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Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses

BACKGROUND: Phenotypic plasticity, i.e. the capacity to change the phenotype in response to changes in the environment without alteration of the genotype, is important for coping with unstable environments. In spite of the ample evidence that microorganisms are a major environmental component playin...

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Autores principales: Leroy, Magali, Mosser, Thomas, Manière, Xavier, Alvarez, Diana Fernández, Matic, Ivan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3483211/
https://www.ncbi.nlm.nih.gov/pubmed/22998555
http://dx.doi.org/10.1186/1471-2148-12-187
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author Leroy, Magali
Mosser, Thomas
Manière, Xavier
Alvarez, Diana Fernández
Matic, Ivan
author_facet Leroy, Magali
Mosser, Thomas
Manière, Xavier
Alvarez, Diana Fernández
Matic, Ivan
author_sort Leroy, Magali
collection PubMed
description BACKGROUND: Phenotypic plasticity, i.e. the capacity to change the phenotype in response to changes in the environment without alteration of the genotype, is important for coping with unstable environments. In spite of the ample evidence that microorganisms are a major environmental component playing a significant role in eukaryotic organisms health and disease, there is not much information about the effect of microorganism-induced developmental phenotypic plasticity on adult animals’ stress resistance and longevity. RESULTS: We examined the consequences of development of Caenorhabditis elegans larvae fed with different bacterial strains on stress resistance and lifespan of adult nematodes. Bacterial strains used in this study were either pathogenic or innocuous to nematodes. Exposure to the pathogen during development did not affect larval survival. However, the development of nematodes on the pathogenic bacterial strains increased lifespan of adult nematodes exposed to the same or a different pathogen. A longer nematode lifespan, developed on pathogens and exposed to pathogens as adults, did not result from an enhanced capacity to kill bacteria, but is likely due to an increased tolerance to the damage inflicted by the pathogenic bacteria. We observed that adult nematodes developed on a pathogen induce higher level of expression of the hsp-16.2 gene and have higher resistance to heat shock than nematodes developed on an innocuous strain. Therefore, the increased resistance to pathogens could be, at least partially, due to the early induction of the heat shock response in nematodes developed on pathogens. The lifespan increase is controlled by the DBL-1 transforming growth factor beta-like, DAF-2/DAF-16 insulin-like, and p38 MAP kinase pathways. Therefore, the observed modulation of adult nematode lifespans by developmental exposure to a pathogen is likely a genetically controlled response. CONCLUSIONS: Our study shows that development on pathogens has a hormetic effect on adult nematodes, as it results in increased resistance to different pathogens and to heat shock. Such developmental plasticity of C. elegans nematodes, which are self-fertilizing homozygous animals producing offspring with negligible genetic variation, could increase the probability of survival in changing environments.
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spelling pubmed-34832112012-10-30 Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses Leroy, Magali Mosser, Thomas Manière, Xavier Alvarez, Diana Fernández Matic, Ivan BMC Evol Biol Research Article BACKGROUND: Phenotypic plasticity, i.e. the capacity to change the phenotype in response to changes in the environment without alteration of the genotype, is important for coping with unstable environments. In spite of the ample evidence that microorganisms are a major environmental component playing a significant role in eukaryotic organisms health and disease, there is not much information about the effect of microorganism-induced developmental phenotypic plasticity on adult animals’ stress resistance and longevity. RESULTS: We examined the consequences of development of Caenorhabditis elegans larvae fed with different bacterial strains on stress resistance and lifespan of adult nematodes. Bacterial strains used in this study were either pathogenic or innocuous to nematodes. Exposure to the pathogen during development did not affect larval survival. However, the development of nematodes on the pathogenic bacterial strains increased lifespan of adult nematodes exposed to the same or a different pathogen. A longer nematode lifespan, developed on pathogens and exposed to pathogens as adults, did not result from an enhanced capacity to kill bacteria, but is likely due to an increased tolerance to the damage inflicted by the pathogenic bacteria. We observed that adult nematodes developed on a pathogen induce higher level of expression of the hsp-16.2 gene and have higher resistance to heat shock than nematodes developed on an innocuous strain. Therefore, the increased resistance to pathogens could be, at least partially, due to the early induction of the heat shock response in nematodes developed on pathogens. The lifespan increase is controlled by the DBL-1 transforming growth factor beta-like, DAF-2/DAF-16 insulin-like, and p38 MAP kinase pathways. Therefore, the observed modulation of adult nematode lifespans by developmental exposure to a pathogen is likely a genetically controlled response. CONCLUSIONS: Our study shows that development on pathogens has a hormetic effect on adult nematodes, as it results in increased resistance to different pathogens and to heat shock. Such developmental plasticity of C. elegans nematodes, which are self-fertilizing homozygous animals producing offspring with negligible genetic variation, could increase the probability of survival in changing environments. BioMed Central 2012-09-21 /pmc/articles/PMC3483211/ /pubmed/22998555 http://dx.doi.org/10.1186/1471-2148-12-187 Text en Copyright ©2012 Leroy et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 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
Leroy, Magali
Mosser, Thomas
Manière, Xavier
Alvarez, Diana Fernández
Matic, Ivan
Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses
title Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses
title_full Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses
title_fullStr Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses
title_full_unstemmed Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses
title_short Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses
title_sort pathogen-induced caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3483211/
https://www.ncbi.nlm.nih.gov/pubmed/22998555
http://dx.doi.org/10.1186/1471-2148-12-187
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