Article  CAS  PubMed  Google Scholar 

  • Ramirez CL, Certo MT, Mussolino C, Goodwin MJ, Cradick TJ, McCaffrey AP, Cathomen T, Scharenberg AM, Joung JK (2012) Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects. Nucleic Acids Res 40:5560–5568

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK (2012) FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30:460–465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rukavtsova EB, Lebedeva AA, Zakharchenko NS, Buryanov Y (2013) The ways to produce biologically safe marker-free transgenic plants. Russ J Plant Physiol 60:14–26

    Article  CAS  Google Scholar 

  • Sablok G, Pérez-Quintero AL, Hassan M, Tatarinova T, López C (2011) Artificial microRNAs (amiRNAs) engineering—on how microRNA-based silencing methods have affected current plant silencing research. Biochem Biophys Res Com 406:315–319

    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  PubMed Central  CAS  PubMed  Google Scholar 

  • Sander JD, Maeder ML, Joung JK (2011) Engineering designer nucleases with customized cleavage specificities In: Current protocols in molecular biology. John Wiley and Sons, Inc., New York, pp 12.13.1–12.13.16

    Google Scholar 

  • Sanders KL, Catto LE, Bellamy SRW, Halford SE (2009) Targeting individual subunits of the FokI restriction endonuclease to specific DNA strands. Nucleic Acids Res 37:2105–2115

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sautter C, Leduc N, Bilang R, Iglesias VA, Gisel A, Wen X, Potrykus I (1995) Shoot apical meristems as a target for gene-transfer by microballistics. Euphytica 85:45–51

    Article  CAS  Google Scholar 

  • Schaart JG, Krens FA, Pelgrom KTB, Mendes O, Rouwendal GJA (2004) Effective production of marker-free transgenic strawberry plants using inducible site-specific recombination and a bifunctional selectable marker gene. Plant Biotechnol J 2:233–240

    Article  CAS  PubMed  Google Scholar 

  • Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shan Q, Wang Y, Chen K, Liang Z, Li J, Zhang Y, Zhang K, Liu J, Voytas DF, Zheng X, Zhang Y, Gao C (2013a) Rapid and efficient gene modification in rice and Brachypodium using TALENs. Mol Plant 6:1365–1368

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013b) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688

    Article  CAS  PubMed  Google Scholar 

  • Shi R, Yang C, Lu S, Sederoff R, Chiang V (2010) Specific down-regulation of PAL genes by artificial microRNAs in Populus trichocarpa. Planta 232:1281–1288

    Article  CAS  PubMed  Google Scholar 

  • Shukla VK 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 

  • Siebert R, Puchta H (2002) Efficient repair of genomic double-strand breaks by homologous recombination between directly repeated sequences in the plant genome. Plant Cell 14:1121–1131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sorek R, Lawrence CM, Wiedenheft B (2013) CRISPR-mediated adaptive immune systems in bacteria and archaea. Ann Rev Biochem 82:237–266

    Article  CAS  PubMed  Google Scholar 

  • Sreekala C, Wu L, Gu K, Wang D, Tian D, Yin Z (2005) Excision of a selectable marker in transgenic rice (Oryza sativa L.) using a chemically regulated Cre/loxP system. Plant Cell Rep 24:86–94

    Article  CAS  PubMed  Google Scholar 

  • Srivastava V, Ow DW (2001) Single-copy primary transformants of maize obtained trhough the co-introduction of a recombinase-expressing construct. Plant Mol Biol 46:561–566

    Article  CAS  PubMed  Google Scholar 

  • Srivastava V, Anderson OD, Ow DW (1999) Single-copy transgenic wheat generated through the resolution of complex integration patterns. Proc Natl Acad Sci USA 96:11117–11121

    Google Scholar 

  • Stam M, Mol JNM, Kooter JM (1997) The silence of genes in transgenic plants. Ann Bot-London 79:3–12

    Article  CAS  Google Scholar 

  • Stoddard BL (2011) Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure 19:7–15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Szankowski I, Waidmann S, Degenhardt J, Patocchi A, Paris R, Silfverberg-Dilworth E, Broggini G, Gessler C (2009) Highly scab-resistant transgenic apple lines achieved by introgression of HcrVf2 controlled by different native promoter lengths. Tree Genet Genomes 5:349–358

    Article  Google Scholar 

  • Tovkach A, Zeevi V, Tzfira T (2009) A toolbox and procedural notes for characterizing novel zinc finger nucleases for genome editing in plant cells. Plant J 57:747–757

    Article  CAS  PubMed  Google Scholar 

  • 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ, Joung JK (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotech 32:569–576

    Article  CAS  Google Scholar 

  • Tzfira T, Frankman LR, Vaidya M, Citovsky V (2003) Site-specific integration of Agrobacterium tumefaciens T-DNA via double-stranded intermediates. Plant Physiol 133:1011–1023

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD (2010) Genome editing with engineered zinc finger nucleases. Nat Rev Genet 11:636–646

    Article  CAS  PubMed  Google Scholar 

  • Vanblaere T, Szankowski I, Schaart J, Schouten H, Flachowsky H, Broggini GAL, Gessler C (2011) The development of a cisgenic apple plant. J Biotechnol 154:304–311

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis and activity of plant microRNAs. Cell 136:669–687

