by Brian Dick, PhD and Mark Jones, PhD
The Rio Star Grapefruit
Herman Joseph Muller (1890-1967) is best known for his work on the genetic effects of ionizing radiation, and the development of X-ray mutagenesis. After graduating from Columbia University, he began to take an interest in the genetics work being done in Thomas Hunt Morgan’s famous Drosophila Fly Room and joined Morgan’s group in 1912. Muller subsequently became Professor of Zoology at the University of Texas in Austin where he announced his discovery of the mutagenic effects of X-rays in 1926. His pioneering contributions were honored with a Nobel Prize in Physiology or Medicine in 1946. Muller was also active politically – after World War II, he encouraged public awareness of the long-term effects of radioactive fallout.
Suggestions for further reading...
A. M. van Harten. (1998). Mutation Breeding: Theory and Practical Applications. Cambridge: Cambridge University Press.
Q. Y. Shu. (2009). Induced Plant Mutations in the Genomic Era. Ed. Rome: Food and Agricultural Organization of the United Nations.
B. S. Ahloowalia, M. Maluszynski, and K. Nichterlein. (2004). “Global impact of mutation-derived varieties.” Euphytica. 135: 187-204.
Special thanks to Kirsten Stead for providing technical expertise and comments on earlier drafts, Helen Anne Curry for sharing her dissertation research, and Paige Johnson for her input and permission to use her photograph of Muriel Howorth.
LSF Magazine: Spring 2012
Atomic Gardens: Public Perceptions and Public Policy
In 2007, restaurants in Shanghai, China began offering patrons a purple potato called Purple Orchid Three. It was bred from seeds exposed to mutation-inducing cosmic radiation during a trip into outer space. The unusual color resulted from overexpression of the flavonoid anthocyanin. Grown by the Haikou Purple Orchid Co. on Hainan Island, China’s southernmost province, Purple Orchid Three enjoyed a faddish popularity. But it wasn’t a novelty. Since 1987, China’s space breeding program has produced dozens of mutant crop varieties.
Radiation-induced mutagenesis has a long history. The United States and the Soviet Union began sending seeds and plants into space in the 1960s, and earthbound mutation breeding experiments date back to the beginning of the 20th century. Environmental conditions in space (microgravity, weak geomagnetic fields, and an ultra-clean vacuum) are especially conducive to genetic alteration, but terrestrial applications of X-rays and gamma rays are also effective means of crop modification and improvement.
The aim of mutation breeding is to introduce genetic variation. As rates of genetic change increase, so do chances to select desirable traits for propagation. Most mutations caused by exposure to radiation or chemical mutagens prove useless, but some increase crop yields, confer resistance to diseases or pests, or enhance fitness in stressful environmental conditions, such as drought, frost, or poor soils (with depleted nutrients, extremes in salinity, acidity, or alkalinity, etc).
Over 2,700 mutant plant varieties have been developed by irradiation. Many are ornamentals (the familiar chrysanthemum, for example), but 65% are food crops bred for human consumption. Best-selling mutants include the red-fleshed Rio Star® grapefruit (see sidebar), the disease-resistant Gold Nijisseiki pear, and high-yield Creso durum wheat, along with varieties of alfalfa, barley, chickpeas, pepper, rice, sesame, tomato, and many more.
Today, mutant plant varieties are widely distributed. Consuming them is practically impossible to avoid, but relatively few people are aware of their ubiquity. There is irony in this circumstance. Scientific assessments of risks associated with agricultural biotechnologies show no appreciable difference between plants modified by traditional selection, hybridization, radiation, or the tools of molecular genetics, yet public fears have prompted governments to impose strict forms of regulation on experimentation and industrial production involving recombinant DNA. Policy debates on genetically modified organisms can be gainfully informed by an historical review of radiation mutation breeding.
