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Nucleic Acids Research Pages 3154-3158  

Meiotic role of SWI6 in Saccharomyces cerevisiae
Introduction
Materials And Methods
   Microorganisms and plasmids
   Procedure of sporulation
   Northern blot analysis
   Flow cytometry
Results
   Sporulation of a [Delta]swi6 mutant
   Premeiotic DNA replication in [Delta]swi6 mutant cells
   SWI6 is required for meiotic recombination
   SWI6 enhances expression of genes required for meiotic recombination
   The SWI6 transcript is induced in early meiosis
   The meiotic recombination frequency depends on dosage of SWI6
Discussion
Acknowledgements
References

Meiotic role of SWI6 in Saccharomyces cerevisiae

Meiotic role of SWI6 in Saccharomyces cerevisiae

Sun-Hee Leem1,2, Chung-Nam Chung2, Yangil Sunwoo2, Hiroyuki Araki1,*

1Department of Biochemistry and Molecular Biology, Research Institute for Microbial Diseases, Osaka University, Yamada-oka 3-1, Suita, Osaka 565-0871, Japan and 2Department of Biology, Dong-A University,Pusan 604-714, Korea

Received March 24, 1998; Revised and Accepted May 11, 1998

ABSTRACT

The transcript levels of DNA replication genes and some recombination genes in Saccharomyces cerevisiaefluctuate and peak at the G1/S boundary in the mitotic cell cycle. This fluctuation is regulated by MCB (MluI cell cycle box) elements which are bound by the DSC1/MBF1 complex consisting of Swi6 and Mbp1. It is also known that some of the MCB-regulated genes are induced by treatment with DNA damaging agents and in meiosis. In this report, the function of SWI6 in meiosis was investigated. [Delta]swi6 cells underwent sporulation as did wild-type cells. However, the deletion mutant cells showed reduced spore viability and lower frequency of recombination. The transcript levels of the recombination genes RAD51 and RAD54, which have MCB elements, were reduced in [Delta]swi6 cells. The transcript levels of SWI6 itself were also induced and declined in meiosis. Furthermore, an increased dosage of SWI6 enhanced the transcript level of the RAD51 gene and also the recombination frequency in meiosis. These results suggest that SWI6 enhances the expression level of the recombination genes in meiosis in a dosage-dependent manner, which results in an effect on the frequency of meiotic recombination.

INTRODUCTION

In Saccharomyces cerevisiae, the DNA replication genes as well as some of the recombination genes are regulated transcriptionally during the cell cycle. Their transcript levels fluctuate and peak at the G1/S boundary during the mitotic cell cycle. These genes have MCB (MluI cell cycle box) elements in the upstream region. The DSC1/MBF (DNA synthesis control/MCB binding factor) complex binds at MCBs in a cell cycle-dependent manner and activates these genes (1). It is known that the DSC1 complex consists of Swi6 and Mbp1 and Mbp1 directly interacts with MCB (2). In a deletion mutant of the SWI6 or MBP1 genes, genes having MCBs are constitutively expressed at a reduced level (1,2). Swi6 also forms the SBF complex (SCB binding factor) with another protein, Swi4, which binds at SCB (Swi4/Swi6 cell cycle box) elements and activates genes bearing SCBs in the upstream region.

Some of the genes whose transcript levels are regulated by MCBs in mitosis are also induced in early meiosis (3-7) and by DNA damaging agents (3,4,6,8). The regulatory sequence required for the response to DNA damaging agents was examined in the RAD54 gene, whose transcript level fluctuates during the cell cycle and has MCB elements. It has been shown that a 26 bp sequence containing the MCBs is required for induction by UV and MMS (9). However, MCB elements have no essential role in the DNA damage response, while they enhance the transcript level (10). Moreover, deleting this 26 bp regulatory sequence does not affect induction in meiosis (9). Thus, the regulatory sequences required for induction by DNA damaging agents and in meiosis differ. The transcript levels of genes bearing MCB elements peak at exactly the same time in mitosis, while, in contrast, their transcript levels increase with different kinetics during meiosis (5).

Although the function of the SWI6 gene in the mitotic cell cycle is known to some extent, the involvement of this gene in the regulation of meiosis has not been examined. Therefore, we studied the effect of the deletion of SWI6 on meiosis and the meiotic transcript levels of recombination genes. The transcript levels of the RAD51 and RAD54 genes were reduced by deletion of SWI6. Moreover, the spore viability and recombination frequency decreased in [Delta]swi6 mutants. These observations indicate an important role for SWI6 in meiosis.

