Centriole elimination duringC. elegansoogenesis initiates with loss of the central tube protein SAS-1

Abstract

Centrioles are lost during oogenesis in most metazoans, 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 inC. 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. Moreover, we find that neither Polo-like kinases nor the PCM, which modulate oogenesis centriole elimination inDrosophila, do so inC. elegans. Furthermore, we demonstrate that the central tube protein SAS-1 normally departs first from the organelle, which loses integrity earlier insas-1mutants. Overall, our work provides novel mechanistic insights regarding the fundamental process of oogenesis centriole elimination.

Towards understanding centriole elimination

“…Similarly, if sas-1 function is lacking maternally, centrioles form initially but disintegrate during embryogenesis. Recently, a role for SAS-1 was also proposed during oogenesis centriole elimination, whereby SAS-1 disappears from centrioles earlier than other components, concomitant with loss of the central tube, to which SAS-1 localizes [78]. Moreover, in sas-1(t1521ts) mutant worms, centriolar microtubule and SAS-4 signals decay faster than normal, along with premature loss of organelle integrity [78].…”

“…In a first mode occurring for instance in X. laevis , M. musculus and H. sapiens , as well as in C. elegans and Drosophila , centrioles are eliminated during the prolonged prophase of meiosis I, resulting in acentriolar meiotic spindles [75,76] (reviewed by [77]) (figure 2 b ). Recent correlative light electron microscopy (CLEM) analysis in C. elegans revealed that centrioles lose the so-called central tube in late pachytene, which is followed by the lack of a recognizable centriole at the beginning of diplotene [78]. In Drosophila , the maturing oocyte is first endowed with a cluster containing many centrioles contributed by the 15 supporting nurse cells [79,80].…”

“…As mentioned above, ultrastructural analysis of C. elegans oogenesis centriole elimination revealed that the initial change in organelle architecture is the loss, in late pachytene, of the central tube, which is located just inside the centriolar microtubule wall [78]. Merely remnants of centriolar microtubules are observed in early diplotene, approximately 4 h thereafter [78]. During Drosophila oogenesis, centriolar protein foci diminish in intensity starting at stages 9/12, and are completely undetectable at stage 14 [81], corresponding to approximately one day of development (reviewed by [157]).…”

“…Likewise, in C. elegans , centrioles are eliminated from the ciliary base despite the presence of PCM components [130,131]. Moreover, PLK-1 is absent from centriolar foci in the L1 larvae and from the germline, except in the mitotic zone, whereas depletion of PLK-1, PLK-2 and PLK-3 does not lead to precocious elimination during oogenesis [78,125,208]. Regardless, it will be interesting to discover what governs Polo removal from centrioles in Drosophila , and investigate the consequences of such removal.…”

“…[77]) (figure 2b). Recent correlative light electron microscopy (CLEM) analysis in C. elegans revealed that centrioles lose the so-called central tube in late pachytene, which is followed by the lack of a recognizable centriole at the beginning of diplotene [78]. In Drosophila, the maturing oocyte is first endowed with a cluster containing many centrioles contributed by the 15 supporting nurse cells [79,80].…”