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Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta

The traditional view of innate immunity in insects is that every exposure to a pathogen triggers an identical and appropriate immune response and that prior exposures to pathogens do not confer any protective (i.e., adaptive) effect against subsequent exposure to the same pathogen. This view has bee...

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Autores principales: Roesel, Charles L., Rosengaus, Rebeca B., Smith, Wendy, Vollmer, Steven V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593158/
https://www.ncbi.nlm.nih.gov/pubmed/33144962
http://dx.doi.org/10.1002/ece3.6764
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author Roesel, Charles L.
Rosengaus, Rebeca B.
Smith, Wendy
Vollmer, Steven V.
author_facet Roesel, Charles L.
Rosengaus, Rebeca B.
Smith, Wendy
Vollmer, Steven V.
author_sort Roesel, Charles L.
collection PubMed
description The traditional view of innate immunity in insects is that every exposure to a pathogen triggers an identical and appropriate immune response and that prior exposures to pathogens do not confer any protective (i.e., adaptive) effect against subsequent exposure to the same pathogen. This view has been challenged by experiments demonstrating that encounters with sublethal doses of a pathogen can prime the insect's immune system and, thus, have protective effects against future lethal doses. Immune priming has been reported across several insect species, including the red flour beetle, the honeycomb moth, the bumblebee, and the European honeybee, among others. Immune priming can also be transgenerational where the parent's pathogenic history influences the immune response of its offspring. Phenotypic evidence of transgenerational immune priming (TGIP) exists in the tobacco moth Manduca sexta where first‐instar progeny of mothers injected with the bacterium Serratia marcescens exhibited a significant increase of in vivo bacterial clearance. To identify the gene expression changes underlying TGIP in M. sexta, we performed transcriptome‐wide, transgenerational differential gene expression analysis on mothers and their offspring after mothers were exposed to S. marcescens. We are the first to perform transcriptome‐wide analysis of the gene expression changes associated with TGIP in this ecologically relevant model organism. We show that maternal exposure to both heat‐killed and live S. marcescens has strong and significant transgenerational impacts on gene expression patterns in their offspring, including upregulation of peptidoglycan recognition protein, toll‐like receptor 9, and the antimicrobial peptide cecropin.
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spelling pubmed-75931582020-11-02 Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta Roesel, Charles L. Rosengaus, Rebeca B. Smith, Wendy Vollmer, Steven V. Ecol Evol Original Research The traditional view of innate immunity in insects is that every exposure to a pathogen triggers an identical and appropriate immune response and that prior exposures to pathogens do not confer any protective (i.e., adaptive) effect against subsequent exposure to the same pathogen. This view has been challenged by experiments demonstrating that encounters with sublethal doses of a pathogen can prime the insect's immune system and, thus, have protective effects against future lethal doses. Immune priming has been reported across several insect species, including the red flour beetle, the honeycomb moth, the bumblebee, and the European honeybee, among others. Immune priming can also be transgenerational where the parent's pathogenic history influences the immune response of its offspring. Phenotypic evidence of transgenerational immune priming (TGIP) exists in the tobacco moth Manduca sexta where first‐instar progeny of mothers injected with the bacterium Serratia marcescens exhibited a significant increase of in vivo bacterial clearance. To identify the gene expression changes underlying TGIP in M. sexta, we performed transcriptome‐wide, transgenerational differential gene expression analysis on mothers and their offspring after mothers were exposed to S. marcescens. We are the first to perform transcriptome‐wide analysis of the gene expression changes associated with TGIP in this ecologically relevant model organism. We show that maternal exposure to both heat‐killed and live S. marcescens has strong and significant transgenerational impacts on gene expression patterns in their offspring, including upregulation of peptidoglycan recognition protein, toll‐like receptor 9, and the antimicrobial peptide cecropin. John Wiley and Sons Inc. 2020-09-17 /pmc/articles/PMC7593158/ /pubmed/33144962 http://dx.doi.org/10.1002/ece3.6764 Text en © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Roesel, Charles L.
Rosengaus, Rebeca B.
Smith, Wendy
Vollmer, Steven V.
Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta
title Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta
title_full Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta
title_fullStr Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta
title_full_unstemmed Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta
title_short Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta
title_sort transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in manduca sexta
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593158/
https://www.ncbi.nlm.nih.gov/pubmed/33144962
http://dx.doi.org/10.1002/ece3.6764
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