REVIEW
Meiotic telomeres: a matchmaker for homologous
chromosomes
Yasushi Hiraoka*
Kansai Advanced Research Center, Communications Research Laboratory, 588-2 Iwaoka, Iwaoka-cho, Nishi-ku, Kobe 651-2401, Japan
Telomeres, with their special structures and special schemes of synthesis, are essential for
protecting the ends of eukaryotic linear chromosomes during cell proliferation. In addition to this
basic function, the meiosis-specific functions of telomeres have long been inferred from the
cytological observations of characteristic chromosome configurations in meiotic prophase.
Recent studies in the fission yeast Schizosaccharomyces pombe have provided deeper insights into the
role of meiotic telomeres in the pairing of homologous chromosomes. Here I have summarized
our current understanding of the meiotic behaviour of telomeres in S. pombe, and discuss the role
of telomeres in meiosis.
Introduction
Meiosis is a process of universal importance in
eukaryotic organisms, generating variation in the
heritable haploid genome as a consequence of the
recombination and rearrangement of chromosomes.
The pairing of homologous chromosomes, a prerequisite for homologous recombination, occurs during the
meiotic prophase. During this period, chromosomes
show a characteristic arrangement, generally called a
‘bouquet’ structure, in which they are bundled together
at the telomeres to form a bouquet-like arrangement
(reviewed in Fussel 1987; John 1990). The regular and
widespread formation of the bouquet structure suggests
that meiotic telomeres have functions which are
specifically required for meiotic chromosomal events.
The most striking example of telomere clustering is
observed in the fission yeast Schizosaccharomyces pombe;
in this organism, all telomeres form a single cluster
near the spindle-pole body (SPB; the centrosomeequivalent structure of fungi) during meiotic prophase
(Chikashige et al. 1994, 1997). Evidence that this
telomere clustering is important for homologous
chromosome pairing in S. pombe has been obtained
from several recent studies (Shimanuki et al. 1997;
Cooper et al. 1998; Nimmo et al. 1998). The pairing of
* Correspondence: E-mail: yasushi@crl.go.jp
q Blackwell Science Limited
homologous chromosomes is essential not only for
meiotic chromosomal recombination, but also for the
faithful segregation of homologous chromosomes.
The aim of this review is to summarize our current
understanding of the meiotic behaviour of telomeres
in fission yeast and illustrate the general role of
telomeres in the pairing of homologous chromosomes.
Nuclear architecture during mitosis and
meiosis
Eukaryotic chromosomes are spatially organized within
the nucleus; such nuclear architecture provides a
physical framework for the genetic activities of
chromosomes, and yet this framework is dynamic,
being able to change its functional organization as the
cell moves from one cell cycle stage to another. In the
mitotic interphase, centromeres are confined to a small
region of the nucleus near the centrosome, while
telomeres are positioned at the opposite side of the
nucleus (Fig. 1A). This polarized orientation of
chromosomes (often called the Rabl orientation; Rabl
1885) has been observed in a wide range of organisms,
and is believed to be a relic of the previous anaphase
during which the segregating chromosomes were
pulled to the opposite ends of the dividing cell via
their centromeres, with their telomeres trailing behind
(reviewed in Fussel 1987; John 1990). On the other
Genes to Cells (1998) 3, 405–413
405
Y Hiraoka
Figure 1 Nuclear architecture in mitosis and meiosis. (A) Rabl
orientation of chromosomes in mitotic interphase (Rabl 1885).
(B) The bouquet structure of chromosomes in meiotic prophase
(e.g. Mohr 1916).
hand, in meiotic prophase (Fig. 1B), telomeres are
clustered in a small confinement near the centrosome
(Mohr 1916; Hughes-Schrader 1943; reviewed in
Fussel 1987; John 1990; Therman & Susman 1992;
Dernburg et al. 1995). Thus, reorganization of the
nuclear architecture could take place during meiosis by
a rotation of the nuclear contents or a migration of the
centrosome (Schreiner & Schreiner 1906; Gelei 1921,
Janssens 1924; reviewed in Hughes-Schrader 1943).
However, despite the large body of cytological
observations of meiotic chromosomal events in a wide
range of animals and plants which has accumulated over
the course of this century, the underlying molecular
mechanisms for meiotic nuclear reorganization are still
not well understood. One model organism being
studied is the fission yeast S. pombe. S. pombe, as
illustrated in Fig. 2, shows distinct mitotic and meiotic
configurations of chromosomes (Chikashige et al. 1994,
1997). With their distinct phenotype of telomere
clustering and telomere-led nuclear movement, the
fission yeast is providing a simple and unique experimental system for studying meiotic phenomena and the
role of telomeres in these events.
