, 23:1125 | Cite as

Transgene stability and dispersal in forest trees

  • Mulkh Raj Ahuja


Transgenics from several forest tree species, carrying a number of commercially important recombinant genes, have been produced, and are undergoing confined field trials in a number of countries. However, there are questions and issues regarding stability of transgene expression and transgene dispersal that need to be addressed in long-lived forest trees. Variation in transgene expression is not uncommon in the primary transformants in plants, and is undesirable as it requires screening a large number of transformants in order to select transgenic lines with acceptable levels of transgene expression. Therefore, the current focus of plant transformation is toward fine tuning of transgene expression and stability in the transgenic forest trees. Although a number of studies have reported a relatively stable transgene expression for several target traits, including herbicide resistance, insect resistance, and lignin modification, there was also some unintended transgene instability in the genetically modified (GM) forest trees. Transgene dispersal from GM trees to feral forest populations and their containment remain important biological and regulatory issues facing commercial release of GM trees. Containment of transgenes must be in place to effectively prevent escape of transgenic pollen, seed, and vegetative propagules in economically important GM forest trees before their commercialization. Therefore, it is important to devise innovative technologies in genetic engineering that lead to genetically stable transgenic trees not only for qualitative traits (herbicide resistance, insect resistance), but also for quantitative traits (accelerated growth, increased height, increased wood density), and also prevent escape of transgenes in the forest trees.


Forest trees Recombinant genes Transgenic trees Transgene stability Gene flow Transgene dispersal Containment 



I thank the Institute of Forest Genetics, USDA Forest Service, and the Department of Plant Sciences, University of California, Davis, for facilities. I also thank David Neale for helpful suggestions on the manuscript.


  1. Ahuja MR (1987) Somaclonal variation. In: Bonga JM, Durzan DJ (eds) Cell and tissue culture in forestry. vol 1. Martinus Nijhoff Publishers, Dordrecht, pp 272–285Google Scholar
  2. Ahuja MR (1988) Gene transfer in forest trees. In: Hanover JE, Keathley DE (eds) Genetic manipulation of woody plants. Plenum Press, New York, pp 25–41Google Scholar
  3. Ahuja MR (1997) Transgenes and genetic instability. In: Klopfenstein NB, Chun WYW, Kim M-S, Ahuja MR (eds) Micropropagation and genetic engineering and molecular genetics of Populus. Technical Report RM-GTR-297, USDA Forest Service, Rocky Mountain Research Station, Fort Collins, pp 90–100Google Scholar
  4. Ahuja MR (1998) Somaclonal genetics of forest trees. In: Jain SM, Brar DS, Ahloowalia BS (eds) Somaclonal variation and induced mutations in crop improvement. Kluwer, Dordrecht, pp 105–121Google Scholar
  5. Ahuja MR (2000) Genetic engineering in forest trees: state of the art and future perspectives. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants. vol. 1. Kluwer, Dordrecht, pp 31–49Google Scholar
  6. Ahuja MR (2001) Recent advances in molecular genetics of forest trees. Euphytica 121:73–195CrossRefGoogle Scholar
