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What is a holocentric chromosome?

What is a holocentric chromosome?


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I was doing this question that asked: "How many centromeres does a typical chromosome have?"

I thought one and the answer was:"One, except for holocentric chromosomes."

So then what are "holocentric chromosomes"?

I assume they would be chromosomes with more than one centromere, but then why do they need more than one centromere? And where can I get some more information on them? I tried googling but did not find much info on this.


In most eukaryotes, the kinetochore protein complex assembles at a single locus termed the centromere to attach chromosomes to spindle microtubules. Holocentric chromosomes have the unusual property of attaching to spindle microtubules along their entire length.

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Holocentric chromosomes

Holocentric chromosomes possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes. Ώ] they have been described for the first time in cytogenetic experiments dating from 1935 and, since this first observation, the term holocentric chromosome has referred to chromosomes that: i. lack the primary constriction corresponding to centromere observed in monocentric chromosomes ΐ] ii. possess multiple kinetochores dispersed along the chromosomal axis so that microtubules bind to chromosomes along their entire length and move broadside to the pole from the metaphase plate Α] These chromosomes are also termed holokinetic, because, during cell division, chromatids move apart in parallel and do not form the classical V-shaped figures typical of monocentric chromosomes. Β] Γ] Δ] holocentric chromosomes evolved several times during both animal and plant evolution and are currently reported in about eight hundred diverse species, including plants, insects, arachnids and nematodes Ε] Ζ] As a consequence of their diffuse kinetochores, holocentric chromosomes may stabilize chromosomal fragments favouring karyotype rearrangements. Η] ⎖] However, holocentric chromosome may also present limitations to crossing over causing a restriction of the number of chiasma in bivalents. ⎗] and may cause a restructuring of meiotic divisions resulting in an inverted meiosis ⎘]


WHAT ARE HOLOCENTRIC CHROMOSOMES GOOD FOR?

Chromosomes in eukaryotes are nucleoprotein packages whereby DNA is faithfully transmitted across cell and organismal generations. In each cell division, spindle microtubules grab chromosomes by their ‘handles’ and pull them to daughter cells. In eukaryotes with monocentric chromosomes, this handle – the kinetochore – is formed in a centromeric region. Some eukaryotic lineages, however, have independently evolved holocentric chromosomes that form the kinetochore along their entire length ( Figs 1 and 2 Mola and Papeschi, 2006 Melters et al., 2012 Bureš et al., 2013). Although the repeated origin of holocentric chromosomes by convergent evolution implies that holocentrism is adaptive, the conditions under which holocentrism may have provided a selective advantage are unclear.

Fragmentation of holocentric and monocentric chromosomes and gamma radiation response in monocentrics and holocentrics. Top: holocentric chromosomes and monocentric chromosomes are the two alternative chromosomal structures that have evolved in eukaryotes. The reason why holocentric chromosomes tolerate fragmentations is that they attach spindle microtubules along their entire length during cell divisions, and therefore all their fragments are normally inherited by daughter cells that receive a proper set of genetic material. Monocentric chromosomes, by contrast, attach spindle microtubules to the kinetochore (shown in red), which is formed in a small centromeric region, and their fragments without a centromere are distributed randomly to daughter cells and eventually lost, which is often lethal. Bottom: gamma irradiation causes chromosomal fragmentations that need to be repaired, and for that purpose, the cell cycle is arrested in G2 phase in plants. Therefore, the number of G2 cells in gamma-irradiated plants should increase, resulting in a higher G2/G1 ratio. If the G2/G1 ratio of an irradiated plant is divided by the G2/G1 ratio of a non-irradiated control, the resulting value shows the overall response in cell cycle arrest to gamma irradiation (y-axis). These values for 13 monocentric and ten holocentric species are shown in the two box-plots. Relative to monocentrics, there is basically no increase in the G2/G1 ratio in holocentrics after irradiation, suggesting that holocentrics cope with chromosomal fragmentation more effectively. Monocentric species are represented by Asplenium bulbiferum, Begonia bowerae, Cymbalaria muralis, Euonymus japonicus, Kalanchoë delagoensis, Lavandula angustifolia, Lysimachia nemorum, Peperomia glabella, Pisum sativum, Plectranthus amboinicus, Sedum spurium, Senecio articulatus and Silene nocturna. Holocentric species are represented by Carex grayi, C. humilis, C. pilulifera, Drosera capensis, D. scorpioides, Eleocharis palustris, Isolepis prolifera, Luzula sylvatica, Prionium serratum and Scirpus cernuus. See Zedek et al. (2016) for further details.

