Spermatogenesis is an ongoing differentiation process that occurs in the seminiferous epithelium in the testis in males to produce spermatozoa (sperm) and is sustained by a tissue-specific stem cell termed the “spermatogonial stem cell.”

From: Encyclopedia of Reproduction (Second Edition), 2018

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R. Renkawitz-Pohl, ... M.A. Schäfer, in Comprehensive Molecular Insect Science, 2005

1.4.1 Introduction

Spermatogenesis is a highly specialized process of cellular differentiation resulting in the formation of functional spermatozoa for successful reproduction. In principle, the process of spermatogenesis is well conserved in all sexually proliferating organisms, although the size and shape of the mature sperm vary considerably among different species. Many details are comparable between mammals and Drosophila making the fly a very good model system to study fertility defects. Drosophila germ cells, like those of mammals, are set aside early in embryonic development and migrate through the primordium of the hindgut into the interior of the embryo where they join the somatic parts of the embryonic gonads (review: Zhao and Garbers, 2002). At the end of the third larval instar and the onset of pupariation, the first germ cells enter meiosis (Figure 1).

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Figure 1. Stages of spermatogenesis in testes of late third instar larvae and adult males. (a) Testis anlage of a larva showing the hub and stem cell region at the apex (asterisk), a cyst with spermatogonia (white arrow), and a cyst with primary spermatocytes (black arrowhead). (b) Testis of an adult male showing the apical tip with hub and stem cells (asterisk), spermatogonia (white arrow), spermatocytes (arrowhead), and elongated spermatids (black arrow). (c) The cyst shows synchronous meiotic divisions. (d) The left cyst shows a Nebenkern stage shortly after the second meiotic division. In the phase contrast optics the nucleus (n) appears light, the Nebenkern (nk) dark. The right cyst contains young spermatids with a round nucleus (n) and an elongating flagellum (F). (e) β1-LacZ reporter gene expression in the male reproductive tract (Wβ1K-carrying transgenic line; Buttgereit and Renkawitz-Pohl, 1993). Within the testes (T), stem cells and spermatogonia express β-galactosidase. In addition, β-galactosidase expression is also observed in the vas deferens (V), in accessory glands (G), and in the ejaculatory duct (AD). (f) β2-LacZ reporter gene expression in the male reproductive tract (Michiels et al., 1989).

Spermatogenesis is a continuous process during adult life and, thus, the adult testes contain all stages from stem cells to mature sperm (Figure 1). As in mammals, the germ cells develop in close contact with somatic cells, in this case the cyst cells, which are of mesodermal origin. At the very tip of the testis tube, the so-called hub is formed by somatic support cells (asterisk in Figure 1) to which the germline stem cells (GSCs) and the cyst cell progenitors (somatic stem cells, SSCs) are physically connected. In close contact to the hub, both stem cell types divide asymmetrically depending on the JAK-STAT signaling pathway (see Section for details). One daughter cell remains connected to the hub and maintains stem cell characteristics. The other daughter cell becomes disconnected from the hub and enters the differentiation process. This germ cell, now called spermatogonium, is surrounded by two cyst cells, thus forming a cyst in which the germ cell undergoes four mitotic divisions, meiosis, and sperm morphogenesis until individualization (see Figure 3 for an overview).

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The ultrastructure and cytology of Drosophila melanogaster spermatogenesis has been extensively reviewed by Fuller (1993). This complex differentiation process from round cells to the highly specialized structure of spermatozoa is controlled by a large number of genes (up to 1500) affecting spermatogenesis, which is reflected in the large number of male sterile mutants (reviews: Lindsley and Tokuyasu, 1980; Hackstein et al., 2000). The focus here is on the recent advances in understanding the molecular basis for the dramatic changes in cell morphology during germ cell development starting with the asymmetric division of stem cells into a stem cell and a spermatogonium as the entry point to germ cell differentiation. Control of mitotic proliferation and entry into meiosis are discussed and various aspects of sperm morphogenesis highlighted, such as the formation of the axoneme and the mitochondrial derivative, the Nebenkern. Then the importance of cell interactions during the process is discussed (Figure 4), and finally transcriptional and translational control mechanisms during meiotic prophase, and their relevance for sperm morphogenesis (Figure 3).