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Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis

BACKGROUND: Pathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In...

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Autores principales: Behrens, Sarah, Peuß, Robert, Milutinović, Barbara, Eggert, Hendrik, Esser, Daniela, Rosenstiel, Philip, Schulenburg, Hinrich, Bornberg-Bauer, Erich, Kurtz, Joachim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4079954/
https://www.ncbi.nlm.nih.gov/pubmed/24908078
http://dx.doi.org/10.1186/1471-2164-15-445
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author Behrens, Sarah
Peuß, Robert
Milutinović, Barbara
Eggert, Hendrik
Esser, Daniela
Rosenstiel, Philip
Schulenburg, Hinrich
Bornberg-Bauer, Erich
Kurtz, Joachim
author_facet Behrens, Sarah
Peuß, Robert
Milutinović, Barbara
Eggert, Hendrik
Esser, Daniela
Rosenstiel, Philip
Schulenburg, Hinrich
Bornberg-Bauer, Erich
Kurtz, Joachim
author_sort Behrens, Sarah
collection PubMed
description BACKGROUND: Pathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In order to characterize the molecular mechanisms underpinning the two different infection routes, the transcriptomes of beetles of two different T. castaneum populations – one recently collected population (Cro1) and a commonly used laboratory strain (SB) – were analyzed using a next generation RNA sequencing approach. RESULTS: The genetically more diverse population Cro1 showed a significantly larger number of differentially expressed genes. While both populations exhibited similar reactions to pricking, their expression patterns in response to oral infection differed remarkably. In particular, the Cro1 population showed a strong response of cuticular proteins and developmental genes, which might indicate an adaptive developmental flexibility that was lost in the SB population presumably as a result of inbreeding. The immune response of SB was primarily based on antimicrobial peptides, while Cro1 relied on responses mediated by phenoloxidase and reactive oxygen species, which may explain the higher resistance of this strain against oral infection. CONCLUSIONS: Our data demonstrate that immunological and physiological processes underpinning the two different routes of infection are clearly distinct, and that host populations particularly differ in responses to oral infection. Furthermore, gene expression upon pricking infection entailed a strong signal of wounding, highlighting the importance of pricking controls in future infection studies. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-445) contains supplementary material, which is available to authorized users.
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spelling pubmed-40799542014-07-14 Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis Behrens, Sarah Peuß, Robert Milutinović, Barbara Eggert, Hendrik Esser, Daniela Rosenstiel, Philip Schulenburg, Hinrich Bornberg-Bauer, Erich Kurtz, Joachim BMC Genomics Research Article BACKGROUND: Pathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In order to characterize the molecular mechanisms underpinning the two different infection routes, the transcriptomes of beetles of two different T. castaneum populations – one recently collected population (Cro1) and a commonly used laboratory strain (SB) – were analyzed using a next generation RNA sequencing approach. RESULTS: The genetically more diverse population Cro1 showed a significantly larger number of differentially expressed genes. While both populations exhibited similar reactions to pricking, their expression patterns in response to oral infection differed remarkably. In particular, the Cro1 population showed a strong response of cuticular proteins and developmental genes, which might indicate an adaptive developmental flexibility that was lost in the SB population presumably as a result of inbreeding. The immune response of SB was primarily based on antimicrobial peptides, while Cro1 relied on responses mediated by phenoloxidase and reactive oxygen species, which may explain the higher resistance of this strain against oral infection. CONCLUSIONS: Our data demonstrate that immunological and physiological processes underpinning the two different routes of infection are clearly distinct, and that host populations particularly differ in responses to oral infection. Furthermore, gene expression upon pricking infection entailed a strong signal of wounding, highlighting the importance of pricking controls in future infection studies. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-445) contains supplementary material, which is available to authorized users. BioMed Central 2014-06-07 /pmc/articles/PMC4079954/ /pubmed/24908078 http://dx.doi.org/10.1186/1471-2164-15-445 Text en © Behrens et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Behrens, Sarah
Peuß, Robert
Milutinović, Barbara
Eggert, Hendrik
Esser, Daniela
Rosenstiel, Philip
Schulenburg, Hinrich
Bornberg-Bauer, Erich
Kurtz, Joachim
Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis
title Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis
title_full Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis
title_fullStr Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis
title_full_unstemmed Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis
title_short Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis
title_sort infection routes matter in population-specific responses of the red flour beetle to the entomopathogen bacillus thuringiensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4079954/
https://www.ncbi.nlm.nih.gov/pubmed/24908078
http://dx.doi.org/10.1186/1471-2164-15-445
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