Analysis of Meiotic Recombination Pathways in the Yeast Saccharomyces cerevisiae

INVESTIGATIONS

Analysis of Meiotic Recombination Pathways in the Yeast Saccharomyces cerevisiae

Y. Mao-Draayer, A. M. Galbraith, D. L. Pittman, M. Cool and R. E. Malone
Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242

In the yeast, Saccharomyces cerevisiae, several genes appear to act early in meiotic recombination. HOP1 and RED1 have been classified as such early genes. The data in this paper demonstrate that neither a red1 nor a hop1 mutation can rescue the inviable spores produced by a rad52 spo13 strain; this phenotype helps to distinguish these two genes from other early meiotic recombination genes such as SPO11, REC104, or MEI4. In contrast, either a red1 or a hop1 mutation can rescue a rad50S spo13 strain; this phenotype is similar to that conferred by mutations in the other early recombination genes (e.g., REC104). These two different results can be explained because the data presented here indicate that a rad50S mutation does not diminish meiotic intrachromosomal recombination, similar to the mutant phenotypes conferred by red1 or hop1. Of course, RED1 and HOP1 do act in the normal meiotic interchromosomal recombination pathway; they reduce interchromosomal recombination to ~10% of normal levels. We demonstrate that a mutation in a gene (REC104) required for initiation of exchange is completely epistatic to a mutation in RED1. Finally, mutations in either HOP1 or RED1 reduce the number of double-strand breaks observed at the HIS2 meiotic recombination hotspot.

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				K. Nabeshima, A. M. Villeneuve, and K. J. Hillers Chromosome-Wide Regulation of Meiotic Crossover Formation in Caenorhabditis elegans Requires Properly Assembled Chromosome Axes Genetics, November 1, 2004; 168(3): 1275 - 1292. [Abstract] [Full Text] [PDF]

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				K. Jiao, L. Salem, and R. Malone Support for a Meiotic Recombination Initiation Complex: Interactions among Rec102p, Rec104p, and Spo11p Mol. Cell. Biol., August 15, 2003; 23(16): 5928 - 5938. [Abstract] [Full Text] [PDF]

				T. L. Peoples, E. Dean, O. Gonzalez, L. Lambourne, and S. M. Burgess Close, stable homolog juxtaposition during meiosis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB-independent pairing contacts Genes & Dev., July 1, 2002; 16(13): 1682 - 1695. [Abstract] [Full Text] [PDF]

				T. de los Santos, J. Loidl, B. Larkin, and N. M. Hollingsworth A Role for MMS4 in the Processing of Recombination Intermediates During Meiosis in Saccharomyces cerevisiae Genetics, December 1, 2001; 159(4): 1511 - 1525. [Abstract] [Full Text] [PDF]

				M. Molnar, S. Parisi, Y. Kakihara, H. Nojima, A. Yamamoto, Y. Hiraoka, A. Bozsik, M. Sipiczki, and J. Kohli Characterization of rec7, an Early Meiotic Recombination Gene in Schizosaccharomyces pombe Genetics, February 1, 2001; 157(2): 519 - 532. [Abstract] [Full Text]

				A. Malkova, F. Klein, W.-Y. Leung, and J. E. Haber HO endonuclease-induced recombination in yeast meiosis resembles Spo11-induced events PNAS, December 19, 2000; 97(26): 14500 - 14505. [Abstract] [Full Text] [PDF]

				M. Shinohara, S. L. Gasior, D. K. Bishop, and A. Shinohara Tid1/Rdh54 promotes colocalization of Rad51 and Dmc1 during meiotic recombination PNAS, September 26, 2000; 97(20): 10814 - 10819. [Abstract] [Full Text] [PDF]

				D. Woltering, B. Baumgartner, S. Bagchi, B. Larkin, J. Loidl, T. de los Santos, and N. M. Hollingsworth Meiotic Segregation, Synapsis, and Recombination Checkpoint Functions Require Physical Interaction between the Chromosomal Proteins Red1p and Hop1p Mol. Cell. Biol., September 15, 2000; 20(18): 6646 - 6658. [Abstract] [Full Text]

