THE ROLE OF THE SPO11 GENE IN MEIOTIC RECOMBINATION IN YEAST

1 Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, Illinois 60637

Several complementary experimental approaches were used to demonstrate that the SPO11 gene is specifically required for meiotic recombination. First, sporulating cultures of spo11-1 mutant diploids were examined for landmark biochemical, cytological and genetic events of meiosis and ascosporogenesis. Cells entered sporulation with high efficiency and showed a near-doubling of DNA content. Synaptonemal complexes, hallmarks of intimate homologous pairing, and polycomplex structures appeared during meiotic prophase. Although spontaneous mitotic intra- and intergenic recombination occurred at normal levels, no meiotic recombination was observed. Whereas greater than 50% of cells completed both meiotic divisions, packaging of the four meiotic products into mature ascospores took place in only a small subset of asci. Haploidization occurred in less than 1% of viable colony-forming units. Second, the Rec- meiotic defect conferred by spo11-1 was confirmed by dyad analysis of spores derived from spo13-1 single-division meiosis in which recombination is not a requirement for viable ascospore production. Diploids homozygous for the spo13-1 mutation undergo meiotic levels of exchange followed by a single predominantly equational division and form asci containing two near-diploid spores. With the introduction of the spo11-1 mutation, high spore viability was retained, whereas intergenic recombination was reduced by more than 100-fold.

Submitted on October 5, 1984
Accepted on February 23, 1985




This article has been cited by other articles:


Home page
GeneticsHome page
G. G. Tevzadze, J. V. Pierce, and R. E. Esposito
Genetic Evidence for a SPO1-Dependent Signaling Pathway Controlling Meiotic Progression in Yeast
Genetics, March 1, 2007; 175(3): 1213 - 1227.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
K. L. Auld, A. L. Hitchcock, H. K. Doherty, S. Frietze, L. S. Huang, and P. A. Silver
The Conserved ATPase Get3/Arr4 Modulates the Activity of Membrane-Associated Proteins in Saccharomyces cerevisiae
Genetics, September 1, 2006; 174(1): 215 - 227.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
G. Valentin, E. Schwob, and F. D. Seta
Dual Role of the Cdc7-regulatory Protein Dbf4 during Yeast Meiosis
J. Biol. Chem., February 3, 2006; 281(5): 2828 - 2834.
[Abstract] [Full Text] [PDF]


Home page
JCBHome 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
Genes Dev.Home page
S. Prieler, A. Penkner, V. Borde, and F. Klein
The control of Spo11's interaction with meiotic recombination hotspots
Genes & Dev., January 15, 2005; 19(2): 255 - 269.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
H. Bhuiyan and K. Schmekel
Meiotic Chromosome Synapsis in Yeast Can Occur Without Spo11-Induced DNA Double-Strand Breaks
Genetics, October 1, 2004; 168(2): 775 - 783.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
R. Strich, M. J. Mallory, M. Jarnik, and K. F. Cooper
Cyclin B-Cdk Activity Stimulates Meiotic Rereplication in Budding Yeast
Genetics, August 1, 2004; 167(4): 1621 - 1628.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
W. Li, C. Chen, U. Markmann-Mulisch, L. Timofejeva, E. Schmelzer, H. Ma, and B. Reiss
The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis
PNAS, July 20, 2004; 101(29): 10596 - 10601.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
K. A. Henderson and S. Keeney
Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks
PNAS, March 30, 2004; 101(13): 4519 - 4524.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
A. Storlazzi, S. Tesse, S. Gargano, F. James, N. Kleckner, and D. Zickler
Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division
Genes & Dev., November 1, 2003; 17(21): 2675 - 2687.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. H. Enyenihi and W. S. Saunders
Large-Scale Functional Genomic Analysis of Sporulation and Meiosis in Saccharomyces cerevisiae
Genetics, January 1, 2003; 163(1): 47 - 54.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
M. A. Shonn, R. McCarroll, and A. W. Murray
Spo13 protects meiotic cohesin at centromeres in meiosis I
Genes & Dev., July 1, 2002; 16(13): 1659 - 1671.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
J. L. Gerton and J. L. DeRisi
Mnd1p: An evolutionarily conserved protein required for meiotic recombination
PNAS, May 14, 2002; 99(10): 6895 - 6900.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
K. Kee and S. Keeney
Functional Interactions Between SPO11 and REC102 During Initiation of Meiotic Recombination in Saccharomyces cerevisiae
Genetics, January 1, 2002; 160(1): 111 - 122.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
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]


