Báo cáo khoa học: From meiosis to postmeiotic events: Alignment and recognition of homologous chromosomes in meiosis ppt

MINIREVIEW
From meiosis to postmeiotic events: Alignment and
recognition of homologous chromosomes in meiosis
Da-Qiao Ding
1
, Tokuko Haraguchi
1,2,3
and Yasushi Hiraoka
1,2,3
1 Kobe Advanced ICT Research Center, National Institute of Information and Communications Technology, Kobe, Japan
2 Graduate School of Frontier Biosciences, Osaka University, Suita, Japan
3 Department of Biology, Graduate School of Science, Osaka University, Toyonaka, Japan
Introduction
Meiosis is an essential process for sexually reproducing
eukaryotic organisms, producing haploid gametes or
spores from a diploid cell. In this process, one round
of DNA replication is followed by two consecutive
nuclear divisions to halve the number of chromosomes.
A characteristic feature of meiosis is the behavior
exhibited by homologous chromosomes. Homologous
chromosomes form a pair and recombine with each
other in meiosis, whereas they behave independently in
mitotic cell cycles. Meiotic recombination of homolo-
gous chromosomes is important for ensuring the cor-
rect segregation of chromosomes during the two
rounds of nuclear division: reductional segregation of
homologous chromosomes in the first division,
and equational segregation of sister chromatids in the
second division.
The process of homologous recombination has been
extensively studied at the molecular level (L. Sze

´
kvo
¨
l-
gyi and A. Nicolas, this issue [1]), and mechanisms for
DNA strand exchange have been determined at atomic
resolution (W. Kagawa and H. Kurumizaka, this issue
[2]). However, before a pair of homologous DNA
strands can interact with each other, they must find
each other within the cell nucleus. How chromosomes
can find their homologous partners to be paired has
been a long-standing question [3–8]. Considering the
enormous size of the genome, it is unlikely that DNA
sequences are directly compared over the entire gen-
ome in the nucleus, like a nucleotide blast search of a
database. Instead, the process of homologous recogni-
tion may involve chromosome-specific identifiers that
can recognize homology at a first glance without com-
Keywords
bouquet arrangement; double-strand break;
homologous chromosome pairing; KASH
domain protein; meiosis; recombination;
SUN domain protein; synaptonemal
complex; telomere; transcription
Correspondence
Y. Hiraoka, Graduate School of Frontier
Biosciences, Osaka University,
1-3 Yamadaoka, Suita, Japan
Fax: +81 6 6879 4622
Tel: +81 6 6879 4620

E-mail:
(Received 10 August 2009, revised 21
October 2009, accepted 5 November 2009)
doi:10.1111/j.1742-4658.2009.07501.x
Recombination of homologous chromosomes is essential for correct reduc-
tional segregation of homologous chromosomes, which characterizes meio-
sis. To accomplish homologous recombination, chromosomes must find
their homologous partners and pair with them within the spatial con-
straints of the nucleus. Although various mechanisms have developed in
different organisms, two major steps are involved in the process of pairing:
first, alignment of homologous chromosomes to bring them close to each
other for recognition; and second, recognition of the homologous partner
of each chromosome so that they can form an intimate pair. Here, we dis-
cuss the various mechanisms used for alignment and recognition of homol-
ogous chromosomes in meiosis.
Abbreviations
DSB, double-strand break; SC, synaptonemal complex; SPB, spindle-pole body.
FEBS Journal 277 (2010) 565–570 ª 2009 The Authors Journal compilation ª 2009 FEBS 565
paring nucleotide sequences in detail, e.g. structural fea-
tures specific to each chromosome. In fact, pairing of
homologous chromosomes involves several cytological
steps: spatial alignment of homologous chromosomes
accompanied by extensive intracellular rearrangement
of chromosomes, dramatic changes in chromosome
structures, recognition of homologous chromosomes,
recombination of homologous chromosomes, and devel-
opment of a structure called the synaptonemal complex
(SC), which intimately connects the homologous chro-
mosomes along their entire lengths [9] (Fig. 1). Of these
steps, it is recognition for which the mechanisms remain

