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Corresponding author: William S. Saunders, Department of Biological Sciences, 258 Crawford Hall, University of Pittsburgh, Pittsburgh, PA 15260.
Communicating editor: M. D. ROSE
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Meiotic cell division includes two separate and distinct types of chromosome segregation. In the first segregational event the sister chromatids remain attached at the centromere; in the second the chromatids are separated. The factors that control the order of chromosome segregation during meiosis have not yet been identified but are thought to be confined to the centromere region. We showed that the centromere protein Slk19p is required for the proper execution of meiosis in Saccharomyces cerevisiae. In its absence diploid cells skip meiosis I and execute meiosis II division. Inhibiting recombination does not correct this phenotype. Surprisingly, the initiation of recombination is apparently required for meiosis II division. Thus Slk19p appears to be part of the mechanism by which the centromere controls the order of meiotic divisions.
MEIOSIS is a special type of cell division that generates haploid gametes to fulfill the needs of sexual reproduction. To achieve this end, a single round of DNA replication is followed by two successive rounds of chromosome segregation, reductional (meiosis I) and equational (meiosis II). While meiosis II is mechanically similar to mitosis, meiosis I is quite distinct from both mitosis and meiosis II. During anaphase of meiosis I, sister chromatids do not separate from each other. Instead they segregate as a unit away from the other homologous chromosome.
The two separate meiotic divisions are not interdependent, as demonstrated by single-division meiosis in Saccharomyces cerevisiae mutants, such as cdc5, cdc14, spo12, spo13, and cdc28 (
Substantial progress has been made to identify what determines whether chromosomes will undergo reductional or equational segregation (reviewed in
Centromeres perform multiple functions related to chromosome segregation during cell division. The most well characterized is attachment of the chromosome to the microtubules of the spindle, but centromeres also play less-well-defined roles in cell cycle control, spindle structure/assembly, and sister chromatid cohesion (reviewed in
As centromeres are a critical part of how the cell distinguishes between the different meiotic divisions, it is expected that some centromere proteins will play a key role in the ordering of meiosis I and II. We find here that the centromere protein Slk19p is required for this task. SLK19 was identified previously in a synthetic lethal screen to identify genes with functions similar to that of the kinesin motor KAR3. It encodes a potential coiled-coil protein of ~98 kD and shares no significant homology to previously characterized proteins. Like kar3 mutants, slk19 mutants have short spindles and more cytoplasmic microtubules than normally present during mitosis (
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Yeast strains, plasmids, and media:
Strains and plasmids used in this study are listed in Table 1. All strains are derivatives of S288C. Media have been described (
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Nomenclature:
The segregation of heterozygous markers in the two-spored asci (dyads) is represented by the format +: -. The + indicates the number of spores with the phenotype of the dominant allele, while - indicates the number of spores with the phenotype of the recessive allele.
Intergenic recombination:
Diploid strains WSY1302 (slk19) and WSY1303 (wild type) were sporulated. The resulting tetrads were dissected as described (
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Heteroallelic recombination:
To determine the frequencies of heteroallelic recombination, diploid strains of wild-type (WSY1118) or slk19
(WSY1117) with ade2 heteroalleles (ade2-1/ade2-R) were constructed. Individual diploid colonies were inoculated into YEPD liquid and cultured at 30° with shaking until OD600 reached 2.0. The cultures were then divided into two parts. One part was used directly to determine the mitotic recombination rates by spreading onto YEPD and -ade selective plates and counting the frequency of adenine prototrophy. The other part was washed with sporulation medium twice and resuspended in sporulation medium to induce meiosis and sporulation. The sporulation culture was vigorously aerated at 26° for 48 hr, at which time the cells were plated onto YEPD and -ade plates to determine the meiotic recombination frequencies.
Canavanine reversion:
The ploidy of the spores was determined based on the frequencies of canavanine-resistant colonies after UV treatment. Diploid cells homozygous for slk19 and CAN1 were sporulated at 26° and the resulting dyads were dissected. Resulting individual colonies were serial diluted onto YEPD plates and incubated at 30° for 2 days. Cells were then replicated from YEPD plates onto canavanine plates and treated with UV light immediately after replica plating. The UV light was delivered from a UV crosslinker (FB-UVXL-1000, Fisher Scientific) with 9000 µJ/cm2 energy. The UV-treated cells were then incubated at 30° for 2 days to allow canavanine-resistant colonies to grow.
