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TRENDS in Genetics Vol.23 No.3 FulltKtprovidedbywww.sctencsdirsct.com
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ĽLSĽV1ĽR
Plant centromere organization:
a dynamic structure with conserved
functions *
Jianxin Ma1
, Rod A. Wing2
, Jeffrey L. Bennetzen3
and Scott A. Jackson1
1
Department of Agronomy, Purdue University, 915 West State Street, West Lafayette, IN 47907, USA
2
Department of Plant Sciences, Arizona Genomics Institute, University of Arizona, 1145 East Fourth Street, Tucson, AZ 85721, USA
3
Department of Genetics, University of Georgia, 1057 Green Street, Athens, GA 30602, USA
f 1
Although the structural features of centromeres from
most multicellular eukaryotes remain to be characterized,
recent analyses of the complete sequences of two
centromeric regions of rice, together with data from
Arabidopsis thaliana and maize, have illuminated the
considerable size variation and sequence divergence
of plant centromeres. Despite the severe suppression
of meiotic chromosomal exchange in centromeric and
pericentromeric regions of rice, the centromere core
shows high rates of unequal homologous recombination
in the absence of chromosomal exchange, resulting in
frequent and extensive DNA rearrangement. Not only is
the sequence of centromeric tandem and non-tandem
repeats highly variable but also the copy number,
spacing, order and orientation, providing ample natural
variation as the basis for selection of superior centromere
performance. This review article focuses on the
structural and evolutionary dynamics of plant centromere
organization and the potential molecular mechanisms
responsible for the rapid changes of centromeric
components.
Introduction
The centromeres of eukaryotic chromosomes are
responsible for sister chromatid cohesion (see Glossary)
and for normal chromosomal segregation during mitosis
and meiosis, which are essential for development and
cellular proliferation in all organisms. These functions
are conserved across species, but the DNA components
that are involved in kinetochore formation differ greatly,
even between closely related species [1-5]. Given the functional
importance of centromeres and their rapidly diverging
sequence, it is not surprising that many studies have
focused on characterizing centromeres in terms of their
structure, function and evolution. Deciphering the structural
features and the sequence variation of centromeres is
essential for a more complete understanding of centromere
function(s). Here, we review recent studies on plant centromere
organization with respect to the nature, timing,
evolutionary processes and biological consequences of
centromeric DNA amplification, recombination and
Corresponding author: Jackson, S.A. (sjackson@purdue.edu).
Available online 1 February 2007.
rearrangement, thereby providing insights into the
conserved functions of this dynamic structure.
Molecular components of plant centromeres
Repetitive DNA is ubiquitous and abundant in centromeric
regions of higher eukaryotes. In all flowering plants investigated
so far, different centromeres from an individual
genome are generally composed of the same types of DNA
component, mainly large arrays of centromeric satellite
repeats and centromeric retrotransposons (CRs) [6-14].
However, the abundance and the arrangement of these
repeats vary substantially, both within and among species
[8,10,12,13,15]. In Arabidopsis thaliana, centromeres contain
180-base satellite repeats organized in tandem arrays
xhat range from 0.4 to 1.4 Mb on different chromosomes. By
contrast, the amount of CentO satellite DNA in rice (Oryza
sativa) centromeres differs even more [10], ranging from
60 kb to 1.9 Mb on different chromosomes. Highly variable
amounts of centromeric satellite DNA (CentC) were also
detected in different maize (Zea mays) centromeres
[6,14,15]. In general, these satellite repeats are specific
to centromeric regions, with few copies and no long arrays
found elsewhere in the genome [16-19], suggesting that
these repeats are crucial for centromere function.
There is also substantial variation in the copy number of
satellite repeats in homologous centromeric regions from
different ecotypes [20], inbred lines [15] and subspecies
Glossary
Centromere drive: a model that proposes selection for the unequal transmission
of competing centromeres in female meiosis.