Search for homologous chromosome
partners
Pairing of homologous chromosomes is a requisite for
meiotic recombination and faithful chromosome segregation. The pairing process is well characterized:
chromosomes search for their homologous partners, the
homologous chromosomes then become spatially
aligned side by side, and finally a synapsis forms
between the homologous chromosomes, stably holding
the pair in register. The process by which the
homologous chromosomes find each other, however,
406
Genes to Cells (1998) 3, 405–413
remains largely unknown. Several models have been
proposed for mechanisms for homologous chromosome
searching; these include a premeiotic alignment of
homologous chromosomes, chance contact of homologous chromosomes, and homologous recombinationinitiated synapsis (Maguire 1984; Loidl 1990; Kleckner
1996; Roeder 1997).
During meiotic prophase, chromosome movement is
required to achieve an alignment of homologous
chromosomes, and any heterologous chromosomes
caught between homologous pairs need to be moved
out of the way. The most extreme example of
chromosome movement can be seen in zygotic meiosis
in fungi in which the fusion of haploid nuclei is
immediately followed by meiosis (Fussel 1987). In this
case, homologous sets of chromosomes remain separate
in their respective haploid nuclei until nuclear fusion;
after fusion, the homologous chromosomes need to
move about within the nucleus in order to align
themselves alongside their homologous partners. This is
best exemplified in the fission yeast S. pombe, in which
the meiotic behaviours of the nucleus has been
examined in living cells (Fig. 3). In the fission yeast,
haploid cells of the opposite mating type conjugate
upon nitrogen starvation and enter meiosis (zygotic
meiosis); alternatively, diploid cells can be directly
induced to undergo meiosis (azygotic meiosis) (Yamamoto et al. 1997). During meiotic prophase both in
zygotic and azygotic meiosis, the whole nucleus
migrates back and forth between the cell poles
continuously for 2–3 h until the first meiotic division
(Chikashige et al. 1994). A model has been proposed
from observations of telomere-led nuclear movement in
S. pombe (Kohli 1994; Ding et al. 1998; Chikashige et al.
1994, 1997); in this model, all of the chromosomes,
both homologous and heterologous, are bundled into a
small confined volume at the telomeres, then the
linearly aligned chromosomes are shuffled around each
other to search for a homologous partner during
oscillatory nuclear movement.
In azygotic meiosis in fungi, a diploid cell directly
enters the meiotic process. Azygotic meiosis resembles
the situation in higher eukaryotes in the sense that
homologous chromosomes are retained within a
diploid nucleus; in a diploid nucleus, homologous
chromosomes may reside in close proximity to each
other prior to meiosis, although the existence of such
premeiotic alignment in many diploid organisms
remains debatable (Fussel 1987). The arrangement of
homologous chromosomes during azygotic meiosis
has been examined in spread preparations of chromosomes in fission yeast: results show that a pair of
q Blackwell Science Limited
Telomeres in meiosis
Figure 2 Nuclear architecture in the fission yeast S. pombe. (A) The genome of fission yeast S. pombe is composed of three
chromosomes. Like those of other eukaryotes, fission yeast chromosomes have telomeric repeats of a short nucleotide sequence; the
telomeric repeat is assigned as 50 -GGTTACA-30 with some variations in the number of G residues (Sugawara & Szostak 1986; reviewed
in Henderson 1995; Hiraoka et al. 1998). Chromosomes I and II share a telomere-adjacent sequence; chromosome III does not have this
telomere-adjacent sequence but instead the telomeric repeats are immediately flanked by repeats of ribosomal RNA genes (Yanagida
et al. 1991). All three chromosomes share the centromeric repetitive sequence (Chikashige et al. 1989). Telomere repeats are indicated by
the red box; centromeres are indicated by the green circle labelled ‘Cen’; the telomere-adjacent sequences are indicated by the yellow
circle labelled ‘Telo’; and the repeats of ribosomal RNA genes are indicated by the light blue circle labelled ‘rRNA’. (B, left panel) The
fission yeast nucleus in mitotic interphase is comprised of two hemispherical compartments, one hemisphere which is rich in RNA (a
nucleolus) and a second hemisphere of chromatin with two protrusions of chromatin extending into the RNA-rich hemisphere
(Yanagida et al. 1986); the protrusions of chromatin embedded in the nucleolus are repeats of ribosomal RNA genes located at both ends
of chromosome III (Uzawa & Yanagida 1992). The three chromosomes of S. pombe are organized within the chromatin hemisphere and
display a polarized configuration of centromeres and telomeres: the centromeres are clustered near the SPB which is located at the side
away from the nucleolus, and telomeres are located proximal to the nucleolus (Funabiki et al. 1993). (B, right panel) In meiotic prophase,
the fission yeast nucleus shows an elongated morphology and is generally referred to as the ‘horse tail’ nucleus because of its shape
(Robinow 1977; Robinow & Hyams 1989). The horse-tail nucleus oscillates between the cell poles; throughout this oscillatory nuclear
movement, the telomeres of all of the chromosomes remain clustered at the SPB located at the leading edge of nuclear movement and
centromeres are trailing behind (Chikashige et al. 1994, 1997). Once meiotic chromosome division starts, chromosomes resume the
mitotic configuration in which centromeres are again associated with the SPB. Reproduced from Chikashige et al. (1997).
