October 2003
Case Study in Gene Flow
In recent years, the potential impact of transgenic crops on the environment has been a topic of intense international debate. Arguments in favor of genetic engineering point to the possible environmental benefits of genetically modified (GM) crops. These include a reduction in the amount of chemicals applied to agricultural systems, a
transition to less toxic chemical treatments, and the facilitation of zero-till agriculture. Environmental objections to GM crops, on the other hand, are largely based on factors such as the possible negative effects of transgenes on non-target organisms and the potential for transgene escape via crop-wild hybridization to facilitate the evolution of increasingly weedy or invasive plants. Predictions regarding the particular crops or traits that are likely to pose the greatest environmental risks can be made. For example, crops that hybridize readily with wild relatives represent greater risks than those that do not. Likewise, transgenes that are advantageous in wild or weedy forms of a plant are most likely to pose a risk, whereas those that are neutral or disadvantageous will do little to disrupt the evolutionary dynamics of the recipient population(s). Current concern stems from the fact that many of the traits that are the target of genetic manipulation such as pest or pathogen resistance and tolerance of various abiotic stresses may be highly advantageous in the wild.
In many cases, the conditions necessary for hybridization between crop plants and their wild relatives are met, and hybridization appears to be frequent. For example, there is evidence that twelve of the world's thirteen most important food crops hybridize with at least one wild relative in at least part of their range of cultivation. Thus, until an acceptable terminator technology has been devised, there will be potential for gene flow. Research on the risks associated with transgene escape should, for now, focus on the fitness consequences of the gene(s) in question, rather than on rates of gene flow. Until recently, however, virtually nothing was known about the fitness effects of pest or pathogen resistance transgenes in wild plant populations.
Of the more than three dozen pathogens that afflict sunflower, white mold is one of the most common and widespread, having been reported from all sunflower growing regions throughout the world. White mold infection, which typically begins at the
base of the stem, results in the rapid wilting and death of cultivated sunflower plants, greatly reducing seed output. Infection rates as high as 100 percent have been reported in North American sunflower fields, and white mold has been known to reduce yield by as much as 70 percent. Attempts to develop resistant cultivars via traditional plant breeding techniques have met with little success in sunflower, and alternative methods can be economically prohibitive. Attention has turned, therefore, to genetic modification. Because oxalic acid plays a key role in the pathogenicity of white mold, it has been hypothesized that the insertion of an oxalate oxidase (OxOx) transgene would provide otherwise susceptible plants with a mechanism of resistance. This approach has now been used by seed companies to successfully enhance white mold resistance in cultivated sunflower. Unfortunately, the potential for transgene escape is especially high in sunflower. Nearly all of the cultivated sunflower acreage in the United States is contained within the geographic range of common sunflower, and range-wide surveys of the potential for reproductive contact have revealed that approximately two-thirds of all cultivated sunflower fields in the United States occur in close proximity to, and flower coincidentally with, common sunflower populations. Moreover, the results of previous research indicate that, where they come into contact, cultivated and wild sunflower often hybridize. Thus, crop-wild gene flow is a virtual certainty throughout the range of sunflower cultivation in the United States. To address this, the fitness effects of a transgene that confers resistance to white mold (Sclerotinia sclerotiorum) following its `escape' from cultivated into common sunflower were followed systematically.
Transgene escape was replicated by crossing the OxOx transgene into common sunflower and growing the resulting plants at field sites located in California, Indiana, and North Dakota. The final result revealed a set of populations consisting of wild-like plants that were segregating for the OxOx transgene. By inoculating a subset of these plants at each location with white mold and keeping the remainder as controls, the fitness benefits afforded by the OxOx transgene in the face of a pathogen challenge could be examined, as well as any possible fitness costs associated with it in the absence of white mold. Analysis indicated that there was no "cost of resistance" associated with the OxOx transgene in the absence of a pathogen challenge. This gene did appear, however, to protect its carriers from white mold infection. In terms of seed output, however, the story was somewhat different. Following inoculation, there was no detectable difference in the productivity of transgenic and non-transgenic individuals.
The results suggest that the OxOx transgene will do little more than diffuse neutrally following its escape, and therefore, will have little effect on the evolutionary dynamics of wild sunflower populations. In other words, it appears that, by giving the OxOx transgene to wild sunflower, it was effectively given something that it already had (i.e., some degree of white mold resistance). In the broader context, the results illustrate the importance of quantifying transgene fitness more directly than through the use of a presumptive correlate such as disease incidence. Indeed, if infection rate had been the sole endpoint, rather than looking directly at reproductive output (albeit only through female function), the conclusions would have been quite different. This work also represents an important counterpoint to a recently published report in which a B.t. transgene was shown to decrease herbivore damage and increase fecundity in common sunflower grown under field conditions. (Open Letter of J. Burke, Vanderbilt University, 9/5/03, edited from Agnet).