Kinetochore formation: the formation of a protein structure that assembles on
the centromere and links the chromosome to microtubule polymers, which are
attached to the mitotic spindle during mitosis and meiosis in eukaryotes. The
kinetochore contains two regions: an inner kinetochore, which is tightly
associated with the centromeric DNA; and an outer kinetochore, which
interacts with the microtubules.
Negative selection: natural selection that selectively removes rare alleles that
are deleterious.
Positive selection: natural selection that favors a single allele, resulting in allele
frequency continuously shifting in one direction.
Recombinational cold spots: the genomic regions where meiotic recombination
is severely or completely suppressed in contrast to the genomic regions
where meiotic recombination occurs normally or more frequently.
Sister chromatid cohesion: the joining of the sister chromatids of a replicated
chromosome along the entire length of the chromosome, a process that occurs
during mitosis. This cohesion cycle is crucial for high-fidelity transmission of
chromosomes.
www.sciencedirect.com 0168-9525/$- see front matter  2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tig.2007.01.004
TRENDS in Genetics Vol.:
[10]. For example, the centromeric region of O. sativa
chromosome 6 contains over fourfold more copies of CentO
in the japonica subspecies than in the indica subspecies
[10]. A similar phenomenon was observed recently in
different inbred lines of maize [15]. Given that the haplotypes
compared in each of these studies diverged from each
other between only a few thousand and half a million years
ago [21], it is clear that rapid growth and/or shrinkage of
centromeric satellite-repeat arrays can occur within short
evolutionary time frames.
In addition to copy number variation among organisms,
the sequence of centromeric satellite repeats differs markedly
among organisms, even among closely related species
[2-5]. Short conserved motifs are detected between CentO
(rice) and CentC (maize) [10], suggesting that they originated
from a common progenitor ~50-70 million years ago
(Mya) [22]. However, a recent study using chromatin
immunoprecipitation (ChIP) reported that CentO repeats
were absent from the entire data set recovered from functional
centromeres of Oryza brachyantha, a species of wild
rice that last shared a common ancestor with rice only ~7--
9 Mya [23,24]. A different centromeric satellite repeat,
CentO-F, was found in all centromeres of O. brachyantha,
with no detectable homologous copies in the entire O.
sativa genome. This finding suggests that old centromeric
satellite repeats have completely disappeared and that
new centromeric satellite repeats have been generated
in the short time since their independent descent from a
common ancestor.
Centromere organization was also shown to vary greatly 4
with respect to CRs, such as CRRs (in rice) [10] and CRMs
(in maize) [25]. Similar to other long terminal repeat (LTR)
retrotransposon families in centromeric, pericentromeric
and euchromatic regions [26], the CRRs with two intact
LTRs that were identified in centromeric regions are very
young evolutionarily, most having been inserted within the
past few million years [11,27]. Therefore, it is not surprising
that the distribution patterns and abundance of CRs
among centromeres in an individual organism or among
homologous centromeres from different species are highly
variable [10,15,25,28]. In all (non-centromeric) orthologous
regions of grass species that have been compared, including
for rice, maize, wheat (Triticum monococcum), barley
(Hordeum vulgare) and sorghum (Sorghum bicolor), few or
no specific LTR-retrotransposon insertions are detected at
orthologous loci in different species [29-34], largely owing
to their rapid removal by illegitimate recombination and
unequal homologous recombination [35,36]. However,
some highly conserved CR sequences are present in the
centromeric regions of most grasses that have been investigated
[37,38]. This finding suggests that CRs evolve more
slowly than other retroelements because they are selected
for an important centromere function, or are located in a
more slowly evolving portion of the genome, or both. An
exception to the general conservation of grass CRs was
recently reported in O. brachyantha, in which CRR-related
sequences were found to be absent from all functional
centromeres [23].
