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Previous Article | Next Article 
Molecular and Cellular Biology, June 2003, p. 3965-3973, Vol. 23, No. 11
0270-7306/03/$08.00+0 DOI: 10.1128/MCB.23.11.3965-3973.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo,1 SORST, Japan Science and Technology Corporation, Hongo, Tokyo 113-0033, Japan2
Received 13 December 2002/ Returned for modification 13 February 2003/ Accepted 10 March 2003
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ABSTRACT |
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cells undergo equational rather than random division has not been clarified; therefore, it has been unclear whether equational segregation is due to a loss of cohesin in general or to a loss of a specific requirement for Rec8. We report here that the equational segregation at meiosis I depends on substitutive Rad21, which relocates to the centromeres if Rec8 is absent. Moreover, we demonstrate that even if sufficient amounts of Rad21 are transferred to the centromeres at meiosis I, thereby establishing cohesion at the centromeres, rec8 cells never recover monopolar attachment but instead secure bipolar attachment. Thus, Rec8 and Rad21 define monopolar and bipolar attachment, respectively, at meiosis I. We conclude that cohesin is a crucial determinant of the attachment manner of kinetochores to the spindle microtubules at meiosis I in fission yeast. |
INTRODUCTION |
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During meiosis, cohesin subunit Rad21/Scc1 is largely replaced by its meiotic counterpart, Rec8 (9, 18, 19, 30). There are three crucial features of the chromosome at meiosis I that are not observed in mitosis (13, 26, 32). First, pairing and recombination occurs between homologous chromosomes in meiotic prophase, resulting in the formation of chiasmata. Second, sister kinetochores always attach to microtubules from same spindle pole, which is called monopolar attachment and is known to ensure that sister chromatids segregate to the same pole at meiosis I. Third, cohesion between sister chromatids in the vicinity of centromeres persists until the onset of the second meiotic division. Remarkably, all of these features of meiotic chromosomes are disrupted in Schizosaccharomyces pombe rec8 cells, suggesting that a meiosis-specific cohesin complex plays a central role in the assembly of meiotic chromosomes (12, 30). In particular, because Rec8 preferentially locates at centromeres and rec8 cells undergo equational chromosome segregation at meiosis I, it has been proposed that Rec8 is required at centromeres to construct kinetochores that orient to the same pole (30, 31). However, it has been shown in Saccharomyces cerevisiae that if the Scc1/Rad21 cohesin subunit, but not Rec8, is expressed by the REC8 promoter, then monopolar attachment is established, although sister chromatid cohesion at the centromeres is disrupted during anaphase I (27). Thus, at least in S. cerevisiae, Scc1/Rad21 can allow proper orientation and monopolar attachment of sister kinetochores at meiosis I. Therefore, there is an argument that the equational segregation observed in S. pombe rec8 cells may be due to a loss of cohesin in general rather than a specific requirement for the Rec8 subunit of cohesin (10).
Here we address the open question presented above. First, we examined why S. pombe rec8 cells undergo equational rather than random division. We show that if Rec8 is absent during meiosis, Rad21 relocates to the centromeres to back up the cohesion of sister kinetochores. Thus, substitutive Rad21 is the reason for the occurrence of equational division. Moreover, we demonstrate that even though enough Rad21 is transferred to the centromeres by an ectopic expression, rec8 cells never undergo reductional division but instead secure equational division. From these results and others we conclude that Rec8 and Rad21 determine the manner of kinetochore attachment to microtubules at meiosis I, at least in fission yeast.
