Survival ofDrosophila melanogaster Progeny after Prolonged Suppression of Pairing and Recombination in Autosome 3

Two laboratory strains of Drosophila melanogaster carrying autosome 3 with a meiotic mutation c(3)G, that is maintained since 1985 in various balancer chromosomes, were used to study progeny survival. The conditions of maintenance of these strains and the effect of c(3)G mutation completely suppress pairing and crossing over in autosome 3. In addition, selection pressure was reduced because of permanent heterozygosity, mediating mutation accumulation in the studied chromosome. In both strains, all homozygotes for autosome 3 (c(3)G/c(3)G) perished. The hybrid homozygotes carrying chromosomes with c(3)G mutation from different strains survived in 0.4 of the progeny. Higher viability was observed after normal pairing and meiotic recombination of the studied chromosome with the chromosome from the wild-type line. The possible nature of mutations accumulated after prolonged suppression of chromosome pairing and recombination is discussed.     

Deleterious mutations in various Drosophila melanogaster strains carrying meiotic mutation c(3)G

In the absence of meiotic recombination, deleterious mutations, decreasing the viability, are accumulated and fixed in small Drosophila populations. Study of the viability of hybrid progenies of three laboratory Drosophila melanogaster strains carrying meiotic mutation c(3)G17 has suggested that the deleterious mutations are negatively synergistic in their interaction. The deleterious mutations localized to the pericentromeric region of chromosome 3 are threefold more efficient as compared with the mutations located in distal regions. Substitution of a new chromosome for the balancer chromosome in a strain with meiotic mutation c(3)G17 partially restores (by approximately 20%) the viability of homozygotes c(3)G17/c(3)G17 over the first 20-30 generations. Further cultivation for 30 generations with the same balancer again decreases the viability to the initial level. An epigenetic nature of deleterious mutations is discussed.     

Sustained and rapid chromosome movements are critical for chromosome pairing and meiotic progression in budding yeast

Telomere-led chromosome movements are a conserved feature of meiosis I (MI) prophase. Several roles have been proposed for such chromosome motion, including promoting homolog pairing and removing inappropriate chromosomal interactions. Here, we provide evidence in budding yeast that rapid chromosome movements affect homolog pairing and recombination. We found that csm4Δ strains, which are defective for telomere-led chromosome movements, show defects in homolog pairing as measured in a "one-dot/two-dot tetR-GFP" assay; however, pairing in csm4Δ eventually reaches near wild-type (WT) levels. Charged-to-alanine scanning mutagenesis of CSM4 yielded one allele, csm4-3, that confers a csm4Δ-like delay in meiotic prophase but promotes high spore viability. The meiotic delay in csm4-3 strains is essential for spore viability because a null mutation (rad17Δ) in the Rad17 checkpoint protein suppresses the delay but confers a severe spore viability defect. csm4-3 mutants show a general defect in chromosome motion but an intermediate defect in chromosome pairing. Chromosome velocity analysis in live cells showed that while average chromosome velocity was strongly reduced in csm4-3, chromosomes in this mutant displayed occasional rapid movements. Lastly, we observed that spo11 mutants displaying lower levels of meiosis-induced double-strand breaks showed higher spore viability in the presence of the csm4-3 mutation compared to csm4Δ. On the basis of these observations, we propose that during meiotic prophase the presence of occasional fast moving chromosomes over an extended period of time is sufficient to promote WT levels of recombination and high spore viability; however, sustained and rapid chromosome movements are required to prevent a checkpoint response and promote efficient meiotic progression.     

