Online citations, reference lists, and bibliographies.
← Back to Search

Gene Copy-Number Variation In Haploid And Diploid Strains Of The Yeast Saccharomyces Cerevisiae

H. Zhang, A. F. Zeidler, Wei Song, Christopher M Puccia, Ewa Malc, P. Greenwell, P. Mieczkowski, T. Petes, J. L. Argueso
Published 2013 · Biology, Medicine

Cite This
Download PDF
Analyze on Scholarcy
Share
The increasing ability to sequence and compare multiple individual genomes within a species has highlighted the fact that copy-number variation (CNV) is a substantial and underappreciated source of genetic diversity. Chromosome-scale mutations occur at rates orders of magnitude higher than base substitutions, yet our understanding of the mechanisms leading to CNVs has been lagging. We examined CNV in a region of chromosome 5 (chr5) in haploid and diploid strains of Saccharomyces cerevisiae. We optimized a CNV detection assay based on a reporter cassette containing the SFA1 and CUP1 genes that confer gene dosage-dependent tolerance to formaldehyde and copper, respectively. This optimized reporter allowed the selection of low-order gene amplification events, going from one copy to two copies in haploids and from two to three copies in diploids. In haploid strains, most events involved tandem segmental duplications mediated by nonallelic homologous recombination between flanking direct repeats, primarily Ty1 elements. In diploids, most events involved the formation of a recurrent nonreciprocal translocation between a chr5 Ty1 element and another Ty1 repeat on chr13. In addition to amplification events, a subset of clones displaying elevated resistance to formaldehyde had point mutations within the SFA1 coding sequence. These mutations were all dominant and are proposed to result in hyperactive forms of the formaldehyde dehydrogenase enzyme.
This paper references
10.1128/MCB.11.3.1222
A unique pathway of double-strand break repair operates in tandemly repeated genes.
B. A. Ozenberger (1991)
10.1016/0092-8674(85)90153-9
Genetic analysis of the mitotic transmission of minichromosomes
D. Koshland (1985)
10.1093/nar/gki941
Duplication processes in Saccharomyces cerevisiae haploid strains
Joseph Schacherer (2005)
10.1371/journal.pgen.1000303
The Repertoire and Dynamics of Evolutionary Adaptations to Controlled Nutrient-Limited Environments in Yeast
D. Gresham (2008)
Mutants of yeast defective in iso-1-cytochrome c.
F. Sherman (1974)
10.1016/j.cell.2006.04.042
The Pattern of Gene Amplification Is Determined by the Chromosomal Location of Hairpin-Capped Breaks
Vidhya Narayanan (2006)
10.1007/BF00633833
Unequal crossing-over and gene conversion at the amplifiedCUP1 locus of yeast
J. Welch (2004)
Gene duplication in Saccharomyces cerevisiae.
P. Hansche (1978)
10.1093/OXFORDJOURNALS.MOLBEV.A026009
Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment.
C. Brown (1998)
10.1002/(SICI)1097-0061(199910)15:14<1541::AID-YEA476>3.0.CO;2-K
Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae
A. Goldstein (1999)
10.1371/journal.pgen.1001228
Competitive Repair by Naturally Dispersed Repetitive DNA during Non-Allelic Homologous Recombination
M. Hoang (2010)
10.1038/nature05205
Amplification of histone genes by circular chromosome formation in Saccharomyces cerevisiae
Diana E. Libuda (2006)
10.2217/fon.12.34
Germline copy number variations and cancer predisposition.
A. Krepischi (2012)
10.1016/j.tig.2010.11.001
Genome organization influences partner selection for chromosomal rearrangements.
