A chromosome-level genome assembly of the soybean pod borer: insights into larval transcriptional response to transgenic soybean expressing the pesticidal Cry1Ac protein

Authors: WANG, YANGZHOU - Jilin Academy Of Agricultural Sciences; YAO, YAO - Jilin Academy Of Agricultural Sciences; ZHANG, YUNYUE - Jilin Academy Of Agricultural Sciences; QIAN, XUEYAN - Jilin Academy Of Agricultural Sciences; GUO, DONGQUAN - Jilin Academy Of Agricultural Sciences; Coates, Brad

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/12/2024
Publication Date: 4/9/2024
Citation: Wang, Y., Yao, Y., Zhang, Y., Qian, X., Guo, D., Coates, B.S. 2024. A chromosome-level genome assembly of the soybean pod borer: Insights into larval transcriptional response to transgenic soybean expressing the pesticidal Cry1Ac protein. BMC Genomics. 25. https://doi.org/10.1186/s12864-024-10216-2.
DOI: https://doi.org/10.1186/s12864-024-10216-2

Interpretive Summary: Genetically modified (GM) crop plants that express one or more Bacillus thuringiensis (Bt) pesticidal proteins are used to manage feeding damage caused by pest insects. Bt proteins damage cells in the gut of susceptible insects which causes them to cease feeding and eventually leads to their death. The development of Bt resistance among pest insects threatens the effectiveness of these GM crops. Mechanisms that cause death or adaptations that allow insects to survive while feeding on Bt crops remain unknown. To partially address these unknowns, an ARS scientist along with an international team of collaborators compared the expression of genes between larvae of the pest insect, the soybean pod borer (SPB), fed on conventional (non-Bt) soybean or Bt soybean that express the Bt protein Cry1Ac. SPB larvae fed Bt soybean showed an increase in expression of genes involved in stress response and metabolism, relative to larvae fed conventional non-Bt soybean. Changes in the expression of stress response genes, including those involved in cell repair mechanisms, and may determine if cells can recover from damage caused by eating Bt soybean. The differentially expressed genes identified in this study provide insight into the potential response of insects to Bt soybean, and potential mechanisms by which Bt resistance may evolve. This research is of interest to university, government, and industry stakeholders, as well as regulatory agencies concerned about impacts resistant insect populations have on the sustainability of crop management tactics that rely on Bt pesticidal proteins.

Technical Abstract: Genetically modified (GM) crop plants with transgenic expression of Bacillus thuringiensis (Bt) pesticidal proteins are used to manage feeding damage by pest insects. The durability of this technology is threatened by the selection for resistance in pest populations. The molecular mechanism(s) involved in insect physiological response or evolution of resistance to Bt is not fully understood. To investigate the response of a susceptible target insect to Bt, the soybean pod borer, Leguminivora glycinivorella (Lepidoptera: Tortricidae), was exposed to soybean, Glycine max, expressing Cry1Ac pesticidal protein or the non-transgenic parental cultivar. Assessment of larval changes in gene expression was facilitated by a third-generation sequenced and scaffolded chromosome-level assembly of the L. glycinivorella genome (657.4 Mb; 27 autosomes + Z chromosome), and subsequent structural annotation of 18,197 RefSeq gene models encoding 23,735 putative mRNA transcripts. Exposure of L. glycinivorella larvae to transgenic Cry1Ac G. max resulted in prediction of significant differential gene expression for 204 gene models (64 up- and 140 and down-regulated) and differential splicing among isoforms for 10 genes compared to unexposed cohorts. Differentially expressed genes (DEGs) included putative peritrophic membrane constituents, orthologs of previously identified Bt resistance genes, and those involved in stress response. Putative functional Gene Ontology (GO) annotations assigned to DEGs were significantly enriched for 36 categories at GO level 2, respectively. Most significantly enriched cellular component (CC), biological process (BP), and molecular function (MF) categories corresponded to vacuolar and microbody, transport and metabolic processes, and binding and reductase activities. The DEGs in enriched GO categories were biased for those that were down-regulated (= 0.783), with only MF categories GTPase and iron binding activities were bias for up-regulation genes. This study provides insights into pathways and processes involved larval response to Bt intoxication, which may inform future investigations into mechanisms of resistance.