The Origins of Radiation Induced-Mutations in Plants
X-rays and radioactivity were discovered at the end of the 19th century, and biologists as well as physicists soon began to investigate their effects. Testing the hypothesis that radiation induces genetic changes, Dutch botanist Hugo de Vries began exposing plants to radium. Others, such as Charles Stuart Gager, Director of the Brooklyn Botanic Garden, built on de Vries’ work and subjected a wide variety of plants to X-rays. But solid evidence of artificially produced mutations was not marshaled until the late 1920s.
In 1927, while working at the University of Texas in Austin, Herman Joseph Muller (see sidebar), a student of famed Columbia University geneticist Thomas Hunt Morgan, established that X-rays did indeed cause genetic mutations in fruit flies. The following year, geneticist Lewis J. Stadler published three papers reporting X-ray induced mutations in barley.
Stadler was an assistant professor at the University of Missouri and a consultant to the U.S. Department of Agriculture. He had taken up the study of maize genetics in 1920 after reading Morgan’s classic text, The Physical Basis of Heredity. Following his 1928 success, Stadler continued experiments on numerous food crops, including barley, oats, and wheat.
Geneticists of the era concluded, perhaps over-optimistically, that mutations could be artificially induced at rates exceeding those of spontaneous change. Stadler remained skeptical, and continued to pursue the question experimentally. Nevertheless, his discovery motivated many researchers to set up X-ray machines in their laboratories.
Scientists in the late 1920s and the 1930s explored the effects of radiation on a wide variety of plants. Investigations continued during the Second World War, although scientific communications were often stymied by wartime secrecy.
Gamma Fields And Peaceful Applications Of Atomic Energy
Plants are set up in preparation for a radiation exposure. The telescoping shield is seen at it's maximum extension, allowing for the highest possible dose of radiation.
After the war, interest grew in peaceful applications of atomic energy. In 1946, President Harry Truman signed the Atomic Energy Act, which established the U.S. Atomic Energy Commission (AEC) and placed the development of nuclear weapons and power under civilian control. Radiobiological research programs were assembled at nuclear energy development sites.
National laboratories in the United States, Europe, and the Soviet Union began using gamma rays to induce mutagenesis in plants. Many prepared plots that came to be called ‘gamma fields’ or ‘atomic gardens.’ The first gamma field was established in 1948 at the Brookhaven National Laboratory on Long Island. By 1964 the lab had installed a number of different ‘gamma’ facilities to study plant irradiation—a field, a forest, a greenhouse, a cell, and a pool. In a 1967 issue of Radiation Botany, a journal first published in 1961 for specialists in radiation mutation breeding research, Brookhaven radiobiologist Arnold H. Sparrow provided a complete survey of the Laboratory’s radiation facilities.
The gamma field encompassed 12.8 acres of land that Brookhaven scientists used to experiment on more than 300 plant species. In 1959, the researchers observed that radiation from the gamma field had injured nearby trees. The finding prompted them to create a ‘gamma forest,’ which examined the effects of gamma rays on an entire ecosystem. The gamma greenhouse was a concrete structure with a lead cap surrounded by earthen embankments. Cobalt-60 was raised from a shielded receptacle in the floor. The ‘hot cell’ was a small (2 meter) shielded chamber. A radiation source was lowered from the ceiling. Plants were placed on removable shelves that could be accessed through a set of sliding doors coated with lead. In the gamma pool, radioactive materials were lowered into the water to shower plant specimens placed at the bottom.
Gamma Field at the Institute of Radiation Breeding in Japan
The world’s largest gamma field (100 meters in radius) opened in April 1962 at the Institute of Radiation Breeding (IRB) in Ohmiya, Japan. Plants were arranged into concentric circles surrounding a radiation source (Cobalt-60). A shielding dike eight meters tall surrounded the field to prevent gamma rays from escaping. The radiation source was raised on a tower up to six meters above the ground. The plants were exposed to different levels of radiation to produce varying rates of mutation depending on proximity to the source—from 300,000 times the normal background radiation level at the closest point to 2,000 times at the furthest. The IRB has officially released 470 mutant cultivars, including Reimei rice, Raiden and Raikou soybeans, and the Golden Nijisseiki pear.
