Tree Genetics & Genomes

, Volume 3, Issue 2, pp 75–100

Genetic containment of forest plantations

  • Amy M. Brunner
  • Jingyi Li
  • Stephen P. DiFazio
  • Olga Shevchenko
  • Brooke E. Montgomery
  • Rozi Mohamed
  • Hao Wei
  • Cathleen Ma
  • Ani Anna Elias
  • Katherine VanWormer
  • Steven H. Strauss
Review

Abstract

Dispersal of pollen, seeds, or vegetative propagules from intensively bred, exotic, or recombinant DNA modified forest plantations may cause detrimental or beneficial ecological impacts on wild or managed ecosystems. Insertion of genes designed to prevent or substantially reduce dispersal could reduce the risk and extent of undesired impacts. Containment measures may also be required by law or marketplace constraints, regardless of risks or benefits. We discuss: (1) the context for when genetic containment or mitigation systems may be needed; (2) technology approaches and mechanisms; (3) the state of knowledge on genes/genomics of sexual reproduction in forest trees; (4) stability of transgene expression during vegetative growth; (5) simulation studies to define the level of containment needed; and (6) needed research to deliver effective containment technologies. We illustrate progress with several examples from our research on recombinant DNA modified poplars. Our simulations show that even partial sterility can provide very substantial reductions in gene flow into wild trees. We conclude that it is impossible to define the most effective containment approaches, nor their reliability, based on current genomic knowledge and technological tools. Additional genomic and technological studies of a wide variety of options are needed. Studies in field environments are essential to provide data relevant to ecological analysis and regulatory decisions and need to be carried out in phylogenetically diverse representatives of the economically most important taxa of forest trees.

Keywords

Populus Pinus Eucalyptus Sterility Confinement Ablation Excision Genetic engineering Genetic modification Forest biotechnology Gene flow Trees Simulation Stability 

References

  1. Al-Ahmad H, Galili S, Gressel J (2004) Tandem constructs to mitigate transgene persistence: tobacco as a model. Mol Ecol 13:697–710PubMedGoogle Scholar
  2. Albert VA, Soltis DE, Carlson JE, Farmerie WG, Wall PK, Ilut DC, Solow TM, Mueller LA, Landherr LL, Hu Y, Buzgo M, Kim S, Yoo MJ, Frohlich MW, Perl-Treves R, Schlarbaum SE, Bliss BJ, Zhang X, Tanksley SD, Oppenheimer DG, Soltis PS, Ma H, DePamphilis CW, Leebens-Mack JH (2005) Floral gene resources from basal angiosperms for comparative genomics research. BMC Plant Biol 5:5PubMedGoogle Scholar
  3. Albertsen M, Huffman G (2002) Biotin-binding compounds for induction of sterility in plants. United States Patent and Trademark Office 20020129399Google Scholar
  4. Baudot G, Garcia D, Hodge R, Perez P (2001) DNA sequences coding for a protein conferring male sterility. United States Patent and Trademark Office 6,207,883Google Scholar
  5. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363PubMedGoogle Scholar
  6. Belostotsky DA, Meagher RB (1996) A pollen-, ovule-, and early embryo-specific poly (A) binding protein from Arabidopsis complements essential functions in yeast. Plant Cell 8:1261–1275PubMedGoogle Scholar
  7. Bern-d-Souza RB, Grossi de Sa MF, Ellis DD, McCown BH (2000) A rat ribonuclease fused to late cotton pollen promoter severely reduces pollen viability in tobacco plants. Genet Mol Biol 23:435–443Google Scholar
  8. Bettany AJE, Dalton S, Timms E, Morris P (1998) Stability of transgene expression during vegetative propagation of protoplast-derived tall fescue (Festuca arundinacea Schreb) J Exp Bot 49:1797–1804Google Scholar
  9. Boettiger S, Bennett AB (2006) Bayh-Dole: if we knew then what we know now. Nat Biotechnol 24:320–323PubMedGoogle Scholar
  10. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) The conserved CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043PubMedGoogle Scholar
  11. Borkowska M, Kleczkowski K, Pawelczak A, Wielgat B (1995) Transformation of diploid potato with an Agrobacterium tumefaciens binary vector system. II. Stability of transformation in tubers, micropropagated and greenhouse grown plants. Acta Physiol Plant 17:275–280Google Scholar
  12. Borner R, Kampmann G, Chandler J, Gleibner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24:591–599PubMedGoogle Scholar
  13. Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:18–31Google Scholar
  14. Bradford K, Van Deynze A, Gutterson N, Parrott W, Strauss SH (2005) Regulating transgenic crops sensibly: lessons from plant breeding, biotechnology and genomics. Nat Biotechnol 23:439–444PubMedGoogle Scholar
  15. Bradshaw HD Jr, Stettler RF (1993) Molecular genetics of growth and development in Populus. I. Triploidy in hybrid poplars. Theor Appl Genet 86:301–307Google Scholar
