scholarly journals Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC

2005 ◽  
Vol 168 (5) ◽  
pp. 683-689 ◽  
Author(s):  
Kentaro Nabeshima ◽  
Anne M. Villeneuve ◽  
Monica P. Colaiácovo

Homologous chromosome pairs (bivalents) undergo restructuring during meiotic prophase to convert a configuration that promotes crossover recombination into one that promotes bipolar spindle attachment and localized cohesion loss. We have imaged remodeling of meiotic chromosome structures after pachytene exit in Caenorhabditis elegans. Chromosome shortening during diplonema is accompanied by coiling of chromosome axes and highly asymmetric departure of synaptonemal complex (SC) central region proteins SYP-1 and SYP-2, which diminish over most of the length of each desynapsing bivalent while becoming concentrated on axis segments distal to the single emerging chiasma. This and other manifestations of asymmetry along chromosomes are lost in synapsis-proficient crossover-defective mutants, which often retain SYP-1,2 along the full lengths of coiled diplotene axes. Moreover, a γ-irradiation treatment that restores crossovers in the spo-11 mutant also restores asymmetry of SYP-1 localization. We propose that crossovers or crossover precursors serve as symmetry-breaking events that promote differentiation of subregions of the bivalent by triggering asymmetric disassembly of the SC.

Genome ◽  
1991 ◽  
Vol 34 (6) ◽  
pp. 879-887 ◽  
Author(s):  
M. P. Maguire ◽  
A. M. Paredes ◽  
R. W. Riess

The phenotype of the desynaptic (dy) mutant of maize in microsporocytes at meiotic prophase was compared with normal microsporocytes of a closely related strain and with microsporocytes of a maize inbred line (KYS) assumed to be normal. Strikingly more univalents and open arms of bivalents were found in the mutant cells than in normal cells at diakinesis, and where there was heterozygosity for a distal knob (heterochromatic region), separation was usually equational, indicating the occurrence of normal crossing-over followed by failure of chiasma maintenance in the mutant. Differences found in the mutant by electron microscopy were a statistically significant wider dimension of the synaptonemal complex central region and also less twisting of synapsed configurations at pachytene. It is suggested that these are side-effect symptoms of a defect in the synaptonemal complex (or associated substance), which is expressed later as sporadic loss of chiasma maintenance.Key words: desynaptic, chiasma maintenance, synaptonemal complex.


PLoS Genetics ◽  
2014 ◽  
Vol 10 (11) ◽  
pp. e1004757 ◽  
Author(s):  
Heather Brockway ◽  
Nathan Balukoff ◽  
Martha Dean ◽  
Benjamin Alleva ◽  
Sarit Smolikove

2017 ◽  
Vol 216 (2) ◽  
pp. 393-408 ◽  
Author(s):  
Benjamin Alleva ◽  
Nathan Balukoff ◽  
Amy Peiper ◽  
Sarit Smolikove

In meiotic prophase I, homologous chromosome pairing is promoted through chromosome movement mediated by nuclear envelope proteins, microtubules, and dynein. After proper homologue pairing has been established, the synaptonemal complex (SC) assembles along the paired homologues, stabilizing their interaction and allowing for crossing over to occur. Previous studies have shown that perturbing chromosome movement leads to pairing defects and SC polycomplex formation. We show that FKB-6 plays a role in SC assembly and is required for timely pairing and proper double-strand break repair kinetics. FKB-6 localizes outside the nucleus, and in its absence, the microtubule network is altered. FKB-6 is required for proper movement of dynein, increasing resting time between movements. Attenuating chromosomal movement in fkb-6 mutants partially restores the defects in synapsis, in agreement with FKB-6 acting by decreasing chromosomal movement. Therefore, we suggest that FKB-6 plays a role in regulating dynein movement by preventing excess chromosome movement, which is essential for proper SC assembly and homologous chromosome pairing.


1978 ◽  
Vol 20 (4) ◽  
pp. 567-579 ◽  
Author(s):  
Peter B. Moens

Observations are presented in support of the hypothesis that at meiotic prophase a reciprocal crossover is accompanied by a crossover of the lateral elements of the synaptonemal complex, SC (Moens, 1974). Rat spermatocyte nuclei in developmental stage VII (Clermont, 1972) of the seminiferous epithelium cycle, but not pachytene nuclei in stages I to VI, were found to have SC modifications in the form of a cross connection between the lateral elements. In structure these crossover elements, CO elements, resemble the lateral element. It is found in a variety of positions, usually more or less perpendicular to the SC but also slanted or parallel along the central element or detached from the SC. Reconstructions of entire nuclei indicate an average of one such CO element per SC and a nonrandom distribution of CO elements among the SCs. Because the crossing-over of lateral elements produces a 180° twist or removes a 180° twist, the pattern of SC coiling was examined. Coiling starts in early pachytene prior to CO element formation. At stage VII one nucleus had a total of 78 coils, all counter clockwise, and another nucleus had 97 such 180° coils. It is noted that if SC coils are associated with the process of crossing-over, then the regulation of crossover distribution such as chiasma position interference has an explanation in the structure and behavior of the SC.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Liangyu Zhang ◽  
Simone Köhler ◽  
Regina Rillo-Bohn ◽  
Abby F Dernburg