  7. Ahuja MR, Fladung M (1996) Stability and expression of chimeric genes in Populus. In: Ahuja MR, Boerjan W, Neale DB (eds) Somatic cell genetics and Molecular genetics of trees. Kluwer, Dordrecht, pp 89–96Google Scholar
  8. Al-Ahmad H, Dwer J, Moloney M, Gressel J (2006) Mitigation of establishment of Brassica napus transgenes in volunteers using a tandem construct containing a selectively unfit gene. Plant Biotecnol J 4:7–21CrossRefGoogle Scholar
  9. Allen GC, Spiker S, Thompson WF (2000) Use of matrix attachment regions (MARs) to minimize transgene silencing. Plant Mol Biol 43:361–376PubMedCrossRefGoogle Scholar
  10. Baack EJ (2006) Engineered crops: transgenes go wild. Curr Biol 16:R583–R584PubMedCrossRefGoogle Scholar
  11. Baucher M, Halpin C, Petit-Conil M, Boerjan W (2003) Lignin: genetic engineering and impact on pulping. Crit Rev Biochem Mol Biol 38:305–350PubMedCrossRefGoogle Scholar
  12. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363PubMedCrossRefGoogle Scholar
  13. Bhat SR, Srinivasan S (2002) Molecular and genetic analysis of transgenic plants: considerations and approaches. Plant Sci 163:673–681CrossRefGoogle Scholar
  14. Birch RG (1997) Plant transformation: problems and strategies for practical application. Annu Rev Plant Physiol Mol Biol 48:297–326CrossRefGoogle Scholar
  15. Bishop-Hurley SL, Zubkiewicz RJ, Grace LJ et al (2001) Conifer genetic engineering: transgenic Pinus radiata (D.Don.) and Picea abies (Karst.) plants are resistant to the herbicide Buster. Plant Cell Rep 20:235–243CrossRefGoogle Scholar
  16. Boerjan W (2005) Biotechnology and domestication of forest trees. Curr Opin Biotechnol 16:159–166PubMedCrossRefGoogle Scholar
  17. Bradford KJ, Deynze AV, Gutterson N, Parrott W, Strauss SH (2005) Regulating transgenic crops sensibly: lessons from plant breeding, biotechnology and genomics. Nat Biotechnol 23:439–444PubMedCrossRefGoogle Scholar
  18. Brunner AM, Li J, DiFazio SP, Schevchenko O, Montgomery BE, Mohamed R, Wie H, Ma C, Elias AA, Van Wormer K, Strauss SH (2007) Genetic containment of forest plantations. Tree Genet Genomes 3:75–100CrossRefGoogle Scholar
  19. Burczyk J, DiFazio SP, Adams WT (2004) Gene flow in forest trees: how far do genes really travel? For Genet 11:1–14Google Scholar
  20. Burke JM, Gardner KA, Rieseberg LH (2002) The potential for gene flow between cultivated and wild sunflower (Helianthus annuus) in the United States. Am J Bot 89:1550–1552CrossRefGoogle Scholar
  21. Busov VB, Brunner AM, Meilan R, Filichkin S, Ganio L, Gandhi S, Strauss SH (2005) Genetic transformation: a powerful tool for dissection of adaptive traits in trees. New Phytol 167:9–18PubMedCrossRefGoogle Scholar
  22. Butaye KJM, Goderis IJWM, Wouters PFJ, Pues JMTG, Delauré SL, Boekaert WF, Depicker A, Cammue BPA, De Bolle MFC (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutant and matrix attachment regions. Plant J 39:440–449PubMedCrossRefGoogle Scholar
  23. Butaye KMJ, Cammue BPA, Delauré SL, De Bolle MFC (2005) Approaches to minimize variation in transgene expression in plants. Mol Breed 16:79–91CrossRefGoogle Scholar
  24. Campbell MM, Brunner AM, Jones HM, Strauss SH (2003) Forestry’s fertile crescent: the application of biotechnology to forest trees. Plant Biotechnol J 1:141–154PubMedCrossRefGoogle Scholar
  25. Cervera M, Piña JA, Juárez J, Navarro L, Peña L (2000) A broad exploration of transgenic citrus: stability of gene expression and phenotype. Theor Appl Genet 100:670–677CrossRefGoogle Scholar
