Chromosome segregation, kinetochores and DNA-microtubule interaction: a preferential satellite DNA-MAP interaction may be conserved in evolution.
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Transcription and evolutionary dynamics of the centromeric satellite repeat CentO in rice.
Satellite DNA is a major component of centromeric heterochromatin in most multicellular eukaryotes, where it is typically organized into megabase-sized tandem arrays. It has recently been demonstrated that small interfering RNAs (siRNAs) processed from centromeric satellite repeats can be involved in epigenetic chromatin modifications which appear to underpin centromere function. However, the structural organization and evolution of the centromeric satellite DNA is still poorly understood. We analyzed the centromeric satellite repeat arrays from rice chromosomes 1 and 8 and identified higher order structures and local homogenization of the CentO repeats in these 2 centromeres. We also cloned the CentO repeats from the CENH3-associated nucleosomes by a chromatin immunoprecipitation (ChIP)-based method. Sequence variability analysis of the ChIPed CentO repeats revealed a single variable domain within the repeat. We detected transcripts derived from both strands of the CentO repeats. The CentO transcripts are processed into siRNA, suggesting a potential role of this satellite repeat family in epigenetic chromatin modification.
Base Sequence↗
Drosophila melanogaster and D. simulans rescue strains produce fit offspring, despite divergent centromere-specific histone alleles.
The interaction between rapidly evolving centromere sequences and conserved kinetochore machinery appears to be mediated by centromere-binding proteins. A recent theory proposes that the independent evolution of centromere-binding proteins in isolated populations may be a universal cause of speciation among eukaryotes. In Drosophila the centromere-specific histone, Cid (centromere identifier), shows extensive sequence divergence between D. melanogaster and the D. simulans clade, indicating that centromere machinery incompatibilities may indeed be involved in reproductive isolation and speciation. However, it is presently unclear whether the adaptive evolution of Cid was a cause of the divergence between these species, or merely a product of postspeciation adaptation in the separate lineages. Furthermore, the extent to which divergent centromere identifier proteins provide a barrier to reproduction remains unknown. Interestingly, a small number of rescue lines from both D. melanogaster and D. simulans can restore hybrid fitness. Through comparisons of cid sequence between nonrescue and rescue strains, we show that cid is not involved in restoring hybrid viability or female fertility. Further, we demonstrate that divergent cid alleles are not sufficient to cause inviability or female sterility in hybrid crosses. Our data do not dispute the rapid divergence of cid or the coevolution of centromeric components in Drosophila; however, they do suggest that cid underwent adaptive evolution after D. melanogaster and D. simulans diverged and, consequently, is not a speciation gene.
Animals↗
Adaptive evolution of the histone fold domain in centromeric histones.
Centromeric DNA, being highly repetitive, has been refractory to molecular analysis. However, centromeric structural proteins are encoded by single-copy genes, and these can be analyzed by using standard phylogenetic tools. The centromere-specific histone, CenH3, replaces histone H3 in centromeric nucleosomes, and is required for the proper distribution of chromosomes during cell division. Whereas histone H3s are nearly identical between species, CenH3s are divergent, with an N-terminal tail that is highly variable in length and sequence. Both the N-terminal tail and histone fold domain (HFD) are subject to adaptive evolution in Drosophila. Similarly, comparisons between Arabidopsis thaliana and Arabidopsis arenosa detected adaptive evolution, but only in the N-terminal tail. We have extended our evolutionary analyses of CenH3s to other members of the Brassicaceae, which allowed the detection of positive selection in both the N-terminal tail and in the HFD. We find that adaptively evolving sites in the HFD can potentially interact with DNA, including sites in the loop 1 region of the HFD that are required for centromeric targeting in Drosophila. Other adaptively evolving sites in the HFD can be localized on the structure of the nucleosome core particle, revealing an extended surface in addition to loop 1 in which conformational changes might alter histone-DNA contacts or water bridges. The identification of adaptively evolving sites provides a structural basis for the interaction between centromeric DNA and the protein that is thought to underlie the evolution of centromeres and the accumulation of pericentric heterochromatin.
Amino Acid Sequence↗
Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences.
