Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 27 October 2000:
Vol. 290. no. 5492, pp. 806 - 809
DOI: 10.1126/science.290.5492.806
Prev | Table of Contents | Next

Reports

Direct Coupling Between Meiotic DNA Replication and Recombination Initiation

Valérie Borde,1 Alastair S. H. Goldman,2 Michael Lichten1*

During meiosis in Saccharomyces cerevisiae, DNA replication occurs 1.5 to 2 hours before recombination initiates by DNA double-strand break formation. We show that replication and recombination initiation are directly linked. Blocking meiotic replication prevented double-strand break formation in a replication-checkpoint-independent manner, and delaying replication of a chromosome segment specifically delayed break formation in that segment. Consequently, the time between replication and break formation was held constant in all regions. We suggest that double-strand break formation occurs as part of a process initiated by DNA replication, which thus determines when meiotic recombination initiates on a regional rather than a cell-wide basis.

1 Laboratory of Biochemistry, Division of Basic Science, National Cancer Institute, Bethesda, MD 20892-4255, USA.
2 Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, UK.
*   To whom correspondence should be addressed. E-mail: lichten{at}helix.nih.gov

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis.
P. Jordan, A. Copsey, L. Newnham, E. Kolar, M. Lichten, and E. Hoffmann (2009)
Genes & Dev. 23, 2237-2251
   Abstract »    Full Text »    PDF »
Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes.
K. Kugou, T. Fukuda, S. Yamada, M. Ito, H. Sasanuma, S. Mori, Y. Katou, T. Itoh, K. Matsumoto, T. Shibata, et al. (2009)
Mol. Biol. Cell 20, 3064-3076
   Abstract »    Full Text »    PDF »
Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis.
W. P. Pawlowski, C.-J. R. Wang, I. N. Golubovskaya, J. M. Szymaniak, L. Shi, O. Hamant, T. Zhu, L. Harper, W. F. Sheridan, and W. Z. Cande (2009)
PNAS 106, 3603-3608
   Abstract »    Full Text »    PDF »
Cdc7-Dbf4 Regulates NDT80 Transcription as Well as Reductional Segregation during Budding Yeast Meiosis.
H.-C. Lo, L. Wan, A. Rosebrock, B. Futcher, and N. M. Hollingsworth (2008)
Mol. Biol. Cell 19, 4956-4967
   Abstract »    Full Text »    PDF »
Cohesin and Recombination Proteins Influence the G1-to-S Transition in Azygotic Meiosis in Schizosaccharomyces pombe.
E. Doll, M. Molnar, G. Cuanoud, G. Octobre, V. Latypov, K. Ludin, and J. Kohli (2008)
Genetics 180, 727-740
   Abstract »    Full Text »    PDF »
SWI1 Is Required for Meiotic Chromosome Remodeling Events.
K. A. Boateng, X. Yang, F. Dong, H. A. Owen, and C. A. Makaroff (2008)
Mol Plant 1, 620-633
   Abstract »    Full Text »    PDF »
Coupling meiotic chromosome axis integrity to recombination.
A. Storlazzi, S. Tesse, G. Ruprich-Robert, S. Gargano, S. Poggeler, N. Kleckner, and D. Zickler (2008)
Genes & Dev. 22, 796-809
   Abstract »    Full Text »    PDF »
Targeted induction of meiotic double-strand breaks reveals chromosomal domain-dependent regulation of Spo11 and interactions among potential sites of meiotic recombination.
T. Fukuda, K. Kugou, H. Sasanuma, T. Shibata, and K. Ohta (2008)
Nucleic Acids Res. 36, 984-997
   Abstract »    Full Text »    PDF »
Regulating the formation of DNA double-strand breaks in meiosis.
H. Murakami and S. Keeney (2008)
Genes & Dev. 22, 286-292
   Full Text »    PDF »
Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast.
L. Wan, H. Niu, B. Futcher, C. Zhang, K. M. Shokat, S. J. Boulton, and N. M. Hollingsworth (2008)
Genes & Dev. 22, 386-397
   Abstract »    Full Text »    PDF »
Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination.
