Genetics, Vol. 159, 453-470, October 2001, Copyright © 2001

Genes Involved in Sister Chromatid Separation and Segregation in the Budding Yeast Saccharomyces cerevisiae

Sue Bigginsa, Needhi Bhallaa, Amy Changa, Dana L. Smitha, and Andrew W. Murraya
a Department of Physiology, University of California, San Francisco, California 94143

Corresponding author: Sue Biggins, Division of Basic Sciences, Fred Hutchinson Cancer Research Ctr., 1100 Fairview Ave. N., A2-168, Seattle, WA 98109., sbiggins{at}fhcrc.org (E-mail)

Communicating editor: L. PILLUS

Accurate chromosome segregation requires the precise coordination of events during the cell cycle. Replicated sister chromatids are held together while they are properly attached to and aligned by the mitotic spindle at metaphase. At anaphase, the links between sisters must be promptly dissolved to allow the mitotic spindle to rapidly separate them to opposite poles. To isolate genes involved in chromosome behavior during mitosis, we microscopically screened a temperature-sensitive collection of budding yeast mutants that contain a GFP-marked chromosome. Nine LOC (loss of cohesion) complementation groups that do not segregate sister chromatids at anaphase were identified. We cloned the corresponding genes and performed secondary tests to determine their function in chromosome behavior. We determined that three LOC genes, PDS1, ESP1, and YCS4, are required for sister chromatid separation and three other LOC genes, CSE4, IPL1, and SMT3, are required for chromosome segregation. We isolated alleles of two genes involved in splicing, PRP16 and PRP19, which impair {alpha}-tubulin synthesis thus preventing spindle assembly, as well as an allele of CDC7 that is defective in DNA replication. We also report an initial characterization of phenotypes associated with the SMT3/SUMO gene and the isolation of WSS1, a high-copy smt3 suppressor.





This article has been cited by other articles:


Home page
GeneticsHome page
N. Meednu, H. Hoops, S. D'Silva, L. Pogorzala, S. Wood, D. Farkas, M. Sorrentino, E. Sia, P. Meluh, and R. K. Miller
The Spindle Positioning Protein Kar9p Interacts With the Sumoylation Machinery in Saccharomyces cerevisiae
Genetics, December 1, 2008; 180(4): 2033 - 2055.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
K. Uzunova, K. Gottsche, M. Miteva, S. R. Weisshaar, C. Glanemann, M. Schnellhardt, M. Niessen, H. Scheel, K. Hofmann, E. S. Johnson, et al.
Ubiquitin-dependent Proteolytic Control of SUMO Conjugates
J. Biol. Chem., November 23, 2007; 282(47): 34167 - 34175.
[Abstract] [Full Text] [PDF]


Home page
Mol. Biol. CellHome page
S. Thomas and K. B. Kaplan
A Bir1p Sli15p Kinetochore Passenger Complex Regulates Septin Organization during Anaphase
Mol. Biol. Cell, October 1, 2007; 18(10): 3820 - 3834.
[Abstract] [Full Text] [PDF]


Home page
Mol. Biol. CellHome page
A. C.J. Vas, C. A. Andrews, K. Kirkland Matesky, and D. J. Clarke
In Vivo Analysis of Chromosome Condensation in Saccharomyces cerevisiae
Mol. Biol. Cell, February 1, 2007; 18(2): 557 - 568.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
R. S. Hawley and W. D. Gilliland
Sometimes the Result Is Not the Answer: The Truths and the Lies That Come From Using the Complementation Test
Genetics, September 1, 2006; 174(1): 5 - 15.
[Abstract] [Full Text] [PDF]


Home page
ScienceHome page
W. J. Palframan, J. B. Meehl, S. L. Jaspersen, M. Winey, and A. W. Murray
Anaphase Inactivation of the Spindle Checkpoint
Science, August 4, 2006; 313(5787): 680 - 684.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Endocrinol. Metab.Home page
M. Vigodner, T. Ishikawa, P. N. Schlegel, and P. L. Morris
SUMO-1, human male germ cell development, and the androgen receptor in the testis of men with normal and abnormal spermatogenesis
Am J Physiol Endocrinol Metab, May 1, 2006; 290(5): E1022 - E1033.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
D. Nathan, K. Ingvarsdottir, D. E. Sterner, G. R. Bylebyl, M. Dokmanovic, J. A. Dorsey, K. A. Whelan, M. Krsmanovic, W. S. Lane, P. B. Meluh, et al.
Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications
Genes & Dev., April 15, 2006; 20(8): 966 - 976.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
Z. Wang, G. M. Jones, and G. Prelich
Genetic Analysis Connects SLX5 and SLX8 to the SUMO Pathway in Saccharomyces cerevisiae
Genetics, March 1, 2006; 172(3): 1499 - 1509.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
Y. Takahashi, V. Yong-Gonzalez, Y. Kikuchi, and A. Strunnikov
SIZ1/SIZ2 Control of Chromosome Transmission Fidelity Is Mediated by the Sumoylation of Topoisomerase II
Genetics, February 1, 2006; 172(2): 783 - 794.
[Abstract] [Full Text] [PDF]