homologous chromosomes tends to occupy conjoinal
territory prior to meiosis, and a pairing of homologous
chromosomes is initiated at both the telomere and the
centromere during meiotic prophase (Scherthan et al.
1994). It should be noted, however, that telomere
clustering and telomere-led nuclear movement also
take place during the prophase of azygotic meiosis
(Chikashige et al. 1994). The joint territory occupied
by homologous chromosomes may not be sufficient
q Blackwell Science Limited
for aligning the homologous chromosomes completely
in register, and further shuffling of the chromosomes
may be required.
The dramatic nuclear movement exhibited by S.
pombe has not been observed in any other organism. In
diploid organisms, the nuclear movement, if any, may
not be so striking; one of the rare examples of rotational
movement of chromosomes within a stationary nucleus
occurs in rat spermatocytes (Parvinen & Söderström
Genes to Cells (1998) 3, 405–413
407
Y Hiraoka
Figure 3 Nuclear reorganization during fission yeast meiosis.
Haploid cells of the opposite mating type, hþ and h – , conjugate
upon nitrogen starvation and enter zygotic meiosis. (A) At the
time of induction to meiosis, centromeres form a single cluster
near the SPB and telomeres are separated from the SPB. (B) In
the haploid nuclei of the conjugated zygote, telomeres form a
cluster close to the SPB and centromeres become separated from
the SPB. (C) During nuclear fusion, the telomere is the site of
initial contact between homologous chromosomes. After nuclear
fusion, the entire nucleus and the chromosomes are pulled by the
SPB; the movement distorts the nucleus into the horse-tail shape.
(D) In the oscillating horse-tail nucleus, homologous sets of
chromosomes attain the same orientation of polarized telomerecentromere configuration.
1976). It is likely that most commonly, the shuffling of
chromosomes around the bouquet axis in meiotic
prophase increases the chance of contact between
homologous loci facilitating partner search. Once a
pair of homologous chromosomes becomes spatially
aligned side by side, an intimate physical contact, or
synapsis, can be established between them.
While the bouquet formation is well documented in a
408
Genes to Cells (1998) 3, 405–413
wide range of eukaryotic species, until fairly recently, it
was not known whether the bouquet structure was simply
carried over from the Rabl orientation or whether this
structure formed de novo during meiotic prophase. Two
reports have demonstrated that in mouse, human
(Scherthan et al. 1996) and maize (Bass et al. 1997), the
bouquet structure forms de novo after the cell enters
meiotic prophase and is transient, observable only during
a limited period of meiotic prophase. In S. pombe, it has
been demonstrated that telomere clustering occurs de novo
in response to the mating pheromone (Chikashige et al.
1997). Thus, the universality of directed telomere
movement as the cell moves into meiotic prophase has
been confirmed in such evolutionarily distant organisms
as fission yeast, higher plants and mammals, supporting a
model in which telomere movement is a fundamental
aspect of meiosis, most likely being involved in homologous chromosome pairing via telomere-led nuclear
movement in S. pombe, and by bouquet formation in most
other eukaryotes.
In the budding yeast Saccharomyces cerevisiae, there is
actually no direct cytological evidence that telomere
movement is involved in meiosis: in this organism,
telomeres do not form a single cluster at any stage of
mitosis or meiosis, but instead form multiple clusters
near the nuclear membrane throughout the process of
meiosis (Hayashi et al. 1998). However, mutation of the
tam1/ndj1 protein, a meiosis-specific telomere-binding
protein, affects chromosome synapsis in meiosis (Chua
& Roeder 1997; Conrad et al. 1997), suggesting that in
budding yeast also, telomeres are involved in meiotic
events.
