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Sequential evolution of resistance by western corn rootworm to multiple Bacillus thuringiensis traits in transgenic maize
Friday, 2025/03/21 | 08:24:13

Aaron J. GassmannBen D. BrenizerAbigail L. KropfJohn B. McCullochDevin L. RadosevichRam B. ShresthaEliott M. Smith, and Coy R. St. Clair

PNAS; March 10, 2025; 122 (11) e2422337122; https://doi.org/10.1073/pnas.2422337122

Significance

The sequential evolution of resistance to multiple Bacillus thuringiensis (Bt) traits in transgenic maize by western corn rootworm, a serious insect pest of maize in the United States, has caused substantial feeding injury in the field. Bt crops play an important role in managing key insect pests worldwide and reduce the environmental impact of agriculture. However, the evolution of pest resistance is the greatest threat to the continued use of Bt crops. To delay the sequential evolution of resistance, strategies to manage resistance should recognize the heightened risk of resistance to a transgenic pyramid when one trait is already compromised by resistance, avoiding this scenario when possible, and mitigating the risk of resistance by planting larger refuges and diversifying management.

Abstract

Transgenic crops that produce insecticidal toxins derived from the bacterium Bacillus thuringiensis (Bt) are grown worldwide to manage insect pests. Western corn rootworm is a serious pest of maize in the United States and is managed with Bt maize. In the United States, the commercial cultivation of a Bt crop requires an accompanying resistance-management strategy to delay the evolution of Bt resistance. One of the primary resistance-management strategies consists of non-Bt refuges along with a Bt crop that produces two Bt toxins (i.e., a pyramid) that kill the same pest species. This approach delays resistance because individuals with resistance to one toxin are killed by the second. However, if a pest species is resistant to one toxin in a pyramid, the effectiveness of a pyramid to delay resistance is compromised, potentially leading to the evolution of resistance to both toxins. Here, we apply a meta-analysis to demonstrate the sequential evolution of resistance by western corn rootworm to Bt maize producing Cry3Bb1 followed by resistance to Gpp34/Tpp35Ab1 maize, with resistance to each Bt toxin increasing in a linear manner over time. Additionally, we show that Bt-resistant western corn rootworm imposed substantial feeding injury, in the field, to maize containing a pyramid of Gpp34/Tpp35Ab1 and Cry3Bb1. To minimize the risk of sequential evolution of resistance to multiple transgenic traits, an emphasis should be placed on developing transgenic pyramids not compromised by prior resistance, and in cases where resistance is already present, larger non-Bt refuges and more diversified pest-management approaches should be applied.

 

See https://www.pnas.org/doi/10.1073/pnas.2422337122

 

Figure 4

Meta-analysis of corrected survival over time of western corn rootworm populations in plant-based bioassays. Corrected survival is calculated as survival on Bt maize divided by survival on non-Bt maize, with 0 indicating no survival on Bt maize and 1 indicating equal survival on Bt and non-Bt maize (1420). Western corn rootworm populations were sampled from fields with (A) high levels of feeding injury to Cry3 maize (i.e., Cry3Bb1 maize or mCry3A maize) between 2009 and 2012 and (B) high levels of feeding injury to Bt maize that produced Gpp34/Tpp35Ab1, either alone or in a pyramid with Cry3, between 2013 and 2020. Data points are sample means and error bars are the SEM. In panel A, the red line represents the regression equation for corrected survival on Cry3Bb1 maize over time [regression analysis: F = 6.11; df = 1,21; P = 0.02; slope (change in corrected survival per year) ± SE = 0.14 + 0.06], while the blue and black lines show average corrected survival, across years, for field populations on Gpp34/Tpp35Ab1 maize and Bt-susceptible control populations on Bt maize (both Cry3Bb1 maize and Gpp34/Tpp35Ab1 maize), respectively. For panel B, the blue line represents the regression equation for corrected survival on Gpp34/Tpp35Ab1 maize over time [regression analysis: F = 20.67; df = 1,15; P = 0.0004; slope (change in corrected survival per year) ± SE = 0.09 ± 0.02], while the red and black lines show average corrected survival, across years, for field populations on Cry3Bb1 maize and Bt-susceptible control populations on Bt maize (both Cry3Bb1 maize and Gpp34/Tpp35Ab1 maize), respectively. Although regression lines are displayed with population means, regression analyses were conducted with raw data.

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