Science in Society Archive

Terminator Trees

Sterile GM trees cannot contain transgenes, instead, they raise special safety concerns for health and biodiversity Prof. Joe Cummins and Dr. Mae-Wan Ho

Transgenic or genetically modified (GM) trees have been tested extensively in large open plots with little concern over the spread of transgenes. Studies on the dispersal of pollen and seeds from forest trees have shown that gene-flow can be measured in kilometres [1,2]. It is clear that the transgenes from GM trees cannot be contained once released into the environment. For that reason, a great deal of effort has been devoted to developing genetic modifications - commonly referred to as terminator techniques - that prevent flowering or pollen production.

In view of the serious threats posed by GM forest trees to the forest ecosystems of the world (see "GM forest trees - the ultimate threat", this series), commercial release of transgenic trees is widely rejected unless strict containment of transgenes can be assured, it is hoped, through engineering such 'terminator trees'.

For the most part, the methods used to control flowering or pollination involved interfering with the genetic programme for floral development or for deleting cells involved in floral development. A group of genes - MADS-box genes - code for the protein transcription factors that recognize DNA binding domains (See "View from MADS house", this series). The plant MADS genes are related to the extensively studied animal homeotic (HOX) genes that regulate developmental pathways [3]. Unraveling the functions of MADS genes has allowed flower development to be manipulated.

Flowering is prevented by anti-sense genes, or small regulatory RNA to prevent active gene products such as the MADS box transcription factor from being formed. Also deployed is a kind of genetic abortion using a suicide gene. The preferred suicide gene is the barnase ribonuclease from the soil bacterium Bacillus amylolquefaciens. The ribonuclease is placed under the control of a promoter specific to floral or pollen development. When activated, the gene product effectively kills the cells in which the gene is expressed. Another suicide gene used is the diphtheria toxin from the bacterium Cornyebacterium diphtheria or related ADP-Ribosyltransferase toxins from other bacteria; but these toxin genes are less commonly used than the barnase gene. The preferred barnase gene is a part of the genetic construction that first attracted the label "terminator" for engineered sterility, designed to place seed production under corporate control [5,6].

Professor Steven Strauss of Oregon State University pioneered flower and pollen control in poplar. He and his colleagues have led in the area of flowering control in forest trees. Strauss pointed out that when complete floral sterility is achieved, the plant would require vegetative propagation [7]. Floral sterility has begun to be extended from poplar to shade trees [8]. Strauss has argued that management of GM poplar is comparable to conventional poplar even though he is well aware of the seed and pollen dispersal with transgenic poplar [9]. Along with the exploration of floral sterility, Strauss has investigated speeding flower development (trees normally take years to develop sexually) to allow rapid breeding and selection cycles [10]. Of course the rapid breeding cycle is fraught with uncertainty regarding the subsequent development of the mature tree. Strauss has pioneered the use of the poplar homologue to the floral MADS box genes, the poplar promoter gene PTD [11]. The PTD promoter was combined with the diphtheria-toxin gene, DTA, to produce sterile polar without the detrimental effects on yield encountered earlier [12]. The problem of somaclonal variation is hardly mentioned in the discussion of flower control in poplar even though the problem was discussed in a report on a four-year field trial of herbicide tolerant poplar carried out by the Strauss group [13]. Somaclonal variation results from the cell culture technique used to select and propagate transgenic plants. It results in extremely high levels of mutation and chromosome instability, which could reverse floral sterility. Earlier reports showed that poplar cell culture resulted in extremely high levels of somaclonal variation [14,15].

In Finland, investigators from Sopanen University have studied the control of flowering in silver birch. Those investigators identified the MADS box genes controlling flowering in the birch tree [16,17]. When a flower specific birch promoter gene BpMADS1 was used to drive the barnase gene, floral cell ablation prevented flowering but there were marked side effects affecting leaves and branching [18]. The side effects were likely a pleiotropic effect of the gene insertion but could, as well have been affected by somaclonal variation from cell culture. A recent report altered the name of the MADS box gene from BpMADS to BpFULL1. As in the previous study flowering was prevented but the gene modification affected leaves and branching [19]. The pleiotropic effects observed may extend into areas not yet detected and they require more extensive study.

Ecological and health hazards of terminator trees

Trees that do not flower and fruit will provide no food for the multitude of insects, birds and mammals that feed on pollen, nectar, seed and fruit, and will inevitably have huge impacts on biodiversity. The ablation toxins used to create sterile trees are themselves an additional hazard. Barnase ribonuclease proved toxic to the kidneys of rats [20] Barnase was cytotoxic in mice and in human cell lines [21]. Animals may not find the GM forests welcoming. Diphtheria toxin has been associated with anaphylactic response [22]. As the song goes: "If you go down in the (transgenic) woods today, You're sure of a big surprise."

Even if these trees are sterile, they can still spread by asexual means and certainly, the genes can spread horizontally to soil bacteria, fungi and other organisms in the extensive root system of the forest trees, with unpredictable impacts on the soil biota and fertility. There is a remote chance that such genes could also spread horizontally to other forest trees, making those also infertile.

As transgenic traits tend to be unstable, they could break down and revert to flower-development, thereby spreading transgenes to native trees, or create pollen that poison bees and other pollinators as well as causing potential harm to human beings.

