Cargando…

Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae

The centriole is a minute cylindrical organelle present in a wide range of eukaryotic species. Most centrioles have a signature ninefold radial symmetry of microtubules that is imparted to the axonemes of the cilia and flagella they template, with nine centriolar microtubule doublets growing into ni...

Descripción completa

Detalles Bibliográficos
Autores principales: Bezler, Alexandra, Woglar, Alexander, Schneider, Fabian, Douma, Friso, Bürgy, Léo, Busso, Coralie, Gönczy, Pierre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635282/
https://www.ncbi.nlm.nih.gov/pubmed/35544302
http://dx.doi.org/10.1091/mbc.E22-04-0123
_version_ 1784824679854243840
author Bezler, Alexandra
Woglar, Alexander
Schneider, Fabian
Douma, Friso
Bürgy, Léo
Busso, Coralie
Gönczy, Pierre
author_facet Bezler, Alexandra
Woglar, Alexander
Schneider, Fabian
Douma, Friso
Bürgy, Léo
Busso, Coralie
Gönczy, Pierre
author_sort Bezler, Alexandra
collection PubMed
description The centriole is a minute cylindrical organelle present in a wide range of eukaryotic species. Most centrioles have a signature ninefold radial symmetry of microtubules that is imparted to the axonemes of the cilia and flagella they template, with nine centriolar microtubule doublets growing into nine axonemal microtubule doublets. There are exceptions to the ninefold symmetrical arrangement of axonemal microtubules in some species, with lower or higher fold symmetries. In the few cases where this has been examined, such alterations in axonemal symmetries are grounded in similar alterations in centriolar symmetries. Here, we examine the question of microtubule number continuity between centriole and axoneme in flagellated gametes of the gregarine Lecudina tuzetae, which have been reported to exhibit a sixfold radial symmetry of axonemal microtubules. We used time-lapse differential interference microscopy to identify the stage at which flagellated gametes are present. Thereafter, using electron microscopy and ultrastructure-expansion microscopy coupled to stimulated emission depletion superresolution imaging, we uncover that a six- or fivefold radial symmetry in the axoneme is accompanied by an eightfold radial symmetry in the centriole. We conclude that the transition between centriolar and axonemal microtubules can be characterized by unexpected plasticity.
format Online
Article
Text
id pubmed-9635282
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher The American Society for Cell Biology
record_format MEDLINE/PubMed
spelling pubmed-96352822022-11-07 Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae Bezler, Alexandra Woglar, Alexander Schneider, Fabian Douma, Friso Bürgy, Léo Busso, Coralie Gönczy, Pierre Mol Biol Cell Articles The centriole is a minute cylindrical organelle present in a wide range of eukaryotic species. Most centrioles have a signature ninefold radial symmetry of microtubules that is imparted to the axonemes of the cilia and flagella they template, with nine centriolar microtubule doublets growing into nine axonemal microtubule doublets. There are exceptions to the ninefold symmetrical arrangement of axonemal microtubules in some species, with lower or higher fold symmetries. In the few cases where this has been examined, such alterations in axonemal symmetries are grounded in similar alterations in centriolar symmetries. Here, we examine the question of microtubule number continuity between centriole and axoneme in flagellated gametes of the gregarine Lecudina tuzetae, which have been reported to exhibit a sixfold radial symmetry of axonemal microtubules. We used time-lapse differential interference microscopy to identify the stage at which flagellated gametes are present. Thereafter, using electron microscopy and ultrastructure-expansion microscopy coupled to stimulated emission depletion superresolution imaging, we uncover that a six- or fivefold radial symmetry in the axoneme is accompanied by an eightfold radial symmetry in the centriole. We conclude that the transition between centriolar and axonemal microtubules can be characterized by unexpected plasticity. The American Society for Cell Biology 2022-06-23 /pmc/articles/PMC9635282/ /pubmed/35544302 http://dx.doi.org/10.1091/mbc.E22-04-0123 Text en © 2022 Bezler et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial-Share Alike 4.0 International Creative Commons License.
spellingShingle Articles
Bezler, Alexandra
Woglar, Alexander
Schneider, Fabian
Douma, Friso
Bürgy, Léo
Busso, Coralie
Gönczy, Pierre
Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae
title Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae
title_full Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae
title_fullStr Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae
title_full_unstemmed Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae
title_short Atypical and distinct microtubule radial symmetries in the centriole and the axoneme of Lecudina tuzetae
title_sort atypical and distinct microtubule radial symmetries in the centriole and the axoneme of lecudina tuzetae
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635282/
https://www.ncbi.nlm.nih.gov/pubmed/35544302
http://dx.doi.org/10.1091/mbc.E22-04-0123
work_keys_str_mv AT bezleralexandra atypicalanddistinctmicrotubuleradialsymmetriesinthecentrioleandtheaxonemeoflecudinatuzetae
AT woglaralexander atypicalanddistinctmicrotubuleradialsymmetriesinthecentrioleandtheaxonemeoflecudinatuzetae
AT schneiderfabian atypicalanddistinctmicrotubuleradialsymmetriesinthecentrioleandtheaxonemeoflecudinatuzetae
AT doumafriso atypicalanddistinctmicrotubuleradialsymmetriesinthecentrioleandtheaxonemeoflecudinatuzetae
AT burgyleo atypicalanddistinctmicrotubuleradialsymmetriesinthecentrioleandtheaxonemeoflecudinatuzetae
AT bussocoralie atypicalanddistinctmicrotubuleradialsymmetriesinthecentrioleandtheaxonemeoflecudinatuzetae
AT gonczypierre atypicalanddistinctmicrotubuleradialsymmetriesinthecentrioleandtheaxonemeoflecudinatuzetae