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.