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.     

Prevalence of B chromosomes in Orthoptera is associated with shape and number of A chromosomes

We analyze the prevalence of B chromosomes in 1,601 species of orthopteran insects where chromosome number and shape are known. B chromosomes have been reported in 191 of these species. Bs are not uniformly distributed among orthopteran superfamilies, with evident hotspots in the Pyrgomorphoidea (32.3% of species carrying Bs), Grylloidea (14.9%), Acridoidea (14.6%) and Tetrigoidea (14.3%). As expected under the theory of centromeric drive, we found a correlation between B chromosome presence and A chromosome shape-Bs are more frequent in karyotypes with more acrocentric A chromosomes. We also found that Bs are less common in species with high chromosome numbers and appear to be most common at the modal chromosome number (2n = 24). Study effort, measured for each genus, was not associated with B prevalence, A chromosome shape or A chromosome number. Our results thus provide support for centromeric drive as an important and prevalent force in the karyotypic evolution of Orthoptera, just as it appears to be in mammals. We suggest that centromeric drive may provide a mechanistic explanation for White's principle of karyotypic orthoselection.     

Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers

Centromeres are essential mediators of chromosomal segregation, but both centromeric DNA sequences and associated kinetochore proteins are paradoxically diverse across species. The selfish centromere model explains rapid evolution by both components via an arms-race scenario: centromeric DNA variants drive by distorting chromosomal transmission in female meiosis and attendant fitness costs select on interacting proteins to restore Mendelian inheritance. Although it is clear than centromeres can drive and that drive often carries costs, female meiotic drive has not been directly linked to selection on kinetochore proteins in any natural system. Here, we test the selfish model of centromere evolution in a yellow monkeyflower (Mimulus guttatus) population polymorphic for a costly driving centromere (D). We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years. We use quantitative genetic mapping to demonstrate that context-dependence in the strength of drive (from near-100% D transmission in interspecific hybrids to near-Mendelian in within-population crosses) primarily reflects variable vulnerability of the non-driving competitor chromosomes, but also map an unlinked modifier of drive coincident with kinetochore protein Centromere-specific Histone 3 A (CenH3A). Finally, CenH3A exhibits a recent (<1000 years) selective sweep in our focal population, implicating local interactions with D in ongoing adaptive evolution of this kinetochore protein. Together, our results demonstrate an active co-evolutionary arms race between DNA and protein components of the meiotic machinery in Mimulus, with important consequences for individual fitness and molecular divergence.     

Restriction enzyme and fluorochrome banding analysis of the constitutive heterochromatin of Saguinus species (Callitrichidae, Primates)

Metaphases of Saguinas fuscicollis fuscicollis and Saguinas mystax were subjected to restriction enzyme banding (Alu I, Hae III, Hin fI, Rsa I, Dde I, Mbo I and Msp I) and sequenced C-banding, together with fluorochrome staining (CMA3 and DAPI). Both species showed large C-bands in the pericentromeric regions. S. f. fuscicollis also manifested distal C-bands in both arms of pair 5 and in the short arms of pairs 8-15. In each species the heterochromatin revealed different reactions to the restriction enzymes and fluorochromes. This was related to its location in the genome (centromeric, pericentromeric, distal), making possible the identification of distinct categories of constitutive heterochromatin. In S. f. fuscicollis there were at least five types, namely centromeric in bi-armed chromosomes, centromeric in acrocentrics, pericentromeric, distal, and cryptic bands, detected only with the Alu I. There were three types in S. mystax, viz centromeric in bi-armed chromosomes, centromeric in acrocentric, and pericentromeric chromosomes. Several aspects of their constitution and origin are discussed.     

Conflict begets complexity: the evolution of centromeres

Centromeres mediate the faithful segregation of eukaryotic chromosomes. Yet they display a remarkable range in size and complexity across eukaryotes, from approximately 125 bp in budding yeast to megabases of repetitive satellites in human chromosomes. Mapping the fine-scale structure of complex centromeres has proven to be daunting, but recent studies have provided a first glimpse into this unexplored bastion of our genomes and the evolutionary pressures that shape it. Evolutionary studies of proteins that bind centromeric DNA suggest genetic conflict as the underlying basis of centromere complexity, drawing interesting parallels with the myriad selfish elements that employ centromeric activity for their own survival.     