Cytological observation of the centromeres in S.
cerevisiae, unlike that of the telomeres, has shown that
the centromeres undergo a dramatic repositioning as the
cell enters meiotic prophase: interphase centromeres are
clustered at the SPB, but become scattered within the
nucleus in meiotic prophase (Jin et al. 1998; Hayashi
et al. 1998). This situation is reminiscent of the
separation of centromeres from the SPB which has
been observed in S. pombe meiosis (Chikashige et al.
1994, 1997). The functional significance of centromere
repositioning is not currently known, however, considerable chromosome movement is indicated.
Driving forces for homologous
chromosome pairing
Cytological studies, mostly in higher plants, have shown
that homologous chromosome synapsis is affected in
pollen mother cells treated with a microtubule polymerization inhibitor, colchicine (reviewed in Fussel
q Blackwell Science Limited
Telomeres in meiosis
that microtubules are involved in homologous chromosome searching but not in synapsis formation.
In the fission yeast, dramatic reorganization of
microtubules takes place during meiosis. In mitotic
interphase, arrays of cytoplasmic microtubules extend
along the length of the cell, but astral microtubules
radiating from the SPB are absent (Hagan & Hyams
1988). When fission yeast cells are induced to undergo
meiosis, the microtubules change their organization and
originate exclusively from the SPB (Hagan & Yanagida
1995; Svoboda et al. 1995; Ding et al. 1998). Thus, the
SPB acquires microtubule-nucleating activity upon
entering meiosis. It has been demonstrated that
telomere-led oscillatory nuclear movement is mediated
by astral microtubules radiating from the SPB (Ding et al.
1998). Therefore, in both wheat and fission yeast,
microtubules are implicated in the process of homologous chromosome searching. Because telomeres are
attached to the nuclear membrane in many organisms
(reviewed in Dernburg et al. 1995), it may be possible
that telomeres interact with microtubules via telomerebinding nuclear membrane components. The driving
forces that actually induce the clustering of the
telomeres, however, have not yet been identified;
there is no direct evidence that telomere clustering is
driven by microtubules in fission yeast.
The role of telomeres in homologous
chromosome pairing
Figure 4 Nuclear location of centromeres and telomeres in
mutants. Position of centromeres and telomeres in a horse-tail
nucleus in a wild-type cell (A); kms1 mutant (B); taz1 and lot2
mutants (C). In the kms1 mutant, the smaller squares represent
fragments of the SPB as detected by anti-sad1 antibody
(Shimanuki et al. 1997; also see Fig. 5).
1987). An interesting implication for the involvement
of microtubules in homologous chromosome searching
has been obtained from experiments in wheat pollen
mother cells bearing an isochromosome. An isochromosome is a metacentric chromosome composed of
two homologous chromosome arms joined to a
common centromere; during the meiotic prophase,
the homologous arms of an isochromosome are paired
to each other. Colchicine inhibits the formation of
synapsis in ordinary homologous chromosomes, but not
in an isochromosome (Driscoll & Darvey 1970). Since
the homologous arms of an isochromosome are relieved
from searching for pairing partners, these results suggest
q Blackwell Science Limited
Insights into the molecular role of telomeres in meiosis
have so far been provided only in the fission yeast S.
pombe. In higher eukaryotes, while cytological evidence
supports the role of telomeres in meiosis, the requirement of telomeric function for meiotic processes has
not been demonstrated at the molecular level.
In fission yeast, the role of telomeres in aligning
homologous chromosomes has been indicated by
studies on the localizations of an artificial linear
minichromosome in the nucleus. The minichromosome contains an < 400 kbp centromeric portion of
chromosome III directly flanked by telomeric repeats
(Matsumoto et al. 1987; Niwa et al. 1989). In the
meiotic prophase nucleus, the minichromosome is
aligned with authentic telomeres and separated from
authentic centromeres, indicating that telomere clustering, rather than DNA sequence homology, is a
predominant step in aligning homologous chromosomes (Chikashige et al. 1997). These results also show
that the telomeric repeats of 50 -GGTTACA-30 at the
very ends of a chromosome—since they are the only
sequences shared by the ends of the three authentic
Genes to Cells (1998) 3, 405–413
409
Y Hiraoka
chromosomes and the minichromosome—are sufficient to induce telomere clustering in meiotic prophase.
More recently, it has been reported that the pairing
of homologous chromosomes is impaired in several
mutants that are defective in telomere clustering at the
SPB (Fig. 4). The kms1 mutant fails to form a
telomere cluster due to the disintegration of the SPB
structure; intriguingly, a kms1 mutant strain exhibited
a reduced rate of meiotic recombination (Shimanuki
et al. 1997). The taz1 protein was identified as a
telomere-binding protein in S. pombe (Cooper et al.