Fragmentation of holocentric and monocentric chromosomes and gamma radiation response in monocentrics and holocentrics. Top: holocentric chromosomes and monocentric chromosomes are the two alternative chromosomal structures that have evolved in eukaryotes. The reason why holocentric chromosomes tolerate fragmentations is that they attach spindle microtubules along their entire length during cell divisions, and therefore all their fragments are normally inherited by daughter cells that receive a proper set of genetic material. Monocentric chromosomes, by contrast, attach spindle microtubules to the kinetochore (shown in red), which is formed in a small centromeric region, and their fragments without a centromere are distributed randomly to daughter cells and eventually lost, which is often lethal. Bottom: gamma irradiation causes chromosomal fragmentations that need to be repaired, and for that purpose, the cell cycle is arrested in G2 phase in plants. Therefore, the number of G2 cells in gamma-irradiated plants should increase, resulting in a higher G2/G1 ratio. If the G2/G1 ratio of an irradiated plant is divided by the G2/G1 ratio of a non-irradiated control, the resulting value shows the overall response in cell cycle arrest to gamma irradiation (y-axis). These values for 13 monocentric and ten holocentric species are shown in the two box-plots. Relative to monocentrics, there is basically no increase in the G2/G1 ratio in holocentrics after irradiation, suggesting that holocentrics cope with chromosomal fragmentation more effectively. Monocentric species are represented by Asplenium bulbiferum, Begonia bowerae, Cymbalaria muralis, Euonymus japonicus, Kalanchoë delagoensis, Lavandula angustifolia, Lysimachia nemorum, Peperomia glabella, Pisum sativum, Plectranthus amboinicus, Sedum spurium, Senecio articulatus and Silene nocturna. Holocentric species are represented by Carex grayi, C. humilis, C. pilulifera, Drosera capensis, D. scorpioides, Eleocharis palustris, Isolepis prolifera, Luzula sylvatica, Prionium serratum and Scirpus cernuus. See Zedek et al. (2016) for further details.

Phylogenetic distribution of holocentric chromosomes and terrestrialization events. The distribution of holocentric lineages (yellow) and terrestrialization events (red sparks) in eukaryotes is shown on simplified dated phylogenies of Viridiplantae and Ecdysozoa. The remaining lineages, depicted in green in Viridiplantae and brown in Ecdysozoa, are either monocentric or with unknown chromosomal structure, and the ancestral states of these clades can be either monocentric or holocentric (see main text for further discussion). The tree for Ecdysozoa and terrestrialization events was modified from Rota-Stabelli et al. (2013). The tree topology and node ages for Viridiplantae are based on Wickett et al. (2014) and Kumar et al. (2017). Dashed branches in the Viridiplantae tree indicate uncertainty in node ages (not in topology). The cyperid clade in Viridiplantae includes families Cyperaceae, Juncaceae and Thurniaceae.

Phylogenetic distribution of holocentric chromosomes and terrestrialization events. The distribution of holocentric lineages (yellow) and terrestrialization events (red sparks) in eukaryotes is shown on simplified dated phylogenies of Viridiplantae and Ecdysozoa. The remaining lineages, depicted in green in Viridiplantae and brown in Ecdysozoa, are either monocentric or with unknown chromosomal structure, and the ancestral states of these clades can be either monocentric or holocentric (see main text for further discussion). The tree for Ecdysozoa and terrestrialization events was modified from Rota-Stabelli et al. (2013). The tree topology and node ages for Viridiplantae are based on Wickett et al. (2014) and Kumar et al. (2017). Dashed branches in the Viridiplantae tree indicate uncertainty in node ages (not in topology). The cyperid clade in Viridiplantae includes families Cyperaceae, Juncaceae and Thurniaceae.