MATERIALS AND METHODS

Microorganisms and plasmids

Escherichia coli DH5[alpha] (11) was used for all plasmid DNA manipulations. Saccharomyces cerevisiae SK1 derivative strains used in this study were as follows: SLH105 (MATa lys2 ho::LYS2 ura3 leu2::hisG his4-X trp1::hisG), SLH108 (MAT[alpha] lys2 ho::LYS2 ura3 leu2::hisG his4-B trp1::hisG), SLD101 (MATa/MAT[alpha] lys2/lys2 ho::LYS2/ho::LYS2 ura3/ura3 leu2::hisG/leu2::hisG his4-X/his4-B trp1::hisG/trp1::hisG), SLD102 (as SLD101 except for [Delta]ime1::LEU2), SLD109 (as SLD101 except for [Delta]swi4::LEU2), SLD113 (as SLD101 except for [Delta]swi6::TRP1), NKY857 (MATa lys2 ho::LYS2 ura3 leu2::hisG his4-X) and NKY860 (MAT[alpha] lys2 ho::LYS2 ura3 leu2::hisG his4-B). SLH105 and SLH108 strains were constructed as follows. A 4.7 kb DNA fragment of pNKY1009 (12) containing the TRP1 disruption (trp1::hisG-URA3-hisG) was digested with EcoRI and BglII and was used for transformation of NKY857 and NKY860. Ura- derivatives of Ura+ Trp- transformants were initially obtained by patching onto 5-fluoroorotic acid (5-FOA) plates, which are selective for Ura- strains. To construct SLD109 and SLD113, [Delta]swi4::LEU2 or [Delta]swi6::TRP1 derivatives of SLH105 and SLH108 obtained by a one-step disruption method (13) using Bd194 and Bd197 plasmids (14) were mated and the diploid strain was selected by the inability to mate with the a or [alpha] haploid strain. As the [Delta]swi4 and [Delta]swi6 diploid strains are unstable and often lose the ability to sporulate, the resultant diploid was immediately used for further experiments. To construct SLD102, SLH105 and SLH108 were transformed with a linearized [Delta]ime1::LEU2 plasmid in which the 1.3 kb HindIII-NruI fragment of IME1 (15) was replaced by a 1.6 kb BamHI fragment spanning LEU2 DNA, obtained from plasmid YDp-L (16), and the resultant [Delta]ime1 derivatives were mated.

SLD252 (MATa/[alpha] leu2/leu2 his4-4/his4-290 CAN1/can1r ura3/ura3 ho::LYS2/ho::LYS2 trp1/trp1 CYH2/cyh2r ADE6/ade6 ade2/ade2 lys2/lys2) and SLD330 (SLD252 [Delta]swi6::TRP1) are not SK1 derivatives and were used to measure intergenic recombination. SLD330 was constructed as SLD113.

YEpSWI6 is identical to BA354 (14). YCpSWI6 was constructed by connecting a SalI-BamHI fragment spanning SWI6 (14) with YCplac33 (17).

Procedure of sporulation

The diploid SK1 strains were streaked on YPG plates (1% yeast extract, 2% polypeptone, 3% glycerol, 2% agar) and incubated at 30°C for 12 h (18,19). A single colony on a YPG plate was streaked on YPD (1% yeast extract, 2% polypeptone, 2% glucose, 2% agar) and incubated for 2-3 days. In the case of cells harbouring plasmids, the cells were streaked on SD-Leu or SD-Ura (2% glucose, 0.67% yeast nitrogen base, 2% agar, supplemented with the necessary amino acids lacking leucine or uracil) and incubated for 2-3 days. A single colony from the plate was grown in YPD or SD liquid medium for 18-24 h. Each culture was diluted 100-fold into YPA (1% yeast extract, 2% polypeptone, 2% potassium acetate) or 10-fold into SA (2% potassium acetate, 0.67% yeast nitrogen base, supplemented with the necessary amino acids lacking leucine or uracil) medium, for cells harboring plasmids, and incubated for 12 h. Cells (1-2 × 107 cells/ml) were harvested, washed twice with sterile water and resuspended at the same density in SPM (0.3% potassium acetate, 0.03% raffinose). Then, the suspension was incubated at 30°C with vigorous shaking.