Absence of Positive Selection on Centromeric Histones in Tetrahymena Suggests Unsuppressed Centromere-Drive in Lineages Lacking Male Meiosis

Centromere-drive is a process where centromeres compete for transmission through asymmetric "female" meiosis for inclusion into the oocyte. In symmetric "male" meiosis, all meiotic products form viable germ cells. Therefore, the primary incentive for centromere-drive, a potential transmission bias, is believed to be missing from male meiosis. In this article, we consider whether male meiosis also bears the primary cost of centromere-drive. Because different taxa carry out different combinations of meiotic programs (symmetric?+?asymmetric, symmetric only, asymmetric only), it is possible to consider the evolutionary consequences of centromere-drive in the context of these differing systems. Groups with both types of meiosis have large, rapidly evolving centromeric regions, and their centromeric histones (CenH3s) have been shown to evolve under positive selection, suggesting roles as suppressors of centromere-drive. In contrast, taxa with only symmetric male meiosis have shown no evidence of positive selection in their centromeric histones. In this article, we present the first evolutionary analysis of centromeric histones in ciliated protozoans, a group that only undergoes asymmetric "female" meiosis. We find no evidence of positive selection acting on CNA1, the CenH3 of Tetrahymena species. Cytological observations of a panel of Tetrahymena species are consistent with dynamic karyotype evolution in this lineage. Our findings suggest that defects in male meiosis, and not mitosis or female meiosis, are the primary selective force behind centromere-drive suppression. Our study raises the possibility that taxa like ciliates, with only female meiosis, may therefore undergo unsuppressed centromere drive.     

THE CONTRIBUTION OF FEMALE MEIOTIC DRIVE TO THE EVOLUTION OF NEO‐SEX CHROMOSOMES

Sex chromosomes undergo rapid turnover in certain taxonomic groups. One of the mechanisms of sex chromosome turnover involves fusions between sex chromosomes and autosomes. Sexual antagonism, heterozygote advantage, and genetic drift have been proposed as the drivers for the fixation of this evolutionary event. However, all empirical patterns of the prevalence of multiple sex chromosome systems across different taxa cannot be simply explained by these three mechanisms. In this study, we propose that female meiotic drive may contribute to the evolution of neo‐sex chromosomes. The results of this study showed that in mammals, the XY₁Y₂ sex chromosome system is more prevalent in species with karyotypes of more biarmed chromosomes, whereas the X₁X₂Y sex chromosome system is more prevalent in species with predominantly acrocentric chromosomes. In species where biarmed chromosomes are favored by female meiotic drive, X‐autosome fusions (XY₁Y₂ sex chromosome system) will be also favored by female meiotic drive. In contrast, in species with more acrocentric chromosomes, Y‐autosome fusions (X₁X₂Y sex chromosome system) will be favored just because of the biased mutation rate toward chromosomal fusions. Further consideration should be given to female meiotic drive as a mechanism in the fixation of neo‐sex chromosomes.     

The distribution of B chromosomes across species

In this review we look at the broad picture of how B chromosomes are distributed across a wide range of species. We review recent studies of the factors associated with the presence of Bs across species, and provide new analyses with updated data and additional variables. The major obstacle facing comparative studies of B chromosome distribution is variation among species in the intensity of cytogenetic study. Because Bs are, by definition, not present in all individuals of a species, they may often be overlooked in species that are rarely studied. We give examples of corrections for differences in study effort, and show that after a variety of such corrections, strong correlations remain. Several major biological factors are associated with the presence of B chromosomes. Among flowering plants, Bs are more likely to occur in outcrossing than in inbred species, and their presence is also positively correlated with genome size and negatively with chromosome number. They are no more frequent in polyploids than in diploids, nor in species with multiple ploidies. Among mammals, Bs are more likely to occur in species with karyotypes consisting of mostly acrocentric chromosomes. We find no evidence for an association with chromosome number or genome size in mammals, although the sample for genome size is small. The associations with breeding system and acrocentric chromosomes were both predicted in advance, but those with genome size and chromosome number were discovered empirically and we can offer only tentative explanations for the very strong associations we have uncovered. Our understanding of why B chromosomes are present in some species and absent in others is still in its infancy, and we suggest several potential avenues for future research.     

Chromosomal banding pattern and idiogram of the cotton rat,Sigmodon arizonae (Rodentia,Muridae)

A procedure for obtaining G-bands on chromosomes of mammals is outlined. The procedure was utilized in an investigation of the idiogram and banding pattern of the mitotic chromosomes of the cotton rat, Sigmodon arizonae. The diploid number of this species is 22, and each pair of homologues is easily separated on the basis of size, centromeric position, and banding pattern. The autosomes are represented by four pairs of large submetacentric chromosomes, three pairs of medium to small submetacentric chromosomes, two pairs of large subtelocentric chromosomes and one pair of small acrocentric chromosomes. The X chromosome is acrocentric and averages from 5.42% to 5.46% of the haploid female complement. The Y chromosome is a minute acrocentric and easily separated from the smallest acrocentric autosome. The usefulnes of Sigmodon arizonae as a laboratory animal for cytogenetic studies is substantiated.     

