Meiotic Synapsis in the Absence of Recombination

Abstract

Although in Saccharomyces cerevisiae the initiation of meiotic recombination, as indicated by double-strand break formation, appears to be functionally linked to the initiation of synapsis, meiotic chromosome synapsis in Drosophila females occurs in the absence of meiotic exchange. Electron microscopy of oocytes from females homozygous for either of two meiotic mutants (mei-W68 and mei-P22), which eliminate both meiotic crossing over and gene conversion, revealed normal synaptonemal complex formation. Thus, synapsis in Drosophila is independent of meiotic recombination, consistent with a model in which synapsis is required for the initiation of meiotic recombination. Furthermore, the basic processes of early meiosis may have different functional or temporal relations, or both, in yeast and Drosophila.In the classical view of meiosis, homologous chromosome synapsis, as indicated by the formation of an elaborate ribbonlike structure called the synaptonemal complex (SC), was thought to be the first and primary event of meiotic prophase, essential for the initiation of meiotic recombination (1). Studies in Saccharomyces cerevisiae, however, have created a different view of the meiotic process in which the initiation of recombination, as evidenced by a doublestrand break (DSB), precedes the initiation of synapsis (2, 3). Three lines of evidence support this view of early meiotic prophase in yeast. First, the initiating event of meiotic recombination, the formation of a DSB, appears before SC formation (4). Second, meiotic mutants that either fail to create DSBs or to process DSBs to make single-stranded tails prevent the formation of a mature SC (2). Third, some mutants allow high levels of meiotic recombination but prevent the production of a mature SC (5). These data are consistent with a model in which single-stranded DNA generated by a DSB carries out a homology search required for synapsis and SC formation. In contrast, synapsis is not an absolute prerequisite for either the initiation (6) or completion of meiotic recombination (7).To assess the relation between synapsis and the initiation of recombination in Drosophila oocytes, we examined both recombination and SC formation in oocytes homozygous for either of two null-recombination mutations. The mei-W68 and mei-P22 (8) mutants prevent the initiation of meiotic recombination as defined by four independent assays: (i) reduction or elimination of meiotic gene conversion; (ii) elimination of meiotic crossing over, as assayed by measuring either intragenic crossing over or the frequency of meiotic crossing over along entire chromosome arms; (iii) lack of doublestrand DNA breaks that persist into metaphase or anaphase I; and (iv) failure to produce either early or late recombination nodules (RNs).To assay the effects of the mei-W68 and mei-P22 mutations on meiotic crossing over, we examined intragenic recombination at the rosy locus (9). No gene conversion events or intragenic crossovers were observed among the progeny of mei-W68 or mei-P22 females (Table 1 and Fig...

Origins and evolution of the recA / RAD51 gene family: Evidence for ancient gene duplication and endosymbiotic gene transfer

“…It is known that these organisms exhibit distinct features in their meiotic recombination (12,13,34). It is possible that functional divergence in meiotic recombination and its relationship with other chromosomal interactions are related to the rapid evolution of RAD51 and loss of DMC1 in these organisms.…”

Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

“…However, since repetitive elements comprise 30%-50% of mammalian genomes, wide-range homology search, rather than regional DNA sequence identity, might be important to avoid nonallelic pairing and recombination in meiosis (Zickler and Kleckner 1999;Page and Hawley 2004;Sasaki et al 2010). In fact, in some organisms undergoing recombinationless meiosis, homologs are properly paired and even synapsed in a DSB-independent manner (Dernburg et al 1998;McKim et al 1998). Also, in fungi (yeasts and Sordaria), while a tight association is established by Ó 2014 Ishiguro et al This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml).…”

Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks

“…These results place Spo11 action upstream of SC formation, both temporally and functionally. This coupling is not universal, however; in Drosophila melanogaster and Caenorhabditis elegans, normal SC is formed in mutants defective for recombination initiation (21,22), and in yet other organisms (e.g., females of the silk moth Bombyx mori), SC formation in the absence of recombination is the norm (23).How is the linkage achieved when recombination and SC formation are tied together? At least a part of this coupling may come through nucleation of SC formation at sites where meiotic recombination is occurring and in particular at the subset of sites that will give rise to crossovers.…”

“…These results place Spo11 action upstream of SC formation, both temporally and functionally. This coupling is not universal, however; in Drosophila melanogaster and Caenorhabditis elegans, normal SC is formed in mutants defective for recombination initiation (21,22), and in yet other organisms (e.g., females of the silk moth Bombyx mori), SC formation in the absence of recombination is the norm (23).…”