Analysis of the epigenetic status of telomeres
by using ChIP-seq data
Marı ´a I. Vaquero-Sedas1, Chongyuan Luo2and Miguel A. Vega-Palas1,*
1Instituto de Bioquı ´mica Vegetal y Fotosı ´ntesis, CSIC-Universidad de Sevilla, IBVF (CSIC-USE), c/ Ame ´rico
Vespucio n?49, 41092 Seville, Spain and2Department of Plant Biology and Pathology, Rutgers University,
New Brunswick, NJ, USA
Received June 8, 2012; Accepted July 6, 2012
The chromatin structure of eukaryotic telomeres
plays an essential role in telomere functions.
However, their study might be impaired by the
presence of interstitial telomeric sequences (ITSs),
which have a widespread distribution in different
model systems. We have developed a simple
approach to study the chromatin structure of
Arabidopsis telomeres independently of ITSs by
analyzing ChIP-seq data. This approach could be
used to study the chromatin structure of telomeres
in some other eukaryotes. The analysis of ChIP-seq
experiments revealed that Arabidopsis telomeres
have higher density of histone H3 than centromeres,
which might reflects their short nucleosomal organ-
Arabidopsis telomeres have lower levels of hetero-
chromatic marks than centromeres (H3K9Me2and
marks (H3K4Me2and H3K9Ac) and similar or lower
H3K36Me2, H3K36Me3and H3K18Ac). Interestingly,
H3K27Me3, a repressive mark that associates with
many euchromatic genes. The epigenetic profile of
Arabidopsis telomeres is closely related to the pre-
viously defined chromatin state 2. This chromatin
state is found in 23% of Arabidopsis genes, many
At least, in part, this scenario is similar in rice.
Telomeres prevent chromosome fusions and degradation
by exonucleases and are implicated in DNA repair, hom-
ologous recombination, chromosome pairing and segrega-
tion. Telomeric DNA usually contains tandem repeats of a
short GC-rich motif, which can also be found at intersti-
tial chromosomal loci (1–5). These interstitial telomeric
sequences (ITSs) have a widespread distribution in differ-
ent model systems, including Arabidopsis, and have been
hot spots for recombination and diseases caused by
genomic instability, although their functions remain
Two major chromatin organizations can be found inside
the cell nucleus: heterochromatin and euchromatin.
Heterochromatic regions are highly condensed in inter-
phase nuclei giving rise to the so-called chromocenters
and usually associate with repetitive and silent DNA,
although certain level of transcription is required for
their establishment and maintenance. By contrast, euchro-
matic regions have an open conformation and are often
related to the capacity to be transcribed. Both kinds of
chromatin organizations exhibit defined epigenetic modi-
fications that influence their biochemical behavior. In
Arabidopsis, chromocenters contain pericentromeric het-
erochromatin, which associates with the 178-bp satellite
repeats (also known as 180-bp repeats) and with other
repetitive DNA sequences including mobile elements and
ITSs (9–15). Arabidopsis heterochromatin is characterized
by high levels of cytosine methylation, which can be
targeted at CpG, CpNpG or CpNpN residues (where N
is any nucleotide), and by H3K9Me1,2, H3K27Me1,2and
characterized by H3K4Me1,2,3, H3K36Me1,2,3, H4K20Me2,3
and by histones acetylation (16). In addition, many genes
that localize in Arabidopsis euchromatin are labeled with
H3K27Me3, a repressive mark that is thought to regulate
tissue-specific gene expression (17–19).
The analysis of telomeric chromatin structure from
ChIP, ChIP-on-chip or ChIP-seq experiments might be
challenged by the presence of ITSs (20). This problem
might also be extensive to other repetitive sequences.