  26. Chapman MA, Burke JM (2006) Letting the gene out of the bottle: populations genetics of genetically modified crops. New Phytol 170:429–443PubMedCrossRefGoogle Scholar
  27. Charest PJ, Michel MF (1991) Basics of plant genetic engineering and its potential applications to tree species. Information Report Pl-X-104. Petawawa National Forestry Institute, Forestry Canada, pp 1–48Google Scholar
  28. Charity JA, Holland L, Grace LJ, Walter C (2005) Consistent and stable expression of the nptII, uidA and bar genes in transgenic Pinus radiata after Agrobacterium tumefaciens-mediated transformation using nurse cultures. Plant Cell Rep 23:606–616PubMedCrossRefGoogle Scholar
  29. Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20:581–586PubMedCrossRefGoogle Scholar
  30. Daniell H, Kumar S, Dufourmantel N (2005) Breakthrough in chloroplast genetic engineering of agronomically important crops. Trends Biotechnol 23:238–245PubMedCrossRefGoogle Scholar
  31. De Bolle MFC, Butaye MMJ, Couke WJW, Goderis IJWM, Wouters PFJ, van Boxel N, Brockaert WF, Cammue BPA (2003) Analysis of the influence of promoter elements and matrix attachment region on the inter-individal variation of transgene expression in populations of Arabidopsis thaliana. Plant Sci 165:169–179CrossRefGoogle Scholar
  32. DiFazio SP, Slavov GT, Burczyk J, Leonardi S, Strauss SH (2004) Gene flow from tree plantations and implications for transgenic risk assessment. In: Walter C, Carson M (eds) Plantation forest biotechnology for the 21st Century. Research Signpost, Trivandrum, pp 405–422Google Scholar
  33. Donahue RA, Davis TD, Riemenschneider DF, Michler CH, Carter DR, Marquardt PE, Sankhala D, Haissig BE, Isebrands JG (1994) Growth, photosynthesis, and herbicide tolerance of genetically modified hybrid poplar. Can J For Res 24:2377–2383CrossRefGoogle Scholar
  34. Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst 30:539–563CrossRefGoogle Scholar
  35. Ewald D, Hu J, Yang M (2006) Transgenic forest trees in China. In: Fladung M, Ewald D (eds) Tree transgenesis: recent developments. Springer, Berlin, pp 25–45Google Scholar
  36. Fagard M, Vauchert H (2000) (Tans)gene silencing in plants: how many mechanisms? Annu Rev Plant Physiol Plant Mol Biol 51:167–194PubMedCrossRefGoogle Scholar
  37. Farnum P, Lucier A, Meilan R (2007) Ecological and population genetics research imperatives for transgenic trees. Tree Genet Genomes 3:119–133CrossRefGoogle Scholar
  38. Fillatti JJ, Selmer J, McCown B, Haissig B, Comai L (1987) Agrobacterium mediated transformation and regeneration of Populus. Mol Gen Genet 206:192–199CrossRefGoogle Scholar
  39. Finnegan J, McElroy D (1994) Transgene inactivation: plants fight back. Biotechnology 12:883–888CrossRefGoogle Scholar
  40. Finstad K, Bonfils AC, Shearer W, Macdonald P (2007) Trees with novel traits in Canada: regulation and related scientific issues. Tree Genet Genomes 3:135–139CrossRefGoogle Scholar
  41. Fladung M (1999) Gene stability in transgenic aspen (Populus). I. Flanking DNA sequences and T-DNA structure. Mol Gen Genet 260:1097–1103Google Scholar
  42. Fladung M, Kumar S, Ahuja MR (1997) Genetic transformation with different chimeric gene constructs: transformation efficiency and molecular analysis. Transgenic Res 6:111–121CrossRefGoogle Scholar
  43. Gilbertson L (2003) Cre-lox recombination: cre-active tools for plant biotechnology. Trends Biotechnol 21:550–555PubMedCrossRefGoogle Scholar