  16. Brenner ED, Katari MS, Stevenson DW, Rudd SA, Douglas AW, Moss WN, Twigg RW, Runko SJ, Stellari GM, McCombie WR, Coruzzi GM (2005) EST analysis in Ginkgo biloba: an assessment of conserved developmental regulators and gymnosperm specific genes. BMC Genomics 6:143PubMedGoogle Scholar
  17. Bridges I, Bright S, Greenland A, Schuch W (2001) Plant gene construct encoding a protein capable of disrupting the biogenesis of viable pollen. United States Patent and Trademark Office 6,172,279Google Scholar
  18. Brown G (2002) Method for enhancement of naturally occurring cytoplasmic male sterility and for restoration of male fertility and uses thereof in hybrid crop production. United States Patent and Trademark Office 20020133851, 2 patentsGoogle Scholar
  19. Brunner AM, Nilsson O (2004) Revisiting tree maturation and floral initiation in the poplar functional genomics era. New Phytol 164:43–51Google Scholar
  20. Brunner AM, Rottmann WH, Sheppard LA, Krutovskii K, DiFazio SP, Leonardi S, Strauss SH (2000) Structure and expression of duplicate AGAMOUS orthologues in poplar. Plant Mol Biol 44:619–634PubMedGoogle Scholar
  21. Burch-Smith TM, Anderson JC, Martin GB, Dinesh-Kumar SP (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J 39:734–746PubMedGoogle Scholar
  22. Burgess DG, Ralston EJ, Hanson WG, Heckert M, Ho M, Jenq T, Palys JM, Tang K, Gutterson N (2002) A novel, two-component system for cell lethality and its use in engineering nuclear male-sterility in plants. Plant J 31:113–125PubMedGoogle Scholar
  23. Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 24:288–299Google Scholar
  24. Carlsbecker A, Sundstrom J, Tandre K, Englund M, Kvarnheden A, Johanson U, Engstrom P (2003) The DAL10 gene from Norway spruce (Picea abies) belongs to a potentially gymnosperm-specific subclass of MADS-box genes and is specifically active in seed cones and pollen cones. Evol Dev 5:551–561PubMedGoogle Scholar
  25. Carlsbecker A, Tandre K, Johanson U, Englund M, Engstrom P (2004) The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). Plant J 40:546–557PubMedGoogle Scholar
  26. Cashore B, Auld G, Newsom D (2003) Forest certification (eco-labeling) programs and their policymaking authority: explaining divergence among North American and European case studies. FPE 5:225–247Google Scholar
  27. Cervera M, Pina JA, Juárez J, Navarro L, Peña L (2000) A broad exploration of a transgenic population of citrus: stability of gene expression and phenotype. Theor Appl Genet 100:670–677Google Scholar
  28. Chen Y, Schneeberger RG, Cullis CA (2005) A site-specific insertion sequence in flax genotrophs induced by environment. New Phytol 167:171–180PubMedGoogle Scholar
  29. Cho H, Kim S, Kim M, Kim B (2001) Production of transgenic male sterile tobacco plants with the cDNA encoding a ribosome inactivating protein in Dianthus sinensis. Mol Cells 11:326–333PubMedGoogle Scholar
  30. Chrimes D, Rogers HJ, Francis D, Jones HD, Ainsworth C (2005) Expression of fission yeast cdc25 driven by the wheat ADP-glucose pyrophosphorylase large subunit promoter reduces pollen viability and prevents transmission of the transgene in wheat. New Phytol 166:185–192PubMedGoogle Scholar
  31. Chuang CF, Meyerowitz EM (2000) Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:4985–4990PubMedGoogle Scholar
  32. Cigan A, Albertsen M (2002) Reversible nuclear genetic system for male sterility in transgenic plants. United States Patent and Trademark Office 6,399,856, 8 patentsGoogle Scholar
  33. Cigan AM, Unger-Wallace E, Haug-Collet K (2005) Transcriptional gene silencing as a tool for uncovering gene function in maize. Plant J 43:929–940PubMedGoogle Scholar
  34. Clark JS, Lewis M, McLachlan JS, HilleRisLambers J (2003) Estimating population spread: what can we forecast and how well? Ecology 84:1979–1988Google Scholar
  35. Comai L, Cartwright RA (2005) A toxic mutator and selection alternative to the non-Mendelian RNA cache hypothesis for hothead reversion. Plant Cell 17:2856–2858PubMedGoogle Scholar
  36. Conner AJ, Mlynrov L, Stiekema WJ, Nap J (1998) Meiotic stability of transgene expression is unaffected by flanking matrix-associated regions. Mol Breed 4:47–58Google Scholar
  37. Crawley MJ, Brown SL (1995) Seed limitation and the dynamics of feral oilseed rape on the M25 motorway. Proc R Soc Lond B Biol Sci 259:49–54Google Scholar
  38. Cseke LJ, Zheng J, Podila GK (2003) Characterization of PTM5 in aspen trees: a MADS-box gene expressed during woody vascular development. Gene 318:55–67PubMedGoogle Scholar
  39. Cummins J, Ho MW (2005) Terminator Trees ISIS http://www.i-sis.org.uk/full/TerminatorTreesFull.php (accessed March 10, 2006)
  40. Daniel TW, Helms JA, Baker FS (1979) Principles of silviculture. McGraw-Hill, NYGoogle Scholar
