Abstract
In S. pombe strains mutant for rec15 aberrant ascus morphology, reduced spore viability and severe reduction of meiotic recombination was detected. Genetic and cytological analysis identified frequent interruption of meiosis after the first division, and nondisjunction I, as the main segregation errors in the mutant. Chromosome segregation at meiosis I was not random in rec15, suggesting the presence of a backup system for correct segregation of achiasmate chromosomes. The analysis of meiotic progression in time-course experiments revealed that the major meiotic events, such as the onset of premeiotic DNA synthesis, of horse-tail nuclear movement, and of the first meiotic division occurred earlier in rec15 than in wild-type. The early onset of meiotic events is a novel observation for an early recombination mutant and implies a function of rec15 protein already at or before DNA synthesis.
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References
Bähler J, Wyler T, Loidl J, Kohli J (1993) Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis. J Cell Biol 121:241–256
Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A III et al (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943–951
Beach D, Rodgers L, Gould J (1985) RAN1 + controls the transition from mitotic division to meiosis in fission yeast. Curr Genet 10:297–311
Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, et al (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264:270–273
Davis L, Smith GR (2001) Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe. Proc Natl Acad Sci U S A 98:8395–8402
De Veaux LC, Hoagland NA, Smith GR (1992) Seventeen complementation groups of mutations decreasing meiotic recombination in Schizosaccharomyces pombe. Genetics 130:251–261
Egel R (1973) Commitment to meiosis in fission yeast. Mol Gen Genet 121:277–284
Egel R, Egel-Mitani M (1974) Premeiotic DNA Synthesis in Fission Yeast. Exptl Cell Res 88:127–134
Gomez EB, Forsburg SL (2004) Analysis of the fission yeast Schizosaccharomyces pombe cell cycle. Methods Mol Biol 241:93–111
Gutz H, Heslot H, Leupold U, Loprieno N (1974) Schizosaccharomyces pombe. In: King RC (eds) Handbook of genetics. Plenum Press, New York, pp 395–446
Haraguchi T, Ding DQ, Yamamoto A, Kaneda T, Koujin T et al (1999) Multiple-color fluorescence imaging of chromosomes and microtubules in living cells. Cell Struct Funct 24:291–298
Hiraoka Y, Ding DQ, Yamamoto A, Tsutsumi C, Chikashige Y (2000) Characterization of fission yeast meiotic mutants based on live observation of meiotic prophase nuclear movement. Chromosoma 109:103–109
Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168
Kitajima TS, Miyazaki Y, Yamamoto M, Watanabe Y (2003) Rec8 cleavage by separase is required for meiotic nuclear divisions in fission yeast. EMBO J 22:5643–5653
Kohli J, Hottinger H, Munz P, Strauss A, Thuriaux P (1977) Genetic mapping in Schizosaccharomyces pombe by mitotic and meiotic analysis and induced haploidization. Genetics 87:471–489
Kupfer DM, Drabenstot SD, Buchanan KL, Lai H, Zhu H et al (2004) Introns and splicing elements of five diverse fungi. Eukaryot Cell 3:1088–1100
Lin Y, Smith GR (1995) An intron-containing meiosis-induced recombination gene, rec15, of Schizosaccharomyces pombe. Mol Microbiol 17: 439–448
Lorenz A, Wells JL, Pryce DW, Novatchkova M, Eisenhaber F et al (2004) S pombe meiotic linear elements contain proteins related to synaptonemal complex components. J Cell Sci 117:3343–3351
Mata J, Lyne R, Burns G, Bahler J (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32:143–147
Maundrell K (1990) nmt1 of fission yeast. J Biol Chem 265:10857–10864
Molnar M, Bahler J, Sipiczki M, Kohli J (1995) The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics 141:61–73
Molnar M, Bahler J, Kohli J, Hiraoka Y (2001a) Live observation of fission yeast meiosis in recombination-deficient mutants: a study on achiasmate chromosome segregation. J Cell Sci 114:2843–2853
Molnar M, Parisi S, Kakihara Y, Nojima H, Yamamoto A et al (2001b) Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe. Genetics 157:519–532
Molnar M, Doll E, Yamamoto A, Hiraoka Y, Kohli J (2003) Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing. J Cell Sci 116:1719–1731
Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194:795–823
Nabeshima K, Nakagawa T, Straight AF, Murray A, Chikashige Y et al (1998) Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol Biol Cell 9:3211–3225
Niwa O, Yanagida M (1985) Triploid meiosis and aneuploidy in Schizosaccharomyces pombe: an unstable aneuploid disomic for chromosome III. Curr Genet 9:463–470
Olson LW, Edén U, Egel-Mitani M, Egel R (1978) Asynaptic meiosis in fission yeast?. Hereditas 89:189–199
Page SL, Hawley RS (2004) The Genetics and Molecular Biology of the Synaptonemal Complex. Annu Rev Cell Dev Biol
Parisi S, McKay MJ, Molnar M, Thompson MA, van der Spek PJ, et al (1999) Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 19:3515–3528
Ponticelli AS, Smith GR (1989) Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics 123:45–54
Sharif WD, Glick GG, Davidson MK, Wahls WP (2002) Distinct functions of S. pombe Rec12 (Spo11) protein and Rec12-dependent crossover recombination (chiasmata) in meiosis I; and a requirement for Rec12 in meiosis II. Cell Chromosome 1:1
Shimoda C (2004) Forespore membrane assembly in yeast: coordinating SPBs and membrane trafficking. J Cell Sci 117:389–396
Sipiczki M, Ferenczy L (1977) Protoplast fusion of Schizosaccharomyces pombe Auxotrophic mutants of identical mating-type. Mol Gen Genet 151:77–81
Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464
Watanabe Y, Lino Y, Furuhata K, Shimoda C, Yamamoto M (1988) The S.pombe mei2 gene encoding a crucial molecule for commitment to meiosis is under the regulation of cAMP. EMBO J 7:761–767
Yamamoto A, West RR, McIntosh JR, Hiraoka Y (1999) A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J Cell Biol 145:1233–1249
Young JA, Hyppa RW, Smith GR (2004) Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167:593–605
Acknowledgements
We thank M. Yanagida (University of Kyoto) and G. Smith (Hutchinson Cancer Research Center, Seattle) for S. pombe strains. This work was supported by the Swiss National Science Foundation. It was part of the PhD thesis of E. Doll submitted to the Faculty of Science, University of Berne, Switzerland.
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Communicated by M. Yamamoto
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Doll, E., Molnar, M., Hiraoka, Y. et al. Characterization of rec15, an early meiotic recombination gene in Schizosaccharomyces pombe . Curr Genet 48, 323–333 (2005). https://doi.org/10.1007/s00294-005-0024-3
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DOI: https://doi.org/10.1007/s00294-005-0024-3