Fate of transgenic plant DNA in the environment

Environ. Biosafety Res. 6 (2007) 15–35 c ISBR, EDP Sciences, 2007  DOI: 10.1051/ebr:2007037 Available online at: www.ebr-journal.org Thematic Issue on Horizontal Gene Transfer Review article Fate of transgenic plant DNA in the environment Alessandra PONTIROLI1 , Pascal SIMONET1 , Asa FROSTEGARD2 , Timothy M. VOGEL1 and Jean-Michel MONIER1 * 1 Environmental Microbial Genomics Group, Laboratoire Ampère, École centrale de Lyon, 36 avenue Guy de Collongue, 69134 Ecully Cedex, France 2 Dept. of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, P.O. Box 5003, 1432 Aas, Norway This review addresses the possible ecological effects of transgenic plants on micro-organisms in the field, hence, in the phytosphere and in the soil matrix. The important steps involved in the interaction between plant DNA and bacteria and the factors that influence the horizontal gene transfer (HGT) process will be discussed. HGT is a process in which two partners are involved, even if indirectly. In the first section, aspects concerning bacteria, such as their physico-chemical, biological and genetic characteristics, are described. Parameters affecting transgenic DNA fate in the environment are described in the second section. Subsequently, terrestrial habitats are evaluated in terms of their capacity to favor horizontal gene transfer. Finally, we focused on several studies in order to evaluate possible perturbations of soil bacterial community composition due to cultivation of transgenic plants in the field. Keywords: GMO / bacteria / transgene / fate / microbial GENETICALLY ENGINEERED PLANTS: HISTORY, FEATURES AND APPLICATIONS Since the dawn of agriculture, humans have shaped the characteristics of domesticated plants in order to develop better-adapted varieties and to increase yields by taking advantage of the natural occurrence of mutants. Despite the poor understanding of the process, plant breeding was a popular activity even before the botanist Gregor Mendel in 1865 published his findings on how dominant and recessive alleles produce specific traits that can be passed to offspring (http://www.mendelweb.org/Mendel.plain.html). This was the first major insight into the science behind the art, and breeders soon applied the new understanding of genetics to traditional techniques of self-pollination and cross-pollination. Later, at the beginning of the 20th century, scientific advances in other disciplines, such as physics and chemistry, led to a science-based approach for the genetic modification of plants, thus providing the means for plant breeders to enhance plant genetic diversity at a faster pace. After the discovery of deoxyribonucleic acid (DNA) in the early 1950s as the basis of life and, shortly thereafter, the determination of its molecular structure by * Corresponding author: Watson, Crick and Franklin, genetic traits could be manipulated directly. Techniques for the insertion of foreign genes into bacteria were first developed in the early 1970s, and only a decade later, the ability to transfer foreign genes to plants via transgenesis was achieved (Comai et al., 1985; Horsch et al., 1985; Krens et al., 1982). Thus, plant genetic engineering was added to the long list of methods that broaden the available genetic diversity of a given plant species (Belzile, 2002). The worldwide expectations generated by this technology among scientists and supporters were so optimistic that the term Doubly Green Revolution was introduced to describe the extent of the innovation and to summarize the potential benefits for mankind (Wisniewski et al., 2002). Early transgenic plants were laboratory specimens, but already in the mid-1990s transgenic plants with commercially useful properties appeared on the market. They carried traits of agricultural interest, such as plant protection from insects or pests, herbicide resistance and tolerance to stress, in addition to qualities such as prolonged shelf life and enhanced nutrient content. The potential of the second generation of transgenic plants currently under development is for the production of vaccines and proteins of pharmaceutical interest. Finally, aesthetic applications might be proposed, such as ornamental bright Article published by EDP Sciences and available at http://www.ebr-journal.org or http://dx.doi.org/10.1051/ebr:2007037 A. Pontiroli et al. colored fluorescent lawn grasses (Marvier and van Acker, 2005). The US patent database provides a view of the state of the art of commercial applications of plant genetic engineering and describes which plant-derived products might be available on the market in the near future (Dunwell, 1999). The U.S. Food and Drug Administration web site (http://www.cfsan.fda.gov/∼lrd/biocon.html) offers a nearly complete list of currently commercialized genetically modified plants (GMPs). Currently, the transgenic crops that are cultivated most successfully and widely are herbicide-tolerant soybean, oilseed rape, cotton and maize, and insect-resistant cotton and maize. In 2005, they were grown in a total of 21 countries, among which the United States, Argentina, Canada, Brazil, China and South Africa accounted for 99% of the planted surface. Between 1996, when the first transgenic crops were commercialized, and 2006, the global acreage devoted to these plants has increased 50-fold, from 1.7 to 102 million hectares (James, 2006). POTENTIAL ECOLOGICAL RISKS LINKED TO FIELD RELEASE OF GMPS Despite the increasing surface dedicated to these crops, public concerns were raised, particularly in Europe, in primis, on their safety in relation to human health and the environment, and also on the sustainability of this new agricultural technology and on its impacts on global agro-food production and society at large (Hails and Kinderlerer, 2003). An argument against approval of transgenic plants involves the dependence upon seeds protected by intellectual property rights and owned by major agrochemical companies, thus enriching large corporations and depriving farmers from their rights to reuse the seeds. Other reasons of dispute concern the elimination of crop and herbicide rotations, the potential for seed dispersal through contamination, cross-pollination with wild plants creating “superweeds” and the inability of the public to be adequately informed about the presence of genetically modified food (Greenpeace, 2003). During the period 1999–2004 a de facto moratorium on cultivation and import was in place in Europe; since then the use of GMPs in Spain, Portugal, France, Germany and in the Czech Republic is still limited to a single variety of maize (insect-resistant due to expressing the insecticidal protoxin of Bacillus thuringiensis). Transgenic plants cultivated in the field can be regarded as reservoirs of transgenes, which could be released in the surrounding environment either by roots, during plant decay or by pollen (Fig. 1). Some researchers suggest that transgenic crops c (...truncated)