The 3D architecture and molecular foundations of de novo centriole assembly via bicentrioles.


Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
11 10 2021
Historique:
received: 07 01 2021
revised: 01 06 2021
accepted: 26 07 2021
pubmed: 26 8 2021
medline: 9 4 2022
entrez: 25 8 2021
Statut: ppublish

Résumé

Centrioles are structurally conserved organelles, composing both centrosomes and cilia. In animal cycling cells, centrioles often form through a highly characterized process termed canonical duplication. However, a large diversity of eukaryotes assemble centrioles de novo through uncharacterized pathways. This unexplored diversity is key to understanding centriole assembly mechanisms and how they evolved to assist specific cellular functions. Here, we show that, during spermatogenesis of the bryophyte Physcomitrium patens, centrioles are born as a co-axially oriented centriole pair united by a cartwheel. Interestingly, we observe that these centrioles are twisted in opposite orientations. Microtubules emanate from the bicentrioles, which localize to the spindle poles during cell division. After their separation, the two resulting sister centrioles mature asymmetrically, elongating specific microtubule triplets and a naked cartwheel. Subsequently, two motile cilia are assembled that appear to alternate between different motility patterns. We further show that centriolar components SAS6, Bld10, and POC1, which are conserved across eukaryotes, are expressed during spermatogenesis and required for this de novo biogenesis pathway. Our work supports a scenario where centriole biogenesis, while driven by conserved molecular modules, is more diverse than previously thought.

Identifiants

pubmed: 34433076
pii: S0960-9822(21)01053-8
doi: 10.1016/j.cub.2021.07.063
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4340-4353.e7

Informations de copyright

Copyright © 2021. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Sónia Gomes Pereira (S)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal. Electronic address: sagp.19@gmail.com.

Ana Laura Sousa (AL)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal.

Catarina Nabais (C)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal.

Tiago Paixão (T)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal.

Alexander J Holmes (AJ)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal.

Martin Schorb (M)

Electron Microscopy Core Facility, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.

Gohta Goshima (G)

Sugashima Marine Biological Laboratory, Graduate School of Science, Nagoya University, Sugashima, 429-63, Toba 517-0004, Japan; Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8602, Japan.

Erin M Tranfield (EM)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal.

Jörg D Becker (JD)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal; Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal. Electronic address: jbecker@itqb.unl.pt.

Mónica Bettencourt-Dias (M)

Instituto Gulbenkian de Ciência (IGC), Rua da Quinta Grande, 6, 2780-156 Oeiras, Portugal. Electronic address: mdias@igc.gulbenkian.pt.

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Classifications MeSH