Talk presented at the Agronomy Continuing Conference held in Davis, CA, on February 23, 2000.

What's Out There in Terms of Genetically Engineered Crop Plants and What's Likely to be Coming in the Future?

Peggy G. Lemaux

What is a GMO?

Literally GMO stands for genetically modified organism. When I first heard the term coming out of Europe, I was puzzled because as we all know every living organism has been genetically modified throughout evolution. Genes are randomly mixed during the process of fertilization to create the next generation of progeny. In addition, deletions, additions and rearrangements occur, giving rise to mutation that often leads to new characteristics in the resulting organism. This process has led us from the ancient tomato to the modern cultivars and from an ancient ancestor of maize to modern hybrid corn.

But GMO, as used by the popular press, does not refer to this type of genetic modification; it refers to organisms created through the use of the new tools of genetic engineering. Just to make sure we are all on the same page here, the latter means accomplishes change by identifying a single gene from the tens of thousands of genes in an organism, manipulating it in the laboratory to give it new properties or different regulatory signals and then introduced into single plant cells (using a gun, a needle or a bacterium) and then allowing the transformed cell to divide and give rise to an entire organism, each cell of which has the new gene permanently embedded in its genome.

There are some aspects of this process that are the same as those involved in classical genetic exchange and others that are different. In both cases, of course, the exchange occurs via DNA, the fundamental chemical structure in a cell that dictates its makeup. In addition many of the same enzymes are used in the laboratory to insert genes, as are used during the process inside the cell. But genetic engineering involves the very precise manipulation of specific segments of DNA, whereas with classical genetic hybridization the exchange of genetic material between two organisms is random. During the random exchange rearrangements of genetic material can occur, where two new segments of DNA are joined together to bring new genes and regulatory sequences together. This has occurred throughout evolution and sometimes allows species to make adaptations that allow them to adapt better to new environments. The genes introduced during genetic engineering also find themselves juxtaposed to new sequences in much the same manner, since the process of insertion is mostly random. Methods currently under development will permit the precise positioning of the new genes.

Another difference with the newer methods of genetic manipulation is that it is possible to control the manner in which the gene is expressed. If it is necessary to express the gene only in the anthers, only in the epidermis or only in the endosperm of the seed, it is possible to identify regulatory sequences that can do that. It has even been possible to isolate promoters that are activated only when a nematode burrows into a root. They do not activate when you break or damage the root in another way. This gives a great deal of precision to the way in which these genes are controlled and will allow the creation of engineered crops that avoid some of the problems with the initial offering, like the B.t. maize that expressed the insecticidal protein in the pollen and roots of the plant.

Lastly, the source of the genetic material involved in the exchange has to be closely related in the case of classical hybridization. For example, two species of tomatoes can exchange genetic material but tomato and potato, which are closely related, cannot cross breed. With genetic engineering, the source of the genetic material to be inserted into the plant can be any living organism. For example, you could use a gene from the species itself, as was done with the Flavr Savr Tomato, or you could use a gene from another plant species, for example a disease resistance gene from a wild tomato species could be used to modify potato or broccoli. The gene could also come from a bacterium, as has been done with herbicide resistance genes.

What Crops Have Been Genetically Modified?

The first demonstration of the genetic modification of a plant occurred in 1984 with the engineering of tobacco with a marker gene. Since that time more sophisticated methods of gene exchange have been developed that allow researchers to modify nearly every plant species. In general these methods involve identifying the gene of interest (i.e., what do you want to change), and then finding some way to get the gene to integrate permanently into the plant cell and regenerate a fertile plant. This process has been easily accomplished with model species and particularly with dicot species, but many crop species have been troublesome. The more difficult crops have included cotton, sugarbeet and most of the cereal species.

However, over time the hurdles to the efficient transformation of these species have been overcome and the transformation of many species has become routine. To date, over 50 different plant species have been successfully transformed with a number of traits. Initial attempts at manipulating plant species made use of easily transformable varieties and easily identified genes, such as those for herbicide tolerance and certain types of pest resistance. The latter used an approach based on a naturally occurring toxin from a soil bacterium, Bacillus thuringiensis, which had been used by backyard gardeners for years. It was also determined early in the process that the expression of certain viral genes themselves, e.g., the coat protein, were capable of conferring viral tolerance to the host. Plants are being grown commercially that utilize these approaches, for example the Roundup Ready soybean, BollGard cotton and viral resistant potato and papaya.

The road from the initial finding of the function of a gene to the production of a crop species that bears this new characteristic is long. Commercialization involves identifying plants that stably express the characteristic, extensive field testing to insure that the crop performs in the field, clearing regulatory hurdles with the USDA, EPA and FDA, in the case of a human food, clearing intellectual property hurdles and perhaps the final challenge winning consumer acceptance.

How Have the GM Crops Performed?

