Resistance to Bacillus thuringiensis linked with a cadherin transmembrane mutation affecting cellular trafficking in pink bollworm from China

Authors: WANG, LING - Chinese Academy Of Agricultural Sciences; MA, YUEMIN - Central China Normal University; WAN, PENG - Hubei Academy Of Agricultural Sciences; LIU, KAIYU - Central China Normal University; XIAO, YUTAO - Chinese Academy Of Agricultural Sciences; WANG, JINTAO - Huazhong Agricultural University; CONG, SHENGBO - Hubei Academy Of Agricultural Sciences; XU, DONG - Hubei Academy Of Agricultural Sciences; WU, KONGMING - Chinese Academy Of Agricultural Sciences; Fabrick, Jeffrey; LI, XIANCHUN - University Of Arizona; TABASHNIK, BRUCE - University Of Arizona

Submitted to: Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/23/2018
Publication Date: 2/2/2018
Publication URL: https://handle.nal.usda.gov/10113/5912403
Citation: Wang, L., Ma, Y., Wan, P., Liu, K., Xiao, Y., Wang, J., Cong, S., Xu, D., Wu, K., Fabrick, J.A., Li, X., Tabashnik, B.E. 2018. Resistance to Bacillus thuringiensis linked with a cadherin transmembrane mutation affecting cellular trafficking in pink bollworm from China. Insect Biochemistry and Molecular Biology. 94:28-35. https://doi.org/10.1016/j.ibmb.2018.01.004.
DOI: https://doi.org/10.1016/j.ibmb.2018.01.004

Interpretive Summary: Insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) are widely used in transgenic crops to control some of the world’s most devastating insect pests, including the pink bollworm (Pectinophora gossypiella), an important global pest of cotton. Whereas Bt cotton remains an essential tool for the management of pink bollworm in the U.S. and China, this technology no longer provides effective control of this pest in some parts of India due to wide-spread resistance. Comparison of resistance mechanisms to Bt cotton in three major lepidopteran pests, including the pink bollworm, reveal an association with mutations that disrupt a cadherin protein that binds one of the primary Bt toxins, Cry1Ac, in the gut of susceptible larvae. To date, all of these mutations cause changes within regions of the cadherin protein located either on the outside or inside of the cell. Here, an ARS scientist at Maricopa, AZ and collaborators report the first evidence of a cadherin mutation affecting the region that spans the cell membrane is associated with insect resistance to a Bt crop. A pink bollworm strain from China harboring this mutant protein had 220-fold resistance to Cry1Ac relative to a susceptible strain and was able to complete its life cycle on Bt plants. These data reveal how mutations in Bt cadherin receptor proteins can lead to resistance that allow important insect pests to adapt to current management practices. Such information is vital for delaying the onset of resistance and for extending the life of essential Bt technologies.

Technical Abstract: Transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) are cultivated extensively worldwide. However, their benefits are being eroded by increasingly rapid evolution of resistance in pests. In some previously analyzed strains of three major lepidopteran pests, resistance to Bt toxin Cry1Ac in transgenic cotton is associated with mutations disrupting the extracellular or cytoplasmic domains of cadherin proteins that bind Cry1Ac in the midgut of susceptible larvae. Here we report the first evidence of a cadherin transmembrane mutation associated with insect resistance to a Bt crop. We discovered this mutation in a resistant strain of the devastating global cotton pest, the pink bollworm (Pectinophora gossypiella), isolated from a field population in the Yangtze River Valley of China. The mutant allele evaluated here has a 207 base pair deletion and encodes a cadherin protein lacking its transmembrane domain. Relative to a susceptible strain, a strain homozygous for this allele had 220-fold resistance to Cry1Ac and 2.1-fold cross-resistance to Cry2Ab. On Bt cotton plants, no susceptible larvae survived, but larvae from the resistant strain completed the full life cycle. Inheritance of resistance to Cry1Ac was autosomal, recessive and tightly linked with the cadherin gene. Transportation of cadherin protein to the cell membrane and susceptibility to Cry1Ac occurred in transfected insect cells expressing the wild type cadherin allele, but not in transfected insect cells expressing the mutant cadherin allele. The results imply that the mutant cadherin allele analyzed here confers resistance of pink bollworm to Bt cotton producing Cry1Ac.