Presented at the California Weed Science Society Conference in Sacramento, CA, on January 10, 2000.

Issues Related to the Development and Use of Engineered Herbicide-Tolerant Crops in California

F.L. Erickson and P.G. Lemaux
Department of Plant and Microbial Biology
University of California, Berkeley


I think a recent quote by Robert Shapiro, president of Monsanto, on consumer backlash to genetically modified crops provides an interesting perspective on some of the nontechnical issues that relate to the use of herbicide-tolerant crops.

"The public accepts biotechnology in medicine because it sees a clear benefit: saving lives. But about all crop biotechnology can do for now is make plants that are easier and cheaper for farmers to grow. While that's great for farmers it's hardly an appeal to middle-class consumers, particularly when they are being cautioned by opponents that the foods' safety hasn't been approved."

To me this was not a revelation; many of us questioned the wisdom of aggressively putting forward these products with improved agricultural traits as the first ones demonstrating the "promise of biotechnology". But, agrochemical companies proceeded and consumer backlash occurred, first in Europe and then in the US. It has been much more vehement than many of us following the issue anticipated. Such attitudes will likely result in a temporary slowing of the progress in the development of modified crop species, but it is not likely to stop the use of the technology in the long-term.

What is the status of crops being developed through biotechnology?

Methods have been devised to identify the genes involved in herbicide tolerance as well as other traits and to introduce those traits into many different crop species. Indeed, products produced from such biotechnological approaches are no longer just a promise; much is reality. Currently there are crops in the field and products in the marketplace that have been genetically engineered and are being eaten by consumers. In the summer of 1999, total acreage for corn and soybean was up to 25.8 million acres and 40 million acres, respectively. The actual percentage of production acreage that was genetically enhanced in the U.S. was 50% of cotton, 55% of soybean, 40% of maize and 3% of potato.

The products in commercial production today represent only the first, rather crude attempts to use engineering to improve crop plants. Much, much more is on the way. According to U.S. Department of Agriculture records, over 4,500 field tests of genetically-enhanced plant varieties have been conducted in this country, more than 1,000 in the last year alone. Only 50 engineered varieties have been deregulated, 13 varieties of corn, eleven of tomatoes, four of soybeans, two of squash, and even one type of radicchio. Hundreds more are in the pipeline and many of the field tests being conducted are in this category. These include plants that will improve disease and pest resistance, change postharvest or processing traits, alter nutritional or antinutritional qualities, improve agronomic traits, like enhancing nitrogen utilization and tolerance to herbicides. The technology will also be used to produce industrial compounds, such as industrial oils, substitutes for gasoline and biodegradable plastics. There is also work in progress to use plants as mini-factories to produce vaccines and other medicinals, foods that can help prevent a variety of diseases, like Type II juvenile diabetes.

What about herbicide-tolerant crops?

To date, herbicide-tolerant crops (HTCs) created through biotechnology are the most frequent application of genetic engineering to crop plants. This is because herbicide resistance is a simple, easily engineered trait that involves a single gene and the biochemistry of tolerance to certain herbicides is well-understood. At present, most engineered herbicide-tolerant varieties involve two herbicides: glyphosate marketed by Monsanto as Roundup; and phosphinothricin, or glufosinate, marketed by AgrEvo under various brand names such as Basta, Finale, and Liberty. In the case of tolerance to glyphosate the alteration is in an amino acid biosynthetic pathway. Tolerance can be engineered by overexpressing the native enzyme, modifying the enzyme to function in the presence of the herbicide or the use of a degradative pathway. With glufosinate the mechanism used to date has involved a degradative pathway. Engineering specific herbicide tolerances has allowed companies to link the sale of HTCs to the sale of their proprietary herbicides.

Early in the 1990's some effort was expended on developing bromoxynil tolerant varieties of cotton and tomato, but according to public records these efforts are no longer being conducted. Examples of California crops that are being engineered for glyphosate tolerance are corn, cotton, lettuce, rice, soybean, sugarbeet, tomato and wheat. Crops engineered for phosphinothricin tolerance include canola, chicory, alfalfa, corn, melon, rice, sugarbeet, tomato, cotton, and soybean. Currently, to my knowledge "Roundup-Ready" cotton is the only HTC being commercially grown in California. During the 1999 growing season, 5% of California's cotton was herbicide tolerant.

These products or their next generation relatives should provide useful, complementary weed management alternatives. With these benefits, however, come a variety of issues related to their use.

What are the issues related to their use?

