, Volume 20, Issue 2, pp 131–144 | Cite as

Biosafety in Populus spp. and other forest trees: from non-native species to taxa derived from traditional breeding and genetic engineering

  • Hans Hoenicka
  • Matthias FladungEmail author


Forest trees are fundamental components of our environment, mainly due to their long lifetime and important role in forest ecology. In the past, some non-native tree species and taxa from traditional breeding have induced severe environmental impacts such as biological invasion, changes in the ‘gene pool’, and spread of diseases in forestry. Genetically modified trees obtained in different research groups worldwide are particularly confronted with increased concerns regarding biosafety issues. In the light of current biosafety research worldwide, various threats facing forests and natural tree populations are evaluated in this review: biological invasions, horizontal gene transfer, vertical gene transfer and effects on other organisms. Results available from groups working in biosafety research and risk avoidance using forest trees, with emphasis on transgenic trees, are reviewed. Independent biosafety research as well as the establishment of biosafety research programs for forest trees financed by national and international authorities is now more important than ever before. Biosafety problems detected in the past clearly show the importance of a prior case-by-case evaluation of non-native species, new taxa and also genetically modified trees according to the precautionary principle before their release to avoid risks to the environment and human health.


Biosafety Vertical gene transfer Horizontal gene transfer Non-native species Populus GM trees Biological invasion Gene flow Transgenic trees 



We thank K. Gartland (University of Abertay, Scotland) and reviewers for critical reading and their helpful comments on the manuscript, and J. Buschbom (BFH, Institute for Forest Genetics and Forest Tree Breeding) for correcting the English style. The authors apologize to colleagues whose relevant work has not been mentioned.


  1. Aldhouse P (2000) Inquiry blames missed warnings for scale of Britain's BSE Crisis. Nature 408:3–5CrossRefADSGoogle Scholar
  2. Anderson TW (1974) The chestnut pollen decline as a time horizont in lake sediments in eastern North America. Can J Earth Sci 11:678–685Google Scholar
  3. Aoki S, Syono K (1999) Horizontal gene transfer and mutation: Ngrol genes in the genome of Nicotiana glauca. Proc Nat Acad Scien 96:13229–13234CrossRefADSGoogle Scholar
  4. Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The Genetics of colonizing Species. Academic Press, New York, USA, pp 147–168Google Scholar
  5. Baker HG (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24CrossRefGoogle Scholar
  6. Bauce E, Carisey N, Dupont A, van Frankenhuyzen K (2004) Bacillus thuringiensis subsp. kurstaki aerial spray prescriptions for balsam fir stand protection against spruce budworm (Lepidoptera: Tortricidae). J Econ Entomol 97:1624–1634PubMedGoogle Scholar
  7. Bevan M (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acid Res 12:8711–8721PubMedCrossRefGoogle Scholar
  8. Binggeli P (1996) A taxonomic, biogeographical and ecological overview of invasive woody plants. J Veg Sci 7:121–124CrossRefGoogle Scholar
  9. BioSicherheit (2003)
  10. Bizili SP, Rugh CL, Meagher RB (2000) Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nat Biot 18:213–217CrossRefGoogle Scholar
  11. BMVEL (2004) Bundesministerium für Verbraucherschutz, Ernährung und Landwirtschaft.
  12. Boland GJ, Brimner T (2004) Nontarget effects of biological control agents. New Phytologist 163:455–457CrossRefGoogle Scholar
  13. Brasileiro ACM, Leplé JC, Muzzin J, Ounnoughi D, Michel MF, Jouanin L (1991) An alternative approach for gene transfer in trees using wild-type Agrobacterium strains. Plant Mol Biol 17:441–452CrossRefPubMedGoogle Scholar
  14. Brayshaw TC (1965) Native poplars of southern Alberta and their hybrids, Publ No. 1109. Department of Forestry, Otawa, Canada, pp 40Google Scholar
  15. Bright C (1999) Life out of bounds. Bioinvasion in a borderless world. Earthscan Publications Ltd, New York, USAGoogle Scholar
  16. Brimner TA, Boland GJ (2003) A review of the non-target effects of fungi used to biologically control plant diseases. Agric Ecosyst Environ 100:3–16CrossRefGoogle Scholar
  17. Brown JR (2003) Ancient horizontal gene transfer. Nature Rev Gen 4(2):121–132CrossRefGoogle Scholar
  18. Brunner AM, Mohamed R, Meilan R, Sheppard LA, Rottman WH, Strauss S (1998) Genetic engineering of sexual sterility in shade trees. J Arboriculture 24:263–271Google Scholar
  19. Cadogan BL, Scharbach RD (2003) Design and evaluation of an aerial spray trial with true replicates to test the efficacy of Bacillus thuringiensis insecticide in a boreal forest. J Econ Entomol 96:388–395PubMedGoogle Scholar
  20. Cagelli L, Lefèvre F (1995) The conservation of Populus nigra L. and gene flow with cultivated poplars in Europe. For Genet 2:135–144Google Scholar
  21. Campbell MM, Brunner AM, Jones HM, Strauss SH (2003) Forestry's Fertile Crescent: The application of biotechnology to forest trees. Plant Biotech J 1:141–154CrossRefGoogle Scholar