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MATERIALS AND METHODS |
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Construction of plasmids carrying cyan-GFP variant (CFP)-tagged Gar1 or Mis6 protein. We constructed pREP81-gar1+-CFP and pREP81-mis6+-CFP. The gar1+ open reading frame was amplified by PCR with wild-type genomic DNA as a template and forward primer 5'-GCCGGGTCGACAATGAGTTTTAGAGGCGGTCGC-3' (the SalI site is underlined) and reverse primer 5'-GGGAGGGATCCAAGAATCTGCCACGGAAACCAC-3' (the BamHI site is underlined). The mis6+ open reading frame was amplified with forward primer 5'-CGGCCAGATCTTAATGGAAAGCTTTGAGA-3' (the BglII site is underlined) and reverse primer 5'-CCCCGCGGCCGCAAACGATTTAATGTTGAAA-3' (the NotI site is underlined). These PCR products were cloned into pGFT81 (7), and then the C-terminal GFP was replaced with the cloned CFP fragment.
Construction of strains overexpressing Rad21 from the adh1 or rec8 promoter.
To construct pREP-Prec8-rad21+-GFP, the rec8 promoter region (ca. -108 to -1), the rad21+-GFP fusion gene, the ura4+ cassette, and the 3'-untranslated region of rec8 (
600 bp) were cloned between the PstI and SacI sites of pREP1. To construct pREP-Padh1-rad21+-GFP, an adh1 promoter fragment was additionally inserted into the 5' site of the rad21 sequence. These plasmid constructs were linearized by SacI and ClaI to cut out the Prec8-rad21+-GFP and Padh1-rad21+-GFP regions and then transformed into rec8::kanr cells to replace the chromosomal rec8::kanr locus with these constructs by homologous recombination at the rec8 promoter region and 3' untranslated region. For construction of Prec8-rad21+-FLAG and Padh1-rad21+-FLAG alleles on the chromosomes, the GFP sequences of the preceding constructs were replaced by a FLAG fragment.
Preparation of synchronous meiotic cells and observation of chromosomes marked with GFP.
Cells were cultured to log phase, collected by centrifugation, suspended in 20 g of leucine liter-1, and then spotted onto a SPA. When we marked only one chromosome by GFP, we cultured opposite mating-type cells, one marked with GFP and the other not, and mixed them prior to spotting them onto SPA. This allows subsequent synchronous conjugation and meiosis. When cells undergoing meiosis I and II or cells arrested at late prophase I by mei4 became abundant in the population, they were observed without fixation or after being fixed with cold methanol; zygotes were monitored for GFP and DAPI (4',6-diamidino-2-phenylindole). Images were obtained by using a microscope (Axioplan 2; Zeiss) equipped with a cooled charge-coupled device camera (Quantix; Photometrics) and Metamorph software (Universal Imaging Corporation). Seven Z sections for GFP signals were converted into single two-dimensional images by taking the maximum signal at each pixel position in the images.
Synchronous meiosis. We induced synchronous meiosis with a temperature-sensitive pat1-114 allele as described previously (31). Cells were cultured in MM-N at 25°C for 16 h and then shifted to 32°C, and 0.1 g of NH4Cl liter-1 was added. The cells were harvested and fixed with 1% formaldehyde (Wako) for chromatin immunoprecipitation (ChIP) assay and with methanol for microscopy and fluorescence-activated cell-sorting analysis. For microscopy, fixed cells were washed and suspended in PEMS buffer (100 mM PIPES, pH 6.9; 1 mM EGTA; 1 mM MgSO4; 1.2 M sorbitol) with DAPI.