H. Sasanuma, K. Hirota, T. Fukuda, N. Kakusho, K. Kugou, Y. Kawasaki, T. Shibata, H. Masai, and K. Ohta (2008)
Genes & Dev. 22, 398-410
   Abstract »    Full Text »    PDF »
Mei4p coordinates the onset of meiosis I by regulating cdc25+ in fission yeast.
Y. Murakami-Tonami, C. Yamada-Namikawa, A. Tochigi, N. Hasegawa, H. Kojima, M. Kunimatsu, M. Nakanishi, and H. Murakami (2007)
PNAS 104, 14688-14693
   Abstract »    Full Text »    PDF »
Meiotic recombination-related DNA synthesis and its implications for cross-over and non-cross-over recombinant formation.
M. Terasawa, H. Ogawa, Y. Tsukamoto, M. Shinohara, K. Shirahige, N. Kleckner, and T. Ogawa (2007)
PNAS 104, 5965-5970
   Abstract »    Full Text »    PDF »
Genome-Wide Redistribution of Meiotic Double-Strand Breaks in Saccharomyces cerevisiae.
N. Robine, N. Uematsu, F. Amiot, X. Gidrol, E. Barillot, A. Nicolas, and V. Borde (2007)
Mol. Cell. Biol. 27, 1868-1880
   Abstract »    Full Text »    PDF »
Meiotic association between Spo11 regulated by Rec102, Rec104 and Rec114.
H. Sasanuma, H. Murakami, T. Fukuda, T. Shibata, A. Nicolas, and K. Ohta (2007)
Nucleic Acids Res. 35, 1119-1133
   Abstract »    Full Text »    PDF »
Perturbation of the Activity of Replication Origin by Meiosis-specific Transcription.
S. Mori and K. Shirahige (2007)
J. Biol. Chem. 282, 4447-4452
   Abstract »    Full Text »    PDF »
Chemical Inactivation of Cdc7 Kinase in Budding Yeast Results in a Reversible Arrest That Allows Efficient Cell Synchronization Prior to Meiotic Recombination.
L. Wan, C. Zhang, K. M. Shokat, and N. M. Hollingsworth (2006)
Genetics 174, 1767-1774
   Abstract »    Full Text »    PDF »
The Arabidopsis SKP1 homolog ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus.
X. Yang, L. Timofejeva, H. Ma, and C. A. Makaroff (2006)
J. Cell Sci. 119, 3754-3763
   Abstract »    Full Text »    PDF »
Saccharomyces cerevisiae Mer2, Mei4 and Rec114 Form a Complex Required for Meiotic Double-Strand Break Formation.
J. Li, G. W. Hooker, and G. S. Roeder (2006)
Genetics 173, 1969-1981
   Abstract »    Full Text »    PDF »
Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast.
K. Ogino, K. Hirota, S. Matsumoto, T. Takeda, K. Ohta, K.-i. Arai, and H. Masai (2006)
PNAS 103, 8131-8136
   Abstract »    Full Text »    PDF »
Global Analysis of the Relationship between the Binding of the Bas1p Transcription Factor and Meiosis-Specific Double-Strand DNA Breaks in Saccharomyces cerevisiae.
P. A. Mieczkowski, M. Dominska, M. J. Buck, J. L. Gerton, J. D. Lieb, and T. D. Petes (2006)
Mol. Cell. Biol. 26, 1014-1027
   Abstract »    Full Text »    PDF »
Rad3-Cds1 Mediates Coupling of Initiation of Meiotic Recombination with DNA Replication: Mei4-DEPENDENT TRANSCRIPTION AS A POTENTIAL TARGET OF MEIOTIC CHECKPOINT.
K. Ogino and H. Masai (2006)
J. Biol. Chem. 281, 1338-1344
   Abstract »    Full Text »    PDF »
Activation of an Alternative, Rec12 (Spo11)-Independent Pathway of Fission Yeast Meiotic Recombination in the Absence of a DNA Flap Endonuclease.
