Academic journal article Genetics

Meiotic Centromere Coupling and Pairing Function by Two Separate Mechanisms in Saccharomyces Cerevisiae

Academic journal article Genetics

Meiotic Centromere Coupling and Pairing Function by Two Separate Mechanisms in Saccharomyces Cerevisiae

Article excerpt

ACCURATE chromosome segregation in meiosis is important for preservation of the genome of an organism through multiple generations. In meiosis I, the cell is presented with a unique challenge in which homologous chromosomesmust segregate from one another. This is followed by a mitosis-like segregation of the sister chromatids in meiosis II. In Saccharomyces cerevisiae, chromosomes interact with other chromosomes in meiosis I in four defined ways that will be introduced here: crossing over, centromere coupling, synaptonemal complex (SC) formation, and centromere pairing (reviewed in Kurdzo and Dawson 2015).

During meiotic prophase, homologous chromosome partners go through a series of events that culminate in the formation of crossovers between the homologous partners. In early prophase, double-strand breaks (DSBs) in theDNAare created by the endonuclease Spo11 (Keeney et al. 1997), homologous partners align, and a proteinaceous structure called the SC assembles along the axes of the homologs (reviewed in Kurdzo and Dawson 2015). The SC is comprised of two axial elements that run along the axes of each homolog and a central region that joins the axial elements together along their length. Repair of the DSBs by homologous recombination is critical for the formation of crossovers that, together with sister chromatid cohesion, serves to tether homologous partners together as they go through the process of attaching to the meiotic spindle (Keeney et al. 1997; Celerin et al. 2000).

Coincident with the formation of DSBs, centromeres undergo a period of pairwise associations that are homology independent and are referred to as centromere coupling (Tsubouchi and Roeder 2005; Obeso and Dawson 2010). Similar coupling or clustering of centromeres, or regions of pericentric heterochromatin, have been observed in a number of organisms, including onion (Church and Moens 1976), wheat (Bennett 1979; Martínez-Pérez et al. 1999), rice (Prieto et al. 2004), fission yeast (Ding et al. 2004; Tsubouchi and Roeder 2005; Obeso and Dawson 2010), maize (Zhang et al. 2013), and mouse (Scherthan et al. 1996; Takada et al. 2011). The reason behind this centromere coupling or clustering remains unclear, but recent studies in yeast suggest the chromosomes show a lengthdependent preference for partner choice during centromere coupling, which may improve the efficiency of homologous pairing later in meiosis (Lefrancois et al. 2016).

As the chromosomes begin to synapse with their homologs, the centromeres seem to transition individually from nonhomologous coupling to pairing with their homologous centromere, as there is never a time in wild-type (WT) cells when all the centromeres are fully dispersed between the coupling and pairing stages (Obeso and Dawson 2010). When the homologous partners are fully synapsed (pachytene stage), remaining pairs of natural or artificial chromosomes that have failed to recombine (achiasmate partners) can be seen to pair at their centromeres (called centromere pairing) (Kemp et al. 2004; Gladstone et al. 2009; Newnham et al. 2010).

As the cells transition out of pachytene, the SC largely disassembles to reveal a small stretch of Zip1 leftbehind at the centromeres; suggesting that, like achiasmate partners, the chiasmate homologous chromosomes are also joined at their centromeres in pachytene. This type of pairing has been observed in yeast (Kemp et al. 2004; Gladstone et al. 2009; Newnham et al. 2010), but similar centromere-centromere interactions in late prophase (after SC disassembly) have also been observed in Drosophila (Dernburg et al. 1996; Takeo et al. 2011), fission yeast (Davis and Smith 2003; Ding et al. 2004), and mouse spermatocytes (Bisig et al. 2012; Qiao et al. 2012). Centromere pairing has been proposed to serve as an alternative means to tether partners that have failed to become joined by chiasmata (Dawson et al. 1986), and has been shown in genetic experiments to promote the biorientation of homologous chiasmate partners on the spindle (Gladstone et al. …

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