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Transformation as a Tool for Genetic Analysis in Populus

  • Victor B. Busov
  • Steven H. Strauss
  • Gilles Pilate
Chapter
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 8)

Abstract

We summarize the outlook for using transformation as a genetic tool in Populus. Transformation approaches avoid the major obstacle to performing genetics experiments in trees – namely long generation cycles and the difficulty of inbreeding to reveal loss of function alleles. Dominant transgenic alleles allow modifications in gene function to be readily observed in primary transformants. Although transformation has been mainly used for reverse genetics (where the gene sequence of interest is known), transgenic mutagenesis approaches such as activation tagging and gene/enhancer traps have also been shown to enable forward genetics (where the phenotype, not the gene, is known). We outline challenges and needs for more efficient use of transformation tools. These include expansion of the transformation toolbox (e.g., promoters, vectors, targeting), and improved ability to conduct field trialsto study gene function in native and plantation environments (in spite of regulatory obstacles). Because of the power of transformation, it will remain a major genetic research tool for dissection of gene function in Populus for many years to come. It is the key biological attribute that makes poplar the most powerful model organism for genetic analysis of woody plant growth, adaptation, and development.

Keywords

Tobacco Rattle Virus Post Transcriptional Gene Silence Virus Induce Gene Silence Transcriptional Gene Silence Enhancer Trap 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, 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, Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657.PubMedGoogle Scholar
  2. 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.PubMedGoogle Scholar
  3. An G, Lee S, Kim SH, Kim SR (2005) Molecular genetics using T-DNA in rice. Plant Cell Physiol 46:14–22.PubMedGoogle Scholar
  4. Arias RS, Filichkin SA, Strauss SH (2006) Divide and conquer: Development and cell cycle genes in plant transformation. Trends Biotechnol 24:267–273.PubMedGoogle Scholar
  5. Aufsatz W, Mette MF, van der Winden J, Matzke AJ, Matzke M (2002) RNA-directed DNA methylation in Arabidopsis. Proc Natl Acad Sci USA 99(Suppl 4):16499–16506, Epub@2002 Aug 8: 16499–16506.PubMedGoogle Scholar
  6. Baucher M, Chabbert B, Pilate G, Doorsselaere Jv, Tollier MT, Petit-Conil M, Cornu D, Monties B, Montagu Mv, Inze D, Jouanin L, Boerjan W (1996) Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol 112:1479–1490.PubMedGoogle Scholar
  7. Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043.PubMedGoogle Scholar
  8. Bradshaw HD, Ceulemans R, Davis J, Stettler R (2001) Emerging model systems in plant biology: Poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313.Google Scholar
  9. Bradshaw HD, Strauss SH (2001) Breeding strategies for the 21st century: Domestication of poplar. In: DI Dickman, JG Isebrands, JE Eckenwalder, J Richardson, (eds) Poplar Culture in North America. Part B. NRC Research Press. Ottawa, pp. 383–394.Google Scholar
  10. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280.PubMedGoogle Scholar
  11. Brunner AM, Li J, DiFazio SP, Shevchenko O, Montgomery BE, Mohamed R, Wei H, Ma C, Elias AA, VanWormer K, Strauss SH (2007) Genetic containment of forest plantations. Tree Genet Genomes 3:75–100.Google Scholar
  12. Burch-Smith TM, Anderson JC, Martin GB, Kumar SP (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J 39:734–746.PubMedGoogle Scholar
  13. Busov VB, Brunner AM, Meilan R, Filichkin S, Ganio L, Gandhi S, Strauss SH (2005a) Genetic transformation: A powerful tool for dissection of adaptive traits in trees. New Phytol 167:9–18.PubMedGoogle Scholar
  14. Busov VB, Fladung M, Groover A, Strauss SH (2005b) Insertional mutagenesis in Populus: Relevance and feasibility. Tree Genet Genomes 1:135–142.Google Scholar