  22. Carlton JT (1999) A journal of biological invasions. Biol Invas 1:1CrossRefGoogle Scholar
  23. CBD (2003) Convention on Biological Diversity.
  24. Chiang V (2002) From rags to riches. Nat Biot 20:557–558CrossRefPubMedGoogle Scholar
  25. Chilton MD, Drummond MH, Merlo DJ, Sciaky D, Montoya AL, Gordon MP, Nester EW (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11:263–271CrossRefPubMedGoogle Scholar
  26. Cock MJW (2003) Biosecurity and forests: An introduction with particular emphasis on forest pests. FAO (Food and Agriculture Organization of the United Nations). Forestry Department. pp 60
  27. Coyle DR, Nebeker TE, Hart ER, Mattson WJ (2005) Biology and management of insect pests in North American intensively managed hardwood forest systems. Annu Rev Entomol 50:1–29CrossRefPubMedGoogle Scholar
  28. Dale PJ, Clarke B, Fontes EMG (2002) Potential for the environmental impact of transgenic crops. Nat Biot 20(6):567–574CrossRefGoogle Scholar
  29. DeAngelis CD (2000) Conflict of interest and the Public Trust. JAMA 284:2237–2238CrossRefPubMedGoogle Scholar
  30. Demeritt ME (1990) Populus L. Poplar hybrids. Salicaceae—Willow family. In: Burns RM, Honkala BH (eds) Silvics of North America, Vol 2. USDA For Serv, Washington, USA, pp 570–576Google Scholar
  31. DiFazio SP (2002) Measuring and Modelling Gene Flow from Hybrid Poplar Plantations: Implications for Transgenic Risk Assessment. PhD Dissertation, Oregon State UniversityGoogle Scholar
  32. Dong X (2004) Pathogen-induced systemic DNA rearrangement in plants. Trends Plant Sci 9:60–61CrossRefPubMedGoogle Scholar
  33. Dörfler W, Schubbert R (1998) Uptake of foreign DNA from the environment: the gastrointestinal tract and the placenta as portals of entry. Weiner Klin Woch 110–112:40–44Google Scholar
  34. Doyle U (2002) Ist die rechtliche Regulierung gebietsfremder Organismen in Deutschland ausreichend? In: Kowarik I, Starfinger U (eds) Biologische Invasionen: Herausforderung zum Handeln? Neobiota 1:259–272Google Scholar
  35. Dwinell LD (1997) The pinewood nematode: regulation and mitigation. Annu Rev Phytopathol 35:153–166CrossRefPubMedGoogle Scholar
  36. Eckenwalder JE (1977) North American cottonwoods (Populus, Salicaceae) of sections Abaso and Aigeiros. J Arnold Arboretum 58:193–208Google Scholar
  37. Eckenwalder JE (1984a) Natural intersectional hybridization between North American species of Populus (Salicaceae) in sections Aigeiros and Tacamahaca. I. Population studies. Can J Bot 62:317–324CrossRefGoogle Scholar
  38. Eckenwalder JE (1984b) Natural intersectional hybridization between North American species of Populus (Salicaceae) in sections Aigeiros and Tacamahaca. II. Taxonomy. Can J Bot 62:325–335CrossRefGoogle Scholar
  39. Eckenwalder JE (1984c) Natural intersectional hybridization between North American species of Populus (Salicaceae) in sections Aigeiros and Tacamahaca. III. Paleobotany and evolution. Can J Bot 62:336–342CrossRefGoogle Scholar
  40. EEA (European Environmengt Agency) (2004) Late lessons from early warnings: the precautionary principle 1896–2000 Environmental issue report No 22.
  41. Ellstrand NC, Kristina A, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Nat Acad Sci USA 97:7043–7050CrossRefPubMedADSGoogle Scholar
  42. EFSA (2004) Opinion of the Scientific Panel on Genetically Modified Organisms on the use of antibiotic resistance genes as marker genes in genetically modified plants. EFSA J 48:1–18,
  43. Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biot 18:784–788CrossRefPubMedGoogle Scholar
  44. FDA (Food and Drug Administration, USA) (1998) Use of Antibiotic Resistance Marker Genes in Transgenic Plants: Guidance for Industry.