Features of the chromocenter structure in Drosophila melanogaster larva cells, mutant for genes C(3)G and NOD

Homolog pairing, chromosome morphology, and chromosome disjunction in the first meiotic division were studied in the oocytes of c(3)G/c(3)G female Drosophila melanogaster at developmental stages 3-4 and 14. It was found that homologs were completely or partly paired in some cells (about 20% in either case). The lengths of chromosomes in +/+, +/c(3)G, and c(3)G/c(3)G cells were at a ratio of 1.0:1.6:2.2. The chromocenters of homozygous cells had an abnormal structure. There was no meiotic block in metaphase 1, and chromosomes only segregated equally in about 80% of anaphases of the first meiotic division. The data obtained correspond to the abnormal variants of the formation of the chromocenter in c(3)G/c(3)G females that could be predicted based on the two-ring structure of the chromocenter. The mechanism of the effect of the homo- and heterozygosity for the hypomorphic mutation c(3)G on the formation of the synaptonemal complex (SC) and crossing over frequency was suggested. In nod/nod homozygous females, asynapsis of pericentromeric regions of homologs was observed in the chromocenter. It was assumed that NOD kinezin is necessary at the last stages of pairing of the pericentromeric regions of homologs and formation of the coordinating bonds between them.     

The influence of the Robertsonian translocation Rb(X.2)2Ad on anaphase I non-disjunction in male laboratory mice

A Robertsonian translocation in the mouse between the X chromosome and chromosome 2 is described. The male and female carriers of the Rb(X.2)2Ad were fertile. A homozygous/hemizygous line was maintained. The influence of the X-autosomal Robertsonian translocation on anaphase I non-disjunction in male mice was studied by chromosome counts in cells at metaphase II of meiosis and by assessment of aneuploid progeny. The results conclusively show that the inclusion of Rb2Ad in the male genome induces non-disjunction at the first meoitic division. In second metaphase cells the frequency of sex-chromosomal aneuploidy was 10.8%, and secondary spermatocytes containing two or no sex chromosome were equally frequent. The Rb2Ad males sired 3.9% sex-chromosome aneuploid progeny. The difference in aneuploidy frequencies in the germ cells and among the progeny suggests that the viability of XO and XXY individuals is reduced. The pairing configurations of chromosomes 2, Rb2Ad and Y were studied during meiotic prophase by light and electron microscopy. Trivalent pairing was seen in all well spread nuclei. Complete pairing of the acrocentric autosome 2 with the corresponding segment of the Rb2Ad chromosome was only seen in 3.2% of the cells analysed in the electron microscope. The pairing between the X and Y chromosome in the Rb2Ad males corresponded to that in males with normal karyotype. Reasons for sex-chromosomal non-disjunction despite the normal pairing pattern between the sex chromosomes may be seen in the terminal chiasma location coupled with the asynchronous separation of the sex chromosomes and the autosomes.(ABSTRACT TRUNCATED AT 250 WORDS)     

Allelic and Ectopic Interactions in Recombination-Defective Yeast Strains

Ectopic recombination in the yeast Saccharomyces cerevisiae has been investigated by examining the effects of mutations known to alter allelic recombination frequencies. A haploid yeast strain disomic for chromosome III was constructed in which allelic recombination can be monitored using leu2 heteroalleles on chromosome III and ectopic recombination can be monitored using ura3 heteroalleles on chromosomes V and II. This strain contains the spo13-1 mutation which permits haploid strains to successfully complete meiosis and which rescues many recombination-defective mutants from the associated meiotic lethality. Mutations in the genes RAD50, SPO11 and HOP1 were introduced individually into this disomic strain using transformation procedures. Mitotic and meiotic comparisons of each mutant strain with the wild-type parental strain has shown that the mutation in question has comparable effects on ectopic and allelic recombination. Similar results have been obtained using diploid strains constructed by mating MATa and MAT alpha haploid derivatives of each of the disomic strains. These data demonstrate that ectopic and allelic recombination are affected by the same gene products and suggest that the two types of recombination are mechanistically similar. In addition, the comparison of disomic and diploid strains indicates that the presence of a chromosome pairing partner during meiosis does not affect the frequency of ectopic recombination events involving nonhomologous chromosomes.     

