Genetics, Vol 147, 1533-1543, Copyright © 1997

INVESTIGATIONS

RDH54, a RAD54 Homologue in Saccharomyces cerevisiae, Is Required for Mitotic Diploid-Specific Recombination and Repair and for Meiosis

H. L. Klein
Department of Biochemistry and Kaplan Cancer Center, New York University Medical Center, New York, New York 10016

Most mitotic recombination and repair genes of Saccharomyces cerevisiae show no specificity of action for the genome ploidy. We describe here a novel repair and recombination gene that is specific for recombination and repair between homologous chromosomes. The RDH54 gene is homologous to the RAD54 gene, but rdh54 mutants do not show sensitivity to methyl methanesulfonate at concentrations that sensitize a rad54 mutant. However, the rdh54 null mutation enhances the methyl methanesulfonate sensitivity of a rad54 mutant and single rdh54 mutants are sensitive to prolonged exposure at high concentrations of methyl methanesulfonate. The RDH54 gene is required for recombination, but only in a diploid. We present evidence showing that the RDH54 gene is required for interhomologue gene conversion but not intrachromosomal gene conversion. The rdh54 mutation confers diploid-specific lethalities and reduced growth in various mutant backgrounds. These phenotypes are due to attempted recombination. The RDH54 gene is also required for meiosis as homozygous mutant diploids show very poor sporulation and reduced spore viability. The role of the RDH54 gene in mitotic repair and in meiosis and the pathway in which it acts are discussed.


This article has been cited by other articles:


Home page
 Mol. Cell. Biol.Home page
M. Trickey, M. Grimaldi, and H. Yamano
The Anaphase-Promoting Complex/Cyclosome Controls Repair and Recombination by Ubiquitylating Rhp54 in Fission Yeast
Mol. Cell. Biol., June 15, 2008; 28(12): 3905 - 3916.
[Abstract] [Full Text] [PDF]

Home page
 Genes Dev.Home page
V. Busygina, M. G. Sehorn, I. Y. Shi, H. Tsubouchi, G. S. Roeder, and P. Sung
Hed1 regulates Rad51-mediated recombination via a novel mechanism
Genes & Dev., March 15, 2008; 22(6): 786 - 795.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
A. V. Nimonkar, I. Amitani, R. J. Baskin, and S. C. Kowalczykowski
Single Molecule Imaging of Tid1/Rdh54, a Rad54 Homolog That Translocates on Duplex DNA and Can Disrupt Joint Molecules
J. Biol. Chem., October 19, 2007; 282(42): 30776 - 30784.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
F. Cortes-Ledesma, C. Tous, and A. Aguilera
Different genetic requirements for repair of replication-born double-strand breaks by sister-chromatid recombination and break-induced replication
Nucleic Acids Res., October 8, 2007; 35(19): 6560 - 6570.
[Abstract] [Full Text] [PDF]

Home page
 Genes Dev.Home page
L. S. Symington and W.-D. Heyer
Some disassembly required: role of DNA translocases in the disruption of recombination intermediates and dead-end complexes
Genes & Dev., September 15, 2006; 20(18): 2479 - 2486.
[Full Text] [PDF]

Home page
 Genes Dev.Home page
T. M. Holzen, P. P. Shah, H. A. Olivares, and D. K. Bishop
Tid1/Rdh54 promotes dissociation of Dmc1 from nonrecombinogenic sites on meiotic chromatin
Genes & Dev., September 15, 2006; 20(18): 2593 - 2604.
[Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
W.-D. Heyer, X. Li, M. Rolfsmeier, and X.-P. Zhang
Rad54: the Swiss Army knife of homologous recombination?
Nucleic Acids Res., September 10, 2006; 34(15): 4115 - 4125.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
P. Chi, Y. Kwon, C. Seong, A. Epshtein, I. Lam, P. Sung, and H. L. Klein
Yeast Recombination Factor Rdh54 Functionally Interacts with the Rad51 Recombinase and Catalyzes Rad51 Removal from DNA
J. Biol. Chem., September 8, 2006; 281(36): 26268 - 26279.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
M. D. Yandeau-Nelson, Y. Xia, J. Li, M. G. Neuffer, and P. S. Schnable
Unequal Sister Chromatid and Homolog Recombination at a Tandem Duplication of the a1 Locus in Maize
Genetics, August 1, 2006; 173(4): 2211 - 2226.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
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]

Home page
 GeneticsHome page
H. Shaked, N. Avivi-Ragolsky, and A. A. Levy
Involvement of the Arabidopsis SWI2/SNF2 Chromatin Remodeling Gene Family in DNA Damage Response and Recombination
Genetics, June 1, 2006; 173(2): 985 - 994.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
A. Flaus, D. M. A. Martin, G. J. Barton, and T. Owen-Hughes
Identification of multiple distinct Snf2 subfamilies with conserved structural motifs
Nucleic Acids Res., May 31, 2006; 34(10): 2887 - 2905.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
J. Wesoly, S. Agarwal, S. Sigurdsson, W. Bussen, S. Van Komen, J. Qin, H. van Steeg, J. van Benthem, E. Wassenaar, W. M. Baarends, et al.
Differential Contributions of Mammalian Rad54 Paralogs to Recombination, DNA Damage Repair, and Meiosis
Mol. Cell. Biol., February 1, 2006; 26(3): 976 - 989.
[Abstract] [Full Text] [PDF]

