Biosafety of Bt-Crops Safe Transition
 
P. Ananda Kumar, NRC on Plant Biotechnology, Indian Agricultural Research Institute, New Delhi
 
 
Introduction
 
Insect pest management in agriculture is important to safeguard crop yields and productivity. A large number of chemical insecticides that effectively control insect pests have been proven to be harmful to human health and environment. There is a need to reduce the dependence on pesticides by using safer alternatives to manage insect pests. Many insecticidal proteins and molecules are available in nature, which are effective against agriculturally important pests but innocuous to mammals, beneficial insects and other organisms. Insecticidal proteins present in the soil borne bacterium, Bacillus thuringiensis (Bt), which has demonstrated its efficacy as a spray formulation in agriculture over the past five decades, have been
expressed in many crop species with positive results (Kumar et al., 1996). Bt-transgenic crop species (cotton, corn, rice, tomato and potato) have been commercialized with substantial benefits to the farmers (Kumar 2003). Bt crops were cultivated in an area of 32.1 million hectares out of the global transgenic area of 102.0 million hectares in 2006 (James 2006).
 
Bacillus thuringiensis
 
Bt is a gram-positive, aerobic, endospore-forming bacterium belonging to morphological group I along with Bacillus cereus, Bacillus anthracis and Bacillus laterosporus. All these bacteria have endospores. Bt, however, is recognized by its parasporal body (known as the crystal) that is proteinaceous in nature (see figure above) and which possesses insecticidal properties. The parasporal body comprises of crystals varying in size, shape and morphology. The crystals are tightly packed with proteins called protoxins or-endotoxins.

There are many subspecies and serotypes of Bt with a range of well-characterized insecticidal proteins or Bt toxins (-endotoxins). At present it has been estimated that over 60,000 isolates of Bt are being maintained in culture collections worldwide. Known Bt toxins kill subsets of insects among the Lepidoptera, Coleoptera, Diptera and nematodes. The host range of Bt has expanded considerably in recent years due to extensive screening programs. Currently more than 140 different genes encoding Bt toxins have been cloned. Recent information about Bt toxins/genes can be obtained from http://www.biols.susx.ac.uk/Home/Neil_Crickmore/Bt/.

 
Mode of action
 
The Bt toxins exert their toxicity by forming pores in the larval midgut epithelial membranes. Initially the protoxins are activated in the midgut by trypsin-like proteases to toxins (see figure below). The active toxins bind to specific receptors located on the apical brush border membrane of the columnar cells. Binding is followed by insertion of the toxin into the apical membrane leading to pore formation (see figure below). The formation of toxin-induced pores in the columnar cell apical membrane allows rapid fluxes of ions. Different studies revealed that the pores are K+ selective, permeable to cations, anions or permeable to small solutes like sucrose,
irrespective of the charge. It appears that the toxin forms or activates a relatively large aqueous channel in the membrane. The disruption of gut integrity results in the death of the insect from starvation or septicemia.
 
Applications of Bt
 
 
The first practical application of Bt dates back to 1938 when it was sold as 'Sporeine' in France for the control of European corn borer. The growing realization that organic insecticides are deleterious to the environment and human health spurred a renewed interest in Bt in the 1960s, which led to the introduction of viable Bt biopesticides like Thuricide and Dipel. Bt is the most popular biological control agent with worldwide sales of about $100 million. Bt spray formulations comprise 5% of total global pesticide market. The use of conventional Bt biopesticides, however, was found to have limitations like narrow specificity, short shelf life, low potency, lack of systemic activity, and the presence of viable spores.

An elegant and most effective delivery system for Bt toxins is the transgenic plant. The major benefits of this system are economic, environmental, and qualitative. In addition to the reduced input cost to
 
the farmer, the transgenic plants provide season-long protection independent of weather conditions, effective control of burrowing insects difficult to reach with sprays and control at all of the stages of insect development. The important feature of such a system is that only insects infesting the crop are exposed to the toxin.
 
Introduction and expression of Bt genes in crop plants conferred significant protection against target pests. The first transgenic Bt-crops viz., cotton, corn and potato were commercialized in USA in 1995 and 1996. Currently more than a dozen countries cultivate Bt-crops. Bt-cotton was permitted for commercial cultivation in India in 2002.
 
Biosafety
Safety of Bt toxins in terms of toxicity and allergenicity towards mammals and other non-target organisms is well documented (Glare and O'Callaghan, 2000). The salient features are:
 