Northern blot analysis

To analyse the transcripts during meiosis, cells were sporulated in 1 l SPM, samples were removed at intervals and total RNA was prepared as previously described (18). About 10 µg total RNA was heat denatured at 65°C for 10 min and run on a 6% formaldehyde gel (1.2% Sea-kem agarose gel; FMC BioProducts) with MOPS buffer. After electrophoresis, the gel was washed with distilled water and blotted onto a nylon membrane (Hybond-N; Amersham). The RNA on the membrane was cross-linked by UV, prehybridized and hybridized with [32P]dCTP-labeled DNA probes. The DNA probes used were as follows: SWI4 probe; 1.9 kb BamHI-PstI fragment (20), SWI6 probe; 1.4 kb BglII-PvuII fragment (14), RAD51 probe; 1.2 kb StuI-BstEII fragment (8), RAD54 probe; 1.9 kb BamHI fragment (21), ACT1 probe; 1 kb XhoI-HindIII fragment (22).

Table 1. Spore viability of the swi4::LEU2 and swi6::TRP1 strains
Strain Total asci
dissected		 Viable spores/ascus Spore viability (%)
0 1 2 3 4
Wild-type 44 0 0 1 3 40 97.2
[Delta]swi4 113 13 38 37 14 11 43.8
[Delta]swi6 72 23 23 17 9 0 27.3

Flow cytometry

To prepare meiotic samples for flow cytometry, 2 ml sporulating culture were withdrawn at each time point and the cells were fixed by addition of ethanol to a final concentration of 70%. Flow cytometry was carried out as previously described (23).

RESULTS

Sporulation of a [Delta]swi6 mutant

To elucidate the role of SWI6 in meiosis, we first observed sporulation of a swi6 deletion mutant in synchronous culture. It is known that Swi4 makes a complex, SBF, with Swi6 that binds to SCB elements. Thus, the effect of swi4 deletion was also examined. Microscopic observation revealed that the [Delta]swi6 mutant formed asci at a frequency (88%) better than the wild-type (72%) after 12 h in sporulation medium and mature asci appeared ~2-3 h earlier than in the wild-type. A [Delta]swi4 homozygous diploid mutant showed almost the same phenotype as [Delta]swi6, suggesting that both genes are not essential for spore formation.

Several mutants defective in meiosis show a low viability of spores, although they apparently form normal asci (24). Thus, we examined the spore viability of [Delta]swi4 and [Delta]swi6 strains by dissecting asci after sporulation. As shown in Table 1, only 27% of [Delta]swi6 spores and 44% of [Delta]swi4 spores made viable colonies, whereas the wild-type strain showed 97% spore viability. Further microscopic observation revealed that half of the inviable spore clones did not germinate, while the remaining half germinated but cell growth arrested with various cell shapes. This result clearly indicates that Swi4 and Swi6 are required for normal meiosis.

Premeiotic DNA replication in [Delta]swi6 mutant cells

We examined premeiotic DNA replication in a [Delta]swi6 strain, as Swi6 and Mbp1 form the MBF complex that regulates expression of DNA replication genes during mitotic growth, although three viable spore clones in an ascus from the [Delta]swi6 strain suggested that premeiotic DNA replication must occur in [Delta]swi6. Cells transferred to sporulation medium were withdrawn, sonicated, stained with propidium iodide and subjected to flow cytometry. As shown in Figure 1, the DNA content in [Delta]swi6 cells increased to 4C faster than in wild-type cells, whereas [Delta]ime1 cells did not increase their DNA content, as previously reported (15). These results suggest that premeiotic DNA replication is almost complete in [Delta]swi6 strains. Thus, the low viability of spores in [Delta]swi6 cells seems not to be caused by the absence of premeiotic DNA replication.


Figure 1. Flow cytometry of [Delta]swi6 cells during meiosis. SLD101(SWI6), SLD113([Delta]swi6) and SLD102([Delta]ime1) cells taken at various time after transfer to sporulation medium were treated with RNase, stained with propidium iodide and subjected to flow cytometry (3). [Delta]ime1 cells were used as a control, as they cannot initiate premeiotic DNA replication.