Paraformaldehyde-fixed tissue from mouse cerebellum was hybridized with biotin-labeled satellite DNA for identification of centromeres. By using avidin-peroxidase conjugates, it was possible to define the nuclear position of centromeres at the ultrastructural level. Three-dimensional analysis of well-resolved centromere arrays were aided by computer reconstruction of serial sections. Different cell types displayed distinct, nonrandom centromere locations. In Purkinje neurons, the majority of detected sequences were clustered together around the central nucleolus, whereas in granule neurons, more numerous, dispersed centromere clusters were associated with the nuclear membrane. In Purkinje cells, peroxidase-labeled regions corresponded to dense heterochromatic aggregates were detected in Purkinje cells of several different species. These observations suggest that in these highly differentiated cells, the nuclear position of centromeres is maintained in evolution despite species differences in centromeric DNA sequence. Such defined ordering of centromeres may be integral to specific functional capacities.
Animals↗
Structural features of the rice chromosome 4 centromere.
A complete sequence of a chromosome centromere is necessary for fully understanding centromere function. We reported the sequence structures of the first complete rice chromosome centromere through sequencing a large insert bacterial artificial chromosome clone-based contig, which covered the rice chromosome 4 centromere. Complete sequencing of the 124-kb rice chromosome 4 centromere revealed that it consisted of 18 tracts of 379 tandemly arrayed repeats known as CentO and a total of 19 centromeric retroelements (CRs) but no unique sequences were detected. Four tracts, composed of 65 CentO repeats, were located in the opposite orientation, and 18 CentO tracts were flanked by 19 retroelements. The CRs were classified into four types, and the type I retroelements appeared to be more specific to rice centromeres. The preferential insert of the CRs among CentO repeats indicated that the centromere-specific retroelements may contribute to centromere expansion during evolution. The presence of three intact retrotransposons in the centromere suggests that they may be responsible for functional centromere initiation through a transcription-mediated mechanism.
Base Sequence↗
Genetic conflicts during meiosis and the evolutionary origins of centromere complexity.
Centromeric DNA evolves rapidly, ranging in size and complexity over several orders of magnitude. Traditional attempts at studying centromeres have left unexplained the causes underlying this complexity and rapid evolution. Instead of directly studying centromeric DNA sequence, our approach has been to study the proteins that epigenetically determine centromere identity. We have discovered that centromeric histones (CenH3s) have evolved under positive selection in multiple lineages, suggesting an involvement in recurrent genetic conflict. Our hypothesis is that 'centromere-drive' is the source of this conflict. Under this model, centromeres compete via microtubule attachments for preferential transmission in female meioses occurring in animals and plants. Since only one of four meiotic products will become the egg, this competition confers a selfish advantage to chromosomes that can make more microtubule attachments, resulting in runaway expansions of centromeric satellites. While beneficial to the 'driving' chromosome, these expansions can have deleterious effects on the fitness of an organism and of the species. CenH3s as well as other heterochromatin proteins have evolved under positive selection to suppress the deleterious consequences of 'centromere-drive' by restoring meiotic parity.
Animals↗
Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice.
The abundance of repetitive DNA varies greatly across centromeres within an individual or between different organisms. To shed light on the molecular mechanisms of centromere repeat proliferation, we performed structural analysis of LTR-retrotransposons, mostly centromere retrotransposons of rice (CRRs), and phylogenetic analysis of CentO satellite repeats harbored in the core region of the rice chromosome 4 centromere (CEN4). The data obtained demonstrate that the CRRs in the centromeric region we investigated have been enriched more significantly by recent rounds of segmental duplication than by original integration of active elements, suggesting that segmental duplication is an important process for CRR accumulation in the centromeric region. Our results also indicate that segmental duplication of large arrays of satellite repeats is primarily responsible for the amplification of satellite repeats, contributing to rapid reshuffling of CentO satellites. Intercentromere satellite homogenization was revealed by genome-wide comparison of CentO satellite monomers. However, a 10-bp duplication present in nearly half of the CEN4 monomers was found to be completely absent in rice centromere 8 (CEN8), suggesting that CEN4 and CEN8 may represent two different stages in the evolution of rice centromeres. These observations, obtained from the only complex eukaryotic centromeres to have been completely sequenced thus far, depict the evolutionary dynamics of rice centromeres with respect to the nature, timing, and process of centromeric repeat amplification.