Despite their preferential accumulation in centromeric
regions, CRRs are present in pericentromeric and euchromatic
regions of all 12 rice chromosomes [28]. However,
N0.3 135
retrotransposons that are not CRs are also present in
centromeric regions of maize [39] and rice [12,13]. It is
particularly intriguing that >50% of the retrotransposon
sequences isolated by ChIP cloning in Oryza rhizomatis, a
wild rice species that last shared a common ancestor with
rice more recently than O. brachyantha, show clear
homology to previously identified non-CRR families present
in both centromeric and non-centromeric regions of
rice [23]. This result supports the idea that non-CRRs could
be converted to fill a functional role similar to CRRs. It is
also possible that some non-CR sequences might be
required for the maintenance of centromere function
[25,40].
Chromatin structures of plant centromeres
Although there is tremendous divergence in centromeric
DNA sequences and marked variation in centromere
organization, centromeric chromatins have similar structural
features in eukaryotes. In general, centromeric chromatin
is distinguished from the surrounding
pericentromej^ nfcprochromatin by the presence of a
specialized histone H3 called CENH3 (also known as
CENP-A). CENH3 replaces the canonical histone H3
and interacts with other core histone proteins to form a
specific type of nucleosome that is essential for kinetochore
formation [1,41]. Species-specific CENH3 molecules have
been identified in all eukaryotes investigated so far, including
humans {Homo sapiens) [42], budding yeast (Saccharomyces
cerevisiae) [43], Drosophila melanogaster [44],
Arabidopsis [40], rice [11], maize [25], sugarcane (Saccharum
officinarum) [45] and Luzula nivea [46]. Because
ICENH3 is present exclusively in functional domains of
centromeres [1,4,47], ChlP-based analyses with a
CENH3-specific antibody have been used routinely to
characterize functional DNA components found to bind
to CENH3, such as CentO and CRRs in rice [11] and CentC
and CRMs in maize [25]. In a comprehensive ChlP-based
analysis using a set of tiled DNA sequences from rice Cen8
(the centromeric region of chromosome 8), Nagaki et dl.
identified a ~750 kb CENH3-binding domain, which
defines the boundaries of functional Cen8 [11]. The interactions
between CENH3 and centromeric repeats (both
CRs and centromeric satellite repeats) also have been
documented recently in other plants [45,46]. Therefore,
it is probable that this interaction is a universal phenomenon
in the plant kingdom.
Epigenetic features of plant centromeres
Not all centromeric repeats in a centromeric region are
associated with CENH3 [25,40]. For example, two ~1.4 kb
CentO blocks (CentO-IV and CentO-V), which are
separated from the other three main CentO blocks
(CentO-I, CentO-II and CentO-III), are not found in the
CENH3-binding domain of rice Cen8 [11] (Figure 1). It is
particularly intriguing that recent observations obtained
from neocentromeres in primates [41] and barley [48]
convincingly showed that the canonical centromeric
repeats are dispensable for attaining some centromere
functions. If normal centromeres are lost or inactivated,
regions without centromeric repeats can recruit CENH3
and other centromere-associated proteins to assemble a
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136 Review TRENDS in Genetics Vol.23 No.3
71 kb
8S
CentO
a b c
CENH3-binding domain of CenS
- M -- 8L
CentO
4S 111 1 1 | I I Uli 4L
Core region of Cen4
Figure 1. Segmental duplication in centromeric regions of rice, (a} The CENH3-binding domain of CenS [11,12]. (b} The core region of Cen4 [13]. Satellite arrays are shown
as green blocks in the lower part of each panel, and the monomers are numbered on the basis of their positions in the respective regions. The upper part of each panel
shows an enlargement of the satellite monomers (green), with the most identical monomer pairs (as revealed by phylogenetic analyses) shown as black lines [27,56]
connected by curved lines. The orientations of satellite-repeat clusters or blocks are also indicated (red arrows). Boxes labeled a, b and c indicate tandemly triplicated
segments.
functional kinetochore that promotes chromosome
segregation [48-51]. Therefore, it is probable that
epigenetic mechanisms have essential roles in mediating
centromere assembly, whereas, in most higher eukaryotes,
centromeric repeats seem to accumulate after a new centromere
has been formed [1,2], and the repeats provide a
favorable environment for establishing centromeric chromatin,
probably by recruiting sequence-specific binding
proteins, to ensure the stable inheritance of centromeres
[47,50].
