Heterochromatic Threads Connect Oscillating Chromosomes during Prometaphase I in Drosophila Oocytes

Abstract

In Drosophila oocytes achiasmate homologs are faithfully segregated to opposite poles at meiosis I via a process referred to as achiasmate homologous segregation. We observed that achiasmate homologs display dynamic movements on the meiotic spindle during mid-prometaphase. An analysis of living prometaphase oocytes revealed both the rejoining of achiasmate X chromosomes initially located on opposite half-spindles and the separation toward opposite poles of two X chromosomes that were initially located on the same half spindle. When the two achiasmate X chromosomes were positioned on opposite halves of the spindle their kinetochores appeared to display proper co-orientation. However, when both Xs were located on the same half spindle their kinetochores appeared to be oriented in the same direction. Thus, the prometaphase movement of achiasmate chromosomes is a congression-like process in which the two homologs undergo both separation and rejoining events that result in the either loss or establishment of proper kinetochore co-orientation. During this period of dynamic chromosome movement, the achiasmate homologs were connected by heterochromatic threads that can span large distances relative to the length of the developing spindle. Additionally, the passenger complex proteins Incenp and Aurora B appeared to localize to these heterochromatic threads. We propose that these threads assist in the rejoining of homologs and the congression of the migrating achiasmate homologs back to the main chromosomal mass prior to metaphase arrest.

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

“…These tethers appear to be built from pericentromeric heterochromatin and are proposed to establish tension between chromosomes not held together by chiasmata, thus allowing homologous coorientation to be established (Hughes et al 2009(Hughes et al , 2011. Similar tethers have been inferred by micromanipulation experiments in grasshopper spermatocytes (LaFountain et al 2002) and by PICH localization to DNA threads connecting mitotic sister kinetochores in mammalian cultured cells (Baumann et al 2007).…”

Heterochromatin-Mediated Association of Achiasmate Homologs Declines With Age When Cohesion Is Compromised

“…In wild-type Drosophila oocytes, 6-12% of normal X chromosome bivalents fail to recombine and therefore belong to the E 0 tetrad exchange rank (Ashburner 1989;Zwick et al 1999 Reduced centromere-proximal heterochromatin contributes to age-dependent NDJ of achiasmate chromosomes in ord 4 /ord 10 oocytes: In addition to promoting arm cohesion and meiotic exchange, ORD also functions at the centromere and is highly enriched at pericentric heterochromatin (see Figure 1). Homologous pairing of centromere proximal heterochromatin is essential for proper achiasmate chromosome disjunction in Drosophila oocytes Hawley and Theurkauf 1993;Karpen et al 1996) and this pairing is maintained until anaphase I (Dernburg et al 1996;Gilliland et al 2009;Hughes et al 2009). One possibility is that the FM7a chromosome is more vulnerable to increased NDJ in aged ord 4 /ord 10 oocytes because a large portion of the pericentric heterochromatin is displaced to the distal end of the chromosome ( Figure 3B).…”

“…Furthermore, there is a linear relationship between the amount of pericentric heterochromatin and the fidelity of achiasmate segregation (Karpen et al 1996). Cytological analyses of Drosophila oocytes indicate that the centromere-proximal heterochromatin of homologous chromosomes remains associated from pachytene until anaphase I (Dernburg et al 1996;Gilliland et al 2009;Hughes et al 2009). However, whether or how specific heterochromatin proteins promote this association has not been investigated.…”

“…Stages 2-6 represent pachytene oocytes and stages 7-11 correspond to oocytes after synaptonemal complex disassembly but before nuclear envelope breakdown or spindle formation (Ashburner 1989). Although pairing between homologous euchromatic regions is lost at the end of pachytene (Dernburg et al 1996), the pericentric heterochromatin of homologs remains in contact until anaphase I (Dernburg et al 1996;Gilliland et al 2009;Hughes et al 2009). Therefore, analysis of FM7a/X heterochromatin pairing during stages 2-11 allowed us to examine the behavior of this achiasmate bivalent during pachytene and postpachytene stages.…”

Chromatid Abnormalities in Meiosis: A Brief Review and a Case Study in the Genus Agave (Asparagales, Asparagaceae)

“…(C) As shown by Hughes et al [35], achiasmate homologs can be found on the same side of the metaphase plate. This is the irst demonstration that this coniguration can occur, and it suggests that achiasmate homologs can move in unison.…”