				A. Miyajima, M. Seki, F. Onoda, M. Shiratori, N. Odagiri, K. Ohta, Y. Kikuchi, Y. Ohno, and T. Enomoto Sgs1 Helicase Activity Is Required for Mitotic but Apparently Not for Meiotic Functions Mol. Cell. Biol., September 1, 2000; 20(17): 6399 - 6409. [Abstract] [Full Text]

				L. H. Rutkowski and R. E. Esposito Recombination Can Partially Substitute for SPO13 in Regulating Meiosis I in Budding Yeast Genetics, August 1, 2000; 155(4): 1607 - 1621. [Abstract] [Full Text]

				K. Muniyappa, S. Anuradha, and B. Byers Yeast Meiosis-Specific Protein Hop1 Binds to G4 DNA and Promotes Its Formation Mol. Cell. Biol., February 15, 2000; 20(4): 1361 - 1369. [Abstract] [Full Text]

				R. S. Cha, B. M. Weiner, S. Keeney, J. Dekker, and N. Kleckner Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p Genes & Dev., February 15, 2000; 14(4): 493 - 503. [Abstract] [Full Text]

				J. M. Grushcow, T. M. Holzen, K. J. Park, T. Weinert, M. Lichten, and D. K. Bishop Saccharomyces cerevisiae Checkpoint Genes MEC1, RAD17 and RAD24 Are Required for Normal Meiotic Recombination Partner Choice Genetics, October 1, 1999; 153(2): 607 - 620. [Abstract] [Full Text] [PDF]

				F. Paques and J. E. Haber Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae Microbiol. Mol. Biol. Rev., June 1, 1999; 63(2): 349 - 404. [Abstract] [Full Text] [PDF]

				K. Jiao, S. A. Bullard, L. Salem, and R. E. Malone Coordination of the Initiation of Recombination and the Reductional Division in Meiosis in Saccharomyces cerevisiae Genetics, May 1, 1999; 152(1): 117 - 128. [Abstract] [Full Text]

				M. Vedel and A. Nicolas CYS3, a Hotspot of Meiotic Recombination in Saccharomyces cerevisiae: Effects of Heterozygosity and Mismatch Repair Functions on Gene Conversion and Recombination Intermediates Genetics, April 1, 1999; 151(4): 1245 - 1259. [Abstract] [Full Text]

				L. Salem, N. Walter, and R. Malone Suppressor Analysis of the Saccharomyces cerevisiae Gene REC104 Reveals a Genetic Interaction With REC102 Genetics, April 1, 1999; 151(4): 1261 - 1272. [Abstract] [Full Text]

				T. de los Santos and N. M. Hollingsworth Red1p, a MEK1-dependent Phosphoprotein That Physically Interacts with Hop1p during Meiosis in Yeast J. Biol. Chem., January 15, 1999; 274(3): 1783 - 1790. [Abstract] [Full Text] [PDF]

				K. M. Kironmai, K. Muniyappa, D. B. Friedman, N. M. Hollingsworth, and B. Byers DNA-Binding Activities of Hop1 Protein, a Synaptonemal Complex Component from Saccharomyces cerevisiae Mol. Cell. Biol., March 1, 1998; 18(3): 1424 - 1435. [Abstract] [Full Text]

				A. V. Smith and G. S. Roeder The Yeast Red1 Protein Localizes to the Cores of Meiotic Chromosomes J. Cell Biol., March 10, 1997; 136(5): 957 - 967. [Abstract] [Full Text] [PDF]

				S. A. Bullard, S. Kim, A. M. Galbraith, and R. E. Malone Double strand breaks at the HIS2 recombination hot spot in Saccharomyces cerevisiae PNAS, November 12, 1996; 93(23): 13054 - 13059. [Abstract] [Full Text] [PDF]

				D. van Heemst, E. Kafer, T. John, C. Heyting, M. van Aalderen, and D. Zickler BimD/SPO76 is at the interface of cell cycle progression, chromosome morphogenesis, and recombination PNAS, May 22, 2001; 98(11): 6267 - 6272. [Abstract] [Full Text] [PDF]