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What happens when artificial genes move from commercial crops into the wild? Introduction Plants have been exchanging genes with closely related species for millennia. It is one of the strategies that they have evolved to cope with environmental change. Now that plant breeders are taking genes from other species and putting them into commercial plants to provide them with increased resistance to disease and insects, increase nutritional value and for other meritorious purposes, plant promiscuity presents a potential problem: What will the environmental consequences be when these genes move from the fields into wild populations. Some feel that these “transgenes” could upset the environmental balance by increasing the hardiness of weeds and other wild plants. Others contend that such risks are very small. Now a study performed by plant scientists at Vanderbilt and Indiana University find that putting one particular transgene in sunflowers is unlikely to have a major environmental impact, reinforcing the argument that such genetic modifications should be evaluated on a case-by-case basis. Transgene Study One of the major environmental concerns that has been raised about the use of genetically modified (GM) crops has been the possible effects that artificially inserted genes, called transgenes, may have if they spread to wild relatives. A number of studies performed in the last ten or so years have found that commercial plants exchange genetic material with wild relatives in their vicinity with considerable regularity. But now one of the first studies of what actually happens to a transgene when it moves from a genetically modified cultivar into a wild population indicates that such transfers need not have a major environmental impact. Results of the field study, which was conducted by plant scientists at Vanderbilt University and Indiana University, are reported in the May 23 issue of the journal Science. The subject of the study was a transgene that can provide commercial sunflowers with additional protection against a disease called white mold, which is caused by a pathogen named Sclerotinia sclerotiorum. The experiment found that wild sunflowers already possess a degree of resistance to white mold that the commercial variety lacks. As a result, wild sunflowers that pick up the transgene do not gain a reproductive advantage that would cause them to spread widely. Although subject to some significant caveats, the finding suggests that this particular transgene is unlikely to spread throughout the wild sunflower population, making wild varieties hardier and more aggressive. White mold is one of the worst diseases afflicting commercial sunflowers. Sunflower is one of the world’s four most important oilseed crops, with a value of $40 billion per year. White mold infection, which causes the rapid wilting and death of cultivated sunflower plants, is the source of economic losses that range from $50 million to $80 million annually. Efforts of sunflower breeders to improve the resistance of their plants to this disease using traditional techniques have been unsuccessful and the application of chemical fungicides is costly and often ineffective. The situation led Pioneer Hi-Bred International – a subsidiary of E.I. du Pont de Nemours and Company – to genetically modify one of their varieties of sunflower by inserting a gene isolated from wheat. Much of the damage that white mold inflicts on sunflowers is caused by its production -1- What happens when artificial genes move from commercial crops into the wild? of an organic acid called oxalic acid. The wheat gene, called OxOx, allows the sunflowers to produce a compound called oxalate oxidase that breaks down oxalic acid. Pioneer Hi-Bred then funded a study to help determine the likelihood that the wheat gene would spread into the surrounding wild sunflower community, which was carried out by John Burke, assistant professor of biological sciences at Vanderbilt, and Loren Rieseberg, professor of biology at Indiana University. In the first stage in the study, the researchers surveyed the areas in the United States where commercial sunflowers are grown looking both for the incidence of white mold infections among wild sunflowers and for the points of contact between wild and commercial varieties. It took two years and involved driving more than 8,000 miles throughout the Midwest and Southwest. The survey also found wild sunflowers growing next to fields of cultivated sunflowers almost everywhere that they looked. They also confirmed the conclusion of previous studies that cultivated sunflowers hybridize (exchange genetic material) with their wild relatives when they come in contact. “We showed that contact between cultivated and wild sunflowers occurs throughout the entire range of cultivation, making gene escape inevitable,” says Burke. The close relationship between cultivated and wild sunflowers means that the risk that transgenes will jump from commercial plants to their wild cousins is particularly high. But there is another factor that governs whether these genes will spread widely throughout the wild population. If the transgene confers a reproductive advantage to the wild plants that obtain it, then it will spread. If it does not provide such an advantage, however, then it won’t spread and so shouldn’t become an environmental problem. “It’s time to move beyond all the hand-wringing about whether and how often transgenes are going to escape and start attacking the real root of the problem, which is what impact will specific transgenes have if they get out,” Burke says. In order to address the question of the likely impact of OxOx transgene escape, Burke and Rieseberg simulated the early stages of gene escape by “backcrossing” the gene into wild sunflowers. They grew the resulting plants – roughly half with the transgene – in containment cages at three sites, one in Indiana, one in North Dakota and one in California. Just before the plants flowered, they inoculated half of them at each location with Sclerotinia