The first concern with HTCs is the potential to promote the overuse of their associated herbicide, leading to the generation of herbicide-resistant weeds. Certain characteristics of herbicides and their use make them more likely to lead to this problem: single target sites for the herbicide, long soil residuals, season-long use and/or frequent and long-term application of a particular herbicide.

Glyphosate is considered low-risk for promoting herbicide-resistant weeds, but low-risk is not no-risk. This table was taken from a talk that I gave to this group in 1995. Since that time glyphosate resistance has been discovered in rigid ryegrass (Lolium rigidum) in both the United States and Australia and a glyphosate-resistant goosegrass appeared in an oil palm plantation in Malaysia. In all cases this occurred after repeated annual applications of glyphosate over many years. The fact that to my knowledge no examples of weeds resistant to glufosinate have occurred likely reflects the fact that this herbicide has not been used as widely or as long as glyphosate.

Another mechanism that might lead to herbicide-resistant plants other than the HTC is through the spread of herbicide tolerance genes to wild species, sexually compatible weeds or non-engineered plants, like those being organically grown. Of all traits being introduced by genetic engineering, herbicide tolerance is the one most likely to result in observable gene movement to other plants. Why? Observation of the presence of the tolerance gene is easily detected following herbicide application.

Outcrossing seems manageable. Genes for tolerance could certainly be transferred to related weed species; however, in the U.S., most crops do not have weedy relatives with which they can outcross. Exceptions are canola, carrots, certain cucurbits, lettuce, oats, radish, rice and sugarbeet. Outcrossing could be a problem when HTCs are used in developing countries, many of them centers of diversity for our crop species.

In situations where sexually compatible weeds or other species are present, farmers must be very cautious about using HTCs. Weeds growing nearby that can outcross with HTCs are likely to be kept under control by herbicide application and therefore not flower or at least not at the time when pollen-shed occurs from the engineered plant. If, however, pollen travels long distances and pollinates weeds located at a distance, where herbicide application does not happen, outcrossing might occur. With no selection pressure from herbicide application, however, this trait is not likely to endure in these populations.

Another means of managing the transfer and perpetuation of the herbicide tolerance gene in intermingled weed populations is to alternate the type of herbicide used from one season to the next or to use another herbicide to control the weed population during the season. A third solution would involve the use of so-called gene protection systems, the best known of which has been called the terminator technology. This strategy results in plants that cannot reproduce themselves because embryo development is halted. Although maligned because farmers cannot save seed, it would ensure that a compatible plant receiving pollen from an HTC would not reproduce.

Weed-shift is another problem that can occur with repeated application of the same or a related herbicide. This refers to the change in species composition in an ecosystem, which might occur due to elimination of controllable species and proliferation of those that are naturally tolerant of the herbicide. Development and utilization of germplasm tolerant to a single agent, without comparable development of cultivars tolerant to other herbicides with dissimilar modes of action, would likely exacerbate both the resistant weed and weed-shift problems and lead to the existence of herbicide-tolerant volunteers from previous HTCs. If farmers can purchase their preferred cultivars with tolerance to herbicides with different modes of action, then herbicide rotation is more likely to occur.

One benefit of HTCs, also demonstrated by this slide, is the potential for low-till or no-till agriculture. Farmers can wait until weeds have established foliage and root systems and then spray for control. The decaying weeds then form a mulch that prevents soil erosion and minimizes water loss.


Proponents of HTCs assert they are more profitable than non-GM crops because of reductions in herbicide costs and increased crop yields. However, to date evidence that these claims are true is sketchy. One report from Iowa State states that in 1998 Iowa soybean farmers using RR seed saved roughly 30% on their herbicide costs, but that yield drag caused a loss of 2 bushels per acre, meaning that total cost per acre for GM and non-GM soybean was about the same.

Charles Benbrook, an independent biotechnology consultant, recently published a review on RR soybean drag based on the results of over 8200 university-based soybean varietal trials performed in eight Midwestern states. His report concluded that in 1998 the yield drag of RR soybean compared to all other varieties tested, averaged between 5 and 10 percent lower, making them an economic wash. Nonetheless, he claims, they are popular with farmers because of simplified weed management practices.

Current RR soybeans yield less probably because the engineered traits were not introgressed into crop varieties that perform best in different growing regions. In the future companies developing HTCs will have to work with public- and private-sector breeders to introgress herbicide tolerance traits into cultivars adapted to perform optimally for specific growing regions.

