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Chromosome pairing in wild-type wheat closely resembles the process in both yeast and Drosophila. The recent characterisation of a mutant Ph1 wheat and the observation that chromosome pairing in the absence of Ph1 more closely resembles that of mammals and maize has shed light on the evolution of chromosome pairing in the cereals.
Chiasmate pairing between homoeologous chromosomes at metaphase I (MI) of meiosis in wheat is prevented by the activity of the Ph1 locus on chromosome 5B. Several hypotheses have been proposed sharing the assumption that Ph1 regulates MI chromosome pairing by regulating centromere-mediated chromosome alignment before the onset of meiosis. To test the relevance of the putative predetermination of chromosome pairing at MI by the centromere-mediated chromosome association prior to meiosis, a 2BL.2RL homoeoisochromosome was constructed and its MI pairing was assessed in the presence and absence of the Ph1 locus. Although the 2BL and 2RL arms of the homoeoisochromosome paired with each other at MI in the absence of Ph1, they never paired with each other at MI in the presence of Ph1. Since the two arms were permanently associated in the homoeoisochromosome via a common centromere, it is unlikely that Ph1 predetermines MI pairing between homoeologous chromosomes solely by controlling premeiotic association of centromeres. These findings are consistent with the idea that Ph1 determines the chromosome pairing pattern at MI by scrutinizing homology across the entire chromosome.
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To understand how the meiotic spindle is formed and maintained in higher plants, we studied the organization of microtubule arrays in wild-type maize meiocytes and three maize meiotic mutants, desynaptic1 (dsy1), desynaptic2 (dsy2), and absence of first division (afd). All three meiotic mutations have abnormal chromosome pairing and produce univalents by diakinesis. Using these three mutants, we investigated how the absence of paired homologous chromosomes affects the assembly and maintenance of the meiotic spindle. Before nuclear envelope breakdown, in wild-type meiocytes, there were no bipolar microtubule arrays. Instead, these structures formed after nuclear envelope breakdown and were associated with the chromosomes. The presence of univalent chromosomes in dsy1, dsy2, and afd meiocytes and of unpaired sister chromatids in the afd meiocytes did not affect the formation of bipolar spindles. However, alignment of chromosomes on the metaphase plate and subsequent anaphase chromosome segregation were perturbed. We propose a model for spindle formation in maize meiocytes in which microtubules initially appear around the chromosomes during prometaphase and then the microtubules self-organize. However, this process does not require paired kinetochores to establish spindle bipolarity.
Meiotic chromosome pairing of primary trisomics of rye was analysed by electron microscopy in surface-spread prophase I nuclei and compared with light-microscopic observations of metaphase I cells. Despite the large-sized chromosomes of rye, prophase I trivalent frequencies were close to the two thirds expected on a simple model with two terminal independent pairing initiation sites per trisome (set of three homologous chromosomes). Direct observations mostly reveal one pairing partner switch (PPS) in prophase I trivalents, which confirms this supposition. There were no significant differences between the number of trivalent and bivalent plus univalent configurations observed at prophase and metaphase I; therefore, synapsed segments form chiasmata. In all of the trisomics, the three homologues showed variations not only in the number of telomeric C-bands but also in the amount of heterochromatin of these bands, which allowed identification of chromosomes or chromosome arms associated in most metaphase I configurations. In trisomics for chromosomes 2, 3 and 5, some metaphase I chromosome configuration frequencies did not fit those expected under the assumption of random chromosome association among all partners, suggesting the existence of preferences for pairing between two given chromosome arms of the trisome. No preferential associations either at metaphase I or pachytene were observed in the trisomics for chromosome 6. The fit between theoretical pairing models and the experimental data is also discussed.
Rye chromosomes were selectively stained in the meiosis of triticale by means of heterochromatin banding techniques. Compared to wheat chromosomes, rye chromosomes showed reduced pairing at first meiotic metaphase. Within the rye genome this pairing failure was associated with the presence of large, terminal heterochromatic bands. Since these terminal bands of rye chromosomes are late replicating, the effect of heterochromatin could arise from an overlap between the processes of chromosome replication and chromosome pairing.
Using Giemsa staining, C-banding and Ag-NOR staining techniques, we analyzed chromosomes in adult male and female Hynobius quelpaertensis and in embryos of this species in egg sacs collected from eight localities of Cheju Island, South Korea. Chromosome pair 21 was consistently homomorphic in male specimens, while it was heteromorphic in female specimens, suggesting the occurrence of ZZ/ZW sex chromosome constitution in this species. The W chromosome, being much larger than the Z chromosome, was of three morphologically distinct types: WA, WB and WC. Lampbrush chromosomes examined in the oocytes of one female specimen having the WA chromosome showed that the short arm of the WA chromosome and the long arm of the Z chromosome paired closely and hence are genetically homologous. We also tried to analyze the structural relationship among the three types of W chromosomes based on their C-banding and Ag-NOR patterns.
Human pachytene chromosome pairs have been characterized electron microscopically in spread preparations on the basis of synaptonemal complex length, kinetochore position and attached nucleoli when present. The X and Y chromosomes can be followed by their filamentous axial cores from partial synapsis, through precocious disjuction and end-to-end attachment, to differentiation of a network in the sex chromosome pair.