J. A. Farah, G. Cromie, L. Davis, W. W. Steiner, and G. R. Smith (2005)
Genetics 171, 1499-1511
   Abstract »    Full Text »    PDF »
Set1- and Clb5-deficiencies disclose the differential regulation of centromere and telomere dynamics in Saccharomyces cerevisiae meiosis.
E. Trelles-Sticken, S. Bonfils, J. Sollier, V. Geli, H. Scherthan, and C. de La Roche Saint-Andre (2005)
J. Cell Sci. 118, 4985-4994
   Abstract »    Full Text »    PDF »
A Meiosis-Specific Cyclin Regulated by Splicing Is Required for Proper Progression through Meiosis.
J. Malapeira, A. Moldon, E. Hidalgo, G. R. Smith, P. Nurse, and J. Ayte (2005)
Mol. Cell. Biol. 25, 6330-6337
   Abstract »    Full Text »    PDF »
A checkpoint control linking meiotic S phase and recombination initiation in fission yeast.
Y. Tonami, H. Murakami, K. Shirahige, and M. Nakanishi (2005)
PNAS 102, 5797-5801
   Abstract »    Full Text »    PDF »
Meiosis-Specific Regulation of the Saccharomyces cerevisiae S-Phase Cyclin CLB5 Is Dependent on MluI Cell Cycle Box (MCB) Elements in Its Promoter but Is Independent of MCB-Binding Factor Activity.
S. A. Raithatha and D. T. Stuart (2005)
Genetics 169, 1329-1342
   Abstract »    Full Text »    PDF »
Involvement of Sir2/4 in Silencing of DNA Breakage and Recombination on Mouse YACs during Yeast Meiosis.
Y. Klieger, O. Yizhar, D. Zenvirth, N. Shtepel-Milman, M. Snoek, and G. Simchen (2005)
Mol. Biol. Cell 16, 1449-1455
   Abstract »    Full Text »    PDF »
The control of Spo11's interaction with meiotic recombination hotspots.
S. Prieler, A. Penkner, V. Borde, and F. Klein (2005)
Genes & Dev. 19, 255-269
   Abstract »    Full Text »    PDF »
Loss of Meiotic Rereplication Block in Saccharomyces cerevisiae Cells Defective in Cdc28p Regulation.
L. M. Rice, C. Plakas, and J. T. Nickels Jr. (2005)
Eukaryot. Cell 4, 55-62
   Abstract »    Full Text »    PDF »
Does Chromosome Size Affect Map Distance and Genetic Interference in Budding Yeast?.
D. Turney, T. de los Santos, and N. M. Hollingsworth (2004)
Genetics 168, 2421-2424
   Abstract »    Full Text »    PDF »
Compartmentalization of the Yeast Meiotic Nucleus Revealed by Analysis of Ectopic Recombination.
H. B. Schlecht, M. Lichten, and A. S. H. Goldman (2004)
Genetics 168, 1189-1203
   Abstract »    Full Text »    PDF »
Modifying sister chromatid cohesion for meiosis.
Y. Watanabe (2004)
J. Cell Sci. 117, 4017-4023
   Abstract »    Full Text »    PDF »
Cyclin B-Cdk Activity Stimulates Meiotic Rereplication in Budding Yeast.
R. Strich, M. J. Mallory, M. Jarnik, and K. F. Cooper (2004)
Genetics 167, 1621-1628
   Abstract »    Full Text »    PDF »
Non-random asynchronous replication at 22q11.2 favours unequal meiotic crossovers leading to the human 22q11.2 deletion.
A Baumer, M Riegel, and A Schinzel (2004)
J. Med. Genet. 41, 413-420
   Abstract »    Full Text »    PDF »
The Meiosis-specific Protein Kinase Ime2 Directs Phosphorylation of Replication Protein A.
D. M. Clifford, S. M. Marinco, and G. S. Brush (2004)
J. Biol. Chem. 279, 6163-6170
   Abstract »    Full Text »    PDF »
A CDC45 Homolog in Arabidopsis Is Essential for Meiosis, as Shown by RNA Interference-Induced Gene Silencing.
