Complete meiotic pairing of crested newt chromosomes.

The longest chromosome (number 1) of Trituturus cristatus carries a heteromorphic segment, a heterozygosity perpetuated by a balanced lethal system. The heteromorphic segment is regarded as achiasmate and has been claimed to be asynaptic. Direct observations of chromosome pairing in spermatocytes and oocytes yield some cases where all homologous chromosomes appear to be completely paired, but the individual bivalents could not be identified as pachytene is not particularly clear in this species. The long arms of bivalent 1 usually remain attached by a terminal chiasma in spermatocytes of T. c. cristatus but the corresponding chiasma is only rarely present in T. c. carnifex spermatocytes. Synaptonemal complexes have been measured in both spermatocytes and oocytes of T. c. cristatus. A karyotype constructed from these measurements matches the main features of somatic and lampbrush chromosome karyotypes, indicating that all chromosomes must be completely paired and proportionately represented as synaptonemal complex. The total length of synaptonemal complex is much the same in spermatocytes and oocytes and is similar to the length in spermatocytes of Xenopus laevis. These two amphibian examples supplement a recent survey of other vertebrate classes to reinforce its conclusion that synaptonemal complex length is not related to genome size in vertebrates.     

Centromere pairing precedes meiotic chromosome pairing in plants

Meiosis is a specialized eukaryotic cell division, in which diploid cells undergo a single round of DNA replication and two rounds of nuclear division to produce haploid gametes. In most eukaryotes, the core events of meiotic prophase I are chromosomal pairing,synapsis and recombination. To ensure accurate chromosomal segregation, homologs have to identify and align along each other at the onset of meiosis. Although much progress has been made in elucidating meiotic processes, information on the mechanisms underlying chromosome pairing is limited in contrast to the meiotic recombination and synapsis events. Recent research in many organisms indicated that centromere interactions during early meiotic prophase facilitate homologous chromosome pairing, and functional centromere is a prerequisite for centromere pairing such as in maize. Here, we summarize the recent achievements of chromosome pairing research on plants and other organisms, and outline centromere interactions, nuclear chromosome orientation,and meiotic cohesin, as main determinants of chromosome pairing in early meiotic prophase.     

The mechanism of meiotic homologue pairing

Homologous chromosome pairing involves the moving together of matching chromosomes or chromosome segments across substantial distances within a nucleus. Although the time in the life cycle of initial association of homologues varies among organisms, it may well be that similar underlying mechanisms for its occurrence prevail throughout sexually reproducing eukaryotes. The means by which pairing its accomplished is in no case understood. In the apparent absence of a long range specific force of attraction, simple partial models have been proposed which relay for the most part upon interactions of chromosome ends (telomeres) with specialized portions of the nuclear envelope. While such interactions, as well as the persistence of chromosome orientation established by mitotic anaphase poleward movement of centromere regions, may provide in many cases for closer than random positioning of some parts of homologues, the distances remaining to be traversed are still long range in physical-chemical terms. Also, the specific pairing observed in some kinds of rearranged segments is not facilitated by such circumstances, even if synapsis is initiated at available homologous telomere pairs and proceeds to completion by a "zip-up" process. A unified, more complex model is considered which is designed to accommodate the various relevant findings. It invokes the interaction of intranuclear structures with intercalary and/or terminal chromosomal pairing sites, e.g. filamentous structures which specifically bind to these, and a contractile system involving proteins such as actin and myosin to draw homologues together.     

GISH analysis of meiotic chromosome pairing in Solanum lycopersicoides introgression lines of cultivated tomato.

Meiotic chromosome pairing was studied in introgression lines of cultivated tomato, Lycopersicon esculentum (= Solanum lycopersicum), containing 1 or 2 chromosome segments from the wild species Solanum lycopersicoides. Genomic in situ hybridization (GISH) was used to compare the relative lengths at diakinesis of the different introgressed segments and to measure the chiasmate arm frequency for the chromosome pair involved in the introgression(s). Longer segments generally produced stronger GISH signals than shorter segments. GISH signal intensity also depended on whether or not an introgressed segment encompassed the centromeric region. For example, a 29 cM segment that included the centromeric region produced a stronger GISH signal than a 42 cM segment that did not. In each line the chromosome arm containing the homeologous segment showed a reduction in chiasmate arm frequency that was most pronounced in lines with long segments. This reduction was accompanied by an increased chiasmate arm frequency on the other arm. Double introgression lines, heterozygous in repulsion phase for 2 introgressions on opposite chromosome arms, showed a lower frequency of chiasmata than single introgression lines. Pairing failure, indicated by the presence of univalents, was highest in the double introgression and whole chromosome substitution lines. These results are discussed with respect to observations of suppressed recombination in these stocks and potential practical implications for reducing linkage drag in breeding programs.     

