A molecular view of plant centromeres
Jiming Jiang1
, James A. Birchler2
, Wayne A. Parrott3
and R. Kelly Dawe4
1
Department of Horticulture, University of Wisconsin-Madison, Madison, WI 53706, USA
2
Division of Biological Science, University of Missouri, Columbia, MO 65211, USA
3
Department of Crop and Soil Sciences, University of Georgia, Athens, GA 30602, USA
4
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA
Although plants were the organisms of choice in
several classical centromere studies, molecular and biochemical
studies of plant centromeres have lagged
behind those in model animal species. However, in the
past several years, several centromeric repetitive DNA
elements have been isolated in plant species and their
roles in centromere function have been demonstrated.
Most significantly, a Ty3/gypsy class of centromerespecific
retrotransposons, the CR family, was discovered
in the grass species. The CR elements are highly enriched
in chromatin domains associated with CENH3, the
centromere-specific histone H3 variant. CR elements as
well as their flanking centromeric satellite DNA are
actively transcribed in maize. These data suggest that
the deposition of centromeric histones might be a
transcription-coupled event.
Centromeres are responsible for sister chromatid cohesion
and are the sites for kinetochore assembly and spindle
fiber attachment, thereby enabling faithful segregation of
chromosomes during cell division. Although these functions
are conserved among all eukaryotes, there is no
conservation of centromeric DNA sequences: different
organisms have strikingly different centromeric DNAs.
This enigma has led to extensive studies in several model
eukaryotes, including Saccharomyces cerevisiae, Schizosaccharomyces
pombe, Drosophila melanogaster and
humans. Here we review the recent progress on centromere
research in plants.
Centromeric histone H3 defines the boundaries of the
centromere
Although centromeres can be defined cytologically or
genetically, currently the most widely used definition of
the centromere is biochemical: if a DNA sequence interacts
with the kinetochore it is part of the functional centromere.
At least 14 demonstrated or putative kinetochore
proteins have been identified in plants, and these are
generally localized in two domains, the inner and outer
kinetochore [1­4]. The outer kinetochore proteins are
transient and only necessary during chromosome segregation,
whereas the inner kinetochore proteins recognize
centromeric DNA and establish a specialized chromatin
environment.
A fundamental feature of the inner kinetochore is a
specialized histone H3 variant known as centromeric
histone CENH3 [5,6]. The first CENH3 (CENP-A) was
identified in humans [7,8], and homologous proteins have
since been identified in all eukaryotes studied, including
Arabidopsis thaliana [3] and maize [4]. CENH3 differs
from the common form of histone H3 because it has a
highly divergent N-terminal tail, which can vary substantially
in length and composition even among closely
related organisms [3,9]. CENH3 is present only in the
functional centromeres of dicentric chromosomes in
humans [10]. In addition, blocks of CENH3-associated
nucleosomes and regular H3-associated nucleosomes are
linearly interspersed in functional centromeres [11,12].
Thus, the boundary of the centromere can be defined by
identifying DNA sequences that interact with CENH3.
Centromeric satellite arrays
The simple point centromeres of S. cerevisiae consist of
only ,125 base pairs (bp) of unique sequence [13].
However, the centromeres in multicellular eukaryotic
species are much larger and are embedded within megabases
of highly repetitive DNA sequences. Satellite DNA is
often the dominant DNA component in centromeres [14].
For example, the most abundant sequence in human
centromeres is the ,171 bp a-satellite repeat, which is
organized into long arrays of between ,250 kb and .4 Mb
[15]. Human artificial chromosomes were successfully
assembled using either synthetic or cloned a-satellite
DNA, suggesting that long stretches of a-satellite DNA
could act as a functional human centromere [16­18].
Satellite repeats associated with centromeres have
been reported in several plant species (Table 1). These
centromeric satellite repeats are highly abundant and can
be readily visualized and cloned by restriction digestion of
the genomic DNA [19­23]. Like the a-satellite in human
centromeres, the centromeric satellites in plants are
organized into arrays that can be several megabases
long [24­26]. A common characteristic of centromeric
satellite repeats is their rapid divergence [6]. Although
weak homology can sometimes be detected between
centromeric repeats of distantly related species (e.g. rice
and maize [26]), most plant centromeric satellite repeats
are specific to only closely related species [19­22,27,28]. In
spite of their phenomenal rate of evolution, centromeric
satellites appear to serve as the core of the centromere. In
maize and Arabidopsis, chromatin immunoprecipitation
Corresponding authors: Jiming Jiang (jjiang1@wisc.edu),
R. Kelly Dawe (kelly@dogwood.botany.uga.edu).
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(ChIP) experiments have demonstrated a clear interaction
between CENH3 and centromeric satellites [4,29].