An evolutionary model involving 'centromere drive'
[2,52] has been proposed recently to explain the rapid
sequence divergence of the genes encoding CENH3
proteins and centromere DNA repeats. According to this
model, during female meiosis in plants and animals, centromeres
compete by microtubule attachments for
inclusion in the single meiotic product that becomes the
egg nucleus and is preferentially transmitted to the next
generation. This preferential inheritance, although
beneficial to the next-generation hopes of a selfish centromere,
would be detrimental to the equal likelihood inheritance
of parental chromosomes in mendelian genetics.
Therefore, it is expected that CENH3 proteins would be
selected for nonpreferential properties at the same time
that centromere cis components (i.e. DNA and epigenetically
inherited chromatin features) would be selected for
preferential segregation properties. This hypothesis is
supported by the findings that CENH3 and/or CENP-C,
a poorly conserved centromeric protein, have undergone
positive selection, thereby suppressing centromere drive
by restoring meiotic parity epigenetically in plants and
animals [40,53]. By contrast, both CENH3 and CENP-C
show signs of negative selection in budding yeast, in which
centromere drive is predicted to be absent, given the
consistent equal transmission of all parental centromeres
[2]. This model also is reminiscent of the meiotic drive
process for maize knob repeats (which are extra-centromeric
satellites), which condition preferential segregation
and transmission to progeny through female meiosis [54].
The rates of transmission of these knob repeats in female
meiosis correlate with the sizes of satellite-repeat arrays
[55]. Assuming that centromere variants with expanded
satellite-repeat arrays increase microtubule-binding ability
during female meiosis in plants and animals, preferential
accumulation of centromeric satellite repeats during
centromere evolution would be an expected outcome of
centromere drive.
Rearrangement of centromeric sequences in Cen8 and
Cen4 of rice
Segmental duplication and inversion of centromeric
DNA revealed by structural and phylogenetic analyses
Recent in-depth analyses of the rice Cen8 and Cen4
sequences [27,56] have provided insights into the evolutionary
dynamics, processes and molecular mechanisms
that have resulted in rapid amplification and variation of
centromeric DNA in higher eukaryotes. One unexpected
observation is the presence of large, tandemly triplicated
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TRENDS in Genetics Vol.:
segments (96 kb, 90 kb and 26 kb, respectively) in the Cen8
region (Figure 1), accounting for 212 kb of the ~750kb
CENH3-binding domain. According to the insertion dates
of shared LTR retrotransposons and the sequence identities
between these three segments, it was estimated that
two duplication events were involved and occurred successively
at similar times within the last ~0.3 million years,
and these were followed by partial deletion of one segment.
In addition, on the basis of phylogenetic analysis of all
satellite monomers in Cen8, 48 satellite monomers in
CentO block I (in Cen8) were found to have respective best
(98-99% identical) matches (i.e. monomers) arranged in
opposite orientation but conserved order in CentO block
III, indicating a recent segmental duplication of the CentO
satellite-repeat arrays in the functional domain of Cen8.
A similar study was carried out on the core region of rice
Cen4 [56]. Phylogenetic analysis of all 460 satellite monomers
in this core region revealed several apparent segmental
duplications of CentO satellite arrays and CRRs
interspersed in the satellite arrays [56]. Hence, segmental
duplication is likely to be a common process driving centromeric
DNA amplification, probably in all plant centromeres.
