Synaptonemal Complex Components Promote Centromere Pairing in Pre-meiotic Germ Cells

Nicolas Christophorou,Thomas Rubin,Jean-René Huynh,R Scott Hawley

doi:10.1371/journal.pgen.1004012

Nicolas Christophorou, Thomas Rubin + Show 2 more

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https://doi.org/10.1371/journal.pgen.1004012

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Abstract

Mitosis and meiosis are two distinct cell division programs. During mitosis, sister chromatids separate, whereas during the first meiotic division, homologous chromosomes pair and then segregate from each other. In most organisms, germ cells do both programs sequentially, as they first amplify through mitosis, before switching to meiosis to produce haploid gametes. Here, we show that autosomal chromosomes are unpaired at their centromeres in Drosophila germline stem cells, and become paired during the following four mitosis of the differentiating daughter cell. Surprisingly, we further demonstrate that components of the central region of the synaptonemal complex are already expressed in the mitotic region of the ovaries, localize close to centromeres, and promote de novo association of centromeres. Our results thus show that meiotic proteins and meiotic organization of centromeres, which are key features to ensure reductional segregation, are laid out in amplifying germ cells, before meiosis has started.

Highlights

In Drosophila females, mitosis and meiosis occur sequentially throughout adult life in two distinct regions of the germarium at the tip of each ovary [1]
Unpaired centromeres in germline stem cells To distinguish the different stages of region 1, we marked the fusome with an antibody against a-spectrin, a membrane skeletal protein, and to visualize centromeres, we used an anti-CID antibody marking the Drosophila homologue of Cenp-A, a histone H3 variant present only in centromeric regions [15] (Figure 1C– E)
We found in germline stem cells (GSCs) and CBs an average of 6 dots of CID (GSCs: 5.960.8, n = 36; CBs: 5.960.8, n = 27), which indicates that centromeres were not all paired (Figure 1F)

Summary

Introduction

In Drosophila females, mitosis and meiosis occur sequentially throughout adult life in two distinct regions of the germarium at the tip of each ovary [1]. In the mitotic zone (called region 1), germline stem cells (GSCs) generate a precursor cell called a cystoblast (CB), which undergoes exactly four mitoses to produce a germline cyst made of 16 cells (Figure 1A). These mitoses are not complete and all 16 sister cells remain connected through ring canals and by an organelle called the fusome, which links all cells. Cysts enter region 2 and all 16 cells start meiosis [3]. During differentiation in region 2, only one cell per cyst, remains in meiosis, while the 15 others exit meiosis and endoreplicate their DNA [4]

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