sclerotiorum. “Faced with such a severe pathogen challenge, we expected the plants with the OxOx gene to have quite an advantage,” says Burke. “Somewhat surprisingly, that was not what we found.” The researchers discovered that although the transgene did provide some protection against becoming infected, the transgenic plants did not produce any more seeds than those without the OxOx gene. As a result, the gene does not appear to confer any reproductive benefit even under the unusually severe exposure to the pathogen that the researchers imposed. When taken with the survey results that found little evidence of white mold infection among wild sunflower populations, Burke and Rieseberg conclude that it appears that wild sunflowers already possess some level of resistance to white mold that their commercial cousins lack. “It looks like we are giving the wild sunflower a degree of resistance to white mold that it already has, so it isn’t a big advantage,” says Burke. Because wild sunflowers with the transgene don’t look as if they will reproduce at a faster rate than those without it, the scientists have concluded that the OxOx gene appears unlikely to spread widely through wild populations and so does not represent a significant environmental threat. There are some important caveats to their conclusion, however. The study was performed in a single season. There could be multi-year cycles of white mold infection that would give the transgenic sunflowers a selective advantage that is not reflected in the study. Also, the experiment did not examine the effects of environmental stress, like drought. Stress could work either way: It could -2- What happens when artificial genes move from commercial crops into the wild? enhance the advantage of the transgenic plants or penalize them in ways that would restrict their spread. Finally, the study only looked at three locations. There was enough variation among the locales to suggest that there could be some circumstances under which wild, transgenic sunflowers might do better than indicated. The researchers recommend that these questions be addressed in future studies. Sunflower History Ah, Sun-flower! Weary of time, Who countest the steps of the Sun; Seeking after that sweet golden clime Where the traveler’s journey is done: -- William Blake, 1794 The sunflower is a dramatic plant, one that has inspired poets and artists down through the centuries. Decorative varieties ornament many gardens. It is also an important food crop. Commercial sunflowers are one of the world’s four most important oilseed crops, with a value of $40 billion per year. Wild sunflowers cover thousands of acres in North America. In prehistoric times, the sunflower was an important source of food, medicine and oil for many natives. For food, they harvested the sunflower’s seeds, roasted them, ground them into powder and formed them into cakes. The Zunis used the sunflower as a cure for rattlesnake bites and the Dakotas used it to relieve chest pains. Other tribes used it to treat wounds to speed healing and prevent infection. The sunflower played an important place in the religion of many tribes. Hopis wore wild sunflowers in their hair during certain ceremonies and carved sunflowers on wooden disks used in other religious observances. The creation myth of the Onondagas mentions sunflowers, along with corn, beans and squash. About 4,000 years ago, Native Americans living somewhere in the vicinity of Kentucky appear to be the first to domesticate the sunflower. Giant domesticated varieties grew more than six feet tall and had seeds even larger than those in today’s commercial varieties. Some tribes used the flour to make bread. Others used the oil to season food, as hair dressing and as a base for face paint. By the time that the Europeans reached North America, the cultivated sunflowers were widely distributed across the continent. The Spaniards were among the first to introduce the sunflower to Europe. There it was first grown as a curiosity. It took the Europeans more than a century to discover the value of sunflower seeds and oil. It was not until the sunflower reached Russia that it became a spectacular success. At the time, the Russian Orthodox Church had strict rules governing people’s diets at Lent and Christmas. Nearly all foods rich in oil were prohibited during these periods, which totaled nearly one quarter of the year. The sunflower was not on the prohibited list, so the Russians eagerly adopted it. Russian plant breeders created the Mammoth Russian or Russian giant, one of the best known sunflower varieties. Meanwhile, North American colonists did not grow sunflowers and it died out as a food crop. It wasn’t until 1880 when American seed companies began offering the Mammoth Russian that sunflowers were again raised as a food crop. As a result, nearly all commercial sunflower varieties grown in the United States come by way of Russia. At the turn of the century, sunflowers remained a crop of relatively minor importance. In the th 1930’s, it ranked about 10 in value among world sources of vegetable oil. In the decades since it has risen gradually in value until now the sunflower stands with rapeseed, peanuts and soybeans as one of the four major sources of vegetable oil worldwide. -3- What happens when artificial genes move from commercial crops into the wild? Despite its success worldwide, the sunflower has remained a minor oil seed crop in North America. However, consumption of sunflowers for snack food and for wild bird seed has become increasingly important in recent years. ADDITIONAL INFORMATION Sunflower: An American Native http://muextension.missouri.edu/xplor/agguides/crops/g04290.htm Sunflower: An Alternative Crops Manual http://www.hort.purdue.edu/newcrop/afcm/sunflower.html The Sunflower Story http://www.fargo.ars.usda.gov/sun/sun_stry.htm Biographical Sketch John Burke grew up in Bloomington, Minnesota – in the Twin Cities area. His father was a high school chemistry teacher, so he and his brothers were raised in a scientifically literate home environment. As a result, it