  44. Grace LJ, Charity JA, Gresham B, Kay N, Walter C (2005) Insect resistance transgenic Pinus radiata. Plant Cell Rep 24:103–111PubMedCrossRefGoogle Scholar
  45. Gressel J (1999) Tandem constructs preventing the rise of super weeds. Trends Biotechnol 17:361–366PubMedCrossRefGoogle Scholar
  46. Groover AT (2007) Will genomics guide a greener forest biotechnology? Trends Plant Sci 12:234–238PubMedCrossRefGoogle Scholar
  47. Halpin C, Thain SC, Tilston EL, Guiney E, Lapierre C, Hopkin DW (2007) Ecological impacts of trees with modified lignin. Tree Genet Genomes 3:101–110CrossRefGoogle Scholar
  48. Halweg C, Thompson WF, Spiker S (2005) The Rb7 matrix attachment region increases the likelihood and magnitude of transgene expression in tobacco cells: a flow cytometric study. Plant Cell 17:418–429PubMedCrossRefGoogle Scholar
  49. Hancock JE, Loya WM, Giardina CP, Li L, Chiang VL, Pregitzer KS (2007) Plant growth, biomass partitioning and soil carbon formation in response to altered lignin biosynthesis in Populus tremuloides. New Phytol 173:732–742PubMedCrossRefGoogle Scholar
  50. Harcourt RL, Kyozuka J, Floyd RB, Bateman KS, Tanaka H, Decroocq V, Llewellyn DJ, Zhu X, Peacock WJ, Dennis ES (2000) Insect- and herbicide-resistant transgenic eucalypts. Mol Breed 6:307–315CrossRefGoogle Scholar
  51. Hawkins S, Leplé JC, Cornu D, Jouanin L, Pilate G (2003) Stability of transgene expression in poplar: a model forest tree species. Ann For Sci 60:427–438CrossRefGoogle Scholar
  52. Heinemann JA, Traavik T (2004) Problems in monitoring horizontal gene transfer in field trials of transgenic plants. Nat Biotechnol 22:1105–1109PubMedCrossRefGoogle Scholar
  53. Hoenicka H, Fladung M (2006a) Genomic instability in woody plants derived from genetic engineering. In: Fladung M, Ewald D (eds) Transgenesis: recent developments. Springer, Berlin, pp 301–321Google Scholar
  54. Hoenicka H, Fladung M (2006b) Biosafety in Populus spp. and other forest trees: from non-native species to taxa derived from traditional breeding and genetic engineering. Trees 20:131–144CrossRefGoogle Scholar
  55. Hu W-J, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai C-J, Chiang V (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotechnol 17:808–812PubMedCrossRefGoogle Scholar
  56. Jaffe G (2004) Regulating transgenic crops: a comparative analysis of different regulatory processes. Transgenic Res 13:5–19PubMedCrossRefGoogle Scholar
  57. James C (2008) Global status of commercialized Biotech/GM Crops 2008. The International Service for the Acquisition of Agri-biotech Applications (ISAAA Brief # 39), Ithaca, NY.
  58. Jing ZP, Gallardo F, Pascual MB, Sampalo P, Romero J, Torres de Navarra A, Canovas FM (2004) Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytol 164:137–145CrossRefGoogle Scholar
  59. Käppeli O, Auberson L (1998) How safe is safe enough in plant genetic engineering? Trends Plant Sci 3:276–281CrossRefGoogle Scholar
  60. Kawaoka A, Mutsanga E, Endo S, Kondo S, Yoshida K, Shinmyo A, Ebinuma H (2003) Ectopic expression of a horseradish peroxidase enhances growth rate and increase oxidative stress in hybrid aspen. Plant Physiol 132:1177–1185PubMedCrossRefGoogle Scholar
  61. Kikuchi A, Watanabe K, Tanaka Y, Kamada H (2008) Recent progress on environmental biosafety assessment of genetically modified trees and floricultural plants in Japan. Plant Biotechnol 25:9–15Google Scholar
