- Open Access
Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives
© The Author(s). 2017
- Received: 3 May 2017
- Accepted: 1 June 2017
- Published: 21 June 2017
Paradoxically, centromeres are known both for their characteristic repeat sequences (satellite DNA) and for being epigenetically defined. Maize (Zea mays mays) is an attractive model for studying centromere positioning because many of its large (~2 Mb) centromeres are not dominated by satellite DNA. These centromeres, which we call complex centromeres, allow for both assembly into reference genomes and for mapping short reads from ChIP-seq with antibodies to centromeric histone H3 (cenH3).
We found frequent complex centromeres in maize and its wild relatives Z. mays parviglumis, Z. mays mexicana, and particularly Z. mays huehuetenangensis. Analysis of individual plants reveals minor variation in the positions of complex centromeres among siblings. However, such positional shifts are stochastic and not heritable, consistent with prior findings that centromere positioning is stable at the population level. Centromeres are also stable in multiple F1 hybrid contexts. Analysis of repeats in Z. mays and other species (Zea diploperennis, Zea luxurians, and Tripsacum dactyloides) reveals tenfold differences in abundance of the major satellite CentC, but similar high levels of sequence polymorphism in individual CentC copies. Deviation from the CentC consensus has little or no effect on binding of cenH3.
These data indicate that complex centromeres are neither a peculiarity of cultivation nor inbreeding in Z. mays. While extensive arrays of CentC may be the norm for other Zea and Tripsacum species, these data also reveal that a wide diversity of DNA sequences and multiple types of genetic elements in and near centromeres support centromere function and constrain centromere positions.
- Centromere drift
- Centromere stability
- Satellite DNA
Eukaryotes segregate their chromosomes during cell division using spindle microtubules, where the microtubules attach to chromosomes via complex protein structures called kinetochores. Centromeres are the parts of the chromosomes where kinetochores assemble and are marked by specific DNA binding proteins, usually including the centromeric histone H3 variant cenH3 (also widely known as CENP-A) . The size and sequence composition of centromeres, as defined by cenH3 footprints, varies widely between species. Centromeres have been reported from 40 kb in length in chicken  to 4 Mb in oat  and are usually dominated by tandem repeats (known as satellites) in plants and animals [4, 5]. In plants, a conserved family of Gypsy retrotransposons called centromeric retrotransposons specifically targets centromeres as well [6, 7]. In some species the chromosomes are holocentric (or polycentric) and characterized by multiple sites of centromere formation, and satellite DNA has been discovered in the polycentric centromeres of several plant genera [8, 9].
In most species the role of centromere sequence in conferring centromere function is unclear. With the exception of some fungi with small centromeres , no known centromere sequence motifs or structural features strictly define centromeres. Centromere sequences can vary widely even between homologous chromosomes in the same species [11, 12]. Some species, such as the African ass, potato, and maize, have a mixture of different types of centromeres, with some being rich in satellite DNA and others containing large numbers of retrotransposons and little or no satellite DNA [11, 13–16]. Centromeres without long arrays of satellite DNA have been referred to as evolutionarily new centromeres (ENCs)  and as neocentromeres . These terms reflect the fact that centromeres have often been observed to form de novo at entirely new positions that lack satellite DNA . Because of its innate instability, however, satellite DNA could also be lost from existing centromeres. Here we simply refer to centromeres that lack extensive satellite arrays as “complex” centromeres to describe the fact that they consist of a variety of retrotransposons and other polymorphic genetic elements. This sequence complexity, if assembled into a reference genome, allows for unambiguous mapping of short reads.
Experiments with human tissue culture and grass species have shown that the amount of cenH3/CENP-A loaded on centromeres is determined by cellular context rather than by the size or structure of the centromeric domains [18–20]. Consistent with this, overexpression of cenH3 (CID) in Drosophila causes ectopic centromere formation at multiple loci per chromosome . However, the fact that cenH3 occupies smaller domains in neocentromeres than what is normally present on established centromeres suggests that sequence composition may also be important for centromere size and function [22–24]. Only about 100 CENP-A-containing nucleosomes occupy each centromere during cell division in human cells, leaving most of the nucleosomes to contain other forms of histone H3 . During each cell cycle, the total amount of CENP-A is diluted by DNA replication but is replaced as a part of a self-propagating system of centromere maintenance where preexisting centromere proteins signal the deposition of new ones . There are also mechanisms that remove cenH3. For instance, cenH3 removal occurs naturally as a part of plant gametogenesis [25, 26]. Similarly, budding yeast uses an E3 ligase-based mechanism to remove ectopically placed cenH3 from chromosome arms [27, 28]. It is likely that plants and animals have similar mechanisms to prevent the formation of ectopic centromeres and constrain normal centromere boundaries.
