Distribution and morphological changes of the Golgi apparatus during Drosophila spermatogenesis

Abstract

In spermatogenesis, the Golgi apparatus is important for the formation of the acrosome, which is a sperm-specific organelle essential for fertilization. Comprehensive examinations of the spatiotemporal distribution and morphological characterizations of the Golgi in various cells during spermatogenesis are necessary for functional analyses and mutant screenings in the model eukaryote Drosophila. Here, we examined the distribution and morphology of the Golgi during Drosophila spermatogenesis with immunofluorescence and electron microscopy. In pre-meiotic germ cells, the Golgi apparatuses were distributed evenly in the cytoplasm. In contrast, they were located exclusively in two regions near the poles during the meiotic metaphase, where they were segregated prior to the chromosomes. In cells in anaphase to telophase, the Golgi were predominantly left behind in the equatorial region between the separating daughter nuclei. After completion of meiosis, the dispersed Golgi were assembled at the apical side of the spermatid nucleus to form the acrosome. Further investigation of the Golgi distribution in b2-tubulin mutants showed aberrant and uneven distributions of the Golgi among sister cells in the meiotic spermatocytes and in the post-meiotic spermatids. At the ultrastructural level, the Golgi apparatus in pre-meiotic spermatocytes comprised a pair of stacks. The two stacks were situated adjacent to each other, as if they had duplicated before entering into meiotic division. These results highlight the dynamic nature of the Golgi during spermatogenesis and provide a framework for analyzing the correlations between the dynamics of the Golgi and its function in sperm development.

The role of acroblast formation duringDrosophilaspermatogenesis

“…2C-E). Early in the development process, in primary spermatocytes, the RFP stained Golgi is randomly distributed throughout the cytoplasm, similarly to the distribution found for GM130 and other medial/ trans Golgi markers (Yasuno et al, 2013) (Fig. 2C).…”

“…Yet, the acroblast is unusual in Drosophila, as it forms a ribbon as opposed to the scattered stacks typical for Golgi architecture in other fruit fly cells (Kondylis and Rabouille, 2009). The molecular determinants of acroblast formation and its breakdown upon acrosome formation are not very well understood, but the Golgi architecture leading to acrosome formation has been recently documented (Yasuno et al, 2013). After meiosis the Golgi is organized around the nucleus and participates in the formation of the acroblast (Fig.…”

“…It is therefore often difficult to tease out direct effects on Golgi architecture from secondary effects due to delays in spermatogenesis and associated defects in polarization. Such factors include microtubules (Yasuno et al, 2013), the phosphatidylinositol transfer protein Giotto (Giansanti et al, 2006), the small GTPase Rab11 (Giansanti et al, 2007), the TRAPP II complex (Robinett et al, 2009), as well as the Cog5 and Cog7 subunits of COG (Belloni et al, 2012; Farkas et al, 2003). …”

Myt1 inhibition of Cyclin A/Cdk1 is essential for fusome integrity and premeiotic centriole engagement inDrosophilaspermatocytes

“…We quantified these data by counting Lva-labeled Golgi stacks from merged, deconvolved Z -stack images and observed similar numbers in the controls (average = 16, n = 74, SD = 2.8) and myt1 mutants (average = 15, n = 85, SD = 3.2). Golgi stacks disassemble for the meiotic divisions before reassembling again to organize the acroblast ( Belloni et al ., 2012 ; Yasuno et al ., 2013 ). We observed similar Golgi dynamics at these stages in both the controls and the myt1 mutant spermatocytes (Supplemental Figure S2C).…”

The Organization of the Golgi Structures during Drosophila Male Meiosis Requires the Citrate Lyase ATPCL

“…Just prior to and during the nuclear elongation phase of spermatogenesis, the Golgi stacks condense and assemble in a ribbon-like structure at the apical side of the spermatid nucleus to form the acroblast. This unique Golgi assemblage is essential for fertilization since it is required to organize the secretory pathway in the highly polarized spermatids [ 12 , 13 ] and for the subsequent acrosome formation, nuclear elongation and therefore sperm maturation. Despite several Golgi resident proteins having been detected and localized in Drosophila male meiosis, how Golgi-derived vesicles are organized throughout spermatogenesis has not been fully addressed.…”