Centriole elimination during Caenorhabditis elegans oogenesis initiates with loss of the central tube protein SAS‐1

Abstract

In most metazoans, centrioles are lost during oogenesis, ensuring that the zygote is endowed with the correct number of two centrioles, which are paternally contributed. How centriole architecture is dismantled during oogenesis is not understood. Here, we analyze with unprecedent detail the ultrastructural and molecular changes during oogenesis centriole elimination in Caenorhabditis elegans. Centriole elimination begins with loss of the so‐called central tube and organelle widening, followed by microtubule disassembly. The resulting cluster of centriolar proteins then disappears gradually, usually moving in a microtubule‐ and dynein‐dependent manner to the plasma membrane. Our analysis indicates that neither Polo‐like kinases nor the PCM, which modulate oogenesis centriole elimination in Drosophila, do so in C. elegans. Furthermore, we demonstrate that the central tube protein SAS‐1 normally departs initially from the organelle, which loses integrity earlier in sas‐1 mutants. Overall, our work provides novel mechanistic insights regarding the fundamental process of oogenesis centriole elimination.

A delta-tubulin/epsilon-tubulin/Ted protein complex is required for centriole architecture

“…Using expansion microscopy, we find that centriole loss is correlated with loss of the SASS6 cartwheel in mitosis. In this regard, mutant centrioles with singlet microtubules resemble centriole loss within C. elegans oocytes, in which an analogous structure to the cartwheel named the central tube is lost prior to centriole widening and subsequent loss of the centriolar microtubules (Pierron et al, 2023). In addition, centriole loss in our mutant cells occurs through a stereotyped progression of architectural changes in mitosis, starting with centriole over elongation in prometaphase and culminating with centriole fragmentation and loss.…”

“…Centriole loss is not unique to centrioles lacking compound microtubules: mammalian cells engineered to lack CEP295 also form centrioles that are lost through the cell cycle, due to an inability to undergo centriole to centrosome conversion (Izquierdo et al, 2014). Similarly, in Drosophila oocytes, down-regulation of Polo kinase and pericentriolar material triggers centriole elimination (Pimenta-Marques et al, 2016). We find that CEP295 is properly localized in mutant centrioles with singlet microtubules, indicating that centriole loss in this context may be independent of centriole to centrosome conversion and pericentriolar material recruitment.…”