Finally, the effect of preventing sexual reproduction is to drastically reduce genetic recombination that generates genetic diversity and evolutionary novelty in nature. The sterile monocultures are much more likely to succumb to disease or senescence, which could potentially wipe out entire plantations.

Article first published 01/03/05


References

  1. DiFazio S, Slavov G, Burczyk J, Leonardi S and Strauss S. Gene flow from tree plantations and implications for transgenic risk assessment. Plantation Forest Biotechnology for the 21st Century eds. Walter,C. and Carson,M. 405-22, 2004.
  2. Slavov G, DiFazio S. and Strauss S. Gene flow from forest trees: from empirical estimates to transgenic risk assessment. Scientific methods workshop: ecological and agronomic consequences of gene flow from transgenic crops to wild relatives Columbus, Ohio, 2002.
  3. Ng M. and Yanofsky M. Function and evolution of the plant MADS -Box gen family Nature Reviews Genetics 2001, 2,186-96
  4. Skinner J, Meilan M, Brunner A. and Strauss S. Options for genetic engineering of floral sterility in forest trees. Molecular Biology of Woody Plants, Jain S and Minocha S. eds, Kluwer Academic publishers Netherlands, 2000.
  5. Ho MW and Cummins J. Terminate the terminators! I-SIS Report July 12, 2001 https://www.i-sis.org.uk/terminator.php
  6. Ho MW and Cummins J. Chronicle of an ecological disaster foretold. ISIS report 2/02/03 https://www.i-sis.org.uk/CEDF.php; also Science in Society 2003, 18, 26-27 https://www.i-sis.org.uk/isisnews.php
  7. Strauss S, Rottman W, Brunner A and Sheppard L. Genetic engineering of reproductive sterility in forest trees. Molecular Breeding 1995, 1, 5-26.
  8. Brunner A, Mohamed R, Meilan R, Sheppard L, Rottman W and Strauss S. Genetic engineering of sexual sterility in shade trees. J. Arboculture 1998, 24, 263-73.
  9. Strauss S, DiFazio S and Meilan R. Genetically modified poplars in context. The Forestry Chronicle 2001, 77, 271-80.
  10. Strauss, S and Brunner A. Tree biotechnology in the 21st century: Transforming trees in the light of comparative genomics. In S.H. Strauss and H.D. Bradshaw (Eds.), The BioEngineered Forest: Challenges to Science and Society, Pp 76-97. Resources for the Future, Washington, D.C., USA, 2004.
  11. Meilan R Brunner A, Skinner J and Strauss S. Modification of flowering transgenic trees. Molecualr Breeding of Woody Plants (Morohoshi M and Komamine A. eds.), Elsevier Science B.V. 247-57, 2001.
  12. Skinner J, Meilan R, Ma C and Strauss S. The poplar PTD promoter imparts floral predominant expression and enables high levels of floral organ ablation in Populus, Nicotiana and Arabidopsis. Molecular Breeding 2003, 12,119-32.
  13. Meilan R, Auerbach D, Ma C, DiFazio S and Strauss S. Stability of herbicide resistance and GUS expression in transgenic hybrid poplars during four years of field trials and vegetative propagation. Hort Sci 2002, 37, 277-80.
  14. Antoneti L and Pinon J. Somaclonal variation within poplar. Plant Cell, Tissue and Organ culture 1993, 35,99-106.
  15. Wang G, Castiglione S, Chen Y, Li L, Han Y and Tian Y. Poplar (Populus nigra L.) plants transformed with a Bacillus thuringiensis toxin gene: insecticidal activity and genomic analysis. Transgenic Res 1996, 5, 289-301.
  16. Lemmetyinen J, Hassinen M, Elo A, Porali I, Keinonen K, Makela H and Sopanen T. Functional characterization of SEPALLATA3 and AGAMOUS orthologues in silver birch. Physiologia Plantarum 2004, 121,149-62.
  17. Lannenpa M, Janonen I, Holtta-Vuor M, Gardemeister M, Porali I and Sopanen T. A new SBP-box gene BpSPL1 in silver birch (Betula pendula). Physiologia Plantarum 2004, 120,491-500.
  18. Lemmetyinen J, Keinonen K and Sopanen T. Prevention of the flowering of a tree, silver birch. Molecular Breeding 2004, 13, 243-9.
  19. Lännenpää M, Ranki A, Hölttä-Vuori M, Lemmetyinen J, Keinonen K and Sopanen
  20. T. Prevention of flower development in birch and other plants using a pFULL1::BARNASE construct 2005 Plant Cell Reports in press doi 10.1007/s00299-004-0903-y
  21. Ilinskaya,O. and Vamvakas,S. Nepherotoxic effects of bacterial ribonuclease in the isolated perfused rat kidney. Toxicology 1997, 120, 55-63.
  22. Prior T, Kunwar S. and Pastan I. Studies on the activity of barnase toxins in vitro and in vivo 1996 Bioconjugate Chemistry 1996, 7, 23-9.
  23. Rosenberg A. Immunogenicity of biological therapeutics: a hierarchy of concerns Developmental Biology 2003, 112,15-21.

Got something to say about this page? Comment

Comment on this article

Comments may be published. All comments are moderated. Name and email details are required.

Name:
Email address:
Your comments:
Anti spam question:
How many legs on a tripod?