Unravelling the mystery of female meiotic drive: where we are

Female meiotic drive is the phenomenon where a selfish genetic element alters chromosome segregation during female meiosis to segregate to the egg and transmit to the next generation more frequently than Mendelian expectation. While several examples of female meiotic drive have been known for many decades, a molecular understanding of the underlying mechanisms has been elusive. Recent advances in this area in several model species prompts a comparative re-examination of these drive systems. In this review, we compare female meiotic drive of several animal and plant species, highlighting pertinent similarities.     

Cytogenetic aspects of phylogeny in the Bovidae. II. C-banding

Constitutive heterochromatin in the Bovidae, as revealed by C-banding, was mostly located in the centromeric regions. Considerable variation was, however, evident in the size of the C-bands both within and between subfamilies. Some evidence was found for a reduction in the amount of centromeric heterochromatin in bi-armed relative to acrocentric autosomes, and these findings are discussed in relation to karyotype evolution in the group.     

B chromosomes and Robertsonian fusions of Dichroplus pratensis (Acrididae): intraspecific support for the centromeric drive theory

We tested the centromeric drive theory of karyotypic evolution in the grasshopper Dichroplus pratensis, which is simultaneously polymorphic for eight Robertsonian fusions and two classes of B chromosomes. A logistic regression analysis performed on 53 natural populations from Argentina revealed that B chromosomes are more probably found in populations with a higher proportion of acrocentric chromosomes, as the theory predicts. Furthermore, frequencies of B-carrying individuals are significantly negatively correlated with the mean frequency of different Robertsonian fusions per individual. No significant correlations between presence/absence or frequency of Bs, and latitude or altitude of the sampled populations, were found. We thus provide the first intraspecific evidence supporting the centromeric drive theory in relation to the establishment of B chromosomes in natural populations.     

Chromosome banding studies in an Indian mullet: evidence of structural rearrangements from NOR locations

C-, G- and NOR bands have been studied in the female sex of Rhinomugil corsula. (Mugilidae, Pisces) by deploying the conventional methodologies with suitable modifications of minor nature. The diploid metaphase complements contained 48 acrocentric chromosomes. The localization of C-band heterochromatin was found to be mostly at or near the centromeric regions of the acrocentric chromosomes. The G-type bands were not so well defined, but some of the G-banded chromosomes also contained C-bands. Interestingly, silver-positive NORs were found at the telomeric ends of five acrocentric chromosomes, including one homologous pair having NORs in both chromatids, while one chromosome showed NORs in both of its chromatids and the other two had only one NOR localized at one of its chromatids. This would suggest that one homologue of the second pair of NOR-bearing chromosomes possibly underwent a chromatid exchange with a non-NOR bearing chromosome. This is quite a unique situation not reported earlier in any species of fish., though some other form of NOR-polymorphism/heteromorphism has rarely been reported. Therefore, further exploration in natural populations of this species to examine the other sex and to verify if there also exists other chromosomally polymorphic races (in respect of NOR-polymorphism) of this species, would be rewarding.     

X chromosome drive in a widespread Palearctic woodland fly,Drosophila testacea

Selfish genes that bias their own transmission during meiosis can spread rapidly in populations, even if they contribute negatively to the fitness of their host. Driving X chromosomes provide a clear example of this type of selfish propagation. These chromosomes have important evolutionary and ecological consequences, and can be found in a broad range of taxa including plants, mammals and insects. Here, we report a new case of X chromosome drive (X drive) in a widespread woodland fly, Drosophila testacea. We show that males carrying the driving X (SR males) sire 80–100% female offspring and possess a diagnostic X chromosome haplotype that is perfectly associated with the sex ratio distortion phenotype. We find that the majority of sons produced by SR males are sterile and appear to lack a Y chromosome, suggesting that meiotic defects involving the Y chromosome may underlie X drive in this species. Abnormalities in sperm cysts of SR males reflect that some spermatids are failing to develop properly, confirming that drive is acting during gametogenesis. By screening wild‐caught flies using progeny sex ratios and a diagnostic marker, we demonstrate that the driving X is present in wild populations at a frequency of ~ 10% and that suppressors of drive are segregating in the same population. The testacea species group appears to be a hot spot for X drive, and D. testacea is a promising model to compare driving X chromosomes in closely related species, some of which may even be younger than the chromosomes themselves.     

