The desynaptic mutant of maize as a combined defect of synaptonemal complex and chiasma maintenance

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.

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.


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.


1984 ◽  
Vol 71 (1) ◽  
pp. 159-176 ◽  
Author(s):  
S.M. Stack

A combined light- and electron-microscopic examination of chromosomes from two angiospermous plants, Plantago ovata and Lycopersicon esculentum, and a mammal, Mus musculus, was performed. From this investigation three observations have been made that may be relevant to the observed lack of crossing over in heterochromatin. (1) Differential staining indicates that heterochromatin represents a smaller fraction of the length of pachytene chromosomes than it represents in the length of mitotic metaphase chromosomes. Since the synaptonemal complex (SC) runs throughout the length of these pachytene chromosomes, it is under-represented in heterochromatin. Considering the evidence for a rough correlation between the length of SC and the amount of crossing over, this could result in less crossing over in heterochromatin than expected on the basis of its length in mitotic metaphase chromosomes. (2) Electron microscopy indicates that, unlike the SC in euchromatin, the SC in heterochromatin is densely ensheathed in highly compact chromatin. If crossing over occurs in the SC or even in the surrounding chromatin, the compaction of the chromatin may prevent the penetration of enzymes needed in recombination. (3) Finally, a difference in the structure of SCs in euchromatin versus heterochromatin was observed that could be associated with the lack of crossing over in heterochromatin.


2021 ◽  
Author(s):  
Rosario Ortiz ◽  
Olga M Echeverria ◽  
Sergej Masich ◽  
Christer Hoog ◽  
Abrahan Hernandez-Hernandez

Genetic variability in sexually reproducing organisms results from an exchange of genetic material between homologous chromosomes. The genetic exchange mechanism is dependent on the synaptonemal complex (SC), a protein structure localized between the homologous chromosomes. Current structural models of the SC are based on electron microscopy, super resolution, and expansion microscopy studies using chemical fixatives and sample dehydration of gonads, which are methodologies known to produce structural artifacts. We have developed a novel electron microscopy sample-preparation approach where pachytene cells are isolated from mouse testis by FACS, followed by cryo-fixation and cryo-substitution to achieve visualization of a close-to-native structure of the SC. We found that the central region of the SC was wider than previously recognized, and the transverse filaments more densely packed in the central region. Furthermore, we identified a structure nucleating the central element of the SC.


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.


2017 ◽  
Author(s):  
Divya Pattabiraman ◽  
Baptiste Roelens ◽  
Alexander Woglar ◽  
Anne M. Villeneuve

AbstractDuring meiotic prophase, a structure called the synaptonemal complex (SC) assembles at the interface between aligned pairs of homologous chromosomes, and crossover recombination events occur between their DNA molecules. Here we investigate the inter-relationships between these two hallmark features of the meiotic program in the nematode C. elegans, revealing dynamic properties of the SC that are modulated by recombination. We demonstrate that the SC incorporates new subunits and switches from a more highly dynamic/labile state to a more stable state as germ cells progress through the pachytene stage of meiotic prophase. We further show that the more dynamic state of the SC is prolonged in mutants where meiotic recombination is impaired. Moreover, in meiotic mutants where recombination intermediates are present in limiting numbers, SC central region subunits become preferentially stabilized on the subset of chromosome pairs that harbor a site where pro-crossover factors COSA-1 and MutSγ are concentrated. Polo-like kinase PLK-2 becomes preferentially localized to the SCs of chromosome pairs harboring recombination sites prior to the enrichment of SC central region proteins on such chromosomes, and PLK-2 is required for this enrichment to occur. Further, late pachytene nuclei in a plk-2 mutant exhibit the more highly dynamic SC state. Together our data demonstrate that crossover recombination events elicit chromosome-autonomous stabilizing effects on the SC and implicate PLK-2 in this process. We discuss how this recombination-triggered modulation of SC state might contribute to regulatory mechanisms that operate during meiosis to ensure the formation of crossovers while at the same time limiting their numbers.