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–918

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang T, Wei JJ, Sabatini DM, Lander ES (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science 343:80–84

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Y, Yau YY, Perkins-Balding D, Thomson JG (2011) Recombinase technology: applications and possibilities. Plant Cell Rep 30:267–285

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Waterhouse PM, Graham MW, Wang MB (1998) Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc Natl Acad Sci USA 95:13959–13964

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Waterhouse PM, Helliwell CA (2003) Exploring plant genomes by RNA-induced gene silencing. Nat Genet 4:29–38

    Article  CAS  Google Scholar 

  • Wehrkamp-Richter S, Degroote F, Laffaire JB, Paul W, Perez P, Picard G (2009) Characterisation of a new reporter system allowing high throughput in planta screening for recombination events before and after controlled DNA double strand break induction. Plant Physiol Biochem 47:248–255

    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 

  • Wesley SV, Helliwell CA, Smith NA, Wang M, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27:581–590

    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 

  • 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 

  • Yang M, Djukanovic V, Stagg J, Lenderts B, Bidney D, Falco SC, Lyznik LA (2009) Targeted mutagenesis in the progeny of maize transgenic plants. Plant Mol Biol 70:669–679

    Article  CAS  PubMed  Google Scholar 

  • Yoshikawa M (2013) Biogenesis of trans-acting siRNAs, endogenous secondary siRNAs in plants. Genes Genet Syst 88:77–84

    Article  CAS  PubMed  Google Scholar 

  • Zeng Y, Wagner EJ, Cullen BR (2002) Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol Cell 9:1327–1333

    Article  CAS  PubMed  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. Proc Natl Acad Sci USA 107:12028–12033

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG, Bogdanove AJ, Voytas DF (2013a) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol 161:20–27

    Article  PubMed Central  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 ZJ (2014) Artificial trans-acting small interfering RNA: a tool for plant biology study and crop improvements. Planta 239:1139–1146

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Subbarao S, Addae P, Shen A, Armstrong C, Peschke V, Gilbertson L (2003) Cre/lox-mediated marker gene excision in transgenic maize (Zea mays L.) plants. Theor Appl Genet 107:1157–1168

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li H, Ouyang B, Lu Y, Ye Z (2006) Chemical-induced autoexcision of selectable markers in elite tomato plants transformed with a gene conferring resistance to lepidopteran insects. Biotechnol Lett 28:1247–1253

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Wang W, Bai X, Qi Y (2008) Gene silencing by artificial microRNAs in Chlamydomonas. Plant J 58:157–164

    Article  PubMed  CAS  Google Scholar 

  • Zhu C, Naqvi S, Breitenbach J, Sandmann G, Christou P, Capell T (2008) Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize. Proc Natl Acad Sci USA 105:18232–18237

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zuo J, Niu QW, Moller SG, Chua NH (2001) Chemical-regulated, site-specific DNA excision in transgenic plants. Nat Biotechnol 19:157–161

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fruit Biotechnology Group, Department of Plant Breeding, CEBAS-CSIC Campus Universitario de Espinardo, 30100, Murcia, Spain

    Nuria Alburquerque & Lorenzo Burgos

  2. Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), 6041, Gosselies, Belgium

    Fabien Baldacci-Cresp, Marie Baucher & Mondher El Jaziri

  3. Center for Research in Agricultural Genomics, CRAG (CSIC-IRTA-UAB-UB), Campus UAB, Cerdanyola Del Vallès, 08193, Barcelona, Spain

    Josep M. Casacuberta

  4. INRA AgroParisTech, IJPB, UMR 1318, INRA Centre de Versailles, route de Saint Cyr, 78026, Versailles Cedex, France

    Cécile Collonnier & Fabien Nogué

Authors
  1. Nuria Alburquerque
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabien Baldacci-Cresp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marie Baucher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josep M. Casacuberta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cécile Collonnier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mondher El Jaziri
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fabien Nogué
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lorenzo Burgos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lorenzo Burgos .

Editor information

Editors and Affiliations

  1. Inst.of Biosci. and Biores.(IBBR)-UOS Fl, National Research Council (CNR), Sesto Fiorentino, Italy

    Cristina Vettori

  2. Dept.de BiologíaMol.y BioquímicaFacultad, Universidad de Málaga, Malaga, Spain

    Fernando Gallardo

  3. Dept. of Genetics and physiology, Univ of Oulu, Oulu, Finland

    Hely Häggman

  4. Department of Forestry & Natural Environ, Eastern Macedonia & Thrace Inst of Tech., Drama, Greece

    Vassiliki Kazana

  5. National Research Council (CNR), Inst. of Chem.of Organometallic Comp(ICC, Sesto Fiorentino, Italy

    Fabio Migliacci

  6. Inst.Nati. de laRechercheAgronomique(INR, UR0588,Amélioration,Génétique et Phys. F, Orleans, France

    Gilles Pilate

  7. Thuenen-Institute of Forest Genetics, Großhansdorf, Germany

    Matthias Fladung

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Alburquerque, N. et al. (2016). New Transformation Technologies for Trees. In: Vettori, C., et al. Biosafety of Forest Transgenic Trees. Forestry Sciences, vol 82. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7531-1_3

Download citation

Publish with us

Policies and ethics

Search

Navigation