  45. Filkowski J, Yeoman A, Kovalchuk O, Kovalchuk I (2004) Systemic plant signal triggers genome instability. Plant J 38:1–11CrossRefPubMedGoogle Scholar
  46. Fink S (1999) Pathological and regenerative plant anatomy. In: Zimmermann W, Braun HJ (eds) Encyclopedia of plant anatomy, Bd. 14, Teil 6. Borntaeger, Berlin, StuttgartGoogle Scholar
  47. Fisahn A, Winter G (1999) Die Aussetzung gebietsfremder Organismen. Recht und Praxis. Texte des Umweltbundesamtes 55/99, Berlin, 204 ppGoogle Scholar
  48. Fisher R, Budde I, Hain R (1997) Stilbene synthase gene expression causes changes in flower colour and male sterility in tobacco. The Plant J 11:489–498CrossRefGoogle Scholar
  49. Fitter A, Perrins J, Williamson M (1990) Weed probability challenged. Biotechnol 8:473CrossRefGoogle Scholar
  50. Fladung M (1999) Gene stability in transgenic aspen-Populus. I. Flanking DNA sequences and T-DNA structure. Mol Gen Genet 260:574–581CrossRefPubMedGoogle Scholar
  51. Fladung M, Gieffers W (1993) Resistance reactions of leaves and tubers of rolC transgenic tetraploid potato to bacterial and fungal pathogens. Correlation with sugar, starch and chlorophyll content. Phys Mol Plant Pathol 42:123–132CrossRefGoogle Scholar
  52. Fladung M, Gieffers W (2003) Untersuchungen zum Hormon- und Kohlenhydrat-Metabolismus in rolC transgenen Aspenklonen und deren mögliche Auswirkungen auf phytopathologische Eigenschaften. In: Fladung M (ed) Mitteilungen der Bundesforschungsanstalt für Forst- und Holzwirtschaft, Nr. 214, Hamburg, Germany, pp 81–112Google Scholar
  53. Fladung M, Großmann K, Ahuja MR (1997) Alterations in hormonal and developmental characteristics in transgenic Populus conditioned by the rolC gene from Agrobacterium rhizogenes. J Plant Physiol 150:420–427Google Scholar
  54. Fladung M, Hoenicka H (2004) Erzeugung transgener steriler Zitterpappeln zur Verhinderung eines vertikalen Gentransfers in forstliche Ökosysteme. Gesunde Pflanzen 56:195–200CrossRefGoogle Scholar
  55. Fladung M, Kaldorf M, Gieffers W, Ziegenhagen B, Muhs HJ, Kumar S (2004) Field analysis of transgenic aspen. In: Walter C, Carson M (eds) Plantation forest biotechnology for the 21st century. Research Signpost, Kerala, India, pp 393–403Google Scholar
  56. Fladung M, Kumar S (2002) Gene stability in transgenic aspen-Populus. III. T-DNA repeats influence transgene expression differentially among different transgenic lines. Plant Biology 4:329–338CrossRefGoogle Scholar
  57. Fladung M, Nowitzki O, Ziegenhagen B, Kumar S (2003) Vegetative and generative dispersal capacity of field released transgenic aspen trees. Trees 17:412–416Google Scholar
  58. Gartland KMA, Kellison RC, Fenning TM (2002) biotechnology and Europe's Forests of the future. A Challenge document for presentation and discussion at Forest Biotechnology Forum in Europe: Impending Barriers, Policy, and Implications. Edinburgh, Scotland, September 12–13, 2002Google Scholar
  59. Gartland KMA, Crow RM, Fenning TM, Gartland JS (2003) Genetically modified trees: production, properties and potential. J Arboriculture 29:259–266Google Scholar
  60. Gelvin SB (2003) Improving plant genetic engineering by manipulating the host. Trends Biotechnol 21:95–98CrossRefPubMedGoogle Scholar
  61. Genissel A, Viard F, Bourguet D (2000) Population genetics of Chrysomela tremulae: a first step towards management of transgenic Bacillus thuringiensis poplars Populus tremula × P. tremuloides. Hereditas 133:85–93CrossRefPubMedGoogle Scholar
  62. Glandorf DCM, Bakker PAHM, Van Loon LC (1997) Influence of the production of antibacterial and antifungal proteins by transgenic plants on the saprophytic soil microsflora. Acta Bot Neerl 46:85–104Google Scholar
  63. Golz C (1999) Stand der internationalen Regulierung von gentechnisch veränderten Organismen und der Risikoabschätzung. In: Gebietsfremde Organismen in Deutschland. Ergebnisse des Arbeitsgespräches am 5. und 6. März 1998, Texte des Umweltbundesamtes 55/99:99–107Google Scholar
  64. Grant V (1981) Plant Speciation. Columbia University Press, New York, USAGoogle Scholar
