Heterochromatic Threads Connect Oscillating Chromosomes during Prometaphase I in Drosophila Oocytes

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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. Proper chromosome segregation is essential during the production of eggs and sperm. Chromosome missegregation during meiosis results in the lethality of the offspring or in children carrying extra copies of a given chromosome (for example, Down syndrome). Recombination results in homologous chromosomes becoming physically interlocked in a manner that is normally sufficient to ensure proper segregation. Chromosomes that fail to undergo recombination require additional mechanisms to ensure their proper segregation. In Drosophila melanogaster oocytes we show that chromosomes that fail to recombine undergo dynamic movements on the meiotic spindle prior to their proper segregation. Although previous studies had shown that non-recombinant chromosomes move to opposite sides of the developing meiotic spindle, we show that these chromosomes can cross the spindle and re-associate with their homologs to attempt reorientation. Additionally, we observed threads connecting separated non-recombinant chromosomes that contained heterochromatic DNA and passenger complex proteins. These threads could assist the non-recombinant chromosomes in locating their homologs during their dynamic movements on the spindle. These chromosome movements and the heterochromatic threads are likely part of the mechanism ensuring proper segregation of nonexchange chromosomes.