Home page
 J. Cell Biol.Home page
A. V. Kateneva, A. A. Konovchenko, V. Guacci, and M. E. Dresser
Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae
J. Cell Biol., October 24, 2005; 171(2): 241 - 253.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
H. Xu, C. Boone, and H. L. Klein
Mrc1 Is Required for Sister Chromatid Cohesion To Aid in Recombination Repair of Spontaneous Damage
Mol. Cell. Biol., August 15, 2004; 24(16): 7082 - 7090.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
P. Schar, M. Fasi, and R. Jessberger
SMC1 coordinates DNA double-strand break repair pathways
Nucleic Acids Res., July 27, 2004; 32(13): 3921 - 3929.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
M. Smirnova, S. Van Komen, P. Sung, and H. L. Klein
Effects of Tumor-associated Mutations on Rad54 Functions
J. Biol. Chem., June 4, 2004; 279(23): 24081 - 24088.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Biol. CellHome page
M. G. Catlett and S. L. Forsburg
Schizosaccharomyces pombe Rdh54 (TID1) Acts with Rhp54 (RAD54) to Repair Meiotic Double-Strand Breaks
Mol. Biol. Cell, November 1, 2003; 14(11): 4707 - 4720.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
J. Yoshida, K. Umezu, and H. Maki
Positive and Negative Roles of Homologous Recombination in the Maintenance of Genome Stability in Saccharomyces cerevisiae
Genetics, May 1, 2003; 164(1): 31 - 46.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
M. Shinohara, K. Sakai, A. Shinohara, and D. K. Bishop
Crossover Interference in Saccharomyces cerevisiae Requires a TID1/RDH54- and DMC1-Dependent Pathway
Genetics, April 1, 2003; 163(4): 1273 - 1286.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
J. Schmuckli-Maurer, M. Rolfsmeier, H. Nguyen, and W.-D. Heyer
Genome instability in rad54 mutants of Saccharomyces cerevisiae
Nucleic Acids Res., February 1, 2003; 31(3): 1013 - 1023.
[Abstract] [Full Text] [PDF]

Home page
 Microbiol. Mol. Biol. Rev.Home page
L. S. Symington
Role of RAD52 Epistasis Group Genes in Homologous Recombination and Double-Strand Break Repair
Microbiol. Mol. Biol. Rev., December 1, 2002; 66(4): 630 - 670.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
M. Maftahi, J. C. Hope, L. Delgado-Cruzata, C. S. Han, and G. A. Freyer
The severe slow growth of {Delta}srs2{Delta}rqh1 in Schizosaccharomyces pombe is suppressed by loss of recombination and checkpoint genes
Nucleic Acids Res., October 15, 2002; 30(21): 4781 - 4792.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
E. Shor, S. Gangloff, M. Wagner, J. Weinstein, G. Price, and R. Rothstein
Mutations in Homologous Recombination Genes Rescue top3 Slow Growth in Saccharomyces cerevisiae
Genetics, October 1, 2002; 162(2): 647 - 662.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
G. Ira and J. E. Haber
Characterization of RAD51-Independent Break-Induced Replication That Acts Preferentially with Short Homologous Sequences
Mol. Cell. Biol., September 15, 2002; 22(18): 6384 - 6392.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
W. J. Kim, E. J. Park, H. Lee, R. H. Seong, and S. D. Park
Physical Interaction between Recombinational Proteins Rhp51 and Rad22 in Schizosaccharomyces pombe
J. Biol. Chem., August 9, 2002; 277(33): 30264 - 30270.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
P. M. Kim, K. S. Paffett, J. A. Solinger, W.-D. Heyer, and J. A. Nickoloff
Spontaneous and double-strand break-induced recombination, and gene conversion tract lengths, are differentially affected by overexpression of wild-type or ATPase-defective yeast Rad54
Nucleic Acids Res., July 1, 2002; 30(13): 2727 - 2735.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
K. Tanaka, W. Kagawa, T. Kinebuchi, H. Kurumizaka, and K. Miyagawa
Human Rad54B is a double-stranded DNA-dependent ATPase and has biochemical properties different from its structural homolog in yeast, Tid1/Rdh54
Nucleic Acids Res., March 15, 2002; 30(6): 1346 - 1353.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
M. Fasullo, P. Giallanza, Z. Dong, C. Cera, and T. Bennett
Saccharomyces cerevisiae rad51 Mutants Are Defective in DNA Damage-Associated Sister Chromatid Exchanges but Exhibit Increased Rates of Homology-Directed Translocations
Genetics, July 1, 2001; 158(3): 959 - 972.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
L. Signon, A. Malkova, M. L. Naylor, H. Klein, and J. E. Haber
Genetic Requirements for RAD51- and RAD54-Independent Break-Induced Replication Repair of a Chromosomal Double-Strand Break
Mol. Cell. Biol., March 15, 2001; 21(6): 2048 - 2056.
[Abstract] [Full Text]