  41. Davis W (2000) Mutant male sterile gene of soybean. United States Patent and Trademark Office 6,046,385Google Scholar
  42. de Folter S, Immink RG, Kieffer M, Parenicova L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17:1424–1433PubMedGoogle Scholar
  43. Dellaporta S, Moreno M (2004) Methods and compositions to reduce or eliminate transmission of a transgene. United States Patent and Trademark Office 20040154054Google Scholar
  44. Dievart A, Dalal M, Tax FE, Lacey AD, Huttly A, Li J, Clark SE (2003) CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell 15:1198–1211PubMedGoogle Scholar
  45. DiFazio SP (2002) Measuring and Modeling Gene Flow from Hybrid Poplar Plantations: Implications for Transgenic Risk Assessment. Ph.D. Thesis, Oregon State University, Corvallis, OR. http://www.fsl.orst.edu/tgerc/dif_thesis/difaz_thesis.pdf
  46. Dirks R, Trinks K, Uijtewaal B, Bartsch K, Peeters R, Hofgen R, Pohlenz H-D (2001) Process for generating male sterile plants. United States Patent and Trademark Office 6,262,339Google Scholar
  47. Doering DS (2004) Designing genes: aiming for safety and sustainability in U.S. agriculture and biotechnology. World Resources Institute, Washington, DC, p 43Google Scholar
  48. Dunning JB, Stewart DJ, Danielson BJ, Noon BR, Root TL, Lamberson RH, Stevens EE (1995) Spatially explicit population models: current forms and future uses. Ecol Appl 5:3–11Google Scholar
  49. Ellstrand NC (2003) Dangerous liaisons? when cultivated plants mate with their wild relatives. The Johns Hopkins University Press, Baltimore p 244Google Scholar
  50. Elo A, Lemmetyinen J, Turunen ML, Tikka L, Sopanen T (2001) Three MADS-box genes similar to APETALA1 and FRUITFUL from silver birch (Betula pendula). Physiol Plant 112:95–103PubMedGoogle Scholar
  51. Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M (2005) Ectopic expression of an FT homolog from citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 14:703–712PubMedGoogle Scholar
  52. ETC (2006) Terminator threat looms. ETC Group http://www.etcgroup.org/ (accessed March 10, 2006)
  53. Ferrario S, Busscher J, Franken J, Gerats T, Vandenbussche M, Angenent GC, Immink RG (2004) Ectopic expression of the petunia MADS box gene UNSHAVEN accelerates flowering and confers leaf-like characteristics to floral organs in a dominant-negative manner. Plant Cell 16:1490–1505PubMedGoogle Scholar
  54. Fisher RA (1937) The wave of advance of advantageous genes. Ann Eugen 7:355–369Google Scholar
  55. Fladung M (1999) Gene stability in transgenic aspen (Populus). I. Flanking DNA sequences and T-DNA structure. Mol Gen Genet 260:574–581PubMedGoogle Scholar
  56. Gallo-Meagher M, Irvine JE (1996) Herbicide resistant transgenic sugarcane plants containing the bar gene. Crop Sci 36:1367–1374CrossRefGoogle Scholar
  57. Gilbertson L (2003) Cre-lox recombination: cre-ative tools for plant biotechnology. Trends Biotechnol 21:550–555PubMedGoogle Scholar
  58. Goetz M, Godt DE, Giuvarch A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98:6522–6527PubMedGoogle Scholar
  59. Gressel J (1999) Tandem constructs: preventing the rise of superweeds. Trends Biotechnol 17:361–366PubMedGoogle Scholar
  60. Groover AT (2005) What genes make a tree a tree? Trends Plant Sci 10:210–214PubMedGoogle Scholar
  61. Guan X, Stege J, Kim M, Dahmani Z, Fan N, Heifetz P, Barbas CF 3rd, Briggs SP (2002) Heritable endogenous gene regulation in plants with designed polydactyl zinc finger transcription factors. Proc Natl Acad Sci USA 99:13296–13301PubMedGoogle Scholar
  62. Guerineau F, Sorensen A, Fenby N, Scott RJ (2003) Temperature sensitive diphtheria toxin confers conditional male-sterility in Arabidopsis thaliana. Plant Biotechnol J 1:33–42PubMedGoogle Scholar
  63. Hails RS, Morley K (2005) Genes invading new populations: a risk assessment perspective. Trends Ecol Evol 20:245–252PubMedGoogle Scholar
  64. Han Y, Griffiths A, Li H, Grierson D (2004) The effect of endogenous mRNA levels on co-suppression in tomato. FEBS Lett 563:123–128PubMedGoogle Scholar
  65. Harberd N, Peng J, Carol P, Richards D (2004a) Nucleic acid encoding GAI gene of Arabidopsis thaliana. United States Patent and Trademark Office 6,830,930Google Scholar
  66. Harberd N, Richards DE, Peng J (2004b) Genetic control of plant growth and development. United States Patent and Trademark Office 6,762,348Google Scholar
  67. Hawkins S, Leplé J, Cornu D, Jouanin L, Pilate G (2003) Stability of transgene expression in poplar: a model forest tree species. Ann For Sci 60:427–438Google Scholar
  68. Haygood R, Ives AR, Andow DA (2003) Consequences of recurrent gene flow from crops to wild relatives. Proc Biol Sci 270:1879–1886PubMedGoogle Scholar
