Modifications of crop plants can be organized into two main categories: those that benefit the producer and those that benefit the consumer. Modifications that protect the crop from either biotic or abiotic stress or increase total crop yield benefit the producer and are called input traits. The majority of modified crops in commercial use fit in this group. Scientists have just begun to tap the large potential of biotechnology to produce varieties of plants that confer a wide spectrum of advantages to consumers. These varieties are modified with output traits.
One of the most publicized uses of biotechnology in agriculture is the modification of corn to express proteins produced by the common soil bacterium, Bacillus thuringiensis (Bt). Organic farmers have been using Bt as an insecticidal spray for over 40 y. Bt organisms have been modified to express a class of insecticidal proteins called Cry. These proteins are effective against certain insect pests but are harmless to humans, mammals and birds. Bt corn was introduced as a commercial crop in 1996 and has been described as "the most important technological advancement in insect pest management since the development of synthetic insecticides" because of its inherent resistance to infestation by one of the most serious corn pests, the European corn borer (Ostrinia nubilalis) (6 ).
In addition to decreasing yields, infestation of corn by the European corn borer facilitates spoilage by the mold, fusarium, which forms a mycotoxin, fumonosin, in corn (7 ). Fumonosin is a toxic substance that, among other things, has produced liver damage in all animals studied. Although currently inconclusive, some evidence suggests that it may also play a role in human esophageal cancer (8 ). Studies challenging maize hybrids with the European corn borer found decreased fumonisin concentrations for transgenic maize varieties expressing specific Cry proteins, 2.1 ug/g compared to 16.5 ug/g for nontransgenic maize hybrids (7 ).
Beyond the health benefit to livestock and consumers, infected corn becomes an economic problem. Corn that exceeds levels allowable for the intended use must either be discarded or used for another purpose, causing a loss of profit (9 ). In fact, overall losses to farmers as a result of the European corn borer-infested crops (including corn, cotton, sorghum, and other vegetables) total 1 billion dollars a year (10 ). On the whole, Bt corn and Bt cotton have improved farm efficiency (11 –13 ). A report by the U.S. Department of Agriculture concludes by saying that even though the benefit and performance of genetically modified crops varies depending on many factors including region and pest infestation levels, the adoption of crops such as Bt cotton in the Southwest and herbicide-tolerant soybeans led to significant increases in net yield, and a significant decrease in the application of insecticide (14 ).
An expansion of the same report by the Economic Research Service investigating same-year differences between average pesticide use of adopting and nonadopting farmers showed that those using genetically modified corn, soybeans and cotton combined used 7.6 million fewer acre-treatments (acres being treated multiplied by the number of treatments) of pesticides compared to nonadopters in 1997. In 1998 the difference increased to almost 17 million fewer acre-treatments by adopters (15 ).
On the other hand, others have concluded that despite a sharp increase in planting Bt corn, the percentage of corn treated with insecticides has remained constant throughout the period (6 ). Moreover, some research suggested that Bt corn pollen was harmful to the Monarch butterfly (16 ). Collaborative research by scientists from universities and research institutions in the US and Canada have concluded that potential risks of Bt corn to Monarchs is low. This is due to the density and time of pollen shed in relation to the period of larvae activity. Also, the proportion of milkweed plants growing near cornfields and the proportion of fields that are planted with Bt corn are other mitigating factors cited for the low risk to Monarch butterflies (17 ).
Other traits have been added to a variety of crops to defend from biological insults. Tomato, potato, squash and papaya are among a variety of crops that have been modified to resist infection by viruses or insect pests (18 ).
In addition to biotic stressors, plant productivity is influenced by abiotic factors such as herbicides, soil composition, water supply, and temperature. Therefore, conferring plants with genes that will help them withstand a wider range of environmental conditions could increase productivity. Plants are also being engineered to withstand drought, heat, cold temperatures and poor soil conditions such as salinity and aluminum contamination (19 –23 ).
Increased total yield of harvest also can be achieved by enhancing efficiencies in the metabolic and photosynthetic pathways. Examples of pathways that could be improved to increase crop yield include nitrogen assimilation, starch biosynthesis, and modification of photosynthesis (24 –26 ).
After harvest, time to market is an important economic factor due to the perishability of produce. Changing the rate of ripening would seem to be a benefit to both the farmer, by decreasing post harvest losses, and the consumer by increasing shelf life. To prevent delivering spoiled fruit, mature tomatoes are harvested while still green and ripened during delivery by exposure to ethylene, a ripening hormone in tomatoes. In 1994 the Food and Drug Administration approved a brand of tomato that had a genetic solution to this processing problem (27 ). The producers of the tomato used antisense technology to silence a gene that produces polygalacturonase, a pectin-degrading enzyme found in ripe tomatoes, thus slowing the ripening process (28 ).