  62. Kumar S, Fladung M (2001) Controlling transgene integration in plants. Trends Plant Sci 6:156159Google Scholar
  63. Kumar S, Fladung M (2002) Transgene integration in aspen: structures of integration sites and mechanisms of T-DNA integration. Plant J 31:543–551PubMedCrossRefGoogle Scholar
  64. Kumar S, Fladung M (2004) Stability of transgene expression in aspen. In: Kumar S, Fladung M (eds) Molecular genetics and breeding of forest trees. Food Products Press, Binghamton, pp 293–308Google Scholar
  65. Kuparinen A, Schurr F (2007) A flexible modeling framework linking the spatio-temporal dynamics of plant genotypes and populations: applications to gene flow from transgenic forests. Ecol Modell 202:476–486CrossRefGoogle Scholar
  66. Kuparinen A, Schurr F (2008) Assessing the risk of gene flow from genetically modified trees carrying mitigation transgenes. Biol Invasions 10:281–290CrossRefGoogle Scholar
  67. Kusaba M (2004) RNA interference in crop plants. Curr Opin Biotechnol 15:139–143PubMedCrossRefGoogle Scholar
  68. Lachance D, Hamel L-P, Pelltier E, Valéro J, Bernier-Cardou M, Chapman K, Van Frankenhuyzen K, Séguin A (2007) Expression of a Bacillus thuringiensis cry1Ab gene in transgenic white spruce and its efficacy against the spruce budworm (Choristoneura fumiferana). Tree Genet Genomes 3:153–167CrossRefGoogle Scholar
  69. Lännenpää M, Hassinen M, Ranki A, Hölttä-Vuora M, Lemmetyinen J, Keinonnen K, Sopanen T (2005) Prevention of flower development in birch and other plants using a BPFULLI::BARNASE construct. Plant Cell Rep 24:69–78PubMedCrossRefGoogle Scholar
  70. Larkin PJ, Scowcroft WR (1981) Somaclonal variation—a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214CrossRefGoogle Scholar
  71. Lemmetyinen J, Keinonen K, Sopanen T (2004) Prevention of flowering of a tree, silver birch. Mol Breed 13:243–249CrossRefGoogle Scholar
  72. Leple J, Bonadebottino M, Augustin S, Pilate G, Letan VD, Delplanque A, Cornu D, Jouanin L (1995) Toxicity to Chrysomela tremulae (Coleoptera, chrysomelidae) of transgenic poplars expressing a cysteine proteinase-inhibitor. Mol Breed 1:319–328CrossRefGoogle Scholar
  73. Li L, Zhou Y, Sun J, Marita JM, Ralph J, Chiang VL (2003) Combinatorial modification of multiple lignin traits in tree through multigene cotransformation. Proc Natl Acad Sci USA 100:4939–4944PubMedCrossRefGoogle Scholar
  74. Li J, Brunner AM, Meilan R, Strauss SH (2008a) Stability of transgenes in trees: expression of two reporter genes in poplar over two field seasons. Tree Physiol 29:299–312PubMedCrossRefGoogle Scholar
  75. Li J, Meilan R, Ma C, Barish M, Strauss SH (2008b) Stability of herbicide resistance over eight years of coppice in field-grown, genetically engineered poplars. West J Appl For 23:89–93Google Scholar
  76. Li J, Brunner AM, Schevchenko O, Meilan R, Ma C, Skinner JS, Strauss SH (2008c) Efficient and stable transgene suppression via RNAi in field-grown poplars. Transgenic Res 17:679–694PubMedCrossRefGoogle Scholar
  77. Lida W, Yifan H, Jianjun H (2004) Transgenic forest trees for insect resistance. In: Kumar S, Fladung M (eds) Molecular genetics and breeding of forest trees. The Haworth Press, Binghamton, pp 243–261Google Scholar
  78. Lu B-R (2003) Transgenic containment by molecular means—is it possible and cost effective? Environ Biosafety Res 2:3–8PubMedGoogle Scholar
