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Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
Gene expression oscillators can structure biological events temporally and spatially. Different biological functions benefit from distinct oscillator properties. Thus, finite developmental processes rely on oscillators that start and stop at specific times, a poorly understood behavior. Here, we hav...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7370751/ https://www.ncbi.nlm.nih.gov/pubmed/32687264 http://dx.doi.org/10.15252/msb.20209498 |
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author | Meeuse, Milou WM Hauser, Yannick P Morales Moya, Lucas J Hendriks, Gert‐Jan Eglinger, Jan Bogaarts, Guy Tsiairis, Charisios Großhans, Helge |
author_facet | Meeuse, Milou WM Hauser, Yannick P Morales Moya, Lucas J Hendriks, Gert‐Jan Eglinger, Jan Bogaarts, Guy Tsiairis, Charisios Großhans, Helge |
author_sort | Meeuse, Milou WM |
collection | PubMed |
description | Gene expression oscillators can structure biological events temporally and spatially. Different biological functions benefit from distinct oscillator properties. Thus, finite developmental processes rely on oscillators that start and stop at specific times, a poorly understood behavior. Here, we have characterized a massive gene expression oscillator comprising > 3,700 genes in Caenorhabditis elegans larvae. We report that oscillations initiate in embryos, arrest transiently after hatching and in response to perturbation, and cease in adults. Experimental observation of the transitions between oscillatory and non‐oscillatory states at high temporal resolution reveals an oscillator operating near a Saddle Node on Invariant Cycle (SNIC) bifurcation. These findings constrain the architecture and mathematical models that can represent this oscillator. They also reveal that oscillator arrests occur reproducibly in a specific phase. Since we find oscillations to be coupled to developmental processes, including molting, this characteristic of SNIC bifurcations endows the oscillator with the potential to halt larval development at defined intervals, and thereby execute a developmental checkpoint function. |
format | Online Article Text |
id | pubmed-7370751 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-73707512020-07-20 Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans Meeuse, Milou WM Hauser, Yannick P Morales Moya, Lucas J Hendriks, Gert‐Jan Eglinger, Jan Bogaarts, Guy Tsiairis, Charisios Großhans, Helge Mol Syst Biol Articles Gene expression oscillators can structure biological events temporally and spatially. Different biological functions benefit from distinct oscillator properties. Thus, finite developmental processes rely on oscillators that start and stop at specific times, a poorly understood behavior. Here, we have characterized a massive gene expression oscillator comprising > 3,700 genes in Caenorhabditis elegans larvae. We report that oscillations initiate in embryos, arrest transiently after hatching and in response to perturbation, and cease in adults. Experimental observation of the transitions between oscillatory and non‐oscillatory states at high temporal resolution reveals an oscillator operating near a Saddle Node on Invariant Cycle (SNIC) bifurcation. These findings constrain the architecture and mathematical models that can represent this oscillator. They also reveal that oscillator arrests occur reproducibly in a specific phase. Since we find oscillations to be coupled to developmental processes, including molting, this characteristic of SNIC bifurcations endows the oscillator with the potential to halt larval development at defined intervals, and thereby execute a developmental checkpoint function. John Wiley and Sons Inc. 2020-07-20 /pmc/articles/PMC7370751/ /pubmed/32687264 http://dx.doi.org/10.15252/msb.20209498 Text en © 2020 The Authors. Published under the terms of the CC BY 4.0 license 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 | Articles Meeuse, Milou WM Hauser, Yannick P Morales Moya, Lucas J Hendriks, Gert‐Jan Eglinger, Jan Bogaarts, Guy Tsiairis, Charisios Großhans, Helge Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans |
title | Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
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title_full | Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
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title_fullStr | Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
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title_full_unstemmed | Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
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title_short | Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
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title_sort | developmental function and state transitions of a gene expression oscillator in caenorhabditis elegans |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7370751/ https://www.ncbi.nlm.nih.gov/pubmed/32687264 http://dx.doi.org/10.15252/msb.20209498 |
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