  65. Gregor W, Mette MF, Staginnus C, Matzke MA, Matzke AJ (2004) A distinct endogenous pararetrovirus family in Nicotiana tomentosiformis, a diploid progenitor of polyploid tobacco. Plant Physiol 134:1191–1199CrossRefPubMedGoogle Scholar
  66. Gullner G, Komives T, Rennenberg H (2001) Enhanced tolerance of transgenic poplar plants overexpressing gamma-glutamylcysteine synthase towards chloroacetanilide herbicides. J Exp Bot 52:971–979CrossRefPubMedGoogle Scholar
  67. Hackett WP (1985) Juvenility, maturation and rejuvenation in woody plants. Hort Rev 7:109–155Google Scholar
  68. Hancock JF, Grumet R, Hokanson SC (1996) The opportunity for escape of engineered genes from transgenic crops. Hort Sci 31:1080–1085Google Scholar
  69. Hancock JF (2003) A Framework for Assessing the Risk of Transgenic crops. Bio Sci 53:512–519Google Scholar
  70. Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 105:1–102CrossRefGoogle Scholar
  71. Hawkins S, Leple JC, Cornu D, Jouanin L, Pilate G (2003) Stability of transgene expression in poplar: a model forest tree species. Ann Forest Sci 60:427–438CrossRefGoogle Scholar
  72. Hoenicka H, Fladung M (2003) Evaluation of strategies for avoiding vertical gene transfer. Proceedings International Congress “BIOFOR 02”-Sustainable Forestry, Wood products and Biotechnology; Vitoria-Gasteiz, Spanien, NEIKER (Instituto Vasco de Investigación y Desarrollo Agrario), pp 221–226Google Scholar
  73. Hu WJ, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai CJ, Chiang VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotechnol 17:808–812CrossRefPubMedGoogle Scholar
  74. Huenneke LF, Vitousek PM (1990) Seedling and clonal recruitment of the invasive tree Psidium cattleianum: implications for management of native Hawaiian forests. Biological Conservation 53:199–211CrossRefGoogle Scholar
  75. Hull R, Covey SN, Dale P (2000) Genetically modified plants and the 35S promoter: assessing the risks and enhancing the debate. Micr Ecol Health Dis 12:1–5Google Scholar
  76. Inderjit, Duke S (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539CrossRefPubMedGoogle Scholar
  77. InfoNet-Umwelt-SH (Schleswig Holstein) (2004)
  78. Jakowitsch J, Mette MF, van der Winden J, Matzke MA, Matzke AJM (1999) Integrated sequences define a unique class of dispersed DNA in plants. Proc Natl Acad Sci 87:1633–1637Google Scholar
  79. Kaldorf M, Fladung M, Muhs HJ, Buscot F (2002) Mycorrhizal colonization of transgenic aspen in a field trial. Planta 214:653–660CrossRefPubMedGoogle Scholar
  80. Kazazian HH Jr (2004) Mobile elements: drivers of genome evolution. Science 303:1626–1632CrossRefPubMedADSGoogle Scholar
  81. Klopfenstein NB, Shi N-Q, Kernan A, McNabb HS, Hall RB, Hart ER, Thornburg RW (1991) A transgenic Populus hybrid expresses a wound-inducible potato Proteinase Inhibitor II-CAT gene fusion. Can J For Res 21:1321–1328CrossRefGoogle Scholar
  82. Kohli A, Griffiths S, Palacios N, Twyman RM, Vain P, Laurie DA and Christou P (1999) Molecular characterization of transforming plasmid rearrangements in transgenic rice reveals a recombination hotspot in the CaMV 35S promoter and confirms the predominance of microhomology mediated recombination. The Plant J 17:591–601CrossRefGoogle Scholar
  83. Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2:1201–1224CrossRefPubMedGoogle Scholar
  84. Kondo N, Nikoh N, Ijichi N, Shimada M, Fukatsu T (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Nat Acad Sci 99:14280–14285CrossRefPubMedADSGoogle Scholar
  85. Kouassi KC, Lorenzetti F, Guertin C, Cabana J, Mauffette Y (2001) Variation in the susceptibility of the forest tent caterpillar (Lepidoptera: Lasiocampidae) to Bacillus thuringiensis variety kurstaki HD-1: effect of the host plant. J Econ Entomol 94:1135–1141PubMedCrossRefGoogle Scholar
  86. Kovalchuk I, Kovalchuk O, Kalck V, Boyko V, Filkowski J, Heinlein M, Hohn B (2003) Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423:760–762CrossRefPubMedADSGoogle Scholar