The extended kinetochore of holocentric chromosomes may suppress the meiotic drive of centromeric repeats and its negative consequences ( Talbert et al., 2008 Malik and Henikoff, 2009 Zedek and Bureš, 2016). However, the hypothesis of centromere drive suppression only explains the evolution of chromosomal holocentrism in meiosis, not in mitosis ( Zedek and Bureš, 2016). Moreover, lineages exist that are holocentric only in mitosis but not in meiosis (reviewed by Marques and Pedrosa-Harand, 2016). Conceivably, the origin of mitotic holocentrism could sometimes entail meiotic holocentrism – perhaps due to a shared machinery between these two types of cell division – which could then be adopted for centromere drive suppression, or mitotic and meiotic holocentrism may be two unrelated adaptations ( Zedek and Bureš, 2016). In any case, the repeated evolution of mitotic/somatic holocentrism ( Mola and Papeschi, 2006 Melters et al., 2012 Bureš et al., 2013), a feature that all currently known holocentric organisms have in common ( Marques and Pedrosa-Harand, 2016), requires an explanation of its own.

Mitosis is central to development, and any disruptions of this process may reduce an individual’s fitness and chances of surviving to a reproductive age. The key to the adaptive value of mitotic holocentrism may therefore lie in the tolerance of holocentric chromosomes to fragmentation due to their extended kinetochore ( Mandrioli and Manicardi, 2012 Bureš et al., 2013). During cell divisions, all the fragments of holocentric chromosomes retain their kinetic activity and are normally transmitted to daughter cells, each of which receives half of the genetic material ( Fig. 1 Nordenskiöld, 1963 Murakami and Imai, 1974 Sheikh et al., 1995 Carpenter et al., 2005 Jankowska et al., 2015). In fact, the regular inheritance of chromosomal fragments is considered strong evidence of holocentrism (reviewed by Mola and Papeschi, 2006 Melters et al., 2012 Bureš et al., 2013). In contrast, the fragmentation of monocentric chromosomes generates acentric fragments that are randomly distributed to daughter cells and eventually lost in subsequent cell generations ( Fig. 1). Moreover, if centric fragments of monocentric chromosomes fuse, they form aberrant dicentric chromosomes ( Stear and Roth, 2002 Carpenter et al., 2005 Lowden et al., 2011). Holocentric chromosomes should therefore provide a selective advantage by directly protecting DNA in times of exposure to agents causing chromosomal fragmentation, i.e. clastogens. Such clastogens may include cosmic radiation (UV, gamma rays, X-rays Kovalchuk et al., 2000 Waterworth et al., 2011), natural radiation from radioactive elements ( Takahashi, 1976), desiccation/freezing ( Waterworth et al., 2011) or a broad range of chemicals ( Ishidate et al., 1988). However, although holocentric chromosomes tolerate fragmentation, the question as to whether this tolerance also provides a selective advantage over monocentric organisms is an entirely different matter. We are not aware of any systematic research that has investigated the competitiveness of monocentrics and holocentrics or their comparison in clastogenic conditions and considered the potential consequences of holocentric tolerance to fragmentation for the evolution of eukaryotes and holocentrism itself.

Below is a summary of the available evidence that holocentric chromosomes may, indeed, confer a selective advantage in clastogenic environments and conditions. The causes of clastogenic exposure are discussed and it is shown that such conditions, of various duration and intensity, have occurred many times throughout the history of Earth’s biota. The role of holocentric chromosomes in eukaryotic evolution is also considered, with a particular emphasis on plant and animal terrestrialization half a billion years ago. The paper then moves on to the negative consequences of holocentrism and discusses potential biases in our knowledge of its distribution across eukaryotes. The paper concludes with proposals for future research that is needed to test the anticlastogenic hypothesis of holocentrism and its evolutionary consequences.


Evolution of Meiosis

Based on centromere organization, chromosomes are essentially classified into two main types, monocentric chromosomes with a single centromere domain per chromosome and holocentric chromosomes with multiple centromere domains distributed genome-wide. It is known that monocentric organisms show restricted or even non-meiotic recombination at and near centromeres (cold regions). Therefore, it is of particular interest to understand how meiotic recombination works in plants with holocentric chromosomes. Holocentric plants also show several adaptations during meiosis, e. g. chiasmatic and achiasmatic inverted meiosis, where homologs segregation is postponed to second meiosis. As holocentric plants developed several adaptations to bypass meiosis, they do not only offer an exciting model to understand how these adaptations take place during evolution but are also of interest for comparative biology. In our team, we aim to decipher the molecular mechanisms associated with meiotic adaptations observed in holocentric plants.


Our research will mainly focus on the model species (but not only) R. pubera (2n=10) and R. tenuis (2n=4). Taking advantage of cutting-edge technologies, we will develop several analyses aiming at the characterization of meiotic recombination rates and the role of meiotic proteins as well as the potential identification of new proteins involved in the evolution of meiotic adaptations observed in these organisms. Using holocentric plants as a model to understand how meiotic recombination is regulated at centromeric regions will potentially unveil new strategies to address meiotic recombination issues on monocentric organisms.