Genesis of bivalent pairing in hexaploid clump Verbena

Both 6x Verbena aubletia (n=15) and 2x V. tenuisecta (n=5) form bivalents during meiosis, however, their 4x F₁ hybrid (V. aubletia × V. tenuisecta) shows almost complete homoeologous pairing involving on average 19.74 out of its 20 chromosomes. In 10% cells there are 4IV+2II indicating that essentially there may be 4 homoeologous sets of 5 chromosomes each in the F₁ hybrid. Evidently, V. aubletia is segmental allo-hexaploid involving 3 homoeologous genomes (A₁A₁ A₂A₂ A₃A₃). Whether its cytologically diploid behaviour is the result of a multivalent suppressor system or due to an acute property of preferential pairing, cannot be answered with certainty. In either case intergenomal homoeologies are totally suppressed resulting in bivalent pairing, meiotic isolation of the 3 genomes and institution of normal fertility.     

The meiotic pairing of nine wheat chromosomes

Summary The meiotic identification of nine pairs of chromosomes at metaphase I of meiosis of Triticum aestivum (B genome, 4A and 7A) has been achieved using a Giemsa C-banding technique. As a result, the analysis of the pairing of each chromosome arm in disomic and monosomic intervarietal hybrids between Chinese Spring and the Spanish cultivar Pané 247 could be carried out. Differences in the chiasmata frequencies per chromosome arm cannot be explained on the basis of relative arm lengths only. Possible effects of arm-to-arm heterochromatic differences on meiotic pairing are discussed.     

Chromosome-associated control of meiotic pairing differentiation. Variation within Secale cereale

The frequency of association of two specific chromosome arms in marked (telocentric) trisomics is reported for different chromosome genotypes, and compared with expected frequencies with random pairing. It appears that gross-structurally identical but genetically slightly different chromosomes of the same species, although they pair very efficiently in the diploid, show considerable variation in respect to association in a competitive situation in trisomies. The critical sites can be transferred by corssing over, thus changing the pairing pattern. The two arms of one chromosome are independent in respect to their pairing properties.     

Estimating meiotic chromosome pairing and recombination parameters in telocentric trisomics.

Telocentric trisomics (telotrisomics; one arm of a metacentric chromosome present in addition to two complete genomes) are used in theoretical studies of pairing affinities and chiasma formation in competitive situations and applied in genome analysis, gene localization, gene transfer, and breakage of close linkages. These applications require knowledge of the recombination characteristics of telotrisomics. Appropriate cytological and molecular markers and favorable chromosome morphology are not always available or applicable for quantitative analyses. We developed new mathematical models for extracting the maximum information from simple metaphase I observations. Two types of telotrisomics of the short arm of chromosome 1R of rye (Secale cereale), including several genotypes, were used as test material. In simple telotrisomics, pairing between morphologically identical complete chromosomes was more frequent than pairing between the telocentric and either of the normal chromosomes. In the telocentric substitution, morphologically identical telocentrics paired less frequently with each other than either one with the normal chromosome. Pairing partner switch was significant. Interaction between the two arms was variable. Variation within plants was considerable. Telotrisomics without markers are suitable for analyzing pairing preferences, for gene localization and gene transfer, and for breaking tight linkages, but less so for genome analysis.     

