Minghui Jin, Yinxue Shan, Yan Peng, Wenhui Wang, Huihui Zhang, Kaiyu Liu, David G. Heckel, Kongming Wu, Bruce E. Tabashnik, and Yutao Xiao

PNAS October 24, 2023; 120 (44) e2306932120

Spodoptera frugiperda

Significance

Crops 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 pest resistance to crystalline Bt proteins has decreased these benefits, promoting adoption of transgenic crops that produce a Bt vegetative insecticidal protein called Vip3Aa. Better understanding of resistance to Vip3Aa is urgently needed to proactively combat pest resistance to this protein. Here we found that reduced expression of a gene encoding a protein that regulates transcription decreased susceptibility to Vip3Aa in the fall armyworm, one of the world’s most voracious crop pests. The identification of this genetic basis of resistance may help to improve management of resistance and enhance sustainability of Bt crops.

Abstract

Transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) have revolutionized control of some major pests. However, more than 25 cases of field-evolved practical resistance have reduced the efficacy of transgenic crops producing crystalline (Cry) Bt proteins, spurring adoption of alternatives including crops producing the Bt vegetative insecticidal protein Vip3Aa. Although practical resistance to Vip3Aa has not been reported yet, better understanding of the genetic basis of resistance to Vip3Aa is urgently needed to proactively monitor, delay, and counter pest resistance. This is especially important for fall armyworm (Spodoptera frugiperda), which has evolved practical resistance to Cry proteins and is one of the world’s most damaging pests. Here, we report the identification of an association between downregulation of the transcription factor gene SfMyb and resistance to Vip3Aa in S. frugiperda. Results from a genome-wide association study, fine-scale mapping, and RNA-Seq identified this gene as a compelling candidate for contributing to the 206-fold resistance to Vip3Aa in a laboratory-selected strain. Experimental reduction of SfMyb expression in a susceptible strain using RNA interference (RNAi) or CRISPR/Cas9 gene editing decreased susceptibility to Vip3Aa, confirming that reduced expression of this gene can cause resistance to Vip3Aa. Relative to the wild-type promoter for SfMyb, the promoter in the resistant strain has deletions and lower activity. Data from yeast one-hybrid assays, genomics, RNA-Seq, RNAi, and proteomics identified genes that are strong candidates for mediating the effects of SfMyb on Vip3Aa resistance. The results reported here may facilitate progress in understanding and managing pest resistance to Vip3Aa.

See https://www.pnas.org/doi/10.1073/pnas.2306932120

Fig. 1: Region on chromosome 27 associated with S. frugiperda resistance to Vip3Aa. Manhattan plots: (A) SNPs and (B) indels for all 31 chromosomes; (C) SNPs and (D) indels for a region on chromosome 27. Horizontal dashed lines indicate the threshold for significant association. Below the Manhattan plots for (C) and (D) are models of the nine genes in the region and LD heatmaps based on SNPs and indels, respectively. The gene models show the two expressed genes (SfMyb and SfNup62) in dark blue and the other seven genes in light blue.