  87. Kowarik I (1992) Einführung und Ausbreitung nichteinheimischer Gehölzarten in Berlin und Brandenburg. Verh Bot Ver Berlin Brandenburg Beih 3:188Google Scholar
  88. Kowarik I (1995) Time-lags in biological invasions. In: Pyšek P, Prach K, Rejmánek M, Wade W (eds) Plant invasions:general aspects and special problems. SPB Academic Publ, Amsterdam, pp 15–38Google Scholar
  89. Kowarik I (1999) Ecological aspects of the release of transgenic trees- experiences from biological invasions, In: Proceedings “Release of transgenic trees- present achievements, problems, future prospects”. Humboldt University, Berlin, pp 66–73Google Scholar
  90. Kowarik I (2003a) Human agency in biological invasions: secondary releases foster naturalization and population expansion of alien plant species. Biol Invas 5:293–312Google Scholar
  91. Kowarik I (2003b) Biologische Invasionen: Neophyten und Neozoen in Mitteleuropa. Verlag Eugen Ulmer, Stuttgart (Hohenheim)Google Scholar
  92. Kumar A, Bennetzen J (1999) Plant retrotransposons. Annu Rev Genet 33:479–532CrossRefPubMedGoogle Scholar
  93. Kumar S, Fladung M (2000a) Determination of T-DNA repeat formation and promoter methylation in transgenic plants. Bio Techniques 28:1128–1137Google Scholar
  94. Kumar S, Fladung M (2000b) Transgene repeats in aspen: molecular characterization suggests simultaneous integration of independent T-DNAs into a receiptive spot of host genome. Mol Gen Genet 264:20–28CrossRefPubMedGoogle Scholar
  95. 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 213:731–740CrossRefPubMedGoogle Scholar
  96. Kumar S, Fladung M (2002) Transgene integration in aspen: structures of integration sites and mechanism of T-DNA integration. Plant J 31:543–551CrossRefPubMedGoogle Scholar
  97. Lebel EG, Masson J, Bogucki A, Paszkowski J (1993) Stress-induced intrachromosomal recombination in plant somatic cells. Proc Natl Acad Sci USA 90:422–426PubMedCrossRefADSGoogle Scholar
  98. Lefèvre F, Legionnet A, de Vries S, Turok J (1998) Strategies for the conservation of a pioneer tree species, Populus nigra L., in Europe. Genet Sel Evol 30:S181–S196CrossRefGoogle Scholar
  99. Leplé JC, Brasileiro ACM, Michel MF, Delmotte F, Jouanin L (1992) Transgenic poplars: expression of chimeric genes using four different constructs. Plant Cell Rep 11:137–141CrossRefGoogle Scholar
  100. Lida W, Yifan H, Jianjun H (2003) Transgenic forest trees for insect resistance, Chapter 10. In: Kumar S, Fladung M (eds) Molecular Genetics and Breeding of Forest Trees. The Haworth Press, Binghamton, USA, pp 243–261Google Scholar
  101. Liebold AM, MacDonald WL, Bergdahl D, Mastro VC (1995) Invasion by exotic forest pests: a threat to forest ecosystems. Forest Science 41:1–49Google Scholar
  102. Loope LL, Müller-Dumbois D (1989) Characteristics of invaded islands, with special reference to Hawaii. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmanek M, Williamson M (eds) Biological invasions: a global perspective. John J Wiley and Sons Ltd., Scope, pp 257–280Google Scholar
  103. Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602PubMedGoogle Scholar
  104. Luby JJ, McNichol RF (1995) Gene flow from cultivated to wild raspberries in Scotland: developing a basis for risk assessment for testing and development of transgenic cultivars. Theor Appl Genet 90:113–1137CrossRefGoogle Scholar
  105. Lucht JM, Mauch-Mani B, Steiner HY, Metraux JP, Ryals J, Hohn B (2002) Pathogen stress increases somatic recombination frequency in Arabidopsis. Nature Genetics 30:311–314CrossRefPubMedGoogle Scholar
  106. MacNabb H (1971) A new look at Dutch elm disease control. The Amer Forest 58:14–18Google Scholar
  107. Mariani C, DeBeuckeleer J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by a chimeric ribonuclease gene. Nature 347:737–741CrossRefADSGoogle Scholar
  108. Matzke MA, Mette MF, Aufsatz W (2000) More on CaMV. Nat Biot 18:579CrossRefGoogle Scholar
  109. McNabb H (1971) A new look at Dutch elm disease control. The Ames Forester 58:14–18Google Scholar
