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Managing Insect Pests in Field Corn using Transgenic Bt Technology

Much of the field corn produced in the United States expresses an insecticidal toxin from Bacillus thuringiensis (Bt) that helps the plant control or suppress insect pests without the need for insecticidal sprays. This article provides an overview of Bt corn, the availability and efficacy of different Bt products, and the management of resistance among target insect pests. The intended audience of this article includes farmers, agricultural consultants, and all those involved in pest management.

Introduction

The majority of field corn grown in the United States has been genetically engineered to express insecticidal toxins from the bacterium Bacillus thuringiensis (Bt).1 Known as “Bt corn,” this technology was first commercialized in 1996 and provides control or suppression of a range of insect pests. Foliar insecticides based on Bt toxins have been used for decades in both organic and conventional agriculture. Bt insecticides are effective on a range of Lepidopteran larvae (i.e., immature stages of moths and butterflies) and other types of insects (beetles, mosquitoes), depending on the type of Bt toxin. Bt insecticides are among the safest insecticides for both the user and the environment, as they have a narrow spectrum of activity with limited impact on non-target arthropods and humans.2 In a Bt crop, the plant itself produces the Bt toxins, therefore providing control without having to spray an insecticide. While Bt sweet corn hybrids are also available, this article focuses only on the use of Bt technology in field corn.

Overview

Traditional breeding methods use selective breeding and cross-breeding to develop varieties of plants with improved characteristics (e.g., higher yields, improved quality, resistance to biotic and abiotic stressors). A major issue with this approach is that it takes a long time and is challenging to create specific and precise changes. The development of new molecular techniques led to genetic engineering, where a specific gene or set of genes from any organism can be precisely and rapidly inserted into the DNA of a plant. The successful insertion of DNA in genetic engineering (i.e., an “event”) can include genes coding for Bt toxins, which are then expressed in plant tissues, in addition to other genetic material necessary for the expression of the Bt toxins themselves.

The bacterium species Bacillus thuringiensis is commonly found living in soils and produces crystal proteins during sporulation that have insecticidal activity.2 These crystal proteins, also called Bt toxins, are used as insecticides, with different types of Bt toxins having activity on different groups of insects. The insect first ingests Bt toxins in the form of protoxins. The protoxins are then converted to activated toxins by enzymes in the midgut of the insect.3 These toxins then bind to receptors in the midgut, causing the insect to stop feeding, the midgut walls to break down, and the insect to die. The specificity of the different types of Bt toxins is based on the Bt toxin’s capacity to bind with the receptors in the midgut. Because humans do not have these receptors, Bt toxins are safe as used in Bt foliar insecticides and Bt crops.2

Approval of transgenic crops (also referred to as GMOs [genetically modified organisms]) that contain Bt and other traits involves the Environmental Protection Agency (EPA), the US Department of Agriculture (USDA), and the Food and Drug Administration (FDA), to ensure transgenic crops are safe for humans, plants and animals.

Types of Bt Corn

Bt Corn for Above-Ground Pests

The first generation of Bt corn traits was developed for above-ground insect pests. The European corn borer (Ostrinia nubilalis) was the main target, with yield losses and control costs exceeding $1 billion per year. The first Bt corn traits were commercialized in 1996 (YieldGard Corn borer and Agrisure CB/LL),4 which both expressed the Bt toxin Cry1Ab. A second Bt trait expressing Cry1F (Herculex I) was commercialized in 2002, also with European corn borer as the primary target. These three traits also have activity on other insects: corn earworm (Helicoverpa zea), southwestern corn borer (Diatraea grandiosella), southern cornstalk borer (Diatraea crambidoides), fall armyworm (Spodoptera frugiperda), lesser cornstalk borer (Elasmopalpus lignosellus), and sugarcane borer (Diatraea saccharalis). Corn expressing Cry1F also has activity on the black cutworm (Agrotis ipsilon). Single-toxin Bt corn is no longer commercially available in the U.S., as all Bt corn hybrids for above-ground pests express two or more toxins.