Another puzzling observation is that the quantity of
centromeric satellites varies substantially from chromosome
to chromosome. In most cases, centromeric satellites
are present in vast excess. Each of the five Arabidopsis
centromeres contains ,2­4 Mb of the 180-bp centromeric
satellite repeat [30­32] and the centromeric region of the B
chromosome in maize contains up to 9 Mb of the B-specific
repeat [33]. A centromere can be broken in two by a process
known as misdivision [34,35]. Using the B chromosome
centromere of maize, which contains a unique repeat that
serves as a specific marker, numerous misdivision derivatives
were analyzed [33,36]. The B-specific repeat cluster
in some rearranged B centromeres was reduced from 9 Mb
to as small as 200­500 kb. Further misdivision derivatives
of these small centromeres can be recovered, but the size of
the repeat cluster remains similar or is increased
(T. Phelps-Durr and J.A. Birchler, unpublished). ChIP
studies also indicate that only a portion of the satellites
in the cell can be precipitated by anti-CENH3 antibodies
[4,29]. These results show that only a portion of the
centromeric satellite is included in CENH3-associated
centromeric chromatin.
The characteristic variability of centromeric satellites
suggests that they might evolve by a process akin to
meiotic drive [37], where chromosomes compete for access
to the next generation by skewing mendelian segregation
in their favor [38]. On the basis that the N-terminus and
Loop 1 regions of CENH3 show evidence of adaptive
evolution, Steve Henikoff and colleagues argued that
CENH3 might be adapting to bind the rapidly evolving
centromere [3,9]. Under this model, centromeric DNAs
that are most efficient at binding to kinetochore proteins
are likely to arrive at spindle poles first and be segregated
to the functional megaspore (plants) or pronucleus
(animals). The analogy is drawn to an arms race, where
the satellites are evolving to bind more efficiently to the
kinetochore and enhance their chances of being segregated
to progeny whereas the host is evolving to modulate the
interaction so that each of the chromosomes segregate
with roughly the same efficiency. The result of the arms
race is an ever-changing population of long uniform
satellite arrays. Sequence data from Arabidopsis, derived
from 457 satellite repeats, support this scenario [39].
Tandem repeats are well suited to this environment
because of their susceptibility to unequal recombination
[40], which can sweep new polymorphisms through an
array in a relatively short time frame.
Centromere-specific retrotransposons in plants
In general, the abundance of retrotransposons is much
lower in centromeres than would be expected based on
their frequency in other parts of the genome [41,42].
Recent characterization of the centromere of human X
chromosome showed that the functional domain contains
highly homogenized a-satellite arrays and lacks transposon
insertions, whereas the flanking domains contain
diverged a-satellite arrays and significantly more transposons
[43]. These results imply that transposon invasion
interferes with centromere function or that the satellites
in the functional core domain are homogenized by frequent
unequal recombination, a process that would also remove
inserted transposons.
Table 1. Centromere-associated repetitive DNA elements reported in plants
Plant species Repeat and description Refs
Arabidopsis arenosa pAa214: 166­179-bp tandem repeat [21]
Arabidopsis thaliana pAL1: 180-bp tandem repeat [66,67]
Beta species pBV1: ,326-bp tandem repeat [28]
pT55: ,160-bp tandem repeat
ppHC8: 162-bp tandem repeat
pTS4.1: 312-bp tandem repeat
pBp10, pBv26: centromere-enriched retrotransposons
Brachycome dichromosomatica Bd49: 176-bp tandem repeat specific to the centromeres of B chromosomes [68]
Brachypodium sylvaticum CCS1: centromere-specific retrotransposon (CR family) [44]
Brassica campestris pBT11, pBcKB4: ,175-bp tandem repeat [19,69]
Brassica oleracea pBoKB1: ,171-bp tandem repeat [19]
Hordeum vulgare (barley) (AGGGAG)n satellite DNA [47,70]
Cereba: centromere-specific retrotransposon (CR family)
Oryza sativa (rice) CentO: 155-bp tandem repeat [26,49,71]
CRR: centromere-specific retrotransposon (CR family)
Pennisetum glaucum pPgKB19: 137-bp tandem repeat [20]
Petunia hybrida pBS-SB1-B5: 666-bp tandem repeat [72]
Saccharum officinarum (sugar cane) pSG1-2: 140-bp tandem repeat [23]
Secale cereale (rye) Bilby: centromere-specific retrotransposon [73]
Sorghum bicolor (sorghum) pSau3A10, pCEN38: ,137-bp tandem repeat [27,45,46,74]
pSau3A9, pHind22: centromere-specific retrotransposon (CR family)
Triticum aestivum (wheat) TailI: 570-bp tandem repeat [75,76]
pBS301: 250-bp tandem repeat
Vigna unguiculata pVuKB1: 488-bp tandem repeat [22]
Zea mays (maize) CentC: 156-bp tandem repeat [51,52,77,78]
Cent4: ,740-bp tandem repeat specific to chromosome 4
CentA, CRM: centromere-specific retrotransposon (CR family)
B repeat: B centromere-specific tandem repeat
Zingeria biebersteiniana Zbcen1: 755-bp tandem repeat [79]
Zb47A: centromere-enriched retrotransposon
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In contrast to the low abundance of many retrotransposon
families in plant centromeres [42], there are
a few plant retrotransposon families that are significantly
enriched in the centromeric regions or highly specific to
the centromeres (Table 1). A particularly intriguing class
is the centromeric retrotransposon (CR) family discovered
in grass species. Sequences derived from the CR family
were first isolated from Brachypodium sylvaticum [44] and
sorghum [45]. These sequences were later found to be
derived from a Ty3/gypsy class of retrotransposon [46­48].
