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Mismatch between lab-generated and field-evolved resistance to transgenic Bt crops in Helicoverpa zea
Friday, 2024/11/22 | 08:17:06
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Andrew W. Legan, Carson W. Allan, Zoe N. Jensen, Benjamin A. Degain, Fei Yang, David L. Kerns, Kyle M. Benowitz, Jeffrey A. Fabrick, Xianchun Li, Yves Carrière, Luciano M. Matzkin, and Bruce E. Tabashnik PNAS; November 6, 2024; 121 (47) e2416091121; https://doi.org/10.1073/pnas.2416091121 SignificanceCrops genetically engineered to produce insect-killing proteins from the bacterium Bacillus thuringiensis (Bt) control some major pests and reduce use of insecticide sprays. However, evolution of resistance to Bt crops has decreased these benefits. Understanding of the genetic basis of resistance is needed to improve the ability to detect and counter pest resistance. We found that field-evolved resistance to Bt crops of the corn earworm, one of the most damaging crop pests in the United States, was not associated with mutations in 20 genes previously implicated in Bt resistance. Resistance was generally, but not always, associated with increased copies of a cluster of genes encoding trypsin proteins. This knowledge may facilitate better monitoring and management of pest resistance. AbstractTransgenic crops producing crystalline (Cry) proteins from the bacterium Bacillus thuringiensis (Bt) have been used extensively to control some major crop pests. However, many populations of the noctuid moth Helicoverpa zea, one of the most important crop pests in the United States, have evolved practical resistance to several Cry proteins including Cry1Ac. Although mutations in single genes that confer resistance to Cry proteins have been identified in lab-selected and gene-edited strains of H. zea and other lepidopteran pests, the genetic basis of field-evolved resistance to Cry proteins in H. zea has remained elusive. We used a genomic approach to analyze the genetic basis of field-evolved resistance to Cry1Ac in 937 H. zea derived from 17 sites in seven states of the southern United States. We found evidence for extensive gene flow among all populations studied. Field-evolved resistance was not associated with mutations in 20 single candidate genes previously implicated in resistance or susceptibility to Cry proteins in H. zea or other lepidopterans. Instead, resistance in field samples was associated with increased copy number of a cluster of nine trypsin genes. However, trypsin gene amplification occurred in a susceptible sample and not in all resistant samples, implying that this amplification does not always confer resistance and mutations in other genes also contribute to field-evolved resistance to Cry1Ac in H. zea. The mismatch between lab-generated and field-evolved resistance in H. zea is unlike other cases of Bt resistance and reflects challenges for managing this pest.
See https://www.pnas.org/doi/10.1073/pnas.2416091121
Figure 2: Genome-wide association study (GWAS) of H. zea resistance to Cry1Ac based on analysis of 4.2 million SNPs from field-derived insects that were resistant (TAMU-R) or susceptible (TAMU-S) to Cry1Ac in laboratory bioassays. Analysis of GWAS based on (A) single SNPs and (B) sliding windows (500 Kb each). Analysis of (C) single SNPs and (D) sliding windows within the region of chromosome 9 (4.84 to 5.79 Mb) significantly associated with resistance in the genome-wide sliding window analysis (B). The red horizontal lines show the Bonferroni-corrected thresholds for significant association with resistance: P = 1.2e−8 for single SNPs (A and C) and P = 3.3e−5 for sliding windows (B and D). Genes are shown by arrows pointing from the 5’ to 3’ end with orange for trypsin genes and gray for other genes. From Left to Right, the proteins encoded by the nine trypsin genes are granzyme M-like (a serine protease), chymotrypsin-like elastase family member 2A, anionic trypsin-2-like, trypsin-like, trypsin delta-like, serine protease 30-like (two variants), and trypsin 3A1-like (two variants). The two genes immediately upstream of the nine trypsin genes encode proteins myrosinase 1-like and disks large homolog 2-like.
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