Centromere and telomere redistribution precedes homologue pairing and terminal synapsis initiation during prophase I of cattle spermatogenesis

Abstract

Alterations in nuclear topology associated with meiotic chromosome pairing were studied in premeiotic cells and spermatocytes I of adult bovine males. To this end, we performed FISH with chromosome, pericentromeric satellite-DNA and telomere-specific probes in combination with immunostaining of synaptonemal complex proteins (SCP3, SCP1) on testis tissue sections. Nuclei of premeiotic cells (spermatogonia) exhibited a scattered telomere distribution while pericentromeres formed a few intranuclear clusters. We observed that the chromosome pairing process in cattle prophase I is preceded by repositioning of centromeres and telomeres to the nuclear periphery during preleptotene. Clustering of chromosome ends (bouquet formation) was observed during the transition from leptonema to zygonema and coincided with pairing of a sub-centromeric marker of bovine chromosomes 7. Dissolution of bouquet topology during zygonema left perinuclear telomeres scattered over the nuclear periphery at pachynema. SCP3 staining in frozen tissue sections revealed the appearance of this axial element protein in intranuclear aggregates during preleptotene, followed by extensive axial element formation during leptotene. Synapsis as revealed by SCP1 staining initiated peripherally at earliest zygotene, at this stage nuclei still contained numerous SCP3 clusters. Our observations reveal prominent non-homologous satellite-DNA associations in spermatogonia and indicate the conservation of topological features of the meiotic chromosome pairing process among mammals. The comparison of telomere dynamics in mouse and cattle prophase I suggests that a larger number of chromosomes prolongs the duration of the bouquet stage.

Increased ploidy and KAR3 and SIR3 disruption alter the dynamics of meiotic chromosomes and telomeres

“…Meiosis induction in the diploid SK1 strain and the tetraploid SK1 strain derived therefrom revealed that prophase I progression, bouquet formation and meiotic divisions were delayed in tetraploid meiosis compared with diploid wild-type meiosis -which contrasts with the situation in diploid versus allopolyploid plants (Martinez-Perez et al, 2000;Moore, 2002) and indicates that accelerated prophase I progression in polyploid plants is not a universal feature that extends to other kingdoms. Besides other possibilities, the prophase I delay in the polyploid yeast is in agreement with the assumption that a genome with increased chromosome number will require a more elaborate and time-consuming homologue search during prophase I (Dorninger et al, 1995;Pfeifer et al, 2001). How, then, according to such a scenario, is prophase I progression accelerated in polyploid plants?…”

“…This is probably related to the fact that the homologue search and alignment process and the correction of non-homologous premeiotic centromere associations in polyploid plants takes place prior to the onset of meiotic prophase (Martinez-Perez et al, 2001). By contrast, the redistribution of pericentromeric heterochromatin (centromeres) in mammals and yeast occurs during the onset of first meiotic prophase (Hayashi et al, 1999;Pfeifer et al, 2001;Scherthan et al, 1996;Trelles-Sticken et al, 1999). Therefore, the elaborate architectural changes in the diploid meiocyte nucleus that occur after the initiation of meiosis probably extend the time required for the transit though prophase I, whereas the rapid prophase I progression in polyploid plants obviously benefits from the premeiotic alignment of homologous pericentromeres (Martinez-Perez et al, 2001).…”

Isolation and cytogenetic characterization of zebrafish meiotic prophase I mutants

“…The expression of Sycp3 commenced in preleptotene spermatocytes, identified by the presence of one or more intranuclear Sycp3 aggregates (Fig. 5A), which have been shown to mark the onset of prophase I in male germ cells in mouse and cow (Scherthan et al, 1996;Pfeifer et al, 2001). In zebrafish spermatocytes at the leptotene stage, the Sycp3 signals were detectable as short fine threads, starting from one side of the nucleus with a distinct polarity (Fig.…”

FIGLA, a Basic Helix-Loop-Helix Transcription Factor, Balances Sexually Dimorphic Gene Expression in Postnatal Oocytes

“…Sycp3 and Ccna1 (cyclin A1) are expressed during the first meiotic division (35,39). The abundance of their transcripts was comparable in TSPY1-Figla transgenic and normal mice, indicating a similar complement of spermatocytes (Fig.…”