Here, we have developed an approach to study the epigen-
etic modifications of Arabidopsis telomeres independently
of ITSs by analyzing genome-wide ChIP-seq data. The
ChIP-seq experiments revealed that Arabidopsis telomeres
*To whom correspondence should be addressed. Tel: +34 954 489574; Fax: +34 954 460065; Email: email@example.com
Published online 1 August 2012Nucleic Acids Research, 2012, Vol. 40, No. 21 e163
? The Author(s) 2012. Published by Oxford University Press.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/
by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
have higher density of histone H3 than centromeres. These
experiments also revealed that Arabidopsis telomeres have
lower levels of heterochromatic marks than centromeres
(H3K9Me2and H3K27Me), higher levels of some euchro-
matic marks (H3K4Me2and H3K9Ac) and similar or
lower levels of other euchromatic marks (H3K4Me3,
H3K36Me2, H3K36Me3and H3K18Ac). Interestingly, the
ChIP-seq data also revealed that Arabidopsis telomeres
exhibit higher levels of H3K27Me3than centromeres. At
least, in part, this scenario is similar in rice.
MATERIALS AND METHODS
Determination of the relative amounts of (CCCTAAA)4
sequences at telomeres and ITSs
To analyze the chromatin structure of Arabidopsis telo-
meres using genome-wide ChIP-seq experiments, we had
to define a specific DNA sequence that revealed telomeres
times that the sequence (CCCTAAA)4appears at internal
chromosomal loci and at telomeres in the Arabidopsis
thaliana (Col-0) genome. First, we performed Blast
analyses at the Map Viewer web site in National Center
for Biotechnology Information (NCBI) to determine the
number of times that the sequence (CCCTAAA)4appears
at internal chromosomal loci (http://www.ncbi.nlm.nih.
gov/mapview). In the case that a specific ITS contained
five perfect tandem telomeric repeats, the Blast analyses
revealed two overlapping (CCCTAAA)4sequences. If the
ITS contained six perfect tandem telomeric repeats, the
Blast analyses revealed three overlapping (CCCTAAA)4
sequences and so on. We found 118 (CCCTAAA)4se-
quences at internal positions in the five chromosomes of
Arabidopsis, including subtelomeric regions.
To estimate the number of times that the sequence (CC
CTAAA)4is found at Arabidopsis telomeres, we assumed
that Arabidopsis thaliana (Col-0) telomeres are composed
of perfect telomeric repeats that spread about 3750bp
(21,22). We estimated that the five Arabidopsis chromo-
somes should contain about 5350 overlapping (CCCTAA
A)4 sequences at telomeres [(3750/7)?10]. Therefore,
when the frequency of reads containing the sequence (C
CCTAAA)4is determined in input samples of Arabidopsis
ChIP-seq experiments, only 2% of these reads should cor-
respond to ITSs [(118?100)/(118+5350)]. In conse-
quence, the frequency of the (CCCTAAA)4 sequence
ChIP-seq experiments. In the case of rice (Oryza sativa
ssp. japonica cv. Nipponbare), the frequency of the (CC
CTAAA)4sequence should also reveal telomeres. The rice
genome contains a similar number of (CCCTAAA)4
sequences at internal chromosomal loci than Arabidopsis
(127), has more chromosomes (twelve) and similar telo-
meric length (23).