  110. Meilan R, Brunner AM, Skinner JS, Strauss SH (2001) Modification of Flowering in Transgenic Trees. In: Morohoshi N, Komamine A (eds) Molecular Breeding of Woody Plants. Elsevier Science, BV, pp 247–256CrossRefGoogle Scholar
  111. Meyer P (1995) Gene silencing in higher plants and related phenomena in other eukaryotes. Springer Verlag, Berlin, GermanyGoogle Scholar
  112. Mitzukami Y, Huang H, Tudor M, Hu Y, Ma H (1996) Functional domains of the floral regulator AGAMOUS: Characterization of the DNA binding domain and analysis of dominant and analysis of dominant negative mutations. Plant Cell 8:831–845CrossRefPubMedGoogle Scholar
  113. Morra MJ (1994) Assessing the impact of transgenic plant products on soil organisms. Mol Ecol 3:53–55CrossRefGoogle Scholar
  114. Mouradov A, Sawbridge T, Hamdorf B, Glassick T, Murphy L, Marla S, Yang Y, Teasdale RD (1998) Genetic engineering of reproductive sterility in Pinus radiata. Acta Hoticulturae 461:417–423Google Scholar
  115. Mower JP, Stefanovic S, Young GJ, Palmer D (2004) Gene transfer from parasitic to host plants. Nature 432:165–166CrossRefPubMedADSGoogle Scholar
  116. Mullin TJ, Bertrand S (1998) Environmental release of transgenic trees in Canada-potencial benefits and assessment of biosafety. The Forestry Chronicle 74:203–220Google Scholar
  117. Myers RL (1983) Site susceptibility to invasion by the exotic tree Melaleuca quinquenervia in southern Florida. J App Ecol 20:645–658CrossRefGoogle Scholar
  118. Myhr AI, Traavik T (2002) Genetically modified (GM) crops: precautionary science and conflicts of interests. J Agric Env Ethics 16:227–247CrossRefGoogle Scholar
  119. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–305CrossRefPubMedADSGoogle Scholar
  120. OECD (2000) Environmental Health and Safety Publications. Series on harmonization of regulatory oversight in Biotechnology No. 16. Consensus document on the Biology of Populus L. (Poplars). Paris, FranceGoogle Scholar
  121. Pääbo S, Gifford JA, Wilson AC (1988) Mitochondrial DNA sequences from a 7000-year old brain. Nucl Ac Res 16:9775–9787CrossRefGoogle Scholar
  122. Palmiter RD, Behringer RR, Quaife CJ, Maxwell F, Maxwell IH, Brinster RL (1987) Cell lineage ablation in transgenic mice by cell-specific expression of a toxin gene. Cell 50:435–443CrossRefPubMedGoogle Scholar
  123. Paszkowski J (1994) Homologous recombination and gene silencing in plants. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  124. Peerenboom E (2000) German health minister calls time out for Bt maize. Nat Biot 18:374CrossRefGoogle Scholar
  125. Pilate G, Ellis D, Hawkins S (1997) Transgene expression in field-grown poplar. In: Klopfstein NB, Chun YW, Kim MS, Ahuia MR (eds) Micropropagation, Genetic Engineering, and Molecular Biology of Populus. Gen. Tech. Rep. RM-GRT-297. USDA, Fort Collins, CO, pp 84–89Google Scholar
  126. Pilate G, Emma G, Holt K, Petit-Conil M, Lapierre C, Leplè JC, Pollet B, Mila I, Webster EA, Marstorp H, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat Biot 20:607–612CrossRefPubMedGoogle Scholar
  127. Puchta H, Swoboda P, Gal S, Blot M, Hohn B (1995) Somatic intrachromosomal homologous recombination events in populations of plant siblings. Plant Mol Biol 28:281–292CrossRefPubMedGoogle Scholar
  128. Puls J, Reisen M, Saake B (2003) Vergleichende Untersuchungen zur Zusammensetzung der Zellwandkomponenten gentechnisch veränderter Aspen. In: Fladung M (ed) Mitteilungen der Bundesforschungsanstalt für Forst- und Holzwirtschaft, Nr. 214, Hamburg, Germany, pp 45–52Google Scholar
  129. Reichert S, Hamilton CW (1997) Predicting invasions of woody plants introduced into North America. Conservation Biology 11:193–203CrossRefGoogle Scholar
  130. Richardson DM, Higgins SI (1998) Pines as invaders in the southern hemisphere. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 450–473Google Scholar
  131. Richert-Poggeler KR, Shepherd RJ (1997) Petunia vein-clearing virus: a plant pararetrovirus with the core sequences for an integrase function. Virology 236:137–146CrossRefPubMedGoogle Scholar