A Neurospora crassa mutation, mei-2, affecting recombination and pairing of homologous chromosomes during meiosis, was characterized for its effect on repeat-induced point mutation (RIP). We found that RIP, which depends on recognition of DNA sequence homology, is not inhibited by mei-2, suggesting that the defect in chromosome pairing of this mutant is not due to a defect in DNA pairing and that DNA pairing is not dependent on chromosome pairing.
Mechanistic and regulatory aspects of meiotic chromosome pairing and segregation have received increasing attention in recent years. This review is concerned with the role of chromosomal sites and chromosome organization in pairing and sperm development in Drosophila. Two major topics are reviewed. The first concerns the distribution and identification of meiotic pairing sites in male Drosophila. Cytogenetic data show that pairing sites are distributed widely in the euchromatin of autosomes but are absent from centromeric heterochromatin. The reverse distribution holds for the X, where the major pairing site is located in the central region of the centric heterochromatin, co-mapping with the rDNA locus. Recent transgenic studies have demonstrated that this pairing site consists mainly of a 240-bp repeated sequence in the intergenic spacers of the rDNA repeats. These spacer repeats contain RNA polymerase I promoters, which must be functional for the repeats to have pairing activity, suggesting a mechanistic connection between pairing and transcription. The general idea that pairing sites coincide with transcribed sequences is discussed. The second major topic involves the effects of sex chromosome rearrangements on spermiogenesis. A variety of rearrangements involving the sex chromosomes, including heterochromatic deletions and translocations with autosomes, have been shown to lead either to meiotic drive or to sterility. Recent evidence strongly implicates the X chromosome pairing site in the etiology of these effects. These findings are discussed in terms of a novel model that interprets the spermiogenic disruptions associated with sex chromosome rearrangements as resulting from disabling of spermatids due to triggering of a checkpoint concerned with monitoring chromosome alignment at meiotic metaphase.
Pairing of homologous chromosomes is important for homologous recombination and correct chromosome segregation during meiosis. It has been proposed that telomere clustering, nuclear oscillation, and recombination during meiotic prophase facilitate homologous chromosome pairing in fission yeast. Here we examined the contributions of these chromosomal events to homologous chromosome pairing, by directly observing the dynamics of chromosomal loci in living cells of fission yeast. Homologous loci exhibited a dynamic process of association and dissociation during the time course of meiotic prophase. Lack of nuclear oscillation reduced association frequency for both centromeric and arm regions of the chromosome. Lack of telomere clustering or recombination reduced association frequency at arm regions, but not significantly at centromeric regions. Our results indicate that homologous chromosomes are spatially aligned by oscillation of telomere-bundled chromosomes and physically linked by recombination at chromosome arm regions; this recombination is not required for association of homologous centromeres.
Meiotic chromosome pairing is a process that is amenable to genetic and experimental analysis. The combined use of these two approaches allows for the process to be dissected into several finite periods of time in which the developmental stages of pairing can be precisely located. Evidence is now available, in particular in plants, that shows that the pairing of homologous chromosomes, as observed at metaphase I, is affected by events occurring as early as the last premeiotic mitosis; and that the maintenance of this early determined state is subsequently maintained by constituents (presumably proteins) that are sensitive to either colchicine, temperature or gene control. A critical assessment of this evidence in wheat and a comparison of the process of pairing in wheat with the course of meiotic pairing in other plants and animals is presented.
Homologous chromosome pairing is a central feature of meiosis I, contributing to the correct segregation of chromosomes during meiosis. The fission yeast, Schizosaccharomyces pombe, has been widely used to study meiotic chromosome dynamics, partly because studies in this yeast are simplified due to the lack of post-pairing synaptic structures. Chromosome pairing in Sz. pombe occurs differentially throughout the genome. Telomeres cluster at the spindle pole body (SPB) at the onset of meiosis, imposing a spatial restriction on pairing events. Subsequently, centromeres dissociate from the SPB and pair in a recombination- and heterochromatin (Swi6)-independent fashion. Pairing of telomere distal regions occurs during meiotic prophase, concomitant with a dynamic association/dissociation of homologous regions, with interhomologue associations becoming increasingly stable. The stabilization of paired regions is enhanced by factors required for the initiation of meiotic recombination, suggesting that recombination stabilizes paired regions. However, substantial pairing is initiated in the absence of recombination; this is dependent upon another factor, the conserved Meu13 protein, demonstrating that recombination is not required for initial pairing interactions. During meiotic prophase Sz. pombe exhibits a pronounced dynein-dependent nuclear oscillation, which drives the pairing of centromeric and interstitial regions. Dynein is also required for the significant levels of achiasmate reductional segregation observed in Sz. pombe, possibly implicating the centromere-associated pairing with achiasmate homologue segregation. Whilst Sz. pombe does not form discernable synaptic structures continuously along the meiotic chromosomes, it does form proteinacious, meiosis-specific, linear structures (linear elements). However, the role, if any, of these structures in mediating homologue pairing is unknown.