Large-scale genetic changes such as chromosomal rearrangements, deletions, and insertions or bursts of retrotransposon activity could force centromere positions to change. However, little is known about the dynamics and stability of centromeres at the purely epigenetic level. Centromeres in horse tissue culture cells were reported to occupy distinct positions ranging over a couple hundred kilobases, but the lines chosen may have also differed at the genetic level . Perhaps the best evidence for epigenetic instability comes from chicken tissue cultured cells, where lines derived from a common parent showed clear evidence for centromere drifting on a scale of tens of kilobases . The observed centromere movement occurred over an unknown number of cellular generations in wild-type chicken cells, but greater than 40. In contrast, lines containing mutants in key inner kinetochore proteins exhibited drift in as little as 40 cellular generations. We previously compared centromere positions between maize populations with genetically identical centromeres and found no evidence for centromere drift between populations, but left open the possibility of small scale drift between individual plants .
Here we take advantage of the complex centromeres in maize (Zea mays mays, the cultivated Zea mays subspecies) and a comparative analysis of its wild relatives to explore centromere dynamics and diversity in terms of both genetics (sequence composition) and epigenetics (cenH3 localization). Focusing on the B73 inbred stock, with its complex centromeres, we found that centromere boundaries are not rigidly defined, but ebb and flow between individuals, with visible differences on the order of hundreds of kilobases. These differences, however, were not shared between siblings, suggesting that positional shifts are generally not heritable. We found no evidence that centromere size or position were affected by centromeres at non-equivalent positions in inter- and intra-species F1 hybrids. We also found examples of complex centromeres in each of the three other Z. mays subspecies, with Z. mays huehuetenangensis having as many or more complex centromeres than Z. mays mays. In the genomes we sampled, the major satellite sequence CentC had a tenfold range in abundance, and sequences of individual CentC copies were highly polymorphic. The distributions of mutations in CentC copies were strikingly similar among species and subspecies. Surprisingly, polymorphic CentC copies were strongly enriched in CENH3 ChIP samples despite their dissimilarity to the consensus sequence. Taken together, these results indicate that centromeres can drift along the DNA as if untethered, but rather than progressing, maintain stable equilibrium over generations, suggesting a level of genetic control that is not apparent at the sequence level.
Resilience of complex centromere positions to epigenetic drift and hybridization
The analysis of centromere positions and stability in maize relies primarily on the interpretation of ChIP-seq data aligned to the B73 reference genome. This is possible because most of the centromeres in B73 are complex, having little CentC, but large numbers of ancient retroelements that are nested within each other and effectively unique over the length of a 150-nucleotide Illumina read. However, three of the ten chromosomes in B73—1, 6, and 7—have large arrays of CentC that are presumably the locations of centromeres . For these centromeres ChIP-seq fails for two reasons: because the physical map for these centromeres is incomplete and short reads cannot be uniquely mapped.
We also wondered how centromeres would be affected by outcrossing. In Arabidopsis thaliana, cenH3 is erased from the egg cell such that only the sperm contributes cenH3 , raising the possibility that paternal centromeres specify the positions of both centromeres in the zygote. We previously identified two maize inbreds with centromeres at different positions relative to B73: NS701, where centromere 5 is at a different position; and LH74, where centromeres 5 and 8 are at different positions. We made bidirectional crosses between both inbreds and B73 and carried out ChIP-seq to test whether both parental centromere positions would be maintained in the hybrids or one position would shift to match the paternal one. We found that both positions were maintained with no evidence of any change in position (Fig. 1). We also carried out CENH3 ChIP-seq on an interspecies hybrid, B73 × Zea luxurians. Z. luxurians has a 50% larger genome and centromeres with long arrays of CentC [32, 33]. In the F1 hybrid, the centromeres on the B73 chromosomes neither shifted outside the normal range nor changed in size. Since these experiments were carried out specifically in F1 hybrids, it remains a possibility that centromere positions could shift or increase in size after subsequent generations in hybrid genetic backgrounds. These results, however, indicate that centromere positions are generally resilient to change when the genetic structure of the chromosome remains constant.