Fragile,unfaithful and persistent Ys—on how meiosis can shape sex chromosome evolution

Sex-linked inheritance is a stark exception to Mendel’s Laws of Heredity. Here we discuss how the evolution of heteromorphic sex chromosomes (mainly the Y) has been shaped by the intricacies of the meiotic programme. We propose that persistence of Y chromosomes in distantly related mammalian phylogroups can be explained in the context of pseudoautosomal region (PAR) size, meiotic pairing strategies, and the presence of Y-borne executioner genes that regulate meiotic sex chromosome inactivation. We hypothesise that variation in PAR size can be an important driver for the evolution of recombination frequencies genome wide, imposing constraints on Y fate. If small PAR size compromises XY segregation during male meiosis, the stress of producing aneuploid gametes could drive function away from the Y (i.e., a fragile Y). The Y chromosome can avoid fragility either by acquiring an achiasmatic meiotic XY pairing strategy to reduce aneuploid gamete production, or gain meiotic executioner protection (a persistent Y). Persistent Ys will then be under strong pressure to maintain high recombination rates in the PAR (and subsequently genome wide), as improper segregation has fatal consequences for germ cells. In the event that executioner protection is lost, the Y chromosome can be maintained in the population by either PAR rejuvenation (extension by addition of autosome material) or gaining achiasmatic meiotic pairing, the alternative is Y loss. Under this dynamic cyclic evolutionary scenario, understanding the meiotic programme in vertebrate and invertebrate species will be crucial to further understand the plasticity of the rise and fall of heteromorphic sex chromosomes.Subject terms: Sexual selection, Genome, Cytogenetics, Evolutionary biology     

Meiotic recombination in Drosophila females depends on chromosome continuity between genetically defined boundaries

In the pairing-site model, specialized regions on each chromosome function to establish meiotic homolog pairing. Analysis of these sites could provide insights into the mechanism used by Drosophila females to form a synaptonemal complex (SC) in the absence of meiotic recombination. These specialized sites were first established on the X chromosome by noting that there were barriers to crossover suppression caused by translocation heterozygotes. These sites were genetically mapped and proposed to be pairing sites. By comparing the cytological breakpoints of third chromosome translocations to their patterns of crossover suppression, we have mapped two sites on chromosome 3R. We have performed experiments to determine if these sites have a role in meiotic homolog pairing and the initiation of recombination. Translocation heterozygotes exhibit reduced gene conversion within the crossover-suppressed region, consistent with an effect on the initiation of meiotic recombination. To determine if homolog pairing is disrupted in translocation heterozygotes, we used fluorescent in situ hybridization to measure the extent of homolog pairing. In wild-type oocytes, homologs are paired along their entire lengths prior to accumulation of the SC protein C(3)G. Surprisingly, translocation heterozygotes exhibited homolog pairing similar to wild type within the crossover-suppressed regions. This result contrasted with our observations of c(3)G mutant females, which were found to be defective in pairing. We propose that each Drosophila chromosome is divided into several domains by specialized sites. These sites are not required for homolog pairing. Instead, the initiation of meiotic recombination requires continuity of the meiotic chromosome structure within each of these domains.     

Molecular analysis of recombination in a family with Duchenne muscular dystrophy and a large pericentric X chromosome inversion.

It has been demonstrated in animal studies that, in animals heterozygous for pericentric chromosomal inversions, loop formation is greatly reduced during meiosis. This results in absence of recombination within the inverted segment, with recombination seen only outside the inversion. A recent study in yeast has shown that telomeres, rather than centromeres, lead in chromosome movement just prior to meiosis and may be involved in promoting recombination. We studied by cytogenetic analysis and DNA polymorphisms the nature of meiotic recombination in a three-generation family with a large pericentric X chromosome inversion, inv(X)(p21.1q26), in which Duchenne muscular dystrophy (DMD) was cosegregating with the inversion. On DNA analysis there was no evidence of meiotic recombination between the inverted and normal X chromosomes in the inverted segment. Recombination was seen at the telomeric regions, Xp22 and Xq27-28. No deletion or point mutation was found on analysis of the DMD gene. On the basis of the FISH results, we believe that the X inversion is the mutation responsible for DMD in this family. Our results indicate that (1) pericentric X chromosome inversions result in reduction of recombination between the normal and inverted X chromosomes; (2) meiotic X chromosome pairing in these individuals is likely initiated at the telomeres; and (3) in this family DMD is caused by the pericentric inversion.     