  132. Ries G, Buchholz G, Frohnmeyer H, Hohn B (2000) UV-damage-mediated induction of homologous recombination in Arabidopsis is dependent on photosynthetically active radiation. Proc Natl Acad Sci USA 97:13425–13429CrossRefPubMedADSGoogle Scholar
  133. Riesenberg LH, Ellstrand NC (1993) What can molecular and morphological markers tell us about plant hybridisation? Crit Rev Plant Sci 12:213–241CrossRefGoogle Scholar
  134. Rogers DL (2002) In situ genetic conservation of Monterey pine (Pinus radiata D. Don): Information and recommendations. 2002. Report No. 26. University of California Division of Agriculture and Natural Resources, Genetic Resources Conservation Program, Davis, CA, USA. 92 p,
  135. Rood SB, Campbell JS, Despins T (1986) Natural poplar hybrids from southern Alberta. I. Continuous variation for foliar characteristics. Can J Bot 64:1382–1388CrossRefGoogle Scholar
  136. Rouget M, Richardson DM, Nel JL, van Wilgen BW (2002) Commercially important trees as invasive alien- towards spatially explicit risk assessment at a national scale. Biological Invasions 4:397–412CrossRefGoogle Scholar
  137. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:737–738CrossRefPubMedGoogle Scholar
  138. Schell J, Van Montagu M, De Beuckeleer M, De Block M, Depicker A, De Wilde M, Engler G, Genetello C, Hernalsteens JP, Holsters M, Seurinck J, Silva B, Van Vliet F, Villarroel R (1979) Interactions and DNA transfer between Agrobacterium tumefaciens, the Ti-plasmid and the plant host. Proc R Soc Lond B Biol Sci 204:251–266PubMedADSCrossRefGoogle Scholar
  139. Schlüter K, Potrykus I (1996) Horizontaler Gentransfer von transgenen Pflanzen zu Mikroorganismen (Bakterien und pilzen) und seine ökologische Relevanz. In: Schulte E, Käppeli O (eds) Gentechnisch veränderte krankheits- und schädlingsresistente Nutzpflanzen. Basel, Switzerland, pp 161–191Google Scholar
  140. Schreiner EJ (1974) Populus L. Poplar. In: Schopmeyer CS (ed) Agricultural Handbook No 450, Forest Service, Seeds of woody plants in the United States. USDA, Washington, DC, pp 645–655Google Scholar
  141. Schubbert R, Renz D, Schmitz B, Doerfler W (1997) Foreign (M13) DNA ingested by mice reaches peripheral leukocytes, spleen, and liver via the intestinal wall mucosa and can be covalently linked to mouse DNA. Proc Nat Acad Sci USA 94:961–966CrossRefPubMedADSGoogle Scholar
  142. Schwab E, Krause HA (2003) Holztechnologische Untersuchungen an gentechnisch veränderten Aspen. In: Fladung M (ed) Mitteilungen der Bundesforschungsanstalt für Forst- und Holzwirtschaft, Nr. 214, Hamburg, Germany, pp 53–80Google Scholar
  143. Shine C, Williams N, Gündling L (2000) A guide to designing legal and institutional frameworks on alien invasive species. Environmental policy and Law Paper No. 40. IUCN, Gland, Cambridge, Bonn, XVI + 138 ppGoogle Scholar
  144. Simberloff D, Relva MA, Nuñez M (2002) Gringos en el bosque: introduced tree invasion in a native Nothofagus/Austrocedrus forest. Biol Invasions 4:35–53CrossRefGoogle Scholar
  145. Simberloff D (2003) Confronting introduced species: a form of xenophobia? Biol Invasions 5:179–192CrossRefGoogle Scholar
  146. Skinner JS, Meilan R, Ma C, Strauss S (2003) The Populus PTD promoter imparts floral-predominant expression and enables high levels of floral-organ ablation in Populus, Nicotiana and Arabidopsis. Mol Breed 12:119–132CrossRefGoogle Scholar
  147. Smalla K, Van Overbeek LS, Pukall R, Van Elsas JD (1993) Prevalence of nptII and Tn5 in kanamycin-resistant bacteria from different environments. FEMS Microb Ecol 13:47–58CrossRefGoogle Scholar
  148. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, LondonGoogle Scholar
  149. Starfinger U (1998) On success in plant invasions. In: Starfinger U, Edwards K, Kowarik I, Williamson M (eds) Plant invasions: Ecological Mechanisms and Human Responses. Backhuys, Leiden, The Netherlands, pp 33–42Google Scholar
  150. Starfinger U, Kowarik I, Rode M, Schepker H (2003) From desirable ornamental plant to pest accepted addition to the flora?- the perception of an alien tree species through the centuries. Biol Invas 5:323–335CrossRefGoogle Scholar
