World population is projected to increase well into the next century reaching 9.3 billion by 2050 and with limited arable land available; meeting the growing population's needs is a hard task which requires accelerated progress for cost effective, sustainable yield increases. Arthropod pests are responsible for major damage to the world's important agricultural crops reducing yield and acting as vectors of diseases. Insect attack resistant transgenic crops offer and alternative strategy of pest control compared to a comprehensive reliance upon chemical pesticides. A wide range of transgenic crops which express proteins with insecticidal properties from Bacillus thuringiensis have been commercialised starting from the mid 1990's and have assisted in increasing yields through their ability to kill phytophagous insects, protecting crops and increasing yields. Recently cases of resistance in insect pests to certain strains of B.thuringiensis toxins expressed in transgenic plants have occurred. Resulting in the need to identify novel resistance genes which can be compiled in plants to delay advances in insect resistance to the insecticidal products and widen the domain of pests affected, overall improving the global state of transgenic crops.
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The projected increase of the world's 7 billion population rises well into the next century, reaching 9.3 billion by 2050 and a further 10.1 billion by 2100 (UN Population Division 2011). This increase will be primarily visible in developing regions of the world, with Asia staying the most inhabited major world area during the 21st century whereas Africa's population will more than triple with it increasing through 1 billion in 2011 to 3.6 billion in 2100 (Fig. 1). With this population increase comes a greater drive and demand for food and the need for significant increase in food production and productivity to be able to achieve food security.
Feeding a world population in 2050 of 9.1 billion people has been projected to require food production increases or around 70% between 2005/07 and 2050. Also developing countries production would be required to almost double (Fig. 2). Adequately feeding the world population would also mean production of foods that are lacking to ensure nutrition security (Bruinsma 2009).
Figure 1. Projected changes in relative population growth, from 1950-2095.
Source: United Nations, Department of Economic and Social Affairs, Population Division (2011). World Population 2010, (Wall Chart).
Figure 2. Targets of cereal production (left). Between 1961 and 2007 cereal production on a global scale has risen from 877 million tonnes to 2351 million tonnes. Rises in production will need to occur to figures of over 4000 million tonnes by 2050 if these forecasted demands are to be reached. Yield increase rate must increase by 37% to meet these demands.
Source: [Based on FAO data] - FAO world agriculture: toward 2030/2050. Interim report, global perspective studies unit (FAO Rome, 2006).
The question is how to tackle this much needed increase. The majority of necessary production increases will arise from large cropping intensity increases and major yield advances with developing countries having to increase these 80 percent in comparison to the production increases from expansion of arable land at around 20 percent in developing countries (Anon 2009).
Closing the Yield Gap - The use of Biotechnology
Major Constraints on productivity arrive from factors such as plant disease, nutrient and land availability, and damage from pests. With the best locally obtained yields depending on the extent of farmers to use and access, things such as water for irrigation, the right seeds and nutrients, and pest management measures. This review will focus specifically on strategies' incorporating transgenic plants to protect crops from insect pest damage.
Of the minimal amount of arthropods which are classified as pests, many of these induce harmfull implications on crops with destruction of world crop production being 14% causeing around "$100 billion of damage each year" (Nicholson 2007). One current measure in place to reduce losses in crop yield due to insect pests is the use of synthetic insecticides which without use, would cause drastic losses in global crop yeild. Insecticides have and are a incredibly effective method for control of crop pests rapidly when crop safety is at risk. However the major limiting factor on the use of insecticides to tackle crop pests is the increasing resistance of insects to insecticides with reports of resistance being reported in more than 500 species (Nicholson 2007). There are also environmental and health concerns around insecticides with improper and unreasonable use of pesticides leading to outbreaks of pests due to the unintentional destruction of the pests natural enemies (Pimentel 2009). Thus other strategies are being investigated to address the global crop pest problem with one of these being the use of recombinant DNA technology.
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Recombinant DNA technology is used to produce transgenic crops which have increased stress tolerance, biotic or abiotic. These transgenic crops contribute a significant input into achieving greater food security whether by increasing resistance to disease, insect pests or even by increasing nutrient levels of the plant to enhance the probability of people meeting their dietary needs for a healthy life. Plants containing transgenes are often called transgenic or genetically engineered (GE) crops, however the reality is that all modern crops have been bred and engineered from their wild state by domestication, selection for preferred traits and controlled breeding through time. Currently the major commercialized transgenic crops have undergone simple manipulations to insert genes to benefit the plant for example genes for herbicide tolerance or pest-insect toxin. In the near future developments in combining desirable traits and new novel traits such as resistance to drought in plants will be brought about. However there are issues of public acceptance of biotechnology with differences in acceptance of genetically engineered plants paired to food production in Europe. Currently applications of biotechnology including those of genetic engineering is encouraged but there are some suspicions that application of biotechnological methods towards production of food could jeopardize modern agriculture and the health and safety of our food. However modern molecular biological methods present enormous prospects for expanding production and reducing risks in production of food. Therefore there is a demand for increased acceptance by the public in biotechnology before it can openly assist in improving global food security. This review focuses on insect resistant transgenic crops.