The first Bt trait with two toxins expressed Cry1A.105 + Cry2Ab2 in a single event and was commercialized in 2009 as YieldGard VT Double Pro. The expression of two toxins provides improved control of some insects, in addition to a reduction in the size of the non-Bt refuge (see resistance management section below). The term “pyramided” Bt corn hybrid refers to corn hybrids with two or more Bt corn traits for the same type of pest (i.e., above- or below-ground). Among pyramided Bt corn products, another two-toxin product was commercialized in 2011 (Pioneer Optimum Intrasect), expressing Cry1Ab + Cry1F. Following the approval in 2010 of the trait expressing the Vip3A toxin, corn products with three toxins were then commercialized as Dow PowerCore (Cry1A.105 + Cry2Ab2 + Cry1F), Agrisure Viptera and Optimum Leptra (both Cry1Ab + Cry1F + Vip3Aa20), and Trecepta (Cry1A.105 + Cry2Ab2 + Vip3Aa20). The Vip3A toxin also has activity on fall armyworm and the western bean cutworm (Striacosta albicosta), which is a pest of corn in the northern and western United States, but not in the southeastern United States.5

Bt Corn for Below-Ground Pests

Bt traits are also available for the western corn rootworm (Diabrotica virgifera virgifera) and the northern corn rootworm (Diabrotica barberi). Corn rootworms are major pests of corn in many parts of the U.S. Several Bt traits are available to manage corn rootworms. While the northern corn rootworm does not occur in South Carolina, the western corn rootworm can be a pest of corn in the state, but only in rare cases when corn is planted year after year with no rotation. Bt traits for rootworms are therefore not recommended in South Carolina. Available traits include both single and multiple toxin products. The first Bt rootworm product was commercialized in 2003 as YieldGard rootworm, which expressed Cry3Bb1. Subsequent products include Herculex RW (Cry34Ab1 + Cry35Ab1) in 2004, Agrisure RW (mCry3A) in 2007, and Agrisure Duracade (eCry3.1Ab) in 2012.

Bt Corn for Above- and Below-Ground Pests

A number of Bt products combine traits for both above and below-ground pests. “Stacked” Bt corn hybrids refer to corn hybrids with a trait for above-ground pests and a trait for below-ground pests. Most Bt products available in the southeastern United States are currently pyramided Bt corn hybrids, with stacked Bt corn hybrids dominating in midwestern states where both rootworms and corn borers are more frequent pests.

Efficacy and Benefits of Using Bt Corn in South Carolina

Because corn rootworms are not economic pests in South Carolina, the remainder of this article is focused on Bt traits for above-ground pests. The decision to plant a Bt corn hybrid is made long before knowing what type of pest and pest pressure will be present in a field. As such, any benefit of Bt corn relative to non-Bt corn will only be apparent in the presence of sufficient numbers of an economic pest. While European corn borer was once a more frequent pest in the United States, including in South Carolina,6 it is no longer an economic pest due to a decline in populations From widespread planting of Bt corn across the United States.7 Corn earworm populations have also declined in some parts of the United States due to Bt corn, though the insect remains a major pest on a number of crops.7 Pests in South Carolina targeted by above-ground Bt corn include corn earworm, fall armyworm, lesser cornstalk borer, and cutworms. While insecticide use during the season is generally limited in field corn, planting Bt corn can help reduce the use of insecticides, which has benefits for the environment, including conserving natural enemies.

Corn Earworm

Corn earworm (figure 1a) can feed on corn leaves; however, this category of feeding is infrequent and does not lead to yield reductions.8 Feeding on the corn ear is more common (figure 1b) but can be limited to the tip of the ear only where kernels do not fully develop. Kernel feeding generally remains limited, and corn earworm is typically not deemed an economic pest when corn is planted at the proper time.9 In addition to direct feeding, corn earworm injury may provide entry for fungal pathogens leading to an increase in levels of mycotoxins (fumonisins and aflatoxins), which pose a threat to human and animal health.10,11 Some studies have suggested that Bt corn may help prevent mycotoxin contamination, though the effect of Bt corn is not consistent.12,13 Most Bt corn traits provide inconsistent levels of control of corn earworm due to widespread resistance to Bt toxins in corn earworm populations. Only traits expressing Vip3A currently provide excellent levels of control (see table 1, Relative efficacy of various Bt corn products.)14

A corn earworm adult on the left and a larva on the right.

Figure 1. Corn earworm adult (a) with larva and damage to corn (b). Image credits: Joe Culin, Clemson University, Bugwood.org, and Eric Burkness, Bugwood.org.