  69. Higgins SI, Cain ML (2002) Spatially realistic plant metapopulation models and the colonization-competition trade-off. J Ecol 90:616–626Google Scholar
  70. Higgins SI, Richardson DM (1999) Predicting plant migration rates in a changing world: the role of long-distance dispersal. Am Nat 153:464–475Google Scholar
  71. Higgins SI, Richardson DM, Cowling RM (1996) Modeling invasive plant spread: the role of plant–environment interactions and model structure. Ecology 77:2043–2054Google Scholar
  72. Hill RA (2005) Conceptualizing risk assessment methodology for genetically modified organisms. Environ Biosafety Res 4:67–70PubMedGoogle Scholar
  73. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739PubMedGoogle Scholar
  74. Hird DL, Paul W, Hollyoak JS, Scott RJ (2000) The restoration of fertility in male sterile tobacco demonstrates that transgene silencing can be mediated by T-DNA that has no DNA homology to the silenced transgene. Transgenic Res 9:91–102PubMedGoogle Scholar
  75. Hoenicka H, Fladung M (2006a) Biosafety in Populus spp. and other forest trees: from non-native species to taxa derived from traditional breeding and genetic engineering. Trees 20:131–144Google Scholar
  76. Hoenicka H, Fladung M (2006b) Genome instability in woody plants derived from genetic engineering. In: Fladung M, Ewald D (eds) Tree transgenesis-recent developments. Springer, Berlin Heidelberg New York, pp 301–321Google Scholar
  77. Höfig KP, Möller R, Donaldson L, Putterill J, Walter C (2006) Towards male-sterility in Pinus radiata—a stilbene synthase approach to genetically engineer nuclear male sterility. Plant Biotechnol J 4:333–343PubMedGoogle Scholar
  78. Howard RD, DeWoody JA, Muir WM (2004) Transgenic male mating advantage provides opportunity for Trojan gene effect in a fish. Proc Natl Acad Sci USA 101:2934–2938PubMedGoogle Scholar
  79. Hsu CY, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18(8):1846–1861PubMedGoogle Scholar
  80. Iglesias VA, Moscone EA, Papp I, Neuhuber F, Michalowshi S, Phelan T, Spiker S, Matzke M, Matzke AJM (1997) Molecular and cytogenetic analyses of stably and unstably expressed transgene loci in tobacco. Plant Cell 9:1251–1264PubMedGoogle Scholar
  81. Irish VF, Litt A (2005) Flower development and evolution: gene duplication, diversification and redeployment. Curr Opin Genet Dev 15:454–460PubMedGoogle Scholar
  82. ISAAA (2006) Brazil: curtailing research and technological innovation. CropBiotech Update, International Service for the Acquisition of Agri-biotech Applications, SEAsia Center, 14 July 2006. http://www.cedab.it/newsletter_ISAAA.asp?IDnews=127#ancora2, accessed July 29, 2006
  83. Jackson AL, Linsley PS (2004) Noise amidst the silence: off-target effects of siRNAs? Trends Genet 20:521–524PubMedGoogle Scholar
  84. Jager M, Hassanin A, Manuel M, Le Guyader H, Deutsch J (2003) MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Mol Biol Evol 20:842–854PubMedGoogle Scholar
  85. James RR, DiFazio SP, Brunner AM, Strauss SH (1998) Environmental effects of genetic engineering of woody biomass crops. Biomass Bioenergy 14:403–414Google Scholar
  86. James V, Worland B, Snape JW, Vain P (2004) Strategies for precise quantification of transgene expression levels over several generations in rice. J Exp Bot 55:1307–1313PubMedGoogle Scholar
  87. Jeon JS, Jang S, Lee S, Nam J, Kim C, Lee SH, Chung YY, Kim SR, Lee YH, Cho YG, An G (2000) Leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12:871–884PubMedGoogle Scholar
  88. Johnson B, Kirby K (2004) Potential impacts of genetically modified trees on biodiversity of forestry plantations: a global perspective. In: Strauss SH, Bradshaw HD (eds) The bio engineered forest: challenges to science and society. Resources for the future. Washington DC, pp 190–207Google Scholar
  89. Katul GG, Porporato A, Nathan R, Siqueira M, Soons MB, Poggi D, Horn HS, Levin SA (2005) Mechanistic analytical models for long-distance seed dispersal by wind. Am Nat 166:368–381PubMedGoogle Scholar
  90. Kelly CK, Bowler MG, Breden F, Fenner M, Poppy GM (2005) An analytical model assessing the potential threat to natural habitats from insect resistance transgenes. Proc Biol Sci 272:1759–1767PubMedGoogle Scholar
  91. Kerschen A, Napoli CA, Jorgensen RA, Muller AE (2004) Effectiveness of RNA interference in transgenic plants. FEBS Lett 566:223–228PubMedGoogle Scholar
  92. Kilby NJ, Leyser HMO, Furner IJ (1992) Promoter methylation and progressive transgene inactivation in Arabidopsis. Plant Mol Biol 20:103–112PubMedGoogle Scholar
  93. Knox R, Singh M, Xu H (2004) Developmental regulation in anther tissue of plants. United States Patent and Trademark Office 6,740,748Google Scholar
  94. Kohli A, Gahakwa D, Vain P, Laurie DA, Christou P (1999) Transgene expression in rice engineered through particle bombardment: molecular factors controlling stable expression and transgene silencing. Planta 208:88–97Google Scholar