1997); in the taz1 mutant, telomeres fail to connect to
the SPB in meiotic prophase, and in this mutant,
recombination frequency is markedly reduced, indicating improper pairing of homologous chromosomes
(Cooper et al. 1998). The lot2 mutant affects telomere
length and transcriptional silencing at the telomere;
here also, telomeres fail to cluster at the SPB in
meiotic prophase and, similarly to the taz1 mutant,
recombination frequency is markedly reduced
(Nimmo et al. 1998). In addition, a mutant in the
dynein heavy chain (designated dhc1), in which
meiotic prophase nuclear movement is impaired,
also exhibited a phenotype of reduced meiotic
recombination frequency and improper positioning
of homologous loci (A. Yamamoto, R.R. West, J.R.
McIntosh & Y. Hiraoka, manuscript in preparation).
Taken together, these results strongly support the idea
that telomere clustering at the SPB and telomere-led
nuclear movement are necessary for the proper
pairing of homologous chromosomes.
It should be pointed out that while recombination is
reduced by about 2–10-fold, a significant level of
recombination is retained in all of the above mentioned
mutants, kms1, taz1, lot2 and dhc1. In these cells,
homologous loci can presumably align, at a low level of
efficiency, by chance contact even without telomere-led
nuclear movement; recombination then takes place
because the molecular machines required for recombination are operative.
Do the ends justify the means?’
When the special scheme of telomere synthesis was
first worked out, researchers thought that ‘the ends
justified the means’ (Blackburn 1984). We have just
begun asking again whether ‘the ends justify the
means’ in meiosis. A universal goal of meiosis is to
produce recombined sets of haploid genomes to be
inherited by the parent’s offspring. Present-day
organisms have evolved diverse strategies to ensure
proper pairing, recombination and segregation of
410
Genes to Cells (1998) 3, 405–413
homologous chromosomes. Search and pairing of
homologous chromosomes is a mechanistic process,
and strategies for homologous partner search may
depend on mechanistic systems which may be diverse
among species.
The oscillatory movement of an entire nucleus has
not been observed in any organisms other than S.
pombe. S. pombe appears to rely primarily on a chance
contact between telomere-aligned homologous chromosomes, this chance being increased by the telomere-led chromosome movement. This choice of
strategy may be related to one or more mechanistic
features in S. pombe: this organism has a small number
of chromosomes, exists primarily in the haploid state,
and meiosis is predominantly zygotic (Yamamoto et al.
1997); unlike many other organisms, chromosomes in
S. pombe show no detectable chromosome condensation during meiotic prophase (Chikashige et al. 1994;
Scherthan et al. 1994); and S. pombe chromosomes do
not form the typical tripartite structure of the
synaptonemal complex (SC), although linear elements
resembling axial elements of the SC are formed (Olson
et al. 1978; Bähler et al. 1993; Scherthan et al. 1994).
Lack of the SC, together with lack of chromosome
condensation, results in a flexible chromosome
structure, and the highly mobile meiotic prophase
chromosomes may be reflective of this condition. S.
pombe may thus have evolved a strategy of telomere-led
nuclear movement for homologous chromosome
searching due to—perhaps to compensate for—the
lack of a stable SC structure.
S. cerevisiae has provided a different view of homologous chromosome pairing. This organism, unlike S.
pombe, exists primarily in the diploid state, and thus
meiosis is routinely azygotic (Kupiec et al. 1997).
During azygotic meiosis in this organism, it has been
suggested that initial pairing of homologous loci occurs
prior to meiotic S phase and results in the colocalization of homologous chromosomes to conjoined
areas, the pairing interactions are disrupted as the cell
replicates its DNA but are re-established and stabilized
during meiotic prophase (Weiner & Kleckner 1994;
Kleckner 1996).