Fall Armyworm

Fall armyworm (figure 2a) can be a more serious economic pest, with the insect causing leaf, stalk, and ear damage. However, feeding on vegetative stage corn is more common, particularly in young whorl leaves.15,16 Corn can compensate for some whorl damage, as long as the apical meristem (i.e., the main growing point of the plant) is not damaged, as this can lead to stunted plants and plant death.15 Ear feeding is less frequent than whorl feeding and is similar to corn earworm feeding (figure 2b). Whorl feeding can impact yield, especially when feeding occurs at earlier vegetative stages. Bt corn hybrids can have increased yields relative to non-Bt corn hybrids by gained protection from fall armyworm feeding.17 Single-toxin Bt corn traits provide more inconsistent levels of control; all pyramided Bt corn hybrids provide very good to excellent levels of control (see table 1, Relative efficacy of various Bt corn products.)17

A moth on a leafDescription automatically generated with medium confidence

Figure 2. Fall armyworm adult (a) and larvae on corn ear (b). Image credits: Lyle Buss, University of Florida, Bugwood.org; University of Georgia, Bugwood.org.

Lesser Cornstalk Borer and Cutworms

Both lesser cornstalk borer18 and cutworms19 can reduce corn yields, but they are less common pests of corn. Bt corn hybrids provide good to very good levels of control for lesser cornstalk borer (figure 3), which injures corn plants by feeding on the stem just below the soil surface. Single-toxin Bt corn traits provide more inconsistent levels of control compared with pyramided Bt corn hybrids (see table 1, Relative efficacy of various Bt corn products.) Several species of cutworms can feed on corn, though the black cutworm is the most common species (figure 4a). Cutworm larvae feed on corn leaves and stems, which often leads to the plant being entirely cut off (figure 4b). While all Bt traits expressing only Cry1A toxins provide poor levels of control, Bt traits expressing Cry1F and all other pyramided Bt corn hybrids provide good to very good levels of control.

A picture containing insectDescription automatically generated

Figure 3. Lesser cornstalk borer adult (female) (a), and borer larva (b). Image credits: Mark Dreiling, Bugwood.org; Richard Sprenkel, University of Florida, Bugwood.org.

A picture containing insectDescription automatically generated

Figure 4. Black cutworm adult (a) and larva near a damaged corn plant (b). Image credits: John Capinera, University of Florida, Bugwood.org; Clemson University – USDA Cooperative Extension Slide Series, Bugwood.org.

Resistance to Bt Toxins

Resistance development to Bt toxins is a major threat to the sustainability of Bt crops. Bt corn has generally been a resounding success for managing the European corn borer, with a single case of resistance to Cry1F reported in 2019 in Nova Scotia, 23 years after the initial commercialization of Bt corn.20 A major reason for this success is that Bt corn is considered ‘high dose’ for this insect, which is not the case for many other insects targeted by Bt corn.21 A high dose is defined as a dose of a Bt insecticide that kills >95% of insects that are heterozygous (i.e., individuals with two different alleles for a given gene) for single-allele Bt resistance.21 Among insects reported as resistant in the United States, resistance to some Bt toxins has been reported in populations of corn earworm, fall armyworm, western corn rootworm, and the western bean cutworm. Other insects that have developed resistance to some Bt toxins in corn (not covered here) include the sugarcane borer in Argentina and the stalk borer (Busseola fusca) in South Africa.22

In the southeastern United States, resistance to several Cry toxins has been documented in corn earworm populations,23 with only the Vip3A toxin currently providing excellent levels of control.16 However, a recent study in Texas found evidence of resistance evolving to Vip3A in corn earworm populations.24 While corn earworm does not cause significant yield losses in field corn in most cases, the same or similar Bt toxins are used in Bt cotton where the same insect (known as bollworm) is a major pest. The insect can therefore feed on two Bt crops during a growing season, which favors the development of resistance. Because of the selection for resistance primarily occurring in Bt corn, increased bollworm injury has been observed in Bt cotton, in addition to more frequent applications of insecticide for this pest.25 Because the Vip3A protein is the only effective Bt toxin and is included in both Bt corn and cotton, resistance to Bt toxins is a major concern with this insect.