  95. Kreiman G (2004) Identification of sparsely distributed clusters of cis-regulatory elements in sets of co-expressed genes. Nucleic Acids Res 32:2889–2900PubMedGoogle Scholar
  96. 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 213:731–740PubMedGoogle Scholar
  97. Kuvshinov VV, Koivu K, Kanerva A, Pehu E (2001) Molecular control of transgene escape from genetically modified plants. Plant Sci 160:517–522PubMedGoogle Scholar
  98. Kyozuka J, Harcourt R, Peacock WJ, Dennis ES (1997) Eucalyptus has functional equivalents of the Arabidopsis AP1 gene. Plant Mol Biol 35:573–584PubMedGoogle Scholar
  99. 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 BPFULL1::BARNASE construct. Plant Cell Rep 24:69–78PubMedGoogle Scholar
  100. Lavorel S, Smith MS, Reid N (1999) Spread of mistletoes (Amyema preissii) in fragmented Australian woodlands: a simulation study. Landsc Ecol 14:147–160Google Scholar
  101. Lee YH, Chung KH, Kim HU, Jin YM, Kim HI, Park BS (2003) Introduction of male sterile cabbage using a tapetum-specific promoter from Brassica campestris L. ssp. pekinensis. Plant Cell Rep 22:268–273PubMedGoogle Scholar
  102. Leibbrandt NB, Snyman SJ (2003) Stability of gene expression and agronomic performance of a transgenic herbicide-resistant sugarcane line in South Africa. Crop Sci 43:671–677CrossRefGoogle Scholar
  103. Lemmetyinen J, Keinonen K, Sopanen T (2004a) Prevention of flowering of a tree, silver birch. Mol Breed 13:243–249Google Scholar
  104. Lemmetyinen J, Hassinen M, Elo A, Porali I, Keinonen K, Makela H, Sopanen T (2004b) Functional characterization of SEPALLATA3 and AGAMOUS orthologues in silver birch. Physiol Plant 121:149–162PubMedGoogle Scholar
  105. Li X, Zhong S, Wong WH (2005) Reliable prediction of transcription factor binding sites by phylogenetic verification. Proc Natl Acad Sci USA 102:16945–16950PubMedGoogle Scholar
  106. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol Biol 52:511–526PubMedGoogle Scholar
  107. Lloyd A, Plaisier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci USA 102:2232–2237PubMedGoogle Scholar
  108. Lolle SJ, Victor JL, Young JM, Pruitt RE (2005) Genome-wide non-Mendelian inheritance of extra-genomic information in Arabidopsis. Nature 434:505–509PubMedGoogle Scholar
  109. Luo H, Kausch AP, Hu Q, Nelson K, Wipff JK, Fricker CC, Owen T, Moreno MA, Lee J, Hodges TK (2005) Controlling transgene escape in GM creeping bentgrass. Mol Breed 16:185–188Google Scholar
  110. Mariani C, Beuckeleer M.D, Truettner J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by a chimaeric ribonuclease gene. Nature 347:737–741Google Scholar
  111. Mariani C, Gossele V, Beuckeleer MD, Block MD, Goldberg RB, Greef WD, Leemans J (1992) A chimaeric ribonuclease-inhibitor gene restores fertility to male sterile plants. Nature 357:384–387Google Scholar
  112. Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35PubMedGoogle Scholar
  113. Matzke M, Aufsatz W, Kanno T, Daxinger L, Papp I, Mette MF, Matzke AJ (2004) Genetic analysis of RNA-mediated transcriptional gene silencing. Biochim Biophys Acta 1677:129–141PubMedGoogle Scholar
  114. 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 four years of field trials and vegetative propagation. HortScience 37:277–280Google Scholar
  115. Mellerowicz EJ, Horgan K, Walden A, Coker A, Walter C (1998) PRFLL-a Pinus radiata homologue of FLORICAULA and LEAFY is expressed in buds containing vegetative shoot and undifferentiated male cone primordia. Planta 206:619–629PubMedGoogle Scholar
  116. Meyer P, Linn F, Heidmann I, Meyer H, Niedenhof I, Saedler H (1992) Endogenous and environmental factors influence 35S promoter methylation of a maize A1 gene construct in transgenic petunia and its colour phenotype. Mol Gen Genet 231:345–352PubMedGoogle Scholar
  117. Meza TJ, Kamfjord D, Hakelien A, Evans I, Godager LH, Mandal A, Jakobsen KS, Aalen RB (2001) The frequency of silencing in Arabidopsis thaliana varies highly between progeny of siblings and can be influenced by environmental factors. Transgenic Res 10:53–67PubMedGoogle Scholar
  118. Michiels F, Botterman J, Cornelissen M (2000) Method to obtain male sterile plants. United States Patent and Trademark Office 6,025,546Google Scholar
  119. Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138:1903–1913PubMedGoogle Scholar
  120. Missiaggia AA, Piacezzi AL, Grattapaglia D (2005) Genetic mapping of Eef1, a major effect QTL for early flowering in Eucalyptus grandis. Tree Genet Genomes 1:79–84Google Scholar
  121. Mitsuda N, Hiratsu K, Todaka D, Nakashima K, Yamaguchi-Shinozaki K, Ohme-Takagi M (2006) Efficient production of male and female sterile plants by expression of a chimeric repressor in Arabidopsis and rice. Plant Biotechnol J 4:325–332PubMedGoogle Scholar