The commercial varieties involve only a limited number of crop species and focus on only a few agronomic and pest-resistance traits. Despite this fact, acreage being planted in engineered cotton, soybean, corn and potato varieties is substantial and has been rising over the last three years. In the summer of 1998, 26.5% of the corn planted in the U.S. was genetically engineered; 27% of the soybeans; 44% of the cotton and 3% of potatoes. Acreage continued to rise to approximately 75 million acres during the 1999 growing season and was anticipated to continue rising during the 2000 planting season, but I seriously doubt that at this point due to the demand for segregation and public attitudes toward GM foods.

Despite the short-term prediction, it is important to know how these first varieties performed for farmers in the field? Some farmers have been pleased with the new varieties; others see a lot of room for improvement. As with the first products of many technologies, these offerings are crude in comparison to later generation versions that will likely be more efficient and efficacious and be contained in a wider variety of genetic backgrounds. These new varieties have brought some new changes for farmers, like having to pay upfront for the high-cost seeds before knowing whether the investment would pay off because of high pest or weed pressure. They also have realized that, as with hybrid crops, they are not able to re-plant from saved seeds, although most high-yield farmers do not engage in this practice.

In July of 1999 a report was released by the National Center for Food and Agricultural Policy that attempted to quantify the effects of the new B.t. crops. These are varieties that have been engineered with their own pesticidal compound, a naturally occurring protein made by a soil bacterium known as Bacillus thuringiensis. With some of the engineered varieties, like Bollgard cotton, profits for farmers were realized. Adjusted figures showed an overall reduction of 5.3 million less pesticide treatments, resulting in an overall net benefit to cotton producers of $92 million.

In other crops, like B.t. corn, profits for farmers varied from year to year. Infestation pressure was heavy in 1997, leading to savings for farmers of $72 million; in 1998 when infestations were low, farmers lost $28 million! This resulted from the fact that farmers had to decide whether to pay the increased costs for the engineered varieties before knowing the severity of the infestation. For herbicide-tolerant (HT) varieties, the conclusions were also mixed. A report from Iowa State University showed that in 1998 Iowa soybean farmers using Roundup Ready seed saved roughly 30% on their herbicide costs. This was impressive but the savings realized in chemical inputs was offset by a yield drag in the engineered varieties that caused a loss of 2 bushels per acre, meaning that total costs per acre for GM (i.e., genetically modified) and non-GM soybean were about the same. Recently Charles Benbrook, an independent biotechnology consultant, published a review on Roundup Ready soybean based on over 8200 university soybean varietal trials performed in eight Midwestern states. His report concluded that in 1998 the yield drag of Roundup Ready soybean, compared to all other varieties tested, averaged between 5 and 10 percent lower, again wiping out the savings realized by the lower inputs. Why the yield drag? Likely it is due to the fact that the Roundup Ready trait was only put into a limited number of soybean varieties, which were not optimally suited for growing in all areas. Putting the trait into a larger number of varieties optimized for growth in diverse areas should improve the savings realized by the farmers. Despite the lack of dramatic financial savings, Benbrook claims that the varieties are popular with farmers because of simplified and more diversified weed management options.

Analysis of the use of HT canola showed similar patterns. Although these varieties offer a large weed-control advantage, this did not necessarily translate into yield advantages as large as farmers had hoped for. A big factor in how advantageous these varieties were depended on whether or not weeds were present that were hard-to-control with conventional systems. If farmers had a big problem with difficult weeds, like stork's-bill or cleavers, then the herbicide-tolerant system was a huge advantage, with yield increases of 13 to 39 percent over conventionally controlled fields. But, if the most competitive weeds were not present, yields using conventional seed and weed-control systems were not that much lower. A clear advantage of HT crops is that more weed control options are available, which with proper management can lead to improved weed control strategies and more sustainable systems that include herbicide rotations.

What is in the pipeline for the future of these crops?

How are such technologies being used to modify crops? Some of the earliest products of the technology are in the fields and in the marketplace; others are simply being explored as ideas in university laboratories. The range of changes being targeted is substantial. More recent modifications have made use of fundamental information gained through genetic, biochemical and genomic studies of the plant species themselves and their pathogens. These approaches, only now being studied in laboratories and in limited field tests, will be a part of the next generation of engineered plant species.

Considerable activity has been aimed at increasing resistance to pests. This has included a number of strategies for viral resistance. The most commonly used involves the use of the coat protein gene from the virus itself. This has been used in a number of crops, including potato and papaya. The engineering of papaya to be resistant to papaya ringspot virus has reinstated this crop in certain areas of Hawaii that had been devastated by this disease. Strategies other than the coat protein approach are currently being developed that will allow newer generation approaches that might provide a wider range of protection against viruses.