Higher eukaryotes, bearing a large number of
chromosomes within a diploid nucleus, may have
evolved different strategies from those in fungi (Loidl
1990; Roeder 1997; McKim et al. 1998). Nevertheless,
considering the universality of the mitotic Rabl
orientation and the meiotic bouquet structure, it is
likely that, in general, telomere clustering is important
in facilitating homologous chromosome searching by
increasing the chance of contact between homologous
q Blackwell Science Limited
Telomeres in meiosis
Figure 5 Meiotic telomere-SPB complex in fission yeast. The meiotic SPB acts as a nucleation centre of astral microtubules; these astral
microtubules mediate oscillatory nuclear movement during meiotic prophase (Ding et al. 1998). Only a small number of components
have been identified in the meiotic telomere–SPB complex in fission yeast. The sad1 protein was identified as a constitutive SPB
component which is essential for mitotic growth (Hagan & Yanagida 1995). The kms1 protein is another constitutive component of the
SPB (Shimanuki & Niwa, personal communication); the kms1 protein is nonessential in mitotic growth, and functions specifically in the
progression of meiosis (Shimanuki et al. 1997). The S. pombe telomeric repeat is assigned as 50 -GGTTACA-30 (Sugawara & Szostak
1986; reviewed in Henderson 1995; Hiraoka et al. 1998). The taz1 protein is a constitutive telomere binding protein that specifically
binds to the S. pombe telomeric repeat (Cooper et al. 1997).
loci of chromosomes that are aligned in a defined spatial
orientation.
Our current understanding of the meiotic telomere–
SPB complex in the fission yeast is summarized in Fig.
5. Meiosis-specific components or modification of
constitutive components that bring telomeres to the
SPB remain to be identified in the telomere, the SPB, or
nuclear membrane. Because telomeric repeats are well
conserved among species (Henderson 1995; Hiraoka
et al. 1998) and telomere binding proteins, taz1 in fission
yeast, Rap1 in budding yeast, and TRF1 in mammals,
share a structural motif (Cooper et al. 1997; König &
Rhodes 1997; van Steensel & de Lange 1997), we may
expect that molecular machines for telomere-mediated
search for homologous chromosomes are mechanistically conserved in eukaryotes. Further molecular and
structural studies of chromosome ends—their activities,
their clustering, the consequences of their justification—in diverse organisms will lead to a better
understanding of universal means by which eukaryotes
accomplish meiosis.
Acknowledgements
The author would like to thank Mizuki Shimanuki and Osami
Niwa for communicating their observations prior to publication;
q Blackwell Science Limited
and David Alexander, Tokuko Haraguchi and Hubert Renauld
for a critical reading of the manuscript.
References
Bähler, J., Wyler, T., Loidl, J. & Kohli, J. (1993) Unusual nuclear
structures in meiotic prophase of fission yeast: a cytological
analysis. J. Cell. Biol. 121, 241–256.
Bass, H.W., Marshall, W.F., Sedat, J.W., Agard, D.A. & Cande,
W.Z. (1997) Telomeres cluster de novo before the initiation of
synapsis: a three-dimensional spatial analysis of telomere
positions before and during meiotic prophase. J. Cell. Biol.
137, 5–18.
Blackburn, E.H. (1984) Telomeres: do the ends justify the
means? Cell 37, 7–8.
Chikashige, Y., Ding, D.Q., Funabiki, H., et al. (1994) Telomereled premeiotic chromosome movement in fission yeast. Science
264, 270–273.
Chikashige, Y., Ding, D.-Q., Imai, Y., Yamamoto, M.,
Haraguchi, T. & Hiraoka, Y. (1997) Meiotic nuclear
reorganization: switching the position of centromeres and
telomeres in fission yeast Schizosaccharomyces pombe. EMBO J.
16, 193–202.
Chikashige, Y., Kinoshita, N., Nakaseko, Y., et al. (1989)
Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites.
Cell 57, 739–751.
Chua, P.R. & Roeder, G.S. (1997) Tam1, a telomere-associated
meiotic protein, functions in chromosome synapsis and
crossover interference. Genes Dev. 11, 1786–1800.
Genes to Cells (1998) 3, 405–413
411
Y Hiraoka
Conrad, M.N., Dominguez, A.M. & Dresser, M.E. (1997) Ndj1,
a meiotic telomere protein required for normal chromosome
synapsis and segregation in yeast. Science 276, 1252–1255.
Cooper, J.P., Nimmo, E.R., Allshire, R.C. & Cech, T.R. (1997)
Regulation of telomere length and function by a Myb-domain
protein in fission yeast. Nature 385, 744–747.
Cooper, J.P., Watanabe, Y. & Nurse, P. (1998) Fission yeast Taz1
protein is required for meiotic telomere clustering and
recombination. Nature 392, 828–831.
Dernburg, A.F., Sedat, J.W., Cande, W.Z. & Bass, H.W. (1995)
Cytology of telomeres. In: Telomeres (eds E.H. Blackburn &
C.W. Greider), pp. 295–338. Cold Spring Harbor, New York:
Cold Spring Harbor Laboratory Press.
