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. 1997 Dec;17(12):7029–7039. doi: 10.1128/mcb.17.12.7029

SSP1, a gene necessary for proper completion of meiotic divisions and spore formation in Saccharomyces cerevisiae.

D K Nag 1, M P Koonce 1, J Axelrod 1
PMCID: PMC232559  PMID: 9372934

Abstract

During meiosis, a diploid cell undergoes two rounds of nuclear division following one round of DNA replication to produce four haploid gametes. In yeast, haploid meiotic products are packaged into spores. To gain new insights into meiotic development and spore formation, we followed differential expression of genes in meiotic versus vegetatively growing cells in the yeast Saccharomyces cerevisiae. Our results indicate that there are at least five different classes of transcripts representing genes expressed at different stages of the sporulation program. Here we describe one of these differentially expressed genes, SSP1, which plays an essential role in meiosis and spore formation. SSP1 is expressed midway through meiosis, and homozygous ssp1 diploid cells fail to sporulate. In the ssp1 mutant, meiotic recombination is normal but viability declines rapidly. Both meiotic divisions occur at the normal time; however, the fraction of cells completing meiosis is significantly reduced, and nuclei become fragmented soon after meiosis II. The ssp1 defect does not appear to be related to a microtubule-cytoskeletal-dependent event and is independent of two rounds of chromosome segregation. The data suggest that Ssp1 is likely to function in a pathway that controls meiotic nuclear divisions and coordinates meiosis and spore formation.