Tomato speck and fungal resistance. A number of other approaches are being pursued at the research level and these include those involving natural resistance genes. Plants are hosts to thousands of infectious diseases caused by a vast array of pathogenic fungi, bacteria, viruses, and nematodes. Some plant species can resist the invading pathogens by inducing rapid defense responses that inhibit the spread of pathogen infection. Resistance to a pathogen usually depends on the presence of specific resistance gene in the plant that functions in recognizing a specific pathogen. Over the past few years, dozens of plant resistance genes have been identified and isolated from numerous plant species. Much of this work involves the identification of natural resistance genes, such as the discovery of the rice blast gene here on the UCD campus, the N viral resistance gene at the USDA Plant Gene Expression Center and a bacterial resistance gene from tomato at UCB. Surprisingly, these genes encode highly similar proteins, which suggests that similar mechanisms are involved in recognizing diverse pathogens. Indeed, one of these resistance genes, the tomato Mi gene, identified here at UCD, provides resistance against both nematodes and aphids. As information on how these genes offer protection against pests, they can be used to engineer resistance to a broader array of pests and diseases in the host and other plant species. Approaches to insect damage in the commercial sector have focused on those involving the Bacillus thuringiensis genes. These have resulted in Bollgard Cotton and European Corn Borer resistant maize. Issues relating to resistance management in these plants have led the EPA to issue a recent mandate specifying the percent of acres a farmer must plant in non-B.t. crops in order to provide a sensitive population of insects to interbreed with any resistant organisms that develop as a result of pesticide ingestion. Second generation insect resistance strategies are also being developed with different mechanisms of action.

Molecular approaches are also being devised to improve agronomic traits. Such strategies might provide tolerance for plants from stresses, such as floods, cold and salt. These strategies are more complicated, often involving several genes and requiring more research in order to demonstrate successfully a change in a trait. Work is also focused on understanding the mechanisms by which plants take up and utilize fertilizer. By understanding the biochemical basis for this process, strategies are being devised to engineer plants to be more efficient at the process, thereby sparing chemical inputs. The symbiosis of plant roots by nitrogen-fixing microorganisms is now understood in considerable detail and the mechanisms of nitrogen fixation and transfer of nutrients from bacteria to plants has also been scrutinized. With this understanding comes the possibility of increasing the efficiency of the process. In fact some improved strains of Rhizobium have been developed but have not been released into the environment.

Among the first engineered plants available commercially are herbicide-tolerant crops. If deployed responsibly, these varieties can lead to lower inputs of pesticides, to lower soil erosion through low-till approaches to weed control and to easier, more flexible weed control strategies. Herbicide tolerance has been engineered into nearly every major crop species and is in the pipeline in many of the more minor ones. The major approaches are either with Monsanto's Roundup or AgrEvo's Liberty herbicides.

Some effort has been expended on post-harvest and processing characteristics. These include stopped- or slow-ripening melons, tomatoes, bananas, raspberries and even cut flowers. They also include more uniformly ripening cherry tomatoes and higher solids tomatoes and potatoes. Future strategies might include engineering grains to be more easily processed and, in the case of barley, faster malting varieties.

Another area of interest for genetic engineering approaches is the creation of so-called "functional foods" or nutraceuticals. This is likely to be the area of greatest activity in the private sector in the future. With these types of foods it is easy for the consumer to see a benefit. What are these types of foods? It involves the engineering of an edible plant part to deliver an extra benefit to the consumer. This can be accomplished in one of two ways. First through the removal of an antinutritional, e.g., making foods like rice and wheat less allergenic or removing toxic compounds, like the glycoalkaloids from potatoes and cassava or the phytate from certain animal foods. A second way to create a functional food would be through the addition of a component that renders a food more nutritious, e.g., by raising the level of certain vitamins, amino acids or minerals in the food. Low phytate varieties. Examples of this approach include increasing the beta-carotene or iron content of rice or the antioxidant content of broccoli. Another goal of functional foods is to use foods as a delivery vehicle for medicinals. Examples of this use are foods that when consumed vaccinate humans and animals against disease. Foods can also be used as a vehicle to develop immunotolerance, which can help prevent diseases like Type II juvenile diabetes.

Plants can also be used to make other products currently being made in other ways. An example in sugarbeet is rather ironic. It is the use of sugarbeets to make the sugar substitute fructans. This has now been achieved at commercially viable levels; up to 40% of the cry weight of the tuber can be fructans without impairing the growth or phenotype of the sugarbeet. In addition plants can be used to make products that are currently being made with non-renewable resources, items like industrial oils, gasoline substitutes and biodegradable plastics. While work on the latter has been suspended for the moment, major strides have been made at the research level to make this approach viable. Plants are our ultimate renewable resource and can be grown year after year to provide these in-demand products.

How will it all play out?

How will the current scenario play out? Will there be labeling? Will segregation of GM crops be mandated and enforced? Will GM varieties be appealing to farmers and consumers alike? 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 food production. Why? Many of the current products have not achieved the potential necessary for user or consumer acceptance. New information gained from analyses of the current generation of plants and from studies of the genome will provide new avenues for crop improvement that cannot be achieved and that will be accepted and likely even sought after by consumers in any other way. Strategies for creating the new foods will be improved and refined, just as the computer evolved from a machine that took up city blocks to one that fits on your wrist. In addition consumers will gain familiarity with the foods and have time to judge their safety and new generation GM crops will offer more tangible benefits to them.

In the end, some products of the technology will find favor with users and consumers; some will not. Some will be a commercial success; some will not. Some will be developed in the private sector; some in the public sector. 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.

2000 Peggy G. Lemaux