Centromeres: long intergenic spaces with adaptive features

Centromeres are composed of inner kinetochore proteins, which are largely conserved across species, and repetitive DNA, which shows comparatively little sequence conservation. Due to this fundamental paradox the formation and maintenance of centromeres remains largely a mystery. However, it has become increasingly clear that a long-standing balance between epigenetic and genetic control governs the interactions of centromeric DNA and inner kinetochore proteins. The comparison of classical neocentromeres in plants, which are entirely genetic in their mode of operation, and clinical neocentromeres, which are sequence-independent, illustrates the conflict between genetics and epigenetics in regions that control their own transmission to progeny. Tandem repeat arrays present in centromeres may have an origin in meiotic drive or other selfish patterns of evolution, as is the case for the CENP-B box and CENP-B protein in human. In grasses retrotransposons have invaded centromeres to the point of complete domination, consequently breaking genetic regulation at these centromeres. The accumulation of tandem repeats and transposons causes centromeres to expand in size, effectively pushing genes to the sides and opening the centromere to ever fewer constraints on the DNA sequence. On genetic maps centromeres appear as long intergenic spaces that evolve rapidly and apparently without regard to host fitness.     

A study of cryptic terminal chromosome rearrangements in recurrent miscarriage couples detects unsuspected acrocentric pericentromeric abnormalities

Fifty chromosomally normal couples with three or more miscarriages were examined using fluorescent in situ hybridisation (FISH) and a library of subtelomere-specific probes together with alphoid repeats mapping to the acrocentric centromeres. Six abnormalities were found. Firstly, a cryptic reciprocal subtelomere translocation between the long arm of a chromosome 3 and the short arm of a chromosome 10. The other five cryptic abnormalities involved the acrocentric chromosome pericentromeric regions and in one case also Yp. Two patients had a rearranged chromosome 13, where the centromeric region was found to be derived from the short arm, centromere and proximal long arm of chromosome 15. Another two patients had a derived chromosome 22, where the centromere was replaced by two other centromeres, one derived from chromosome 14 and the other from either chromosome 13 or 21, while one patient had the subtelomere region of Yp translocated onto the short arm of a chromosome 21. These abnormalities may be the underlying cause of the recurrent miscarriages, because they may result in abnormal pairing configurations at meiosis leading to non-disjunction of whole chromosomes at metaphase I. The frequency of rearrangements seen in the recurrent miscarriage patient population was significantly different from that in the control group ( P=0.0096, Fisher's exact test) due to the acrocentric pericentromeric abnormalities.     

A REC8-dependent plant Shugoshin is required for maintenance of centromeric cohesion during meiosis and has no mitotic functions

During meiosis, sequential release of sister chromatid cohesion (SSC) during two successive nuclear divisions allows the production of haploid gametes from diploid progenitor cells. Release of SSC along chromosome arms allows first a reductional segregation of homologs, and, subsequently, release of centromeric cohesion at anaphase II allows the segregation of chromatids. The Shugoshin (SGO) protein family plays a major role in the protection of centromeric cohesion in Drosophila and yeast. We have isolated a maize mutant that displays premature loss of centromeric cohesion at anaphase I. We showed that this phenotype is due to the absence of ZmSGO1 protein, a maize shugoshin homolog. We also show that ZmSGO1 is localized to the centromeres. The ZmSGO1 protein is not found on mitotic chromosomes and has no obvious mitotic function. On the basis of these results, we propose that ZmSGO1 specifically maintains centromeric cohesion during meiosis I and therefore suggest that SGO1 core functions during meiosis are conserved across kingdoms and in large-genome species. However, in contrast to other Shugoshins, we observed an early and REC8-dependent recruitment of ZmSGO1 in maize, suggesting that control of SGO1 recruitment to chromosomes is different in plants than in other model organisms.     

Maize centromeres: where sequence meets epigenetics

The centromere is a highly organized structure mainly composed of repeat sequences, which make this region extremely difficult for sequencing and other analyses. It plays a conserved role in equal division of chromosomes into daughter cells in both mitosis and meiosis. However, centromere sequences show notable plasticity. In a dicentric chromosome, one of the centromeres can become inactivated with the underlying DNA unchanged. Furthermore, formerly inactive centromeres can regain activity under certain conditions. In addition, neocentromeres without centromeric repeats have been found in a wide spectrum of species. This evidence indicates that epigenetic mechanisms together with centromeric sequences are associated with centromere specification.     

Sequence of centromere separation of mitotic chromosomes in Chinese hamster

Chromosome preparations in late metaphase cells from bone marrow of colcemid treated male Chinese hamsters were used to analyse the sequence of separation of sister centromeres. Chromatids of chromosomes 2 and 1 are the first ones to separate at centromeres, followed by members of group B, D and C. Some acrocentric chromosome is always the last one to separate at the centromere. The data point to a possible correlation between the position of a centromere in the separation sequence in the genome and the amount of centromeric heterochromatin as well as relation to the phenomenon of non-disjunction.