Cross-pollination in seed-blended refuge and selection for Vip3A resistance in a lepidopteran pest as detected by genomic monitoring

Proc Natl Acad Sci U S A. 2024 Mar 26;121(13):e2319838121. doi: 10.1073/pnas.2319838121. Epub 2024 Mar 21.

Abstract

The evolution of pest resistance to management tools reduces productivity and results in economic losses in agricultural systems. To slow its emergence and spread, monitoring and prevention practices are implemented in resistance management programs. Recent work suggests that genomic approaches can identify signs of emerging resistance to aid in resistance management. Here, we empirically examined the sensitivity of genomic monitoring for resistance management in transgenic Bt crops, a globally important agricultural innovation. Whole genome resequencing of wild North American Helicoverpa zea collected from non-expressing refuge and plants expressing Cry1Ab confirmed that resistance-associated signatures of selection were detectable after a single generation of exposure. Upon demonstrating its sensitivity, we applied genomic monitoring to wild H. zea that survived Vip3A exposure resulting from cross-pollination of refuge plants in seed-blended plots. Refuge seed interplanted with transgenic seed exposed H. zea to sublethal doses of Vip3A protein in corn ears and was associated with allele frequency divergence across the genome. Some of the greatest allele frequency divergence occurred in genomic regions adjacent to a previously described candidate gene for Vip3A resistance. Our work highlights the power of genomic monitoring to sensitively detect heritable changes associated with field exposure to Bt toxins and suggests that seed-blended refuge will likely hasten the evolution of resistance to Vip3A in lepidopteran pests.

Keywords: Bacillus thuringiensis; Helicoverpa zea; genomic monitoring; pesticide resistance; polygenic adaptation.

MeSH terms

  • Animals
  • Bacillus thuringiensis* / genetics
  • Bacterial Proteins / metabolism
  • Endotoxins* / genetics
  • Endotoxins* / metabolism
  • Genomics
  • Hemolysin Proteins / metabolism
  • Insecticide Resistance / genetics
  • Larva / metabolism
  • Pest Control, Biological / methods
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • Pollination
  • Seeds / metabolism
  • Zea mays / genetics

Substances

  • Endotoxins
  • Bacterial Proteins
  • Hemolysin Proteins