Genome ◽  
1993 ◽  
Vol 36 (5) ◽  
pp. 797-807 ◽  
Author(s):  
M. P. Maguire ◽  
R. W. Riess ◽  
A. M. Paredes

Homozygotes for the dsy1 desynaptic mutant of maize show massive failure of chiasma maintenance during diplotene and diakinesis. Although some chiasmata persist until anaphase I in most microsporocytes expressing this mutant, homozygotes are completely or nearly completely sterile, owing apparently to disjunctive irregularities. Pachytene synaptic errors and some synaptic failure also are found, but recombination nodules are common in homologously synapsed regions, and equational separation of a heterozygous knob into univalents or open arms at diakinesis clearly demonstrates that chiasma failure occurs following crossing-over. A wider than normal synaptonemal complex central region and uniform apparent weakness of central region cross connections to spreading procedures strongly suggest the presence of a genetic lesion in a synaptonemal complex central region component. The dsy1 mutant may provide an especially important source of material for molecular studies on the nature of chiasma maintenance mechanism.Key words: chiasma maintenance, synaptonemal complex, meiotic mutant.


Genetics ◽  
1990 ◽  
Vol 126 (3) ◽  
pp. 563-574 ◽  
Author(s):  
B Rockmill ◽  
G S Roeder

Abstract The Saccharomyces cerevisiae red1 mutant fails to assemble synaptonemal complex during meiotic prophase. This mutant displays locus-specific reductions in interchromosomal gene conversion and a moderate reduction in crossing over. The occurrence of a significant amount of meiotically induced recombination in the red1 mutant indicates that the synaptonemal complex is not absolutely required for meiotic exchange. The RED1 gene product is required for intrachromosomal recombination in some assays but not others. Chromosomes that have undergone reciprocal exchange nevertheless nondisjoin in red1 mutants, indicating that crossovers are not sufficient for disjunction. Epistasis studies reveal that HOP1 is epistatic to RED1, and that RED1 acts in an independent pathway from MER1. A model for the function of the RED1 gene product in chromosome synapsis is discussed.


Genetics ◽  
2003 ◽  
Vol 163 (4) ◽  
pp. 1337-1356 ◽  
Author(s):  
Adelaide T C Carpenter

Abstract The meiotic phenotypes of two mutant alleles of the mei-W68 gene, 1 and L1, were studied by genetics and by serial-section electron microscopy. Despite no or reduced exchange, both mutant alleles have normal synaptonemal complex. However, neither has any early recombination nodules; instead, both exhibit high numbers of very long (up to 2 μm) structures here named “noodles.” These are hypothesized to be formed by the unchecked extension of identical but much shorter structures ephemerally seen in wild type, which may be precursors of early recombination nodules. Although the mei-W68L1 allele is identical to the mei-W681 allele in both the absence of early recombination nodules and a high frequency of noodles (i.e., it is amorphic for the noodle phene), it is hypomorphic in its effects on exchange and late recombination nodules. The differential effects of this allele on early and late recombination nodules are consistent with the hypothesis that Drosophila females have two separate recombination pathways—one for simple gene conversion, the other for exchange.


Genetics ◽  
2003 ◽  
Vol 163 (2) ◽  
pp. 539-544 ◽  
Author(s):  
Hasanuzzaman Bhuiyan ◽  
Gunilla Dahlfors ◽  
Karin Schmekel

Abstract The synaptonemal complex (SC) keeps the synapsed homologous chromosomes together during pachytene in meiotic prophase I. Structures that resemble stacks of SCs, polycomplexes, are sometimes found before or after pachytene. We have investigated ndt80 mutants of yeast, which arrest in pachytene. SCs appear normal in spread chromosome preparations, but are only occasionally found in intact nuclei examined in the electron microscope. Instead, large polycomplexes occur in almost every ndt80 mutant nucleus. Immunoelectron microscopy using DNA antibodies show strong preferential labeling to the lateral element parts of the polycomplexes. In situ hybridization using chromosome-specific probes confirms that the chromosomes in ndt80 mutants are paired and attached to the SCs. Our results suggest that polycomplexes can be involved in binding of chromosomes and possibly also in synapsis.


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