  15. Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1283–1291.PubMedGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. Chupeau MC, Pautot V, Chupeau Y (1994) Recovery of transgenic trees after electroporation of poplar protoplasts. Transgenic Res 3:13–19.Google Scholar
  18. Citovsky V, Gafni Y, Tzfira T.,(2008) Localizing protein-protein interactions by bimolecular fluorescence complementation in planta. Methods. 45196–206PubMedGoogle Scholar
  19. Confalonieri M, Balestrazzi A, Bisoffi S, Carbonera D (2003) In vitro culture and genetic engineering of Populus spp.: Synergy for forest tree improvement. Plant Cell Tiss Org Cult 72:109–138.Google Scholar
  20. Cseke LJ, Cseke SB, Podila GK (2007) High efficiency poplar transformation. Plant Cell Rep 26:1529–1538.PubMedGoogle Scholar
  21. Dai W, Cheng ZM, Sargent W (2003) Plant regeneration and Agrobacterium-mediated transformation of two elite aspen hybrid clones from in vitro leaf tissues. In Vitro Cell Dev Biol Plant 39:6–11.Google Scholar
  22. De Block M (1990) Factors influencing the tissue culture and the Agrobacterium tumefaciens-mediated transformation of hybrid Aspen and Poplar clones. Plant Physiol 93:1110–1116.PubMedGoogle Scholar
  23. De Block M, Herrera-Estrella L van Montagu M, Schell J, Zambryski P (1984) Expression of foreign genes in regenerated plants and in their progeny. EMBO J 3:1681–1689.PubMedGoogle Scholar
  24. Dubin M, Bowler C, Benvenuto G (2008) A modified Gateway cloning strategy for overexpressing tagged proteins in plants. Plant Meth 4:3.Google Scholar
  25. 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.PubMedGoogle Scholar
  26. Ebinuma H, Sugita K, Matsunaga E, Yamakado M (1997) Selection of marker-free transgenic plants using the isopentenyl transferase gene. Proc Natl Acad Sci USA 94:2117–2121.PubMedGoogle Scholar
  27. Filichkin SA, Meilan R, Busov VB, Ma C, Brunner AM, Strauss SH (2006a) Alcohol-inducible gene expression in transgenic Populus. Plant Cell Rep 25:660–667.PubMedGoogle Scholar
  28. Filichkin SE, Qian W, Busov VB, Meilan R, Lanz-Garcia C, Groover A, Goldgarb B, Ma C, Dharmawardhana P, Brunner A, Strauss S (2006b) Enhancer trapping in woody plants: Isolation of the ET304 gene encoding a putative AT-hook motif transcription factor and characterization of the expression patterns conferred by its promoter in transgenic Populus and Arabidopsis. Plant Sci 17:206–216.Google Scholar
  29. Fillatti JJ, Sellmer J, McCown B, Haissig B, Comai L (1987) Agrobacterium-mediated transformation and regeneration of Populus. Mol Gen Genet 206:192–199.Google Scholar
  30. Flachowsky H, Hanke M-V, Peil A, Strauss SH, Fladung M (2009) A review on transgenic approaches to accelerate breeding of woody plants. Plant Breed 128:217–226.Google Scholar
  31. Fladung M, Deutsch F, Honicka H, Kumar S (2004) T-DNA and transposon tagging in aspen. Plant Biol (Stuttg) 6:5–11.Google Scholar
  32. Fladung M, Kumar S, Ahuja MR (1997) Genetic transformation of Populus genotypes with different chimaeric gene constructs: Transformation efficiency and molecular analysis. Transgenic Res 6:111–121.Google Scholar
  33. Gill G, Brown G, Neale D (2003) A sequence mutation in the cinnamyl alcohol dehydrogenase gene associated with altered lignification in loblolly pine. Plant Biotechnol J 1:253–258.PubMedGoogle Scholar
  34. Groover A, Fontana J, Dupper G, Ma C, Martienssen R, Strauss S, Meilan R (2004) Gene and enhancer trap tagging of vascular-expressed genes in poplar trees. Plant Physiol 134:1742–1751.PubMedGoogle Scholar
  35. Han KH, Meilan R, Ma C, Strauss SH (2000) An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus). Plant Cell Rep 19:315–320.Google Scholar
  36. Hao W, Meilan R, Brunner AM, Skinner JS, Ma C, Strauss SH (2005) Transgenic sterility in Populus: Expression properties of the poplar PTLF, Agrobacterium NOS, and two minimal 35S promoters in vegetative tissues. Tree Physiol 26:401–410.Google Scholar
  37. Harrison EJ, Bush M, Plett JM, Mcphee DP, Vitez R, O’Malley B, Sharma V, Bosnich W, Seguin A, MacKay J, Regan S (2007) Diverse developmental mutants revealed in an activation-tagged population of poplar. Can J Botany-Revue Canadienne de Botanique 85:1071–1081.Google Scholar
