Insights into the meiotic behavior and evolution of multiple sex chromosome systems in spiders

A characteristic feature of spider karyotypes is the predominance of unusual multiple X chromosomes. To elucidate the evolution of spider sex chromosomes, their meiotic behavior was analyzed in 2 major clades of opisthothele spiders, namely, the entelegyne araneomorphs and the mygalomorphs. Our data support the predominance of X(1)X(2)0 systems in entelegynes, while rare X(1)X(2)X(3)X(4)0 systems were revealed in the tuberculote mygalomorphs. The spider species studied exhibited a considerable diversity of achiasmate sex chromosome pairing in male meiosis. The end-to-end pairing of sex chromosomes found in mygalomorphs was gradually replaced by the parallel attachment of sex chromosomes in entelegynes. The observed association of male X univalents with a centrosome at the first meiotic division may ensure the univalents' segregation. Spider meiotic sex chromosomes also showed other unique traits, namely, association with a chromosome pair in males and inactivation in females. Analysis of these traits supports the hypothesis that the multiple X chromosomes of spiders originated by duplications. In contrast to the homogametic sex of other animals, the homologous sex chromosomes of spider females were already paired at premeiotic interphase and were inactivated until prophase I. Furthermore, the sex chromosome pairs exhibited an end-to-end association during these stages. We suggest that the specific behavior of the female sex chromosomes may have evolved to avoid the negative effects of duplicated X chromosomes on female meiosis. The chromosome ends that ensure the association of sex chromosome pairs during meiosis may contain information for discriminating between homologous and homeologous X chromosomes and thus act to promote homologous pairing. The meiotic behavior of 4 X chromosome pairs in mygalomorph females, namely, the formation of 2 associations, each composed of 2 pairs with similar structure, suggests that the mygalomorph X(1)X(2)X(3)X(4)0 system originated by the duplication of the X(1)X(2)0 system via nondisjunctions or polyploidization.     

Sex chromosome-autosome translocations in the leaf-nosed bats, family Phyllostomidae. II. Meiotic analyses of the subfamilies Stenodermatinae and Phyllostominae

Analyses of meiotic pairing and synaptonemal complexes of the composite sex chromosomes of male phyllostomid bats with X-autosome or X- and Y-autosome translocations were performed using Giemsa and silver staining procedures. Typical mammalian sex vesicles were absent in all species analyzed. Stenodermatine species with X-autosome translocations possessed an open ring and tail configuration of the XY1Y2 trivalent. Species with both X- and Y-autosome translocations possessed a closed ring and tail configuration of the neo-XY bivalent. In both cases, the tail represented the autosomal short arm of the X paired with its homologue, either the Y2 in XY1Y2 species or the autosomal arm of the composite Y in neo-XY species. Autosomal pairing of the composite sex bivalent in neo-XY species replaced an association between the original X and Y in late prophase I. The absence of a sex vesicle, the unusual pairing configurations of the composite sex chromosomes, and the presumed absence of meiotic nondisjunction in these species is discussed in light of current hypotheses of sex chromosome behavior in male gametogenesis in mammals.     

Chromosome pairing in meiosis of partially fertile wheat/rye hybrids

The normal course of meiosis depends on regular pairing of homologous chromosomes. In intergeneric hybrids, including those of wheat, there is no chromosome pairing because there are no homologs. In F₁ wheat/rye hybrids, pairing is largely prevented by the pairing homoeologous1 (Ph1) gene. In its presence, there are only rare instances of pairing; most chromosomes are univalent, and their orientation at metaphase I initiates different pathways of the meiotic cycle. The meiotic-like pathway includes a combination of the reductional and the equational + reductional steps at AI followed by the second division. The resulting gametes are mostly non-functional. The mitotic-like pathway involves equational division of univalents at AI and the absence of the second division. Any fertility of wheat/rye hybrids depends on the production of unreduced gametes arising from meiotic restitution (mitotic-like division). We examined the meiotic pairing in wheat/rye hybrids created from wheat lines with single rye chromosome substitutions and Ph1 present. This guaranteed F₁ meiosis with one pair of rye homologs. All hybrids formed bivalents, but proportions of meiocytes with bivalents varied. In the meiocytes where bivalents were present, there was a higher tendency for the meiotic-like pathway, while in meiocytes where bivalent pairing failed, the tendency was stronger for the mitotic-like pathway. Among the equationally dividing cells, we observed more than 90 % of meiocytes without bivalents, where rye homologs did not form bivalents, too. The data indicate a potential application of wheat/rye lines in producing genetic stocks of amphidiploids with designated genomic constitutions.     