  122. Mohamed R (2006) Expression and function of Populus homologs to TERMINAL FLOWER 1 genes: roles in onset of flowering and shoot phenology. Ph.D. Thesis, Oregon State University, Corvallis, Oregon USA. 136 pp. http://www.fsl.orst.edu/tgerc/strauss/Rozi_Mohamed_PhD Thesis_January 2006.pdf (accessed March 16, 2006)
  123. Morina K, Olsen O, Shimamoto K (1999) Silencing of an aleurone-specific gene in transgenic rice is caused by a rearranged trangsgene. Plant J 17:275–285Google Scholar
  124. Mou Z, Wang X, Fu Z, Dai Y, Han C, Ouyang J, Bao F, Hu Y, Li J (2002) Silencing of phosphoethanolamine N-methyltransferase results in temperature-sensitive male sterility and salt hypersensitivity in Arabidopsis. Plant Cell 14:2031–2043PubMedGoogle Scholar
  125. Mouradov A, Glassick T, Hamdorf B, Murphy L, Fowler B, Marla S, Teasdale RD (1998) NEEDLY, a Pinus radiata ortholog of FLORICAULA/LEAFY genes, expressed in both reproductive and vegetative meristems. Proc Natl Acad Sci USA 95:6537–6542PubMedGoogle Scholar
  126. Müller AJ, Mendel RR, Schiemann J, Simoens C, Inzé D (1987) High meiotic stability of a foreign gene introduced into tobacco by Agrobacterium-mediated transformation. Mol Gen Genet 207:171–175PubMedGoogle Scholar
  127. Mlynárová L, Conner AJ, Nap J-P (2006) Directed microspore-specific recombination of transgenic alleles to prevent pollen-mediated transmission of transgenes. Plant Biotechnol J 4:445–452PubMedGoogle Scholar
  128. 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 418:409–413PubMedGoogle Scholar
  129. Nathan R, Perry G, Cronin JT, Strand AE, Cain ML (2003) Methods for estimating long-distance dispersal. Oikos 103:261–273Google Scholar
  130. 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 Methods 124:27–36PubMedGoogle Scholar
  131. NRC (2004) Biological confinement of genetically engineered organisms. The National Academies, Washington, DC p 256Google Scholar
  132. Ottaviani MP, Hanisch ten Cate CH, Doting LV (1992) Expression of introduced genes after tuber propagation of transgenic potato plants. Plant Breed 109:89–96Google Scholar
  133. Ouellet T, Singh J, Tao T, Simmonds J (2003) Corn silk gene and regulatory region. United States Patent and Trademark Office 6,515,204Google Scholar
  134. Parker IM, Kareiva P (1996) Assessing the risks of invasion for genetically engineered plants: acceptable evidence and reasonable doubt. Biol Conserv 78:193–203Google Scholar
  135. Patell V, Rayapuram N, Venkataramiah M, Joma J, Goswami S (2003) Process for generating cytoplasmic male sterile line in rice and other crops by RNA editing. United States Patent and Trademark Office 20030163856Google Scholar
  136. Pavingerová D, Dostál J, Bísková R, Benetka V (1994) Somatic embryogenesis and Agrobacterium-mediated transformation of chrysanthemum. Plant Sci 97:95–101Google Scholar
  137. Pena L, Martin-Trillo M, Juarez J, Pina JA, Navarro L, Martinez-Zapater JM (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat Biotechnol 19:263–267PubMedGoogle Scholar
  138. Petersen BO, Albrechtsen M (2005) Evidence implying only unprimed RdRP activity during transitive gene silencing in plants. Plant Mol Biol 58(4):575–583PubMedGoogle Scholar
  139. Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Lepl’e J, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, and Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat Biotechnol 20:607–612PubMedGoogle Scholar
  140. Pilson D, Prendeville HR (2004) Ecological effects of transgenic crops and the escape of transgenes into wild populations. Annu Rev Ecol Evol Syst 35:149–174Google Scholar
  141. Poovaiah B, Patil S, Takezawa D (2002) Compositions and methods for production of male-sterile plants. United States Patent and Trademark Office 6,403,352Google Scholar
  142. Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995PubMedGoogle Scholar
  143. Quandt J, Bartsch K, Knittel N (2002) Conditional sterility in wheat. United States Patent and Trademark Office 6,384,304Google Scholar
  144. Raser JM, O’Shea EK (2004) Control of stochasticity in eukaryotic gene expression. Science 304:1811–1814PubMedGoogle Scholar
  145. Ray A, Golden T (2004) Gene encoding short integuments and uses thereof. United States Patent and Trademark Office 6,737,561Google Scholar
  146. Rees M, Paynter Q (1997) Biological control of Scotch broom: modeling the determinants of abundance and the potential impact of introduced insect herbivores. J Appl Ecol 34:1203–1221Google Scholar
  147. Rombauts S, Florquin K, Lescot M, Marchal K, Rouze P, van de Peer Y (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiol 132:1162–1176PubMedGoogle Scholar
  148. Rood SB, Kalischuk AR, Polzin ML, Braatne JH (2003) Branch propagation, not cladoptosis, permits dispersive, clonal reproduction of riparian cottonwoods. For Ecol Manag 186:227–242Google Scholar
