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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...

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Autores principales: Meeuse, Milou WM, Hauser, Yannick P, Morales Moya, Lucas J, Hendriks, Gert‐Jan, Eglinger, Jan, Bogaarts, Guy, Tsiairis, Charisios, Großhans, Helge
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
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.
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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
title_full Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
title_fullStr Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
title_full_unstemmed Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
title_short Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans
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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