largely unknown. Mechanisms dependent on or inde-
pendent of double-strand breaks (DSBs) of DNA have
both been found. Here, we give an overview of the cur-
rent understanding of how homologous chromosomes
pair in meiosis. We focus on the mechanisms used for
homologous alignment obtained from recent studies in
the fission yeast Schizosaccharomyces pombe and the
nematode Caenorhabditis elegans, and propose models
for homologous recognition.
Alignment of homologous
chromosomes
Pairing of homologous chromosomes occurs at an
early stage of meiosis, involves searching for homolo-
gous partners, and leads to intimate connections along
the entire lengths of homologous chromosomes. At
this stage of meiosis, a characteristic arrangement of
chromosomes called the ‘bouquet’ arrangement, in
which chromosomes are bundled at the telomere to
form a bouquet-like arrangement, is observed in a
wide variety of organisms [3,4,10–12] (Fig. 1C,D). To
form a bouquet arrangement, telomeres are attached
to a restricted area of the nuclear envelope, generating
a polarized configuration of chromosomes (Fig. 1B–D).
These chromosomal events occur during meiotic pro-
phase, while the nuclear envelope is intact.
An extreme form of the bouquet arrangement has
been observed in the fission yeast Schiz. pombe, and
the underlying molecular mechanisms have been exten-
sively studied in this organism. Schiz. pombe cells nor-
mally grow in the haploid state in the presence of

sufficient nutrients; upon nitrogen starvation, haploid
cells of the opposite mating type conjugate to form a
diploid zygote. In a zygote, two nuclei fuse together,
and fusion of haploid nuclei is immediately followed
by characteristic movements of the elongated nucleus,
called a ‘horsetail’ nucleus. The horsetail nucleus
moves back and forth between the cell ends for about
2 h. After the nuclear movements cease, two rounds of
nuclear division occur. Thus, the horsetail period, cor-
responding to meiotic prophase, provides the only
opportunity for homologous chromosomes to pair and
recombine with their homologous partners. This situa-
tion has made Schiz. pombe an attractive experimental
system, as we can investigate every event that occurs
between homologous chromosomes during the horse-
tail period of a few hours.
Premeiotic interphase
Meiotic prophase
A
B
C
D
E
Fig. 1. Pairing and recognition of homologous chromosomes. Two pairs of homologous chromosomes are shown inside the nucleus, with
the centrosome immediately outside the nucleus. Each pair of homologous chromosomes is shown in magenta or green; dark and light lines
of the same color indicate homologous chromosomes. Centromeres are indicated by closed circles (A–E). Putative chromosome identifiers
are indicated by shaded circles (B, C). (A) During premeiotic interphase, unpaired homologous chromosomes are distributed within the
nucleus. (B) Putative chromosome identifiers are formed along each chromosome at the beginning of meiotic prophase. (C, D) After chromo-
somes are aligned by bouquet formation, putative chromosome identifiers recognize the homologous partner. (E) A pair of homologous chro-
mosomes are synapsed along their entire length at the end of meiotic prophase.

Homologous chromosome pairing in meiosis D Q. Ding et al.
566 FEBS Journal 277 (2010) 565–570 ª 2009 The Authors Journal compilation ª 2009 FEBS
The Schiz. pombe horsetail nuclear movements are
mediated by astral microtubules, which radiate from
the spindle-pole body (SPB; a microtubule-organizing
center in fungi), and a dynein protein motor [13,14].
The telomeres remain clustered at the leading edge of
the moving nucleus throughout the movements [13,15].
Observation of homologous pairing in living meiotic
cells has demonstrated that telomere clustering and
oscillatory chromosomal movements spatially align
homologous chromosomes in the early stages of mei-
otic prophase to promote their contact [16]. In the
early stages, the arm regions of homologous chromo-
somes become close to each other independently of
recombination (in the absence of Rec12), and these
contacts are stabilized later in a recombination-depen-
dent (Rec12-dependent) manner [16,17]. Schiz. pombe
Rec12 is a homolog of Saccharomyces cerevisiae
Spo11, which is required for DSB formation, and
therefore for recombination [18]. At the centromere
regions, however, homologous associations gradually
increase during the horsetail stage, with similar dynam-
ics being observed in both wild-type and rec12 mutant
cells, suggesting that pairing at the centromere is stabi-
lized in a DSB-independent manner [16].
The ultimate form of pairing is synapsis, which, in
many organisms, is accomplished by the formation of
the SC, a tripartite structure connecting homologous
chromosomes (Fig. 1E). It is known, however, that