Lack of receptors that bind to Bt toxins and instant degradation of Bt toxins in human digestive system make them innocuous to human beings.
Community exposure to Bt toxins/spray formulations over a period of six decades has not resulted in any adverse effects.
Lack of homology to any allergenic protein/epitope sequences makes Bt toxins non-allergenic.
Consumption of foods derived from Bt corn, potato, tomato and rice over the past one decade has not led to any adverse effects in the populations. Consumption of foods derived from Bt corn, potato, tomato and rice over the past one decade has not led to any adverse effects in the populations.
Federation of Animal Societies of USA (2001) observed that Bt crop products (corn) fed to chicken-broilers, chicken-layers, catfish, swine, sheep, lactating dairy cattle and beef cattle did not show any adverse effects on growth, performance, observed health of the animals and composition of meal, milk, eggs, etc.,
Dairy cows fed with corn and Bt-corn did not exhibit any significant differences in lactation and ruminal fermentation
Bt, Bt-sprays, Bt-crops and Bt-crop products are safe to non-target organisms such as soil microorganisms (protozoa and fungi) collembola, molluscs, crustaceans, spiders, aquatic insects, predators, parasitoids, arthropods, honey bees, lady bird beetles, earthworms, salamanders, bird species, small and large mammals, etc.
Benefits of Bt-crops
The International Service for the Acquisition of Agri-biotech Applications (ISAAA) conducted a detailed survey of the Bt-cotton cultivation, adoption and performance in eight countries (USA, Australia, China, India, Mexico, Argentina, South Africa and Indonesia) in 2002 (James, 2002). All the countries that have introduced Bt cotton have derived significant and multiple benefits. These include increases in yield, decreased production costs, a reduction of at least 50% in insecticide applications resulting in substantial environmental and health benefits to small producers, and significant economic and social benefits. In a recent study at Indian Institute of Management (Ahmedabad), Gandhi and Namboodiri (2006) observed that cotton farmers in major cotton-growing states such as Gujarat, Maharashtra, Andhra Pradesh and Tamil Nadu were benefited significantly. On a global basis, the benefits from the deployment of Bt cotton between 1998 and 2001 were estimated to be $1.7 billion. Surveys conducted among small resource-poor farmers in developing countries, mainly in China and South Africa, revealed that Bt cotton contributed to reduction in poverty by increasing incomes of small farmers.
 
The environmental benefits of cultivating pest-resistant transgenic crops are more profound and invisible. These are enumerated below:
Reduction in use of pesticides: The estimated total savings of insecticides on Bt cotton in 2001 was of the order of 10,627 MT, which is equivalent to 13% of the 81,200 MT of all insecticides used on cotton globally in 2001.
Fewer insecticides in aquifers and the environment: The substantial decrease in insecticides associated with the cultivation of Bt cotton has led to significant decrease in insecticide run off into watersheds, aquifers, soils and generally into the environment. More widespread global cultivation of Bt-cotton will further improve the water quality.
Reduced farmer exposure to insecticides and improvement of human health: Substitution of the chemical insecticides with Bt cotton has clearly reduced the risks to farm workers and to others in the farm community who may be exposed to the former’s toxicity. These effects are particularly important in developing countries where modern application techniques are neither always adopted nor available for use.
Increased populations of beneficial insects: The global use of broad spectrum insecticides on cotton has adversely affected and decreased the populations of non-target species including the arthropod natural enemies that can provide effective control of non-lepidopteran pests. Various studies confirmed that the arthropod natural enemy populations in Bt cotton are greater than in non-Bt cotton. In addition to reducing the number of sprays for the bollworm/budworm complex, Bt cotton has also reduced the number of sprays for other insects such as thrips and aphids. This effect has been attributed to higher populations of beneficial predators and parasitic insects that are eliminated by insecticide sprays.
Reduced risk for wildlife: Reduction in the use of insecticides, many of which are highly toxic to wildlife will reduce the risks to mammals, birds, bees, fish and other organisms. Many birds are dependent on insects for food and their elimination through the use of insecticides deprives birds of their food source.
Reduced fuel and raw material consumption and decreased pollution: Lowering the demand for insecticides through the use of Bt cotton reduces tractor fuel usage as a result of reduction in number of sprays, which in turn reduces air pollution. For example, in the Hebei Province of China, where adoption of Bt cotton increased dramatically from its introduction in 1997 to 97% in 2001, farmers have noticed a substantial improvement from the chronic air, soil and water pollution levels prior to the introduction of Bt cotton in 1997, caused by the intensive spraying of cotton with insecticides.
 
The ecological benefits of cultivating Bt-crops were recently documented in a comprehensive manner by Sanvido et al. (2006). According to this study cultivation of Bt corn and Bt cotton resulted in significant environmental benefits. In conclusion, Bt crops are safe and beneficial to farmers, human society, non-target organisms, biodiversity and environment in general.
References
 
Dale, P. J., Clarke, B. and Fontes, E. M. G. 2002. Potential for the environmental impact of transgenic crops. Nature Biotechnology. 20: 567-574.
Gandhi, V. P. and Namboodiri, N. V. 2006. The adoption and economics of Bt-cotton in India. W.P. No. 2006-09-04, IIM, Ahmedabad
Glare, T. R. and O'Callaghan, M. 2000. Bacillus thuringiensis: Biology, Ecology and Safety. John Wiley, Chichester.
James, C. 2002. Global review of commercialized transgenic crops: 2001. Feature: Bt-cotton. ISAAA Brief No. 26, ISAAA, Ithaca.
James, C. 2006. Global status of commercialized Biotech/GM crops. ISAAA Brief No. 35, ISAAA, Ithaca.
Kumar, P. A., Sharma, R. P. and Malik,. V. S. 1996. Insecticidal proteins of Bacillus thuringiensis. Advances in Applied Microbiology. 42:1-43.
Kumar, P. A. 2003. Insect pest-resistant transgenic crops. In: Advances in Microbial Control of Insect Pests, Upadhyay, R. K. Ed. pp. 71-82. Kluwer Academic, New York.
Sanvido O, Stark M, Romeis J and Bigler F, 2006. Ecological benefits of genetically modified crops. Swiss Expert Committee on Biosafety, Federal Department of Economic Affairs, Switzerland.