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Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development

BACKGROUND: After embryonic development, Caenorhabditis elegans progress through for larval stages, each of them finishing with molting. The repetitive nature of C. elegans postembryonic development is considered an oscillatory process, a concept that has gained traction from regulation by a circadi...

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Autores principales: Mata-Cabana, Alejandro, Romero-Expósito, Francisco Javier, Geibel, Mirjam, Piubeli, Francine Amaral, Merrow, Martha, Olmedo, María
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9047341/
https://www.ncbi.nlm.nih.gov/pubmed/35477393
http://dx.doi.org/10.1186/s12915-022-01295-2
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author Mata-Cabana, Alejandro
Romero-Expósito, Francisco Javier
Geibel, Mirjam
Piubeli, Francine Amaral
Merrow, Martha
Olmedo, María
author_facet Mata-Cabana, Alejandro
Romero-Expósito, Francisco Javier
Geibel, Mirjam
Piubeli, Francine Amaral
Merrow, Martha
Olmedo, María
author_sort Mata-Cabana, Alejandro
collection PubMed
description BACKGROUND: After embryonic development, Caenorhabditis elegans progress through for larval stages, each of them finishing with molting. The repetitive nature of C. elegans postembryonic development is considered an oscillatory process, a concept that has gained traction from regulation by a circadian clock gene homologue. Nevertheless, each larval stage has a defined duration and entails specific events. Since the overall duration of development is controlled by numerous factors, we have asked whether different rate-limiting interventions impact all stages equally. RESULTS: We have measured the duration of each stage of development for over 2500 larvae, under varied environmental conditions known to alter overall developmental rate. We applied changes in temperature and in the quantity and quality of nutrition and analysed the effect of genetically reduced insulin signalling. Our results show that the distinct developmental stages respond differently to these perturbations. The changes in the duration of specific larval stages seem to depend on stage-specific events. Furthermore, our high-resolution measurement of the effect of temperature on the stage-specific duration of development has unveiled novel features of temperature dependence in C. elegans postembryonic development. CONCLUSIONS: Altogether, our results show that multiple factors fine tune developmental timing, impacting larval stages independently. Further understanding of the regulation of this process will allow modelling the mechanisms that control developmental timing. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01295-2.
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spelling pubmed-90473412022-04-29 Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development Mata-Cabana, Alejandro Romero-Expósito, Francisco Javier Geibel, Mirjam Piubeli, Francine Amaral Merrow, Martha Olmedo, María BMC Biol Research Article BACKGROUND: After embryonic development, Caenorhabditis elegans progress through for larval stages, each of them finishing with molting. The repetitive nature of C. elegans postembryonic development is considered an oscillatory process, a concept that has gained traction from regulation by a circadian clock gene homologue. Nevertheless, each larval stage has a defined duration and entails specific events. Since the overall duration of development is controlled by numerous factors, we have asked whether different rate-limiting interventions impact all stages equally. RESULTS: We have measured the duration of each stage of development for over 2500 larvae, under varied environmental conditions known to alter overall developmental rate. We applied changes in temperature and in the quantity and quality of nutrition and analysed the effect of genetically reduced insulin signalling. Our results show that the distinct developmental stages respond differently to these perturbations. The changes in the duration of specific larval stages seem to depend on stage-specific events. Furthermore, our high-resolution measurement of the effect of temperature on the stage-specific duration of development has unveiled novel features of temperature dependence in C. elegans postembryonic development. CONCLUSIONS: Altogether, our results show that multiple factors fine tune developmental timing, impacting larval stages independently. Further understanding of the regulation of this process will allow modelling the mechanisms that control developmental timing. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01295-2. BioMed Central 2022-04-27 /pmc/articles/PMC9047341/ /pubmed/35477393 http://dx.doi.org/10.1186/s12915-022-01295-2 Text en © The Author(s) 2022 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, visithttp://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Mata-Cabana, Alejandro
Romero-Expósito, Francisco Javier
Geibel, Mirjam
Piubeli, Francine Amaral
Merrow, Martha
Olmedo, María
Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development
title Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development
title_full Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development
title_fullStr Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development
title_full_unstemmed Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development
title_short Deviations from temporal scaling support a stage-specific regulation for C. elegans postembryonic development
title_sort deviations from temporal scaling support a stage-specific regulation for c. elegans postembryonic development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9047341/
https://www.ncbi.nlm.nih.gov/pubmed/35477393
http://dx.doi.org/10.1186/s12915-022-01295-2
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