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Selected References

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  1. Alani E., Padmore R., Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990 May 4;61(3):419–436. doi: 10.1016/0092-8674(90)90524-i. [DOI] [PubMed] [Google Scholar]
  2. Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
  3. Bishop D. K., Park D., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992 May 1;69(3):439–456. doi: 10.1016/0092-8674(92)90446-j. [DOI] [PubMed] [Google Scholar]
  4. Burns N., Grimwade B., Ross-Macdonald P. B., Choi E. Y., Finberg K., Roeder G. S., Snyder M. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev. 1994 May 1;8(9):1087–1105. doi: 10.1101/gad.8.9.1087. [DOI] [PubMed] [Google Scholar]
  5. Chakravarti D., Maitra U. Eukaryotic translation initiation factor 5 from Saccharomyces cerevisiae. Cloning, characterization, and expression of the gene encoding the 45,346-Da protein. J Biol Chem. 1993 May 15;268(14):10524–10533. [PubMed] [Google Scholar]
  6. Clancy M. J., Buten-Magee B., Straight D. J., Kennedy A. L., Partridge R. M., Magee P. T. Isolation of genes expressed preferentially during sporulation in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1983 May;80(10):3000–3004. doi: 10.1073/pnas.80.10.3000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coe J. G., Murray L. E., Kennedy C. J., Dawes I. W. Isolation and characterization of sporulation-specific promoters in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1992 Jan;6(1):75–81. doi: 10.1111/j.1365-2958.1992.tb00839.x. [DOI] [PubMed] [Google Scholar]
  8. Collins I., Newlon C. S. Chromosomal DNA replication initiates at the same origins in meiosis and mitosis. Mol Cell Biol. 1994 May;14(5):3524–3534. doi: 10.1128/mcb.14.5.3524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davis L. I. The nuclear pore complex. Annu Rev Biochem. 1995;64:865–896. doi: 10.1146/annurev.bi.64.070195.004245. [DOI] [PubMed] [Google Scholar]
  10. Elder R. T., Loh E. Y., Davis R. W. RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci U S A. 1983 May;80(9):2432–2436. doi: 10.1073/pnas.80.9.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Friesen H., Lunz R., Doyle S., Segall J. Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation. Genes Dev. 1994 Sep 15;8(18):2162–2175. doi: 10.1101/gad.8.18.2162. [DOI] [PubMed] [Google Scholar]
  12. Game J. C., Zamb T. J., Braun R. J., Resnick M., Roth R. M. The Role of Radiation (rad) Genes in Meiotic Recombination in Yeast. Genetics. 1980 Jan;94(1):51–68. doi: 10.1093/genetics/94.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gottlin-Ninfa E., Kaback D. B. Isolation and functional analysis of sporulation-induced transcribed sequences from Saccharomyces cerevisiae. Mol Cell Biol. 1986 Jun;6(6):2185–2197. doi: 10.1128/mcb.6.6.2185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Goyon C., Lichten M. Timing of molecular events in meiosis in Saccharomyces cerevisiae: stable heteroduplex DNA is formed late in meiotic prophase. Mol Cell Biol. 1993 Jan;13(1):373–382. doi: 10.1128/mcb.13.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hartwell L. H., Weinert T. A. Checkpoints: controls that ensure the order of cell cycle events. Science. 1989 Nov 3;246(4930):629–634. doi: 10.1126/science.2683079. [DOI] [PubMed] [Google Scholar]
  16. Hollingsworth N. M., Byers B. HOP1: a yeast meiotic pairing gene. Genetics. 1989 Mar;121(3):445–462. doi: 10.1093/genetics/121.3.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Honigberg S. M., Conicella C., Espositio R. E. Commitment to meiosis in Saccharomyces cerevisiae: involvement of the SPO14 gene. Genetics. 1992 Apr;130(4):703–716. doi: 10.1093/genetics/130.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Honigberg S. M., Esposito R. E. Reversal of cell determination in yeast meiosis: postcommitment arrest allows return to mitotic growth. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6559–6563. doi: 10.1073/pnas.91.14.6559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hugerat Y., Simchen G. Mixed segregation and recombination of chromosomes and YACs during single-division meiosis in spo13 strains of Saccharomyces cerevisiae. Genetics. 1993 Oct;135(2):297–308. doi: 10.1093/genetics/135.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Irie K., Yamaguchi K., Kawase K., Matsumoto K. The yeast MOT2 gene encodes a putative zinc finger protein that serves as a global negative regulator affecting expression of several categories of genes, including mating-pheromone-responsive genes. Mol Cell Biol. 1994 May;14(5):3150–3157. doi: 10.1128/mcb.14.5.3150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kaback D. B., Feldberg L. R. Saccharomyces cerevisiae exhibits a sporulation-specific temporal pattern of transcript accumulation. Mol Cell Biol. 1985 Apr;5(4):751–761. doi: 10.1128/mcb.5.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kleckner N. Meiosis: how could it work? Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167–8174. doi: 10.1073/pnas.93.16.8167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Krisak L., Strich R., Winters R. S., Hall J. P., Mallory M. J., Kreitzer D., Tuan R. S., Winter E. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 1994 Sep 15;8(18):2151–2161. doi: 10.1101/gad.8.18.2151. [DOI] [PubMed] [Google Scholar]
  24. Kurnit D. M. Escherichia coli recA deletion strains that are highly competent for transformation and for in vivo phage packaging. Gene. 1989 Oct 30;82(2):313–315. doi: 10.1016/0378-1119(89)90056-5. [DOI] [PubMed] [Google Scholar]
  25. Kurtz S., Lindquist S. Changing patterns of gene expression during sporulation in yeast. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7323–7327. doi: 10.1073/pnas.81.23.7323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Law D. T., Segall J. The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation. Mol Cell Biol. 1988 Feb;8(2):912–922. doi: 10.1128/mcb.8.2.912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Liang P., Averboukh L., Pardee A. B. Distribution and cloning of eukaryotic mRNAs by means of differential display: refinements and optimization. Nucleic Acids Res. 1993 Jul 11;21(14):3269–3275. doi: 10.1093/nar/21.14.3269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992 Aug 14;257(5072):967–971. doi: 10.1126/science.1354393. [DOI] [PubMed] [Google Scholar]
  29. Lydall D., Nikolsky Y., Bishop D. K., Weinert T. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature. 1996 Oct 31;383(6603):840–843. doi: 10.1038/383840a0. [DOI] [PubMed] [Google Scholar]
  30. Malone R. E., Bullard S., Hermiston M., Rieger R., Cool M., Galbraith A. Isolation of mutants defective in early steps of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics. 1991 May;128(1):79–88. doi: 10.1093/genetics/128.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Malone R. E. Dual regulation of meiosis in yeast. Cell. 1990 May 4;61(3):375–378. doi: 10.1016/0092-8674(90)90517-i. [DOI] [PubMed] [Google Scholar]
  32. Manivasakam P., Weber S. C., McElver J., Schiestl R. H. Micro-homology mediated PCR targeting in Saccharomyces cerevisiae. Nucleic Acids Res. 1995 Jul 25;23(14):2799–2800. doi: 10.1093/nar/23.14.2799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. McCarroll R. M., Esposito R. E. SPO13 negatively regulates the progression of mitotic and meiotic nuclear division in Saccharomyces cerevisiae. Genetics. 1994 Sep;138(1):47–60. doi: 10.1093/genetics/138.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mitchell A. P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994 Mar;58(1):56–70. doi: 10.1128/mr.58.1.56-70.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991 Sep 20;66(6):1239–1256. doi: 10.1016/0092-8674(91)90046-2. [DOI] [PubMed] [Google Scholar]
  36. Percival-Smith A., Segall J. Isolation of DNA sequences preferentially expressed during sporulation in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Jan;4(1):142–150. doi: 10.1128/mcb.4.1.142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pringle J. R., Adams A. E., Drubin D. G., Haarer B. K. Immunofluorescence methods for yeast. Methods Enzymol. 1991;194:565–602. doi: 10.1016/0076-6879(91)94043-c. [DOI] [PubMed] [Google Scholar]
  38. Rockmill B., Roeder G. S. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6057–6061. doi: 10.1073/pnas.85.16.6057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Roeder G. S. Chromosome synapsis and genetic recombination: their roles in meiotic chromosome segregation. Trends Genet. 1990 Dec;6(12):385–389. doi: 10.1016/0168-9525(90)90297-j. [DOI] [PubMed] [Google Scholar]
  40. Rose K., Rudge S. A., Frohman M. A., Morris A. J., Engebrecht J. Phospholipase D signaling is essential for meiosis. Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12151–12155. doi: 10.1073/pnas.92.26.12151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  42. SHERMAN F., ROMAN H. Evidence for two types of allelic recombination in yeast. Genetics. 1963 Feb;48:255–261. doi: 10.1093/genetics/48.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Shuster E. O., Byers B. Pachytene arrest and other meiotic effects of the start mutations in Saccharomyces cerevisiae. Genetics. 1989 Sep;123(1):29–43. doi: 10.1093/genetics/123.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Weir-Thompson E. M., Dawes I. W. Developmental changes in translatable RNA species associated with meiosis and spore formation in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Apr;4(4):695–702. doi: 10.1128/mcb.4.4.695. [DOI] [PMC free article] [PubMed] [Google Scholar]

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