Impact of Transgene Inheritance on the Mitigation of Gene Flow between Crops and Their Wild Relatives: The Example of Foxtail Millet

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ABSTRACT

Developing genetically modified crop plants that are biologically contained could reduce significantly the potential spread of transgenes to conventional and organic crop plants and to wild or weedy relatives. Among several strategies, the hereditary mode of transmission of transgenes, whether dominant, recessive, or maternal, could play a major role in interspecific gene flow. Here we report on the gene flow between foxtail millet (Setaria italica), an autogamous crop, and its weedy relative, S. viridis, growing within or beside fields containing the three kinds of inherited herbicide resistance. Over the 6-year study, in the absence of herbicide selection, the maternal chloroplast-inherited resistance was observed at a 2 × 10^sup -6^ frequency in the weed populations. Resistant weed plants were observed 60 times as often, at 1.2 × 10^sup -4^ in the case of the nuclear recessive resistance, and 190 times as often, at 3.9 × 10^sup -4^ in the case of the dominant resistance. Because the recessive gene was not expressed in the first-generation hybrids, it should be more effective than dominant genes in reducing gene flow under normal agricultural conditions where herbicides are sprayed because interspecific hybrids cannot gain from beneficial genes.

GENETICALLY modified (GM) crops could generate potential benefits in many areas of agricultural performance, including best uses of agrochemicals and simplified farmmanagement, and they may broaden the offer of plant services, including soil detoxification and production of medicinal substances. However, many areas of scientific uncertainty and public concern remain regarding environmental and health hazards. In particular, the question of the (trans)gene flow to wild relatives of GM crops is a hot topic, and the debate is open in Europe about the coexistence of GM and non-GM crops. Spontaneous gene flow from crops in the fields to their wild relatives has been documented for most important crops (Ellstrand 2003).Designing strategies to prevent (trans)genes from moving into genomes of related species therefore should be of the highest priority.

In addition to agronomical management, technologies for the prevention of transgene flow to nontransgenic plants may significantly reduce concern about its impacts on biodiversity and non-GM crops. They include biotechnology-based switch mechanisms, also called genetic use restriction technologies (Hills et al. 2007); transgenic mitigation using a tandem construct where a gene of choice is linked to a gene that is deleterious for a wild recipient plant but neutral for the crop (Al-Ahmad et al. 2005); and transgene incorporation into the plant chloroplast because cultivated species generally inherit plastids from the mother and chloroplast genes are not carried by pollen (Daniell 2002). Although tested in the laboratory, those technologies remain pure theory and there is still little knowledge of their ecological and agronomic effects.

Other genetic strategies, such as multigenic determinism and recessive expression, are advocated. In particular, nuclear recessive genes are not expressed by heterozygous plants, so there is no risk of the presence of the transgene product in the case of a non-GM field pollinated by adjacent GM fields. In addition, they are not expressed in interspecific hybrids between crops and their wild relatives, so that even a beneficial transgene cannot help hybrids to be selected, whatever the habitat. As interspecific hybrids often suffer some lower fitness due to incompatible gene combinations or an unbalanced hybridization process between distantly related species (Ellstrand 2003; Van Tienderen 2004), this can help reduce the spread of the transgenes. However, homozygous recessive plants occur in hybrid progeny, and these plants could be submitted to favorable selection.

In this article, we aimed at comparing over the course of 6 years the efficiency of this strategy with regard to the present situation of a simple nuclear dominant gene and that of the maternal transgene transmission. …