From left to right: Rhynchospora pubera, 1- Mitotic chromosomes showing line-like holocentromeres, 2- meiotic anaphase I showing segregation of sister chromatids with restructured cluster-centromeres, 3- zoomed view of 2, 4- meiotic metaphase II showing the postponed segregation of homologous chromatids. Chromatids (grey), CENH3 (red), tubulin (green).

From left to right: Rhynchospora pubera, 1- Mitotic chromosomes showing line-like holocentromeres, 2- meiotic anaphase I showing segregation of sister chromatids with restructured cluster-centromeres, 3- zoomed view of 2, 4- meiotic metaphase II showing the postponed segregation of homologous chromatids. Chromatids (grey), CENH3 (red), tubulin (green).


Results

Phylogeny and environmental predictors

The topology of the consensus tree (Fig. 1 Notes S2 for parenthetical format matrix in Notes S3) is congruent with the phylogeny published in Waterway et al. (2009) the few minor topological differences can be explained by methodological differences in phylogeny reconstruction between our study and Waterway et al.’s. The tree is scaled to 1.0 total length (from the root to the tip of any single leaf in the ultrametric tree) to facilitate interpretation of parameter estimates. The response and predictor variables are summarized in Table S1. The total variance in climatic variables explained by among-species differences ranges from 30% (BIO12 and BIO15) to 60% (BIO1), and accordingly, 40–70% by within-species differences. Among the five climatic predictors, one pair exhibits correlations of |r | > 0.70 (BIO4:BIO7, R 2 = 0.94). Among the four morphological predictors, no pair exhibits correlations of |r | > 0.70 (maximum R 2 = 0.18, utricle length:lateral-inflorescence unit length). Correlations are also low between morphological and climatic predictor pairs (maximum R 2 = 0.18, BIO1:leaf width). Climatic and morphological variables exhibit a strong phylogenetic signal only in one case was t1/2 < 0.5 (0.30 for BIO15). A t1/2 = 0.5 in units of tree height means that a species entering a new niche would need a time span equal to half the tree length before it has lost half the influence of its ancestral state. Regarding habitat characterization (see Fig. 1 for ancestral character estimation of soil moisture), Waterway et al. (2009) suggested clustered distribution on the tree for these categorical variables, which may reflect niche conservatism. A priori, diploid chromosome number may track all the examined predictors (bioclimatic, morphological and categorical habitat), as all of them display strong phylogenetic signals. In addition, our analyses do not strongly violate the assumption of SLOUCH that predictor variables follow Brownian motion (all include t1/2 = ∞ in their support set).

Ultrametric phylogenetic tree from the consensus of 9000 trees from beast analysis of 139 accessions of Cyperaceae. Forty-three accessions were pruned after analysis. Ancestral character estimation (based on Fitch parsimony) of categorical variables of soil moisture are shown on the branch tree. Blue, water-saturated soils green, intermediate red, dry uplands. Diploid chromosome number range is indicated.

Phylogenetic effects in chromosome number for the ‘single equilibrium O–U model’

In a no-predictor (single equilibrium) O–U model, an estimate of t1/2 = 0 (α = ∞, instantaneous adaptation) implies that there is no influence of the past on trait value (no phylogenetic effect), and all species represent independent draws from the trait distribution. By contrast, if t1/2 = ∞ (α = 0, no adaptation or Brownian-motion model), phylogeny is a strong predictor of trait value. In our case, the point estimate of t1/2 for the no-predictor O–U model suggests a strong phylogenetic effect (t1/2 = 0.60 in units of tree length Fig. 2a), with supported values (values with a log-likelihood until two units lower than the maximum log-likelihood Edwards, 1992 ) ranging from a moderate to very strong phylogenetic effect and the hypothesis of species independence strongly rejected (support interval over t1/2 = 0.26–∞ Fig. 2a).