Unlike other retrotransposon families that diverge rapidly
during evolution, the CR family has been found in the
centromeres of all grass species studied [46], including the
centromeres of B chromosomes [49] and a significantly
rearranged rye centromere [50]. Highly conserved motifs
were found in the long terminal repeats (LTRs) of the CR
elements from rice, maize and barley [51]. CR elements
are frequently found inserted into centromeric satellites
[26,51]. CR elements can also insert into each other, and
often cluster together in long arrays [26].
In maize, CRM (the maize subfamily of CR) elements
are common and extensively intermingled with CentC, a
156-bp centromeric satellite repeat [52] (Figure 1). Such
intermingled CRM and CentC sequences stretch from
300 kb to .2 Mb in the core domains of maize centromeres
(W.W. Jin and J. Jiang, unpublished) (Figure 1). Importantly,
CRM elements are immunoprecipitated by CENH3
antibodies as efficiently as CentC [4], indicating that the
CRM elements are functional components of maize
centromeres. Thus, CRM elements appear to have adapted
to the special environment of the centromeric chromatin.
The adaptation might be as simple as carefully targeting
the centromere [48] and transposing at a rate that is faster
than the rate of removal by unequal recombination.
Alternatively, the transposon might contribute in a positive
manner to centromere function and provide the host
with a selective advantage.
Centromere­kinetochore interface ­ how is centromeric
DNA recognized?
In the past few years, our understanding of kinetochore
proteins and the underlying centromeric DNAs has
expanded at a remarkable pace, but we have been unable
to answer the fundamental question of how the centromere
and inner kinetochore recognize each other. Most authors
agree that interactions must be epigenetic (sequence
independent), but because the centromeres are reliably
maintained at the same loci, this strongly suggests some
sort of DNA­protein recognition process. In humans,
sequence specificity is conferred in part by the kinetochore
protein CENP-B, which is thought to have evolved from a
transposable element. CENP-B has significant homology
to Mariner transposases [53] and binds to a 17-bp motif in
the a-satellite DNA (presumed remnant of a Mariner TIR)
that is required for efficient artificial chromosome formation
in humans [54]. What might have begun as the
invasion of the centromere by a transposable element,
seems to have evolved into a mutualistic relationship
where both the centromere and (a descendent of) the
transposable element benefit. CENP-B and its interaction
with the centromere provides a precedent for the idea that
transposons might be selected for a role in chromosome
segregation [53].
Maize and rice CR elements have substantial homology
in the LTR [4,51], suggesting that there has been selective
pressure at the nucleotide level. Because the transposon
does not appear to be mimicking the satellite DNAs, either
in size or in primary sequence, the selective pressure
might be on the capacity to initiate RNA (i.e. the promoter)
or the RNA itself [55]. CR elements in both maize and
rice are indeed expressed, as judged by the presence of
CR-homologous ESTs in GenBank. CentC RNA, although
not detectable on northern blots or EST databases (only a
single cDNA clone reported), can be readily detected
within the nucleus and on chromatin immunoprecipitated
with CENH3 antibodies (C.X. Zhong et al., unpublished).
These results parallel a recent study in humans showing
that selection for transcription near an array of a-satellite
repeats can induce the formation of a functional centromere
[56]. The CR elements might be under selection for
their capacity to initiate transcription through flanking
satellite DNA. Any centromere-embedded transcription
units, either from transposons or cryptic promoters within
satellite repeats, could fulfill the same function.