The tricky path to recombining X and Y chromosomes in meiosis

Sex chromosomes are the Achilles' heel of male meiosis in mammals. Mis-segregation of the X and Y chromosomes leads to sex chromosome aneuploidies, with clinical outcomes such as infertility and Klinefelter syndrome. Successful meiotic divisions require that all chromosomes find their homologous partner and achieve recombination and pairing. Sex chromosomes in males of many species have only a small region of homology (the pseudoautosomal region, PAR) that enables pairing. Until recently, little was known about the dynamics of recombination and pairing within mammalian X and Y PARs. Here, we review our recent findings on PAR behavior in mouse meiosis. We uncovered unexpected differences between autosomal chromosomes and the X-Y chromosome pair, namely that PAR recombination and pairing occurs later, and is under different genetic control. These findings imply that spermatocytes have evolved distinct strategies that ensure successful X-Y recombination and chromosome segregation.     

Genetic evidence that nonhomologous disjunction and meiotic drive are properties of wild-type Drosophila melanogaster male meiosis

We have followed sex and second chromosome disjunction, and the effects of these chromosomes on sperm function, in four genotypes: wild-type males, males deficient for the Y-linked crystal locus, males with an X chromosome heterochromatic deficiency that deletes all X-Y pairing sites, and males with both deficiencies. Both mutant situations provoke chromosome misbehavior, but the disjunctional defects are quite different. Deficiency of the X heterochromatin, consonant with the lack of pairing sites, mostly disrupts X-Y disjunction with a decidedly second-level effect on major autosome behavior. Deleting crystal, consonant with the cytological picture of postpairing chromatin-condensation problems, disrupts sex and autosome disjunction equally. Even when the mutant-induced nondisjunction has very different mechanics, however, and even more importantly, even in the wild type, there is strong, and similar, meiotic drive. The presence of meiotic drive when disjunction is disrupted by distinctly different mechanisms supports the notion that drive is a normal cellular response to meiotic problems rather than a direct effect of particular mutants. Most surprisingly, in both wild-type and crystal-deficient males the Y chromosome moves to the opposite pole from a pair of nondisjoined second chromosomes nearly 100% of the time. This nonhomologous interaction is, however, absent when the X heterochromatin is deleted. The nonhomologous disjunction of the sex and second chromosomes may be the genetic consequence of the chromosomal compartmentalization seen by deconvolution microscopy, and the absence of Y-2 disjunction when the X heterochromatin is deleted suggests that XY pairing itself, or a previously unrecognized heterochromatic function, is prerequisite to this macrostructural organization of the chromosomes.     

Cytogenetics of chromosome pairing in wheat

Meiotic chromosome pairing in Triticum aestivum is controlled by genetic systems promoting and reducing pairing. The pairing of homoeologous chromosomes is prevented principally by the activity of a single locus (Ph) distally located on the long arm of chromosome 5B. In certain hybrids, supernumerary chromosomes (B chromosomes) from Aegilops species can compensate for the absence of chromosome 5B preventing or reducing homoeologous pairing. Temperature-dependent variants and colchicine sensitivity have been used to show that there are at least two stages in the G1 of meiosis at which the occurrence of meiotic pairing is determined. Wheat may differ from lily in the detailed organization of meiosis.     

