Formation of germ-line cysts with a central cytoplasmic core is accompanied by specific orientation of mitotic spindles and partitioning of existing intercellular bridges

Abstract

Animal germ cells tend to form clonal groups known as clusters or cysts. Germ cells within the cyst (cystocytes) are interconnected by intercellular bridges and thus constitute a syncytium. Our knowledge of the mechanisms that control the formation of germ-cell clusters comes from extensive studies carried on model organisms (Drosophila, Xenopus). Germ-cell clusters have also been described in worms (annelids, flat worms and nematodes), although their architecture differs significantly from that known in arthropods or vertebrates. Their peculiar feature is the presence of a central anucleate cytoplasmic core (cytophore, rachis) around which the cystocytes are clustered. Each cystocyte in such a cluster always has one intercellular bridge connecting it to the central cytoplasmic core. The way that such clusters are formed has remained a riddle for decades. By means of light, fluorescence and electron microscopy, we have analysed the formation and architecture of cystocyte clusters during early stages of spermatogenesis and oogenesis in a few species belonging to clitellate (oligochaetous) annelids. Our data indicate that the appearance of germ cells connected via a central cytophore is accompanied by a specific orientation of the mitotic spindles during cystocyte divisions. Spindle long axes are always oriented tangentially to the surface of the cytophore. In consequence, cystocytes divide perpendicularly to the plane of the existing intercellular bridge. Towards the final stages of cytokinesis, the contractile ring of the cleavage furrow merges with the rim of the intercellular bridge that connects the dividing cystocyte with the cytophore and forces partition of the existing bridge into two new bridges.

A Sterile 20 Family Kinase and Its Co-factor CCM-3 Regulate Contractile Ring Proteins on Germline Intercellular Bridges

“…Unlike organisms such as Drosophila where each intercellular bridge arises from a unique cytokinesis failure [1], the syncytial organization of the C. elegans germline is thought to be achieved by the repeated inheritance of an intercellular bridge generated by one failed cytokinesis early in germline development. This first intercellular bridge is propagated to subsequent germ cells via oriented divisions, analogous to the inheritance of the apical domain during epithelial divisions [13]. …”

Description of ovary organization and oogenesis in a phreodrilid clitellate

“…In annelids, meroistic germ-line cysts were found in some groups of Polychaeta (for more info see Eckelbarger, 1983;Brubacher & Huebner, 2011) and in almost all Clitellata studied to date (Świątek et al, 2009, 2018Urbisz et al, 2017;Świątek & Urbisz, 2019).…”

C. elegans germ cells divide and differentiate along a folded epithelium

“…This 556 mechanism differs from our observations in germ cells of L4 larvae and adults, in which the ring 557 channel bifurcates during division ( Figure 3F). This latter mechanism is reminiscent of primordial 558 germ cell formation in Drosophila (Cinalli and Lehmann, 2013) and is strikingly similar to germ 559 cell division in clitellate annelids (earthworms and leeches) (Swiatek et al, 2009). Germ cells in 560 clitellate annelids connect to a shared cytoplasmic core (Urbisz et al, 2015), and ring channels in 561 this taxon bifurcate during division by being 'pinched' in two by the cytokinetic ring (as shown by 562 transmission electron microscopy in Swiatek et al, 2009).…”