Frequent complex centromeres in geographically and genetically diverse Z. mays
Summary of CENH3 ChIP samples
Place of origin
ChIP reads (in millions)
Input reads (in millions)
CentC in ChIP reads (%)
CentC in input reads (%)
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
Zea mays mays
LH74 x B73
Zea mays mays
B73 x LH74
Zea mays mays
Zea mays mays
B73 x NS701
Zea mays mays
NS701 x B73
Zea mays mays x Zea luxurians
B73 x PI 422162
Zea mays parviglumis
Zea mays parviglumis
Zea mays mexicana
Federal District, Mexico
Zea mays mexicana
Zea mays mexicana
Zea mays huehuetenangensis
Zea mays huehuetenangensis
Guatemala, via Florida
CentC polymorphism and relation to CENH3 binding
Alpha satellites in human cells have been reported to show evidence of homogenization, presumably as a result of repeated expansion and contraction of long identical repeat arrays by unequal recombination . This differs from maize, where, at least in the B73 inbred, CentC repeats are highly polymorphic and show no signs of homogenization nor accumulation of specific variants . We wondered whether genomes with large amounts of CentC (Fig. 3a) would show evidence of CentC homogenization similar to alpha satellites in humans. To this end we took advantage of RepeatExplorer software, which identifies repeats without using a reference that may bias the results . Surprisingly, all Zea species and subspecies examined had the same consensus CentC sequence and a similar level of CentC polymorphism, where the overall level of identity with the consensus was close to 96% (Fig. 3d). Very few CentC copies were identical to the consensus throughout the Zea samples, providing no evidence for sequence homogenization within CentC arrays. In contrast, copies of the tandem repeat knob180 found on maize chromosome arms, which is under selection for meiotic drive in some backgrounds , showed higher levels of identity to its consensus sequence (Fig. 3f).
The observation that CentC is generally conserved (though polymorphic) and reliably present in the centromeres of Zea and Tripsacum raises the question of whether it makes a useful contribution to centromere function. One way it might contribute is by making a good substrate for CENH3 binding (though CENH3 is clearly not limited to CentC). If this were the case, we would expect to see a different distribution of CentC variants from ChIP than whole-genome input. The simplest expectation would be that the fraction of CentC copies bound to CENH3 would more closely resemble the consensus. However, plots of CentC polymorphism in ChIP and input samples produced nearly identical patterns (Fig. 3d, e). Consistent with this, k-mer analysis of CentC sequences in the reads revealed similar frequencies of distinct k-mers both between species and between ChIP and input reads (Additional file 1: Figure S5). For this analysis, we sampled the same number of CentC reads from each species (30,000), trimmed all reads to the same length (100 nucleotides), and counted the frequency (copy number) of distinct 50-mers. With this sampling depth, CentC reads derived from a genome with perfectly homogenous CentC would yield distinct 50-mers with an average copy number of 9808 each (51 50-mers per read times 30,000 reads divided by 156 possible 50-mers in a 156-bp circular sequence). In contrast, in each species that we examined, the vast majority of 50-mers were in copy numbers of less than 100, with a tail of the distributions reaching up to copy numbers of 2000. Taken together the results indicate that although CentC is the predominant genetic substrate for centromeres, any functional contribution has a very loose relation to its linear sequence.
CENH3 is diluted during DNA replication and replenished later in the cell cycle by a mechanism that relies on the presence of other kinetochore proteins [40, 41]. During the growth of a maize plant from a single-cell zygote to the next generation, this dilution/replenishment process occurs around 50 times . In the absence of sequence-specific binding of CENH3 to DNA, one would expect that changes in the distribution of CENH3 nucleosomes would accumulate between individual cells. While we cannot measure CENH3 distributions in individual cells, we can measure the average CENH3 distribution in large numbers of cells derived from two cells (whole seedlings derived from a single egg and sperm). The variation in centromere positions we observe between seedlings (Fig. 1) could be largely determined by the initial position in the zygote or could accumulate throughout development. Consistent with our prior work, we found no evidence of heritable variation between genetically identical individuals, which confirms our conclusion that the genetic makeup of the centromere constrains the average centromere position . This constraint is not easily loosened, neither by parent-of-origin affects in Z. mays mays nor by hybridization, including interspecies hybridization between Z. mays and Z. luxurians.