Differing requirements for RAD51 and DMC1 in meiotic pairing of centromeres and chromosome arms in Arabidopsis thaliana

During meiosis homologous chromosomes pair, recombine, and synapse, thus ensuring accurate chromosome segregation and the halving of ploidy necessary for gametogenesis. The processes permitting a chromosome to pair only with its homologue are not fully understood, but successful pairing of homologous chromosomes is tightly linked to recombination. In Arabidopsis thaliana, meiotic prophase of rad51, xrcc3, and rad51C mutants appears normal up to the zygotene/pachytene stage, after which the genome fragments, leading to sterility. To better understand the relationship between recombination and chromosome pairing, we have analysed meiotic chromosome pairing in these and in dmc1 mutant lines. Our data show a differing requirement for these proteins in pairing of centromeric regions and chromosome arms. No homologous pairing of mid-arm or distal regions was observed in rad51, xrcc3, and rad51C mutants. However, homologous centromeres do pair in these mutants and we show that this does depend upon recombination, principally on DMC1. This centromere pairing extends well beyond the heterochromatic centromere region and, surprisingly, does not require XRCC3 and RAD51C. In addition to clarifying and bringing the roles of centromeres in meiotic synapsis to the fore, this analysis thus separates the roles in meiotic synapsis of DMC1 and RAD51 and the meiotic RAD51 paralogs, XRCC3 and RAD51C, with respect to different chromosome domains.     

Meiotic mutations from natural populations ofDrosophila melanogaster

Two meiotic genes from natural populations are described. A female meiotic mutation,mei(1)g13, mapped to 17.4 on the X chromosome, causes nondisjunction of all homologs except for the fourth chromosomes. In addition, it reduces recombination by 10% in the homozygotes and causes 18% increased recombination in the heterozygotes. A male meiotic mutation,mei-1223 ^m144 , is located on the third chromosome. Although this mutation causes nondisjunction of all chromosomes, each chromosome pair exhibits a different nondisjunction frequency. Large variations in the sizes of the premature sperm heads observed in the homozygotes may reflect irregular meiotic pairing and the subsequent abnormal segregation, resulting in aneuploid chromosome complements.     

Protein Phosphatase 4 Promotes Chromosome Pairing and Synapsis,and Contributes to Maintaining Crossover Competence with Increasing Age

Prior to the meiotic divisions, dynamic chromosome reorganizations including pairing, synapsis, and recombination of maternal and paternal chromosome pairs must occur in a highly regulated fashion during meiotic prophase. How chromosomes identify each other''s homology and exclusively pair and synapse with their homologous partners, while rejecting illegitimate synapsis with non-homologous chromosomes, remains obscure. In addition, how the levels of recombination initiation and crossover formation are regulated so that sufficient, but not deleterious, levels of DNA breaks are made and processed into crossovers is not understood well. We show that in Caenorhabditis elegans, the highly conserved Serine/Threonine protein phosphatase PP4 homolog, PPH-4.1, is required independently to carry out four separate functions involving meiotic chromosome dynamics: (1) synapsis-independent chromosome pairing, (2) restriction of synapsis to homologous chromosomes, (3) programmed DNA double-strand break initiation, and (4) crossover formation. Using quantitative imaging of mutant strains, including super-resolution (3D-SIM) microscopy of chromosomes and the synaptonemal complex, we show that independently-arising defects in each of these processes in the absence of PPH-4.1 activity ultimately lead to meiotic nondisjunction and embryonic lethality. Interestingly, we find that defects in double-strand break initiation and crossover formation, but not pairing or synapsis, become even more severe in the germlines of older mutant animals, indicating an increased dependence on PPH-4.1 with increasing maternal age. Our results demonstrate that PPH-4.1 plays multiple, independent roles in meiotic prophase chromosome dynamics and maintaining meiotic competence in aging germlines. PP4''s high degree of conservation suggests it may be a universal regulator of meiotic prophase chromosome dynamics.     

mei-2, a mutagen-sensitive mutant of Neurospora defective in chromosome pairing and meiotic recombination

Summary A Neurospora crassa mutation, mei-2, affecting meiosis and mutagen sensitivity, was characterized for its effect on meiotic recombination and chromosome pairing. Results from homozygous mei-2 crosses involving distant markers on the same chromosome demonstrated a drastic reduction in meiotic recombination. However, mitotic recombination continued to occur. Cytological observations indicated that pairing of homologous chromosomes in zygotene was greatly reduced or absent, resulting in aberrant segregation at anaphase I and often at subsequent divisions as well. The few mature ascospores produced were frequently disomic for one or more chromosomes.     

