Polygenic basis of Bt Cry resistance evolution in wildHelicoverpa zea

Abstract

In agricultural ecosystems, strong and shifting selective pressures from pest management practices can lead to rapid evolution. Crops expressing pesticidal proteins fromBacillus thuringiensis(Bt) are an important control measure for agricultural pests and a major selective force on pest genomes world wide.Helicoverpa zea, a destructive pest of corn and cotton, has evolved widespread resistance to Bt crystalline (Cry) pesticidal proteins. Here we reveal the polygenic architecture of field evolved Cry resistance inH. zeaand identify multiple previously unknown Cry resistance candidate regions and genes. In the genomic region with the largest effect on Cry1Ab, and Cry1A.105 + Cry2Ab2 resistance, we identified signals of an increase in copy number for an entire cluster of trypsin genes. The genes in this cluster, along with other trypsins genome-wide, are significantly upregulated in Cry resistantH. zea. All field resistant individuals possessed two to four copies of a trypsin in this cluster, but this gene amplification was not found in any samples collected prior to Cry resistance evolution or in susceptible lab colonies. Inhibiting trypsin activity inH. zeadecreased tolerance of Cry toxin in resistant and susceptible populations. Together, our findings suggest that increased expression and amplification of trypsins could allow degradation of activated Cry toxin and explain part of the polygenic Cry resistance observed in wildH. zea.