Heteroduplex DNA Formation and Homolog Pairing in Yeast Meiotic Mutants

INVESTIGATIONS

Heteroduplex DNA Formation and Homolog Pairing in Yeast Meiotic Mutants

D. K. Nag, H. Scherthan, B. Rockmill, J. Bhargava and G. S. Roeder
Molecular Genetics Program, David Axelrod Institute, Wadsworth Center for Laboratories and Research, Albany, New York 12201

Previous studies of Saccharomyces cerevisiae have identified several meiosis-specific genes whose products are required for wild-type levels of meiotic recombination and for normal synaptonemal complex (SC) formation. Several of these mutants were examined in a physical assay designed to detect heteroduplex DNA (hDNA) intermediates in meiotic recombination. hDNA was not detected in the rec102, mei4 and hop1 mutants; it was observed at reduced levels in red1, mek1 and mer1 strains and at greater than the wild-type level in zip1. These results indicate that the REC102, MEI4, HOP1, RED1, MEK1 and MER1 gene products act before hDNA formation in the meiotic recombination pathway, whereas ZIP1 acts later. The same mutants assayed for hDNA formation were monitored for meiotic chromosome pairing by in situ hybridization of chromosome-specific DNA probes to spread meiotic nuclei. Homolog pairing occurs at wild-type levels in the zip1 and mek1 mutants, but is substantially reduced in mei4, rec102, hop1, red1 and mer1 strains. Even mutants that fail to recombine or to make any SC or sc precursors undergo a significant amount of meiotic chromosome pairing. The in situ hybridization procedure revealed defects in meiotic chromatin condensation in mer1, red1 and hop1 strains.

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				D. Y. Lui, T. L. Peoples-Holst, J. Chang Mell, H.-Y. Wu, E. W. Dean, and S. M. Burgess Analysis of Close Stable Homolog Juxtaposition During Meiosis in Mutants of Saccharomyces cerevisiae Genetics, July 1, 2006; 173(3): 1207 - 1222. [Abstract] [Full Text] [PDF]

				E. Trelles-Sticken, C. Adelfalk, J. Loidl, and H. Scherthan Meiotic telomere clustering requires actin for its formation and cohesin for its resolution J. Cell Biol., July 18, 2005; 170(2): 213 - 223. [Abstract] [Full Text] [PDF]

				T. Tsubouchi and G. S. Roeder A Synaptonemal Complex Protein Promotes Homology-Independent Centromere Coupling Science, May 6, 2005; 308(5723): 870 - 873. [Abstract] [Full Text] [PDF]

				T. L. Peoples-Holst and S. M. Burgess Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast Genes & Dev., April 1, 2005; 19(7): 863 - 874. [Abstract] [Full Text] [PDF]

				S. Anuradha and K. Muniyappa Saccharomyces cerevisiae Hop1 Zinc Finger Motif Is the Minimal Region Required for Its Function in Vitro J. Biol. Chem., July 9, 2004; 279(28): 28961 - 28969. [Abstract] [Full Text] [PDF]

				B. Liebe, M. Alsheimer, C. Hoog, R. Benavente, and H. Scherthan Telomere Attachment, Meiotic Chromosome Condensation, Pairing, and Bouquet Stage Duration Are Modified in Spermatocytes Lacking Axial Elements Mol. Biol. Cell, February 1, 2004; 15(2): 827 - 837. [Abstract] [Full Text] [PDF]

				L. F. Revers, J. M. Cardone, D. Bonatto, J. Saffi, M. Grey, H. Feldmann, M. Brendel, and J. A. P. Henriques Thermoconditional modulation of the pleiotropic sensitivity phenotype by the Saccharomyces cerevisiae PRP19 mutant allele pso4-1 Nucleic Acids Res., November 15, 2002; 30(22): 4993 - 5003. [Abstract] [Full Text] [PDF]

				A. J. MacQueen, M. P. Colaiacovo, K. McDonald, and A. M. Villeneuve Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans Genes & Dev., September 15, 2002; 16(18): 2428 - 2442. [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]

				H. Tsubouchi and G. S. Roeder The Mnd1 Protein Forms a Complex with Hop2 To Promote Homologous Chromosome Pairing and Meiotic Double-Strand Break Repair Mol. Cell. Biol., May 1, 2002; 22(9): 3078 - 3088. [Abstract] [Full Text] [PDF]

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				E. Trelles-Sticken, M. E. Dresser, and H. Scherthan Meiotic Telomere Protein Ndj1p Is Required for Meiosis-specific Telomere Distribution, Bouquet Formation and Efficient Homologue Pairing J. Cell Biol., October 3, 2000; 151(1): 95 - 106. [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]

				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]

				J. M. Bailis, A. V. Smith, and G. S. Roeder Bypass of a Meiotic Checkpoint by Overproduction of Meiotic Chromosomal Proteins Mol. Cell. Biol., July 1, 2000; 20(13): 4838 - 4848. [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]

				D. A. Thompson and F. W. Stahl Genetic Control of Recombination Partner Preference in Yeast Meiosis: Isolation and Characterization of Mutants Elevated for Meiotic Unequal Sister-Chromatid Recombination Genetics, October 1, 1999; 153(2): 621 - 641. [Abstract] [Full Text] [PDF]

				T. K. Pandita, C. H. Westphal, M. Anger, S. G. Sawant, C. R. Geard, R. K. Pandita, and H. Scherthan Atm Inactivation Results in Aberrant Telomere Clustering during Meiotic Prophase Mol. Cell. Biol., July 1, 1999; 19(7): 5096 - 5105. [Abstract] [Full Text] [PDF]

				S. M. Burgess, N. Kleckner, and a. B. M. Weiner Somatic pairing of homologs in budding yeast: existence and modulation Genes & Dev., June 15, 1999; 13(12): 1627 - 1641. [Abstract] [Full Text]

				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]

				E Trelles-Sticken, J Loidl, and H Scherthan Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering J. Cell Sci., January 3, 1999; 112(5): 651 - 658. [Abstract] [PDF]

				J. M. Bailis and G. S. Roeder Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein Genes & Dev., November 15, 1998; 12(22): 3551 - 3563. [Abstract] [Full Text]

				K. S. McKim and A. Hayashi-Hagihara mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved Genes & Dev., September 15, 1998; 12(18): 2932 - 2942. [Abstract] [Full Text]

				B. Rockmill and G. S. Roeder Telomere-mediated chromosome pairing during meiosis in budding yeast Genes & Dev., August 15, 1998; 12(16): 2574 - 2586. [Abstract] [Full Text]

				K.-S. Tung and G. S. Roeder Meiotic Chromosome Morphology and Behavior in zip1 Mutants of Saccharomyces cerevisiae Genetics, June 1, 1998; 149(2): 817 - 832. [Abstract] [Full Text] [PDF]

				G. S. Roeder Meiotic chromosomes: it takes two to tango Genes & Dev., October 15, 1997; 11(20): 2600 - 2621. [Full Text] [PDF]

				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]

				B Rockmill, M Sym, H Scherthan, and G S Roeder Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes & Dev., November 1, 1995; 9(21): 2684 - 2695. [Abstract] [PDF]