Abstract
rec7 is involved in intra- and intergenic meiotic recombination in all tested regions of the genome of the fission yeast Schizosaccharomyces pombe. Segregational analysis in a rec7 gene disruption mutant revealed frequent occurrence of two-spored asci. Spores giving rise to diploid colonies were shown to derive from skipping of the second meiotic division. Nondisjunction of homologous chromosomes at the first meiotic division was also frequent. The cytological structures and processes, such as formation of linear elements, pairing of homologous chromosomes, and clustering of telomeres and centromeres, are regular in the mutant. Northern blot experiments revealed meiosis-specific expression of rec7. Screening of a meiotic cDNA library also identified transcripts from the opposite strand in the rec7 region. A Rec7-GFP fusion protein was localized in the nucleus of whole cells before karyogamy, during prophase, and after meiosis I. On spreads of prophase nuclei approximately 50 foci of Rec7-GFP were counted. Some of the observed phenotypes of the disruption mutant and the N-terminal sequence homology suggest that Rec7p is a functional homolog of Rec114p of Saccharomyces cerevisiae. The observed phenotypes of the disruption and the appearance of Rec7-GFP in mating haploid cells and after meiosis I are consistent with Rec7p functions before, during, and after meiotic prophase.
Full Text
The Full Text of this article is available as a PDF (396.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Basi G., Schmid E., Maundrell K. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene. 1993 Jan 15;123(1):131–136. doi: 10.1016/0378-1119(93)90552-e. [DOI] [PubMed] [Google Scholar]
- Beach D., Rodgers L., Gould J. ran1+ controls the transition from mitotic division to meiosis in fission yeast. Curr Genet. 1985;10(4):297–311. doi: 10.1007/BF00365626. [DOI] [PubMed] [Google Scholar]
- Bullard S. A., Kim S., Galbraith A. M., Malone R. E. Double strand breaks at the HIS2 recombination hot spot in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13054–13059. doi: 10.1073/pnas.93.23.13054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bähler J., Wyler T., Loidl J., Kohli J. Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis. J Cell Biol. 1993 Apr;121(2):241–256. doi: 10.1083/jcb.121.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cao L., Alani E., Kleckner N. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell. 1990 Jun 15;61(6):1089–1101. doi: 10.1016/0092-8674(90)90072-m. [DOI] [PubMed] [Google Scholar]
- Cervantes M. D., Farah J. A., Smith G. R. Meiotic DNA breaks associated with recombination in S. pombe. Mol Cell. 2000 May;5(5):883–888. doi: 10.1016/s1097-2765(00)80328-7. [DOI] [PubMed] [Google Scholar]
- Chikashige Y., Ding D. Q., Funabiki H., Haraguchi T., Mashiko S., Yanagida M., Hiraoka Y. Telomere-led premeiotic chromosome movement in fission yeast. Science. 1994 Apr 8;264(5156):270–273. doi: 10.1126/science.8146661. [DOI] [PubMed] [Google Scholar]
- De Veaux L. C., Hoagland N. A., Smith G. R. Seventeen complementation groups of mutations decreasing meiotic recombination in Schizosaccharomyces pombe. Genetics. 1992 Feb;130(2):251–262. doi: 10.1093/genetics/130.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Egel R., Egel-Mitani M. Premeiotic DNA synthesis in fission yeast. Exp Cell Res. 1974 Sep;88(1):127–134. doi: 10.1016/0014-4827(74)90626-0. [DOI] [PubMed] [Google Scholar]
- Engebrecht J. A., Voelkel-Meiman K., Roeder G. S. Meiosis-specific RNA splicing in yeast. Cell. 1991 Sep 20;66(6):1257–1268. doi: 10.1016/0092-8674(91)90047-3. [DOI] [PubMed] [Google Scholar]