ChIP analysis. ChIP assays were carried out essentially as described previously (21). Anti-GFP polyclonal antibodies (Living Colors Full-length A.v. Polyclonal Antibody; Clontech) were used for immunoprecipitation. DNA prepared from whole-cell extracts or immunoprecipitated fractions was analyzed by quantitative PCR with a LightCycler and a LightCycler-DNA Master SYBR Green I kit (Roche). The following primers were used for PCR: forward primer for cnt, 5'-ATCTCATTGCTATTTGGCGAC-3'; reverse primer for cnt, 5'-GCGTTTCTTCGGCGAAATGC-3'; forward primer for imr, 5'-CACATACCAAAAAGTCTGGC-3'; reverse primer for imr, 5'-GCTGAGGCTAAGTATCTGTT-3'; forward primer for dg, 5'-TTTTCAGCGAGACATGTACC-3'; reverse primer for dg, 5'-TCATAAAGCAACACTGGGTG-3'; forward primer for dh, 5'-GTAAGTATGAGCAACTGGCG-3'; reverse primer for dh, 5'-GGAACAAATCAGGAAACCGAG-3'; forward primer for lys1, 5'-ATTTTCGCATCCAACGCTGC-3'; reverse primer for lys1, 5'-ACAACTAAGGCTCTGGGCTT-3'; forward primer for mes1, 5'-CGAAGGCTACTTTCATGCCA-3'; reverse primer for mes1, 5'-CGTACATTCAGACTGTTGAAC-3'; forward primer for rDNA1, 5'-ATGATTCCCTCAGTAACGGCGAG-3'; reverse primer for rDNA1, 5'-CACTCTACTTGTTCGCTATCGGT-3'; forward primer for rDNA2, 5'-CCTCTAACGATAGTTACCTGGTTG-3'; reverse primer for rDNA2, 5'-CAGAAATTTGAATGAACCATCGCC-3'; forward primer for TAS, 5'-CGTTACCCAATTAATTATGAC-3'; and reverse primer for TAS, 5'-CGGTGATGTAGTGTACTATA-3'.
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RESULTS |
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cells become viable by expressing Rec8 with a constitutive adh1 promoter (30), we used rad21 Padh1-rec8+ cells to inspect the requirement of Rad21 for meiosis. We first assayed meiotic recombination in rad21-deleted cells but did not detect any decrease in recombination when tested between the lys3 and ura1 loci (located near the telomere of chromosome I) and between the leu1 and mat1 loci (located near the centromere of chromosome II) (data not shown). We next examined the requirement of Rad21 for meiotic chromosome segregation. Chromosome segregation was analyzed by viewing the LacI-GFP fusion protein, bound to LacO DNA repeats that were integrated at the lys1 locus (cen1-GFP dot), ca. 30 kb from the centromere of chromosome I (14). The normal segregation pattern of cen1-GFP, a single GFP dot in every nucleus of the tetranucleated cells, was prevalent in the rad21 Padh1-rec8+ cells (PZ208) (94%, n = 543), as well as in its rad21+ version (PZ207) (92%, n = 515). Although we do not know the significance of Rad21 enrichment in the nucleolus, these analyses suggest that Rad21 is virtually dispensable for normal meiotic chromosome segregation and recombination as long as Rec8 function is intact.
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cells undergo mostly equational division at meiosis I. If the Rec8 complex is the sole cohesin in meiosis, rec8 cells will lose most sister chromatid cohesion during prophase and then undergo random, rather than equational, chromosome segregation. Indeed, the budding yeast rec8 mutant shows such a phenotype in 70% of cells (9). One explanation for the phenotype of fission yeast rec8 is that residual Rad21 may substitute for centromeric cohesion, because Rad21 is required at the centromeres for equational segregation in mitosis (2, 17, 28). To investigate this possibility, we determined the localization of Rad21 in rec8 cells. Although Rad21 is enriched in the nucleolus of rec8+ cells, an additional distinct dot of Rad21 appears in rec8 cells on the opposite side of the leading edge of the horsetail nucleus (Fig. 1B). To determine the position of the Rad21-GFP dot, we coexpressed a kinetochore protein, Mis6 (21), tagged with CFP. Fluorescence microscopy showed the Rad21-GFP dot colocalizing with the Mis6-CFP dot (Fig. 1C), indicating that a significant amount of Rad21 relocates to the centromeres if Rec8 is depleted. These results raise the possibility that substitutive Rad21 may play a role in ensuring equational chromosome segregation at meiosis I in rec8 cells.
Rad21 is required for equational division during meiosis I in rec8 cells.