Homolog pairing and meiotic progression in Coprinus cinereus

We have used fluorescence in situ hybridization to examine homolog pairing during the synchronous meiosis of the basidiomycete Coprinus cinereus. Using spread preparations of meiotic nuclei, we confirmed previous studies that showed that at 6 h post-karyogamy essentially all meiotic nuclei are in pachytene. We found that homolog pairing occurs rapidly after karyogamy, that a 1 Mb chromosome does not associate more quickly than a 2.5 Mb chromosome, and that interstitial, single-copy sites can associate stably prior to nucleolar fusion. Analysis of two probes for the same pair of homologs revealed that by 4 h after karyogamy each chromosome examined was at least partially paired in all meiotic cells. In addition, these studies showed that chromatin condensation increases after pairing and that chromatin shows stable compaction at pachytene. Received: 4 January 1999; in revised form: 22 June 1999 / Accepted: 20 July 1999     

The distribution of male meiotic pairing sites on chromosome 2 of Drosophila melanogaster: meiotic pairing and segregation of 2-Y transpositions

The distribution of meiotic pairing sites on a Drosophila melanogaster autosome was studied by characterizing patterns of prophase pairing and anaphase segregation in males heterozygous for a number of 2-Y transpositions, collectively coveringall of chromosome arm 2R and one-fourth of chromosome arm 2L. It was found that all transpositions involving euchromatin from chromosome 2, even short stretches, increased the frequency of prophase I quadrivalents involving the sex and second chromosome bivalents above background levels. Quadrivalent frequencies were the same whether the males carried both elements of the transposition or just the Dp (2;Y) element along with two normal chromosome 2s, indicating that pairing is non-competitive. The frequency of quadrivalents was proportional to the size of the transposed region, suggesting that pairing sites are widely distributed on chromosome 2. Moreover, all but the smallest transpositions caused a detectable bias in the segregation ratio, in favor of alternate segregations, indicating that the prophase associations were effective in orienting centromeres to opposite poles. One transposition involving only heterochromatin of chromosome 2 had no effect on quadrivalent frequency, consistent with previous evidence that autosomal heterochromatin lacks meiotic pairing ability in males. One region at the base of chromosome arm 2L proved to be especially effective in stimulating quadrivalent formation and anaphase segregation, indicating the presence of a strong pairing site in this region. It is concluded that autosomal pairing in D. melanogaster males is based on general homology, despite the lack of homologous recombination.by A.C. Spradling     

Genetic control of bivalent pairing in the Avena strigosa polyploid complex

Bivalent pairing in the tetraploid oat A. barbata, the main tetraploid form of A. strigosa polyploid complex, was found to be determined by a single recessive gene in quadriplex condition. This gene segregated in tetrasomic fashion in the A. barbata × A. strigosa autopolyploid, which indicates conspicuously autopolyploid origin of A. barbata and close relationships between the two chromosome sets of this oat, and the chromosomes of the diploid oat A. strigosa. It was speculated that the gene affecting bivalent pairing in A. barbata was evolved already at the diploid level in one of the A. strigosa races and had been recovered in quadriplex state following polyploidization of an intervarietal A. strigosa hybrid.     

Alteration of meiotic chromosomal pairing and synaptonemal complexes by cycloheximide

When cells are exposed to cycloheximide during the synaptic period of meiotic prophase, the structure of the synaptonemal complex is markedly altered. The bulk of the lateral component is removed. When lily zygotene microsporocytes are subsequently transferred into a culture medium free from cycloheximide, normal synaptonemal complexes are again seen. Modification of the structure of the synaptonemal complex by treatment with cycloheximide for 4 days has little permanent effect on meiosis except at late zygonema or early pachynema. Treatment at this time produces meiocytes in which no synaptonemal complexes reform. When these cells proceed into diplotene and diakinesis they are devoid of chiasmatic chromosomes. The data suggest that the synaptonemal complex is essential if chiasmata are to be formed, and that a unique period exists when the formation can be interrupted.This work was supported by grants from the National Science Foundation (GB 5173X and GB 6476) and the National Institutes of Health (GM 16882).     