Determination of enrichment values
We used the Sequence Read Archive database at NCBI
to study different epigenetic modifications in Arabidopsis
and in rice telomeres. In Arabidopsis, we analyzed all the
experiments from study SRP002100 (Gene Expression
Omnibus accession number GSE28398). This ChIP-seq
study was performedusing
We determined the number of reads containing the (CC
CTAAA)4sequence and the number of reads containing
the sequence TTGGCTTTGTATCTTCTAACAAG,
which is a conserved region of the 178-bp satellite
repeats present at centromeres. This sequence served as
heterochromatic reference (12,15). Although a fraction
of the 178-bp sequences associates with CENH3 chroma-
tin, surrounding 178-bp repeats associate with H3 chro-
matin. The conserved sequence that we have selected
spans from positions 56 to 79 of the repeats and do not
contain motifs specifically associated with CENH3 chro-
matin (15). Thus, this sequence is present at the centro-
chromatin and also at the 178-bp repeats that associate
with H3 chromatin. It allowed us to analyze the chromatin
organization of Arabidopsis 178-bp satellite repeats as an
average, whichis known
The study mentioned earlier in the text focused on nine
epigenetic modifications named H3K4Me2, H3K4Me3,
H3K9Me2, H3K27Me, H3K27Me3, H3K36Me2, H3K36Me3,
H3K9Ac and H3K18Ac. The number of telomeric and
centromeric reads corresponding to all these epigenetic
marks were determined (Supplementary Table S1) and
normalized against the input sample. Then, enrichment
values of telomeres versus centromeres were calculated
and normalized against histone H3 occupancy. The result-
ing values are represented in Figure 1. Similar results to
those shown in Figure 1 were obtained when a different
conserved sequence from the 178-bp satellite repeats was
used to estimate relative enrichment values (data not
shown). This sequence (CATATTTGACTCCAAAACA
CTAA) contains the dinucleotide TG at positions 160–
161 of the 178-bp repeats and is not frequent in CENH3
The enrichment values for H3K4Me3and H3K9Ac were
also calculated by analyzing experiments from a different
ChIP-seq study (SRP002650; GSE22276), which was per-
formed using Arabidopsis leaves (26). The enrichment
values obtained for these two epigenetic marks were very
similar to those shown in Figure 1: 0.7 for H3K4Me3and
3.3 for H3K9Ac.
For rice (O. sativa ssp. japonica cv. Nipponbare), en-
richment values were calculated by analyzing experiments
SRX016118, SRX016122, SRX016126 and SRX016130
from study SRP001788 (GSE19602). These experiments
were performed using four-leaf stage seedlings (27). The
number of reads containing the (CCCTAAA)4sequence
and the number of reads containing the sequence CGTTC
GTGGCAAAAACTCACTTCGT, which is part of the
CentO-1 centromeric satellite repeat (positions 1–25)
(28), were determined for four epigenetic modifications
(H3K4Me3, H3K9Ac, H3K27Me3and DNA methylation;
see Supplementary Table S2). The CentO repeats, which
are known to undergo DNA methylation similarly to the
178-bp repeats from Arabidopsis, served as heterochro-
matic reference (29–31). Since study SRP001788 did not
include input samples, relative enrichment values were
calculated. The number of reads corresponding to the
to be heterochromatic
e163Nucleic Acids Research, 2012,Vol.40, No. 21PAGE 2 OF 6
telomeric sequence was divided by the number of CentO-1
reads for every epigenetic modification. Then, relative en-
richment values were calculated by normalizing against
the resulting value for DNA methylation. To obtain a
graphic representation with similar values to those
shown in Figure 1, all the relative enrichment values
were divided by 10.
Epigenetic marks at Arabidopsis telomeres
Arabidopsis telomeres, we analyzed ChIP-seq data. We
determined the relative enrichment of telomeres versus
centromeres, which served as heterochromatic reference.
Previously, we had to find a specific sequence that repre-
sents telomeres but not ITSs in ChIP-seq analyses. Since
Arabidopsis ITSs are mostly composed of very short
stretches of perfect telomeric repeats interspersed with
degenerated repeats (7,8,32,33), a short stretch of perfect
telomeric repeats might essentially represent telomeres.
