Abstract
Meiotic chromosomes assemble characteristic “axial element” structures that are essential for fertility and provide the chromosomal context for meiotic recombination, synapsis and checkpoint signaling. Whether these meiotic processes are equally dependent on axial element integrity has remained unclear. Here, we investigated this question in S. cerevisiae using the putative condensin allele ycs4S. We show that the severe axial element assembly defects of this allele are explained by a linked mutation in the promoter of the major axial element gene RED1 that reduces Red1 protein levels to 20–25% of wild type. Intriguingly, the Red1 levels of ycs4S mutants support meiotic processes linked to axis integrity, including DNA double-strand break formation and deposition of the synapsis protein Zip1, at levels that permit 70% gamete survival. By contrast, the ability to elicit a meiotic checkpoint arrest is completely eliminated. This selective loss of checkpoint function is supported by a RED1 dosage series and is associated with the loss of most of the cytologically detectable Red1 from the axial element. Our results indicate separable roles for Red1 in building the structural axis of meiotic chromosomes and mounting a sustained recombination checkpoint response.
Highlights
Meiosis is a specialized developmental process, in which a diploid cell undergoes two chromosomal divisions without an intervening S phase to produce haploid gametes for sexual reproduction
To ensure proper chromosome segregation, a meiotic cell must induce DNA double strand breaks, repair them with the homologous chromosome, and fully align the homologs. These aspects of meiosis are dependent on specialized meiotic chromosome axes and the proteins that control this structure, such as Red1 in S. cerevisiae
The low Red1 and Hop1 signals localizing to meiotic chromosomes of ycs4S mutants [51] prompted us to test whether total axis protein levels are reduced by this allele
Summary
Meiosis is a specialized developmental process, in which a diploid cell undergoes two chromosomal divisions without an intervening S phase to produce haploid gametes for sexual reproduction. The reduction in ploidy occurs during meiosis I, when homologous chromosomes are segregated. To enable this unique segregation pattern, meiotic cells must identify and physically link homologous chromosome pairs. Meiotic crossover formation relies on the controlled introduction and repair of a large number of programmed DNA double-strand breaks (DSBs). Following DSB formation, nucleolytic processing releases Spo from break ends along with short covalently-linked oligonucleotides [9]. Exonucleases resect the break ends to produce 3’ single-stranded DNA (ssDNA) tails [10] that are used by the recombinases Rad and Dmc to preferentially invade the homologous chromosomes [11,12]. Some of the resulting strand-invasion intermediates are stabilized and processed to produce crossovers [13,14,15,16,17]
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