Patrick J. Wijchers (2011)
10.1371/journal.pgen.1000175
Segmental Duplications Arise from Pol32-Dependent Repair of Broken Forks through Two Alternative Replication-Based Mechanisms
Celia Payen (2008)
10.1038/ncb2472
Increased chromosome mobility facilitates homology search during recombination
Judith Miné-Hattab (2012)
10.1016/j.cell.2012.02.039
CNVs: Harbingers of a Rare Variant Revolution in Psychiatric Genetics
Dheeraj Malhotra (2012)
10.1007/BF02986080
The distribution of the numbers of mutants in bacterial populations
D. Lea (2008)
10.1534/genetics.111.137927
High-Resolution Genome-Wide Analysis of Irradiated (UV and γ-Rays) Diploid Yeast Cells Reveals a High Frequency of Genomic Loss of Heterozygosity (LOH) Events
Jordan St. Charles (2012)
10.1128/MMBR.63.2.349-404.1999
Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae
F. Pâques (1999)
10.1038/nrg3241
De novo mutations in human genetic disease
J. Veltman (2012)
10.1371/journal.pgen.1002539
Rapid Analysis of Saccharomyces cerevisiae Genome Rearrangements by Multiplex Ligation–Dependent Probe Amplification
J. E. Chan (2012)
10.1038/emboj.2008.205
Chromosome fragility at GAA tracts in yeast depends on repeat orientation and requires mismatch repair
Hyunmin Kim (2008)
10.1128/MCB.25.10.3934-3944.2005
The Yeast Chromatin Remodeler RSC Complex Facilitates End Joining Repair of DNA Double-Strand Breaks
E. Shim (2005)
10.1371/journal.pgen.1001270
Friedreich's Ataxia (GAA)n•(TTC)n Repeats Strongly Stimulate Mitotic Crossovers in Saccharomyces cerevisae
W. Tang (2011)
H Zhang
10.1128/MCB.25.16.7226-7238.2005
Saccharomyces cerevisiae as a Model System To Define the Chromosomal Instability Phenotype
C. Putnam (2005)
A mutator affecting the region of the iso-1-cytochrome c gene in yeast.
S. Liebman (1979)
A DELETION IN YEAST AND ITS BEARING ON THE STRUCTURE OF THE MATING TYPE LOCUS.
D. C. Hawthorne (1963)
Spontaneous amplification of the ADH4 gene in Saccharomyces cerevisiae.
M. Dorsey (1992)
10.1126/science.1190966
Loss of DNA Replication Control Is a Potent Inducer of Gene Amplification
B. Green (2010)
10.1016/j.dnarep.2011.11.001
Formaldehyde-induced genome instability is suppressed by an XPF-dependent pathway.
A. Kumari (2012)
10.1002/1098-2280(2000)36:2<105::AID-EM4>3.0.CO;2-X
Telomere sequences at the novel joints of four independent amplifications in Saccharomyces cerevisiae
Irene K. Moore (2000)
10.1111/j.1365-2958.2007.05660.x
Spontaneous deletions and reciprocal translocations in Saccharomyces cerevisiae: influence of ploidy
Yves Tourrette (2007)
10.1371/journal.pgen.1002633
DNA Resection at Chromosome Breaks Promotes Genome Stability by Constraining Non-Allelic Homologous Recombination
F. Tan (2012)
10.1073/pnas.242624799
Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae
M. Dunham (2002)
10.1073/pnas.0701291104
Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789
W. Wei (2007)
10.1002/YEA.320101310
New heterologous modules for classical or PCR‐based gene disruptions in Saccharomyces cerevisiae
A. Wach (1994)
10.1056/NEJMra0803109
Chromosomal abnormalities in cancer.
S. Fröhling (2008)
10.1016/j.cell.2004.12.039
Chromosomal Translocations in Yeast Induced by Low Levels of DNA Polymerase A Model for Chromosome Fragile Sites
Francene J. Lemoine (2005)
10.1101/GAD.1315805
A mechanism of palindromic gene amplification in Saccharomyces cerevisiae.
A. Rattray (2005)
10.1038/sj.emboj.7600503
A novel gene amplification system in yeast based on double rolling‐circle replication
Takaaki Watanabe (2005)
Methods in yeast genetics
F. Sherman (1979)
Gene conversion of deletions in the his4 region of yeast.
G. Fink (1974)
10.1146/annurev-genet-102209-163544
Human copy number variation and complex genetic disease.