Blast analyses of the Arabidopsis genome revealed that
98% of the (CCCTAAA)4sequences are found at telo-
meres, whereas only 2% of these sequences localize at
ITSs (see ‘Materials and Methods’ section). Therefore,
the (CCCTAAA)4 sequence is essentially found at
Arabidopsis telomeres. We chose this sequence to
analyze telomeres in ChIP-seq experiments. For centro-
meres, we selected a conserved sequence from the 178-bp
centromeric satellite repeats. It is well known that these
repeats are heterochromatic and localize to chromocenters
We analyzed ChIP-seq data from a study that focused
on different histone H3 modifications in Arabidopsis. The
epigenetic modifications analyzed in this study were two
characteristic heterochromatic marks (H3K9Me2
study theepigenetic modificationspresent at
H3K27Me) and six marks associated with euchromatin
(H3K4Me2, H3K4Me3, H3K36Me2, H3K36Me3, H3K9Ac
and H3K18Ac). In addition, this study also focused on
unlabeled histone H3 and on H3K27Me3, a repressive
mark found in many euchromatic genes (17–19). We
determined the enrichment of telomeres versus centro-
meres and found that the levels of unlabeled histone
H3 were 1.6 times higher at telomeres (Supplementary
Table S1). In all eukaryotic organisms analyzed, the nu-
cleosomal spacing of telomeres is ?20bp shorter than the
average bulk nucleosome organization (34). This import-
ant chromatin feature is probably related to the straight
nature of telomeric DNA and might condition the epigen-
etic behavior of telomeric nucleosomes (32,35–38). The
high density of histone H3 determined here at telomeres
might reflect the short spacing of telomeric nucleosomes,
which has been previously revealed by micrococcal
nuclease digestion experiments. Alternatively, we cannot
rule out other possibilities including a nucleosomal
spacing of the nucleosomes associated with the 178-bp
repeats longerthan the
We found that the levels of heterochromatic marks
analyzed (H3K9Me2and H3K27Me) were lower at telo-
meres than at centromeres. On the contrary, the levels of
some euchromatic marks were higher at telomeres
indicate that Arabidopsis telomeres exhibit euchromatic
features. However, not all the euchromatic marks
analyzed were enriched in telomeres versus centromeres.
That was the case for H3K4Me3, H3K36Me2, H3K36Me3
and H3K18Ac. The levels of these marks were similar or
even lower at telomeres than at centromeres. Interestingly,
Arabidopsis telomeres were also enriched in H3K27Me3
(Figure 1). Since we have previously found that telomeres
in Arabidopsis are marked with H4K16Ac (14), we
conclude that Arabidopsis telomeres are labeled with
H3K4Me2, H3K9Ac, H3K16Ac and H3K27Me3.
Epigenetic marks at rice telomeres
To study whether some of the epigenetic marks that char-
acterize Arabidopsis telomeres are present in other plant
species, we analyzed a genome-wide study performed
in ricewhere the levels
H3K27Me3and DNA methylation were analyzed (27).
Since the (CCCTAAA)4sequences present at rice ITSs
represent ?1% of the total, these sequences also reveal
telomeres in rice ChIP-seq experiments (see ‘Materials
and Methods’ section). As heterochromatic reference, we
analyzed a sequence from CenO, which is a satellite repeat
present in rice centromeres. We found that the relative
enrichment levels of telomeres versus centromeres were
more than one order of magnitude higher for H3K4Me2,
H3K9Ac and H3K27Me3than for DNA methylation
(Figure 2). These results strongly suggest that rice telo-
meres are also labeled with H3K4Me2, H3K9Ac and
H3K27Me3. However, these results are still compatible
with the existence of low levels of DNA methylation at
rice telomeres, which can also be present at Arabidopsis
nt of telomeres ve
Figure 1. Epigenetic features at Arabidopsis telomeres.
histone H3 epigenetic modifications were analyzed at telomeres and
at centromeres using study SRP002100 (Gene Expression Omnibus ac-
cession number GSE28398). Relative enrichment values of telomeres
versus centromeres were determined and represented as indicated in
the ‘Materials and Methods’ section.