Centromere↗
Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone.
All eukaryotes contain centromere-specific histone H3 variants (CenH3s), which replace H3 in centromeric chromatin. We have previously documented the adaptive evolution of the Drosophila CenH3 (Cid) in comparisons of Drosophila melanogaster and Drosophila simulans, a divergence of approximately 2.5 million years. We have proposed that rapidly changing centromeric DNA may be driving CenH3's altered DNA-binding specificity. Here, we compare Cid sequences from a phylogenetically broader group of Drosophila species to suggest that Cid has been evolving adaptively for at least 25 million years. Our analysis also reveals conserved blocks not only in the histone-fold domain but also in the N-terminal tail. In several lineages, the N-terminal tail of Cid is characterized by subgroup-specific oligopeptide expansions. These expansions resemble minor groove DNA binding motifs found in various histone tails. Remarkably, similar oligopeptides are also found in N-terminal tails of human and mouse CenH3 (Cenp-A). The recurrent evolution of these motifs in CenH3 suggests a packaging function for the N-terminal tail, which results in a unique chromatin organization at the primary constriction, the cytological marker of centromeres.
Amino Acid Sequence↗
Characterization of a maize chromosome 4 centromeric sequence: evidence for an evolutionary relationship with the B chromosome centromere.
Previous work has identified sequences specific to the B chromosome that are a major component of the B centromere. To address the issue of the origin of the B and the evolution of centromere-localized sequences, DNA prepared from plants without B chromosomes was probed to seek evidence for related sequences. Clones were isolated from maize line B73 without B chromosomes by screening DNA at reduced stringency with a B centromeric probe. These clones were localized to maize centromere 4 using fluorescence in situ hybridization. They showed homology to a maize centromere-mapped sequence, to maize B chromosome centromere sequences, and to a portion of the unit repeat of knobs, which act as neocentromeres in maize. A representative copy was used to screen a BAC library to obtain these sequences in a larger context. Each of the six positive BACs obtained was analyzed to determine the nature of centromere 4-specific sequences present. Fifteen subclones of one BAC were sequenced and the organization of this chromosome 4-specific repeat was examined.
Base Sequence↗
Structure and dynamic organization of centromeres/prekinetochores in the nucleus of mammalian cells.
Although considerable research has been focused on understanding the structure and molecular organization of the centromere-kinetochore complex of mitotic chromosomes, few reports have dealt with the centromere (prekinetochore) in the interphase nucleus. In the present study, we utilized anti-centromere antibodies from the serum of patients with the autoimmune disease, scleroderma CREST (calcinosis, Raynaud's phenomenon, esophageal dismotility, sclerodactyly, telangiectasia), as probes to investigate the structure and morphogenesis of the centromere in interphase nuclei of three cell lines using laser scanning confocal microscopy and immunoelectron microscopy. Of particular interest were the chromosomes of the Indian muntjac (2n = 6 in females and 2n = 7 in males), whose large centromeres are thought to have evolved through the tandem fusion of smaller centromeres of a Chinese muntjac-like progenitor species (2n = 46). The various forms and patterns of centromeres observed in the nucleus correlated with stages in the cell cycle as determined by bromodeoxyuridine labeling and apparently represent stages in prereplication, replication and maturation. Immunoelectron microscopic studies using CREST antisera indicated that the high order structure of chromatin associated with each prekinetochore undergoes a regular unfolding-refolding cycle, displaying small bead-like subunits tandemly arranged along a linear thread of centromeric DNA, much like that reported for mitotic chromosomes. Individual centromeres/prekinetochores form a stable association with the 9-13 nm core filaments of the nucleoskeletal network in the nucleus that later become the chromosome scaffold of mitotic chromosomes. Our findings provide morphological support for the hypothesis that the spatial arrangements of individual centromeres within the nucleus may have influenced centromeric translocations and fusions during chromosome evolution. Therefore, the centromere-kinetochore complex, best known for its essential role in partitioning chromosomes in mitosis and meiosis, may also function in chromosome movements and associations in interphase.
Animals↗
Structural dynamics of eukaryotic chromosome evolution.