An unexpected observation was that most CRRs
accumulated in the core region of Cen4 by rounds of segmental
duplication rather than by integration of active
elements. Given that most CRRs and the flanking CentO
monomers were duplicated <0.3 Mya, it is now easier to
understand why the O. sativa subspecies indica and japonica,
which diverged from a common ancestor ~0.44 Mya
[21], show high levels of haplotype variation in orthologous i
centromeric regions [10,27]. However, marked amplification
of centromeric repeats does not result only from recent
segmental duplications. More ancient duplications that
have been deleted, have diverged or have been obscured
by numerous more recent and overlapping DNA rearrangement
events might no longer be detectable. Even in the
most recently duplicated CentO satellite-repeat arrays
(described earlier), insertions or deletions (indels) from a
few monomers up to 130 monomers were frequent [27,56].
Because of the near-complete suppression of homologous
chromosome exchange by recombination that is
expected in all centromeric regions of rice [57], recombinational
conversion and unequal homologous sister-chromatid
recombination [58,59] are likely to be the main
mechanisms underlying the duplication of CentO satellite-repeat
arrays and the array-mediated duplication of
CRRs [27,56]. The rates of these types of recombination
might be increased by the abundance of highly homogeneous
CentO satellite repeats. Although duplication of
CentO satellite-repeat arrays and CRRs is frequent in the
Cen4 core region, it should be noted that unequal recombination
could also lead to deletion of centromeric repeats,
as is predicted to occur in the process of solo-LTR formation.
Given the active expansion of CentO satelliterepeat
arrays in rice centromeres [10], there are probably
selective forces, such as centromere drive [2,52], counteracting
the loss of centromeric satellite DNA and CRRs by
unequal recombination.
Inversions of some duplicated CentO satellite-repeat
arrays were revealed in Cen8 and Cen4 (Figure 1). Unequal
recombination between homologous sequences that are
No.3 137
present in inverted orientation and interspersed in the
CentO satellite-repeat arrays would cause inversion of
the sequences between the recombining sites. Because of
the abundance of CRRs arranged in different transcriptional
orientations in the Cen4 core region, it is possible
that recombination between CRRs has mediated the inversion
of CentO arrays. This probable mechanism is supported
by the presence of LTR retrotransposons (intact or
fragmented) at five of the six junction sites of CentO blocks
arranged in inverted orientation in Cen8 and Cen4
(Figure 1).
Rapid removal of centromeric DNA by unequal
recombination and illegitimate recombination
Although LTR retrotransposons have preferentially
accumulated in the Cen8 region and the Cen4 core region,
processes that remove retrotransposon DNA in both
regions are also active. These are reflected by the presence
of solo-LTRs and various internally deleted or truncated
elements [27,56]. Of the 245 LTR-retrotransposon
elements or fragments identified in a 1.97 Mb region that
contained Cen8, only 26.5% are intact elements, whereas
solo-LTRs and partially deleted elements account for
24.9% and 46.2%, respectively [27]. Most solo-LTRs are
the products of unequal homologous recombination
between the two LTRs of a single element [35], whereas
deleted or truncated elements have been generated mainly
by illegitimate recombination, a mechanism that does not
require extensive sequence homology [26,35]. Hence,
unequal recombination and illegitimate recombination
have removed most of the LTR-retrotransposon sequences
Ifrom Cen8, and similar results were obtained for Cen4 [56].
Deletion of LTR-retrotransposon DNA by unequal
recombination and illegitimate recombination in rice has
been found to be exceptionally efficient. It was estimated
that at least 190 Mb of retrotransposon DNA has been
removed from the rice genome by these processes in the
past 4 million years [21,36]. Because the intact LTR retrotransposons
in the centromeric regions of rice are as young
as those in non-centromeric regions, and because the
relative percentages of intact and truncated elements
are similar to those observed in the entire rice genome
[36], it seems that the elimination of retrotransposon DNA
is similarly efficient in all parts of the rice genome. This
result agrees with similar findings inZ). melanogaster [60],
for which it has been concluded that rates of DNA sequence
loss are identical in euchromatic and heterochromatic
regions.
