Nuclear dispositions of subtelomeric and pericentromeric chromosomal domains during meiosis in asynaptic mutants of rye (Secale cereale L.)

Abstract

The nuclear dispositions of subtelomeric and pericentromeric domains in pollen mother cells (PMCs) were tracked during meiosis in wildtype and two asynaptic mutants of rye (Secale cereale L.) by means of fluorescence in situ hybridization (FISH). Homozygotes for sy1 and sy9 non-allelic mutations form axial elements during leptotene of male meiosis, but fail to form synaptonemal complexes. Consequently, recombination is severely impaired, and high univalency is observed at metaphase I. Simultaneous FISH with pSc200 subtelomeric tandem repeat and CCS1 centromeric sequence revealed that at pre-meiotic interphase the two domains are in a bipolar Rabl orientation in both the PMCs and tapetal cells. At the onset of meiotic prophase, the subtelomeric regions in PMCs of wildtype and sy9 cluster into a typical bouquet conformation. The timing of this event in rye is comparable with that in wheat, and is earlier than that observed in other organisms, such as maize, yeast and mammals. This arrangement is retained until later in leptotene and zygotene when the pericentromeric domains disperse and the subtelomeric clusters fragment. The mutant phenotype of sy9 manifests itself during leptotene to zygotene, when the pericentromeric regions become distinctly more distended than in wildtype, and largely fail to pair during zygotene. This indicates that difference in the nature or timing of chromosome condensation in this region is the cause or consequence of asynapsis. By contrast, sy1 fails to form comparable aggregates of subtelomeric regions at leptotene in only half of the nuclei studied. Instead, two to five aggregates are formed that fail to disperse at later stages of meiotic prophase. In addition, the pericentromeric regions disperse prematurely at leptotene and do not associate in pairs at any subsequent stage. It is supposed that the sy1 mutation could disrupt the nuclear disposition of centromeres and telomeres at the end of pre-meiotic interphase, which could cause, or contribute to, its asynaptic phenotype.

Pericentromeric chromatin reorganisation follows the initiation of recombination and coincides with early events of synapsis in cereals

“…We showed that, in early leptotene, chromosome arms were condensed and organised into irregular globular subdomains with telomeres and centromeres pointing to opposite poles of the nucleus. This condensed early chromosome conformation and the bipolar orientation of telomeres versus centromeres was in agreement with several previous studies analysing chromatin dynamics in wheat-rye introgression lines Maestra et al, 2002;Mart ınez-P erez et al, 1999;Mikhailova et al, 2001;Schwarzacher, 1997). We demonstrated that this condensed chromatin structure coincided with recombination initiation by numerous nucleus wide DSBs, whereas homologous chromosome arms were located at considerable distances from one another (Figure 7).…”

Bouquet Formation Failure in Meiosis of F1 Wheat–Rye Hybrids with Mitotic-Like Division

“…We used such criteria as the number and position of nucleoli in meiocyte nuclei [43,44], character of ASY1 localization, distribution and share of centromeres [17][18][19], and the cell shape [21] described for wheat, barley and rye. In the course of meiocyte development, the nucleoli fuse (reunite) into one before or during leptotene [43,44]; as a result, during the leptotene-to-zygotene transition, one large nucleolus localizes on the nucleus periphery [7,8,21,22,44,45]. For both wheat and rye, full telomere aggregation coincides with nucleoli fusion [19,21,24,25,44].…”

“…To date, no plants without the bouquet structure were found in the studies [3,6,13,14]. The telomere dynamics at the early meiotic prophase is well known in such agricultural crops as maize (Zea maize) [8,15,16], barley (Hordeum vulgare) [17][18][19], rye (Secale cereale) [20][21][22][23] and wheat (Triticum aestivum) [7,19,24,25]. In barley, the telomeric bouquet clustering is completed in late G2; by leptotene, the telomeres are clustered [18], or the bouquet forms during leptotene, persisting during zygotene [17,19].…”

“…In barley, the telomeric bouquet clustering is completed in late G2; by leptotene, the telomeres are clustered [18], or the bouquet forms during leptotene, persisting during zygotene [17,19]. In rye, at early leptotene, a tight cluster is formed at the nuclear envelope [22,23]. In wheat, a fully formed bouquet with a tight telomere cluster is identified at early and mid-zygotene [7,19], despite the pairing in bread wheat being complicated by its hexaploid nature.…”

Meiosis in Polyploids and Implications for Genetic Mapping: A Review

“…During early meiotic PI, telomeres aggregate on the nuclear envelope, forming a cluster or bouquet [102][103][104], facilitating homologous chromosome sorting. The timing of telomere bouquet formation differs across species, appearing earlier at PI in wheat and rye and later in maize [24,105,106]. After the formation of the telomere bouquet, SC formation is initiated near the telomeres during early PI, progressing lengthwise pairing as PI proceeds (Figure 1) [107][108][109].…”