is not surprising that he and his two older brothers all went into technical occupations: His oldest brother is a chemical engineer and middle brother a biologist. “As early as I can remember I have been drawn to biology,” says Burke, who recalls that he and his brothers were always outside “collecting critters and stuff.” When Burke enrolled at the University of Minnesota, he started out as an engineering major, but quickly realized that biology was his true calling. It wasn’t long before he signed up as a biology major. He became particularly interested in biodiversity issues. After graduation he went to the University of Georgia to study with Professor of Genetics Michael Arnold, a leading authority on natural hybridization. There Burke performed a number of experiments designed to investigate the fitness of hybrids (the progeny of crosses between different species) in natural environments. After getting his doctorate, Burke landed a postdoctoral fellowship with Loren Rieseberg at Indiana University who runs another “hot” lab in the field. It was here that he was introduced to the sunflower and sunflower genetics. One of Burke’s professional goals is to “put biology to good use.” That has led him to study commercially important plants and so thrust him into the middle of the genetically modified (GM) foods controversy. Burke believes that there is a middle ground between dismissing genetic modification of crops entirely or introducing them without appropriate scientific study. GM foods have potential environmental hazards, he acknowledges, but they also have important potential benefits, such as promoting no-till agriculture and reducing the amounts of chemical pesticides and herbicides introduced into the environment. As a result, different GM crops must be studied on a case by case basis ”to provide an informed judgment of the relative risks and benefits of each genetically modified plant,” he says.” ADDITIONAL INFORMATION John Burke’s home page http://www.biosci.vanderbilt.edu/mbdept/faculty/burke.html Indiana University Angle -4- What happens when artificial genes move from commercial crops into the wild? Genetically modified crops not necessarily a threat to the environment By David Bricker As concerns rise about the ecological impacts of genetically modified crops, a new Indiana University study urges a pragmatic approach to dealing with "transgenes" that escape from crop plants into the wild. Use of transgenic crops is becoming more common as farmers reap benefits from the plants' decreased susceptibility to disease and increased marketplace value. IU biologist Loren Rieseberg and former postdoctoral fellow John Burke (now at Vanderbilt University) reported in the May 23 issue of Science that a wheat transgene synthetically inserted into sunflowers has little or no effect on crop sunflowers' wild relatives and is not likely to impact the environment. "We found that a certain transgene that gives crop sunflowers resistance to white mold is unlikely to spread rapidly to the wild because the transgene doesn't affect the seed-producing abilities of wild sunflowers in nature," said Rieseberg, who led the study. "We need to examine each transgene and crop on a case-by-case basis. Some transgenes will have major ecological impacts and others probably won't." For example, another study co-authored by Rieseberg, published last month in Ecological Applications, showed that a bacterial transgene inserted into sunflowers significantly increases seed production of wild sunflowers and therefore may incur ecological costs. A common worry about genetically modified (GM) crops is that new, highly advantageous genes will seep through wild populations as crop plants mingle and reproduce with their wild cousins. While the new report by Rieseberg and Burke does not refute that worry, the researchers believe that the movement of certain genes from GM crops into the wild may occur at a glacial pace, meaning wild plants in locations far from their alter egos in farm crops will not encounter the transgenes for a long time. "The question isn't whether these transgenes will escape into wild relatives -- we know they will," Rieseberg said. "Even if the wild hybrids are partially sterile or inviable, genes will still move across the farm property barrier. So it's really the fitness effects of a gene that dictate the speed at which it spreads. Genes that aren't advantageous to the wild plants will spread very slowly. The transgenes that are truly deleterious to wild species won't move much at all." The scientists introduced a wheat gene for the white mold-combating enzyme oxalate oxidase (OxOx) to wild sunflowers and compared wild plants with and without the transgene at natural study sites in California, North Dakota and Indiana. Half of the plants in each group were inoculated with white mold. At the end of the study period, Rieseberg and Burke counted the number of seeds produced by each plant. The researchers found that the OxOx transgene had no appreciable effect on the wild plants' ability to produce seeds. Wild plants lacking the transgene made just as many seeds as plants with the transgene. Rieseberg and Burke also found that the OxOx transgene did not harm any of the sunflowers that possessed it when they were not exposed to the disease. White mold infection has plagued sunflower farmers for years. Attempts at breeding natural resistance in the economically important plant have generally failed. Fungicides are costly and ineffective, and they may carry health consequences for consumers. The introduction of the OxOx gene to sunflower crops may help reduce their susceptibility to mold. Both the Science and the Ecological Applications reports were funded by grants from Pioneer Hi-Bred International Inc., a DuPont Corp. company. ------------------------------David Bricker is a media relations specialist at the University of Indiana -5- What happens when artificial genes move from commercial crops into the wild? ADDITIONAL INFORMATION Loren Rieseberg’s Laboratory home page http://snook.bio.indiana.edu/rieseberg/ -6-