Satellite centromeres were more common than complex centromeres in our survey of Zea, except in Z. mays mays and Z. may huehuetenangensis (Fig. 2). This is consistent with FISH karyotyping of diverse Zea that indicates less CentC in these subspecies than in other Zea . An inverse relationship between the amount of CentC on a chromosome and the presence of a complex centromere has been clearly demonstrated in Z. mays mays, the cultivated subspecies . This could be explained if the loss of CentC induces the formation of the complex centromeres  or if the formation of complex centromeres induces the loss of CentC by exposing them to recombination. We cannot rule out either hypothesis, but our data show that complex centromeres are more common throughout Zea mays when there is less CentC. While it makes sense that centromeres must occupy more complex regions if there are no tandem repeat arrays, the reverse need not be true. For instance, in the B73 inbred, centromere 5 does not overlap with the only mapped CentC array on chromosome 5  and large arrays of CentC are visible by FISH in other maize chromosome arms [3, 43]. Our observation that, as a general rule, centromeres do tend to occupy long CentC arrays when they are present (Fig. 3) supports the hypothesis that CentC is particularly well adapted for centromere function [44, 45]. No empirical studies have addressed the role of tandem repeats in plant centromeres, but several studies of animal cells have demonstrated subtle defects in neocentromeres that lack normal centromeric tandem repeats [24, 46–48].
Our data raise many interesting questions about the dynamics of CentC. How is the CentC consensus sequence conserved across Zea when individual copies are highly polymorphic and the number of copies varies dramatically between subspecies, between individuals, and even between homologous chromosomes (Fig. 3)? Why is CentC conserved in distant grasses such as Oryza yet absent from closer ones such as Sorghum and Miscanthus ? Do Z. mays mays and Z. mays huehuetenangensis have more complex centromeres because of recent loss of CentC or are they better representations of an ancestral type that had little or none (and which would have been like Sorghum and Miscanthus)? Are these repeats frequently transferred horizontally, as centromeric retrotransposons are proposed to do ? Perhaps the most important question is whether CentC contributes towards centromere function, or at the other extreme, whether it is merely a selfish element that hijacks centromeres. Our comparison of CentC copies in the centromere (ChIP) versus CentC copies in the whole genome (input) revealed no overt preference for the conserved CentC consensus sequence in centromeres. Thus, any contribution of CentC to centromere function must allow for a good deal of flexibility in CentC sequence. These data along with our experiments showing stable positioning of complex centromeres demonstrate a general principle of centromeres, which is that they can be stably propagated over a wide diversity of centromere genetic elements.
What are the features of the genetic landscape that determine points of stable equilibrium? Several phenomena have been proposed. One is a negative role of transcribed genes. Centromeres are usually located in gene-poor regions, and evidence from experiments with maize chromosomes suggests genes can help enforce centromere boundaries . The existence of megabase-scale arrays of non-centromeric tandem repeats such as the knob180 repeats in maize indicates that absence of genes is not sufficient to promote centromere formation . A second candidate feature is a positive role for transcription. At first glance this seems like a contradiction; however, a specific form of transcription could occur in tandem repeats that, for example, facilitates incorporation of CENH3 . The sequence features that are important for such transcription might be highly flexible and thus would not be expected to be conserved. A third feature could be related to DNA repair by homologous recombination . Multiple centromere proteins are related to homologous recombination and DNA repair . The tandem repeats of human centromeres (alpha satellites) exhibit a specialized form of DNA repair, including the formation of DNA loops that might be important for centromere organization . Last is the potential for tandem repeats to form strong interactions between DNA and cenH3 nucleosomes, which might be important to tolerate the stresses associated with spindle attachments. This theory has been discussed but not tested [44, 45, 54]. It is likely that multiple features—scarcity of genes, a specific form of non-coding transcription, DNA repair by homologous recombination, and strong nucleosome-DNA interactions—work together to subtly influence the position and function of centromeres in a way that tolerates multiple sequence contexts.
All accessions with PI or Ames numbers were obtained from GRIN, the National Genetics Resource Program (Ames, Iowa). Accession names and geographical origins are indicated in Table 1.
ChIP and library preparation
Whole seedlings including roots between 3 and 13 g in weight were harvested and frozen in liquid nitrogen, then finely ground with pre-chilled mortars and pestles. Between 3 and 4 g of each were used for ChIP using a native ChIP protocol with micrococcal nuclease digestion of the DNA. An antibody raised against rice CENH3, which has broad reactivity to CENH3 in grasses, including oat, wheat, millet, and maize, was used to immunoprecipitate single nucleosomes containing CENH3 [3, 18, 55]. A detailed, step-by-step protocol is included in Additional file 2. For each ChIP, 5–30 ng of DNA was used for preparing Illumina sequencing libraries (KAPA hyper prep kit #KK8500). Barcoded adapters were used for pooling libraries (Bioo Scientific NEXTflex™ Bisulfite-Seq Barcodes, #511912). Libraries were amplified with five or six cycles of PCR, and amplicons of 100–200 bp were separated from longer fragments by gel electrophoresis and purified without heating (Qiagen QIAquick Gel Extraction Kit #28704). The Illumina NextSeq500 platform was used to generate 150-nucleotide single-end reads, and numbers of reads for each sample are listed in Table 1.
