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

Brad S. Coates, USDA-ARS, Corn Insects & Crop Genetics Research Unit, Ames, IAFollow
Emeline Deleury, INRAE, CNRS, Université Côte d’Azur, ISA, FranceFollow
Aaron J. Gassmann, Iowa State UniversityFollow
Bruce E. Hibbard, USDA-ARSFollow
Lance Meinke, University of Nebraska-LincolnFollow
Nicholas J. Miller, Illinois Institute of TechnologyFollow
Jennifer L. Petzold-Maxwell, Iowa State UniversityFollow
B. Wade French, USDA-ARS, North Central Agricultural Research Laboratory, Brookings, SDFollow
Thomas W. Sappington, USDA-ARSFollow
Blair D. Siegfried, University of FloridaFollow
Thomas Guillemaud, INRA, CNRS, Université Côte d’Azur, ISA, France

ORCID IDs

https://orcid.org/0000-0001-8908-1529 Brad S. Coates

Document Type

Article

Date of this Version

2021

Citation

Coates et al. BMC Genomics (2021) 22:639

doi:10.1186/s12864-021-07932-4

Comments

© The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,

Abstract

Background: Resistance of pest insect species to insecticides, including B. 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 and having populations showing increasing levels of resistance to hybrids expressing Bt pesticidal proteins, the cell mechanisms leading to mortality are not fully understood.

Results: Twenty unique RNA-seq libraries from the Bt susceptible D. v. virgifera inbred line Ped12, representing all growth stages and a range of different adult and larval exposures, were assembled into a reference transcriptome. Ten-day exposures of Ped12 larvae to transgenic Bt Cry3Bb1 and Gpp34/Tpp35Ab1 maize roots showed significant differential expression of 1055 and 1374 transcripts, respectively, compared to cohorts on non-Bt maize. Among these, 696 were differentially expressed in both Cry3Bb1 and Gpp34/Tpp35Ab1 maize exposures. Differentially-expressed transcripts encoded protein domains putatively involved in detoxification, metabolism, binding, and transport, were, in part, shared among transcripts that changed significantly following exposures to the entomopathogens Heterorhabditis bacteriophora and Metarhizium anisopliae. Differentially expressed transcripts in common between Bt and entomopathogen treatments encode proteins in general stress response pathways, including putative Bt binding receptors from the ATP binding cassette transporter superfamily. Putative caspases, pro- and anti-apoptotic factors, as well as endoplasmic reticulum (ER) stress-response factors were identified among transcripts uniquely up-regulated following exposure to either Bt protein.

Conclusions: Our study suggests that the up-regulation of genes involved in ER stress management and apoptotic progression may be important in determining cell fate following exposure of susceptible D. v. virgifera larvae to Bt maize roots. This study provides novel insights into insect response to Bt intoxication, and a possible framework for future investigations of resistance mechanisms.