Immunofluorescence microscopy:
To visualize microtubules (MTs) of cells from different meiotic stages, cells were cultured in the sporulation media for ~20 hr and fixed with 3.7% formaldehyde for 2 hr. Antitubulin indirect immunofluorescence was then performed using monoclonal antibody YOL 1/34 (Serotec, Oxford, UK) and rhodamine-conjugated secondary antibody (Jackson Immunoresearch, West Grove, PA) to visualize MT, and DNA-specific fluorescent dye 4,6-diamidino-2-phenylindole (DAPI; Sigma, St. Louis) to identify the position of the nucleus as described (
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Slk19p is required to obtain two successive divisions during meiosis:
To study the function of Slk19p during meiosis, a diploid strain homozygous for slk19 ( mutants usually led to the formation of dyads with two spores per ascus (Fig 1A). The sporulation efficiency of slk19 mutants is normal, with ~50% of the total cells forming asci compared to ~60% in wild-type cells. The frequency of dyads increased from ~11% of total asci for wild type to ~80% for slk19 mutants (see Table 4). Tetrads were rarely observed in slk19 mutants (<1%). The spore viability of the slk19 dyads is slightly lower than that of wild-type tetrads. While wild-type spores maintain >95% viability after dissection, only 70% of slk19 spores were alive among 239 dyads dissected.
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Two types of dyads have been observed previously in S. cerevisiae. The first type is due to an ascospore packaging defect. Under these circumstances, two successive divisions take place but only two of the four nuclei are enclosed into spores ( mutants were the result of an ascospore packaging defect or a single-division meiosis, we determined the ploidy of the spores. Typically only diploid cells can sporulate, and only MATa/MAT
and not MATa/MATa or MAT/MAT diploids can sporulate. Dyads of slk19 mutants were dissected (MATERIALS AND METHODS) and the mating capability of viable spores was tested. Among 42 dyads with two viable spores, 13 dyads contained two spores capable of mating and 29 dyads contained two nonmating spores. Dyads with a mixture of mating and nonmating spores were not observed. The nonmating spores were able to sporulate and again produced dyads which themselves were able to sporulate to dyads (six spores from 3 dyads were tested). These observations indicate that stable diploid progenies are produced by meiosis in slk19 mutants. The ploidy of the spores was confirmed by determining the copy number of chromosome V using a canavanine mutation test. Haploid CAN1 cells have a much higher rate of mutation to canavanine resistance than do diploid CAN1/CAN1 cells. Only three spores out of the 42 dyads contained a single copy of CAN1 based on this analysis. The remaining were concluded to have at least two copies of CAN1 and thus two copies of chromosome V (Fig 1B).
The diploid spores are presumably a result of a single meiotic division. To confirm this, we also examined slk19 mutants in meiosis with antitubulin indirect immunofluorescence. Only one spindle per cell was observed, consistent with the occurrence of a single meiotic division (Fig 2). In conclusion, slk19 mutants form dyads after sporulation because there is a single meiotic division and not because there is an ascospore packaging defect.
The majority of chromosomes in slk19 mutants undergo an equational segregation:
The single meiotic division could be meiosis I, or meiosis II, or a mixture of the two. To address which kind of division was taking place, we studied the segregation pattern of three heterozygous centromere-linked markers. Centromere-linked markers remain associated with centromeres during meiosis and thus segregate with the same reductional and equational properties as chromosomes. For these experiments the markers chosen were trp1 linked to CEN4, ade1 linked to CEN1, and ura3 linked to CEN5. If chromosomes segregate reductionally (meiosis I), we expect to get 1:1 dyads in which one spore is able to grow on selective media, but the other spore cannot (Fig 3). If chromosomes segregate equationally (meiosis II), we expect to get 2:0 dyads in which both spores are able to grow on selective media. The majority of dyads in slk19 mutants were 2:0 dyads for each chosen marker, suggesting that most chromosomes segregate equationally (Table 2). As shown in Fig 3, Fig 2:0 dyads may result from a single normal equational division (Fig 3A), or a single equational segregation accompanied by chromosome loss, or incoordinate segregation (Fig 3B). But only 2:0 dyads resulting from a normal equational division will have both spores heterozygous for the chosen marker. To address whether the 2:0 dyads of slk19 mutants were a result of aberrant chromosome segregation during meiosis, we determined whether these slk19 spores were heterozygous for the tested marker. We transformed a plasmid containing wild-type SLK19 (pXZB9) into four spores from two 2:0 dyads for trp1 marker and allowed them to sporulate. Seven resulting tetrads for each spore were dissected (see MATERIALS AND METHODS) and the trp1 marker segregated 2:2 for each, indicating that those spores were heterozygous for trp1 and thus resulted from a normal equational division and not from aberrant chromosome segregation.
