Transgenic crops have revolutionized insect pest control, but their effectiveness has been reduced by evolution of resistance in pests. We analyzed global monitoring data reported during the first ...two decades of transgenic crops, with each case representing the responses of one pest species in one country to one insecticidal protein from Bacillus thuringiensis (Bt). The cases of pest resistance to Bt crystalline (Cry) proteins produced by transgenic crops increased from 3 in 2005 to 16 in 2016. By contrast, in 17 other cases there was no decrease in pest susceptibility to Bt crops, including the recently introduced transgenic corn that produces a Bt vegetative insecticidal protein (Vip). Recessive inheritance of pest resistance has favored sustained susceptibility, but even when inheritance is not recessive, abundant refuges of non-Bt host plants have substantially delayed resistance. These insights may inform resistance management strategies to increase the durability of current and future transgenic crops.
Evolution of resistance in pests can reduce the effectiveness of insecticidal proteins from Bacillus thuringiensis (Bt) produced by transgenic crops. We analyzed results of 77 studies from five ...continents reporting field monitoring data for resistance to Bt crops, empirical evaluation of factors affecting resistance or both. Although most pest populations remained susceptible, reduced efficacy of Bt crops caused by field-evolved resistance has been reported now for some populations of 5 of 13 major pest species examined, compared with resistant populations of only one pest species in 2005. Field outcomes support theoretical predictions that factors delaying resistance include recessive inheritance of resistance, low initial frequency of resistance alleles, abundant refuges of non-Bt host plants and two-toxin Bt crops deployed separately from one-toxin Bt crops. The results imply that proactive evaluation of the inheritance and initial frequency of resistance are useful for predicting the risk of resistance and improving strategies to sustain the effectiveness of Bt crops.
Fitness costs associated with Cry2Ab resistance alleles could also delay the evolution of resistance in H. armigera and H. punctigera by selecting against these alleles when larvae eat non-Bt ...cotton or any of the other non-Bt host plants of these polyphagous species. Because insect ABC transporters often provide protection against xenobiotics, the resistance-conferring mutations disrupting these proteins may diminish their natural function, yielding higher fitness costs in the presence of toxic substances, such as plant defensive compounds and insecticides other than Bt toxins 12. ...in strains of H. armigera and H. punctigera with ABCA2 mutations, resistance to Cry2Ab is associated with significantly increased susceptibility to the organophospate insecticide chlorpyrifos and the carbamate insecticide methomyl 24.
Evolution of pest resistance reduces the efficacy of insecticidal proteins from the gram-positive bacterium Bacillus thuringiensis (Bt) used widely in sprays and transgenic crops. Better ...understanding of the genetic basis of resistance is needed to more effectively monitor, manage, and counter pest resistance to Bt toxins. Here we used CRISPR/Cas9 gene editing to clarify the genetics of Bt resistance and the associated effects on susceptibility to other microbial insecticides in one of the world's most damaging pests, the cotton bollworm (Helicoverpa armigera). We discovered that CRISPR-mediated knockouts of ATP-binding cassette (ABC) transporter genes HaABCC2 and HaABCC3 together caused >15,000-fold resistance to Bt toxin Cry1Ac, whereas knocking out either HaABCC2 or HaABCC3 alone had little or no effect. Inheritance of resistance was autosomal and recessive. Bioassays of progeny from interstrain crosses revealed that one wild type allele of either HaABCC2 or HaABCC3 is sufficient to sustain substantial susceptibility to Cry1Ac. In contrast with previous results, susceptibility to two insecticides derived from bacteria other than Bt (abamectin and spinetoram), was not affected by knocking out HaABCC2, HaABCC3, or both. The results here provide the first evidence that either HaABCC2 or HaABCC3 protein is sufficient to confer substantial susceptibility to Cry1Ac. The functional redundancy of these two proteins in toxicity of Cry1Ac to H. armigera is expected to reduce the likelihood of field-evolved resistance relative to disruption of a toxic process where mutations affecting a single protein can confer resistance.
Transgenic crop pyramids producing two or more Bacillus thuringiensis (Bt) toxins that kill the same insect pest have been widely used to delay evolution of pest resistance. To assess the potential ...of pyramids to achieve this goal, we analyze data from 38 studies that report effects of ten Bt toxins used in transgenic crops against 15 insect pests. We find that compared with optimal low levels of insect survival, survival on currently used pyramids is often higher for both susceptible insects and insects resistant to one of the toxins in the pyramid. Furthermore, we find that cross-resistance and antagonism between toxins used in pyramids are common, and that these problems are associated with the similarity of the amino acid sequences of domains II and III of the toxins, respectively. This analysis should assist in future pyramid design and the development of sustainable resistance management strategies.
