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Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans

How pathogen infection in a parental generation affects response in future generations to the same pathogen via epigenetic modifications has been the topic of recent studies. These studies focused on changes attributed to transgenerational epigenetic inheritance and how these changes cause an observ...

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Autores principales: Wibisono, Phillip, Sun, Jingru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10556243/
https://www.ncbi.nlm.nih.gov/pubmed/37811492
http://dx.doi.org/10.3389/fphys.2023.1225858
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author Wibisono, Phillip
Sun, Jingru
author_facet Wibisono, Phillip
Sun, Jingru
author_sort Wibisono, Phillip
collection PubMed
description How pathogen infection in a parental generation affects response in future generations to the same pathogen via epigenetic modifications has been the topic of recent studies. These studies focused on changes attributed to transgenerational epigenetic inheritance and how these changes cause an observable difference in behavior or immune response in a population. However, we questioned if pathogen infection causes hidden epigenetic changes to fitness that are not observable at the population level. Using the nematode Caenorhabditis elegans as a model organism, we examined the generation-to-generation differences in survival of both an unexposed and primed lineage of animals against a human opportunistic pathogen Salmonella enterica. We discovered that training a lineage of C. elegans against a specific pathogen does not cause a significant change to overall survival, but rather narrows survival variability between generations. Quantification of gene expression revealed reduced variation of a specific member of the TFEB lipophagic pathway. We also provided the first report of a repeating pattern of survival times over the course of 12 generations in the control lineage of C. elegans. This repeating pattern indicates that the variability in survival between generations of the control lineage is not random but may be regulated by unknown mechanisms. Overall, our study indicates that pathogen infection can cause specific phenotypic changes due to epigenetic modifications, and a possible system of epigenetic regulation between generations.
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spelling pubmed-105562432023-10-07 Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans Wibisono, Phillip Sun, Jingru Front Physiol Physiology How pathogen infection in a parental generation affects response in future generations to the same pathogen via epigenetic modifications has been the topic of recent studies. These studies focused on changes attributed to transgenerational epigenetic inheritance and how these changes cause an observable difference in behavior or immune response in a population. However, we questioned if pathogen infection causes hidden epigenetic changes to fitness that are not observable at the population level. Using the nematode Caenorhabditis elegans as a model organism, we examined the generation-to-generation differences in survival of both an unexposed and primed lineage of animals against a human opportunistic pathogen Salmonella enterica. We discovered that training a lineage of C. elegans against a specific pathogen does not cause a significant change to overall survival, but rather narrows survival variability between generations. Quantification of gene expression revealed reduced variation of a specific member of the TFEB lipophagic pathway. We also provided the first report of a repeating pattern of survival times over the course of 12 generations in the control lineage of C. elegans. This repeating pattern indicates that the variability in survival between generations of the control lineage is not random but may be regulated by unknown mechanisms. Overall, our study indicates that pathogen infection can cause specific phenotypic changes due to epigenetic modifications, and a possible system of epigenetic regulation between generations. Frontiers Media S.A. 2023-09-22 /pmc/articles/PMC10556243/ /pubmed/37811492 http://dx.doi.org/10.3389/fphys.2023.1225858 Text en Copyright © 2023 Wibisono and Sun. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Wibisono, Phillip
Sun, Jingru
Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans
title Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans
title_full Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans
title_fullStr Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans
title_full_unstemmed Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans
title_short Pathogen infection induces specific transgenerational modifications to gene expression and fitness in Caenorhabditis elegans
title_sort pathogen infection induces specific transgenerational modifications to gene expression and fitness in caenorhabditis elegans
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10556243/
https://www.ncbi.nlm.nih.gov/pubmed/37811492
http://dx.doi.org/10.3389/fphys.2023.1225858
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