scholarly journals Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex

2008 ◽  
Vol 121 (15) ◽  
pp. 2445-2451 ◽  
Author(s):  
G. Hamer ◽  
H. Wang ◽  
E. Bolcun-Filas ◽  
H. J. Cooke ◽  
R. Benavente ◽  
...  
Genetics ◽  
2021 ◽  
Author(s):  
Karen Voelkel-Meiman ◽  
Ashwini Oke ◽  
Arden Feil ◽  
Alexander Shames ◽  
Jennifer Fung ◽  
...  

Abstract A large subset of meiotic recombination intermediates form within the physical context of synaptonemal complex (SC), but the functional relationship between SC structure and homologous recombination remains obscure. Our prior analysis of strains deficient for SC central element proteins demonstrated that tripartite SC is dispensable for interhomolog recombination in S. cerevisiae. Here we report that while dispensable for recombination per se, SC proteins promote efficient mismatch repair at interhomolog recombination sites. Failure to repair mismatches within heteroduplex-containing meiotic recombination intermediates leads to genotypically sectored colonies (post meiotic segregation events). We discovered increased post-meiotic segregation at THR1 in cells lacking Ecm11 or Gmc2, or in the SC-deficient but recombination-proficient zip1[Δ21-163] mutant. High-throughput sequencing of octad meiotic products furthermore revealed a genome-wide increase in recombination events with unrepaired mismatches in ecm11 mutants relative to wild type. Meiotic cells missing Ecm11 display longer gene conversion tracts, but tract length alone does not account for the higher frequency of unrepaired mismatches. Interestingly, the per-nucleotide mismatch frequency is elevated in ecm11 when analyzing all gene conversion tracts, but is similar between wild type and ecm11 if considering only those events with unrepaired mismatches. Thus, in both wild type and ecm11 strains a subset of recombination events is susceptible to a similar degree of inefficient mismatch repair, but in ecm11 mutants a larger fraction of events fall into this inefficient repair category. Finally, we observe elevated post-meiotic segregation at THR1 in mutants with a dual deficiency in MutSγ crossover recombination and SC assembly, but not in the mlh3 mutant, which lacks MutSγ crossovers but has abundant SC. We propose that SC structure promotes efficient mismatch repair of joint molecule recombination intermediates, and that absence of SC is the molecular basis for elevated post-meiotic segregation in both MutSγ crossover-proficient (ecm11, gmc2) and MutSγ crossover-deficient (msh4, zip3) strains.


Open Biology ◽  
2012 ◽  
Vol 2 (7) ◽  
pp. 120099 ◽  
Author(s):  
Owen R. Davies ◽  
Joseph D. Maman ◽  
Luca Pellegrini

The successful completion of meiosis is essential for all sexually reproducing organisms. The synaptonemal complex (SC) is a large proteinaceous structure that holds together homologous chromosomes during meiosis, providing the structural framework for meiotic recombination and crossover formation. Errors in SC formation are associated with infertility, recurrent miscarriage and aneuploidy. The current lack of molecular information about the dynamic process of SC assembly severely restricts our understanding of its function in meiosis. Here, we provide the first biochemical and structural analysis of an SC protein component and propose a structural basis for its function in SC assembly. We show that human SC proteins SYCE2 and TEX12 form a highly stable, constitutive complex, and define the regions responsible for their homotypic and heterotypic interactions. Biophysical analysis reveals that the SYCE2–TEX12 complex is an equimolar hetero-octamer, formed from the association of an SYCE2 tetramer and two TEX12 dimers. Electron microscopy shows that biochemically reconstituted SYCE2–TEX12 complexes assemble spontaneously into filamentous structures that resemble the known physical features of the SC central element (CE). Our findings can be combined with existing biological data in a model of chromosome synapsis driven by growth of SYCE2–TEX12 higher-order structures within the CE of the SC.