While most chromosomes segregate equationally, we only observed ~68% of the dyads showing 2:0 phenotype for all three markers (Table 3), indicating that at most 68% of the cells undergo a single equational division of the entire genome. The rest of the dyads showed a 1:1 phenotype for at least one of the three markers. The 1:1 phenotype may be a result of a single reductional segregation, or an aberrant segregation, or a rare meiotic recombination between centromere and linked marker followed by a single equational segregation (Fig 3). The expected number of 1:1 dyads resulting from meiotic recombination followed by a single equational division was calculated based on the distance between the marker locus and the centromere (Table 2). The observed frequency was much higher than expected based on recombination alone, suggesting that most of these 1:1 dyads were not due to recombination, but more likely from a single reductional segregation or an aberrant segregation event. The cells rarely go through reductional division for the entire genome, as we observed only 4.6% of dyads showing 1:1 for all three markers (Table 3). The rest of the dyads showing 1:1 phenotypes for at least one of the markers were probably from a mixed division with some chromosomes segregating equationally and some chromosomes segregating reductionally. The chromosomes did not behave equivalently. For example, chromosome I has a higher tendency than chromosome V to segregate reductionally as evidenced by the observation that more 1:1 dyads were observed for the ade1 marker than for the ura3 marker, even though ade1 is closer to the centromere than ura3.
In conclusion, chromosomes predominantly segregate equationally during meiosis upon loss of Slk19p. Consistent with the previous finding that different chromosomes may have different segregational properties within the same cell, we have also observed different segregational tendencies for different chromosomes.
An excess of cytoplasmic microtubules is not the direct cause of the meiosis I bypass:
Immunofluorescence with antitubulin antibodies revealed that like vegetatively growing slk19 cells, meiotic slk19 cells have an increased amount of cytoplasmic microtubules (Fig 2). These results indicate that Slk19p also influences microtubule numbers and distribution in meiosis. This excess is not an inevitable result of a single equational division, since we did not observe this phenotype in spo13 mutants, which are known to have a single equational division (Fig 2; mutants and one per spindle for spo13 mutants. mutants sporulate in the presence of benomyl, a microtubule depolymerization drug (-tubulin TUB3 gene (tub3 and slk19kip2 mutants also showed no increase in the frequency of tetrad formation compared to slk19 alone (not shown). These results indicate that the excess of cytoplasmic MTs is not likely to be the direct cause of the meiosis I bypass in slk19 mutants.
slk19 mutants exhibit normal or slightly elevated meiotic recombination rates:
Proper meiosis I segregation depends on a stable bipolar spindle, which in turn relies on a stable attachment between homologous chromosomes. Recombination is responsible for most of the association between homologues. In the absence of recombination, a high level of meiosis I nondisjunction is observed ( mutants have normal levels of meiotic recombination, we examined two types of recombination, intergenic recombination and heteroallelic recombination. For intergenic recombination, wild type and slk19 diploid strains heterozygous for ura3 and can1 were sporulated and the resulting tetrads (wild type) or dyads (slk19) were dissected as described (MATERIALS AND METHODS) and scored for the segregation of markers (Table 5; the meiotic events producing various types of dyads are shown in Fig 4). The genetic distance between can1 and ura3 in the slk19 background was calculated to be 64.2 cM, which is higher than the value of 37.3 cM observed in our wild-type background, or the 43 cM registered with the Saccharomyces Genome Database, suggesting that slk19 diploids might have an increased frequency of recombination (see MATERIALS AND METHODS for a description of the calculation of map distance). To further examine recombination frequencies, we measured the intragenic recombination between two ade2 alleles, ade2-1 and ade2-R. Recombination between these heteroalleles is mostly due to gene conversion (
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Loss of SPO11 cannot rescue the meiotic bypass of slk19 mutants:
If the recombination attachment between homologues cannot be resolved at the metaphase I/anaphase I transition, the intact bivalent (the attached meiotic homologues) could segregate to one pole during meiosis I. This may result in disomic spores and genetically appear as a meiosis I bypass. Since recombinant dyads were observed, the recombination attachment must eventually be resolved, but this may not occur until the second meiotic division, with loss of the cohesion between the arms of sister chromatids, which has been proposed as a mechanism to maintain chiasmata (spo11 double mutants. Spo11p is the catalytic subunit of the double-strand break-associated protein (spo11 double mutants failed to perform either meiotic division. No nuclear division was visible by DAPI staining and no spores were observed by differential interference contrast (DIC) microscopy. Therefore, lack of recombination is apparently unable to rescue the meiosis I bypass of slk19 mutants. Furthermore, this result implies that at least the beginning step of recombination is actually required for slk19 mutants to skip meiosis I or to undergo meiosis II.
slk19 mutants utilize a different mechanism from spo13 mutants to bypass meiosis I:
The meiotic phenotype of slk19 mutants is similar to that of spo13 mutants. Both are competent for meiotic recombination but skip meiosis I ( mutants can be partially rescued by delaying meiotic progression, for example, by sporulating at low temperature or in the presence of sublethal concentration of hydroxyurea (HU). HU is a DNA synthesis inhibitor ( mutants at 20° or in the presence of 5 mM HU. The meiotic defect of slk19 mutants could not be improved by these treatments (Table 7 and data not shown). This result further suggests that slk19 mutants bypass meiosis I under different circumstances than spo13 mutants.
