Abstract
Chromosome pairing in meiotic prophase is a prerequisite for the high fidelity of chromosome segregation that haploidizes the genome prior to gamete formation. In the budding yeast Saccharomyces cerevisiae, as in most multicellular eukaryotes, homologous pairing at the cytological level reflects the contemporaneous search for homology at the molecular level, where DNA double-strand broken ends find and interact with templates for repair on homologous chromosomes. Synapsis (synaptonemal complex formation) stabilizes pairing and supports DNA repair. The bouquet stage, where telomeres have formed a transient single cluster early in meiotic prophase, and telomere-promoted rapid meiotic prophase chromosome movements (RPMs) are prominent temporal correlates of pairing and synapsis. The bouquet has long been thought to contribute to the kinetics of pairing, but the individual roles of bouquet and RPMs are difficult to assess because of common dependencies. For example, in budding yeast RPMs and bouquet both require the broadly conserved SUN protein Mps3 as well as Ndj1 and Csm4, which link telomeres to the cytoskeleton through the intact nuclear envelope. We find that mutants in these genes provide a graded series of RPM activity: wild-type>mps3-dCC>mps3-dAR>ndj1Δ>mps3-dNT = csm4Δ. Pairing rates are directly correlated with RPM activity even though only wild-type forms a bouquet, suggesting that RPMs promote homologous pairing directly while the bouquet plays at most a minor role in Saccharomyces cerevisiae. A new collision trap assay demonstrates that RPMs generate homologous and heterologous chromosome collisions in or before the earliest stages of prophase, suggesting that RPMs contribute to pairing by stirring the nuclear contents to aid the recombination-mediated homology search.
Highlights
Haploidization of the genome for sexual reproduction depends critically on homologous chromosome pairing early in meiotic prophase
The impact on rapid meiotic prophase chromosome movements (RPMs) of deletion mps3-dAR is more difficult to predict as there is growing recognition of the roles of Mps3 and this domain in a wide variety of telomere and DNA double-strand break activities at the nuclear envelope in mitotic cells [35,36,37,38,39,40,41,42]
Among RPM mutants with a range of delays in completing synapsis, as in wild-type, we consistently observe that shorter chromosomes are the last to synapse (Figure 8)
Summary
Haploidization of the genome for sexual reproduction depends critically on homologous chromosome pairing early in meiotic prophase. The complexity and efficiency of chromosome pairing has long suggested that the nuclear contents are actively stirred to bring homologous regions into proximity [1]. This notion is supported by the occurrence of well-conserved, rapid meiotic prophase chromosome movements (RPMs; [2,3,4,5,6,7]). These movements are believed to be driven by SUN protein-mediated links through the intact nuclear envelope that connect telomeres to cytoplasmic motors [8,9]. Defects in SUN genes cause defects both in RPMs and in pairing (reviewed in [10,11,12] and see [13,14,15,16])
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