Reads were quality trimmed using the FASTX-Toolkit 0.0.14 fastq_quality_trimmer, with “-Q33 -t 20” parameters (http://hannonlab.cshl.edu/fastx_toolkit/), then adapters removed with Cutadapt with the following parameters: “-a AGATCGGAAGAGC -m 100 -e .05 -O 1 -m 100” . Reads were mapped to the B73 refgen V4 genome  and the W22 version 2.0 assembly (http://www.maizegdb.org/genome/genome_assembly/Zm-W22-REFERENCE-NRGENE-2.0) using the Burrows-Wheeler Aligner BWA-MEM with default parameters . Only uniquely mapping reads, defined by MAPQ values of at least 20, were included for further analysis. The alignments were converted to BAM files and sorted using SAMtools . Read coverage and enrichment were displayed after converting BAM files to tdf files with means of 20,000 kb intervals using the Integrative Genome Viewer . RepeatExplorer  was used to cluster reads independently of genome alignment from each input sample (default parameters). Circular consensus sequences from each set of reads in the CentC cluster produced by RepeatExplorer were made using the Geneious® version 8.0.4 De Novo Assemble tool with default “High Sensitivity/Medium” settings (with the following options selected: “Don't merge variants with coverage over approximately 6”, “Merge homopolymer variants”, and “Circularize contigs with matching ends”). The abundance and percent identity with consensus sequences of repeats in the ChIP and input files was determined using blastall with parameters as follows: “-p blastn -e 1e-5 -W 7 -G 2 -E 1 -r 1 -q -1”. Only reads producing alignments of at least 125 bp in length to consensus sequence dimers were included. The Zea CentC consensus sequence shared in all Zea genomes sampled and used for these analyses is:
The corresponding knob180 consensus sequence is:
JELLYFISH software, version 2.2.3, was used for k-mer analysis . After adapter removal, reads were trimmed to 100 nucleotides and aligned to the CentC consensus dimer sequence as before, except only reads producing alignment lengths of at least 90 bp were included for subsequent analysis. We sampled 30,000 CentC reads from each species ChIP and input.
The CENH3 antibody was generously provided by Paul Talbert. Our ChIP protocol was based on a protocol generously shared by Zixian Zeng, Hainan Zhou, and Jiming Jiang. This study was supported in part by resources and technical expertise from the Georgia Advanced Computing Resource Center and the Georgia Genomics Facility at the University of Georgia.
Funding for this study was provided to R. Kelly Dawe through NSF grant 1444514.
Availability of data and materials
The raw illumina reads generated in this current study are available in the NCBI sequence read archive (SRP105290). Run IDs for each experiment are listed in Additional file 3.
JIG and NW performed experiments and analyzed the data in this study. JIG and RKD planned experiments and wrote the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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- Chen CC, Mellone BG. Chromatin assembly: journey to the CENter of the chromosome. J Cell Biol. 2016;214:13–24.View ArticlePubMedPubMed CentralGoogle Scholar
- Shang WH, Hori T, Martins NM, Toyoda A, Misu S, Monma N, Hiratani I, Maeshima K, Ikeo K, Fujiyama A, et al. Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell. 2013;24:635–48.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang K, Wu Y, Zhang W, Dawe RK, Jiang J. Maize centromeres expand and adopt a uniform size in the genetic background of oat. Genome Res. 2014;24:107–16.View ArticlePubMedPubMed CentralGoogle Scholar
- Alkan C, Cardone MF, Catacchio CR, Antonacci F, O'Brien SJ, Ryder OA, Purgato S, Zoli M, Della Valle G, Eichler EE, Ventura M. Genome-wide characterization of centromeric satellites from multiple mammalian genomes. Genome Res. 2011;21:137–45.View ArticlePubMedPubMed CentralGoogle Scholar