  151. Stirn S (2000) Antibiotic resistance and horizontal gene transfer. BIOGHUM.
  152. Strauss SH, Rottmann WH, Brunner AM, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breed 1:5–26CrossRefGoogle Scholar
  153. Strauss SH, Knowe SA, Jenkins J (1997) Benefits and risk of transgenic, Roundup Ready cottonwoods. J Forestry 95:12–19Google Scholar
  154. Strauss SH, DiFazio SP, Meilan R (2001) Genetically modified poplars in context. The Forestry Chronicle 77:271–279Google Scholar
  155. Strauss SH, Brunner AM, Busov VB, Ma C, Meilan R (2004) Ten lessons from 15 years of transgenic populus research. Forestry 77:455–465CrossRefGoogle Scholar
  156. Tabbener HE, Cottrell JE (2002) The use of PCR based DNA markers to study the paternity of poplar seedlings. For Ecol Manag 179:363–376CrossRefGoogle Scholar
  157. Tepfer M (2002) Risk assessment in virus-resistant transgenic plants. Ann Rev Phytopathol 40:467–491CrossRefGoogle Scholar
  158. Usher MB (1988) Biological invasions of nature reserves: a search for generalisations. Biol Conserv 44:119–135CrossRefGoogle Scholar
  159. Valentine L (2003) Agrobacterium tumefaciens and the Plant: The David and Goliath of Modern Genetics. Plant Physiol 133:948–955CrossRefPubMedGoogle Scholar
  160. Van Aken B, Moon Yoon J, Schnorr JL (2004) Biodegradation of Nitro-substituted explosives 2,4,6-Trinitrotoluene, Hexahydro-1,3,5-Trinitro-1,3,5-Tetrazocine by a Phytosymbiotic Methylobacterium sp. Associated with poplar tissues (Populus deltoides x nigra DN34). App Env Microb 508–517Google Scholar
  161. Van den Eede G, Aarts H, Buhk H-J, Corthier G, Flint HJ, Hammes W, Jacobsen B, Midtvedt T, van den Vossen J., von Wright A, Wackernagel W, Wilks A (2004) The relevance of gene transfer to the safety of food and feed derived from genetically modified (GM) plants. Food Chem Tox 42:1127–1156CrossRefGoogle Scholar
  162. Vitousek PM, D'Antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. New Zealand J Ecol 21:1–16Google Scholar
  163. Vogel G (2005) Safety Research Falls Foul of German Politics. Science 307:1706CrossRefPubMedGoogle Scholar
  164. Wang WX, Vinocur B, Altman A (2004) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14CrossRefGoogle Scholar
  165. Wilcove DS, Rothstein D, Dobow J, Phillips A, Losos E (1998) Quantifying threats to imperilled species in the United States. Assessing the relative importance of habitat destruction, alien species, pollution, overexploitation, and disease. Bioscience 48:607–615CrossRefGoogle Scholar
  166. Williamson M (1993) Invaders, Weeds and the risk from genetically manipulated organisms. Experimentia 49:219–224CrossRefGoogle Scholar
  167. Williamson M, Brown KC (1986) The analysis and modelling of British invasions. Phil Trans R Soc London B 314:505–522CrossRefADSGoogle Scholar
  168. Williamson M, Perrings J, Fitter A (1990) A releasing genetically engineered plants: present proposals and possible hazards. Trend Ecol Evol 5:417–419CrossRefGoogle Scholar
  169. Wilson BC (1990) Gene-pool reserves of Douglas fir. For Ecol Manag 35:121–130CrossRefGoogle Scholar
  170. Witt KA (2002) The landscape ecology of invasive spread. Conservation Biology 16:1192–1203CrossRefGoogle Scholar
  171. Won H, Renner S (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Nat Acad Sc 100:10824–10829CrossRefADSGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Federal Research Centre for Forestry and Forest ProductsInstitute for Forest Genetics und Forest Tree BreedingGrosshansdorfGermany

Personalised recommendations