Up-regulation of apoptotic- and cell survival-related gene pathways following exposures of western corn rootworm to B. thuringiensis crystalline pesticidal proteins in transgenic maize roots

Authors: Coates, Brad; DELEURY, EMELINE - Inra, Génétique Animale Et Biologie Intégrative , Jouy-En-josas, France; GASSMANN, AARON - Iowa State University; Hibbard, Bruce; MEINKE, LANCE - University Of Nebraska; MILLER, NICHOLAS - Illinois Institute Of Technology; PETZOLD-MAXWELL, JENNIFER - Iowa State University; French, Bryan; Sappington, Thomas; SIEGFRIED, BLAIR - University Of Florida; GUILLEMAUD, THOMAS - Inra, Génétique Animale Et Biologie Intégrative , Jouy-En-josas, France

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/4/2021
Publication Date: 9/4/2021
Citation: Coates, B.S., Deleury, E., Gassmann, A.J., Hibbard, B.E., Meinke, L.J., Miller, N.J., Petzold-Maxwell, J., French, B.W., Sappington, T.W., Siegfried, B.D., Guillemaud, T. 2021. Up-regulation of apoptotic- and cell survival-related gene pathways following exposures of western corn rootworm to B. thuringiensis crystalline pesticidal proteins in transgenic maize roots. Biomed Central (BMC) Genomics. 22. Article 639. https://doi.org/10.1186/s12864-021-07932-4.
DOI: https://doi.org/10.1186/s12864-021-07932-4

Interpretive Summary: The development of insecticide resistance in insect pest species is a threat to agricultural production worldwide. Western corn rootworm (WCR) feeding damage results in economically significant yield losses to growers, and is difficult to control due to widespread WCR resistance to multiple insecticides. This includes resistance to all insecticidal Bacillus thuringiensis (Bt) toxins expressed by transgenic corn hybrids. The mechanisms that cause death or adaptations that allow WCR to survive while feeding on Bt corn remain unknown. To partially address these unknowns, ARS scientists along with a team of domestic and international team of collaborators investigated the changes in gene expression among susceptible WCR larvae fed hybrid corn that expressed different Bt toxins. Larvae fed Bt corn showed an increase in expression of genes involved in stress response and metabolism relative to larvae fed non-Bt conventional corn. Stress response genes included those involved in determining if cells are destroyed or recover from damage. This evidence led the research team to propose that a balance between life or death signals determine if WCR larvae survive when feeding on Bt hybrid corn. The differentially expressed genes identified in this study provide insight into the potential response of WCR to Bt maize exposure, and potential mechanisms by which insecticide resistance may evolve. This research is of interest to university, government, and industry stakeholders, as well as regulatory agencies concerned about the adaptation of arthropod populations to insecticidal agents.

Technical Abstract: Adaptations by pest arthropod species to insecticides, including Bacillus thuringiensis (Bt) pesticidal proteins expressed by transgenic plants, is a threat to global food security. Despite the western corn rootworm, Diabrotica virgifera virgifera, being a major pest of maize, with populations with different levels of resistance to hybrids expressing Bt pesticidal proteins, the cell mechanisms leading to mortality are not fully understood. To address this shortfall, 20 unique RNA-seq libraries were used to assemble a reference transcriptome from the Bt susceptible D. v. virgifera inbred line Ped12. Ten-day exposure of Ped12 larvae to transgenic Bt Cry3Bb1 and Gpp34/Tpp35Ab1 maize showed significant differential expression of 1,057 and 1,374 transcripts, respectively, compared to cohorts on non-Bt maize, of which 696 were shared among both Bt exposures. Differentially-expressed transcripts encoded protein domains involved in detoxification, metabolism, binding, and transport, but partially overlapped with those changed following exposure to the entomopathogens Heterorhabditis bacteriophora and Metarhizium anisopliae. These overlapping transcripts encoded proteins within general stress response pathways, and included those for putative Bt binding receptors of the ATP binding cassette transporter superfamily. Regardless, putative caspases, pro- and anti-apoptotic factors, as well as endoplasmic reticulum (ER) stress-response factors were identified among transcripts uniquely up-regulated following both Bt protein exposures. Results suggest that up-regulation of genes involved in ER stress management and apoptotic progression may be important in determining cell fate following Bt protein exposure. This study provides novel insight into insect response to Bt intoxication, and a possible framework for future investigations of resistance mechanisms.