Multiple origins of a single point mutation in the cotton bollworm tetraspanin gene confers dominant resistance to Bt cotton

Authors: GUAN, FANG - Nanjing Agricultural University; HOU, BOFENG - Nanjing Agricultural University; DAI, XIAOGUANG - Nanjing Agricultural University; LIU, SITONG - Nanjing Agricultural University; LIU, JUANJUAN - Nanjing Agricultural University; GU, YAN - Nanjing Agricultural University; YANG, YIHUA - Nanjing Agricultural University; Fabrick, Jeffrey; WU, YIDONG - Nanjing Agricultural University

Submitted to: Pest Management Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/20/2020
Publication Date: 3/1/2021
Citation: Guan, F., Hou, B., Dai, X., Liu, S., Liu, J., Gu, Y., Yang, Y., Fabrick, J.A., Wu, Y. 2021. Multiple origins of a single point mutation in the cotton bollworm tetraspanin gene confers dominant resistance to Bt cotton. Pest Management Science. 77(3):1169-1177. https://doi.org/10.1002/ps.6192.
DOI: https://doi.org/10.1002/ps.6192

Interpretive Summary: Cotton genetically engineered to produce Bacillus thuringiensis (Bt) insecticidal proteins are used to control some of the world’s most important insect pests, including the cotton bollworm (Helicoverpa armigera). The evolution of Bt resistance, in which pests have adapted to survive on Bt crops, is the foremost threat to the continued success of this transgenic technology. The primary strategy to delay resistance to Bt crops relies on the use of non-Bt refuge plants to produce sufficient susceptible insects that mate with rare resistant insects emerging from Bt crops, essentially diluting and/or removing resistance from pest populations. However, a key assumption for the success of this refuge strategy, that the resistance-conferring genes are recessive, is violated by H. armigera in China, where dominant resistance to Cry1Ac Bt cotton is increasing in the field and is associated with a mutation in the tetraspanin HaTSPAN1 gene. Here, an ARS scientist at Maricopa, AZ and collaborators used next generation amplicon DNA sequencing to determine whether the HaTSPAN1 mutation either arose from a single event and spread or that the mutation evolved independently several times throughout northern China. From 28 populations sampled from northern China, four resistant and 50 susceptible DNA sequences indicate that the HaTSPAN1 mutation arose from at least three independent origins and spread to their current distributions. These results not only provide valuable information about the evolutionary origins of dominant resistance to Cry1Ac Bt cotton in northern China, but also offer rationale for the rapid increase in field-evolved resistance in these areas, where the implementation of practical pest management strategies is needed.

Technical Abstract: Transgenic crops producing insecticidal proteins derived from Bacillus thuringiensis are used globally to kill key insect pests and provide numerous benefits, including improved pest management, increased profits, reduced insecticide use, and increased biological control. Unfortunately, such benefits are rapidly being lost by the evolution of Bt resistance by pests. The main strategy to delay resistance relies on the use of non-Bt refuge plants to produce sufficient susceptible insects that mate with rare resistant insects emerging from Bt crops, essentially diluting and/or removing resistance alleles from pest populations. A key assumption for the success of this refuge strategy is that inheritance of resistance is recessive. In China, dominant resistance to Cry1Ac Bt cotton by the cotton bollworm Helicoverpa armigera is increasing and is associated with a mutation in the tetraspanin HaTSPAN1 gene, conferring more than 125-fold resistance. Here, we used amplicon sequencing to test the hypotheses that the HaTSPAN1 mutation either arose from a single event and spread or that the mutation evolved independently several times throughout northern China. From three laboratory strains and 28 field populations sampled from northern China, we identified six resistant and 50 susceptible haplotypes. Phylogenetic analysis indicates that the HaTSPAN1 mutation arose from at least four independent origins and spread to their current distributions. The results provide valuable information about the evolutionary origins of dominant resistance to Cry1Ac Bt cotton in northern China and offer rationale for the rapid increase in field-evolved resistance in these areas, where the implementation of additional practical resistance management is needed.