Genetic Analysis of Sex Chromosomal Meiotic Mutants in DROSOPHILA MELANOGASTER

A total of 209 ethyl methanesulfonate-treated X chromosomes were screened for meiotic mutants that either (1) increased sex or fourth chromosome nondisjunction at either meiotic division in males; (2) allowed recombination in such males; (3) increased nondisjunction of the X chromosome at either meiotic division in females; or (4) caused such females, when mated to males heterozygous for Segregation-Distorter (SD) and a sensitive homolog to alter the strength of meiotic drive in males.-Twenty male-specific meiotic mutants were found. Though the rates of nondisjunction differed, all twenty mutants were qualitatively similar in that (1) they alter the disjunction of the X chromosome from the Y chromosome; (2) among the recovered sex-chromosome exceptional progeny, there is a large excess of those derived from nullo-XY as compared to XY gametes; (3) there is a negative correlation between the frequency of sex-chromosome exceptional progeny and the frequency of males among the regular progeny. In their effects on meiosis these mutants are similar to In(1)sc(4L)sc(8R), which is deleted for the basal heterochromatin. These mutants, however, have normal phenotypes and viabilities when examined as X/0 males, and furthermore, a mapping of two of the mutants places them in the euchromatin of the X chromosome. It is suggested that these mutants are in genes whose products are involved in insuring the proper functioning of the basal pairing sites which are deleted in In(1)sc(4L)sc(8R), and in addition that there is a close connection, perhaps causal, between the disruption of normal X-Y pairing (and, therefore, disjunction) and the occurrence of meiotic drive in the male.-Eleven mutants were found which increased nondisjunction in females. These mutants were characterized as to (1) the division at which they acted; (2) their effect on recombination; (3) their dominance; (4) their effects on disjunction of all four chromosome pairs. Five female mutants caused a nonuniform decrease in recombination, being most pronounced in distal regions, and an increase in first division nondisjunction of all chromosome pairs. Their behavior is consistent with the hypothesis that these mutants are defective in a process which is a precondition for exchange. Two female mutants were allelic and caused a uniform reduction in recombination for all intervals (though to different extents for the two alleles) and an increase in first-division nondisjunction of all chromosomes. Limited recombination data suggest that these mutants do not alter coincidence, and thus, following the arguments of Sandler et al. (1968), are defective in exchange rather than a precondiiton for exchange. A single female mutant behaves in a manner that is consistent with it being a defect in a gene whose functioning is essential for distributive pairing. Three of the female meiotic mutants cause abnormal chromosome behavior at a number of times in meiosis. Thus, nondisjunction at both meiotic divisions is increased, recombinant chromosomes nondisjoin, and there is a polarized alteration in recombination.-The striking differences between the types of control of meiosis in the two sexes is discussed and attention is drawn to the possible similarities between (1) the disjunction functions of exchange and the process specified by the chromosome-specific male mutants; and (2) the prevention of functional aneuploid gamete formation by distributive disjunction and meiotic drive.     

Cytological and molecular characterization of a Triticum aestivum x Lophopyrum ponticum backcross derivative resistant to barley yellow dwarf.

Barley yellow dwarf is the most damaging virus-caused disease in bread wheat (Triticum aestivum L.). A resistant line, SW335.1.2-13-11-1-5 (2n = 47), derived from a cross of T. aestivum x Lophopyrum ponticum was characterized by meiotic chromosome pairing, by in situ DNA hybridization and by expression of molecular markers to determine its chromosome constitution. All progeny of this line had three pairs of L. ponticum chromosomes from homoeologous chromosome groups 3, 5, and 6 and the 2n = 47 progeny had an additional L. ponticum monosome. The pairs from groups 3 and 6 were in the added state, while the group 5 pair was substituted for wheat chromosome 5D. Several wheat-wheat translocations with respect to the parental wheat genotype occurred in this line, presumably owing to the promotion of homoeologous chromosome pairing by L. ponticum chromosomes. It was hypothesized that homoeologous recombination results in homoeologous duplication-deletions in wheat chromosomes. An aberrant 3:1 disjunction creates the potential at each meiosis for replacement of these wheat chromosomes by homoeologous L. ponticum chromosomes. Wheat chromosomes 3A and 6A appeared to be in intermediate stages of this substitution process.     

