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

Abstract

Normally, meiotic crossovers in conjunction with sister-chromatid cohesion establish a physical connection between homologs that is required for their accurate segregation during the first meiotic division. However, in some organisms an alternative mechanism ensures the proper segregation of bivalents that fail to recombine. In Drosophila oocytes, accurate segregation of achiasmate homologs depends on pairing that is mediated by their centromere-proximal heterochromatin. Our previous work uncovered an unexpected link between sister-chromatid cohesion and the fidelity of achiasmate segregation when Drosophila oocytes are experimentally aged. Here we show that a weak mutation in the meiotic cohesion protein ORD coupled with a reduction in centromere-proximal heterochromatin causes achiasmate chromosomes to missegregate with increased frequency when oocytes undergo aging. If ORD activity is more severely disrupted, achiasmate chromosomes with the normal amount of pericentric heterochromatin exhibit increased nondisjunction when oocytes age. Significantly, even in the absence of aging, a weak ord allele reduces heterochromatin-mediated pairing of achiasmate chromosomes. Our data suggest that sister-chromatid cohesion proteins not only maintain the association of chiasmate homologs but also play a role in promoting the physical association of achiasmate homologs in Drosophila oocytes. In addition, our data support the model that deterioration of meiotic cohesion during the aging process compromises the segregation of achiasmate as well as chiasmate bivalents.

The Cohesion Protein SOLO Associates with SMC1 and Is Required for Synapsis, Recombination, Homolog Bias and Cohesion and Pairing of Centromeres in Drosophila Meiosis

“…Similar observations have been reported for solo male meiosis and ord male and female meiosis [51]–[53], [60], [61], [73] and indicate the existence of centromere cohesion that is independent of both SOLO and ORD and perhaps of cohesin (although the possible presence of low levels of cohesin near centromeres in solo and ord mutants cannot be ruled out). Whether this early prophase cohesion is based on a protein complex or on chromatid entanglement remains to be determined.…”

Heterochromatin-Associated Proteins HP1a and Piwi Collaborate to Maintain the Association of Achiasmate Homologs in Drosophila Oocytes

“…Therefore, FM7a/X homologs rely entirely on the achiasmate system for accurate segregation. We have previously shown that because centromere proximal heterochromatin on FM7a is greatly reduced, the FM7a/X pair provides a sensitized system to investigate the mechanisms underlying PHeMAAH (Subramanian and Bickel 2009).…”

“…This means that weakened PHeMAAH between a pair of homologs during prophase I does not always result in missegregation during anaphase I. Our previous work has shown that a reduction of pericentric heterochromatin on one of the chromosomes of an achiasmate X chromosome pair sensitizes it to missegregation under conditions that perturb PHeMAAH (Subramanian and Bickel 2009). This is the case for the FM7a/X achiasmate chromosome pair that we have used in our analyses.…”

Inter-telomeric connections and achiasmate meiosis in Tradescantia spathacea Sw.

“…As such the present report of the presence of achiasmate meiosis coupled with inter-telomeric connections is the first report for T. spathacea. While inter chromosomal connections have been attributed mostly to fixation artifact [33] and to the fusion of heterochromatic region between the chromosomes [16,39,62,65], achiasmate meiosis has been assigned to the presence of mutant gene(s) affecting chiasmata formation [2,21,32,34,60], alteration in temperature/humidity [34,60,67], defective synaptonemal complex formation [14,21,24,60] and to disturbed supply of potassium and phosphate ions to the tissue [2,60]. In the present material inter-telomeric connections cannot be attributed to any of the two factors mentioned elsewhere on account of the fact that this feature was discerned only in some buds while other buds showed meiotic features characteristic of complex translocation heterozygote and supported the earlier reports [17,18,31,36,37,41,42,55,56,64].…”