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slk19 mutant diploids begin the first meiotic division and spore morphogenesis at the same time as the wild-type cells:
Since the slk19 mutant diploids undergo only a single meiotic division, they might be expected to sporulate more rapidly than wild-type cells, which must divide twice prior to spore wall formation. Alternatively, if slk19 mutants attempt both meiotic divisions or if the timing of sporulation is independent of meiotic division, the rates of sporulation may be similar. To see which case is true for slk19 mutants, isogenic slk19 and wild-type diploid cells were sporulated and samples at various timepoints were stained with DAPI to visualize the DNA. The number of binucleate and tetranucleate cells and asci for each sample were counted. Interestingly, we found that slk19 mutants started their meiotic division at nearly the exact time as the first meiotic division of wild-type cells (Fig 5A). The second meiotic division in wild-type cells occurred ~3 hr later than the first meiotic division. Surprisingly, we also found that although only a single meiotic division occurred in slk19 mutants, both wild-type and slk19 mutant cells form asci at the same rate (Fig 5B). This can be explained by two possible mechanisms. First there is a delay between the completion of meiotic division and the spore wall formation in slk19 mutants. Alternatively, there may be an internal clock that regulates the timing of spore wall formation that is independent of meiotic division.
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| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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We have identified a gene in S. cerevisiae that is required if the diploid cell is to complete two successive meiotic divisions. When mutants homozygous for slk19 sporulate, they produce mostly two-spore dyads. The dyads are a result of a single equational division as demonstrated by the following observations: (1) Nonmating spores of the dyads can sporulate, indicating that they are diploid. (2) Mutational frequencies indicate spores of the dyads contain at least two copies of chromosome V on which the CAN1 gene is located, consistent with being diploid. (3) Antitubulin indirect immunofluorescence revealed only a single spindle per cell during meiosis. (4) The segregation pattern of centromere-linked markers indicates that most chromosomes segregate equationally but not reductionally. Therefore Slk19p is essential for the reductional division from a diploid to a haploid genome. Recombination in slk19 mutants was normal or slightly elevated over wild-type cells, consistent with previous observations that meiotic recombination is not necessarily associated with reductional division and that equational division does not rely on prior reductional division (
The meiotic phenotype of slk19 mutants is similar to that of the previously described spo12 and spo13 mutants (
We propose two models to explain the slk19 meiotic phenotype. The first is that Slk19p may be uniquely required for spindle stability in meiosis I. Thus Slk19p has a similar role in meiosis I as mitosis, but becomes essential in meiosis I. Slk19p could become essential due to a difference in the nature of the kinetochore-microtubule attachment. In meiosis I each sister kinetochore pair is attached to only a single spindle pole. Bipolar attachment is important to generate tension and stabilize the microtubule-kinetochore association (reviewed in
A second model proposes that what appears to be a single meiosis II division in slk19 mutants is in fact an aberrant meiosis I. This model can explain why slk19 mutants start their single meiotic division at the same time as the first meiotic division of wild-type cells. The delay between the completion of meiotic division and the spore wall formation in slk19 mutants could result from the failed attempt at a second meiotic division in the slk19 mutants. Chromosomes may segregate equationally during meiosis I if for example, Slk19p is required to hold the sister centromeres together in meiosis I. In slk19 mutants the sister centromeres may separate prematurely in meiosis I, giving the appearance of an equational division. The sister chromatids may also missegregate equationally during meiosis I if Slk19p is required to regulate the timing of sister kinetochore differentiation. Substantial experimental evidence suggests that sister kinetochores undergo functional (
We may be able to distinguish between these two models by electron microscopy. The spindle pole bodies during meiosis I and mitosis have a similar structure, while the meiosis II spindle pole body has an outer plaque that is larger and denser (
Although the underlying mechanism for the single division meiosis of slk19 mutants is not clear, the observation that loss of SLK19 leads to a single equational division is the first identification of a centromere protein that influences the choice between equational and reductional division in meiosis.
| ACKNOWLEDGMENTS |
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The authors thank Drs. Giora Simchen of the Hebrew University of Jerusalem, Israel, for the spo13 mutants and ade2 heteroalleles and Rochelle Esposito of the University of Chicago for the spo11 mutants. The work was funded through American Cancer Society award CB-171 to W.S.S.
Manuscript received August 5, 1999; Accepted for publication February 18, 2000.
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