A number of international meetings and conferences were held in the 1960s with the goal of multiplying mutation breeding programs and expanding practical applications. The most important were organized by the UN’s Food and Agricultural Organization (FAO) and the Vienna-based International Atomic Energy Agency (IAEA). An international symposium sponsored jointly by the FAO and IAEA was held in 1969, and led to the publication of the first Manual on Mutation Breeding. This decisive meeting marked a fundamental shift in the field away from basic research towards practical applications. Eleven years later, another joint symposium, entitled “Induced Mutations—A Tool in Plant Research,” elaborated ways in which induced mutations could serve instrumental purposes in a number of fields, including molecular genetics.
Some twenty gamma fields were eventually constructed worldwide. Only a few remain operational, most in Europe and Asia. U.S. scientists have largely abandoned radiation breeding research, but American programs produced notable results in their time. In his 1967 review in Radiation Botany, Sparrow identified eight widely-cultivated mutants registered by American laboratories between 1953 and 1963. On the list were food industry staples, including early maturing Sanilac beans, disease resistant Alamo X oats, the tough-hulled NC4X peanut, and winter-hardy Pennrad barley.
By the mid-1980s, American and Western European plant researchers had turned to gene splicing, and mutation breeding had migrated to other parts of the world. Radiation-induced mutagenesis produces random mutations; recombinant DNA enables precision interventions. Where know-how and skill in molecular biology accumulated, mutation breeding came to be seen as a relatively blunt instrument, an inferior tool. Paige Johnson, a nanotechnologist who also writes on garden history, provides apt analogies: “If you think of genetic modification today as slicing the genome with a scalpel, in the 1960s they were hitting it with a hammer.”
A radiation tower, where a radioactive source can be elevated to irradiate the plants and trees arrayed nearby.
Despite its lack of specificity, radiation breeding remains an important tool for crop research. It was embraced in the developing world because of low adoption costs. Today, interest in Asia remains particularly strong. In 2008, a gamma greenhouse twice the size of the IRB gamma field was constructed in Malaysia. The extraterrestrial creation of Purple Orchid Three is merely one among many late developments in mutation breeding.
Atomic Advertisements and Atomic Enthusiasts
Experimentation with irradiated seeds was not confined to the hallowed halls of science. From the 1940s through the early 1960s, enterprising businesspersons marketed mutants to the general public. In the 1940s, David Burpee, head of the W. Atlee Burpee Seed Company, foresaw limitless opportunities: “Yesterday we were using the old established catch-as-catch-can methods. Tomorrow we will work in a laboratory as scientifically equipped as that of a chemist or physicist, and our experiments will be systematically planned in advance…through the use of X rays, light rays, aging, mutilation, and chemicals we may induce mutations almost at will.”
Burpee hawked seeds modified by chemical mutagens, but ‘atomic seeds’ were sold in the late 1950s and early 1960s by dentist-turned-entrepreneur, Clarence J. Speas. Speas began experimenting with X-rays in 1937, as an instructor in oral surgery at the University of Vermont. In 1957, he received approval from the Atomic Energy Commission to obtain a quantity of Colbalt-60, which he used to irradiate seeds in a backyard cinderblock bunker on his farm in Tennessee. A series of photos from the May 1, 1958 issue of Life magazine show Speas giving a tour of his facility to high school students and showing off his tray of irradiated seedlings. In 1960, he founded Oak Ridge Atom Industries, Inc. to sell ‘atomic’ products.
On May 24, 1961, the company hosted a conference in Knoxville, Tennessee on ways to improve tobacco by irradiating seeds, seedlings, and flowers. Speas appealed to the tobacco industry for support and explained the science of radiation-induced mutagenesis. Charles M. Sprinkle, Coordinator of Agricultural Research at the R.J. Reynolds Tobacco Co., wrote back to the home office:
"Dr. Speas discussed in detail the work he and his associates have been doing in the field of irradiation. He gave each person present a bound report containing a general outline of a proposed research program for altering or improving tobacco. He pointed out that his organization has close personal contacts with around 6,000 scientists at Oak Ridge who are available to do consulting work. In addition, he can engage people in various agricultural fields at state experiment stations. He said that research could be conducted much faster by private enterprise than by traditional experiment station methods. Experiment station personnel and facilities would be engaged for certain phases of the work."