Ultrastructure of meiotic pairing in B chromosomes of Crepis capillaris

The meiotic pairing behaviour of four B isochromosomes of Crepis capillaris was studied by synaptonemal complex (SC) surface spreading of pollen mother cells. The four B chromosomes form a tightly associated group, separate from the standard chromosomes, throughout zygotene and pachytene. All four B chromosomes are also folded around their axis of symmetry, the centromere, and the eight homologous arms are closely aligned from the earliest prophase I stages. A high frequency of multivalent pairing of the four B chromosomes is observed at pachytene, in excess of 90%, mirroring the situation observed at metaphase I but exceeding the frequency expected (76.2%) on the assumption of random pairing among the eight B isochromosome arms with a single distal pairing initiation site per arm. The higher than expected frequency of multivalents is due to the occurrence of multiple pairing initiations along the B isochromosome arms, resulting in high frequencies of pairing partner switches. Pairing of the standard chromosome set is frequently incomplete in the presence of four B chromosomes, and abnormalities of SC structure such as thickening and splitting of axes and lateral elements are also frequently seen. Similarly, B chromosomes show partial pairing failure, the extent of which is correlated with pairing failure in the standard chromosome set. The B chromosomes themselves also show abnormalities of SC structure. Both standard and B chromosomes show non-homologous foldback pairing of regions that have failed to pair homologously.by D. Schweizer     

The initiation of meiotic chromosome pairing: the cytological view

Opposing views are held with respect to the time when and the mechanisms whereby homologous chromosomes find each other for meiotic synapsis. On the one hand, some evidence has been presented for somatic homologous associations or some other kind of relationship between chromosomes in somatic cells as a preliminary to meiotic pairing. On the other hand, it is argued by many that homologous contacts are first established at meiotic prophase prior to, or in the course of, synaptonemal complex formation. The present paper reviews the controversial cytological evidence, hypotheses, and ideas on how the first contact between homologous chromosomes comes about.     

Inferences from genetical evidence on the course of meiotic chromosome pairing in plants.

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.     

Non-homologue pairing and spontaneous meiotic interchanges in Drosophila melanogaster females

Spontaneous interchange between the X chromosomes and the C(2L) autosomal compound in their centromeric regions was studied in y/XY;C(2L);C(2R) and In(1)dl-49+BM1/XY;C(2L);C(2R) Drosophila melanogaster females. These females were mated with F(2L)/F(2L);C(2R) males. Interchange occurrence was recorded as the appearance of an F1 individual with a half-translocation of either X . 2L or Y . 2L type. 37 interchanges were recovered in y/XY and 67 in In(1)/XY females. The majority of the interchanges were of meiotic origin. The interchanges were mainly C(2L)-XY; the most frequent type of half-translocation was Y . 2L;dl-49+BM1. Inversion increased about 5-fold the interchange frequency. In the course of C(2L)-XY interchange, the other X chromosome and C(2R) compound regularly paired and disjoined. In y/XY females, 8 crossover half-translocations of meiotic origin were recovered. The results obtained indicate that meiotic pairing between the X's and C(2L) occurred in the females examined. According to our estimates, XY-C(2L) pairing is associated with interchange in the heterochromatic centromeric regions with a frequency of 10(-3). The recovery of crossover half-translocations supports the chromocentral model of non-homologous pairing and allows us to assume that a chromosome may simultaneously pair with a homologue and a non-homologue. The disjunction pattern of this trivalent depends on its structure in each particular case. The chromosome-segregation pattern resulting from spontaneous interchanges was similar to that resulting from radiation-induced interchanges in the immature oocytes described by Parker. This similarity suggests that non-homologue pairing occurs in the immature oocytes too. The non-homologue-pairing pattern established by the interchange test conformed well with that previously established in y/XY and In(1)XY females by the distribution test.     

Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast

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.     

Revisiting meiotic pairing in wheat synthetics in relation to the evolution of the meiotic system in wheat

A large panel of hexaploid wheat synthetics was developed. Their tetraploid parents consisted of either four extracted wheat tetraploids (ETWs) or four natural present-day tetraploids, and their diploid parents consisted of twenty accessions of Aegilops tauschii. Analysis of meiotic behaviour of the synthetics showed that chromosome pairing is highly variable and depends on the progenitor. The meiotic behaviour in the four ETWs was compared to that of the natural tetraploid wheats. It appears there was no evolution at the hexaploid level of the meiotic genes carried by the A and B genomes. We also reach the conclusion that the neo-allohexaploids at the origin of present-day wheat had a meiotic behaviour close to that of the present-day hexaploid wheat. It is likely that other neo-hexaploids with an impaired meiosis were formed, but they had no future due to their more or less rapid disappearance due to increasing aneuploidy level and structural changes, mainly Robertsonian translocations.