Novel genetic basis of resistance to Bt toxin Cry1Ac inHelicoverpa zea

Abstract

Crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) have advanced pest management, but their benefits are diminished when pests evolve resistance. Elucidating the genetic basis of pest resistance to Bt toxins can improve resistance monitoring, resistance management, and design of new insecticides. Here, we investigated the genetic basis of resistance to Bt toxin Cry1Ac in the lepidopteran Helicoverpa zea, one of the most damaging crop pests in the United States. To facilitate this research, we built the first chromosome-level genome assembly for this species, which has 31 chromosomes containing 375 Mb and 15,482 predicted proteins. Using a genome-wide association study, fine-scale mapping, and RNA-seq, we identified a 250-kb quantitative trait locus (QTL) on chromosome 13 that was strongly associated with resistance in a strain of H. zea that had been selected for resistance in the field and lab. The mutation in this QTL contributed to but was not sufficient for resistance, which implies alleles in more than one gene contributed to resistance. This QTL contains no genes with a previously reported role in resistance or susceptibility to Bt toxins. However, in resistant insects, this QTL has a premature stop codon in a kinesin gene which is a primary candidate as a mutation contributing to resistance. We found no changes in gene sequence or expression consistently associated with resistance for 11 genes previously implicated in lepidopteran resistance to Cry1Ac. Thus, the results reveal a novel and polygenic basis of resistance.

Population Genomics of Nonrecessive Resistance to Bt Toxin Cry1Ac in Helicoverpa armigera From Northern China

“…The QTL on Chr26 associated with nonrecessive resistance in this study does not contain genes with a previously reported role in resistance or susceptibility to Bt toxins in H. armigera or other lepidopterans (Taylor et al 2021, Benowitz et al 2022, and references cited therein). It remains to be determined if one or more mutations in the QTL on Chr26 cause resistance to Cry1Ac.…”

“…However, it remains to be determined if T92C is important in resistance to Cry1Ac of H. armigera from other regions of China and other parts of the world. Mutations in the tetraspanin gene were not associated with resistance to Cry1Ab or Cry1Ac in populations of the sibling species Helicoverpa zea from the United States (Fritz et al 2020, Taylor et al 2021, Benowitz et al 2022.…”

Inheritance of Resistance to Cry1A.105 in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)

“…Thus, the inheritance of Cry1A.105 resistance in H. zea observed in the current study is similar to the reported resistance to Cry1Ac in H. armigera . However, a recent study suggested that a mutation in a quantitative trait locus on chromosome 13 was related to the resistance to Cry1Ac in a field/lab-selected H. zea strain, but the resistance was likely controlled by more than one locus [ 22 ]. Thus, additional studies are needed to elucidate the detailed genetic basis of resistance to Cry1A.105 in H. zea .…”

“…However, due to the well-known difficulty in selection and maintenance of Bt-resistant H. zea colonies in the laboratory [ 18 , 19 ], inheritance of resistance to Bt toxins in H. zea has been fully studied in only two cases, one with Vip3A resistance and another with Cry2Ab resistance in Texas populations [ 20 , 21 ]. In addition, a recent genome-wide mapping study analyzed the genetic basis of resistance to Cry1Ac in H. zea [ 22 ].…”

Utility and challenges of using whole‐genome resequencing to detect emerging insect and mite resistance in agroecosystems

“…When resistance is detected in a pest population, quantitative genetic and genomic experiments can link changes in a pest's resistance status to one or more causal mutations across the genome (i.e., genome architecture). Commonly used approaches include quantitative trait locus (QTL) analysis (e.g., Gahan et al, 2001 ; Heckel et al, 1999 ; Taylor et al, 2021 ; Wondji et al, 2007 ), bulked segregant analysis (BSA; e.g., Benowitz et al, 2022 ; Fotoukkiaii et al, 2021 ; Van Leeuwen et al, 2012 ), and evolve and resequence studies (Snoeck et al, 2019 ; Wybouw et al, 2019 ). QTL and BSA approaches use offspring from planned crosses between pesticide‐resistant and susceptible populations and SNPs from across the genome to identify genomic regions where genotypic variation is strongly associated with variation in resistance phenotypes.…”