Consumers stand to gain more than just produce with longer shelf lives. While still in its infancy, the technology is being used to produce plants that will have a whole range of output traits including increased nutritional value, medicinal properties, industrial utility, and novel taste and esthetic appeal. Many of our common food crops could be improved to better meet the nutritional requirements of humans or animals. Protein, starch and oil composition and content as well as micronutrient content can all be improved to make foods and feeds more nutritious. (29 –36 ) For example, a new strain of potatoes containing 30–60% more starch has been developed by inserting a bacterial gene for an enzyme in the starch biosynthetic pathway. These high-starch potatoes have less moisture and therefore absorb less fat during frying (37 –39 ). Enzyme biotechnology also is being used to develop specialty oils containing more favorable fatty acid profiles such as high oleic acid peanut oil (40 ).
We have known for a long time that vitamins and minerals elicit biologic responses and have positive effects on health. Carotenoids are another class of nutrients that may be associated with decreased risk for certain cancers and macular degeneration. Among other plants they can be found in papaya (ß-carotene), tomatoes (lycopene), kale and spinach (lutein) (29 ).
Beta-carotene has already been expressed in a genetically engineered rice cultivar, named Golden Rice, by addition of genes for three enzymes in the phytoene synthase pathway (two genes from a daffodil and one from the bacteria Erwinia uredovora) (41 ). This strain was also crossed with a high iron strain of rice to produce a strain with both qualities (42 ). Golden Rice has been the subject of much attention because it represents the potential of future biotechnology crops to benefit people in developing countries. This variety of rice could decrease malnutrition and blindness associated with vitamin A deficiency. However, there have been questions raised about the effectiveness of this rice because of the many biological, cultural and dietary barriers that must be overcome (43 ). These questions will need to be answered as the product is further developed prior to introduction.
Other phytonutrients with purported health benefits include glucosinolates, phytoestrogens, and phytosterols. Found in a wide variety of food sources, these compounds could selectively be overexpressed to therapeutic levels (44 ).
In a much different way, biotechnology is poised to completely change another aspect of preventative health care. Methods are being developed to produce vaccines in plants by introducing genes that express a protein antigen in crops such as corn, potatoes and bananas. When eaten these antigens elicit an immune response and have been shown to provide protection against a subsequent challenge from pathogens (45 ). The feasibility of this approach was demonstrated when mice fed transgenic Hepatitis B surface antigen expressed in potato tubers showed a primary immune response by producing antibody specific to the antigen (46 ). Companies are positioning themselves to become suppliers of a wide range of biotechnology products, including bioactive therapeutic proteins, blood proteins, animal health products, and industrial enzymes.
There are many other possible industrial applications for genetically modified organisms. For example, researchers at the University of Georgia engineered yellow poplar trees to have the ability to extract toxic ionic mercury from soil and convert the toxin to a relatively inert form. The gene was acquired from mercury-resistant bacteria that are soil-borne and thrive at sites polluted with heavy metals. In one study the engineered plants were capable of ten times the rate of mercury removal as compared to nonengineered plants (2 ). This is just one example of how phytoremediation, the use of plants to clean or contain contaminated areas, combined with biotechnology is a promisingly efficient, economical, and environmentally friendly technique that could restore soil health and revegetate contaminated waste sites.
Clearly, consumer preference is playing a role in the industry’s choice of product development. Just as consumers have appreciated seedless oranges and watermelon, the industry is developing other fruiting crops that do not require fertilization to produce seedless fruit. Novel produce such as seedless tomatoes, squash, eggplant, peppers, strawberries, melons and cherries, to list a few of the possibilities, would be attractive to many consumers. Additionally, these fruits would have improved taste due to increased total soluble sugar compared to seeded fruit and may be of economic value to the processing industry as well (47 ).
Also in development is a sweet protein found naturally in the fruit of the African vine, Pentadiplandra brazzeana. This heat stable protein is 500 times as sweet as sucrose at higher concentration and as much as 2000 times as sweet in a two percent (by weight) solution. Lacking bitterness, it has a lot of potential as an alternative low energy sweetener (48 ).
It is clear that plant biotechnology has the potential to have a huge affect on tomorrow’s society. Already over 50 biotechnology crop products have passed the regulatory review process and have been commercialized, ranging from corn and potatoes to tomatoes and squash (18 ). It is interesting to note that crops modified by biotechnology are the most rapidly adopted technology in the history of agriculture. In 1996 only 4.3 million acres of biotech crops had been planted; by 2000 that number increased to 109.2 million acres (49 ).