Sprinkle also listened to K. Wayne Graybeal, a Director at Oak Ridge, who addressed “the removal of carcinogens by irradiating finished cigarettes or by altering the tobacco plant.” Graybeal assured his audience that “if the tobacco industry desires it, a program can be oriented in this direction.”
Oak Ridge Atom Industries failed to develop a non-carcinogenic cigarette, but it did produce a string of successes including early prolific straight neck squash, California Wonder peppers, and New Hampshire midget watermelons. Newspapers occasionally reported on Speas’ more fantastic creations. A 1962 article in the Lodi News-Sentinel told of “200 tomatoes produced on one plant, which grew to a height of more than ten feet in a five-gallon bucket.” Other miraculous results included roses of four different colors on one rose bush, a seven foot-tall petunia, tomatoes shaped like sausages, and corn with eight ears on a stalk.
The first public showing of an ‘atomic garden’ took place on March 4, 1961 at the Home and Flower Show in Cleveland, Ohio. Life magazine published a photo spread on the event. The images drew attention to altered or enhanced traits, such as unusual colorings or bloom sizes. Housewives were shown marveling at atomic plants and seeds. Eventually, ads for atomic gardens appeared in many leading dailies – the New York Times, the Los Angeles Times, and the Chicago Daily Tribune. Common themes were public participation in science, the enjoyment of conducting one’s own experiments, and pecuniary opportunities. An advertisement for Oak Ridge Atom Industries promised a $3,000 cash prize to the winner of a contest for “the most unusual plant.” It also agreed to “purchase or pay royalties on new varieties deemed to have commercial value.”
The atomic gardening fad was brief, but it portrayed radiation-induced mutagenesis in wholly positive terms. Consumers were assured that irradiated seeds were not radioactive, and that mutant plants embodied improvements, not hazards. An Oak Ridge ad in the Chicago Daily Tribune encouraged the public to join in “100% safe scientific experiments. The seeds are safe to handle; the vegetables are safe to eat.” Another ad proclaimed that “Atomic gardening is no longer restricted to the laboratory! Now every ‘green-thumb’ gardener in Chicago can share in this exciting development!”
Public Perceptions and Scientific Understanding
Mutation breeding was popularized during a time of great technological optimism. The dangers of radioactivity were widely-publicized and broadly understood, yet the products of radiation breeding were incorporated into the food supply without generating fear or controversy. Not so for new agricultural biotechnologies employing the methods of molecular biology.
When crops containing genetically-modified organisms (GMOs) first appeared in the 1990s, protests were organized by environmental groups such as Greenpeace, Friends of the Earth, and the Earth Liberation Front. ‘Frankenfood’ horror stories were promulgated by activists: ‘GMOs pose risks of ecological contamination;’ ‘GMOs threaten populations of Monarch butterflies;’ ‘GMOs are potentially allergenic and dangerous to consume.’ The claims were false, dubious, or grossly exaggerated, but, as sociologists Sheldon Krimsky and Roger P. Wrubel have observed, once “techno-myths” become established, they are difficult to dislodge.
Media publicity fed skepticism and hostility toward recombinant crops, and public opposition prompted the European Union to place a moratorium on the importation and sale of GMOs in 1998. The ban was lifted only after the U.S. protested to the World Trade Organization and stricter labeling practices were implemented in 2004. Vague fears of biotech-related hazards became so acute and so widespread during this period that food supplies in humanitarian aid shipments to Zambia and Zimbabwe—where some 2.5 million people were at risk of starvation—were rejected at African ports because they contained GMOs.