some organisms do not develop SCs between paired
sets of homologous chromosomes, although they are
recombined. Schiz. pombe is an example of such organ-
isms lacking canonical SCs [19]. In this organism,
interestingly, the continuous pulling movements of the
chromosomes may compensate for the lack of stable
synapsis between homologous chromosomes.
Motions of chromosomes for their
alignment and pairing
The process of homologous chromosome pairing
requires mechanisms for finding homologous chromo-
somes and, at the same time, preventing non-specific
contacts between heterologous chromosomes. During
this process, significant motions of chromosomes are
expected to occur within the nucleus. It is generally
thought that clustering of telomeres, or the bouquet
formation, provides a way of promoting homologous
pairing by reducing the freedom of movement of chro-
mosomes within the nucleus. Subsequently, oscillatory
movements of the entire nucleus occur in Schiz. pombe.
In some other organisms, intranuclear movements of
chromosomes are observed, e.g. in the budding yeast
S. cerevisiae [20–23] or in rat spermatocytes [24].
Either kind of chromosomal motion probably has dual
roles: first, to act as an attractive force by agitating
chromosomes to increase their chance of contact with
a homologous partner, and second to act as a repulsive
force by disrupting contact between nonhomologous
chromosomes. Contacts between homologous chromo-
somes would result in a stable, physical link, and the

elimination of heterologous chromosomes, and, over
time, homologous chromosomes would eventually pair
along their entire lengths.
Studies in Schiz. pombe have also revealed a mecha-
nism for the intranuclear motion of chromosomes
[25,26]. Members of conserved families of SUN and
KASH domain proteins, Sad1 and Kms1, are involved
in the intranuclear chromosomal motions tethering
telomeres to the SPB. In general, SUN and KASH
domain proteins form a complex that spans the nuclear
envelope [27,28]. The Sad1–Kms1 protein complex is
localized exclusively at the SPB, but is transiently
enriched at the telomeres on the nuclear envelope spe-
cifically during the process of bouquet formation (telo-
mere clustering). During this process, the Sad1–Kms1
protein complex interacts with telomeres on the nucleo-
plasmic side, and with a dynein protein motor on the
cytoplasmic side. In this way, telomeres are moved by
the driving force generated by the dynein motor on
microtubules, which is transmitted by the Sad1–Kms1
protein complex across the nuclear envelope.
An interesting mechanism for homologous pairing
and recognition has been observed in the nematode
C. elegans. In this organism, special nontelomeric
regions on chromosomes play a role analogous to telo-
meres in bouquet arrangement, and act as a pairing
center that promotes pairing and synapsis of the chro-
mosomes [29,30]. The pairing center on each chromo-
some is bound by one of the four zinc finger proteins
HIM-8, ZIM-1, ZIM-2, and ZIM-3, providing a mech-

anism for homologous recognition to occur [31,32].
These proteins then attach to the nuclear envelope,
where they interact with the SUN and KASH domain
proteins, SUN-1 and ZYG-12 [33]. It has been demon-
strated that the SUN–KASH protein complex plays a
role in moving chromosomes along the nuclear enve-
lope using cytoskeletal motor proteins [26,27]. Thus,
this mechanism exhibited by the SUN–KASH protein
complex is analogous to formation of the bouquet
arrangement in Schiz. pombe. Furthermore, recent
studies have revealed that similar mechanisms are
likely to be involved in intranuclear chromosomal
movements in S. cerevisiae [20,21,23,34]. The SUN–
KASH protein complex provides a general mechanism
for moving chromosomes within the nucleus using
cytoskeletal forces through the nuclear envelope.
D Q. Ding et al. Homologous chromosome pairing in meiosis
FEBS Journal 277 (2010) 565–570 ª 2009 The Authors Journal compilation ª 2009 FEBS 567
Recognition of homologous
chromosomes
Bouquet formation appears to be a common mecha-
nism for the alignment of chromosomes in many
organisms. However, the question still remains as to
how chromosomes recognize their homologous part-
ners. It has been proposed that the interactions
between homologous DNAs with DSBs and the con-
sequent recombination are involved in homology
searching in S. cerevisiae [5]. On the other hand,
homologous pairing is independent of recombination
in many organisms [5,6]. After chromosomes have

been aligned, if each chromosome had a unique pat-
tern of blocks of specific molecular components
along its length, such a pattern would generate a
chromosome-specific barcode, which could act as a
chromosome identifier (Fig. 1B,C). Such markers on
the chromosome could be recognized at first glance
without direct comparison of DNA sequences.
Heterochromatin blocks could form such a chromo-
some-specific barcode, and so could transcription
machinery. In meiosis in male Drosophila, homolo-
gous recombination does not occur [35]. In this
organism, it is reported that strong pairing sites cor-
respond to highly transcribed rDNA loci and histone
genes [36]. A previous model proposed roles for
transcription and for a specialized transcription fac-
tory in homologous chromosome recognition and
pairing [37,38]. In this model, DNA regions that are
under active transcription are attached to a specific
transcription factory, in which transcriptional
machinery proteins are aggregated, and those DNA
regions that are not undergoing transcription pro-
trude from the factory and form a chromatin cloud;
therefore, a chromosome appears as a linear array of
many factories and clouds. In meiosis, chromosomes
are aligned in the chromosome bouquet. Because
aligned homologous chromosomes have the same
pattern of factories and clouds in parallel, a chroma-
tin cloud could also join the factory on its homolog
for transcription, and in this way homologous chro-
mosomes would be tethered temporally. When many