The support (log-likelihood) difference from the best model is shown on the ordinate relative to the different parameter combinations. (a) Phylogenetic effects on chromosome number in Cyperaceae based on a model including only an intercept (2n

1 best estimate: t1/2 = 0.60 (0.26–∞) in units of tree height vy = 216.5 chromosome number squared). (b) Phylogenetic effects and inertia in chromosome number based on a model including temperature seasonality as predictor (best estimate: 0.52 (0.22–7.5) vy = 176). (c) Phylogenetic inertia in chromosome number based on a model with lateral inflorescence unit length as predictor (best estimate: t1/2 = 0.50 (0.22–6.75) vy = 171.5). (d) Phylogenetic inertia in chromosome number based on a model including lateral inflorescence unit length, soil moisture and temperature seasonality (best estimate: t1/2 = 0.38 (0.14–1.85) vy = 140).

Adaptation and inertia in chromosome number

None of the predictor variables explained a lot of the variation in chromosome number, but we still found clear evidence for weak effects from several variables. As we will argue in the Discussion, we judge these effects to be biologically important. Mean chromosome number is more strongly predicted by inflorescence unit length than by any other predictor (R 2 = 0.063, AICw = 0.945 relative to a no-predictor O–U model) (Table 1). We interpret inflorescence unit length as a proxy for total resource investment in each inflorescence unit. Chromosome number is negatively correlated with temperature seasonality (BIO4) but with marginal support (R 2 = 0.038, AICw = 0.778 Table 1 Figs 2b, 3a). The correlations between chromosome number and the remaining continuous predictors are weak (R 2 = 0.000–0.038 Table 1). For categorical habitat predictors, the correlation is overall weak (R 2 = 0.035–0.054 Table 1). The best-supported model with only categorical habitat predictors is a model with soil moisture as the sole predictor (R 2 = 0.054, AICw = 0.660 Table 1 Fig. 3c), in which chromosome number is positively correlated with soil moisture (dry soil = 51.5 ± 4.7 chromosomes, intermediate = 63.5 ± 6.2 chromosomes, and water-saturated soil = 73.7 ± 7.8 chromosomes). The slouch confidence intervals for the regression parameters and primary optima are conditional on the alpha and sigma parameters of the Ornstein–Uhlenbeck process and they are local confidence intervals. For BIO4, lateral spike unit length and soil moisture predictor, we have taken some alternative values of alpha and sigma (at the edges of the support intervals, and a few internal points) to estimate global confidence intervals. Our conclusions are also supported by the global confidence intervals for the regression parameters and primary optima (results not shown).

1) are shown. In all models the response variable is 2n, where 2n is diploid chromosome number. Predictor variables are given to the left of the tilde, and a ‘1’ means that the model has only an intercept.


Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae)

Changes in chromosome number as a result of fission and fusion in holocentrics have direct and immediate effects on the recombination rate. We investigate the support for the classic hypothesis that environmental stability selects for increased recombination rates.

We employed a phylogenetic and cytogenetic data set from one of the most diverse angiosperm genera in the world, which has the largest nonpolyploid chromosome radiation (Carex, Cyperaceae 2n = 12–124 2100 spp.). We evaluated alternative Ornstein–Uhlenbeck models of chromosome number adaptation to the environment in an information-theoretic framework.

We found moderate support for a positive influence of lateral inflorescence unit size on chromosome number, which may be selected in a stable environment in which resources for reproductive investment are larger. We found weak support for a positive influence on chromosome number of water-saturated soils and among-month temperature constancy, which would be expected to be negatively select for pioneering species. Chromosome number showed a strong phylogenetic signal.

We argue that our finding of small but significant effects of life history and ecology is compatible with our original hypothesis regarding selection of optima in recombination rates: low recombination rate is optimal when inmediate fitness is required. By contrast, high recombination rate is optimal when stable environments allow for evolutionary innovation.

Table S1 List of species including cytogenetic sampling, mean diploid chromosome number, categorical predictor variables, climate predictor variables and morphological predictor variables

Notes S1 Accession data for voucher specimens for DNA sequences used in this study.

Notes S2 Ultrametric phylogenetic tree in parenthetical format from the consensus (using maximum clade credibility tree and mean heights in TreeAnnotator v.1.61) of 9000 trees from BEAST analysis of 139 accessions of Cyperaceae.

Notes S3 Phylogenetic matrix in nexus format with 139 taxa and 2588 characters.

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In: Chromosome Research , Vol. 20, No. 5, 07.2012, p. 579-593.

