XRS2, a DNA Repair Gene of Saccharomyces cerevisiae, Is Needed for Meiotic Recombination

INVESTIGATIONS

XRS2, a DNA Repair Gene of Saccharomyces cerevisiae, Is Needed for Meiotic Recombination

E. L. Ivanov, V. G. Korolev and F. Fabre
Institut Curie, Section de Biologie, Centre Universitaire, 91405 Orsay Cedex, France Present address: Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, Massachusetts 02254-9110.

The XRS2 gene of Saccharomyces cerevisiae has been previously identified as a DNA repair gene. In this communication, we show that XRS2 also encodes an essential meiotic function. Spore inviability of xrs2 strains is rescued by a spo13 mutation, but meiotic recombination (both gene conversion and crossing over) is highly depressed in spo13 xrs2 diploids. The xrs2 mutation suppresses spore inviability of a spo13 rad52 strain suggesting that XRS2 acts prior to RAD52 in the meiotic recombination pathway. In agreement with the genetic data, meiosis-specific double-strand breaks at the ARG4 meiotic recombination hotspot are not detected in xrs2 strains. Despite its effects on meiotic recombination, the xrs2 mutation does not prevent mitotic recombination events, including homologous integration of linear DNA, mating-type switching and radiation-induced gene conversion. Moreover, xrs2 strains display a mitotic hyper-rec phenotype. Haploid xrs2 cells fail to carry out G2-repair of gamma-induced lesions, whereas xrs2 diploids are able to perform some diploid-specific repair of these lesions. Meiotic and mitotic phenotypes of xrs2 cells are very similar to those of rad50 cells suggesting that XRS2 is involved in homologous recombination in a way analogous to that of RAD50.

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				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]

				W. J. Cummings, S. T. Merino, K. G. Young, L. Li, C. W. Johnson, E. A. Sierra, and M. E. Zolan The Coprinus cinereus adherin Rad9 functions in Mre11-dependent DNA repair, meiotic sister-chromatid cohesion, and meiotic homolog pairing PNAS, November 12, 2002; 99(23): 14958 - 14963. [Abstract] [Full Text] [PDF]

				P. Pichierri, D. Averbeck, and F. Rosselli DNA cross-link-dependent RAD50/MRE11/NBS1 subnuclear assembly requires the Fanconi anemia C protein Hum. Mol. Genet., October 2, 2002; 11(21): 2531 - 2546. [Abstract] [Full Text] [PDF]

				E. A. Morgan, N. Shah, and L. S. Symington The Requirement for ATP Hydrolysis by Saccharomyces cerevisiae Rad51 Is Bypassed by Mating-Type Heterozygosity or RAD54 in High Copy Mol. Cell. Biol., September 15, 2002; 22(18): 6336 - 6343. [Abstract] [Full Text] [PDF]

				C. F. Bender, M. L. Sikes, R. Sullivan, L. E. Huye, M. M. Le Beau, D. B. Roth, O. K. Mirzoeva, E. M. Oltz, and J. H. J. Petrini Cancer predisposition and hematopoietic failure in Rad50S/S mice Genes & Dev., September 1, 2002; 16(17): 2237 - 2251. [Abstract] [Full Text] [PDF]

				G. M. Manthey and A. M. Bailis Multiple Pathways Promote Short-Sequence Recombination in Saccharomyces cerevisiae Mol. Cell. Biol., August 1, 2002; 22(15): 5347 - 5356. [Abstract] [Full Text] [PDF]

				S. Moreau, E. A. Morgan, and L. S. Symington Overlapping Functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 Nucleases in DNA Metabolism Genetics, December 1, 2001; 159(4): 1423 - 1433. [Abstract] [Full Text] [PDF]

				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]

				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]

				S. T. Merino, W. J. Cummings, S. N. Acharya, and M. E. Zolan Replication-dependent early meiotic requirement for Spo11 and Rad50 PNAS, September 5, 2000; (2000) 190346097. [Abstract] [Full Text]

				X. Pan and D. R. F. Leach The roles of mutS, sbcCD and recA in the propagation of TGG repeats in Escherichia coli Nucleic Acids Res., August 15, 2000; 28(16): 3178 - 3184. [Abstract] [Full Text] [PDF]

				H. Tsubouchi and H. Ogawa Exo1 Roles for Repair of DNA Double-Strand Breaks and Meiotic Crossing Over in Saccharomyces cerevisiae Mol. Biol. Cell, July 1, 2000; 11(7): 2221 - 2233. [Abstract] [Full Text]

				D. A. Bressan, B. K. Baxter, and J. H. J. Petrini The Mre11-Rad50-Xrs2 Protein Complex Facilitates Homologous Recombination-Based Double-Strand Break Repair in Saccharomyces cerevisiae Mol. Cell. Biol., November 1, 1999; 19(11): 7681 - 7687. [Abstract] [Full Text] [PDF]

				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]

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				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]

				T. T. Paull and M. Gellert Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex Genes & Dev., May 15, 1999; 13(10): 1276 - 1288. [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]

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				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]

				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]