PAGE 3 OF 6Nucleic Acids Research, 2012,Vol.40, No. 21e163
ChIP-seq data confirm that Arabidopsis telomeres exhibit
We have previously analyzed the chromatin structures of
Arabidopsis telomeres and ITSs by ChIP, digestion with
the restriction endonuclease Tru9I, which digested ITSs,
and hybridization with a telomeric probe. These experi-
ments revealed that, although subtelomeric regions and
ITSs associate with heterochromatic marks, Arabidopsis
telomeres exhibit euchromatic features (14). More specif-
ically, we found that telomeres have lower levels of het-
erochromatic marks than ITSs (H3K9Me2, H3K27Meand
DNA methylation) and higher levels of euchromatic
marks (H3K4Me2, H3K9Ac and H4K16Ac). Here, we
have shown by analyzing ChIP-seq data that telomeres
have lower levels of heterochromatic marks than centro-
meres (H3K9Me2and H3K27Me) and higher levels of some
euchromatic marks (H3K4Me2and H3K9Ac). Thus, these
data confirm our previous results and validate the meth-
odological approach presented here.
The experimental approach that we have used here to
study the chromatin structure of Arabidopsis telomeres
independently of ITSs could be applied to other eukary-
otes. It will depend on how well genomes are assembled,
including subtelomeric regions, and also on the structure
of ITSs, including their length and number of perfect
Arabidopsis telomeres are labeled with H3K27Me3
We have shown that Arabidopsis telomeres are labeled
with H3K273Me, a repressive mark that usually do not
colocalize with DNA methylation. Recently, ?4400
genes have been found to be labeled with this epigenetic
modification. These genes are often expressed in a tissue-
specific manner and many of them might be involved in
plant development. H3K27Me3is established by the
Polycomb Repressive Complex 2. This complex is
conserved along evolution and is present in Arabidopsis,
problems (18,19,39–42). It will be interesting to ascertain
whether some of these problems are related to telomeres
The histone code hypothesis involves a complex inter-
play of writing, reading and erasing activities that regulate
the levels and the output of different epigenetic modifica-
tions (43). We have previously found that Arabidopsis
telomeres are labeled with H3K4Me2, H3K9Ac and
H4K16Ac. Here, we have confirmed these results and
have also shown that Arabidopsis telomeres are labeled
with H3K27Me3. The analysis of telomeres in mutants
affected in the establishment, recognition and/or erasing
of all these epigenetic marks open new avenues for future
The chromatin organization of Arabidopsis telomeres
shares similarities with the previously reported chromatin
Four main chromatin states (CS1–CS4) have been recently
defined in Arabidopsis based on the genome-wide distri-
bution of 12 epigenetic marks analyzed by ChIP-on-chip
(44–46). Since six of these marks were also analyzed here
(H3K4Me2, H3K4Me3, H3K9Me2, H3K27Me, H3K27Me3
and H3K36Me3), we compared both studies and found
that the chromatin organization of Arabidopsis telomeres
is most similar to chromatin state 2 (CS2). This chromatin
state is associated with 23% of Arabidopsis genes, being
many of them repressed or lowly expressed. CS2 is
characterized by the presence of H3K4Me2, H3K27Me2
and, above all, H3K27Me3. In addition, CS2 is also
characterized by the absence of H3K4Me3, H3K9Me2,
H3K9Me3, H3K27Me, H3K36Me3, H3K56Ac, H4K20Me,
H2Bub and5MeC (45).
GSE28398, GSE22276 and GSE19602.
Supplementary Data are available at NAR Online:
Supplementary Tables 1 and 2.
We want to thank the laboratories of Eric Lam, Jeffrey
Chen and Xing-Wang Deng for making available their
ChIP-seq data at the public databases. We are especially
Relative enrihment of telomres versus
Figure 2. Epigenetic features at rice telomeres. Different histone epi-
genetic modifications were analyzed at telomeres and at centromeres
using study SRP001788 (GSE19602). Relative enrichment values of
telomeres versus centromeres were determined and represented as
indicated in the ‘Materials and Methods’ section.
e163 Nucleic Acids Research, 2012,Vol.40, No. 21PAGE 4 OF 6
grateful to Eric Lam for allowing us to use their data prior
to publication. We also thank NCBI for providing the
tools that we have used to analyze the ChIP-seq data.
The Spanish Ministry of Education and Science [grant
BFU2008-02497/BMC] and by FEDER funds. Funding
for open access charge: Waived by Oxford University
Conflict of interest statement. None declared.
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