1 School of Biosciences, The University of Birmingham, Birmingham, B15 2TT,
UK
2 Institut National de la Recherche Agronomique, Station de
Génétique et d'Amélioration des Plantes, Route de
Saint-Cyr, 78026 Versailles, cedex, France
3 Department of Chemistry and Biochemistry, Miami University, Oxford, OH 45056,
USA
* Author for correspondence (e-mail: rmercier{at}versailles.inra.fr and F.C.H.Franklin{at}bham.ac.uk)
Accepted 15 April 2003
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SUMMARY |
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Key words: Meiosis, Recombination, Synaptonemal complex, Sister chromatid cohesion
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INTRODUCTION |
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The process of meiosis involves two rounds of chromosome segregation that
follow a single round of chromosome duplication leading to the production of
haploid gametes. Accurate segregation of chromosomes during meiosis is
essential for the long-term survival of individual species, since any error
may produce infertility or aneuploid offspring. During meiotic prophase I
several crucial events contribute to and determine the subsequent correct
partition of genetic material. One of these is the juxtaposition of homologous
chromosomes during early prophase I to form bivalents. This process commences
at leptotene or in some cases meiotic interphase with the alignment of
homologous chromosomes, a phenomenon called pairing (review by
Zickler and Kleckner, 1998).
During leptotene, each chromosome develops a linear proteinaceous structure
called an axial element (AE). In the following zygotene stage, the homologues
closely associate via the polymerization of a central element between the two
homologous AEs, which are then referred to as lateral elements. This
tripartite structure forms the synaptonemal complex (SC). The polymerization
of the SC, or synapsis, continues throughout zygotene until pachytene at which
stage it is complete. The SC is then disassembled during diplotene (reviewed
by Heyting, 1996
;
Roeder, 1997
;
Zickler and Kleckner,
1999
).
To ensure accurate chromosome segregation at anaphase I each homologue must
remain connected to the other until metaphase I. Since the SC disappears
before the end of prophase I, it cannot directly contribute to the links
between homologues beyond this point. Beyond pachytene inter-homologue
connection is maintained by chiasmata, which are the cytological manifestation
of genetic crossover events, in association with sister-chromatid cohesion.
Cross-overs are the result of homologous recombination, a process that is
initiated at leptotene, by DNA double strand breaks, and is completed by
diplotene (Hunter and Kleckner,
2001; Mahadevaiah et al.,
2001
) (for a review, see Smith
and Nicolas, 1998
).
The chiasmata are finally released at anaphase I when the sister chromatid
cohesion, established earlier in meiotic S phase, is lost along chromosome
arms. As a result the homologues are able to segregate to opposite poles of
the anaphase I cell. Sister chromatid cohesion is therefore another key
element in ensuring accurate chromosome segregation. Release of chromosome arm
cohesion is the first in a two-step process, since cohesion continues to be
maintained at centromeres, thereby ensuring that the sister chromatids remain
associated until metaphase II. At this point centromere cohesion is also lost
enabling the second meiotic division to occur at anaphase II. Cohesion is
dependent on the activity of the evolutionarily conserved cohesin complex
(reviewed by Nasmyth, 2001).
Together these processes facilitate chromosome segregation, although many
aspects of their interdependency remain unresolved (reviewed by
Kleckner, 1996
;
Nasmyth, 2001
;
Roeder, 1997
;
van Heemst and Heyting, 2000
;
Zickler and Kleckner,
1999
).
In plants, relatively few molecular components associated with these
meiotic processes have been identified, although there has been recent
progress in A. thaliana (Bhatt et
al., 2001; Caryl et al.,
2003
; Mercier et al.,
2001a
). To date, ASY1 is the only known plant protein that is
associated with the SC. This protein is required for synapsis and localizes
along lateral elements (Armstrong et al.,
2002
; Caryl et al.,
2000
; Ross et al.,
1997
). It shows limited similarity to the yeast meiotic gene
Hop1 (Hollingsworth et al.,
1990
; Smith and Roeder,
1997
), although it has a slightly different spatial and temporal
distribution. Five genes required for the catalytic steps of recombination
have been described in Arabidopsis, namely RAD50, MRE11, RAD51,
DMC1 and SPO11. These five genes show strong evolutionary
conservation with their counterparts from other species
(Bundock and Hooykaas, 2002
;
Couteau et al., 1999
;
Doutriaux et al., 1998
;
Gallego et al., 2001
;
Grelon et al., 2001
). One
Arabidopsis protein (SYN1/DIF1) has been proposed to have a role in
sister chromatid cohesion (Bai et al.,
1999
; Bhatt et al.,
2001
). This protein exhibits sequence similarity to the Scc1/Rec8
cohesin family. The observation of meiotic chromosome fragmentation in
syn1/dif1 mutants is also consistent with a functional similarity to
Rec8, since the latter is required for double strand break repair during
meiotic recombination (Klein et al.,
1999
). Nevertheless, the role of SYN1/DIF1 in sister chromatid
cohesion has not yet been confirmed. Finally, a cyclin-like protein has been
shown to be involved in synapsis and recombination
(Azumi et al., 2002
).