  149. Rottmann WH, Meilan R, Sheppard LA, Brunner AM, Skinner JS, Ma C, Cheng S, Jouanin L, Pilate G, Strauss SH (2000) Diverse effects of over expression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLOICAULA, in transgenic poplar and Arabidopsis. Plant J 22:235–245PubMedGoogle Scholar
  150. Rutledge R, Regan S, Nicolas O, Fobert P, Cote C, Bosnich W, Kauffeldt C, Sunohara G, Seguin A, Stewart D (1998) Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. Plant J 15:625–634PubMedGoogle Scholar
  151. Scheid OM, Paszkowski J, Potrykus I (1991) Reversible inactivation of a transgene in Arabidopsis thaliana. Mol Gen Genet 228:104–112Google Scholar
  152. Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130:6001–6012PubMedGoogle Scholar
  153. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506PubMedGoogle Scholar
  154. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527PubMedGoogle Scholar
  155. Scortecci KC, Michaels SD, Amasino RM (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that repress flowering. Plant J 26:229–236PubMedGoogle Scholar
  156. Segal DJ, Stege JT, Barbas CF 3rd (2003) Zinc fingers and a green thumb: manipulating gene expression in plants. Curr Opin Plant Biol 6:163–168PubMedGoogle Scholar
  157. Shaked H, Melamed-Bessudo C, Levy AA (2005) High-frequency gene targeting in Arabidopsis plants expressing the yeast RAD54 gene. Proc Natl Acad Sci USA 102:12265–12269PubMedGoogle Scholar
  158. Sheppard LA, Brunner AM, Krutovskii KV, Rottmann WH, Skinner JS, Vollmer SS, Strauss SH (2000) A DEFICIENS homolog from the dioecious tree Populus trichocarpa is expressed in both female and male floral meristems of its two-whorled, unisexual flowers. Plant Physiol 124:627–640PubMedGoogle Scholar
  159. Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, New York, p 205Google Scholar
  160. Shindo S, Ito M, Ueda K, Kato M, Hasebe M (1999) Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Dev 1:180–190PubMedGoogle Scholar
  161. Skinner JS, Meilan R, Brunner AM, Strauss SH (2000) Options for genetic engineering of floral sterility in forest trees. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants. Kluwer, Dordrecht, The Netherlands, pp 135–153Google Scholar
  162. Skinner JS, Meilan R, Ma C, Strauss SH (2003) The Populus PTD promoter imparts floral-predominant expression and enables high levels of floral-organ ablation in Populus, Nicotiana and Arabidopsis. Mol Breed 12:119–132Google Scholar
  163. Slavov, GT, DiFazio SP, Strauss SH (2004) Gene flow in forest trees: gene migration patterns and landscape modeling of transgene dispersal in hybrid poplar. In: den Nijs HCM, Bartsch D, Sweet J (eds) Introgression from genetically modified plants into wild relatives. CAB International, UK, pp 89–106Google Scholar
  164. Smeekens S, Weisbeek P, Proveniers M (2005) Plant gene constructs and their use. United States Patent and Trademark Office 6,864,051Google Scholar
  165. Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. For Ecol Manage 197:21–38Google Scholar
  166. Snow AA, Andow DA, Gepts P, Hallerman EM, Power A, Tiedje JM, Wolfenbarger LL (2005) Genetically engineered organisms and the environment: current status and recommendations. Ecol Appl 15:377–404Google Scholar
  167. Southerton SG, Marshall H, Mouradov A, Teasdale RD (1998) Eucalypt MADS-box genes expressed in developing flowers. Plant Physiol 118:365–372PubMedGoogle Scholar
  168. Spena A, Saedler H, Sommer H, Rotino G (2002) Methods for producing parthenocarpic or female sterile transgenic plants and methods for enhancing fruit setting and development. United States Patent and Trademark Office 6,483,012Google Scholar
  169. Stewart CN, Halfhill MD, Warwick SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Genet 4:806–817PubMedGoogle Scholar
  170. Stoutjesdijk PA, Singh SP, Liu Q, Hurlstone CJ, Waterhouse PA, Green AG (2002) hpRNA-mediated targeting of the Arabidopsis FAD2 gene gives highly efficient and stable silencing. Plant Physiol 129:1723–1731PubMedGoogle Scholar
  171. Strauss SH (2003) Genomics, genetic engineering, and domestication of crops. Science 300:61–62PubMedGoogle Scholar
  172. Strauss SH, Bradshaw HD (eds) (2004) The bioengineered forest: challenges to science and society. Resources for the Future, Washington, DC, p 245Google Scholar
  173. Strauss SH, Brunner AM (2004) Tree biotechnology in the 21st century: Transforming trees in the light of comparative genomics. In: Strauss SH, Bradshaw HD (eds) The bioEngineered forest: challenges to science and society. Resources for the Future, Washington, DC, pp 76–97Google Scholar
  174. Strauss SH, Rottmann WH, Brunner AW, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breed 1:5–26Google Scholar