In animals, CENH3 is incorporated into chromatin in a
replication-independent fashion [11,57]. Henikoff and
colleagues have suggested that histone replacement is
often associated with active transcription ­ a time at
which nucleosomes are destabilized (or fully displaced)
Figure 1. Structure and organization of centromeric DNA in maize. (a) Fluorescence
in situ hybridization (FISH) of centromeric DNA on maize pachytene chromosomes.
The maize centromeric satellite CentC [52] is visualized in red and the
maize centromere-specific retrotransposon CRM is visualized in green. Scale
bar  10 mm. (b) Digitally separated FISH signals derived from CentC. (c) Digitally
separated FISH signals derived from CRM. Both CentC and CRM are highly specific
to the centromeric regions. The amount of CentC varies significantly among
different maize centromeres. The size and intensities of the FISH signals from
CRM are relatively similar among different centromeres. (d) Organization of the
centromeric DNA of maize chromosome 6 revealed by FISH analysis on extended
DNA fibers (fiber-FISH). DNA fibers were prepared from an oat­maize chromosome
addition line 6 [80] and probed with CentC (green) and CRM (red) probes.
The CRM sequences are clustered and intermingled with the CentC satellite.
Each micrometer of the fiber-FISH signals represents ,3.2 kb DNA [81]. Scale
bar  10 mm. (e) A diagram of the DNA structure of maize centromere 6. Green
and red bars represent CentC and CRM sequences, respectively. Blue bars
represent unknown sequences. The FISH images in (a), (b), (c) and (d) are courtesy
of Weiwei Jin.
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and subsequently reassembled [58]. The chromatin disruption
caused by transcription provides an ideal time for
histone replacement. Assuming a slight binding preference
of CENH3 for satellite DNA, transcription of the
centromere might be sufficient to establish a CENH3centered
chromatin environment. However, at least in
maize, much of the centromeric RNA remains associated
with centromeric chromatin. The high local concentration
of RNA might help to recruit CENH3, similar to the role of
human Xist RNA in facilitating the replacement of histone
H2 with macroH2 on inactive X chromosomes [59]. Several
chromatin proteins are known to bind RNA [60,61],
including histones themselves [62]. One can imagine
that centromeric RNA has an affinity for chromatin
remodeling proteins, other kinetochore proteins or
CENH3 itself. As a result, centromere-associated RNA
could facilitate chromosome segregation by helping to
recruit necessary proteins to the centromere (Figure 2a,b).
A transcription-mediated mechanism for CENH3 deposition
might help to explain some aspects of centromere
initiation, but it does not adequately explain the stability
of the centromeres once they are established [63] or why
centromeres often include non-satellite DNA [5]. One idea
is that the centromeric state is reinforced and maintained
by the tension applied during spindle attachment [64]. The
excessive force applied during metaphase and anaphase
(10 000 times what is needed [65]) might tear the histones
from the DNA [11]. The damaged chromatin could then be
marked for repair by a replication-independent mechanism
similar to the one that originally installed CENH3
(Figure 2c). This model allows for considerable plasticity
during centromere establishment, but favors successful
centromeres by continually marking and reusing them.
Acknowledgements
We acknowledge the support of plant centromere research from the
National Science Foundation (grant 9975827 to R.K.D., J.A.B., W.A.P. and
J.J.), the US Department of Energy (grant DE-FG02­01ER15266 to J.J.).
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(a)
(b)
(c)
CENPC
CENPC
RNA POL
RNA
Histone H3
CENH3
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Have you seen the series of GM technology articles
published in Trends in Plant Science in 2003?
Mike J. Wilkinson, Jeremy Sweet and Guy M. Poppy Risk assessment of GM plants: avoiding gridlock? Volume 8, Issue 5, 208­212
Ian S. Curtis The noble radish: past, present and future. Volume 8, Issue 7, 305­307
M. Finlay B. Dale and John E. Bradshaw Progress in improving processing attributes in potato. Volume 8, Issue 7, 310­312
Elizabeth E. Hood Selecting the fruits of your labors. Volume 8, Issue 8, 357­358
Claire Halpin and Wout Boerjan Stacking transgenes in forest trees. Volume 8, Issue 8, 363­365
Matthew A. Escobar and Abhaya M. Dandekar Agrobacterium tumefaciens as an agent of disease. Volume 8, Issue 8, 380­386
Published in this issue:
Carol Auer Tracking genes from seed to supermarket: techniques and trends.
Alan Bennett Out of the Amazon: Theobroma cacao enters the genomic era.
Alain Boudet, Shinya Kajita, Jacqueline Grima-Pettenati, and Deborah Goffner Lignins and lignocellulosics: a better control of
synthesis for new and improved uses.
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