Figure 3. Global Map of Biotech Crop Countries and Mega-Countries in 2011. Source: James, Clive. 2011. Global Status of Commercialized Biotech/GM Crops: 2011. ISAAA Brief No.43. ISAAA: Ithaca, NY.
Insect resistant biotech crops
2011 was the 16th year of commercialisation of biotech crops with a 15 consecutive years of increase and an increase of 12 million ha at a growth rate of 8% from 2010-2011 reaching a record of 160 million ha. Biotech crops have been the fastest adopted crop technology in the history of modern agriculture to date with a 94 times rise in hectarage from 1.7 million in 1996 to 160 million in 2011 (James 2011). Out of all 29 biotech crop planting countries in 2011, 10 were industrial and 19 developing (Fig. 3) with developing countries growing near 50% of the global biotech crops. Adoption of biotech crops by trait sees herbicide resistance having the largest sector with 59% of the global crops compared to 15% of insect resistant trait crops. However it is the stacked gene approach which is the fastest growing area trait wise with 26% of global biotech crop coverage (James 2011). Of insect resistant biotech crops commercialised those expressing Bacillus thuringiensis (Bt) Î´- endotoxins remain the leading and most successful insecticidal toxins
engineered into plants. Positive yield impacts for the use of biotech IR traits in the corn and cotton sectors have occurred in all countries using them (except genetically modified IR cotton in Australia) (Brookes and Barfoot 2012). The impact that these traits had on yield on average across the area planted from 1996-2010 is +9.96% for corn traits and +14.4% for cotton traits (Brookes and Barfoot 2012) (Fig 4).
Figure 4. Yield impacts on average for the effect of biotech IR traits between 1996-2010 by country and trait. IRCB= resistant to corn boring pests, IRCRW= resistant to corn rootworm. Source: Brookes, G. and P. Barfoot (2012). "The income and production effects of biotech crops globally 1996-2010." GM Crops and Food: Biotechnology in Agriculture and the Food Chain 3(4): 265-272.
The Bt Odyssey
Bacillus thuringiensis is a ubiquitous soil bacterium. The protein crystals it secretes are called Bt-toxins, Î´- endotoxins or crystal (cry) proteins which are insecticidal in nature and are produced within its cells during sporulation. Most strains of the bacterium produce several cry-proteins, each of which shows a rather specific host range (Bravo et al. 2007). An example of this comes from the Cry1A, Cry1Ab and Cry1C genes which code for proteins of the same name which have a specific insecticidal spectrum to larval forms of lepidopteran insect pests for example the codling moth (Cydia pomonella), European corn borer (Ostrinia nubilalis)(Cry1A) or African stem borer (Busseola fusca)(Cry1Ab). Differently the CryA3 protein has an insecticidal spectrum to coleopteran pests an example of which is the Colorado potato beetle (Leptinotarsa decemlineata) (George et al. 2012; Bravo et al. 2007). Plants that expressed Bacillus thuringiensis insecticidal proteins were initially commercialized in the 1996 growing season (Bates 2005), and since then a large variety of crop plants have been genetically engineered so that they exhibit the Î´- endotoxin gene. Engineering of these plants has been undergone to exhibit the active toxin in the plants tissues to the result that insects which feed on the crops are killed by the toxin.
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There are two proposed models for the mechanism of action of cry proteins. The first being the pore formation model described in detail by Bravo et al (2007) whereby the cry proteins lead to the forming of lytic pores in apical membranes subsequently instigating cell lysis and causing insect death. The second is a more recently proposed alternative model which is called the signal transduction model. In this model cell death of the insect comes about without the formation of pores. The model proposes that "the toxicity of Cry proteins is due to activation of Mg+2-dependant signal cascade pathway which is triggered by interaction of monomeric 3d-Cry toxin with the cadherin protein receptor. This activates a guanine nucleotide-binding protein which in turn activates an adenylyl cyclase promoting the production of intracellular camp. Increase in camp levels causes protein kinase A activation which in turn activates an intracellular pathway resulting in cell death" (Soberón et al. 2009).