SWI6 is required for meiotic recombination

As most of the mutants defective in meiotic recombination show low spore viability (24), we examined meiotic intragenic and intergenic recombination in a [Delta]swi6 strain. Diploid cells were transferred to sporulation medium and aliquots were withdrawn and spread onto YPD and selective plates after appropriate dilution (`return-to-growth'). The colonies that appeared on selective plates were counted as recombinants. In strain SLD330 ([Delta]swi6), the frequencies of intragenic (his4-4/his4-290) and intergenic (cyh2-ade6) recombination were reduced to 14 and 31% respectively of those in wild-type cells (Table 2). The recombination frequency was also reduced in SLD113 ([Delta]swi6), with a different background. The recombination frequency was also measured in the meiotic products by dissecting asci formed by strains SLD101 and SLD113. In strain [Delta]swi6, only one ascus among 420 dissected had a His+ spore clone, while six out of 115 in wild-type cells had His+ clones (wild-type, 5.2 × 10-2; [Delta]swi6, 4.6 × 10-3). Thus, SWI6 is required for meiotic recombination. The reduced recombination frequency probably accounts for the low spore viability in [Delta]swi6 cells,

Table 2. Meiotic recombination in the [Delta]swi6 mutant
Strain Relevant genotype his4a (×10-4) cyh2-ade6a (×10-4
    0 h 6 h 12 h 0 h 6 h 12 h
SLD252 SWI6 2.5 520 970 3.8 180 4900
SLD330 [Delta]swi6 1.6 57 140 4.2 20 1500
SLD101 SWI6 0.41 37 110 - - -
SLD113 [Delta]swi6 0.18 0.83 10 - - -
SLD113 [Delta]swi6 [YCpSWI6] 0.75 52 160 - - -
SLD113 [Delta]swi6 [YEpSWI6] 0.66 200 340 - - -
aIntragenic recombination frequencies between his4-4 and his4-290 for SLD252 and SLD330 strains and between his4-X and his4-B for SLD101 and SLD113 strains and intergenic recombination between cyh2 and ade6 were examined as described (18).

SWI6 enhances expression of genes required for meiotic recombination

The reduced frequency of recombination in [Delta]swi6 may be caused by reduced expression levels of the recombination genes, since Swi6 works as a transcription factor in the mitotic cell cycle. To examine this possibility, we measured the transcript levels of the RAD51 and RAD54 genes during meiosis in a [Delta]swi6 strain. Both genes have MCB elements in the upstream sequence and are required for meiotic recombination (3,8,10,24,25).

RNA extracted from sporulating cells was subjected to northern analysis and levels of RAD51 and RAD54 transcripts were examined (Fig. 2). The RAD51 and RAD54 transcript levels increased 20-fold during meiosis in the wild-type cells, as previously reported (3,8). In [Delta]swi6 cells, the maximal level of the RAD51 and RAD54 transcripts was reduced to 60% of that in wild-type cells. In [Delta]swi4 cells, on the other hand, the maximal level of the RAD51 and RAD54 transcripts was almost the same as in wild-type cells. These results suggest that Swi6 also functions in meiosis as a transcription factor.


Figure 2. Northern blotting of the recombination genes. Isogenic wild-type (SLD101; [cir]), [Delta]swi4 (SLD109; l) and [Delta]swi6 (SLD113; s) cells were sporulated and cells were withdrawn at various times. RNA extracted from these cells at the indicated times was subjected to northern blotting. The same amount of RNA was loaded into each lane and this was confirmed by staining the gel with ethidium bromide before blotting. The direct image of each analysis is shown in the lower panel with the time in sporulation medium. The intensity of the signal was measured using a Fuji image analyzer and normalized such that the intensity of each transcript at 0 h in the wild-type cells is assigned a value of 1. The membrane used in this experiment is that already described in Leem et al. (19).

The SWI6 transcript is induced in early meiosis

The level of the SWI6 transcript during meiosis has not been examined. Thus, we performed northern analysis of the SWI6 transcript during meiosis. As shown in Figure 3A, the SWI6 transcript level declined and then increased between 2 and 4 h after medium transfer. This is consistent with a role for Swi6 as a transcription factor for the genes containing MCB elements, including the RAD51 and RAD54 genes. We also examined the transcript level of SWI4 in meiosis. Interestingly, the SWI4 transcript was also induced in meiosis (Fig. 3B). However, the timing of its induction is different from that of SWI6. The kinetics of induction are consistent with the meiotic function suggested by spore viability (Table 1).


Figure 3. Induction of SWI6 (A) and SWI4 (B) transcripts in meiosis. RNA extracted from sporulating SLD101 cells was transferred to a nylon membrane after electrophoresis and hybridized with SWI6 and SWI4 DNA. The membrane used in this experiment is that used in Figure 2 for wild-type cells.