Research output : Contribution to journal › Article › peer-review

T1 - Holocentric chromosomes

T2 - Convergent evolution, meiotic adaptations, and genomic analysis

N2 - In most eukaryotes, the kinetochore protein complex assembles at a single locus termed the centromere to attach chromosomes to spindle microtubules. Holocentric chromosomes have the unusual property of attaching to spindle microtubules along their entire length. Our mechanistic understanding of holocentric chromosome function is derived largely from studies in the nematode Caenorhabditis elegans, but holocentric chromosomes are found over a broad range of animal and plant species. In this review, we describe how holocentricity may be identified through cytological and molecular methods. By surveying the diversity of organisms with holocentric chromosomes, we estimate that the trait has arisen at least 13 independent times (four times in plants and at least nine times in animals). Holocentric chromosomes have inherent problems in meiosis because bivalents can attach to spindles in a random fashion. Interestingly, there are several solutions that have evolved to allow accuratemeiotic segregation of holocentric chromosomes. Lastly, we describe how extensive genome sequencing and experiments in nonmodel organisms may allow holocentric chromosomes to shed light on general principles of chromosome segregation.

AB - In most eukaryotes, the kinetochore protein complex assembles at a single locus termed the centromere to attach chromosomes to spindle microtubules. Holocentric chromosomes have the unusual property of attaching to spindle microtubules along their entire length. Our mechanistic understanding of holocentric chromosome function is derived largely from studies in the nematode Caenorhabditis elegans, but holocentric chromosomes are found over a broad range of animal and plant species. In this review, we describe how holocentricity may be identified through cytological and molecular methods. By surveying the diversity of organisms with holocentric chromosomes, we estimate that the trait has arisen at least 13 independent times (four times in plants and at least nine times in animals). Holocentric chromosomes have inherent problems in meiosis because bivalents can attach to spindles in a random fashion. Interestingly, there are several solutions that have evolved to allow accuratemeiotic segregation of holocentric chromosomes. Lastly, we describe how extensive genome sequencing and experiments in nonmodel organisms may allow holocentric chromosomes to shed light on general principles of chromosome segregation.


The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization

In higher plants, the large-scale structure of monocentric chromosomes consists of distinguishable eu- and heterochromatic regions, the proportions and organization of which depend on a species' genome size. To determine whether the same interplay is maintained for holocentric chromosomes, we investigated the distribution of repetitive sequences and epigenetic marks in the woodrush Luzula elegans (3.81 Gbp/1C). Sixty-one per cent of the L. elegans genome is characterized by highly repetitive DNA, with over 30 distinct sequence families encoding an exceptionally high diversity of satellite repeats. Over 33% of the genome is composed of the Angela clade of Ty1/copia LTR retrotransposons, which are uniformly dispersed along the chromosomes, while the satellite repeats occur as bands whose distribution appears to be biased towards the chromosome termini. No satellite showed an almost chromosome-wide distribution pattern as expected for a holocentric chromosome and no typical centromere-associated LTR retrotransposons were found either. No distinguishable large-scale patterns of eu- and heterochromatin-typical epigenetic marks or early/late DNA replicating domains were found along mitotic chromosomes, although super-high-resolution light microscopy revealed distinguishable interspersed units of various chromatin types. Our data suggest a correlation between the centromere and overall genome organization in species with holocentric chromosomes.

Filename Description
tpj12054-sup-0001-DataS1.xlsMS Excel, 40 KB Data S1. Assembled contigs representative of individual clusters of satellite DNA.
tpj12054-sup-0002-FigS1.tifimage/tif, 68.4 MB Figure S1. Dot-plot similarity comparison of assembled contigs representing the most abundant satellite repeats.
tpj12054-sup-0003-FigS2.tifimage/tif, 2.8 MB Figure S2. Southern analysis reveals a ladder-like pattern typical for satellite DNA.
tpj12054-sup-0004-FigS3.tifimage/tif, 5.8 MB Figure S3. Immunolabeling of L. elegans mitotic metaphase chromosomes.
tpj12054-sup-0005-FigS4.tifimage/tif, 5.7 MB Figure S4. Distribution of DNA methylation (5mC immunolabeling) in L. elegans interphase nuclei.
tpj12054-sup-0006-FigS5.tifimage/tif, 15.3 MB Figure S5. DNA replication behavior of L. elegans.
tpj12054-sup-0007-TableS1.docWord document, 54.5 KB Table S1. Sequences of oligonucleotides used in the present study.
tpj12054-sup-0008-TableS2.docWord document, 24 KB Table S2. Sequenced clones from a partial genomic library screened by dot-blot hybridization.
tpj12054-sup-0009-Supportinginformationlegends.docWord document, 21.5 KB

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