  175. Strauss SH, Coventry P, Campbell MM, Pryor SM, Burley J (2001a) Certification of genetically modified forest plantations. Int For Rev 3:87–104Google Scholar
  176. Strauss SH, Campbell MM, Pryor SN, Coventry P, Burley J (2001b) Plantation certification and genetic engineering: banning research is counterproductive. J For 99:4–7Google Scholar
  177. Strauss S, Rottmann W, Brunner A, Sheppard L (2002) Floral homeotic genes for manipulation of flowering in poplar and other plant species. United States Patent and Trademark Office 6,395,892Google Scholar
  178. Strauss SH, Brunner AM, Busov VB, Ma C, Meilan R (2004) Ten lessons from 15 years of transgenic Populus research. Forestry 77:455–465Google Scholar
  179. Sundstrom J, Carlsbecker A, Svensson ME, Svenson M, Johanson U, Theissen G, Engstrom P (1999) MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms. Dev Genet 25:253–266PubMedGoogle Scholar
  180. Tandre K, Albert VA, Sundas A, Engstrom P (1995) Conifer homologues to genes that control floral development in angiosperms. Plant Mol Biol 27:69–78PubMedGoogle Scholar
  181. Vaistij FE, Jones L, Baulcombe DC (2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell 14:857–867PubMedGoogle Scholar
  182. Valenzuela S, Strauss SH (2005) Lost in the woods. Nat Biotechnol 23:532–533PubMedGoogle Scholar
  183. Wagner A, Phillips L, Narayan RD, Moody JM, Geddes B (2005) Gene silencing studies in the gymnosperm Pinus radiata. Plant Cell Rep 24:95–102PubMedGoogle Scholar
  184. Waterhouse P, Wang M-B (2002) Methods for obtaining modified phenotypes in plant cells. United States Patent and Trademark Office 6,423,885Google Scholar
  185. Watson JM, Fusaro AF, Wang M, Waterhouse PM (2005) RNA silencing platforms in plants. FEBS Lett 579:5982–5987PubMedGoogle Scholar
  186. Wei H, Meilan R, Brunner AM, Skinner JS, Ma C, Gandhi HT, Strauss SH (2006) Field trial detects incomplete barstar attenuation of vegetative cytotoxicity in Populus trees containing a poplar LEAFY promoter::barnase sterility transgene. Molec Breed DOI 10.1007/s11032-006-9045-y
  187. Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500PubMedGoogle Scholar
  188. Weisker A (1995) Hybrid safflower production utilizing genetic dwarf male sterility. United States Patent and Trademark Office 5,436,386Google Scholar
  189. Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–1326PubMedGoogle Scholar
  190. Wesley SV, Helliwell CA, Smith NA, Wang MB, 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 27:581–590PubMedGoogle Scholar
  191. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523PubMedGoogle Scholar
  192. Williams CG (2005) Framing the issues on transgenic forests. Nat Biotechnol 23:530–532PubMedGoogle Scholar
  193. Wright DA, Townsend JA, Winfrey Jr 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 44:693–705PubMedGoogle Scholar
  194. Yanofsky M (2000) Seed plants exhibiting early reproductive development and methods of making same. United States Patent and Trademark Office 6,025,543Google Scholar
  195. Li Y, Pei Y (2006) Biotech approaches to improve biomass production of poplar and to produce GM gene free pollen and seed from GM plants. P. 13 (abstracts), Int Poplar Symp IV, June 5-9, Nanjing, ChinaGoogle Scholar
  196. Yui R, Iketani S, Mikami T, Kubo T (2003) Antisense inhibition of mitochondrial pyruvate dehydrogenase E1 α subunit in anther tapetum causes male sterility. Plant J 34:57–66PubMedGoogle Scholar
  197. Zahn LM, Leebens-Mack JH, Arrington JM, Hu Y, Landherr LL, Depamphilis CW, Becker A, Theissen G, Ma H (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 8:30–45PubMedGoogle Scholar
  198. Zhang Y, Shewry PR, Jones H, Barcelo P, Lazzeri PA, Halford NG (2001) Expression of antisense Sn RK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J 28:431–441PubMedGoogle Scholar
  199. Zhang P, Tan HT, Pwee KH, Kumar PP (2004) Conservation of class C function of floral organ development during 300 million years of evolution from gymnosperms to angiosperms. Plant J 37:566–577PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Amy M. Brunner
    • 1
  • Jingyi Li
    • 2
  • Stephen P. DiFazio
    • 3
  • Olga Shevchenko
    • 2
  • Brooke E. Montgomery
    • 2
  • Rozi Mohamed
    • 2
  • Hao Wei
    • 2
  • Cathleen Ma
    • 2
  • Ani Anna Elias
    • 2
  • Katherine VanWormer
    • 2
  • Steven H. Strauss
    • 2
  1. 1.Department of ForestryVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  2. 2.Department of Forest ScienceOregon State UniversityCorvallisUSA
  3. 3.Department of BiologyWest Virginia UniversityMorgantownUSA
  4. 4.Linus Pauling InstituteOregon State UniversityCorvallisUSA
  5. 5.Faculty of ForestryUniversiti Putra MalaysiaSerdangMalaysia

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