Fall armyworm populations resistant to Cry1F have been found in Puerto Rico,26 Brazil,27 as well as the southeastern United States.28 The insect does not overwinter in most of the United States, with annual migration occurring from overwintering areas in south Florida, Texas, Mexico, and the Caribbean. Resistance to Cry1F among migrating populations will be highly variable.28 Because single-toxin Cry1F hybrids are no longer available commercially and other Bt toxins remain effective for fall armyworm, management of the insect using Bt traits remains an effective control tactic.17

Western corn rootworm resistance to Bt has been documented in parts of the Mid-West since it was first found in 2009.29 Resistance has been reported to Cry3Bb1, mCry3A, and eCry3.1Ab, with recent data also suggesting that resistance to Cry34Ab1/Cry35Ab1 is emerging in Mid-Western landscapes.29 Resistance to all available Bt traits in some populations of western corn rootworm represents a significant challenge for sustainable and effective management with Bt traits.

Bt corn hybrids expressing Cry1F initially reduced damage by the western bean cutworm. However, the efficacy of Cry1F declined over time, with resistance now widespread.30 With other Cry toxins having no activity with the insect, Vip3A is the only toxin that provides control for the species.

How to Manage Resistance

Growers are required to plant a non-Bt corn refuge to delay the development of Bt resistance as part of an insecticide resistance management (IRM) strategy.31 This non-Bt structured refuge should be planted within half a mile of a Bt cornfield with a goal of producing Bt susceptible individuals, which will then mate with any potential resistant individuals from the Bt field to dilute potential resistance within populations of the target pest. The size of the non-Bt refuge varies based on two factors: (1) if the region where the corn is planted is a cotton-growing region or not, and (2) the number of toxins expressed in Bt corn.32 In regions that grow cotton (which is the case in all of South Carolina), refuge requirements are 50% for single toxin Bt corn and 20% for multiple toxin Bt corn of total corn acres on a farm. Because pyramided Bt corn produces several toxins that target the same pest, the odds of resistance developing against both toxins are lower than for a single toxin, which is why the refuge can be smaller for pyramided Bt corn. The use of pyramided Bt corn hybrids can therefore help to delay resistance evolution, provided that resistance has not yet developed to any of the Bt toxins expressed in the pyramid.

In non-cotton growing regions, refuge requirements are 20% for single toxin Bt corn and 5% for multiple toxin Bt corn. The reasons for the smaller refuge in corn-only counties are that Bt corn is highly effective for European corn borer and that ear-feeding pests (such as corn earworm) are less abundant. Selection pressure in Bt corn on corn earworm does not have the same implications as in southern regions where cotton is grown. In addition, in northern locations where cotton is not grown, the non-Bt refuge can be blended with the Bt seed, and this type of refuge is often called “refuge-in-a-bag.” Advantages include ease of use by growers and complete compliance by growers to meet IRM requirements. Because corn is mainly wind-pollinated, pollen from a Bt plant can pollinate a refuge plant which occurs more frequently in a blended refuge than when using a separate structured refuge. Wind pollination can lead to expression of Bt toxins even in non-Bt refuge ears.33 Such a situation can lead to ear-feeding pests such as corn earworm being exposed to lower doses of Bt toxins, which can hasten the development of resistance. Because of this, blended refuges are not allowed as IRM practices in southern cotton-growing areas of the United States. If a grower decides to plant a bag of corn seed with a blended refuge, a structured non-Bt corn refuge is still required.

Resistance to Bt toxins is evolving faster than ever today among target insect pests, mainly because of cross-resistance among toxins currently used in pyramided Bt corn.22 Compliance with Bt refuge requirements remains one of the main tools growers can use to delay resistance and preserve the technology.

Summary

The widespread adoption of Bt corn by growers in the United States has led to reductions in crop injury from insect pests, reductions in insecticide usage (which benefits natural enemy populations), and suppression of populations of European corn borer and corn earworm. Yield increases resulting from reduced damage can occur in the presence of sufficient numbers of a given pest. This most significant threat to the sustainability of Bt corn is the development of resistance. In South Carolina and other cotton-growing areas, it is crucial to manage Bt resistance through structured planting of a non-Bt corn refuge which can delay the development of resistance and preserve the effectiveness of Bt traits.

References Cited

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