C-banding and FISH in chromosomes of the blow flies Chrysomya megacephala and Chrysomya putoria (Diptera, Calliphoridae)

The blow flies Chrysomya putoria and C. megacephala have 2n=12 chromosomes, five metacentric pairs of autosomes and an XX/XY sex chromosome pair. There are no substantial differences in the karyotype morphology of these two species, except for the X chromosome which is subtelocentric in C. megacephala and metacentric in C. putoria and is about 1.4 times longer in C. putoria. All autosomes were characterized by the presence of a C band in the pericentromeric region; C. putoria also has an interstitial band in pair III. The sex chromosomes of both species were heterochromatic, except for a small region at the end of the long arm of the X chromosome. Ribosomal genes were detected in meiotic chromosomes by FISH and in both species the NOR was located on the sex chromosomes. These results confirm that C. putoria was the species introduced into Brazil in 1970s, and not C. chloropyga as formerly described.     

Epigenetic control may explain large within-plant heterogeneity of meiotic behavior in telocentric trisomics of rye

In telocentric trisomics (telotrisomics) of organisms in which the chromosomes normally have two distinct arms, a single chromosome arm with a centromere is present in addition to a complete diploid set of chromosomes. It is the simplest form of polysomy and suitable for analyzing meiotic pairing and recombination patterns in situations where chromosomes compete for pairing. When no suitable meiotic chromosome markers are available, four metaphase I configurations can be distinguished. Their relative frequencies are indicative of the pairing and recombination patterns. In short arm (1RS) telotrisomics of chromosome 1R of rye (Secale cereale) we observed great differences in pairing and recombination patterns among spikes from different tillers and clones of the same plants. Anthers within spikes were only very rarely different. We analyzed a large number of genotypes, including inbreds as well as hybrids. The effects of genetic and environmental conditions on heterogeneity, if any, were limited. Considering that the reproductive tissue of a spike is derived from one primordial cell, it seems that at the start of sexual differentiation there was variation among cells in chromosomal control, which at meiosis determines pairing and crossing-over competence. We suggest that it is an epigenetic system that rigidly maintains this pattern through generative differentiation. In competitive situations the combination most competent for pairing will pair preferentially, forming specific meiotic configurations with different frequencies for different spikes of the same plant. This would explain the heterogeneity between spikes and the homogeneity within spikes. The epigenetic system could involve chromatin conformation or DNA methylation. There were no signs of heterochromatinization.     

Parallel occurrence of asynaptic sex chromosomes in gray voles (Microtus Schrank, 1798)

In many eutherian species, pairing and recombination of X and Y chromosomes are indispensable for normal meiotic progression and correct segregation of sex chromosomes. The rodent subfamily Arvicolinae provides an interesting exception. The majority of arvicoline species with asynaptic sex chromosomes belong to the genus Microtus sensu lato. However, some vole species of the genus Microtus and other genera display normal X-Y pairing in meiosis. These observations indicate that synaptic condition was typical for the common ancestor of all voles, but the gaps in taxonomic sampling makes impossible to identify a lineage or lineages, in which the asynapsis occurred. The methods of electron and fluorescent microscopy were used to study the synapsis of sex chromosomes in males of some additional species of the subfamily Arvicolinae. This extended taxonomic list allowed us to identify asynaptic species in every large lineage of the tribe Microtini. Apparently, the ability of sex chromosomes to pair and recombine in male meiosis was lost in arvicoline evolution for at least three times independently. Our results indirectly suggest the unnecessity of sex chromosome pairing in male meiosis of arvicoline rodents, and presence of alternate molecular mechanism of sex chromosome segregation in this large mammalian tribe.     

不同细胞质的普通小麦"中国春"(Triticum aestivum var.Chinese Spring)与小偃麦杂交F1代的育性与减数分裂行为的研究

15个不同细胞质“中国春”小麦与八倍体小偃麦杂交 ,杂种F1减数分裂的染色体行为表明 :普通小麦与天蓝偃麦草的F或E组染色体之间存在着部分同源关系 ;D2 型细胞质促进部分同源染色体配对、但却抑制同源染色体配对 ;Sv 型细胞质对同源染色体或部分同源染色体的配对均有抑制作用 ;G型细胞质促进同源染色体配对。1 5个不同细胞质“中国春”小麦与六倍体小偃麦杂交 ,F1结实率很低 ,减数分裂中期的染色体行为混乱 ,单价体过多 ,或许意味着在天蓝偃麦草 (Elytrigiain termedium)与长穗偃麦草 (E .elongatum)的E组染色体之间存在着很大差别。随着回交代数的增加 ,选出G型、D2 型、Mt 型、Mu 型等细胞质雄性不育的八倍体小偃麦品系 ,其中D2 型细胞质八倍体小偃麦具有光周期敏感性雄性不育的特征 ;G型细胞质“远中 3”育性正常 ,表明八倍体小偃麦“远中 3”的E组染色体中存在G型胞质的育性恢复基因。     

