Genetics, Vol. 156, 1549-1557, December 2000, Copyright © 2000

Decreased Meiotic Intergenic Recombination and Increased Meiosis I Nondisjunction in exo1 Mutants of Saccharomyces cerevisiae

David T. Kirkpatricka, John R. Fergusonb, Thomas D. Petesa, and Lorraine S. Symingtonb
a Department of Biology and Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, North Carolina 27599-3280
b Department of Microbiology, Columbia University College of Physicians and Surgeons, New York, New York 10032

Corresponding author: Lorraine S. Symington, Department of Microbiology and Institute of Cancer Research, Columbia University, 701 W. 168th St., New York, NY 10032., lss5{at}columbia.edu (E-mail)

Communicating editor: M. LICHTEN

Exonuclease I was originally identified as a 5' -> 3' deoxyribonuclease present in fractionated extracts of Schizosaccharomyces pombe and Saccharomyces cerevisiae. Genetic analysis of exo1 mutants of both yeasts revealed no major defect in meiosis, suggesting that exonuclease I is unlikely to be the primary activity that processes meiosis-specific double-strand breaks (DSBs). We report here that exo1 mutants of S. cerevisiae exhibit subtle but complex defects in meiosis. Diploids containing a homozygous deletion of EXO1 show decreased spore viability associated with an increase in meiosis I nondisjunction, while intergenic recombination is reduced about twofold. Exo1p functions in the same pathway as Msh5p for intergenic recombination. The length of heteroduplex tracts within the HIS4 gene is unaffected by the exo1 mutation. These results suggest that Exo1p is unlikely to play a major role in processing DSBs to form single-stranded tails at HIS4, but instead appears to promote crossing over to ensure disjunction of homologous chromosomes. In addition, our data indicate that exonuclease I may have a minor role in the correction of large DNA mismatches that occur in heteroduplex DNA during meiotic recombination at the HIS4 locus.





This article has been cited by other articles:


Home page
GeneticsHome page
J. E. Stone and T. D. Petes
Analysis of the Proteins Involved in the in Vivo Repair of Base-Base Mismatches and Four-Base Loops Formed During Meiotic Recombination in the Yeast Saccharomyces cerevisiae
Genetics, July 1, 2006; 173(3): 1223 - 1239.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. Malkova, J. Swanson, M. German, J. H. McCusker, E. A. Housworth, F. W. Stahl, and J. E. Haber
Gene Conversion and Crossing Over Along the 405-kb Left Arm of Saccharomyces cerevisiae Chromosome VII
Genetics, September 1, 2004; 168(1): 49 - 63.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. K. Zubko, S. Guillard, and D. Lydall
Exo1 and Rad24 Differentially Regulate Generation of ssDNA at Telomeres of Saccharomyces cerevisiae cdc13-1 Mutants
Genetics, September 1, 2004; 168(1): 103 - 115.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. Maringele and D. Lydall
EXO1 Plays a Role in Generating Type I and Type II Survivors in Budding Yeast
Genetics, April 1, 2004; 166(4): 1641 - 1649.
[Abstract] [Full Text] [PDF]


Home page
J. Cell Sci.Home page
D. Lydall
Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways
J. Cell Sci., October 15, 2003; 116(20): 4057 - 4065.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
K. Wei, A. B. Clark, E. Wong, M. F. Kane, D. J. Mazur, T. Parris, N. K. Kolas, R. Russell, H. Hou Jr., B. Kneitz, et al.
Inactivation of Exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility
Genes & Dev., March 1, 2003; 17(5): 603 - 614.
[Abstract] [Full Text] [PDF]


Home page
Mol. Cell. Biol.Home page
J. L. Argueso, A. W. Kijas, S. Sarin, J. Heck, M. Waase, and E. Alani
Systematic Mutagenesis of the Saccharomyces cerevisiae MLH1 Gene Reveals Distinct Roles for Mlh1p in Meiotic Crossing Over and in Vegetative and Meiotic Mismatch Repair
Mol. Cell. Biol., February 1, 2003; 23(3): 873 - 886.
[Abstract] [Full Text]


Home page
GeneticsHome page
E. R. Hoffmann, P. V. Shcherbakova, T. A. Kunkel, and R. H. Borts
MLH1 Mutations Differentially Affect Meiotic Functions in Saccharomyces cerevisiae
Genetics, February 1, 2003; 163(2): 515 - 526.
[Abstract] [Full Text] [PDF]


Home page
Mol. Cell. Biol.Home page
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]


Home page
J. Biol. Chem.Home page
T. Nakagawa and R. D. Kolodner
The MER3 DNA Helicase Catalyzes the Unwinding of Holliday Junctions
J. Biol. Chem., July 26, 2002; 277(31): 28019 - 28024.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. L. Argueso, D. Smith, J. Yi, M. Waase, S. Sarin, and E. Alani
Analysis of Conditional Mutations in the Saccharomyces cerevisiae MLH1 Gene in Mismatch Repair and in Meiotic Crossing Over
Genetics, March 1, 2002; 160(3): 909 - 921.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
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]


Home page
Mol. Cell. Biol.Home page
N. S. Amin, M.-N. Nguyen, S. Oh, and R. D. Kolodner
exo1-Dependent Mutator Mutations: Model System for Studying Functional Interactions in Mismatch Repair
Mol. Cell. Biol., August 1, 2001; 21(15): 5142 - 5155.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
H. M. Kearney, D. T. Kirkpatrick, J. L. Gerton, and T. D. Petes
Meiotic Recombination Involving Heterozygous Large Insertions in Saccharomyces cerevisiae: Formation and Repair of Large, Unpaired DNA Loops
Genetics, August 1, 2001; 158(4): 1457 - 1476.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
P. T. Tran, J. A. Simon, and R. M. Liskay
Interactions of Exo1p with components of MutLalpha in Saccharomyces cerevisiae
PNAS, July 24, 2001; (2001) 161175998.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. E. Novak, P. B. Ross-Macdonald, and G. S. Roeder
The Budding Yeast Msh4 Protein Functions in Chromosome Synapsis and the Regulation of Crossover Distribution
Genetics, July 1, 2001; 158(3): 1013 - 1025.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
T. Nakagawa, H. Flores-Rozas, and R. D. Kolodner
The MER3 Helicase Involved in Meiotic Crossing Over Is Stimulated by Single-stranded DNA-binding Proteins and Unwinds DNA in the 3' to 5' Direction
J. Biol. Chem., August 17, 2001; 276(34): 31487 - 31493.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
P. T. Tran, J. A. Simon, and R. M. Liskay
Interactions of Exo1p with components of MutLalpha in Saccharomyces cerevisiae
PNAS, August 14, 2001; 98(17): 9760 - 9765.
[Abstract] [Full Text] [PDF]