1991 ◽  
Vol 69 (6) ◽  
pp. 1384-1395 ◽  
Author(s):  
Hobart R. Williamson ◽  
Pesach Ben Yitzchak

Fifteen synaptonemal complexes, as determined by three-dimensional reconstruction of serial, ultrathin sections, were present within both antheridial and oogonial zygotene and pachytene nuclei of the oomyceteous fungus Achlya recurva, thus n = 15. The present study represents the first complete reconstruction of synaptonemal complexes in the genus Achlya. The occurrence of both zygonema and pachynema was simultaneous in antheridia and oogonia. Pachytene nuclei of antheridia and oogonia are small, 13 μm3 in volume, and the average length of the synaptonemal complexes ranged from 1.9 to 4.4 μm. Lateral elements at zygotene ranged from 1.2 to 4.7 μm. Both ends of each synaptonemal complex were attached randomly to the nuclear envelope, so a bouquet formation was not observed at pachytene. In A. recurva, the dimensions of the synaptonemal complex were as follows: overall width = 270 nm; the lateral elements = 75 nm each in width and the central region = 120 nm. There was no central element and associated transverse filaments, which may be associated with development of alternative reproductive strategies other than amphimixis, as in nematodes. Of the 15 synaptonemal complexes present, only the one carrying the nucleolus organizer region could be clearly identified from one nucleus to the next. The nucleolar organizer region was on the average 0.75 μm from the telomere in both zygotene and pachytene nuclei. There were an average of three recombination nodules in each nucleus. Synaptonemal complexes have been reported in over 80 different species of fungi and related protista. Karyotypic evolution in the oomycetes and fungi may be the result of poly-ploidization, followed by cytogenetic diversification involving aneuploidy and differing degrees of polyploidy. Such a sequence of events could explain the apparent polyphyletic formation of this group. Key words: karyotype, Oomycetes, pachytene, synaptonemal complexes, three-dimensional reconstruction.


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.


Genetics ◽  
1979 ◽  
Vol 92 (2) ◽  
pp. 511-541
Author(s):  
Adelaide T C Carpenter

ABSTRACT Electron microscope serial section reconstruction analysis of all zygotene-pachytene nuclei of meiotic cells from three wild-type germaria (a subunit of the ovary containing the early meiotic stages arrayed in temporal developmental sequence) of Drosophila melanogaster females corroborates and extends earlier observations (CARPENTER 1975a) on the nature and sequence of ultrastructural events occurring during the time of meiotic recombination. Emphasis has been placed on (1) the time of appearance and disappearance of the synaptonemal complex (SC) and the changes in its dimensions that accompany a cell's progression through pachytene, and (2) the appearance, disappearance, number and chromosomal locations of recombination nodules (CARPENTER 1975b). For both the SC and the recombination nodule the availability of several developmental series has provided an estimate of the biological variability in the properties of these recombination-associated structures. The much more extensive data presented here substantiate the earlier hypothesis that recombination nodules occur at sites where reciprocal meiotic recombination will occur, has occurred, or is occurring. A second morphological type of recombination nodule is reported; it is suggested that the presence of the latter type of nodule may correlate with sites of gene conversion. The hypothesis that there may be two types of meiotic recombination processes is discussed.


2021 ◽  
Author(s):  
Liangyu Zhang ◽  
Weston Stauffer ◽  
David Zwicker ◽  
Abby F. Dernburg

AbstractMeiotic recombination is highly regulated to ensure precise segregation of homologous chromosomes. Evidence from diverse organisms indicates that the synaptonemal complex (SC), which assembles between paired chromosomes, plays essential roles in crossover formation and patterning. Several additional “pro-crossover” proteins are also required for recombination intermediates to become crossovers. These typically form multiple foci or recombination nodules along SCs, and later accumulate at fewer, widely spaced sites. Here we report that in C. elegans CDK-2 is required to stabilize all crossover intermediates and stabilizes interactions among pro-crossover factors by phosphorylating MSH-5. Additionally, we show that the conserved RING domain proteins ZHP-3/4 diffuse along the SC and remain dynamic following their accumulation at recombination sites. Based on these and previous findings we propose a model in which recombination nodules arise through spatially restricted biomolecular condensation and then undergo a regulated coarsening process, resulting in crossover interference.


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