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A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans

Developmental patterning in Caenorhabditis elegans is known to proceed in a highly stereotypical manner, which raises the question of how developmental robustness is achieved despite the inevitable stochastic noise. We focus here on a population of epidermal cells, the seam cells, which show stem ce...

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Autores principales: Koneru, Sneha L., Quah, Fu Xiang, Ghose, Ritobrata, Hintze, Mark, Gritti, Nicola, van Zon, Jeroen Sebastiaan, Barkoulas, Michalis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105389/
https://www.ncbi.nlm.nih.gov/pubmed/33963222
http://dx.doi.org/10.1038/s41598-021-88500-4
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author Koneru, Sneha L.
Quah, Fu Xiang
Ghose, Ritobrata
Hintze, Mark
Gritti, Nicola
van Zon, Jeroen Sebastiaan
Barkoulas, Michalis
author_facet Koneru, Sneha L.
Quah, Fu Xiang
Ghose, Ritobrata
Hintze, Mark
Gritti, Nicola
van Zon, Jeroen Sebastiaan
Barkoulas, Michalis
author_sort Koneru, Sneha L.
collection PubMed
description Developmental patterning in Caenorhabditis elegans is known to proceed in a highly stereotypical manner, which raises the question of how developmental robustness is achieved despite the inevitable stochastic noise. We focus here on a population of epidermal cells, the seam cells, which show stem cell-like behaviour and divide symmetrically and asymmetrically over post-embryonic development to generate epidermal and neuronal tissues. We have conducted a mutagenesis screen to identify mutants that introduce phenotypic variability in the normally invariant seam cell population. We report here that a null mutation in the fusogen eff-1 increases seam cell number variability. Using time-lapse microscopy and single molecule fluorescence hybridisation, we find that seam cell division and differentiation patterns are mostly unperturbed in eff-1 mutants, indicating that cell fusion is uncoupled from the cell differentiation programme. Nevertheless, seam cell losses due to the inappropriate differentiation of both daughter cells following division, as well as seam cell gains through symmetric divisions towards the seam cell fate were observed at low frequency. We show that these stochastic errors likely arise through accumulation of defects interrupting the continuity of the seam and changing seam cell shape, highlighting the role of tissue homeostasis in suppressing phenotypic variability during development.
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spelling pubmed-81053892021-05-10 A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans Koneru, Sneha L. Quah, Fu Xiang Ghose, Ritobrata Hintze, Mark Gritti, Nicola van Zon, Jeroen Sebastiaan Barkoulas, Michalis Sci Rep Article Developmental patterning in Caenorhabditis elegans is known to proceed in a highly stereotypical manner, which raises the question of how developmental robustness is achieved despite the inevitable stochastic noise. We focus here on a population of epidermal cells, the seam cells, which show stem cell-like behaviour and divide symmetrically and asymmetrically over post-embryonic development to generate epidermal and neuronal tissues. We have conducted a mutagenesis screen to identify mutants that introduce phenotypic variability in the normally invariant seam cell population. We report here that a null mutation in the fusogen eff-1 increases seam cell number variability. Using time-lapse microscopy and single molecule fluorescence hybridisation, we find that seam cell division and differentiation patterns are mostly unperturbed in eff-1 mutants, indicating that cell fusion is uncoupled from the cell differentiation programme. Nevertheless, seam cell losses due to the inappropriate differentiation of both daughter cells following division, as well as seam cell gains through symmetric divisions towards the seam cell fate were observed at low frequency. We show that these stochastic errors likely arise through accumulation of defects interrupting the continuity of the seam and changing seam cell shape, highlighting the role of tissue homeostasis in suppressing phenotypic variability during development. Nature Publishing Group UK 2021-05-07 /pmc/articles/PMC8105389/ /pubmed/33963222 http://dx.doi.org/10.1038/s41598-021-88500-4 Text en © The Author(s) 2021 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
Koneru, Sneha L.
Quah, Fu Xiang
Ghose, Ritobrata
Hintze, Mark
Gritti, Nicola
van Zon, Jeroen Sebastiaan
Barkoulas, Michalis
A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans
title A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans
title_full A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans
title_fullStr A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans
title_full_unstemmed A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans
title_short A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans
title_sort role for the fusogen eff-1 in epidermal stem cell number robustness in caenorhabditis elegans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105389/
https://www.ncbi.nlm.nih.gov/pubmed/33963222
http://dx.doi.org/10.1038/s41598-021-88500-4
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