R. Stevens, M. Grelon, D. Vezon, J. Oh, P. Meyer, C. Perennes, S. Domenichini, and C. Bergounioux (2004)
PLANT CELL 16, 99-113
   Abstract »    Full Text »    PDF »
Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites.
H. Murakami, V. Borde, T. Shibata, M. Lichten, and K. Ohta (2003)
Nucleic Acids Res. 31, 4085-4090
   Abstract »    Full Text »    PDF »
The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis.
R. Mercier, Susan. J. Armstrong, C. Horlow, N. P. Jackson, C. A. Makaroff, D. Vezon, G. Pelletier, G. H. Jones, and F. C. H. Franklin (2003)
Development 130, 3309-3318
   Abstract »    Full Text »    PDF »
Meiosis, recombination and chromosomes: a review of gene isolation and fluorescent in situ hybridization data in plants.
T. Schwarzacher (2003)
J. Exp. Bot. 54, 11-23
   Abstract »    Full Text »    PDF »
A role for Ddc1 in signaling meiotic double-strand breaks at the pachytene checkpoint.
E.-J. E. Hong and G. S. Roeder (2002)
Genes & Dev. 16, 363-376
   Abstract »    Full Text »    PDF »
Meiotic Deletion at the BUF1 Locus of the Fungus Magnaporthe grisea Is Controlled by Interaction With the Homologous Chromosome.
M. L. Farman (2002)
Genetics 160, 137-148
   Abstract »    Full Text »    PDF »
Replication protein A is sequentially phosphorylated during meiosis.
G. S. Brush, D. M. Clifford, S. M. Marinco, and A. J. Bartrand (2001)
Nucleic Acids Res. 29, 4808-4817
   Abstract »    Full Text »    PDF »
Counteracting Regulation of Chromatin Remodeling at a Fission Yeast cAMP Responsive Element-Related Recombination Hotspot by Stress-Activated Protein Kinase, cAMP-Dependent Kinase and Meiosis Regulators.
K.-i. Mizuno, T. Hasemi, T. Ubukata, T. Yamada, E. Lehmann, J. Kohli, Y. Watanabe, Y. Iino, M. Yamamoto, M. E. Fox, et al. (2001)
Genetics 159, 1467-1478
   Abstract »    Full Text »    PDF »
Circles: The replication-recombination-chromosome segregation connection.
F.-X. Barre, B. Soballe, B. Michel, M. Aroyo, M. Robertson, and D. Sherratt (2001)
PNAS 98, 8189-8195
   Abstract »    Full Text »    PDF »
Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe.
L. Davis and G. R. Smith (2001)
PNAS 98, 8395-8402
   Abstract »    Full Text »    PDF »
Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2.
A. J. MacQueen and A. M. Villeneuve (2001)
Genes & Dev. 15, 1674-1687
   Abstract »    Full Text »    PDF »
Local Rates of Recombination Are Positively Correlated with GC Content in the Human Genome.
S. M. Fullerton, A. Bernardo Carvalho, and A. G. Clark (2001)
Mol. Biol. Evol. 18, 1139-1142
   Full Text »
Fidelity of Mitotic Double-Strand-Break Repair in Saccharomyces cerevisiae: A Role for SAE2/COM1.
A. J. Rattray, C. B. McGill, B. K. Shafer, and J. N. Strathern (2001)
Genetics 158, 109-122
   Abstract »    Full Text »
The Saccharomyces cerevisiae MUM2 Gene Interacts With the DNA Replication Machinery and Is Required for Meiotic Levels of Double Strand Breaks.
L. Davis, M. Barbera, A. McDonnell, K. McIntyre, R. Sternglanz, Q.-w. Jin, J. Loidl, and J. Engebrecht (2001)
Genetics 157, 1179-1189
   Abstract »    Full Text »
Essential Role of MCM Proteins in Premeiotic DNA Replication.
K. Lindner, J. Gregan, S. Montgomery, and S. E. Kearsey (2002)
Mol. Biol. Cell 13, 435-444
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)