Multi-toxin resistance enables pink bollworm survival on pyramided Bt cotton

Authors: Fabrick, Jeffrey; UNNITHAN, GOPALAN - University Of Arizona; YELICH, ALEX - University Of Arizona; DEGAIN, BEN - University Of Arizona; MASSON, LUKE - National Research Council - Canada; ZHANG, JIE - Chinese Academy Of Agricultural Sciences; CARRIERE, YVES - University Of Arizona; TABASHNIK, BRUCE - University Of Arizona

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2015
Publication Date: 11/12/2015
Publication URL: http://handle.nal.usda.gov/10113/61668
Citation: Fabrick, J.A., Unnithan, G.C., Yelich, A.J., Degain, B., Masson, L., Zhang, J., Carriere, Y., Tabashnik, B.E. 2015. Multi-toxin resistance enables pink bollworm survival on pyramided Bt cotton. Scientific Reports. 5:16554. doi: 10.1038/srep 16554.

Interpretive Summary: Genetically modified or transgenic crops producing Bacillus thuringiensis (Bt) insecticidal proteins are key management tools against several important insect pests, including the pink bollworm (Pectinophora gossypiella). These proteins produced in Bt crops are beneficial as they specifically target insect pests while having little impact on beneficial insects or other plants or animals. However, the development of resistance in pests to Bt crops jeopardizes the usefulness of these important management tools. One strategy to avoid or delay resistance is to "pyramid" two or more Bt toxins in the same plant. In cotton, the most commonly pyramided toxins are Cry1Ac and Cry2Ab. To better understand the underlying mechanisms of resistance to Bt crop pyramids, an ARS scientist at Maricopa, AZ and collaborators used laboratory selection to achieve high levels of resistance to both Cry1Ac and Cry2Ab in pink bollworm. This multi-toxin resistant population represents the first report of pink bollworm that can survive on field-collected Bt cotton bolls producing both toxins. Experiments showed that a different, single resistance gene controls resistance to each toxin. These results demonstrate the risk of resistance development to pyramided Bt crops, particularly when Bt toxins are deployed sequentially (e.g. one at a time) and refuges (areas of non-Bt plants that serve as a source of susceptible insects) are scarce, as seen with pink bollworm resistance to Bt cotton in other parts of the world.

Technical Abstract: Transgenic crops producing Bacillus thuringiensis (Bt) proteins kill key insect pests, providing economic and environmental benefits. However, the evolution of pest resistance threatens the continued success of such Bt crops. To delay or counter resistance, transgenic plant "pyramids" producing two or more Bt proteins that kill the same pest have been adopted extensively. Field populations of the pink bollworm (Pectinophora gossypiella) in the United States have remained susceptible to Bt toxins Cry1Ac and Cry2Ab, but field-evolved practical resistance to Bt cotton producing Cry1Ac has occurred widely in India. Here we used two rounds of laboratory selection to achieve 18,000- to 150,000-fold resistance to Cry2Ab in pink bollworm. Inheritance of resistance to Cry2Ab was recessive, autosomal, conferred primarily by one locus, and independent of Cry1Ac resistance. We created a strain with high resistance to both toxins by crossing the Cry2Ab-resistant strain with a Cry1Ac-resistant strain, followed by one selection with Cry2Ab. This multi-toxin resistant strain survived on field-collected Bt cotton bolls producing both toxins. The results here demonstrate the risk of evolution of resistance to pyramided Bt plants, particularly when toxins are deployed sequentially and refuges are scarce, as seen with Bt cotton and pink bollworm in India.