We then decided to introduce a temperature-sensitive mutation, rad21-K1 (24), into rec8 and examine chromosome segregation at meiosis I. By crossing the cen1-GFP strain with an untagged strain, we monitored the segregation pattern of one pair of sister chromatids during meiosis. Because the two nuclei on either side of the tetrad are derived from the same meiosis I nucleus in fission yeast, reductional or equational segregation in meiosis I can be determined by examining the distribution of the two cen-GFP dots in the zygotes (Fig. 2A). Wild-type zygotes represented mostly reductional segregation patterns: +/+, -/- (Fig. 2B). The occurrence of some +/-, +/- patterns can be explained by recombination between the GFP-associating sequences and the centromere (appearance of recombinants is expected to be 8%). As reported previously (30), rec8 cells mostly displayed equational segregation patterns: +/-, +/- (Fig. 2B). The rad21-K1 mutation by itself showed no meiotic defect. However, when rec8 was combined with rad21-K1, the equational segregation at meiosis I was partly disrupted with the reductional population increasing to 40% (Fig. 2B). Notably, the rec8 rad21-K1 cells with reductional division at meiosis I underwent random second division (Fig. 2B), suggesting that the "reductional" segregation was erroneous. If equational division is disrupted completely, sister cen1-GFP dots will move randomly, producing a complete mixture of equational and reductional patterns (each 50%). Therefore, the observed change would be close to this case. We conclude that Rad21 plays a role in ensuring equational segregation during meiosis I in rec8 cells.
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cells.
For the faithful processing of equational chromosome segregation, centromere cohesion must be preserved at least until the spindle microtubules capture kinetochores. Therefore, centromeric cohesion of rec8 cells would be intact. This was examined by monitoring cen1-GFP marking near the centromere of chromosome I. We utilized a mutation of mei4 to synchronize the meiotic cells at late prophase I (6). In wild-type cells, the cen1-GFP dots were mostly doublet or single at this stage, indicating that sister chromatid cohesion at the centromere was intact and that there was some pairing between homologs (Fig. 3A). The rad21-K1 cells also displayed no defect in sister chromatid cohesion during meiosis, although there were severe defects during mitosis (25; data not shown). Interestingly, rec8 cells preserved centromeric cohesion at the mei4 arrest point in meiotic prophase, although they showed substantially impaired arm cohesion (Fig. 3). Remarkably, the residual centromeric cohesion of rec8 cells was substantially disrupted by the introduction of the rad21-K1 mutation. Taken together, these results strongly suggest that if Rec8 is depleted, Rad21 has a concealed role in preserving sister centromere cohesion at meiosis I, thereby ensuring subsequent equational division.
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cells, which undergo rather random chromosome segregation at meiosis I (9). The fact that the S. pombe Rad21 complex has an affinity for heterochromatin, which covers a vast region of the centromeres (2, 17), whereas S. cerevisiae has no centromeric heterochromatin, might explain why substantial amounts of Rad21/Scc1 relocate to centromeres in fission yeast but not in budding yeast. When Scc1, but not Rec8, is expressed by the REC8 promoter, however, monopolar attachment at meiosis I is mostly established in budding yeast (27). This observation contradicts our current findings that substitutive Rad21 ensures equational division at meiosis I in fission yeast rec8 cells. One may argue that the amount of substitutive Rad21 at the centromeres in fission yeast is not sufficient to provide a full level of "cohesin function." To address this issue, we expressed Rad21-GFP (carrying full function) from the rec8 promoter or the more robust adh1 promoter in rec8 cells and monitored their meioses. Fluorescence microscopy of Rad21-GFP indicated that the centromere signal is indeed stronger in these strains, especially in rec8::Padh1-rad21+-GFP cells (Fig. 4A). To demonstrate further the association of Rad21 with centromere DNA, we performed a ChIP assay. Extracts were prepared from rec8::Padh1-rad21+-GFP cells under synchronous meiosis and mostly within prophase I. In accordance with the cytological observations, the ChIP assay indicated that Rad21-GFP associates mainly with the centromere and rDNA sequences (Fig. 4A and B). S. pombe centromeres are organized into two distinct domains: a heterochromatic outer repeat region and a central core region associated with histone H3 variant CENP-A (Fig. 4A). Endogenous Rad21 associates with the outer centromere regions but less with the central core during mitosis (31) (Fig. 4C) and also during meiosis (Fig. 4B), as has been similarly observed in meiotic rec8::Padh1-rad21+-GFP cells, but the association with chromatin was several times greater in the latter cells (compare Fig. 4A with C). Notably, the increased amount of Rad21 association with the outer centromeric repeat sequences (dg or dh) exceeds that of endogenous Rec8 association during meiosis (Fig. 4A and D). Similar results were obtained with meiotic rec8::Prec8-rad21+-GFP cells, although the amount of Rad21 associated with the outer centromere was similar to that of endogenous Rec8 (data not shown).