Crops genetically engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt) have advanced pest control, but their benefits have been reduced by evolution of resistance in pests.The ...global monitoring data reviewed here reveal 19 cases of practical resistance to Bt crops, which is field-evolved resistance that reduces Bt crop efficacy and has practical consequences for pest control. Each case represents the responses of one pest species in one country to one Bt toxin. The results with pink bollworm (Pectinophora gossypiella) and Bt cotton differ strikingly among the world's three leading cotton-producing nations. In the southwestern United States, farmers delayed resistance by planting non-Bt cotton refuges from 1996 to 2005, then cooperated in a program that used Bt cotton, mass releases of sterile moths, and other tactics to eradicate this pest from the region. In China, farmers reversed low levels of pink bollworm resistance to Bt cotton by planting second-generation hybrid seeds from crosses between Bt and non-Bt cotton. This approach yields a refuge of 25% non-Bt cotton plants randomly interspersed within fields of Bt cotton. Farmers adopted this tactic voluntarily and unknowingly, not to manage resistance, but apparently because of its perceived short-term agronomic and economic benefits. In India, where non-Bt cotton refuges have been scarce and pink bollworm resistance to pyramided Bt cotton producing Cry1Ac and Cry2Ab toxins is widespread, integrated pest management emphasizing shortening of the cotton season, destruction of crop residues, and other tactics is now essential.
The primary strategy for delaying the evolution of pest resistance to transgenic crops that produce insecticidal proteins from Bacillus thuringiensis (Bt) entails refuges of plants that do not ...produce Bt toxins and thus allow survival of susceptible pests. Recent advances include using refuges together with Bt crop ‘pyramids’ that make two or more Bt toxins effective against the same pest, and planting seed mixtures yielding random distributions of pyramided Bt and non-Bt corn plants within fields. We conclude that conditions often deviate from those favoring the success of pyramids and seed mixtures, particularly against pests with low inherent susceptibility to Bt toxins. For these problematic pests, promising approaches include using larger refuges and integrating Bt crops with other pest management tactics.
Crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) have improved pest management and reduced reliance on insecticide sprays. However, ...evolution of practical resistance by some pests has reduced the efficacy of Bt crops. We analyzed global resistance monitoring data for 24 pest species based on the first 25 yr of cultivation of Bt crops including corn, cotton, soybean, and sugarcane. Each of the 73 cases examined represents the response of one pest species in one country to one Bt toxin produced by one or more Bt crops. The cases of practical resistance rose from 3 in 2005 to 26 in 2020. Practical resistance has been documented in some populations of 11 pest species (nine lepidopterans and two coleopterans), collectively affecting nine widely used crystalline (Cry) Bt toxins in seven countries. Conversely, 30 cases reflect no decrease in susceptibility to Bt crops in populations of 16 pest species in 10 countries. The remaining 17 cases provide early warnings of resistance, which entail genetically based decreases in susceptibility without evidence of reduced field efficacy. The early warnings involve four Cry toxins and the Bt vegetative insecticidal protein Vip3Aa. Factors expected to favor sustained susceptibility include abundant refuges of non-Bt host plants, recessive inheritance of resistance, low resistance allele frequency, fitness costs, incomplete resistance, and redundant killing by multi-toxin Bt crops. Also, sufficiently abundant refuges can overcome some unfavorable conditions for other factors. These insights may help to increase the sustainability of current and future transgenic insecticidal crops.
Transgenic crops producing Bacillus thuringiensis (Bt) toxins kill some key insect pests, but evolution of resistance by pests can reduce their efficacy. The predominant strategy for delaying pest ...resistance to Bt crops requires refuges of non-Bt host plants to promote survival of susceptible pests. To delay pest resistance to transgenic cotton producing Bt toxin Cry1Ac, farmers in the United States and Australia planted refuges of non-Bt cotton, while farmers in China have relied on "natural" refuges of non-Bt host plants other than cotton. Here we report data from a 2010 survey showing field-evolved resistance to Cry1Ac of the major target pest, cotton bollworm (Helicoverpa armigera), in northern China. Laboratory bioassay results show that susceptibility to Cry1Ac was significantly lower in 13 field populations from northern China, where Bt cotton has been planted intensively, than in two populations from sites in northwestern China where exposure to Bt cotton has been limited. Susceptibility to Bt toxin Cry2Ab did not differ between northern and northwestern China, demonstrating that resistance to Cry1Ac did not cause cross-resistance to Cry2Ab, and implying that resistance to Cry1Ac in northern China is a specific adaptation caused by exposure to this toxin in Bt cotton. Despite the resistance detected in laboratory bioassays, control failures of Bt cotton have not been reported in China. This early warning may spur proactive countermeasures, including a switch to transgenic cotton producing two or more toxins distinct from Cry1A toxins.
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