  38. Hawkins S, Leple JC, Cornu L, Jouanin L, Pilate G (2003) Stability od transgene expression in poplar: A model tree species. Ann For Sci 60:427–438.Google Scholar
  39. Heuchelin SA, McNabb HS, Klopfenstein NB (1997) Agrobacterium-mediated transformation of Populus × euramericana “Ogy” using the chimeric CaMV 35S pin2 gene fusion. Can J For Res Revue Canadienne de Recherche Forestiere 27:1041–1048.Google Scholar
  40. Hilson P (2006) Cloned sequence repertoires for small- and large-scale biology. Trends Plant Sci 11:133–141.PubMedGoogle Scholar
  41. Hsu CY, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:1846–1861.PubMedGoogle Scholar
  42. Ichikawa T, Nakazawa M, Kawashima M, Iizumi H, Kuroda H, Kondou Y, Tsuhara Y, Suzuki K, Ishikawa A, Seki M, Fujita M, Motohashi R, Nagata N, Takagi T, Shinozaki K, Matsui M (2006) The FOX hunting system: An alternative gain-of-function gene hunting technique. Plant J 48:974–985.PubMedGoogle Scholar
  43. Jeong DH, An S, Kang HG, Moon S, Han JJ, Park S, Lee HS, An K, An G (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol 130:1636–1644.PubMedGoogle Scholar
  44. Johansson AM, Wang CY, Stenberg A, Hertzberg M, Little CHA, Olsson O (2003) Characterization of a PttRPS18 promoter active in the vascular cambium region of hybrid aspen. Plant Mol Biol 52:317–329.PubMedGoogle Scholar
  45. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53.PubMedGoogle Scholar
  46. Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195.PubMedGoogle Scholar
  47. Koroleva OA, Tomlinson ML, Leader D, Shaw P, Doonan JH (2005) High-throughput protein localization in Arabidopsis using Agrobacterium-mediated transient expression of GFP-ORF fusions. Plant J 41:162–174.Google Scholar
  48. Kourtz L, Dillon K, Daughtry S, Peoples OP, Snell KD (2007) Chemically inducible expression of the PHB biosynthetic pathway in Arabidopsis. Transgenic Res 16:759–769.PubMedGoogle Scholar
  49. Kumar S, Allen GC, Thompson WF (2006) Gene targeting in plants: Fingers on the move. Trends Plant Sci 11:159–161.PubMedGoogle Scholar
  50. Kumar S, Fladung M (2001) Gene stability in transgenic aspen (Populus). II. Molecular characterization of variable expression of transgene in wild and hybrid aspen. Planta 213:731–740.PubMedGoogle Scholar
  51. Leple JC, Brasileiro ACM, Michel MF, Delmotte F, Jouanin L (1992) Transgenic poplars: Expression of chimeric genes using four different constructs. Plant Cell Rep 11:137–141.Google Scholar
  52. Li J, Brunner AM, Meilan R, Strauss SH (2008a) Matrix attachment region elements have small and variable effects on transgene expression and stability in field-grown Populus. Plant Biotechnol J 6(9):887–896.PubMedGoogle Scholar
  53. Li J, Brunner AM, Shevchenko O, Meilan R, Ma C, Skinner JS, Strauss SH (2007) Efficient and stable transgene suppression via RNAi in field-grown poplars. Transgenic Res 17:679–694.PubMedGoogle Scholar
  54. Li JY, Brunner AM, Meilan R, Strauss SH (2009) Stability of transgenes in trees: Expression of two reporter genes in poplar over three field seasons. Tree Physiol 29:299–312.Google Scholar
  55. Li JY, Brunner AM, Meilan R, Strauss SH (2009) Stability of transgenes in trees: Expression of two reporter genes in poplar over three field seasons. Tree Physiol 29:299–312.Google Scholar
  56. 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.PubMedGoogle Scholar
  57. Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203.PubMedGoogle Scholar
  58. Ma C, Strauss SH, Meilan R (2004) Agrobacterium-Mediated Transformation of the Genome-Sequenced Poplar Clone, Nisqually-1 (Populus trichocarpa). Plant Mol Biol Rep 22:311–312.Google Scholar
  59. Marjanac G, De PA, Peck I, Jacobs A, De BS, Depicker A (2008) Evaluation of CRE-mediated excision approaches in Arabidopsis thaliana. Transgenic Res 17:239–250.PubMedGoogle Scholar
  60. Matsunaga E, Sugita K, Ebinuma H (2002) Asexual production of selectable marker-free transgenic woody plants, vegetatively propagated species. Mol Breed 10:95–106.Google Scholar
  61. Matthew L (2004) RNAi for plant functional genomics. Comp Func Genomics 5:240–244.Google Scholar