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::Prec8-rad21+-GFP and rec8::Padh1-rad21+-GFP cells predominantly displayed an equational pattern (Fig. 5A). Moreover, we monitored meiotic chromosome segregation more directly by observing the segregation pattern of cen1-GFP marked on one pair of sister chromatids. The results were consistent; both rec8::Prec8-rad21+-FLAG and rec8::Padh1-rad21+-FLAG cells underwent equational division at meiosis I (Fig. 6), as in the case of rec8 cells (Fig. 2B). These results indicate that even if sufficient amounts of Rad21 are loaded into centromeres in meiosis I, rec8 cells never reestablish monopolar attachment but instead establish bipolar attachment. Finally, we examined the kinetics of nuclear division of rec8+, rec8::Prec8-rad21+-FLAG, and rec8::Padh1-rad21+-FLAG cells in synchronous meiosis. We found that the first and second meiotic divisions progressed with similar kinetics in all strains (Fig. 5B). Given that the rec8 rad21+ overproducers undergo equational segregation at the first meiotic division, these results imply that the cohesion between sister kinetochores established by Rad21 is not protected during meiosis I, in contrast to the cohesion mediated by Rec8. Taken together, these findings led us to conclude that Rec8 bears specific roles at meiosis I in establishing monopolar attachment and also in maintaining cohesion between sister centromeres and that Rad21 cannot substitute for either of these functions even if it is fully localized to the centromeres during meiosis.
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DISCUSSION |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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::Prec8-rad21+ cells undergo the first meiotic divisions with the same kinetics as wild-type cells. In budding yeast rec8::Prec8-Scc1+/rad21+ cells, cohesion between sister centromeres mediated by Scc1/Rad21 is also destroyed at the onset of the first meiotic division (27). Thus, the instability of Rad21/Scc1 regarding this aspect of meiosis I is conserved between budding and fission yeast. Earlier work in budding yeast identified a meiosis-specific kinetochore factor, Mam1, that functions in establishing monopolar attachment, and this role can be executed only in the presence of cohesin (either Rec8 or Scc1 complexes) and only during meiosis (27). Another meiotic factor, Spo13, is also involved in the regulation of monopolar attachment in budding yeast (8, 22). So far, Mam1 or Spo13 homologs have not been found in other organisms, including fission yeast, but it may be a conserved feature that a meiosis I-specific factor(s) cooperates with cohesin to establish monopolar attachment at meiosis I. The definitive difference between the two yeasts is that cohesin specificity plays a crucial role in establishing monopolar attachment in fission yeast but not in budding yeast. Studies of the distribution of Rec8 at centromeres in comparison with that of Rad21/Scc1 in other organisms will be interesting, as will further examinations to determine whether cohesins are determinants of monopolar or bipolar attachment at meiosis I in other eukaryotes.
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ACKNOWLEDGMENTS |
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This work was supported in part by grants from the Ministry of Education, Science, and Culture of Japan.
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FOOTNOTES |
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