Home page
GeneticsHome page
R. M. Q. Shanks, R. J. Kamieniecki, and D. S. Dawson
The Kar3-Interacting Protein Cik1p Plays a Critical Role in Passage Through Meiosis I in Saccharomyces cerevisiae
Genetics, November 1, 2001; 159(3): 939 - 951.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. Davis, M. Barbera, A. McDonnell, K. McIntyre, R. Sternglanz, Q.-w. Jin, J. Loidl, and J. Engebrecht
The Saccharomyces cerevisiae MUM2 Gene Interacts With the DNA Replication Machinery and Is Required for Meiotic Levels of Double Strand Breaks
Genetics, March 1, 2001; 157(3): 1179 - 1189.
[Abstract] [Full Text]


Home page
GeneticsHome page
T. M. Lamb and A. P. Mitchell
Coupling of Saccharomyces cerevisiae Early Meiotic Gene Expression to DNA Replication Depends Upon RPD3 and SIN3
Genetics, February 1, 2001; 157(2): 545 - 556.
[Abstract] [Full Text]


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


Home page
GeneticsHome page
K. O. Kelly, A. F. Dernburg, G. M. Stanfield, and A. M. Villeneuve
Caenorhabditis elegans msh-5 Is Required for Both Normal and Radiation-Induced Meiotic Crossing Over but Not for Completion of Meiosis
Genetics, October 1, 2000; 156(2): 617 - 630.
[Abstract] [Full Text]


Home page
Mol. Biol. CellHome page
P. D. Straight, T. H. Giddings Jr., and M. Winey
Mps1p Regulates Meiotic Spindle Pole Body Duplication in Addition to Having Novel Roles during Sporulation
Mol. Biol. Cell, October 1, 2000; 11(10): 3525 - 3537.
[Abstract] [Full Text]


Home page
Mol. Cell. Biol.Home page
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]


Home page
GeneticsHome page
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]


Home page
GeneticsHome page
X. Zeng and W. S. Saunders
The Saccharomyces cerevisiae Centromere Protein Slk19p Is Required for Two Successive Divisions During Meiosis
Genetics, June 1, 2000; 155(2): 577 - 587.
[Abstract] [Full Text]


Home page
Genes Dev.Home page
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]


Home page
GeneticsHome page
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]


Home page
Mol. Cell. Biol.Home page
V. Borde, T.-C. Wu, and M. Lichten
Use of a Recombination Reporter Insert To Define Meiotic Recombination Domains on Chromosome III of Saccharomyces cerevisiae
Mol. Cell. Biol., July 1, 1999; 19(7): 4832 - 4842.
[Abstract] [Full Text] [PDF]


Home page
Mol. Cell. Biol.Home page
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]


Home page
J. Cell Sci.Home page
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]


Home page
Genes Dev.Home page
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]


Home page
GeneticsHome page
J. Engebrecht, S. Masse, L. Davis, K. Rose, and T. Kessel
Yeast Meiotic Mutants Proficient for the Induction of Ectopic Recombination
Genetics, February 1, 1998; 148(2): 581 - 598.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
K. Ohta, A. Nicolas, M. Furuse, A. Nabetani, H. Ogawa, and T. Shibata
Mutations in the MRE11, RAD50, XRS2, and MRE2 genes alter chromatin configuration at meiotic DNA double-stranded break sites in premeiotic and meiotic cells
PNAS, January 20, 1998; 95(2): 646 - 651.
[Abstract] [Full Text] [PDF]


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


Home page
Proc. Natl. Acad. Sci. USAHome page
M. Joachimiak, G. Tevzadze, J. Podkowinski, R. Haselkorn, and P. Gornicki
Wheat cytosolic acetyl-CoA carboxylase complements an ACC1 null mutation in yeast
PNAS, September 2, 1997; 94(18): 9990 - 9995.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
L Xu, B M Weiner, and N Kleckner
Meiotic cells monitor the status of the interhomolog recombination complex.
Genes & Dev., January 1, 1997; 11(1): 106 - 118.
[Abstract] [PDF]


Home page
Genes Dev.Home page
N Burns, B Grimwade, P B Ross-Macdonald, E Y Choi, K Finberg, G S Roeder, and M Snyder
Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae.
Genes & Dev., May 1, 1994; 8(9): 1087 - 1105.
[Abstract] [PDF]


Home page
J. Cell Sci.Home page
G. Jenkins and A. Okumus
Indiscriminate synapsis in achiasmate Allium fistulosum L. (Liliaceae)
J. Cell Sci., October 1, 1992; 103(2): 415 - 422.
[Abstract] [PDF]


Home page
Genes Dev.Home page
K E Kirk and N R Morris
The tubB alpha-tubulin gene is essential for sexual development in Aspergillus nidulans.
Genes & Dev., November 1, 1991; 5(11): 2014 - 2023.
[Abstract] [PDF]