9-fold symmetry is not essential for centriole elongation and formation of new centriole-like structures
Abstract
As daughter centrioles assemble during G2, they recruit conserved Ana3/RTTN followed by its partner Rcd4/PPP1R35. Together, this contributes to the subsequent recruitment of Ana1/CEP295, required for the centriole’s conversion to a centrosome. Here, we show that Rcd4/PPP1R35 is also required to maintain 9-fold centriole symmetry in the Drosophila male germline; its absence causes microtubule triplets to disperse into a reduced number of doublet or singlet microtubules. rcd4-null mutant spermatocytes display skinny centrioles that elongate normally and localize centriolar components correctly. Mutant spermatocytes also have centrioles of normal girth that splay at their proximal ends when induced to elongate by Ana1 overexpression. Skinny and splayed spermatid centrioles can still recruit a proximal centriole-like (PCL) structure marking a capability to initiate features of centriole duplication in developing sperm. Thus, stable 9-fold symmetry of microtubule triplets is not essential for centriole growth, correct longitudinal association of centriole components, and aspects of centriole duplication.
Copyright and License
© The Author(s) 2024. 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, visit http://creativecommons.org/licenses/by/4.0/.
Acknowledgement
We are grateful to Dr. Andres Collazo and Dr. Giada Spigolon of the Biological Imaging Facility at Caltech for their support and to Caltech Beckman Institute Cryo-EM Facility for the use of the Tecnai electron microscope. We are thankful to Paula Coelho, Levente Kovacs, Agota Nagy, and Sarolta Szentes for many discussions. This work was supported by a grant from the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under award no. R01NS113930.
Contributions
P.P contributed to the conception of the study, designed experiments, performed all Drosophila genetics and fluorescence microscopy studies, carried out data analysis and wrote the manuscript; M.S.L prepared samples for and performed all electron tomography studies; D.M.G contributed to the conception and supervision of the study, and in writing the manuscript.
Data Availability
Conflict of Interest
The authors declare no competing interests.
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Additional details
- PMCID
- PMC11127918
- National Institutes of Health
- R01NS113930
- Caltech groups
- Division of Biology and Biological Engineering