yuri gagarinis required for actin, tubulin and basal body functions inDrosophilaspermatogenesis

Abstract

A unique feature of the genus Drosophila is the formation of unusually long sperm tails. Sperm lengths of millimeters are common within this group, with the 1.8 mm sperm of D. melanogaster being fairly typical. This marked expansion in sperm length reflects an unusual aspect of spermatogenesis in these organisms: in contrast to other species in which an intraflagellar transport system is used for growth of the sperm flagellum (Scholey, 2006), Drosophila sperm axonemes are assembled in syncytial cysts by a mechanism that does not require, and is not limited by, this system (Han et al., 2003;Sarpal et al., 2003). This unusual sperm axoneme development and the resulting expansion of sperm tail length have led to distinctive features of spermatogenesis not found in other species. In D. bifurca, a special 'sperm roller' has evolved to package its 6-centimeter-long gametes (Joly et al., 2003). In D. melanogaster, a highly evolved individualization process that generates 64 individual sperm from an elongate cyst containing 64 syncytial spermatids has been identified and studied (Noguchi and Miller, 2003;Tokuyasu et al., 1972a). The distinctive molecular mechanisms needed for this process include a motile filamentous actin system (the investment, or actin, cones) that traverses the entire length of the sperm tails, removing excess cytoplasm and investing each sperm in its own plasma membrane. A specialized microtubulerich structure (the dense complex) is also associated with the sperm nuclei and functions to position the basal body and also possibly to strengthen the nuclei as they undergo extreme condensation (A. D. Tates, Cytodifferentiation during spermatogenesis in Drosophila melanogaster, PhD thesis, Rijksuniversiteit Leiden, The Netherlands, 1971) (Tokuyasu, 1974).We have identified a locus, yuri gagarin (yuri), that we show here has multiple roles in the generation of elongate individualized sperm. The gene is only highly conserved in the genus Drosophila, suggesting specialized roles in these organisms. Interestingly, yuri was initially identified through its function in another specialized organ system of insects and arthropods: the chordotonal organs. These are complex mechanosensory structures with roles in proprioception and graviperception. The first mutation at the locus, yuri c263 , was identified in a screen for mutants affecting gravitaxis. Altered gravitaxis was shown to result from perturbed expression of yuri in subsets of chordotonal neurons (Armstrong et al., 2006). The molecular functions of the locus identified here suggest that yuri mediates specialized actin-and microtubule-related activities in Drosophila tissues. ResultsThe yuri locus in D. melanogaster and other Drosophilids In addition to the cDNA (GH14032) encoding a ~30 kDa protein that we used previously (Armstrong et al., 2006), we identified 11 further yuri ESTs/cDNAs from adult testis, ovary, S2 cells and embryos through FlyBase. Sequencing of these new cDNAs established that three major transcript classes are generated from yuri (Fig...

A Proximal Centriole-Like Structure Is Present in Drosophila Spermatids and Can Serve as a Model to Study Centriole Duplication

“…Although no direct demonstration has been done using immuno-EM on g-tubulin during spermatogenesis, g-tubulin staining shows a remarkably close correlation with the morphogenesis of CA, therefore it is accepted that it most likely represents the centriolar adjunct (Wilson et al 1997;Callaini et al 1999;Baker et al 2004;Texada et al 2008). In early spermatids, g-tubulin labels the vicinity of the giant centriole along most of its length ( Figure 2C).…”

TheDrosophilaSUN protein Spag4 cooperates with the coiled-coil protein Yuri Gagarin to maintain association of the basal body and spermatid nucleus

“…Instead, we have shown that the coiled-coil cytoplasmic protein Yuri Gagarin (Armstrong et al, 2006;Texada et al, 2008) is an essential component of the Spag4-BB anchoring mechanism, and that regulation of dynein-dynactin localization by Spag4 has a role in the process.…”

“…) and for Yuri nuclear localization (Texada et al, 2008). yuri is a complex locus encoding three major classes of ubiquitously expressed isoforms.…”

“…Yuri localization was not determined during these early stages previously (Texada et al, 2008), and was thus investigated as part of this work. We discovered that although Yuri was present on the primary spermatocyte NEs in some spermatocyte cysts (Fig.…”

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

“…4B,C). This phenotype is reminiscent of mutants in the testis-specific proteasome subunit Prosα6T (Zhong and Belote 2007) or yuri (Texada et al 2008).…”