Ding, D.-Q., Chikashige, Y., Haraguchi, T. & Hiraoka, Y. (1998)
Oscillatory nuclear movement in fission yeast meiotic
prophase is driven by astral microtubules as revealed by
continuous observation of chromosomes and microtubules in
living cells. J. Cell Sci. 111, 701–712.
Driscoll, C.J. & Darvey, N.L. (1970) Chromosome pairing: effect
of colchicine on an isochromosome. Science 169, 290–291.
Funabiki, H., Hagan, I.M., Uzawa, S. & Yanagida, M. (1993)
Cell cycle-dependent specific positioning and clustering of
centromeres and telomeres in fission yeast. J. Cell. Biol. 121,
961–976.
Fussel, C.P. (1987) The Rabl orientation: a prelude to synapsis.
In: Meiosis (ed. P.B. Moens), pp. 275–299. San Diego, CA:
Academic Press.
Gelei, J. (1921) Weitere Studien über die Oogenese des
Dedrocoelum lacteum. II Die Längskonjugation der Chromosomen. Arch. Zellforsch. 16, 88–169.
Hagan, I.M. & Hyams, J.S. (1988) The use of cell division cycle
mutants to investigate the control. of microtubule distribution
in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 89,
343–357.
Hagan, I. & Yanagida, M. (1995) The product of the spindle
formation gene sad1þ associates with the fission yeast spindle
pole body and is essential for viability. J. Cell. Biol. 129, 1033–
1047.
Hayashi, A., Ogawa, H., Kohno, K., Gasser, S.M. & Hiraoka, H.
(1998) Meiotic behaviours of chromosomes and microtubules
in budding yeast: relocalization of centromeres and telomeres
during meiotic prophase. Genes Cells, in press.
Henderson, E. (1995) Telomere DNA structure. In: Telomeres
(eds E.H. Blackburn & C.W. Greider), pp. 11–34. Cold
Spring Harbor, New York: Cold Spring Harbor Laboratory
Press.
Hiraoka, Y., Henderson, E. & Blackburn, E.H. (1998) Not so
peculiar: fission yeast telomere repeats. Trends Biochem. Sci. 23,
126.
Hughes-Schrader, S. (1943) Polarization, kinetochore movements, and bivalent structure in the meiosis of male mantids.
Biol. Bull. Woods Hole 85, 265–300.
Janssens, F.A. (1924) La chiasmatypie dans les insectes. La Cellule
34, 134–359.
Jin, Q., Trelles-Sticken, E., Scherthan, H. & Loidl, J. (1998) Yeast
nuclei display prominent centromere clustering that is reduced
in nondividing cells and in meiotic prophase. J. Cell. Biol. 41,
21–29.
John, B. (1990) Meiosis. Cambridge, UK: Cambridge University
Press.
Kleckner, N. (1996) Meiosis: how could it work.? Proc. Natl.
Acad. Sci. USA 6, 8167–8174.
412
Genes to Cells (1998) 3, 405–413
Kohli, J. (1994) Meiosis. Telomeres lead chromosome movement. Curr. Biol. 1, 724–727.
König, P. & Rhodes, D. (1997) Recognition of telomeric DNA.
Trends Biochem. Sci. 22, 43–47.
Kupiec, M., Byers, B., Esposito, R.E. & Mitchell, A.P. (1997)
Meiosis and sporulation in Saccharomyces cerevisiae. In: The
Molecular and Cellular Biology of the Yeast Saccharomyces, Vol. 3.
Cell Cycle and Cell Biology (eds J. R. Pringle, J.R. Broach &
E.W. Jones), pp. 889–1036. Cold Spring Harbor, New York:
Cold Spring Harbor Laboratory Press.
Loidl, J. (1990) The initiation of meiotic chromosome pairing:
the cytological view. Genome 33, 759–778.
Maguire, M.P. (1984) The mechanism of meiotic homologue
pairing. J. Theor. Biol. 106, 605–615.
Matsumoto, T., Fukui, K., Niwa, O., Sugawara, N., Szostak, J.W.
& Yanagida, M. (1987) Identification of healed terminal DNA
fragments in linear minichromosomes of Schizosaccharomyces
pombe. Mol. Cell. Biol. 7, 4424–4430.
McKim, K., Green-Marroquin, B.L., Sekelsky, J.J., et al. (1998)
Meiotic synapsis in the absence of recombination. Science 279,
876–878.
Mohr, O.L. (1916) Studien über die Chromatinreifung der
männlichen Geschlechtszellen bei Locusta viridissima. Arch.
Biol. 29, 579–752.