The meiotic recombination frequency depends on dosage of SWI6

The lack of SWI6 decreased the recombination frequency, presumably by reducing the expression of certain recombination genes. The SWI6 gene on a multicopy or low copy plasmid was introduced into [Delta]swi6 diploid cells. The transcript level of SWI6 in plasmid YEp was 3-fold higher than that in plasmid YCp (data not shown). These strains were subjected to sporulation and aliquots were withdrawn for measurement of recombinants (His+) and for northern blot analysis. The recombination frequency of the cells with SWI6 on a multicopy plasmid increased 2-fold over the cells having SWI6 on a low copy plasmid (Table 2). The RAD51 transcript level in the same cells increased almost 2-fold (Fig. 4). This result strongly suggests that an increased dosage of SWI6 enhances transcription of recombination genes and in consequence increases the recombination frequency.


Figure 4. Increased dosage of SWI6 enhances the level of RAD51 transcript. [Delta]swi6 diploid cells (SLD113) harboring YCpSWI6 (a) (n) and YEpSWI6 (b) ([squ]) were sporulated. RNA extracted from sporulated cells was subjected to northern blotting using the same probe as in Figure 2. As a control, actin transcript was analyzed using ACT1 DNA. The image of a northern blot is shown with the time in sporulation medium and the intensity of RAD51 transcript is normalized to ACT1 transcript.

DISCUSSION

In this study, we have shown that the frequency of meiotic recombination and the transcript level of the recombination genes RAD51 and RAD54 is reduced in [Delta]swi6 mutants. Thus, it is likely that recombination frequency in meiosis depends on the expression level of the recombination genes. This view is strengthened by the observation that an increased dosage of Swi6 enhanced recombination frequency. Increasing the dosage of the RAD51 or RAD54 gene alone could not enhance recombination frequency (our unpublished results). Thus, the reduced level of several transcripts seems to additively affect recombination frequency or a lack of SWI6 reduces the transcript level of an as yet unknown gene(s) which encodes a limiting factor for meiotic recombination.

[Delta]swi6 cells form asci earlier and at a slightly higher frequency than the wild-type and go through premeiotic DNA replication faster than mitotic DNA replication (Fig. 1). These facts suggest that SWI6 also regulates expression of the genes which repress meiosis. The low spore viability and normal recombination frequency in [Delta]swi4 cells (Table 1 and our unpublished results) show that Swi4 is probably involved in a sporulation process other than recombination. However, no gene whose meiotic transcript level is regulated by SWI4 is as yet known.

It was reported that the transcript levels of CDC8, 9 and 21, which have MCBs, increased during meiosis with different kinetics from one another while their transcript levels peaked at exactly the same time in mitosis (5). Our results also show that the transcript levels of RAD51 and RAD54 increase with different kinetics. Moreover, deletion of SWI6 changed the induction pattern of each gene differently; the RAD51 transcript level was high at 0 h in sporulation medium, while induction of the RAD54 transcript was delayed. This may be caused by a complex regulation of these transcripts during meiosis which includes the SWI6 system and other unknown regulation systems.

The RAD51 and RAD54 genes were reported to be induced by DNA damaging agents (3,4,10). In this induction, a lack of MCB elements decreases the induction level, whereas the induction kinetics are similar to wild-type cells. Moreover, [Delta]swi6 strains show weak sensitivity to MMS but not to UV (10). As most of the lesions caused by MMS are healed by recombinational repair (26), the reduced expression of recombination genes in [Delta]swi6 cells could account for the increased sensitivity to MMS. Therefore, it is likely that the same group of recombination genes regulated by SWI6 affect meiotic recombination and the repair of MMS damage. Moreover, [Delta]mbp1 and swi4ts do not affect sensitivity to MMS, suggesting that some unknown factor(s) forms a complex with Swi6 and controls an MCB element (10). Therefore, an unknown factor(s) may interact with the SWI6 system to regulate gene induction also in meiosis.

ACKNOWLEDGEMENTS

We thank S.Harashima, L.H.Johnston, H.Ogawa, A.Shinohara and I.Yamashita for yeast strains and plasmids and L.H.Johnston for critical reading of the manuscript. Our special thanks are offered to A.Sugino for encouragement and helpful suggestions during this study and for critical reading of this manuscript. This work was supported by grants from the Ministry of Education, Science and Culture of Japan, the Kato Memorial Foundation and the Genetic Engineering Research Program, Ministry of Education, Republic of Korea (1997).

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*To whom correspondence should be addressed at: Division of Microbial Genetics, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan. Tel: +81 559 81 6754; Fax: +81 559 81 6762; Email: hiaraki@lab.nig.ac.jp

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