The economic impact or perceived impact appears to be different in South America where Brazil and Argentina have taken different stances on RR soybean. The U.S. and Argentina are the two top soybean producers in the world and both have approved the growth and sale of GM soybean. Brazil, on the other hand, has not approved the planting of bioengineered soybeans and thus have emerged as the world's premier source of non-GM soybeans. European supermarkets proudly proclaim their use of Brazilian beans; one British chain even imports frozen chickens from Brazil because they are fed conventional soy meal.

But Brazilian farmers are not so happy about this. They know that their competitors across the border in Argentina are permitted to use the new seeds and, according to this account in the WSJ, cut their costs by some 20% by avoiding more expensive herbicides. With world soybean prices at a 25-year low, farmers need to lower costs. Brazilian farmers feel this tool is being taken from them and they don't understand the furor. They are smuggling seeds from Argentina and the Brazilian government has responded by inspecting storage sheds, spot checking for genes, burning fields and seizing sacks of seeds.

Consumer Acceptance of Products of Biotechnology

When new technologies are introduced into food production, there are often consumer concerns. Furors occurred over pasteurization, microwave ovens and food irradiation. Biotechnology will not be an exception.

Why do I say that? Unrest over genetically modified foods began to erupt in Europe nearly two years ago. This led to consumer unrest so strong that supermarkets were forced to rid their shelves of products containing GMOs and governments to enact moratoria and strict labeling laws. Protests and vandalism occurred. Newspaper accounts of the turmoil were seen in the U.S. almost daily.

In my opinion, the furor in Europe came about because of some fundamental differences between Europe and the U.S. Consumer concerns there were being fed by scare stories about the potential effects of GMOs, which were made more credible because of the manner in which the government handled two earlier food scares, mad cow disease and dioxin contamination. The pronouncements and decisions made by governmental officials during those controversies were perceived by many to be based on political expediency rather than on public safety concerns. This undermined consumers' confidence in the government to assure the safety of biotech foods. Another clear issue is that blocking U.S. imports of large quantities grain and other agricultural products has a very positive impact on European farmers, the most heavily subsidized in the world.

But we had been through our "uncomfortable" phase in the late 1980's and early 1990's". There had been heated debate and anti-GM legislation enacted over the ice-minus bacterium and later over milk from BGH-injected cows. But this time had passed. The trend toward acceptance of GM foods in the U.S. was seen in many surveys, including some that were very recent. The International Food Information Council in February and again in September of this year determined that the majority of U.S. consumers were willing to "purchase a food modified by biotechnology to taste better or fresher" (62%, Feb; 51%, Oct.) or a food "modified by biotechnology to be protected from insect damage and requiring fewer pesticides" (77%, Feb; 67%, Oct.).

Recent anti-biotech events in the U.S.

However, once tensions and accusations reached a certain peak in Europe, anti-biotechnology efforts crossed the Atlantic to Canada and the U.S. A very significant early event in the U.S. was getting baby-food giant, Gerber, to agree not to use GMOs in their baby food. Not only did Gerber agree to that, but they also agreed to use "organically grown" corn and soy flour. After this pronouncement several other large companies followed suit.

Perhaps the most significant was Archer Daniels Midland, one of the country's largest grain handlers. ADM decided in late summer of this year to demand that their suppliers segregate GM from non-GM grain, only, as they said, because of "a change…in consumer demand". International trade had become a question. What products would and would not be accepted in Europe? Would they have to be guaranteed to be GM-free? Soon food processors paid premiums to farmers for GM-free grain. According to a Kiplinger article of January 6, ADM and Con Agra were extracting a premium of as much as 50 cents a bushel to broker non-GMO grains - about 10% above the average price for soy and 25% above the average for corn. According to some business analysts, the processors themselves stand to increase their profits through the support of this two-tiered pricing structure; there are more opportunities for profit to be made.

But the momentum is not all in that direction. More recently another large processor, Cargill, sent a message to producers stating that they will accept genetically engineered crops at all of their U.S. grain-handling, oilseed processing and wet corn milling facilities this season and next. Most grain-handling facilities will even accept varieties approved in the U.S. but not yet approved in Europe.

And despite an advertising campaign focusing on "Frankenflakes" and "FrankenTony", officials of Kellogg's are standing firm so far. They have stated that they will continue to use GM ingredients in their cereals in the U.S., although they have removed them from products destined for Europe. They believe products made from GM crops are safe and that the majority of consumers are not demanding their removal.

Even the church has taken a stand on biotechnology with the Vatican issuing a statement that "the advantages of genetic engineering of plants and animals are greater than the risks".