We previously reported the isolation of the Arabidopsis SWI1 gene
[also known as DYAD (Agashe et
al., 2002)] that is required for completion of meiosis
(Mercier et al., 2001b
). This
gene does not show significant similarity to any known genes, proteins or
genomic sequences from other species. The swi1-2 mutation results in
a lack of bivalent formation and precocious loss of sister chromatid cohesion
during male meiosis. This leads to the presence of 20 chromatids instead of 5
bivalents at metaphase I. The swi1-2 mutant exhibits the most extreme
phenotype from four alleles so far described
(Agashe et al., 2002
;
Cai and Makaroff, 2001
;
Motamayor et al., 2000
),
suggesting it is a null allele. This initial study led us to propose that
SWI1 is required for the establishment of sister chromatid cohesion
(Mercier et al., 2001b
).
We have now carried out a detailed study of SWI1 function using a combination of genetic analysis and immunocytochemistry. Our data clearly establish a pivotal role for SWI1 during early meiosis. We demonstrate by immunolocalization coupled with BrdU incorporation experiments that SWI1 is expressed exclusively in meiotic G1 and S phase. Examination of swi1-2 mutant male meiocytes reveals that in addition to synapsis and cohesion defects, axial elements do not assemble, although other axis-associated proteins are present, and recombination is probably not initiated. The central role of SWI1 and the dependence between sister chromatid cohesion, axial element formation, synapsis and recombination are discussed.
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MATERIALS AND METHODS |
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Antibodies
The ASY1 polyclonal antibody used in this study was described by Armstrong
et al. (Armstrong et al.,
2002). It was used at a dilution of 1:500.
The full-length coding region of RAD51 from A. thaliana was cloned
into the protein expression vector pET21b (Novagen) as an N terminus fusion to
a HIS tag. Upon induction, the HIS-AtRAD51 fusion accumulated as insoluble
inclusion bodies in E. coli BL21 DE3 (Novagen). Purified, refolded
recombinant protein was prepared as described previously
(Kakeda et al., 1998) and used
to produce a rabbit polyclonal antiserum (ISL, Poole, UK). The working
dilution was 1:500.
The SWI1 sequence SPFPVKPLAAKRPLG was synthesized as a multiple antigenic peptide (www.bham.ac.uk/Alta_Bioscience) and used to produce a rabbit polyclonal antiserum (ISL, Poole, UK). The working dilution was 1:400. Immunolocalization in swi1-2 mutant was used as control.
The SYN1 antibody was raised against a polypeptide derived from amino acid
residues 178-353 of the protein (Cai et
al., 2003). The working dilution was 1:500.
Cytological procedures
Spreads and immunofluorescence light microscope analyses were performed as
described previously (Armstrong et al.,
2002). The pre-immune serum was used as a negative control.
The procedure for silver staining chromosome spreads was described by
Armstrong et al. (Armstrong et al.,
2001). Bromodeoxyuridine (BrdU) pulses were performed and detected
using an anti-BrdU kit (Roche) as described previously
(Armstrong et al., 2001
).
Spreads and double immunodetection of BrdU and SWI1 were performed as for
other immunolocalization (see above) using the following antibody incubations:
rabbit anti-SWI1, 4°C overnight; biotin-conjugated anti-rabbit IgG
(Sigma), 37°C for 45 minutes; mouse anti-BrdU (Roche), 37°C for 30
minutes; Cy3-conjugated streptavidin (Cambio) 37°C for 30 minutes, FITC
anti-mouse IgG (Roche), 37°C for 30 minutes, with 3x 5 minutes
phosphate-buffered saline washes between each step.
Slides were examined using a Nikon Eclipse T300 microscope. Image capture was achieved using an image analysis system (Smart capture 2, Digital Scientific, UK). Figures were prepared using Adobe PhotoShop 6.0.
Double mutant isolation
Heterozygous swi1-2 and dif1-1 mutant plants were crossed
and double heterozygotes were identified in the F1 generation.
Double homozygotes were then identified in the self-fertilized offspring of
these F1 plants by PCR genotyping individual plants using
diagnostic primer sets. Homozygous swi1-2 plants were identified
using CAPS markers previously described by Mercier et al.