Home page
Mol. Biol. CellHome page
K. A. Collins, A. R. Castillo, S. Y. Tatsutani, and S. Biggins
De Novo Kinetochore Assembly Requires the Centromeric Histone H3 Variant
Mol. Biol. Cell, December 1, 2005; 16(12): 5649 - 5660.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
J. T. Hannich, A. Lewis, M. B. Kroetz, S.-J. Li, H. Heide, A. Emili, and M. Hochstrasser
Defining the SUMO-modified Proteome by Multiple Approaches in Saccharomyces cerevisiae
J. Biol. Chem., February 11, 2005; 280(6): 4102 - 4110.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
R. S. Hilgarth, L. A. Murphy, H. S. Skaggs, D. C. Wilkerson, H. Xing, and K. D. Sarge
Regulation and Function of SUMO Modification
J. Biol. Chem., December 24, 2004; 279(52): 53899 - 53902.
[Full Text] [PDF]


Home page
Nucleic Acids ResHome page
B. M. O'Neill, D. Hanway, E. A. Winzeler, and F. E. Romesberg
Coordinated functions of WSS1, PSY2 and TOF1 in the DNA damage response
Nucleic Acids Res., December 14, 2004; 32(22): 6519 - 6530.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
A. K. Sapra, Y. Arava, P. Khandelia, and U. Vijayraghavan
Genome-wide Analysis of Pre-mRNA Splicing: INTRON FEATURES GOVERN THE REQUIREMENT FOR THE SECOND-STEP FACTOR, Prp17 IN SACCHAROMYCES CEREVISIAE AND SCHIZOSACCHAROMYCES POMBE
J. Biol. Chem., December 10, 2004; 279(50): 52437 - 52446.
[Abstract] [Full Text] [PDF]


Home page
J. Cell Sci.Home page
P. A. Coelho, J. Queiroz-Machado, and C. E. Sunkel
Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis
J. Cell Sci., December 1, 2003; 116(23): 4763 - 4776.
[Abstract] [Full Text] [PDF]


Home page
JCBHome page
K. Stead, C. Aguilar, T. Hartman, M. Drexel, P. Meluh, and V. Guacci
Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion
J. Cell Biol., November 24, 2003; 163(4): 729 - 741.
[Abstract] [Full Text] [PDF]


Home page
JCBHome page
Y. Azuma, A. Arnaoutov, and M. Dasso
SUMO-2/3 regulates topoisomerase II in mitosis
J. Cell Biol., November 10, 2003; 163(3): 477 - 487.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
K. Vincent, Q. Wang, S. Jay, K. Hobbs, and B. C. Rymond
Genetic Interactions With CLF1 Identify Additional Pre-mRNA Splicing Factors and a Link Between Activators of Yeast Vesicular Transport and Splicing
Genetics, July 1, 2003; 164(3): 895 - 907.
[Abstract] [Full Text] [PDF]


Home page
Nucleic Acids ResHome page
G. Chawla, A. K. Sapra, U. Surana, and U. Vijayraghavan
Dependence of pre-mRNA introns on PRP17, a non-essential splicing factor: implications for efficient progression through cell cycle transitions
Nucleic Acids Res., May 1, 2003; 31(9): 2333 - 2343.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
M. J. van Hemert, A. M. Deelder, C. Molenaar, H. Y. Steensma, and G. P. H. van Heusden
Self-association of the Spindle Pole Body-related Intermediate Filament Protein Fin1p and Its Phosphorylation-dependent Interaction with 14-3-3 Proteins in Yeast
J. Biol. Chem., April 18, 2003; 278(17): 15049 - 15055.
[Abstract] [Full Text] [PDF]


Home page
MutagenesisHome page
F. Cortes and N. Pastor
Induction of endoreduplication by topoisomerase II catalytic inhibitors
Mutagenesis, March 1, 2003; 18(2): 105 - 112.
[Abstract] [Full Text] [PDF]


Home page
Mol. Biol. CellHome page
C.D. Smith, D.L. Smith, J.L. DeRisi, and E.H. Blackburn
Telomeric Protein Distributions and Remodeling Through the Cell Cycle in Saccharomyces cerevisiae
Mol. Biol. Cell, February 1, 2003; 14(2): 556 - 570.
[Abstract] [Full Text] [PDF]


Home page
Nucleic Acids ResHome page
O. Dahan and M. Kupiec
Mutations in genes of Saccharomyces cerevisiae encoding pre-mRNA splicing factors cause cell cycle arrest through activation of the spindle checkpoint
Nucleic Acids Res., October 15, 2002; 30(20): 4361 - 4370.
[Abstract] [Full Text] [PDF]


Home page
JCBHome page
B. D. Lavoie, E. Hogan, and D. Koshland
In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin
J. Cell Biol., March 4, 2002; 156(5): 805 - 815.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
S. Biggins and A. W. Murray
The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint
Genes & Dev., December 1, 2001; 15(23): 3118 - 3129.
[Abstract] [Full Text] [PDF]


Home page
JCBHome page
B. D. Lavoie, E. Hogan, and D. Koshland
In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin
J. Cell Biol., March 4, 2002; 156(5): 805 - 815.
[Abstract] [Full Text] [PDF]


Home page
Mol. Biol. CellHome page
N. Bhalla, S. Biggins, and A. W. Murray
Mutation of YCS4, a Budding Yeast Condensin Subunit, Affects Mitotic and Nonmitotic Chromosome Behavior
Mol. Biol. Cell, February 1, 2002; 13(2): 632 - 645.
[Abstract] [Full Text] [PDF]