The Chromosomal Courtship Dance—homolog pairing in early meiosis

Abstract

The intermingling of genomes that characterizes sexual reproduction requires haploid gametes in which parental homologs have recombined. For this, homologs must pair during meiosis. In a crowded nucleus where sequence homology is obscured by the enormous scale and packaging of the genome, partner alignment is no small task. Here we review the early stages of this process. Chromosomes first establish an initial docking site, usually at telomeres or centromeres. The acquisition of chromosome-specific patterns of binding factors facilitates homolog recognition. Chromosomes are then tethered to the nuclear envelope (NE) and subjected to nuclear movements that 'shake off' inappropriate contacts while consolidating homolog associations. Thereafter, homolog connections are stabilized by building the synaptonemal complex or its equivalent and creating genetic crossovers. Recent perspectives on the roles of these stages will be discussed.

Telomeric TERB1–TRF1 interaction is crucial for male meiosis

“…Next, we used fluorescence in situ hybridization (FISH) analysis of testis sections to further investigate the meiotic defect of Terb1 AEA/AEA mice. There were very few spermatocytes exhibiting telomere bouquets in WT and heterozygous testis sections, consistent with the fact that telomere clustering in the bouquet configuration occurs transiently during the zygotene stage 34–36 ( Fig. 4e,f ).…”

Recombination, Pairing, and Synapsis of Homologs during Meiosis

“…First, a tendency for colocalization will increase the proximity of a DSB and its cognate partner sequence while concomitantly reducing the complexity of irrelevant sequences that must be scanned and rejected (e.g., Goldman and Lichten 2000). Second, such pairing will tend to place homologous chromosomes in topologically acceptable joint domains, thus reducing the likelihood that creation of many DSB-mediated connections between different homologs will create a tangled mess (Kleckner and Weiner 1993;Klutstein and Cooper 2014).…”

“…Once the pairing pro- cess is underway, telomere-led motion could help to move chromosomes out of the way of one another to permit full-length pairing. Another attractive possibility is that these motions promote resolution of entanglements (Zickler 2006;Koszul et al 2008;Storlazzi et al 2010;Kleckner et al 2012;Klutstein and Cooper 2014). Whole-chromosome entanglements, known as "interlocks," occur during the leptotene pairing process and during synapsis but are absent (and thus must be actively resolved) by the end of pachytene (reviewed in von Wettstein et al 1984;Zickler and Kleckner 1999;Storlazzi et al 2010).…”

“…This role for Mlh1 might be related to its general ability to trigger the disassembly of recombination complexes whose interacting duplexes contain DNA mismatches (e.g., Hunter 2007). Active chromosome movement should similarly facilitate elimination of unwanted DNA links of other types, for example, ectopic recombinational interactions between homologous regions located on different chromosomes (Goldman and Lichten 2000;reviewed in Ding et al 2004;Davis and Smith 2006;Conrad et al 2008;Koszul and Kleckner 2009; further discussion in Klutstein and Cooper 2014).…”

Centromere Associations in Meiotic Chromosome Pairing

“…Is there some form of chromosomal prealignment that facilitates homolog-homolog interactions? Different organisms have developed more than one way to ensure homolog pairing during meiosis, but a general scheme clearly emerges (Figure 1) (8,67). Initial chromosome interactions are first established between particular chromosomal regions such as telomeres, centromeres, or specific pairing centers.…”