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bioRxiv · 10.1101/2023.03.11.532086

Centriole Remodeling Evolved into Centriole Degradation in Mouse Sperm

Khanal, S.·Puente, N.·Chandanayaka, R.·Assefa, K. Y.·Nawras, M.·Turner, K.·Back, E. D.·Royfman, A.·Burkett, J.·Cheong, S. H.·Fisher, H. S.·Sindhwani, P.·Gray, J.·Basappa, R. N.·Avidor-Reiss, T.
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Abstract

Centrioles are subcellular organelles found at the cilia base with an evolutionarily conserved structure and a shock absorber-like function. In sperm, centrioles are found at the flagellum base and are essential for embryo development in basal animals. Yet, sperm centrioles have evolved diverse forms, sometimes acting like a transmission system, as in cattle, and sometimes becoming dispensable, as in house mice. How the essential sperm centriole evolved to become dispensable in some organisms is unclear. Here, we test the hypothesis that this transition occurred through a cascade of evolutionary changes to the proteins, structure, and function of sperm centrioles and was possibly driven by sperm competition. We found that the final steps in this cascade are associated with a change in the primary structure of the centriolar luminal protein FAM161A in rodents. This information provides the first insight into the molecular mechanisms and adaptive evolution underlying a major evolutionary transition within the internal structure of the mammalian sperm neck. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=65 SRC="FIGDIR/small/532086v3_ufig1.gif" ALT="Figure 1"> View larger version (24K): org.highwire.dtl.DTLVardef@bdbe1eorg.highwire.dtl.DTLVardef@10cc2b9org.highwire.dtl.DTLVardef@c42734org.highwire.dtl.DTLVardef@1e9c750_HPS_FORMAT_FIGEXP M_FIG C_FIG Highlights- Barrel-shaped centrioles are present in all rodents except members of the Muridae taxonomical family. - The FAM161A sequence evolved selectively in rodents and specifically in a murid subgroup. - The evolution of centriole degradation is correlated with the expression of a novel FAM161A isoform. - The ancestral centriole remodeling program involves elongation followed by redistribution. - The mouse centriole degradation program involves elongation followed by elimination.

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Khanal, S., Puente, N., Chandanayaka, R., Assefa, K. Y., Nawras, M., Turner, K., Back, E. D., Royfman, A., Burkett, J., Cheong, S. H., Fisher, H. S., Sindhwani, P., Gray, J., Basappa, R. N., Avidor-Reiss, T.. 2023-03-11. Centriole Remodeling Evolved into Centriole Degradation in Mouse Sperm. https://doi.org/10.1101/2023.03.11.532086

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