Nimmo, E.R., Pidoux, A.L., Perry, P.E. & Allshire, R.C. (1998)
Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 23, 825–8.
Niwa, O., Matsumoto, T., Chikashige, Y. & Yanagida, M. (1989)
Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their
centromere. EMBO J. 8, 3045–3052.
Olson, L.W., Eden, U., Egel-Mitani, M. & Egel, R. (1978)
Asynaptic meiosis in fission yeast? Hereditas 89, 189–199.
Parvinen, M. & Söderström, K.O. (1976) Chromosome rotation
and formation of synapsis. Nature 260, 534–535.
Rabl, C. (1885) Über zelltheilung. Morph. Jahrb. 10, 214–330.
Robinow, C.F. (1977) The number of chromosomes in
Schizosaccharomyces pombe: light microscopy of stained preparations. Genetics 87, 491–197.
Robinow, C.F. & Hyams, J.S. (1989) General cytology of fission
yeasts. In: Molecular Biology of the Fission Yeast. (eds A. Nasim, P.
Young & B. Johnson), pp. 273–330. San Diego, CA:
Academic Press.
Roeder, G.S. (1997) Meiotic chromosomes: it takes two to
tango. Genes Dev. 11, 2600–2621.
Scherthan, H., Bähler, J. & Kohli, J. (1994) Dynamics of
chromosome organization and pairing during meiotic prophase in fission yeast. J. Cell. Biol. 127, 273–285.
Scherthan, H., Weich, S., Schwegler, H., Heyting, C., Harle, M.
& Cremer, T. (1996) Centromere and telomere movements
during early meiotic prophase of mouse and man are associated
with the onset of chromosome pairing. J. Cell. Biol. 134,
1109–1125.
Schreiner, A. & Schreiner, K.E. (1906) Über die Entwickelung
der männlichen Geschlechtszellen von Myxine glutonisa. II.
Die Centriolen und ihre Vermehrungsweise. Arch. Biol. 21,
183–314.
Shimanuki, M., Miki, F., Ding, D.Q., et al. (1997) A novel fission
yeast gene, kms1þ, is required for the formation of meiotic
prophase-specific nuclear architecture. Mol. Gen. Genet. 254,
238–249.
van Steensel, B. & de Lange, T. (1997) Control. of telomere
q Blackwell Science Limited
Telomeres in meiosis
length by the human telomeric protein TRF1. Nature 385,
740–743.
Sugawara, N. & Szostak, J.W. (1986) Telomeres of Schizosaccharomyces pombe. Yeast 2(Suppl.), S372.
Svoboda, A., Bähler, J. & Kohli, J. (1995) Microtubuledriven nuclear movements and linear elements as meiosisspecific characteristics of the fission yeasts Schizosaccharomyces
versatilis and Schizosaccharomyces pombe. Chromosoma 104, 203–
214.
Therman, E. & Susman, M. (1992) Human Chromosomes. Berlin:
Spinger-Verlag.
Uzawa, S. & Yanagida, M. (1992) Visualization of centromeric
and nucleolar DNA in fission yeast by fluorescence in situ
hybridization. J. Cell Sci. 101, 267–275.
Weiner, B.M. & Kleckner, N. (1994) Chromosome pairing via
multiple interstitial interactions before and during meiosis in
yeast. Cell 77, 977–991.
q Blackwell Science Limited
Yamamoto, M., Imai, Y. & Watanabe, Y. (1997) Mating and
sporulation in Schizosaccaromyces pombe. In: The Molecular
and Cellular Biology of the Yeast Saccharomyces, Vol. 3. Cell Cycle
and Cell Biology (eds J.R. Pringle, J.R. Broach & E.W. Jones),
pp. 1037–1106. Cold Spring Harbor, New York: Cold Spring
Harbor Laboratory Press.
Yanagida, M., Morikawa, K., Hiraoka, Y., Matsumoto, S.,
Uemura, T. & Okada, S. (1986) Video-connected fluorescence microscopy of large DNA molecules, chromatin, and
chromosomes. In: Applications of Fluorescence in the Biomedical
Sciences (ed. D.L. Taylor), pp. 321–345. New York, NY: Alan
R. Liss, Inc.
Yanagida, M., Niwa, O., Chikashige, Y., et al. (1991) Genome
analysis of Schizosaccharomyces pombe. In: Control of Cell Growth
and Division (eds A. Ishikawa & H. Yoshikawa), pp. 255–262.
Tokyo: Japan Science Society Press, and Berlin: SpringerVerlag.
Genes to Cells (1998) 3, 405–413
413