Perhaps the most interesting observation regarding the
structural variation of LTR retrotransposons in Cen8 was
the discovery of preferential accumulation of solo-LTRs in
a subregion that includes the main CentO blocks in the
CENH3-binding domain [27]. The ratio of solo-LTRs
to intact elements in this subregion is approximately
threefold more than in other centromeric and pericentromeric
subregions and is slightly greater than in non-centromeric
regions of rice [21], indicating a hot spot for
unequal intra-element recombination in Cen8. Given the
near-complete suppression of meiotic chromosomal
exchange in centromeric regions that is indicated by
recombinational mapping [57], and given the high ratio
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13E TRENDS in G..-n.Mic< V o l !
Box 1. Unanswered questions
Roles of centromeric sequences
Both CRs and centromeric satellite repeats interact with CENH3 in all
plant species that have been investigated. Do these two classes of
centromeric repeat have similar or distinct roles in centromere
function? Non-CRs and single-copy sequences can also interact with
CENH3 in some organisms [11,25,40]. Are these CENH3-binding
sequences all required for centromere formation? The development
of artificial plant chromosomes might provide new tools to study
centromere structure and function. What are the minimal requirements
for assembly of a highly efficient artificial chromosome?
Divergence of centromeric components
Centromere drive has been proposed to explain the rapid divergence
of centromeric DNA and proteins (e.g. CENH3 and/or CENP-C)
in most plants and animals. This model might also account for the
disappearance of CentO and CRRs from functional centromeres of
Oryza brachyantha, a wild rice species that diverged from Oryza
sativa (rice) ~7-9 Mya. However, conserved CR sequences, centromeric
satellite repeats and CENH3 were found in multiple grass
species: for example, rice and maize, which diverged from each
other ~50-70 Mya. Why have centromeric repeats undergone such
marked changes in O. brachyantha but not in rice and maize? Are
there genetic factors that could suppress the process of centromere
drive?
Evolutionary stage of rice Cen8
The presence of active genes in the CENH3-binding domain of Cen8
and of low quantities of CentO repeats in the Cen8 region suggested
that Cen8 might represent an intermediate stage in the evolution of
centromeres from genie regions, as in human neocentromeres, to
fully mature centromeres that accumulate megabases of homogeneous
satellite arrays [11]. However, rapid contraction or expansion,
reshuffling and rearrangements of centromeric DNA are
proposed to have occurred in Cen8. Do these changes disguise
the evolutionary stage of Cen8?
of solo-LTRs to intact elements that has been observed in
rice centromeres [27,56], it is probable that centromere
recombination, whether equal or unequal, is reguH|ed by
the cells such that it is rarely associated with crossovers.
Concluding remarks
In-depth analyses of plant centromeric sequences, including
the first completely sequenced rice centromeres, have
deepened our understanding of the dynamic structures,
variation and evolution of higher eukaryotic centromeres.
High rates of unequal (and presumably equal) recombination
in the centromere have been detected, suggesting that
crossover suppression is the main factor underlying the
traditional perception of centromeres as recombinational
cold spots. Rates of DNA removal from centromeric regions
also do not seem to be slower than in other parts of the
genome, suggesting that selection against inserts in
euchromatic regions and/or preferential insertion into heterochromatin
are the main reasons for uneven LTR-retrotransposon
accumulation. The results indicate that
centromere function can be maintained even with high
rates of local genome rearrangement, and they suggest
that this rearrangement could be a considerable component
of centromere drive [2,44]. Therefore, in plants
and animals, this provides a basis for competition for more
successful female gamete transmission of a centromere
that shows superior association with the kinetochore.
Although insights into the dynamic structures of plant
centromeres have been gained from these exciting obser-
No.3
vations, many intriguing questions (Box 1) are also raised
and need to be further investigated.
Acknowledgements
We are grateful to the anonymous reviewers for their valuable comments
and to the National Science Foundation for supporting this work (grant
number DBI-0501814 to J.L.B., DBI-0227414 to S.A.J, and DBI-0321678
to R.A.W. and S.A.J.).
ˇ
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