  62. McCown BH, McCabe DE, Russell DR, Robison DJ, Barton KA (1991) Stable transformation of Populus and incorporation of pest resistance by electric discharge particule acceleration. Plant Cell Rep 9:590–594.Google Scholar
  63. Meilan R, Auerbach DJ, Ma C, DiFazio SP, Strauss SH (2002) Stability of herbicide resistance and GUS expression in transgenic hybrid poplars (Populus sp.) during several years of field trials and vegetative propagation. HortScience 37:1–4.Google Scholar
  64. Naylor M, Reeves J, Cooper JI, Edwards ML, Wang H (2005) Construction and properties of a gene-silencing vector based on Poplar mosaic virus (genus Carlavirus). J Virol Meth 124:27–36.Google Scholar
  65. Nishiguchi M, Yoshida K, Mohri T, Igasaki T, Shinohara K (2006) An improved transformation system for Lombardy poplar (Populus nigra var. italica). J For Res 11:175–180.Google Scholar
  66. Nishimura T, Yokota E, Wada T, Shimmen T, Okada K (2003) An Arabidopsis ACT2 dominant-negative mutation, which disturbs F-actin polymerization, reveals its distinctive function in root development. Plant Cell Physiol 44:1131–1140.PubMedGoogle Scholar
  67. Okumura S, Sawada M, Park Y, Hayashi T, Shimamura M, Takase H, Tomizawa KI (2006) Transformation of poplar (Populus alba) plastids and expression of foreign proteins in tree chloroplasts. Transgenic Res 15:637–646.PubMedGoogle Scholar
  68. Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690.PubMedGoogle Scholar
  69. Parinov S, Sundaresan V (2000) Functional genomics in Arabidopsis: Large-scale insertional mutagenesis complements the genome sequencing project. Curr Opin Biotechnol 11:157–161.PubMedGoogle Scholar
  70. Parsons TJ, Sinkar VP, Stettler RF, Nester EW, Gordon MP (1986) Transformation of poplar by Agrobacterium tumefaciens. Nat Biotech 4:533–536.Google Scholar
  71. Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leple 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 lingification. Nat Biotechnol 20:607–612.PubMedGoogle Scholar
  72. Ratcliff F, Martin-Hernandez AM, Baulcombe DC (2001) Technical Advance. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J 25:237–245.PubMedGoogle Scholar
  73. Ray A, Langer M (2002) Homologous recombination: Ends as the means. Trends Plant Sci 7:435–440.PubMedGoogle Scholar
  74. Redinbaugh MG, Louie R, Ngwira P, Edema R, Gordon DT, Bisaro DM (2001) Transmission of viral RNA and DNA to maize kernels by vascular puncture inoculation. J Virol Meth 98:135–143.Google Scholar
  75. Robertson D (2004) VIGS vectors for gene silencing: Many targets, many tools. Annu Rev Plant Biol 55:495–519.PubMedGoogle Scholar
  76. Rohde A, Prinsen E, De RR, Engler G van Montagu M, Boerjan W (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell 14:1885–1901.PubMedGoogle Scholar
  77. Schob H, Kunz C, Meins F Jr. (1997) Silencing of transgenes introduced into leaves by agroinfiltration: A simple, rapid method for investigating sequence requirements for gene silencing. Mol Gen Genet 256:581–585.PubMedGoogle Scholar
  78. 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.PubMedGoogle Scholar
  79. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, Clarke JD, Cotton D, Bullis D, Snell J, Miguel T, Hutchison D, Kimmerly B, Mitzel T, Katagiri F, Glazebrook J, Law M, Goff SA (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14:2985–2994.PubMedGoogle Scholar
  80. Smith CM, Campbell MM (2004) Complete nucleotide sequence of the genomic RNA of poplar mosaic virus (Genus Carlavirus). Arch Virol 149:1831–1841.PubMedGoogle Scholar
  81. Smith NA, Surinder SP, Wand MB, Stoutjesdijk PA, Green AG, Waterhouse PM (2000) Total silencing by intron-spliced hairpin RNAs. Nature 407:319–320.PubMedGoogle Scholar
  82. Song J, Lu S, Chen ZZ, Lourenco R, Chiang VL (2006) Genetic transformation of Populus trichocarpa genotype Nisqually-1: A functional genomic tool for woody plants. Plant Cell Physiol 47:1582–1589.PubMedGoogle Scholar
  83. Sonti RV, Tissier AF, Wong D, Viret JF, Signer ER (1995) Activity of the yeast FLP recombinase in Arabidopsis. Plant Mol Biol 28:1127–1132.PubMedGoogle Scholar