- Melters DP, Bradnam KR, Young HA, Telis N, May MR, Ruby JG, Sebra R, Peluso P, Eid J, Rank D, et al. Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 2013;14:R10.View ArticlePubMedPubMed CentralGoogle Scholar
- Sharma A, Presting GG. Evolution of centromeric retrotransposons in grasses. Genome Biol Evol. 2014;6:1335–52.View ArticlePubMedPubMed CentralGoogle Scholar
- Neumann P, Navrátilová A, Koblížková A, Kejnovský E, Hřibová E, Hobza R, Widmer A, Doležel J, Macas J. Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA. 2011;2:4.View ArticlePubMedPubMed CentralGoogle Scholar
- Marques A, Ribeiro T, Neumann P, Macas J, Novák P, Schubert V, Pellino M, Fuchs J, Ma W, Kuhlmann M, et al. Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin. Proc Natl Acad Sci U S A. 2015;112:13633–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Neumann P, Pavlíková Z, Koblížková A, Fuková I, Jedličková V, Novák P, Macas J. Centromeres off the hook: massive changes in centromere size and structure following duplication of CenH3 gene in Fabeae species. Mol Biol Evol. 2015;32:1862–79.View ArticlePubMedPubMed CentralGoogle Scholar
- Buscaino A, Allshire R, Pidoux A. Building centromeres: home sweet home or a nomadic existence? Curr Opin Genet Dev. 2010;20:118–26.View ArticlePubMedGoogle Scholar
- Gong Z, Wu Y, Koblízková A, Torres GA, Wang K, Iovene M, Neumann P, Zhang W, Novák P, Buell CR, et al. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell. 2012;24:3559–74.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang L, Zeng Z, Zhang W, Jiang J. Three potato centromeres are associated with distinct haplotypes with or without megabase-sized satellite repeat arrays. Genetics. 2014;196:397–401.View ArticlePubMedGoogle Scholar
- Schneider KL, Xie Z, Wolfgruber TK, Presting GG. Inbreeding drives maize centromere evolution. Proc Natl Acad Sci U S A. 2016;113:E987–996.View ArticlePubMedPubMed CentralGoogle Scholar
- Albert PS, Gao Z, Danilova TV, Birchler JA. Diversity of chromosomal karyotypes in maize and its relatives. Cytogenet Genome Res. 2010;129:6–16.View ArticlePubMedGoogle Scholar
- Piras FM, Nergadze SG, Magnani E, Bertoni L, Attolini C, Khoriauli L, Raimondi E, Giulotto E. Uncoupling of satellite DNA and centromeric function in the genus Equus. PLoS Genet. 2010;6:e1000845.View ArticlePubMedPubMed CentralGoogle Scholar
- Wolfgruber TK, Sharma A, Schneider KL, Albert PS, Koo DH, Shi J, Gao Z, Han F, Lee H, Xu R, et al. Maize centromere structure and evolution: sequence analysis of centromeres 2 and 5 reveals dynamic Loci shaped primarily by retrotransposons. PLoS Genet. 2009;5:e1000743.View ArticlePubMedPubMed CentralGoogle Scholar
- Scott KC, Sullivan BA. Neocentromeres: a place for everything and everything in its place. Trends Genet. 2014;30:66–74.View ArticlePubMedGoogle Scholar
- Zhang H, Dawe RK. Total centromere size and genome size are strongly correlated in ten grass species. Chromosome Res. 2012;20:403–12.View ArticlePubMedPubMed CentralGoogle Scholar
- Bodor DL, Mata JF, Sergeev M, David AF, Salimian KJ, Panchenko T, Cleveland DW, Black BE, Shah JV, Jansen LE. The quantitative architecture of centromeric chromatin. Elife. 2014;3:e02137.View ArticlePubMedPubMed CentralGoogle Scholar
- Ross JE, Woodlief KS, Sullivan BA. Inheritance of the CENP-A chromatin domain is spatially and temporally constrained at human centromeres. Epigenetics Chromatin. 2016;9:20.View ArticlePubMedPubMed CentralGoogle Scholar
- Heun P, Erhardt S, Blower MD, Weiss S, Skora AD, Karpen GH. Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell. 2006;10:303–15.View ArticlePubMedPubMed CentralGoogle Scholar
- Liu Y, Su H, Pang J, Gao Z, Wang XJ, Birchler JA, Han F. Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize. Proc Natl Acad Sci U S A. 2015;112:E1263–71.View ArticlePubMedPubMed CentralGoogle Scholar