During meiosis, each pair of homologous chromosomes typically undergoes at least one crossover (crossover assurance), but these exchanges are strictly limited in number and widely spaced along chromosomes (crossover interference). The molecular basis for this chromosome-wide regulation remains mysterious. A family of meiotic RING finger proteins has been implicated in crossover regulation across eukaryotes. Caenorhabditis elegans expresses four such proteins, of which one (ZHP-3) is known to be required for crossovers. Here we investigate the functions of ZHP-1, ZHP-2, and ZHP-4. We find that all four ZHP proteins, like their homologs in other species, localize to the synaptonemal complex, an unusual, liquid crystalline compartment that assembles between paired homologs. Together they promote accumulation of pro-crossover factors, including ZHP-3 and ZHP-4, at a single recombination intermediate, thereby patterning exchanges along paired chromosomes. These proteins also act at the top of a hierarchical, symmetry-breaking process that enables crossovers to direct accurate chromosome segregation.


2018 ◽  
Author(s):  
Luciana Previato de Almeida ◽  
Jared M. Evatt ◽  
Hoa H. Chuong ◽  
Emily L. Kurdzo ◽  
Craig A. Eyster ◽  
...  

ABSTRACTFaithful chromosome segregation during meiosis I depends upon the formation of connections between homologous chromosomes. Crossovers between homologs connect the partners allowing them to attach to the meiotic spindle as a unit, such that they migrate away from one another at anaphase I. Homologous partners also become connected by pairing of their centromeres in meiotic prophase. This centromere pairing can promote proper segregation at anaphase I of partners that have failed to become joined by a crossover. Centromere pairing is mediated by synaptonemal complex (SC) proteins that persist at the centromere when the SC disassembles. Here, using mouse spermatocyte and yeast model systems, we tested the role of shugoshin in promoting meiotic centromere pairing by protecting centromeric synaptonemal components from disassembly. The results show that shugoshin protects centromeric SC in meiotic prophase and, in anaphase, promotes the proper segregation of partner chromosomes that are not linked by a crossover.SIGNIFICANCEMeiotic crossovers form a connection between homologous chromosomes that allows them to attach to the spindle as a single unit in meiosis I. In humans, failures in this process are a leading cause of aneuploidy. A recently described process, called centromere pairing, can also help connect meiotic chromosome partners in meiosis. Homologous chromosomes become tightly joined by a structure called the synaptonemal complex (SC) in meiotic prophase. After the SC disassembles, persisting SC proteins at the centromeres mediate their pairing. Here, studies in mouse spermatocytes and yeast are used to show that the shugoshin protein helps SC components persist at centromeres and helps centromere pairing promote the proper segregation of yeast chromosomes that fail to become tethered by crossovers.


2003 ◽  
Vol 23 (4) ◽  
pp. 1151-1162 ◽  
Author(s):  
Willy M. Baarends ◽  
Evelyne Wassenaar ◽  
Jos W. Hoogerbrugge ◽  
Gert van Cappellen ◽  
Henk P. Roest ◽  
...  

ABSTRACT The ubiquitin-conjugating enzymes HR6A and HR6B are the two mammalian homologs of Saccharomyces cerevisiae RAD6. In yeast, RAD6 plays an important role in postreplication DNA repair and in sporulation. HR6B knockout mice are viable, but spermatogenesis is markedly affected during postmeiotic steps, leading to male infertility. In the present study, increased apoptosis of HR6B knockout primary spermatocytes was detected during the first wave of spermatogenesis, indicating that HR6B performs a primary role during the meiotic prophase. Detailed analysis of HR6B knockout pachytene nuclei showed major changes in the synaptonemal complexes. These complexes were found to be longer. In addition, we often found depletion of synaptonemal complex proteins from near telomeric regions in the HR6B knockout pachytene nuclei. Finally, we detected an increased number of foci containing the mismatch DNA repair protein MLH1 in these nuclei, reflecting a remarkable and consistent increase (20 to 25%) in crossing-over frequency. The present findings reveal a specific requirement for the ubiquitin-conjugating activity of HR6B in relation to dynamic aspects of the synaptonemal complex and meiotic recombination in spermatocytes.


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