Transgenic crops with individual cry proteins expressed were the first of many commercial varieties available which had precise activity against insect pests of Lepidopterans pests, such as 'MON 810', a maize crop plant that has been modified developed by Monsanto Company with the trade name YieldGard. This MON810 variety of crop contains a Cry1Ac gene which when expressed is toxic to Lepidopteran insects such as the European Corn Borer.
More recent releases of Bt transgenic crops express cry protein encoding and vegetative insecticidal proteins (VIP) active against Coleoptera and Lepidoptera insects, and also sometimes HT genes via gene stacking. A recent commercialised example of this comes from Sygenta and their 'AgrisureÂ® Viptera 3111' trait stack product which includes triple stacked HT traits, protects against 14- above and below ground insects with combination of Both vegetative insecticidal proteins (Vip3A) and cry proteins derived from B.thuringiensis (Sygenta, 2011). By expressing both VIP and Cry proteins, due to the difference in mechanism of action between the two, the durability of the cultivar is effectively extended by decreasing the likelihood of the insects becoming resistant. Xu et al (1996) established that cowpea trypsin inhibitor (CpTI) expression in rice plants improves resistance of the plant to two rice stem borer species. The study showed significant increases in resistance to the striped stem borer (Chilo suppressalis), and pink stem borer (Sesamia inferens) infestation. In 2000 a trait stacked cotton crop expressing Cry1Ac with CpTI was released in China was employed to improve protection representing the sole commercial development of proteinase inhibitors to date (Gatehouse 2011). This is another example of co-expression to reduce likelihood of resistance in insects to the cultivar.
Evolution of the Resistance
The continued progression in resistance to transgenic crops in insects jeopardises the prolonged success of B.thuringiensis toxin producing crops (Tabashnik 2008). The first documented occurance of field evolved resistance to a B.t toxin provoked by a transgenic crop is of Helicoverpa zea to Cry1Ac in transgenic cotton with significantly increased occurance of resistant alleles being found in field populations of H. zea (Tabashnik 2008)(Fig 5). Further examples of resistance to B.thuringiensis toxins produced by a transgenic crop come from western corn rootworm (Diabrotica virgifera virgifera) resistance to Cry3Bb1 maize (Gassman 2011). Furthermore field-evolved resistance in a major target pest, the cottong bollworm (Helicoverpa armigera) to Cry1Ac has been reported in northern China (Zhang, 2011). Despite laboratory bioassays having detected this resistance, resistance of these insects to Cry1Ac and Cry3Bb1 expressing cultivars hasn't caused any broad pest control failures. These negative effects shown of Cry protein resistance should instigate reductions in the use of crops which produce only single toxins and progress towards crops which incorporate two or more B.thuringiensis toxins and other proteins and proteinase inhibitors such as VIP and CpTI.
Figure 5. Resistance in the field from the collective Bt crops planted worldwide from 1996-2007 (>200 million ha). Detected in lepidopteron species : Helicoverpa zea (bollworm), to Bt cotton producing Cry1Ac), Spodoptera frugiperda (fall armyworm) to Bt corn producing Cry1F, and Busseola fusca (stem borer) to Bt corn producing Cry1Ab. Tabashnik, B. E., et al. (2008). "Insect resistance to Bt crops: evidence versus theory." Nat Biotechnol 26(2): 199-202.
Currently the approaches to tackle resistance include the use of management strategies such as the refuge strategy (involves growth of non-Bt crops near the planted Bt crops). This has been shown to delay insect resistance evolution through heightening of the chance that resistant insects will mate with non-resistant partners, producing non-resistant offspring. Gene stacking of different B.t toxins or proteinase inhibitors is a strategy that confers elevated levels of pest control (Ferry et al. 2004). These proactive countermeasures combined have so far been successful in preventing widespread insect resistance to many insecticidal crops. However from evidence of the evolution of insect resistance to single B.thuringiensis toxin expressing crops in the field it has seemed that the refuge strategy alone, although postpones resistance for many years, is not enough keep evolution of resistance at bay.
By monitoring resistance of insects collected from biotech crop fields and DNA screening and incorporating gene stacking and refuge strategies, it should be possible to stay ahead of the curve within relation to insect resistance. However the investigation and search for genes conferring resistance to pests needs to be maintained to identify different genes which can be incorporated into plants to provide increases in the variety of plant pests that are effected and to postpone and prevent further insect resistance these gene products which confer resistane (Peferoen 1997; Ferry et al. 2004).
Future Strategies And Prospects
Potential of insect evolved resistance to transgenic crops is present and although methods to reduce this currently being implimented, alternative strategies to deal with insect pests are being developed.