of these temporal interactions occurred, two homolo-
gous chromosomes would be zipped up their entire
length (Fig. 1C,D). This model provides a possible
mechanism for how transcription results in recogni-
tion and pairing of homologous chromosomes. A
similar model, in which pairing can be achieved
through joining of allelic transcription units to the
same transcription center, has also been proposed
for polyploid plants [39].
Contribution of homologous
recombination to pairing
Formation of DSBs of DNA is essential for the subse-
quent recombination of homologous chromosomes. In
meiosis, DSBs of DNA are deliberately generated and
healed by recombination between homologous chro-
mosomes. On the other hand, pairing and synapsis of
homologous chromosomes can be achieved through
DSB-dependent or DSB-independent mechanisms.
DSB-dependent pairing has been best investigated in
the budding yeast S. cerevisiae, and has also been
found in animals and plants. In meiosis, DNA DSBs are
generated by a type II topoisomerase-like specialized
enzyme, Spo11. Spo11 is then removed by the MRX
(Mre11–Rad50–Xrs2) complex, and the 5¢-ends of DNA
breaks are resected to expose 3¢-single-strand tails; a
RecA-type recombinase, Rad51, then binds to the
ssDNA and plays a role in searching for DNA that
shares sequence homology [5,40]. In S. cerevisiae, about
2100 DSB hot spots have been mapped throughout the
genome [41]. It has been proposed that the interactions

between homologous DNAs involved in the process of
homology searching and recombination along the chro-
mosomes allow DSB-dependent pairing to occur [5].
However, even in a mutant lacking Spo11 and other key
factors for DSB formation and recombination of DNA,
some residual levels of pairing still remain, suggesting
that a DSB-independent pairing mechanism may also be
operating in this organism [42–44].
On the other hand, typical DSB-independent pairing
is found in Drosophila and C. elegans. In these organ-
isms, initiation of pairing and synapsis of homologous
chromosomes does not depend on DSB formation and
recombination, but on the presence of some special
chromosomal regions, although the mechanisms are
different. In Drosophila males, sex chromosomes pair
and segregate without recombination or formation of
SCs. A 240 bp repeated sequence within the intergenic
spacers of the rRNA genes acts as a cis-acting X–Y
pairing site, and is responsible for faithful segregation
of X–Y chromosomes [36]. In C elegans, DSBs are not
required for homologous pairing [45], and instead a set
of four zinc finger proteins, each specifically binding
with one or two pairing centers, are essential for pair-
ing and synapsis, as described above. In addition, it
has been demonstrated that centromere heterochroma-
tin plays a role in mediating DSB-independent pairing
in organisms such as Drosophila [46], C. elegans [45],
and Schiz. pombe [16].
Contribution of homologous recombination to pair-
ing may vary among species, depending on the size

Homologous chromosome pairing in meiosis D Q. Ding et al.
568 FEBS Journal 277 (2010) 565–570 ª 2009 The Authors Journal compilation ª 2009 FEBS
and number of chromosomes, the volume of the
nucleus, or the time allowed for pairing. Physical
models based on computational simulation provide
predictions for contributions of such parameters to
the efficiency of homologous chromosome pairing
[47–49].
Perspectives
Although formation of the bouquet arrangement
reduces the spatial distance between homologous
chromosomes, which could promote the pairing pro-
cess, it does not directly drive recognition of homol-
ogous chromosomes. How chromosomes identify
their homologous partners remains to be elucidated.
The diversity of the underlying mechanisms present
in different organisms further increases the complex-
ity of this problem [5,6]. In C. elegans, chromosome-
specific recognition proteins are linked to cytoskeletal
motor proteins to tether homologous chromosomes.
In Schiz. pombe, we recently uncovered a novel phe-
nomenon relating noncoding RNA to homologous
chromosome pairing (D Q. Ding, unpublished
results), implying that transcribed RNA mediates rec-
ognition of the respective DNA regions of homolo-
gous chromosomes. This idea may be supported by
the finding that meiotic recombination hotspots coin-
cide with loci that express noncoding RNA in
Schiz. pombe [50]. It is tempting to speculate that
particular molecular patterns along each chromosome

provide a chromosomal barcode for the recognition
of homologous chromosomes.
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