Gross incongruities obtain between public perceptions of GMOs and the scientific consensus on the issue. Critics describe the production of GMOs as unnatural, but human beings have been performing genetic manipulations in plants and animals for thousands of years. Agriculture originated with plant domestication via seed selection as early as 10,000 years ago. Plant hybridization and radiation-induced mutagenesis later permitted the artificial introduction of genetic variation. Forms of hybridization – grafting and fusing plants in order to transfer and combine disparate traits in the same organism – were refined in the late 19th century, and allowed semi-directed genetic modification. The principal advantage afforded by radiation-induced mutagenesis was acceleration of random mutation rates. Nearly all foods consumed by human populations are products of one or more of these techniques of intentional genetic manipulation.
Contemporary molecular-scale interventions do not represent a break from prior breeding methods. Recombinant DNA has enabled directed genetic alterations and the design of transgenic species, but there is no scientific basis for distinguishing organisms engineered by recombinant means from organisms produced by spontaneous mutations, selective breeding, hybridization, or irradiation.
Scientific assessments have consistently found that the introduction of recombinant DNA into food supplies does not pose a unique risk. That is, a recombinant organism poses the same kind of risk as a non-recombinant organism. What matters is how an organism interacts with its environment, not how the organism was produced.
Research, Risk, and Regulation
In the United States, the regulatory apparatus for agricultural biotechnologies was sketched in a 1986 statement issued by the Office of Science and Technology Policy (OSTP), called the “Coordinated Framework for Regulation of Biotechnology.” Regulations have been established and enforced by three agencies: the Food and Drug Administration (FDA) evaluates new food products, the Environmental Protection Agency (EPA) determines the safety of microbial pesticides and other microorganisms, and the Department of Agriculture (USDA) considers the status of new plants and weeds.
In 1992, the FDA declared that food products derived from transgenic plants are “not inherently dangerous” and do not require special regulation. The agency could find no rationale for holding recombinant genes, proteins, or organisms to different standards in composition and processing than conventional crops. However, while the FDA determined that recombinant products were identical in form to conventional products, the EPA and USDA – citing ecological concerns – vastly increased the scope of regulation, requiring case-by-case reviews and lengthy field tests. Crops altered by radiation-induced mutagenesis had never provoked such a reaction, and were not bundled into the new classification created for recombinant products.
The policies adopted by the EPA and USDA were more responsive to public concerns and wishes, and placed less emphasis on expert testimonies. They also generated unintended consequences that have since become systemic, bureaucratically-sustained facts of commercial and scientific life: public and private investment in agricultural biotechnology has dried up, technical progress has been retarded, tight regulations have reinforced consumer wariness, and opponents of biotechnology have had more opportunities to delay the development and release of GMOs via litigation in the courts.
In January of 2001, the White House Council on Environmental Quality (CEQ) and the Office of Science and Technology Policy (OSTP) released the results of an exhaustive review: “No significant negative environmental impacts have been associated with the use of any previously approved biotechnology product.” Proponents of agricultural biotechnologies find it ironic that poorly-informed environmental activists have protested and effectively arrested the development of tools that could reduce pesticide use, require less land for farming, and leave more room for natural habitats that promote biodiversity. Yet, it would be counterproductive for those promoting scientific approaches simply to reiterate misunderstood facts and figures.
In a 2000 commentary in Nature Biotechnology, policy analysts Ambuj Sagar, Arthur Daemmrich and Mona Ashiya noted that when confronted by new technological risks, such as those posed by recombinant DNA, public constituencies tend to form opinions not only by evaluating technical facts and expert competence, but also by assessing the ways in which the social ties, economic interests, and political allegiances of policymakers and scientific authorities bear on grounds for trust. “Biotechnology’s future,” they concluded, “ultimately relies on governing institutions listening and responding to the public, rather than discounting key stakeholders as irrational, scientifically illiterate, or technophobic.”
If the potential of agricultural biotechnology to improve crops and solve urgent environmental problems is to be realized, public fears cannot be blithely dismissed and ignored. Fears will dissipate when public understandings of science are enhanced and transformed. As the tale of radiation-induced mutagenesis illustrates, history can serve as a tool of enlightenment.