- Fu S, Lv Z, Gao Z, Wu H, Pang J, Zhang B, Dong Q, Guo X, Wang XJ, Birchler JA, Han F. De novo centromere formation on a chromosome fragment in maize. Proc Natl Acad Sci U S A. 2013;110:6033–6.View ArticlePubMedPubMed CentralGoogle Scholar
- Alonso A, Hasson D, Cheung F, Warburton PE. A paucity of heterochromatin at functional human neocentromeres. Epigenetics Chromatin. 2010;3:6.View ArticlePubMedPubMed CentralGoogle Scholar
- Ingouff M, Rademacher S, Holec S, Soljić L, Xin N, Readshaw A, Foo SH, Lahouze B, Sprunck S, Berger F. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol. 2010;20:2137–43.View ArticlePubMedGoogle Scholar
- Mérai Z, Chumak N, García-Aguilar M, Hsieh TF, Nishimura T, Schoft VK, Bindics J, Slusarz L, Arnoux S, Opravil S, et al. The AAA-ATPase molecular chaperone Cdc48/p97 disassembles sumoylated centromeres, decondenses heterochromatin, and activates ribosomal RNA genes. Proc Natl Acad Sci U S A. 2014;111:16166–71.View ArticlePubMedPubMed CentralGoogle Scholar
- Ohkuni K, Takahashi Y, Fulp A, Lawrimore J, Au WC, Pasupala N, Levy-Myers R, Warren J, Strunnikov A, Baker RE, et al. SUMO-Targeted Ubiquitin Ligase (STUbL) Slx5 regulates proteolysis of centromeric histone H3 variant Cse4 and prevents its mislocalization to euchromatin. Mol Biol Cell. 2016;27(9):1500–10.View ArticlePubMed CentralGoogle Scholar
- Deyter GM, Biggins S. The FACT complex interacts with the E3 ubiquitin ligase Psh1 to prevent ectopic localization of CENP-A. Genes Dev. 2014;28:1815–26.View ArticlePubMedPubMed CentralGoogle Scholar
- Purgato S, Belloni E, Piras FM, Zoli M, Badiale C, Cerutti F, Mazzagatti A, Perini G, Della Valle G, Nergadze SG, et al. Centromere sliding on a mammalian chromosome. Chromosoma. 2015;124:277–87.View ArticlePubMedGoogle Scholar
- Hori T, Kagawa N, Toyoda A, Fujiyama A, Misu S, Monma N, Makino F, Ikeo K, Fukagawa T. Constitutive centromere-associated network controls centromere drift in vertebrate cells. J Cell Biol. 2017;216(1):101–13.View ArticlePubMedGoogle Scholar
- Gent JI, Wang K, Jiang J, Dawe RK. Stable patterns of CENH3 occupancy through maize lineages containing genetically similar centromeres. Genetics. 2015;200:1105–16.View ArticlePubMedPubMed CentralGoogle Scholar
- Tito CM, Poggio L, Naranjo CA. Cytogenetic studies in the genus Zea: 3. DNA content and heterochromatin in species and hybrids. Theor Appl Genet. 1991;83:58–64.View ArticlePubMedGoogle Scholar
- Bilinski P, Distor K, Gutierrez-Lopez J, Mendoza GM, Shi J, Dawe RK, Ross-Ibarra J. Diversity and evolution of centromere repeats in the maize genome. Chromosoma. 2015;124:57–65.View ArticlePubMedGoogle Scholar
- Hufford MB, Bilinski P, Pyhajarvi T, Ross-Ibarra J. Teosinte as a model system for population and ecological genomics. Trends Genet. 2012;28:606–15.View ArticlePubMedGoogle Scholar
- Iltis HH, Doebley JF. Taxonomy of Zea (Gramineae). II. Subspecific categories in the Zea mays complex and a generic synopsis. Am J Bot. 1980;67:12.View ArticleGoogle Scholar
- Hufford MB, Lubinksy P, Pyhajarvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J. The genomic signature of crop-wild introgression in maize. PLoS Genet. 2013;9:e1003477.View ArticlePubMedPubMed CentralGoogle Scholar
- Henikoff JG, Thakur J, Kasinathan S, Henikoff S. A unique chromatin complex occupies young α-satellite arrays of human centromeres. Sci Adv. 2015;1(1).Google Scholar
- Novák P, Neumann P, Pech J, Steinhaisl J, Macas J. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013;29:792–3.View ArticlePubMedGoogle Scholar
- Dawe RK, Hiatt EN. Plant neocentromeres: fast, focused, and driven. Chromosome Res. 2004;12:655–69.View ArticlePubMedGoogle Scholar
- Lermontova I, Schubert V, Fuchs J, Klatte S, Macas J, Schubert I. Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell. 2006;18:2443–51.View ArticlePubMedPubMed CentralGoogle Scholar
- Lermontova I, Kuhlmann M, Friedel S, Rutten T, Heckmann S, Sandmann M, Demidov D, Schubert V, Schubert I. Arabidopsis kinetochore null2 is an upstream component for centromeric histone H3 variant cenH3 deposition at centromeres. Plant Cell. 2013;25:3389–404.View ArticlePubMedPubMed CentralGoogle Scholar