  79. Luo R, Duan H, Zhao D, Zheng X, Deng W, Chen Y, Stewart CN, McAvoy R, Jiang X, Wu Y, He A, Pei Y, Li Y (2007) “GM-gene-deletor”: fused loxP-FRT recognition sequences dramatically improve the efficiency of FLP or GRF recombinase on transgene excision from pollen and seed of tobacco plants. Plant Biotechnol J 5:263–274PubMedCrossRefGoogle Scholar
  80. Mansoor S, Amin I, Hussain M, Zafar Y, Briddon RW (2006) Engineering novel traits in plants through RNA interference. Trends Plant Sci 11:559–565PubMedCrossRefGoogle Scholar
  81. Marvier M, Von Acker RC (2005) Can crop transgenes be kept on a leash? Front Ecol Environ 3:99–106CrossRefGoogle Scholar
  82. Meilan R, Ma C, Cheng S, Eaton JA, Miller LK, Crocket RP, DiFazio SP, Strauss SH (2000) High levels of roundup and leaf beetle resistance in genetically engineered hybrid cottonwoods. In: Blattner KA, Johnson JD, Baumgartner DM (eds) Hybrid poplars in the Pacific Northwest: culture, commerce and capability. Washington State University, Pullman, pp 29–38Google Scholar
  83. Meilan R, Han K-H, Ma C et al (2002) The CP4 transgene provides high levels of tolerance to Roundup herbicide in field-grown hybrid poplars. Can J For Res 32:967–976CrossRefGoogle Scholar
  84. Meilan R, Ellis D, Pilate G, Bruner AM, Skinner J (2004) Accomplishments and challenges in genetic engineering of forest trees. In: Strauss SH, Bradshaw HD (eds) The Bioengineered Forest Challenges for Science and Society. Resources for the Future, Washington, DC, pp 36–51Google Scholar
  85. Mentag R, Luckevich M, Morency MJ, Séguin A (2003) Bacterial disease resistance of transgenic hybrid poplar expressing the synthetic antimicrobial peptide D4E1. Tree Physiol 23:405–411PubMedGoogle Scholar
  86. Meyer P, Saedler H (1996) Homology-dependent gene silencing in plants. Annu Rev Plant Physiol 47:23–48CrossRefGoogle Scholar
  87. Nathan R, Katul GG, Horn HS, Thomas SM, Oren R, Avissar R, Pacala SW, Levin SA (2002) Mechanisms of long-distance dispersal of seeds by wind. Nature 418:409–413PubMedCrossRefGoogle Scholar
  88. Newhouse AE, Schrodt F, Liang H, Maynard CA, Powell WA (2007) Transgenic American elm shows reduced Dutch elm disease symptoms and normal mycorrhizal colonization. Plant Cell Rep 26:977–987PubMedCrossRefGoogle Scholar
  89. Noël A, Levasseur C, Le VQ, Séguin A (2005) Enhanced resistance to fungal pathogens in forest trees by genetic transformation of black spruce and hybrid poplar with a Trichoderma harzianum endochitinase gene. Physiol Mol Plant Pathol 67:92–99CrossRefGoogle Scholar
  90. Okumura S, Sawada M, Park YW, Hayashi T, Shimamura M, Takase H, Tomizawa K (2006) Transformation of poplar (Popolus alba) plastids and expression of foreign proteins in trees. Transgenic Res 15:637–644PubMedCrossRefGoogle Scholar
  91. Ow DW (2002) Recombinase-directed plant transformation for the post-genomic era. Plant Mol Biol 48:163–200Google Scholar
  92. Park YW, Baba K, Furuta Y, Lida I, Sameshima K, Arai M, Hayashi T (2004) Enhanced growth and cellulose accumulation by overexpression of xylogluconase in poplar. FEBS Lett 564:183–187PubMedCrossRefGoogle Scholar
  93. Pasonen H-L, Seppänen S-K, Degefu Y, Rytkönen A, Von Weissenberg K, Pappinen A (2004) Field performance of chitinase transgenic silver birches (Betula pendula): resistance to fungal disease. Theor Appl Genet 109:562–570PubMedCrossRefGoogle Scholar
  94. Peña L, Séguin A (2001) Recent advances in genetic transformation of trees. Trends Biotechnol 12:500–506CrossRefGoogle Scholar
  95. Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leplé J-C, 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 20:607–612PubMedCrossRefGoogle Scholar
