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. image Paternal contribution of centrioles ensures centriole homeostasis in zygotes, but how maternal centrioles are lost in metazoans is unclear. Detailed ultrastructural analyses of centriole elimination during worm oogenesis show that departure of the central tube protein SAS‐1 marks the onset of organelle disassembly. Oogenesis centriole elimination in C. elegans occurs in two steps. Loss of ultrastructural integrity precedes clearance of centriolar protein cluster. Central tube removal and organelle widening mark the onset of centriole elimination. The central tube protein SAS‐1 is required for centriole stability during oogenesis.