- Fox M. E., Smith G. R. Control of meiotic recombination in Schizosaccharomyces pombe. Prog Nucleic Acid Res Mol Biol. 1998;61:345–378. doi: 10.1016/s0079-6603(08)60831-4. [DOI] [PubMed] [Google Scholar]
- Grimm C., Kohli J., Murray J., Maundrell K. Genetic engineering of Schizosaccharomyces pombe: a system for gene disruption and replacement using the ura4 gene as a selectable marker. Mol Gen Genet. 1988 Dec;215(1):81–86. doi: 10.1007/BF00331307. [DOI] [PubMed] [Google Scholar]
- Hawley R. S., Theurkauf W. E. Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet. 1993 Sep;9(9):310–317. doi: 10.1016/0168-9525(93)90249-h. [DOI] [PubMed] [Google Scholar]
- Heim R., Cubitt A. B., Tsien R. Y. Improved green fluorescence. Nature. 1995 Feb 23;373(6516):663–664. doi: 10.1038/373663b0. [DOI] [PubMed] [Google Scholar]
- Hindley J., Phear G., Stein M., Beach D. Sucl+ encodes a predicted 13-kilodalton protein that is essential for cell viability and is directly involved in the division cycle of Schizosaccharomyces pombe. Mol Cell Biol. 1987 Jan;7(1):504–511. doi: 10.1128/mcb.7.1.504. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiraoka Y., Swedlow J. R., Paddy M. R., Agard D. A., Sedat J. W. Three-dimensional multiple-wavelength fluorescence microscopy for the structural analysis of biological phenomena. Semin Cell Biol. 1991 Jun;2(3):153–165. [PubMed] [Google Scholar]
- 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]
- Ivanov E. L., Korolev V. G., Fabre F. XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics. 1992 Nov;132(3):651–664. doi: 10.1093/genetics/132.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jiao K., Bullard S. A., Salem L., Malone R. E. Coordination of the initiation of recombination and the reductional division in meiosis in Saccharomyces cerevisiae. Genetics. 1999 May;152(1):117–128. doi: 10.1093/genetics/152.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johzuka K., Ogawa H. Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics. 1995 Apr;139(4):1521–1532. doi: 10.1093/genetics/139.4.1521. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kitamura K., Shimoda C. The Schizosaccharomyces pombe mam2 gene encodes a putative pheromone receptor which has a significant homology with the Saccharomyces cerevisiae Ste2 protein. EMBO J. 1991 Dec;10(12):3743–3751. doi: 10.1002/j.1460-2075.1991.tb04943.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kobori M., Ikeda Y., Nara H., Kato M., Kumegawa M., Nojima H., Kawashima H. Large scale isolation of osteoclast-specific genes by an improved method involving the preparation of a subtracted cDNA library. Genes Cells. 1998 Jul;3(7):459–475. doi: 10.1046/j.1365-2443.1998.00202.x. [DOI] [PubMed] [Google Scholar]
- Kohli J., Bähler J. Homologous recombination in fission yeast: absence of crossover interference and synaptonemal complex. Experientia. 1994 Mar 15;50(3):295–306. doi: 10.1007/BF01924013. [DOI] [PubMed] [Google Scholar]
- Kohli J. Meiosis. Telomeres lead chromosome movement. Curr Biol. 1994 Aug 1;4(8):724–727. doi: 10.1016/s0960-9822(00)00160-3. [DOI] [PubMed] [Google Scholar]
- Lin Y., Larson K. L., Dorer R., Smith G. R. Meiotically induced rec7 and rec8 genes of Schizosaccharomyces pombe. Genetics. 1992 Sep;132(1):75–85. doi: 10.1093/genetics/132.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loidl J., Scherthan H., Kaback D. B. Physical association between nonhomologous chromosomes precedes distributive disjunction in yeast. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):331–334. doi: 10.1073/pnas.91.1.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mao-Draayer Y., Galbraith A. M., Pittman D. L., Cool M., Malone R. E. Analysis of meiotic recombination pathways in the yeast Saccharomyces cerevisiae. Genetics. 