  96. Reichman JR, Watrud LS, Lee EH, Burdick CA, Bollman MA, Strom MJ, King GA, Mallory-Smith C (2006) Establishment of transgenic herbicide resistant creeping bentgrass (Agrostis stolonifera L.) in non-agronomic habitats. Mol Ecol 15:4243–4255PubMedCrossRefGoogle Scholar
  97. Robischon M (2006) Field trials with transgenic trees- state of art and development. In: Fladung M, Ewald D (eds) Tree transgenesis: recent developments. Springer, Berlin, pp 3–23Google Scholar
  98. Ruf S, Karcher D, Bock R (2007) Determining the transgene containment level provided by chloroplast transformation. Proc Natl Acad Sci USA 104:6998–7002PubMedCrossRefGoogle Scholar
  99. Schuster WSF, Mitton JB (2000) Paternity and gene dispersal in limber pine (Pinus flexilus James). Genet Soc Great Br 84:348–361Google Scholar
  100. Sederoff R (2007) Regulatory science in forest biotechnology. Tree Genet Genomes 3:71–74CrossRefGoogle Scholar
  101. Sedjo RA (2006) Towards commercialization of genetically engineered forests: economic and social considerations. Resources for the Future, Washington, DC, pp 1–50Google Scholar
  102. Seppänen S-K, Syrjälä L, Von Weissenberg K, Teeri TH, Paajanen L, Pappinen A (2004) Antifungal activity of stilbenes in vitro bioassays and in transgenic Populus expressing a gene encoding pinosylvin synthase. Plant Cell Rep 22:584–593PubMedCrossRefGoogle Scholar
  103. Skinner JS, Meilan R, Ma C, Strauss SH (2003) The Populus PTD promoter imparts floral-predeterminant expression and enables high levels of floral-organ ablation in Populus, Nicotiana and Arabidopsis. Mol Breed 12:119–132CrossRefGoogle Scholar
  104. Slavov GT, Leonardi S, Burczyk J, Adams WT, Strauss SH, DiFazio SP (2009) Extensive pollen flow in two ecologically contrasting populations of Populus trichocarpa. Mol Ecol 18:357–373PubMedCrossRefGoogle Scholar
  105. Smouse PE, Robledo-Arnuncio JJ, González-Martínez SC (2007) Implications of natural propagule flow for containment of genetically modified trees. Tree Genet Genomes 3:141–152CrossRefGoogle Scholar
  106. Srivastava V, Ariza-Netto M, Wilson AJ (2004) Cre-mediated site-specific gene integration for consistent transgene expression in rice. Plant Biotech J 2:169–179CrossRefGoogle Scholar
  107. Stam M, Mol JNM, Kooter JM (1997) The silence of genes in transgenic plants. Ann Bot 79:3–12CrossRefGoogle Scholar
  108. Stewart CN, Halfhill MD, Warwick SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Genet 4:806–817PubMedCrossRefGoogle Scholar
  109. Strauss SH (2003) Genomics, genetic engineering, and domestication of crops. Science 300:61–62PubMedCrossRefGoogle Scholar
  110. Strauss SH, Rottmann WH, Brunner AM, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breed 1:5–26CrossRefGoogle Scholar
  111. Strauss SH, Brunner AM, Busov VB, Ma C, Meilan R (2004) Ten lessons from 15 years of transgenic poplar research. Forestry 77:455–465CrossRefGoogle Scholar
  112. Tang W, Newton RJ (2003) Genetic transformation of conifers and its application in forest biotechnology. Plant Cell Rep 22:1–15PubMedCrossRefGoogle Scholar
  113. Tang W, Tian Y (2003) Transgenic loblolly pine (Pinus taeda L.) plants expressing a modified δ-endotoxin gene from Bacillus thuringiensis with enhanced resistance to Dendrolimus punctatus Walker and Crypyothelea formosicola Staud. J Exp Bot 54:835–844PubMedCrossRefGoogle Scholar