Absence of qualitative genes controlling interspecific pairing in rye B chromosomes

Summary The meiotic behaviour of hybrids between Secale cereale carrying B chromosomes and S. vavilovii has been studied in order to estimate the effects of B chromosomes on hybrid meiotic pairing. The possible effect of Bs on the meiotic pairing of the offspring from backcrosses with S. vavilovii has been studied also. The results obtained clearly indicate that no detectable differences existed in chromosome pairing of hybrids with or without B chromosomes. The hypothetical existence of epistatic genes on cereale genome masking the effect of Bs has been rejected after the results obtained in backcrosses. Therefore, lack of qualitative genes controlling interspecific pairing on rye B chromosomes has been concluded. A quantitative effect of B chromosomes was detected only when they were in alien cytoplasm.     

Homoeologous pairing and recombination in <Emphasis Type="Italic">Solanum lycopersicoides</Emphasis> monosomic addition and substitution lines of tomato

We compared meiotic pairing and recombination between tomato ( Lycopersicon esculentum) and homoeologous Solanum lycopersicoides chromosomes in monosomic additions (MAs) and substitution lines (SLs), each representing a single chromosome of the nightshade in a tomato background. Three configurations of each alien chromosome and its two tomato homoeologues were detected by genomic in situ hybridization in MA-7, -8, and -10 at diakinesis/metaphase-I: 1 trivalent (III), 1 bivalent + 1 univalent (II+I), and 3 univalents (3I). The II+I category was by far the most common, and the univalent was from S. lycopersicoides 91-99.5% of the time, indicating a high degree of preferential (homologous) pairing. In the corresponding substitution lines, association of homoeologous chromosomes was much higher (up to 90% of the cells), presumably due to the absence of homologous partners. However, SL-10 showed a surprisingly high frequency of univalents (about 73%). Genome-wide analysis of chromosome pairing revealed a decrease in the average chiasma frequency for both monosomic additions and substitution lines. Recombination between tomato and the nightshade was restricted in all cases, the reduction being more severe in each monosomic addition than in the corresponding substitution line. Recombination rates in the substitutions were less than those observed for the same chromosomes in the first backcross generation. Chromosomes 8 and 10 showed the highest and the lowest rates of homoeologous recombination, respectively. No recombination was detected between markers on the long arm of chromosome 10, presumably due to the presence of a paracentric inversion differentiating the two genomes in this region. The frequency of homoeologous pairing at diakinesis/metaphase-I was significantly higher than the rate of homoeologous recombination detected in the progeny, suggesting a strong selection against recombinant products in meiotic or post-meiotic stages.     

Inheritance of Chromosome-Length Polymorphisms in Coprinus Cinereus

We have investigated the inheritance of chromosome-length polymorphisms in the basidiomycete Coprinus cinereus. The electrophoretic karyotypes of interfertile strains of C. cinereus are strikingly different, and crosses between strains with different karyotypes yield progeny with chromosomes of new sizes. Repeated backcrossing of a mutant to one parent often stabilizes the mutant chromosome at a unique size; this then becomes a chromosome-length polymorphism marker for that mutant gene. A comparison of mutant strains, their wild-type progenitor, and backcrossed strains revealed that these marker chromosomes are not caused by the initial mutagenic treatment and are found only in progeny of crosses between strains with polymorphic chromosomes. Thus, they are most likely formed by meiotic recombination. For the rad12 gene, the marker chromosome can further recombine to become the size of the homolog of the backcross parent. For the rad3 gene, both ectopic and homologous recombination events are likely involved in the generation of the marker chromosomes. As predicted by a recombination model, a cross to a new wild-type parent can change the size of a mutant marker chromosome. Therefore, changes in chromosome length are a common and prominent feature of the genome of this sexual fungus, and a variety of karyotypes is tolerated by the organism.     

