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. 2022 Dec;131(4):193-205.
doi: 10.1007/s00412-022-00777-0. Epub 2022 Aug 12.

Time to match; when do homologous chromosomes become closer?

M Solé  1 , J Blanco #  1 , D Gil  2 , O Valero  3 , B Cárdenas  1 , G Fonseka  4 , E Anton  1 , Á Pascual  1 , R Frodsham  4 , F Vidal  1 , Z Sarrate #  5
Affiliations

Time to match; when do homologous chromosomes become closer?

M Solé et al. Chromosoma. 2022 Dec.

Abstract

In most eukaryotes, pairing of homologous chromosomes is an essential feature of meiosis that ensures homologous recombination and segregation. However, when the pairing process begins, it is still under investigation. Contrasting data exists in Mus musculus, since both leptotene DSB-dependent and preleptotene DSB-independent mechanisms have been described. To unravel this contention, we examined homologous pairing in pre-meiotic and meiotic Mus musculus cells using a three-dimensional fluorescence in situ hybridization-based protocol, which enables the analysis of the entire karyotype using DNA painting probes. Our data establishes in an unambiguously manner that 73.83% of homologous chromosomes are already paired at premeiotic stages (spermatogonia-early preleptotene spermatocytes). The percentage of paired homologous chromosomes increases to 84.60% at mid-preleptotene-zygotene stage, reaching 100% at pachytene stage. Importantly, our results demonstrate a high percentage of homologous pairing observed before the onset of meiosis; this pairing does not occur randomly, as the percentage was higher than that observed in somatic cells (19.47%) and between nonhomologous chromosomes (41.1%). Finally, we have also observed that premeiotic homologous pairing is asynchronous and independent of the chromosome size, GC content, or presence of NOR regions.

Keywords: Chromosome territories; FISH; Homologous chromosomes; Homologous pairing; Meiosis; Premeiotic cells.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
3D-FISH confocal image captures of each round of hybridization (a, b, and c) for four different mice germ cell nuclei (spermatogonia-early preleptotene, mid-preleptotene-zygotene, pachytene, and round spermatids). Different combinations of three chromosomes (Chr.) displayed in FITC, Texas Red, or Aqua DEAC are observed in each nucleus. For each hybridization round are shown maximum intensity projections of confocal serial sections and 3D composite reconstructions using Imaris 9.3 software in both RGB merge and split channels (to view the planes’ sequence of the maximum intensity confocal images and the 3D composite reconstruction of premeiotic cells, see Online resource 1)
Fig. 2
Fig. 2
Graphical representation of the labeling pattern of synaptonemal complex protein 3 (SYCP3), testicle-specific histone 1 (H1T), and a testis-specific nuclear protein known as TRA98 during the spermatogenesis process, along with some relevant meiotic events that occur in primary spermatocytes. The colored bars indicate the presence of each protein: SYCP3 (dark green bar), H1T (red bar), and TRA98 (light green bar), throughout spermatogenesis (the top grey bar)
Fig. 3
Fig. 3
Percentage of homologous chromosome pairing observed in different stages of spermatogenesis: (I) spermatogonia-early preleptotene spermatocytes I, (II) spermatocytes I at mid preleptotene-zygotene stages, (III) spermatocytes I at pachytene stage, and (IV) round spermatids, as well as in lymphocytes (Lym.). In round spermatids (IV), the paired value corresponds to cells with one signal per chromosome
Fig. 4
Fig. 4
Percentage of homologous chromosomes occupying the same territory (one signal) or occupying different territories (two signals) for each chromosome in mice lymphocytes
Fig. 5
Fig. 5
Schematic representation of the dynamics of homologous chromosome pairing and heterologous association from spermatogonia to pachytene spermatocytes of Mus musculus. There are represented three different homologous chromosomes in yellow, garnet, and blue colors. The homologous pairing is indicated by a red arrowhead and the heterologous association by a blue arrowhead. The nuclear background color indicates the presence of TRA98 (green) and H1T (red). The SYCP3 protein is represented in green dotted or continuous filaments
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