1996 Sep;144(1):71–86. doi: 10.1093/genetics/144.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Menees T. M., Ross-MacDonald P. B., Roeder G. S. MEI4, a meiosis-specific yeast gene required for chromosome synapsis. Mol Cell Biol. 1992 Mar;12(3):1340–1351. doi: 10.1128/mcb.12.3.1340. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Molnar M., Bähler J., Sipiczki M., Kohli J. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics. 1995 Sep;141(1):61–73. doi: 10.1093/genetics/141.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Molnar M., Sipiczki M. Polyploidy in the haplontic yeast Schizosaccharomyces pombe: construction and analysis of strains. Curr Genet. 1993 Jul-Aug;24(1-2):45–52. doi: 10.1007/BF00324664. [DOI] [PubMed] [Google Scholar]
- Nakagawa T., Ogawa H. Involvement of the MRE2 gene of yeast in formation of meiosis-specific double-strand breaks and crossover recombination through RNA splicing. Genes Cells. 1997 Jan;2(1):65–79. doi: 10.1046/j.1365-2443.1997.d01-283.x. [DOI] [PubMed] [Google Scholar]
- Parisi S., McKay M. J., Molnar M., Thompson M. A., van der Spek P. J., van Drunen-Schoenmaker E., Kanaar R., Lehmann E., Hoeijmakers J. H., Kohli J. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol. 1999 May;19(5):3515–3528. doi: 10.1128/mcb.19.5.3515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pittman D., Lu W., Malone R. E. Genetic and molecular analysis of REC114, an early meiotic recombination gene in yeast. Curr Genet. 1993;23(4):295–304. doi: 10.1007/BF00310890. [DOI] [PubMed] [Google Scholar]
- Ponticelli A. S., Smith G. R. Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics. 1989 Sep;123(1):45–54. doi: 10.1093/genetics/123.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pâques F., Haber J. E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1999 Jun;63(2):349–404. doi: 10.1128/mmbr.63.2.349-404.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rockmill B., Engebrecht J. A., Scherthan H., Loidl J., Roeder G. S. The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics. 1995 Sep;141(1):49–59. doi: 10.1093/genetics/141.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rockmill B., Roeder G. S. A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination. Genes Dev. 1991 Dec;5(12B):2392–2404. doi: 10.1101/gad.5.12b.2392. [DOI] [PubMed] [Google Scholar]
- Roeder G. S. Meiotic chromosomes: it takes two to tango. Genes Dev. 1997 Oct 15;11(20):2600–2621. doi: 10.1101/gad.11.20.2600. [DOI] [PubMed] [Google Scholar]
- Scherthan H., Bähler J., Kohli J. Dynamics of chromosome organization and pairing during meiotic prophase in fission yeast. J Cell Biol. 1994 Oct;127(2):273–285. doi: 10.1083/jcb.127.2.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sun H., Treco D., Schultes N. P., Szostak J. W. Double-strand breaks at an initiation site for meiotic gene conversion. Nature. 1989 Mar 2;338(6210):87–90. doi: 10.1038/338087a0. [DOI] [PubMed] [Google Scholar]
- Watanabe Y., Lino Y., Furuhata K., Shimoda C., Yamamoto M. The S.pombe mei2 gene encoding a crucial molecule for commitment to meiosis is under the regulation of cAMP. EMBO J. 1988 Mar;7(3):761–767. doi: 10.1002/j.1460-2075.1988.tb02873.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto A., West R. R., McIntosh J. R., Hiraoka Y. A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J Cell Biol. 1999 Jun 14;145(6):1233–1249. doi: 10.1083/jcb.145.6.1233. [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Wettstein D., Rasmussen S. W., Holm P. B. The synaptonemal complex in genetic segregation. Annu Rev Genet. 1984;18:331–413. doi: 10.1146/annurev.ge.18.120184.001555. [DOI] [PubMed] [Google Scholar]