Insect Resistance to Transgenic Crops
The agricultural sector has been so busy writing about/discussing/bemoaning the development of weed resistance to available herbicides that it is easy to forget that the propensity for other pests [e.g., insects, diseases] to develop resistance to pesticides exists as well. Such is the subject of a review article published by Tabashnik and Carrière titled “Surge in insect resistance to transgenic crops and prospects for sustainability” [Nature Biotechnology 35:926-935 (2017)]. Since this article deals with the responses of insect pests to the insecticidal protein from Bacillus thuringiensis [Bt], I will first give a brief history and description of this transgenic insecticidal trait.
Bacillus thuringiensis or Bt is a soil-dwelling bacterium that is commonly used as a biological pesticide. During sporulation, many Bt strains produce crystal proteins [or Cry proteins] that have insecticidal properties, and this has led to their use as insecticides in genetically modified [GM] crops using Bt genes inserted into plants.
Since 1996, plants have been genetically modified with short sequences of Bt genes to express the crystal protein that Bt makes. Thus, plants themselves can produce the Cry proteins that will protect them against targeted insects. Bt corn crops are protected specifically against European corn borer, southwestern corn borer, corn rootworm, and corn earworm, while Bt cotton crops are protected against the tobacco budworm, cotton bollworm, and pink bollworm. See Tables 1 and 2 in the above-cited article for a complete list of targeted insects and the particular Cry protein that is toxic to those insects.
The Bt crystals are toxic to very specific species of insects when eaten by them. The targeted insect stops eating within hours of ingestion because the crystals cause the insect gut wall to break down, allowing the spores and normal gut bacteria to enter the insect’s body and proliferate, causing insect death.
Bt action is very specific, which means that different strains of Bt are specific to different receptors in the insect gut wall. Thus, Bt toxicity depends on recognizing gut receptors since damage to the insect gut by the toxin occurs only when binding to a recognized receptor; i.e., the specific toxin protein must match the specific gut receptor. A particular strain of Bt will only be toxic to a targeted insect species and will thus not harm untargeted beneficial insect species. Humans and other vertebrates do not have these receptors in their bodies, so the toxin is not harmful to them. The advantages from using GM crops that use the Bt transgenic trait are reduced spraying of synthetic insecticides with associated less harm to beneficial insects, and reduced exposure of workers and non-target organisms to synthetic insecticides.
To help control resistance development in insect species targeted by crops with the Bt trait, fields with a Bt crop are required to have a certain percentage of the field area that is devoted to culture of the non-Bt crop. This “refuge” area acts as a source of insects to mate with possible resistant insects to produce non-resistant insects, and is the most widely used strategy for delaying evolution of pest resistance to Bt crops. The insects that have developed resistance to Bt will thus have a chance to mate with an insect that has not developed this resistance, thus producing progenies that are not resistant to Bt.
Now back to the above-cited review by Tabashnik and Carrière. Major points, findings, and conclusions follow.
• Transgenic crops that produce insecticidal proteins from Bt have revolutionized insect pest control in certain crops. The authors analyzed global monitoring data that are available from the first two decades of use of these transgenic crops to determine the magnitude of resistance evolvement among the targeted insect species.
• The acreage planted with Bt crops increased from ~2.7 million in 1996 to ~243.3 million in 2016.
• The authors analyzed published results from 36 cases that represent responses of 15 pest species to Bt crop use in 10 countries.
• Resistance substantially reduced Bt crop effectiveness in 16 cases of practical resistance* as of 2016 compared with only three such cases in 2005. In those cases, the targeted pests evolved resistance in an average of 5.2 years. This practical resistance has reduced the number of Bt toxins in transgenic crops that are effective against some major insect pests. None of these cases met the high-dose standard**.
• In 17 other cases, targeted pests have not evolved resistance–i.e., no decrease in insect susceptibility to the Bt toxin–after 19 years of exposure in some cases. The average for this group was 10.6 years.
• The remaining 3 cases were categorized as “early warning of resistance”, or a statistically significant decrease in susceptibility of the targeted insect but no reported efficacy reduction of the Bt crop.
• The authors concluded from their analyses of the data that when the high-dose standard is not met, the use of abundant refuges can substantially delay resistance development. They also concluded that refuge requirements must be tailored to each insect pest–transgenic crop combination.
• The authors concluded that the high-dose/refuge strategy for delaying insect resistance to Bt crops is working. This is an important finding as more crops such as soybean are engineered to produce Bt toxins to control damaging insect pests.
• Bt crop pyramids are designed to delay the evolution of resistance by producing two or more distinct toxins that kill the same insect pest. The authors’ evidence suggests that smaller refuges can be used for delaying the evolvement of resistance in these pests that are highly susceptible to each of two or more independently acting toxins or traits in a pyramid.
• Faster evolution of insect resistance to Bt toxins is favored by increased adoption rates of these crops, reduced percentages of refuge acres, and an increase in total area planted to Bt crops.
*Practical resistance of an insect to a Bt crop is field-evolved resistance that reduces the efficacy of the Bt crop and has practical consequences for pest control. The criteria for this designation are 1) >50% of targeted insects in a population are resistant, and 2) the efficacy of the Bt crop is reduced in the field.
**The US EPA indicates that Bt plants meet the high-dose standard if they kill at least 99.9% of susceptible insects. If survival of susceptible insects is > 0.01%, then resistance can be delayed by increasing the refuge percentage. Meeting the high-dose standard and a lower risk of resistance evolution are significantly associated.
As of 2017, insect-resistant Bt soybean varieties have not been commercialized in the US. However, the subject of insects developing resistance to the Bt trait is of interest to soybean producers because of the findings from MSPB Project No. 58-2016 [click here for a final report from this project] which indicate that soybean planted in the Midsouth will benefit economically from the Bt insect management strategy. So if/when a market develops for Bt soybean, knowing of the propensity for resistance development in the Bt-targeted insect and methods to delay or prevent this will be important for prolonging the effectiveness of the particular Bt soybean trait.
I encourage my entomology colleagues to read the above article so that, if and when Bt soybean becomes a reality and is used in the Midsouth, they will be prepared to advise growers about how to use this technology so it will remain effective for decades rather than a few years. With future developments in this area, this technology could be an important component for insect management in Midsouth soybeans.
The content of the above-cited article about insect resistance development plus the much-written-about development of resistance in fungal pathogens to overused fungicides further underscore that any pest control measure used in agriculture must include a concurrent plan for delaying or preventing resistance development in the targeted pest. Ignoring this basic tenet when controlling pests with either transgenic methods or the application of pesticides will surely result in the loss of valuable pest control measures.
Composed by Larry G. Heatherly, Oct. 2017, larryheatherly@bellsouth.net