Improper chromosome synapsis is associated with elongated RAD51 structures in the maize<Emphasis Type="Italic"> desynaptic2</Emphasis> mutant

The RecA homolog, RAD51, performs a central role in catalyzing the DNA strand exchange event of meiotic recombination. During meiosis, RAD51 complexes develop on pairing chromosomes and then most disappear upon synapsis. In the maize meiotic mutant desynaptic2 (dsy2), homologous chromosome pairing and recombination are reduced by ~70% in male meiosis. Fluorescent in situ hybridization studies demonstrate that a normal telomere bouquet develops but the pairing of a representative gene locus is still only 25%. Chromosome synapsis is aberrant as exemplified by unsynapsed regions of the chromosomes. In the mutant, we observed unusual RAD51 structures during chromosome pairing. Instead of spherical single and double RAD51 structures, we saw long thin filaments that extended along or around a single chromosome or stretched between two widely separated chromosomes. Mapping with simple sequence repeat (SSR) markers places the dsy2 gene to near the centromere on chromosome 5, therefore it is not an allele of rad51. Thus, the normal dsy2 gene product is required for both homologous chromosome synapsis and proper RAD51 filament behavior when chromosomes pair. Edited by: P. Moens     

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)     

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.     

Terminal regions of wheat chromosomes select their pairing partners in meiosis

Many plant species, including important crops like wheat, are polyploids that carry more than two sets of genetically related chromosomes capable of meiotic pairing. To safeguard a diploid-like behavior at meiosis, many polyploids evolved genetic loci that suppress incorrect pairing and recombination of homeologues. The Ph1 locus in wheat was proposed to ensure homologous pairing by controlling the specificity of centromere associations that precede chromosome pairing. Using wheat chromosomes that carry rye centromeres, we show that the centromere associations in early meiosis are not based on homology and that the Ph1 locus has no effect on such associations. Although centromeres indeed undergo a switch from nonhomologous to homologous associations in meiosis, this process is driven by the terminally initiated synapsis. The centromere has no effect on metaphase I chiasmate chromosome associations: homologs with identical or different centromeres, in the presence and absence of Ph1, pair the same. A FISH analysis of the behavior of centromeres and distal chromomeres in telocentric and bi-armed chromosomes demonstrates that it is not the centromeric, but rather the subtelomeric, regions that are involved in the correct partner recognition and selection.     

Heterochromatin (C-bands) in somatic and male germ cells in three species ofMicrotinae

The C-banding patterns in the chromosomes ofMicrotus oeconomus, M. arvalis andM. ochrogaster demonstrate differences in the amount and distribution of heterochromatin. Autosomal centromeric heterochromatin appears as conspicuous blocks or as small dots, and in several chromosomes no heterochromatin was detected; interstitial heterochromatin was observed in one autosome pair ofM. ochrogaster. The sex chromosomes also demonstrate differences in the C-banding pattern. InM. oeconomus, the X chromosome exhibits a block of centromeric heterochromatin which is larger than that of the autosomes; this characteristic helps to recognize the X chromosomes in the karyotype. InM. arvalis no heterochromatin was appreciated in the sex chromosomes. The Y chromosomes ofM. ochrogaster andM. oeconomus are entirely heterochromatic. During male meiosis heterochromatin shows condensation, association and chiasma prevention; the sex chromosomes pair end to end in the three species. At pairing, the Y chromosome ofM. arvalis is despiralized, but it appears condensed again shortly before separation of the bivalent.     