Home page
 Mol. Cell. Biol.Home page
L. Krejci, J. Damborsky, B. Thomsen, M. Duno, and C. Bendixen
Molecular Dissection of Interactions between Rad51 and Members of the Recombination-Repair Group
Mol. Cell. Biol., February 1, 2001; 21(3): 966 - 976.
[Abstract] [Full Text]

Home page
 GeneticsHome page
H. L. Klein
Mutations in Recombinational Repair and in Checkpoint Control Genes Suppress the Lethal Combination of srs2{{Delta}} With Other DNA Repair Genes in Saccharomyces cerevisiae
Genetics, February 1, 2001; 157(2): 557 - 565.
[Abstract] [Full Text]

Home page
 Proc. Natl. Acad. Sci. USAHome page
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]

Home page
 Genes Dev.Home page
G. Petukhova, P. Sung, and H. Klein
Promotion of Rad51-dependent D-loop formation by yeast recombination factor Rdh54/Tid1
Genes & Dev., September 1, 2000; 14(17): 2206 - 2215.
[Abstract] [Full Text]

Home page
 Mol. Cell. Biol.Home page
M. L. G. Dronkert, H. B. Beverloo, R. D. Johnson, J. H. J. Hoeijmakers, M. Jasin, and R. Kanaar
Mouse RAD54 Affects DNA Double-Strand Break Repair and Sister Chromatid Exchange
Mol. Cell. Biol., May 1, 2000; 20(9): 3147 - 3156.
[Abstract] [Full Text]

Home page
 GeneticsHome page
Y. Bai, A. P. Davis, and L. S. Symington
A Novel Allele of RAD52 That Causes Severe DNA Repair and Recombination Deficiencies Only in the Absence of RAD51 or RAD59
Genetics, November 1, 1999; 153(3): 1117 - 1130.
[Abstract] [Full Text]

Home page
 J. Biol. Chem.Home page
G. Petukhova, S. Van Komen, S. Vergano, H. Klein, and P. Sung
Yeast Rad54 Promotes Rad51-dependent Homologous DNA Pairing via ATP Hydrolysis-driven Change in DNA Double Helix Conformation
J. Biol. Chem., October 8, 1999; 274(41): 29453 - 29462.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
R. Kooistra, A. Pastink, J. B. M. Zonneveld, P. H. M. Lohman, and J. C. J. Eeken
The Drosophila melanogaster DmRAD54 Gene Plays a Crucial Role in Double-Strand Break Repair after P-Element Excision and Acts Synergistically with Ku70 in the Repair of X-Ray Damage
Mol. Cell. Biol., September 1, 1999; 19(9): 6269 - 6275.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
L. K. Lewis, J. W. Westmoreland, and M. A. Resnick
Repair of Endonuclease-Induced Double-Strand Breaks in Saccharomyces cerevisiae: Essential Role for Genes Associated with Nonhomologous End-Joining
Genetics, August 1, 1999; 152(4): 1513 - 1529.
[Abstract] [Full Text]

Home page
 Microbiol. Mol. Biol. Rev.Home page
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]

Home page
 Mol. Cell. Biol.Home page
T. Rijkers, J. Van Den Ouweland, B. Morolli, A. G. Rolink, W. M. Baarends, P. P. H. Van Sloun, P. H. M. Lohman, and A. Pastink
Targeted Inactivation of Mouse RAD52 Reduces Homologous Recombination but Not Resistance to Ionizing Radiation
Mol. Cell. Biol., November 1, 1998; 18(11): 6423 - 6429.
[Abstract] [Full Text]

Home page
 GeneticsHome page
D. A. Bressan, H. A. Olivares, B. E. Nelms, and J. H. J. Petrini
Alteration of N-Terminal Phosphoesterase Signature Motifs Inactivates Saccharomyces cerevisiae Mre11
Genetics, October 1, 1998; 150(2): 591 - 600.
[Abstract] [Full Text]

Home page
 Genes Dev.Home page
A. Ghabrial, R. P. Ray, and T. Schüpbach
okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis
Genes & Dev., September 1, 1998; 12(17): 2711 - 2723.
[Abstract] [Full Text]

Home page
 J. Biol. Chem.Home page
K. M. Trujillo, S.-S. F. Yuan, E. Y.-H. P. Lee, and P. Sung
Nuclease Activities in a Complex of Human Recombination and DNA Repair Factors Rad50, Mre11, and p95
J. Biol. Chem., August 21, 1998; 273(34): 21447 - 21450.
[Abstract] [Full Text] [PDF]

Home page
 Genes Dev.Home page
S. L. Gasior, A. K. Wong, Y. Kora, A. Shinohara, and D. K. Bishop
Rad52 associates with RPA and functions with Rad55 and Rad57 to assemble meiotic recombination complexes
Genes & Dev., July 15, 1998; 12(14): 2208 - 2221.
[Abstract] [Full Text]