  114. Tang W, Newton RJ, Li C, Charles TM (2007) Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis. Plant Cell Rep 26:115–124PubMedCrossRefGoogle Scholar
  115. Tiimonen H, Aronen T, Laakso T, Saranpää P, Chiang V, Ylioja T, Roininen H, Häggman H (2005) Does lignin modification affect feeding preference or growth performance of insect herbivores in transgenic silver birch (Betula pendula Roth)? Planta 222:699–708PubMedCrossRefGoogle Scholar
  116. Tzfira T, Zuker A, Altman A (1998) Forest tree biotechnology: genetic transformation and its application to future forests. Trends Biotechnol 16:439–446CrossRefGoogle Scholar
  117. van Frankenhuzen K, Beardmore T (2004) Current status and environmental impacts of transgenic forest trees. Can J For Res 34:1163–1180CrossRefGoogle Scholar
  118. Wagner A, Phillips L, Narayan RD, Moody JM, Geddes B (2005) Gene silencing studies in the gymnosperm Pinus radiata. Plant Cell Rep 24:95102CrossRefGoogle Scholar
  119. Walter C, Charity J, Grace L, Höfig K, Möller R, Wagner A (2002) Gene technologies in Pinus radiate and Picea abies: tools for conifer biotechnology in the 21st century. Plant Cell Tissue Organ Cult 70:3–12CrossRefGoogle Scholar
  120. Wang G, Castiglione S, Chen Y, 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 5:280–301CrossRefGoogle Scholar
  121. Watrud LS, Lee EH, Fairbrother A, Burdick C, Reichman JR, Bollman M, Storm M, King G, Van de Water Pk (2004) Evidence for landscape-level pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proc Natl Acad Sci USA 101:14533–14538PubMedCrossRefGoogle Scholar
  122. Watson JM, Fusaro AF, Wang M, Waterhouse PM (2005) RNA silencing platforms in plants. FEBS Lett 579:5982–5987PubMedCrossRefGoogle Scholar
  123. Wei H, Meilan R, Brunner AM, Skinner JS, Ma C, Strauss SH (2006) Transgene sterility in Populus: expression properties of the poplar PTLF, Agrobacterium NOS and two minimal 35S promoters in vegetative tissues. Tree Physiol 26:401–410PubMedGoogle Scholar
  124. Wei H, Meilan R, Brunner AM, Skinner JS, Ma C, Gandhi HT, Strauss SH (2007) Field trial detect incomplete barstar attenuation of vegetative cytotoxicity in Populus trees containing a poplar LEAFY promoter::barnase sterility transgene. Mol Breed 19:69–85CrossRefGoogle Scholar
  125. White TL, Adams WT, Neale DB (2007) Forest genetics. CABI Publishing, CambridgeGoogle Scholar
  126. Williams CG (2005) Framing the issues on transgenic forests. Nat Biotechnol 23:530–532PubMedCrossRefGoogle Scholar
  127. Williams CG, Davis BH (2005) Rate of transgenic spread via long-distance dispersal in Pinus taeda. For Ecol Manage 217:95–102CrossRefGoogle Scholar
  128. Wolfenbarger LL, Phifer PR (2000) The ecological risks and benefits of genetically engineered plants. Science 290:2088–2093PubMedCrossRefGoogle Scholar
  129. Yang MS, Lang LS, Gao BJ, Wang JM, Zheng JB (2003) Insecticidal activity and transgene expression stability of transgenic hybrid poplar clone 741 carrying two insect-resistance genes. Silvae Genet 52:197–201Google Scholar
  130. Yu X, Kikuchi A, Matsunga E, Nanto K, Sakurai N, Suzuki H, Shibata D, Shimada T, Wanatabe KN (2009) Establishment of the evaluation system of salt tolerance on transgenic woody plants in the special netted-house. Plant Biotechnol 26:135–142Google Scholar
  131. Zobel BJ, Talbert BJ (1984) Applied forest tree improvement. Wiley, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.New PaltzUSA

Personalised recommendations