  84. Springer PS (2000) Gene traps: Tools for plant development and genomics. Plant Cell 12:1007–1020.PubMedGoogle Scholar
  85. Strauss SH (2003) Genetic technologies. Genomics, genetic engineering, and domestication of crops. Science 300:61–62.PubMedGoogle Scholar
  86. Strauss SH, Brunner AM, Ma C, Busov VB, Meilan R (2004) Ten lessons from 15 years of transgenic Populus research. J For 77:455–465.Google Scholar
  87. Strauss SH, DiFazio SP, Meilan R (2001) Genetically modified poplars in context. Forest Chron 77:271–279.Google Scholar
  88. Szabados L, Kovacs I, Oberschall A, Abraham E, Kerekes I, Zsigmond L, Nagy R, Alvarado M, Krasovskaja I, Gal M, Berente A, Redei GP, Haim AB, Koncz C (2002) Distribution of 1000 sequenced T-DNA tags in the Arabidopsis genome. Plant J 32:233–242.PubMedGoogle Scholar
  89. Thakur AK, Sharma S, Srivastava DK (2005) Plant regeneration and genetic transformation studies in petiole tissue of Himalayan poplar (Populus ciliata Wall.). Curr Sci 89:664–668.Google Scholar
  90. 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.PubMedGoogle Scholar
  91. Tsai CJ, Hubscher SL (2004) Cryopreservation in Populus functional genomics. New Phytol 164:73–81.Google Scholar
  92. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604.PubMedGoogle Scholar
  93. Tzfira T, Jensen CS, Vainstein A, Altman A (1997) Transformation and regeneration of transgenic aspen plants via shoot formation from stem explants. Physiol Plant 99:554–561.Google Scholar
  94. van Beveren KS, Spokevicius AV, Tibbits J, Wang Q, Bossinger G (2006) Transformation of cambial tissue in vivo provides an efficient means for induced somatic sector analysis and gene testing in stems of woody plant species. Func Plant Biol 33:629–638.Google Scholar
  95. Veitia RA (2007) Exploring the molecular etiology of dominant-negative mutations. Plant Cell 19:3843–3851.PubMedGoogle Scholar
  96. Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117.PubMedGoogle Scholar
  97. Wang G, Castiglione S, Chen Y, Li L, Han Y, Tian Y, Gabriel DW, Han Y, Mang K, Sala F (1996) Poplar (Populus nigra L.) plants transformed with a Bacillus thuringiensis toxin gene: Insecticidal activity and genomic analysis. Transgenic Res 5:289–301.Google Scholar
  98. Warthmann N, Chen H, Ossowski S, Weigel D, Herve P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS ONE 3:e1829.PubMedGoogle Scholar
  99. Weigel D, Ahn JH, Blazquez J, Borevitz CSK, Frankhauser C, Ferrandiz C, Kardailsky I, Neff MM, Nguyen JT, Sato S, Wang Z, Xia Y, Dixon RA, Harrison MJ, Lab C, Yanofsky MF, Chory J (2000) Activation tagging in Arabidopsis. Plant Physiol 122:1003–1013.PubMedGoogle Scholar
  100. Weiste C, Iven T, Fischer U, Oñate-Sánchez L, Dröge-Laser W (2007) In planta ORFeome analysis by large-scale over-expression of GATEWAY-compatible cDNA clones: Screening of ERF transcription factors involved in abiotic stress defense. Plant J 52:382–390.PubMedGoogle Scholar
  101. Wright DA, Townsend JA, Winfrey RJ Jr, 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.PubMedGoogle Scholar
  102. Wu L, Joshi CP, Chiang VL (2000) A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress. Plant J 22:495–502.PubMedGoogle Scholar
  103. Yamamoto YY, Tsuhara Y, Gohda K, Suzuki K, Matsui M (2003) Gene trapping of the Arabidopsis genome with a firefly luciferase reporter. Plant J 35:273–283.PubMedGoogle Scholar
  104. Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101:25–33.PubMedGoogle Scholar
  105. Zelasco S, Ressegotti V, Confalonieri M, Carbonera D, Calligari P, Bonadei M, Bisoffi S, Yamada K, Balestrazzi A (2007) Evaluation of MAT-vector system in white poplar (Populus alba L.) and production of ipt marker-free transgenic plants by a single-step transformation. Plant Cell Tiss Org Cult 91:61–72.Google Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Victor B. Busov
    • 1
  • Steven H. Strauss
    • 2
  • Gilles Pilate
    • 3
  1. 1.School of Forest Resources and Environmental Science, Michigan Technological UniversityHoughtonUSA
  2. 2.Department of Forest Ecosystems and SocietyOregon State UniversityCorvallisUSA
  3. 3.INRA OrléansCédexFrance

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