- Otto SP, Walbot V. DNA methylation in eukaryotes: kinetics of demethylation and de novo methylation during the life cycle. Genetics. 1990;124:429–37.PubMedPubMed CentralGoogle Scholar
- Gao Z, Fu S, Dong Q, Han F, Birchler JA. Inactivation of a centromere during the formation of a translocation in maize. Chromosome Res. 2011;19:755–61.View ArticlePubMedGoogle Scholar
- Gent JI, Schneider KL, Topp CN, Rodriguez C, Presting GG, Dawe RK. Distinct influences of tandem repeats and retrotransposons on CENH3 nucleosome positioning. Epigenetics Chromatin. 2011;4:3.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhang T, Talbert PB, Zhang W, Wu Y, Yang Z, Henikoff JG, Henikoff S, Jiang J. The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proc Natl Acad Sci U S A. 2013;110:E4875–83.View ArticlePubMedPubMed CentralGoogle Scholar
- Aldrup-MacDonald ME, Kuo ME, Sullivan LL, Chew K, Sullivan BA. Genomic variation within alpha satellite DNA influences centromere location on human chromosomes with metastable epialleles. Genome Res. 2016;26(10):1301–11.View ArticlePubMedPubMed CentralGoogle Scholar
- Bassett EA, Wood S, Salimian KJ, Ajith S, Foltz DR, Black BE. Epigenetic centromere specification directs aurora B accumulation but is insufficient to efficiently correct mitotic errors. J Cell Biol. 2010;190:177–85.View ArticlePubMedPubMed CentralGoogle Scholar
- Fachinetti D, Diego Folco H, Nechemia-Arbely Y, Valente LP, Nguyen K, Wong AJ, Zhu Q, Holland AJ, Desai A, Jansen LE, Cleveland DW. A two-step mechanism for epigenetic specification of centromere identity and function. Nat Cell Biol. 2013;15:1056–66.View ArticlePubMedPubMed CentralGoogle Scholar
- Henikoff S, Ramachandran S, Krassovsky K, Bryson TD, Codomo CA, Brogaard K, Widom J, Wang JP, Henikoff JG. The budding yeast Centromere DNA Element II wraps a stable Cse4 hemisome in either orientation in vivo. Elife. 2014;3:e01861.View ArticlePubMedPubMed CentralGoogle Scholar
- Peacock WJ, Dennis ES, Rhoades MM, Pryor AJ. Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc Natl Acad Sci U S A. 1981;78:4490–4.View ArticlePubMedPubMed CentralGoogle Scholar
- Wolfgruber TK, Nakashima MM, Schneider KL, Sharma A, Xie Z, Albert PS, Xu R, Bilinski P, Dawe RK, Ross-Ibarra J, et al. High quality maize centromere 10 sequence reveals evidence of frequent recombination events. Front Plant Sci. 2016;7:308.View ArticlePubMedPubMed CentralGoogle Scholar
- Osman F, Whitby MC. Emerging roles for centromere-associated proteins in DNA repair and genetic recombination. Biochem Soc Trans. 2013;41:1726–30.View ArticlePubMedGoogle Scholar
- Aze A, Sannino V, Soffientini P, Bachi A, Costanzo V. Centromeric DNA replication reconstitution reveals DNA loops and ATR checkpoint suppression. Nat Cell Biol. 2016;18:684–91.View ArticlePubMedPubMed CentralGoogle Scholar
- Trifonov EN, Nibhani R. Review fifteen years of search for strong nucleosomes. Biopolymers. 2015;103:432–7.View ArticlePubMedGoogle Scholar
- Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J. Sequencing of a rice centromere uncovers active genes. Nat Genet. 2004;36:138–45.View ArticlePubMedGoogle Scholar
- Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 2011;17:3.Google Scholar
- Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell M, Stein JC, Wei X, Chin C-S, et al. Improved maize reference genome with single molecule technologies. Nature. 2017. doi:10.1038/nature22971. [Epub ahead of print].
- Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60.View ArticlePubMedPubMed CentralGoogle Scholar
- Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14:178–92.View ArticlePubMedGoogle Scholar
- Marçais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011;27:764–70.View ArticlePubMedPubMed CentralGoogle Scholar