(Mercier et al., 2001b).
Plants that were also homozygous for dif-1 were identified using
primers flanking the dif1-1 Ac element insertion site
(5'-TGATCTTCGCGTGCAATGTAGC-3' and
5'-GCCGATGCGAACTTCAATGG-3') in combination with an Ac element
primer (5'-ATACGATAACGGTCGGTAC-3'), which produce different
profiles on +/+, dif1-1/+ and dif1-1/dif1-1 genotypes.
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RESULTS |
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DISCUSSION |
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The lack of chiasmata between the univalents that are transiently present
in swi1-2 (Mercier et al.,
2001b) (see also Fig.
1H, Fig. 2G,
Fig. 4D) implies that genetic
crossing-over (CO) does not occur in the swi1-2 mutant. Together with
the lack of any detectable chromosome fragmentation this suggests that DSBs
that initiate recombination are not produced in the mutant. Our analysis of an
Arabidopsis line homozygous for both swi1-2 and
dif1-1 mutations concurs with this hypothesis. The dif1-1
mutation results in extensive chromosome fragmentation during meiosis
(Bhatt et al., 1999
) (see also
Fig. 5A). The fragmentation
phenotype is suppressed by a spo11 mutation, indicating that the
dif1-1 phenotype is due to a failure in the repair of SPO11-mediated
DSBs (Anuj Bhatt and Mathilde Grelon, personal communication). We showed that
the swi1-2 mutation also suppressed the dif1-1 fragmentation
phenotype, further indicating that swi1-2 mutation impairs
recombination initiation. Nevertheless, it is also possible that in a
swi1-2 background DSBs are produced and are repaired via some
alternative pathway such as gene conversion during a transient interaction
between the homologues or recombination between the sister chromatids prior to
their separation. However, our analysis of the behavior of RAD51 in the
swi1-2 mutant provides evidence against these alternative
possibilities. Rad51 is an evolutionarily conserved protein essential for DSB
repair by homologous recombination regardless of whether the template is the
sister chromatid or the homologous chromosome (review by
Masson and West, 2001
). In
contrast to wild-type meiocytes, no RAD51 foci were detected on
swi1-2 chromosomes during meiotic prophase. This finding is
consistent with a failure of swi1-2 to initiate recombination.
On the basis these experiments it seems that SWI1 has a pivotal role in meiotic chromosome function, as it appears to be required for sister chromatid cohesion, axial element formation and recombination.
How are the functions of SWI1 in sister cohesion, axial element
formation and recombination inter-related?
In this study we have shown that SWI1 is expressed at an early stage in
meiosis. It is first detectable in G1, remains present in S phase
and disappears probably as soon as S phase finishes. On the basis of this
expression pattern we propose that the primary defect of swi1-2 is a
lack of cohesion initiation [already suggested by Mercier et al.
(Mercier et al., 2001b)].
Considerable data, mainly from yeast, suggest a mechanism whereby cohesion is
established during mitotic or meiotic S phase, when the two sister chromatids
originate (reviewed by Nasmyth,
2001
). For example, a delay in expression of the cohesin sub-unit
Scc1 after the mitotic S phase leads to a lack of cohesion in budding yeast
(Uhlmann and Nasmyth, 1998
).
Schizosaccharomyces pombe cells that undergo a meiosis after having
performed a mitotic S-phase have the same phenotype as the rec8
mutant, showing that the meiosis-specific cohesion system is built as early as
S-phase (Watanabe et al.,
2001
). Some proteins, called adherins, have been isolated, that
are required for the loading of cohesins at G1 stage
(Ciosk et al., 2000
;
Furuya et al., 1998
) while
others directly link replication and cohesion establishment (review by
Carson and Christman, 2001
).
These proteins have a mitotic role and are thought to have a similar meiotic
function, although thus far, this has been formally demonstrated only for the
Coprinus cinereus adherin Rad9
(Cummings et al., 2002
). At
present, SWI1 is the only protein to be described that is involved
specifically in meiotic sister chromatid cohesion establishment. Moreover,
detection of the SWI1 protein prior to meiotic S phase places it as the
earliest acting meiotic protein described to date in plants. Hence, it seems
possible that it may prove to be a key target for the as yet unknown factors
that specify this developmental pathway.