THE EVOLUTION OF HETEROMORPHIC SEX CHROMOSOMES

The facts and ideas which have been discussed lead to the following synthesis and model. 1. Heteromorphic sex chromosomes evolved from a pair of homomorphic chromosomes which had an allelic difference at the sex-determining locus. 2. The first step in the evolution of sex-chromosome heteromorphism involved either a conformational or a structural difference between the homologues. A structural difference could have arisen through a rearrangement such as an inversion or a translocation. A conformational difference could have occurred if the sex-determining locus was located in a chromosomal domain which behaved as a single control unit and involved a substantial segment of the chromosome. It is assumed that any conformational difference present in somatic cells would have been maintained in meiotic prophase. 3. Lack of conformational or structural homology between the sex chromosomes led to meiotic pairing failure. Since pairing failure reduced fertility, mechanisms preventing it had a selective advantage. Meiotic inactivation (heterochromatinization) of the differential region of the X chromosome in species with heterogametic males and euchromatinization of the W in species with heterogametic females are such mechanisms, and through them the pairing problems are avoided. 4. Structural and conformational differences between the sex chromosomes in the heterogametic sex reduced recombination. In heterogametic males recombination was reduced still further by the heterochromatinization of the X chromosome, which evolved in response to selection against meiotic pairing failure. 5. Suppression of recombination resulted in an increase in the mutation rate and an increased rate of fixation of deleterious mutations in the recombination-free chromosome regions. Functional degeneration of the genetically isolated regions of the Y and W was the result. In XY males this often led to further meiotic inactivation of the differential region of the X chromosome, and in this way an evolutionary positive-feedback loop may have been established. 6. Structural degeneration (loss of material) followed functional degeneration of Y or W chromosomes either because the functionally degenerate genes had deleterious effects which made their loss a selective advantage, or because shorter chromosomes were selectively neutral and became fixed by chance. 7. The evolutionary routes to sex-chromosome heteromorphism in groups with female heterogamety are more limited than in those with male heterogamety. Oocytes are usually large and long-lived, and are likely to need the products of X- or Z-linked genes. Meiotic inactivation of these chromosomes is therefore unlikely. In the oocytes of ZW females, meiotic pairing failure is avoided through euchromatinization of the W rather than heterochromatinization of the Z chromosome.(ABSTRACT TRUNCATED AT 400 WORDS)     

The dynamics of homologous chromosome pairing during male Drosophila meiosis

BACKGROUND: Meiotic pairing is essential for the proper orientation of chromosomes at the metaphase plate and their subsequent disjunction during anaphase I. In male Drosophila melanogaster, meiosis occurs in the absence of recombination or a recognizable synaptonemal complex (SC). Due to limitations in available cytological techniques, the early stages of homologous chromosome pairing in male Drosophila have not been observed, and the mechanisms involved are poorly understood.RESULTS: Chromosome tagging with GFP-Lac repressor protein allowed us to track, for the first time, the behavior of meiotic chromosomes at high resolution, live, at all stages of male Drosophila meiosis. Homologous chromosomes pair throughout the euchromatic regions in spermatogonia and during the early phases of spermatocyte development. Extensive separation of homologs and sister chromatids along the chromosome arms occurs in mid-G2, several hours before the first meiotic division, and before the G2/M transition. Centromeres, on the other hand, show complex association patterns, with specific homolog pairing taking place in mid-G2. These changes in chromosome pairing parallel changes in large-scale chromosome organization.CONCLUSIONS: Our results suggest that widespread interactions along the euchromatin are required for the initiation, but not the maintenance, of meiotic pairing of autosomes in male Drosophila. We propose that heterochromatic associations, or chromatid entanglement, may be responsible for the maintenance of homolog association during late G2. Our data also suggest that the formation of chromosome territories in the spermatocyte nucleus may play an active role in ensuring the specificity of meiotic pairing in late prophase by disrupting interactions between nonhomologous chromosomes.