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The transcriptional legacy of developmental stochasticity

Genetic and environmental variation are key contributors during organism development, but the influence of minor perturbations or noise is difficult to assess. This study focuses on the stochastic variation in allele-specific expression that persists through cell divisions in the nine-banded armadil...

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Autores principales: Ballouz, Sara, Kawaguchi, Risa Karakida, Pena, Maria T., Fischer, Stephan, Crow, Megan, French, Leon, Knight, Frank M., Adams, Linda B., Gillis, Jesse
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10632366/
https://www.ncbi.nlm.nih.gov/pubmed/37940702
http://dx.doi.org/10.1038/s41467-023-43024-5
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author Ballouz, Sara
Kawaguchi, Risa Karakida
Pena, Maria T.
Fischer, Stephan
Crow, Megan
French, Leon
Knight, Frank M.
Adams, Linda B.
Gillis, Jesse
author_facet Ballouz, Sara
Kawaguchi, Risa Karakida
Pena, Maria T.
Fischer, Stephan
Crow, Megan
French, Leon
Knight, Frank M.
Adams, Linda B.
Gillis, Jesse
author_sort Ballouz, Sara
collection PubMed
description Genetic and environmental variation are key contributors during organism development, but the influence of minor perturbations or noise is difficult to assess. This study focuses on the stochastic variation in allele-specific expression that persists through cell divisions in the nine-banded armadillo (Dasypus novemcinctus). We investigated the blood transcriptome of five wild monozygotic quadruplets over time to explore the influence of developmental stochasticity on gene expression. We identify an enduring signal of autosomal allelic variability that distinguishes individuals within a quadruplet despite their genetic similarity. This stochastic allelic variation, akin to X-inactivation but broader, provides insight into non-genetic influences on phenotype. The presence of stochastically canalized allelic signatures represents a novel axis for characterizing organismal variability, complementing traditional approaches based on genetic and environmental factors. We also developed a model to explain the inconsistent penetrance associated with these stochastically canalized allelic expressions. By elucidating mechanisms underlying the persistence of allele-specific expression, we enhance understanding of development’s role in shaping organismal diversity.
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spelling pubmed-106323662023-11-10 The transcriptional legacy of developmental stochasticity Ballouz, Sara Kawaguchi, Risa Karakida Pena, Maria T. Fischer, Stephan Crow, Megan French, Leon Knight, Frank M. Adams, Linda B. Gillis, Jesse Nat Commun Article Genetic and environmental variation are key contributors during organism development, but the influence of minor perturbations or noise is difficult to assess. This study focuses on the stochastic variation in allele-specific expression that persists through cell divisions in the nine-banded armadillo (Dasypus novemcinctus). We investigated the blood transcriptome of five wild monozygotic quadruplets over time to explore the influence of developmental stochasticity on gene expression. We identify an enduring signal of autosomal allelic variability that distinguishes individuals within a quadruplet despite their genetic similarity. This stochastic allelic variation, akin to X-inactivation but broader, provides insight into non-genetic influences on phenotype. The presence of stochastically canalized allelic signatures represents a novel axis for characterizing organismal variability, complementing traditional approaches based on genetic and environmental factors. We also developed a model to explain the inconsistent penetrance associated with these stochastically canalized allelic expressions. By elucidating mechanisms underlying the persistence of allele-specific expression, we enhance understanding of development’s role in shaping organismal diversity. Nature Publishing Group UK 2023-11-09 /pmc/articles/PMC10632366/ /pubmed/37940702 http://dx.doi.org/10.1038/s41467-023-43024-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ballouz, Sara
Kawaguchi, Risa Karakida
Pena, Maria T.
Fischer, Stephan
Crow, Megan
French, Leon
Knight, Frank M.
Adams, Linda B.
Gillis, Jesse
The transcriptional legacy of developmental stochasticity
title The transcriptional legacy of developmental stochasticity
title_full The transcriptional legacy of developmental stochasticity
title_fullStr The transcriptional legacy of developmental stochasticity
title_full_unstemmed The transcriptional legacy of developmental stochasticity
title_short The transcriptional legacy of developmental stochasticity
title_sort transcriptional legacy of developmental stochasticity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10632366/
https://www.ncbi.nlm.nih.gov/pubmed/37940702
http://dx.doi.org/10.1038/s41467-023-43024-5
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