A synaptonemal complex-derived mechanism for meiotic segregation precedes the evolutionary loss of homology between sex chromosomes in arvicolid mammals

Synapsis and reciprocal recombination between sex chromosomes are restricted to the pseudoautosomal region. In some animal species, sex chromosomes do not present this region, although they utilize alternative mechanisms that ensure meiotic pairing and segregation. The subfamily Arvicolinae (Rodentia, Cricetidae) includes numerous species with achiasmate sex chromosomes. In order to know whether the mechanism involved in achiasmate segregation is an ancient feature in arvicolid species, we have compared the sex chromosomes of both the Mediterranean vole (Microtus duodecimcostatus) and the water vole (Arvicola terrestris). By means of immunofluorescence, we have found that sex chromosomes in M. duodecimcostatus are asynaptic and develop a synaptonemal complex-derived structure that mediates pairing and facilitates segregation. In A. terrestris, sex chromosomes are synaptic and chiasmate but also exhibit a synaptonemal complex-derived filament during anaphase I. Since phylogenetic relationships indicate that the synaptic condition is ancestral in arvicolids, this finding indicates that the mechanism for achiasmate sex chromosome segregation precedes the switching to the asynaptic condition. We discuss the origin of this synaptonemal complex-derived mechanism that, in turn, could counterbalance the disruption of homology in the sex chromosomes of those species.     

Evolution of karyotype,sex chromosomes,and meiosis in mygalomorph spiders (Araneae: Mygalomorphae)

Spider diversity is partitioned into three primary clades, namely Mesothelae, Mygalomorphae, and Araneomorphae. Mygalomorph cytogenetics is largely unknown. Our study revealed a remarkable karyotype diversity of mygalomorphs. Unlike araneomorphs, they show no general trend towards a decrease of 2n, as the chromosome number was reduced in some lineages and increased in others. A biarmed karyotype is a symplesiomorphy of mygalomorphs and araneomorphs. Male meiosis of some mygalomorphs is achiasmatic, or includes the diffuse stage. The sex chromosome system X₁X₂0, which is supposedly ancestral in spiders, is uncommon in mygalomorphs. Many mygalomorphs exhibit more than two (and up to 13) X chromosomes in males. The evolution of X chromosomes proceeded via the duplication of chromosomes, fissions, X–X, and X‐autosome fusions. Spiders also exhibit a homomorphic sex chromosome pair. In the germline of mygalomorph males these chromosomes are often deactivated; their deactivation and pairing is initiated already at spermatogonia. Remarkably, pairing of sex chromosomes in mygalomorph females is also initiated at gonial cells. Some mygalomorphs have two sex chromosome pairs. The second pair presumably arose in early‐diverging mygalomorphs, probably via genome duplication. The unique behaviour of spider sex chromosomes in the germline may promote meiotic pairing of homologous sex chromosomes and structural differentiation of their duplicates, as well as the establishment of polyploid genomes. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 377–408.     

Isolation and cytogenetic characterization of male meiotic mutants of Drosophila melanogaster

Proper segregation of homologous chromosomes in meiosis I is ensured by pairing of homologs and maintenance of sister chromatid cohesion. In male Drosophila melanogaster, meiosis is achiasmatic and homologs pair at limited chromosome regions called pairing sites. We screened for male meiotic mutants to identify genes required for normal pairing and disjunction of homologs. Nondisjunction of the sex and the fourth chromosomes in male meiosis was scored as a mutant phenotype. We screened 2306 mutagenized and 226 natural population-derived second and third chromosomes and obtained seven mutants representing different loci on the second chromosome and one on the third. Five mutants showed relatively mild effects (<10% nondisjunction). mei(2)yh149 and mei(2)yoh7134 affected both the sex and the fourth chromosomes, mei(2)yh217 produced possible sex chromosome-specific nondisjunction, and mei(2)yh15 and mei(2)yh137 produced fourth chromosome-specific nondisjunction. mei(2)yh137 was allelic to the teflon gene required for autosomal pairing. Three mutants exhibited severe defects, producing >10% nondisjunction of the sex and/or the fourth chromosomes. mei(2)ys91 (a new allele of the orientation disruptor gene) and mei(3)M20 induced precocious separation of sister chromatids as early as prometa-phase I. mei(2)yh92 predominantly induced nondisjunction at meiosis I that appeared to be the consequence of failure of the separation of paired homologous chromosomes.