Control of homoeologous chromosomal pairing in hexaploid wheat stems from a balance between a number of suppressor and promoter genes. This study used centromeric behaviour as a tool to investigate the mechanism. Fluorescent in situ hybridization employing centromeric and telomeric sequences as probes was applied to pollen mother cells of wheat and wheat/alien hybrids having different pairing gene combinations. It showed: association of centromeres during pre-meiotic interphase; decondensation of centromeric structure; sister chromatid disjunction of univalent chromosomes in homoeologous pairing situations at anaphase I; and centromeric stretching between univalent sister chromatids in wheat/rye hybrids deficient for pairing genes. The implications of these results are discussed.
In tetraploid rye with single-substitution wheat chromosomes - 1A, 2A, 5A, 6A, 7A, 3B, 5B, 7B - chromosome pairing was analysed at metaphase I in PMCs with the C-banding method. The frequency of univalents of chromosome 1A was considerably higher than that of the other four wheat chromosomes of genome A (6A, 5A, 7A and 2A). Among chromosomes of genome B, the lowest mean frequency of univalents was observed for chromosome 5B. In monosomic lines, wheat chromosomes 1A, 2A, 5A, 6A, 7A and 5B paired with rye homoeologues most often in rod bivalents and in chain quadrivalents (also including 3B). The 47% pairing of 5B-5R chromosomes indicate that the rye genomes block the suppressor Ph1 gene activity. In monosomic plants with chromosomes 5A, 2A, 6A, 7A and 5B, a low frequency of rye univalents was observed. It was also found that the wheat chromosomes influenced the pairing of rye genome chromosomes, as well as the frequency of ring and rod bivalents and tri- and quadrivalents. However, the highest number of terminal chiasmata per chromosome occurred in the presence of chromosomes 5A and 2A, and the lowest - in the presence of chromosomes 3B and 7B. In the presence of chromosome 5B, the highest frequency of bivalents was observed. The results of the present study show that the rye genome is closer related to the wheat genome A of than to genome B. The high pairing of wheat-rye chromosomes, which occurs in tetraploid rye with substitution wheat chromosomes, indicates that there is a high probability of incorporating wheat chromosome segments into rye chromosomes.
The him-8 gene is essential for proper meiotic segregation of the X chromosomes in C. elegans. Here we show that loss of him-8 function causes profound X chromosome-specific defects in homolog pairing and synapsis. him-8 encodes a C2H2 zinc-finger protein that is expressed during meiosis and concentrates at a site on the X chromosome known as the meiotic pairing center (PC). A role for HIM-8 in PC function is supported by genetic interactions between PC lesions and him-8 mutations. HIM-8 bound chromosome sites associate with the nuclear envelope (NE) throughout meiotic prophase. Surprisingly, a point mutation in him-8 that retains both chromosome binding and NE localization fails to stabilize pairing or promote synapsis. These observations indicate that stabilization of homolog pairing is an active process in which the tethering of chromosome sites to the NE may be necessary but is not sufficient.
Chromatin rearrangements in the meiotic prophase are characterized by the assembly and disassembly of synaptonemal complexes (SC), a protein structure that stabilizes the pairing of homologous chromosomes in prophase. We report the identification of human and mouse cDNA coding for stromalin 3 (STAG3), a new mammalian stromalin member of the synaptonemal complex. The stromalins are a group of highly conserved proteins, represented in several organisms from yeast to humans. Stromalins are characterized by the stromalin conservative domain (SCD), a specific motif found in all proteins of the family described to date. STAG3 is expressed specifically in testis, and immunolocalization experiments show that STAG3 is associated to the synaptonemal complex. As the protein encoded by the homologous gene (Scc3p) in Saccharomyces cerevisiae was found to be a subunit of a cohesin complex that binds chromosomes until the onset of anaphase, our data suggest that STAG3 is involved in chromosome pairing and maintenance of synaptonemal complex structure during the pachytene phase of meiosis in a cohesin-like manner. We have mapped the human STAG3 gene to the 7q22 region of chromosome 7; six human STAG3-related genes have also been mapped: two at 7q22 near the functional gene, one at 7q11.22, and three at 7q11.23, two of them flanking the breakpoints commonly associated with the Williams-Beuren syndrome (WBS) deletion. Since the WBS deletion occurs as a consequence of unequal meiotic crossing over, we suggest that STAG3 duplications predispose to germline chromosomal rearrangement within this region.
This article aims to study the homoeologous chromosome pairing and translocation induced by 5A/5R x 6A/6R wheat-rye substitution lines. To clarify the mechanism of homoeologous chromosome pairing and create wheat-rye translocation lines, two wheat-rye substitution lines, 5A/5R and 6A/6R were crossed. The chromosome behavior of pollen mother cells (PMCs) in meiosis was investigated in hybrid F1. Homoeologous chromosome pairing between wheat and rye occurred in 22.91% of PMC. Wheat-rye translocation lines were identified via C-banding and in situ hybridization (GISH) in hybrid F2 and later generations. In F2 generation, translocations happened in 9 of 45 plants, reached to 20%. These translocation lines were generated from homoeologous chromosome pairing, or mis-division and reconstruction of univalent chromosomes.