Large-scale genome sequencing is providing a comprehensive view of the complex evolutionary forces that have shaped the structure of eukaryotic chromosomes. Comparative sequence analyses reveal patterns of apparently random rearrangement interspersed with regions of extraordinarily rapid, localized genome evolution. Numerous subtle rearrangements near centromeres, telomeres, duplications, and interspersed repeats suggest hotspots for eukaryotic chromosome evolution. This localized chromosomal instability may play a role in rapidly evolving lineage-specific gene families and in fostering large-scale changes in gene order. Computational algorithms that take into account these dynamic forces along with traditional models of chromosomal rearrangement show promise for reconstructing the natural history of eukaryotic chromosomes.
Animals↗
Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores.
The centromere-specific histone variant CENP-A (CID in Drosophila) is a structural and functional foundation for kinetochore formation and chromosome segregation. Here, we show that overexpressed CID is mislocalized into normally noncentromeric regions in Drosophila tissue culture cells and animals. Analysis of mitoses in living and fixed cells reveals that mitotic delays, anaphase bridges, chromosome fragmentation, and cell and organismal lethality are all direct consequences of CID mislocalization. In addition, proteins that are normally restricted to endogenous kinetochores assemble at a subset of ectopic CID incorporation regions. The presence of microtubule motors and binding proteins, spindle attachments, and aberrant chromosome morphologies demonstrate that these ectopic kinetochores are functional. We conclude that CID mislocalization promotes formation of ectopic centromeres and multicentric chromosomes, which causes chromosome missegregation, aneuploidy, and growth defects. Thus, CENP-A mislocalization is one possible mechanism for genome instability during cancer progression, as well as centromere plasticity during evolution.
Animals↗
Duplicated KOX zinc finger gene clusters flank the centromere of human chromosome 10: evidence for a pericentric inversion during primate evolution.
Two related zinc finger (ZNF) gene clusters from the pericentromeric region of human chromosome 10, defined by cDNAs of the KOX series, have been cloned in yeast artificial chromosomes (YACs). The two clusters evolved by duplication of an ancestral gene cluster before the divergence of the human and great ape lineages. Included in cluster A are the ZNF gene sequences ZNF11A, ZNF33A, and ZNF37A, while cluster B comprises the related sequences ZNF11B, ZNF33B and ZNF37B. Genes from both clusters are expressed: cDNAs KOX2, KOX31 and KOX21 derive from ZNF11B, ZNF33A and ZNF37A, respectively. Further YACs have been isolated which link ZNF11A and ZNF33A to another gene, ZNF25, defined by cDNA clone KOX19. Therefore ZNF25 also forms part of cluster A, but has no counterpart in cluster B. Surprisingly, the KOX ZNF gene clusters are located on opposite sides of the centromere: cluster A maps to 10p11.2, while cluster B is in 10q11.2. This suggests the occurrence during primate evolution of a previously undescribed pericentric inversion subsequent to the cluster duplication. The evolution of this subset of KOX ZNF genes has therefore involved three types of genetic event: local gene duplication, gene cluster duplication, and chromosome rearrangement.
Amino Acid Sequence↗
A high-resolution whole-genome cattle-human comparative map reveals details of mammalian chromosome evolution.
Approximately 3,000 cattle bacterial artificial chromosome (BAC)-end sequences were added to the Illinois-Texas 5,000-rad RH (RH, radiation hybrid) map. The BAC-end sequences selected for mapping are approximately 1 Mbp apart on the human chromosomes as determined by blastn analysis. The map has 3,484 ordered markers, of which 3,204 are anchored in the human genome. Two hundred-and-one homologous synteny blocks (HSBs) were identified, of which 27 are previously undiscovered, 79 are extended, 26 were formed by previously unrecognized breakpoints in 18 previously defined HSBs, and 23 are the result of fusions. The comparative coverage relative to the human genome is approximately 91%, or 97% of the theoretical maximum. The positions of 64% of all cattle centromeres and telomeres were reassigned relative to their positions on the previous map, thus facilitating a more detailed comparative analysis of centromere and telomere evolution. As an example of the utility of the high-resolution map, 22 cattle BAC fingerprint contigs were directly anchored to cattle chromosome 19 [Bos taurus, (BTA) 19]. The order of markers on the cattle RH and fingerprint maps of BTA19 and the sequence-based map of human chromosome 17 [Homo sapiens, (HSA) 17] were found to be highly consistent, with only two minor ordering discrepancies between the RH map and fingerprint contigs. The high-resolution Illinois-Texas 5,000-rad RH and comparative maps will facilitate identification of candidate genes for economically important traits, the phylogenomic analysis of mammalian chromosomes, proofing of the BAC fingerprint map and, ultimately, aid the assembly of cattle whole-genome sequence.