The swi1-2 defect in axial element formation and as a consequence
the lack of SC, is probably a secondary defect of the sister chromatid
cohesion defect, particularly as SWI1 is no longer detectable by the time the
AE begins to form in leptotene. In a variety of species, AE formation is
dependent on the previous establishment of sister chromatid cohesion (reviewed
by van Heemst and Heyting,
2000): the cohesin mutants rec8 and smc3 from
Saccharomyces cerevisiae, and rec8 from Caenorhabditis
elegans do not form AEs (Klein et
al., 1999
; Pasierbek et al.,
2001
). The Sordaria macrospora spo76-1 mutant also
exhibits a meiotic cohesion defect that results in abnormal and partially
split AEs (van Heemst et al.,
1999
). Similarly, the fission yeast rec8 mutant does not
form a linear element, an AE-like structure
(Molnar et al., 1995
). All the
cohesin sub-units studied so far in various species localize along the axial
cores in leptotene (review by Nasmyth,
2001
). Furthermore in mammals AE-like structures containing
cohesin sub-units are found even in the absence of the AE core constituent
SCP3 (Pelttari et al., 2001
).
Finally, some mammalian cohesin sub-units interact with AE components
(Eijpe et al., 2000
). Taken
together, these data add to a growing consensus that cohesin axes provide the
base for AE formation. Our characterization of the swi1-2 phenotype
accords well with such a model.
SWI1 seems to be required for meiotic recombination initiation (see above).
Several possible explanations might account for this observation. First, the
recombination initiation defect may be a consequence of the lack of AEs.
However, the yeast smc3 and Rec8, and apparently the C.
elegans Rec8 mutants form DSBs in the complete absence of AE
(Klein et al., 1999;
Pasierbek et al., 2001
)
suggesting that the latter is not required for recombination initiation.
Nevertheless, we cannot exclude the possibility that it is not the case in
Arabidopsis since, so far, no Arabidopsis mutants other
than swi1-2 have been described that exhibit a lack of AE. Another
possibility is that the lack of DSB formation in swi1-2 is due to the
absence of sister chromatid cohesion. However, all the cohesion mutants
described to date are able to initiate recombination. In the S. cerevisiae
rec8 and smc3 cohesion mutants, Spo11-mediated DSBs occur but
are not repaired (Klein et al.,
1999
). Similarly, the C. elegans meiocytes lacking Rec8
and the A. thaliana syn1/dif1 mutants exhibit chromosome
fragmentation (Pasierbek et al.,
2001
; Bhatt et al.,
1999
; Bai et al.,
1999
). In the Sordaria spo76-1 mutant, a limited
reduction in the number of Rad51/Dmc1 foci suggests that recombination
initiation is nearly normal (van Heemst et
al., 1999
). If it is the case that DSB formation is independent of
the sister chromatid cohesion establishment, then it could suggest a role for
SWI1 in recombination initiation that is distinct from its cohesion function.
Several lines of evidence indicate a mechanistic link between recombination
initiation and DNA replication (Borde et
al., 2000
; Cha et al.,
2000
; Keeney,
2001
). Some authors proposed that passage of the replication fork
is required to establish a structure permissive for DSB formation, or/and that
factors involved in DSB formation, such as Spo11, might assemble onto DNA
during replication. One can hypothesize that SWI1 may be involved in such an
S-phase process, in addition and contemporaneous to its function in sister
chromatid cohesion establishment.
Functional considerations
SWI1 thus appears required for sister chromatid cohesion establishment,
consequently for AE and SC formation, and, possibly independently, for
recombination initiation. Nevertheless, the actual function of SWI1 remains a
matter of speculation. We have previously proposed
(Mercier et al., 2001b) that
SWI1 could perform a similar function to that of the yeast proteins Scc2/Mis4
and Scc4, which permit the association of the cohesin complex with chromatin
(Ciosk et al., 2000
;
Furuya et al., 1998
). However
this hypothesis appears to be ruled out by our finding that the Rec8 homologue
SYN1/DIF1 localizes on swi1-2 chromosomes
(Fig. 3). At this stage, we
cannot exclude the possibility that SWI1 establishes cohesion in a manner
analogous to the yeast Eco1/Ctf7 or Eso1 protein
(Skibbens et al., 1999
;
Tanaka et al., 2000
;
Toth et al., 1999
), by
interacting with the cohesin protein after the latter has loaded onto the
chromosomes. Alternatively SWI1 could have a role in cohesion (and possibly
recombination) that is completely independent of SYN1/DIF1, via
loading or modifying other components during G1 or S phase.
However, such candidates remain to be identified.
Finally, this study highlights an interesting aspect of developmental regulation of meiosis in Arabidopsis that remains to be resolved. Several genes including SWI1, ASY1 and SYN1 encode proteins that are on current evidence entirely specific to meiosis, yet transcripts from them are detected in other vegetative tissues. This suggests that regulation at the level of translation may be a significant feature of meiosis in Arabidopsis.
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ACKNOWLEDGMENTS |
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