Consumer attitudes

A poll taken on September 23-26, 1999 by Gallup, began to reflect what might be a shift in attitudes toward GMOs in the U.S. Respondents were asked to rate the likelihood that biotechnology poses a serious health hazard to consumers; 53% thought it did not present a serious hazard, 20% were unsure, but what I thought to be a significant fraction, 27%, thought it posed a serious hazard. While admitting to this fear, respondents still had confidence in the U.S. Food and Drug Administration, the regulatory arm that monitors genetically engineered foods. 76% of Americans had a great deal or fair amount of confidence in the federal government to ensure the safety of food.

Labeling Issues

But editorials and other newspaper and journal articles began to ask questions. Why weren't consumers being told that they were eating Frankenflakes? Were they being used as guinea pigs in a giant corporate experiment? Stories questioned the safety of GMOs. They would cause allergies; they might contain new toxins; they killed Monarch butterflies and their antibiotic resistance genes would transfer to humans, rendering human antibiotics ineffectual.

Perhaps in part because of such newspaper headlines, interest in labeling rose. This was reflected in the Gallup poll, where numbers supporting labeling climbed to over 2/3 of respondents, even if it meant an increase in price. This increased interest led the FDA to convene a series of "town hall" meetings around the U.S. to seek consumer input on their labeling policies. I attended the rather heated debate in Oakland on December 13.

What are the issues with labeling? First of all, I don't think for many it is a food safety issue, rather it is a personal choice issue. Some consumers just want to know that they are eating something that has been genetically engineered, simply out of a right to know. Others want to use the label to identify GMOs so they can use their "economic clout" to vote against the technology.

Implications of the Unrest

Is the unrest over GMOs and around labeling just a hiccup that will go away after a short time? If I had been speaking with you a year ago, my answer would have been yes. Today I think my answer is different.

Why do I think that the situation is more serious now? It has to do with international trade issues, increasing public awareness of GMOs, a larger sphere of organizations involved in the effort and public attitudes toward agriculture and risk. All in all it is much easier to instill fear in the short term over a new technology than safety. We live in a technologically complex world and it is often difficult for people to understand the nuances of complicated technologies. When a direct personal benefit is not seen for themselves or the population as a whole, consumers will not want to take a risk, no matter how small. Benefits of GM crops so far have not been to the consumer; benefits to farmers, even if they are said to help the environment, simply don't carry weight anymore.

What individuals define as "safe" is, for them, "acceptable risk". Perceptions of risk depend on the familiarity, "friendliness" and voluntary nature of the risk. Some of consumer reaction to GM foods derives from "involuntariness" of perceived risks; European consumers were not aware that soy and corn from the U.S. was genetically engineered. In the U.S., we eat a much healthier diet and we don't spend much money doing it. With this abundance of food and promise of a longer, healthier life has come a demand for a "risk-free" world. Under the circumstances of our successful food production system, the public is not interested in new technologies for food production, especially if there is a hint of a safety risk.

At the end of the road?

How will the whole labeling and public acceptance scenario play out? It is difficult to make predictions for the short-term (2-5 years), but it is likely that in ten years the technology will pervade agriculture. Why? New information gained from studies of the genome will provide new avenues for crop improvement that cannot be achieved in any other way. These benefits will be realized by the consumer and in improvement in the environment.

The first products of the technology are crude; the Roundup Ready soybean is not the best that can be done in terms of an HTC. Many of these products will not achieve the potential necessary for user or consumer acceptance. But the strategies will be improved and refined, just as the computer has moved from a machine that took up city blocks to one that fits on your wrist.

Some products of the technology will find favor with users and consumers; some will not. Some will be a commercial success; some will not. But in the long-term, biotechnology is likely to find applications and result in products that will be important tools in the farmer's toolbox and that will be accepted and likely even sought after by consumers.


Over the past decade progress in the generation of engineered HTCs has been rapid with major acreage crops in the United States, namely corn, cotton, and soybean. These or later generation HTCs can play an important role in production agriculture if they are properly managed since they provide some distinct advantages for the farmer in combating weed problems and providing the opportunity for lower or no-till agriculture.

While these approaches are available for high-acreage crops, they are not yet available for many of California's minor acreage crops. Their availability for California s fruit, vegetable and nut crops, is likely to be limited in the near term since the economic gains do not justify the expenditure by agrochemical companies in developing them and public sector scientists have difficulty doing this because of intellectual property issues.

Questions regarding the use of HTCs have been raised and will be answered. Currently consumer fears and international trade issues are important factors affecting the desirability and utility of HTCs. With time these issues will be resolved, perhaps by the time minor acreage HTCs are available!

© 2000 Peggy G. Lemaux