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


Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
27 04 2022
Historique:
received: 26 07 2021
accepted: 12 04 2022
entrez: 28 4 2022
pubmed: 29 4 2022
medline: 30 4 2022
Statut: epublish

Résumé

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. 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. 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.

Sections du résumé

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.

Identifiants

pubmed: 35477393
doi: 10.1186/s12915-022-01295-2
pii: 10.1186/s12915-022-01295-2
pmc: PMC9047341
doi:

Substances chimiques

Caenorhabditis elegans Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

94

Subventions

Organisme : NIH HHS
ID : P40 OD010440
Pays : United States

Informations de copyright

© 2022. The Author(s).

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Auteurs

Alejandro Mata-Cabana (A)

Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Avenida Reina Mercedes s/n, 41012, Seville, Spain.

Francisco Javier Romero-Expósito (FJ)

Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Avenida Reina Mercedes s/n, 41012, Seville, Spain.

Mirjam Geibel (M)

Faculty of Medicine, Institute of Medical Psychology, LMU Munich, Goethestrasse 31, 80336, Munich, Germany.

Francine Amaral Piubeli (FA)

Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Sevilla, Profesor García González, 41012, Seville, Spain.

Martha Merrow (M)

Faculty of Medicine, Institute of Medical Psychology, LMU Munich, Goethestrasse 31, 80336, Munich, Germany.

María Olmedo (M)

Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Avenida Reina Mercedes s/n, 41012, Seville, Spain. mariaolmedo@us.es.

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Classifications MeSH