Animals↗
Evolution and domestication-trait associations of ultra-long centromere haplotypes in pepper plants.
Centromeric and pericentromeric regions of most eukaryotic genomes are highly repetitive and strongly recombination-suppressed, confounding efforts to resolve genetic variation, population structure and phenotypic associations. Pepper (Capsicum annuum) centromeres are nearly devoid of satellite repeats, facilitating assembly and population-level comparison of centromeric regions. Here we integrate 9 near-complete genome assemblies, CENH3 ChIP-seq profiles from 26 diverse accessions, and resequencing and phenotypic data from ~400 cultivated and wild accessions to investigate population-level diversity and phenotypic relevance of pepper peri/centromeric regions. Functional centromere positions are largely fixed on 8 of 12 chromosomes, whereas the remaining 4 carry distinct centromeric epialleles shaped mainly by centromere repositioning and pericentromeric inversions. Pepper centromeres are embedded within ultra-long centromere-spanning haplotype (cenhap) blocks, ranging from 29.8 to 112.9 Mb and collectively covering 23.96% of the genome; each block contains only 1-4 major haplotypes. Some cenhaps may act as supergene-like units and are strongly associated with fruit traits, probably because recombination-suppressed intervals harbour multiple fruit-related genes, including OFP and F-box genes. F2 segregation assays further reveal transmission distortion of chromosomes carrying alternative cenhaps. Together, these findings highlight peri/centromeric regions as underrecognized reservoirs of agronomically important variation.
Centromere↗
Genus-specific localization of the TaiI family of tandem-repetitive sequences in either the centromeric or subtelomeric regions in Triticeae species (Poaceae) and its evolution in wheat.
The TaiI family sequences are classified as tandem repetitive DNA sequences present in the genome of tribe Triticeae, and are localized in the centromeric regions of common wheat, but in the subtelomeric heterochromatic regions of Leymus racemosus and related species. In this study, we investigated the chromosomal distribution of TaiI family sequences in other Triticeae species. The results demonstrated a centromeric localization in genera Triticum and Aegilops and subtelomeric localization in other genera, thus showing a genus-dependent localization of TaiI family sequences in one or the other region. The copy numbers of TaiI family sequences in species in the same genus varied greatly, whether in the centromeric or subtelomeric regions (depending on genus). We also examined the evolution of TaiI family sequences during polyploidization of hexaploid common wheat. A comparison of chromosomal locations of the major TaiI family signals in common wheat and in its ancestral species suggested that the centromeric TaiI family sequences in common wheat were inherited from its ancestors with little modification, whereas a mixed origin for the B genome of common wheat was indicated.
Centromere↗
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
The flowering plant Arabidopsis thaliana is an important model system for identifying genes and determining their functions. Here we report the analysis of the genomic sequence of Arabidopsis. The sequenced regions cover 115.4 megabases of the 125-megabase genome and extend into centromeric regions. The evolution of Arabidopsis involved a whole-genome duplication, followed by subsequent gene loss and extensive local gene duplications, giving rise to a dynamic genome enriched by lateral gene transfer from a cyanobacterial-like ancestor of the plastid. The genome contains 25,498 genes encoding proteins from 11,000 families, similar to the functional diversity of Drosophila and Caenorhabditis elegans--the other sequenced multicellular eukaryotes. Arabidopsis has many families of new proteins but also lacks several common protein families, indicating that the sets of common proteins have undergone differential expansion and contraction in the three multicellular eukaryotes. This is the first complete genome sequence of a plant and provides the foundations for more comprehensive comparison of conserved processes in all eukaryotes, identifying a wide range of plant-specific gene functions and establishing rapid systematic ways to identify genes for crop improvement.
Animals↗