S. Girirajan (2011)
10.1038/nature07943
The cancer genome
M. Stratton (2009)
10.1073/PNAS.88.21.9473
Eukaryotic DNA polymerase amino acid sequence required for 3'----5' exonuclease activity.
A. Morrison (1991)
10.1016/J.DNAREP.2007.04.006
Spontaneous duplications in diploid Saccharomyces cerevisiae cells.
Joseph Schacherer (2007)
Structural analysis of aberrant chromosomes that occur spontaneously in diploid Saccharomyces cerevisiae: retrotransposon Ty1 plays a crucial role in chromosomal rearrangements.
K. Umezu (2002)
10.1038/nrg2346
Advances in autism genetics: on the threshold of a new neurobiology
B. Abrahams (2008)
10.1038/sj.emboj.7600024
Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments
R. Koszul (2004)
10.1073/pnas.1006281107
Chromosome rearrangements and aneuploidy in yeast strains lacking both Tel1p and Mec1p reflect deficiencies in two different mechanisms
J. Mcculley (2010)
A microhomologymediated break-induced replication model for the origin of human copy number variation
P J Hastings (2009)
Thomas D. Petes, and Juan Lucas Argueso Copyright © 2013 by the Genetics Society of America DOI: 10.1534/genetics.112.146522 Supporting cited literature
F B Ane
10.1534/genetics.112.141051
Genome Rearrangements Caused by Depletion of Essential DNA Replication Proteins in Saccharomyces cerevisiae
Edith Cheng (2012)
10.1002/j.1460-2075.1996.tb00517.x
Gene conversion plays the major role in controlling the stability of large tandem repeats in yeast.
S. Gangloff (1996)
10.1534/genetics.107.086603
High Rates of “Unselected” Aneuploidy and Chromosome Rearrangements in tel1 mec1 Haploid Yeast Strains
Michael Vernon (2008)
10.1038/nature08217
Specific pathways prevent duplication-mediated genome rearrangements
C. Putnam (2009)
10.1016/j.gde.2012.01.009
Replication stress and mechanisms of CNV formation.
M. Arlt (2012)
10.1371/journal.pgen.1000327
A Microhomology-Mediated Break-Induced Replication Model for the Origin of Human Copy Number Variation
P. Hastings (2009)
10.1038/ncb2465
Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery
Vincent Dion (2012)
Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc. Natl. Acad. Sci. USA
W Wei (2007)
10.1073/pnas.0804529105
Double-strand breaks associated with repetitive DNA can reshape the genome
J. L. Argueso (2008)
10.1101/gr.107680.110
De novo rates and selection of large copy number variation.
A. Itsara (2010)
10.1128/MCB.7.3.1198
Concerted deletions and inversions are caused by mitotic recombination between delta sequences in Saccharomyces cerevisiae.
R. Rothstein (1987)
Methods in Yeast Genetics
M. Rose (1990)
10.1038/12687
Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants
C. Chen (1999)
10.1146/ANNUREV.GENET.34.1.359
DNA mismatch repair and genetic instability.
B. Harfe (2000)
10.1371/journal.pgen.1002089
A Genetic and Structural Study of Genome Rearrangements Mediated by High Copy Repeat Ty1 Elements
J. E. Chan (2011)
10.1038/337285A0
Nonmutagenic carcinogens induce intrachromosomal recombination in yeast
R. Schiestl (1989)
10.1126/SCIENCE.1071398
ATR Homolog Mec1 Promotes Fork Progression, Thus Averting Breaks in Replication Slow Zones
R. Cha (2002)
10.1016/j.tig.2012.03.002
Exploring the role of copy number variants in human adaptation.
Rebecca C. Iskow (2012)
10.1073/pnas.0906552106
Retrotransposon overdose and genome integrity
Lisa Z. Scheifele (2009)
10.1371/journal.pgen.1002016
Origin-Dependent Inverted-Repeat Amplification: A Replication-Based Model for Generating Palindromic Amplicons
B. Brewer (2011)
10.1016/0092-8674(81)90209-9
Ty elements are involved in the formation of deletions in DEL1 strains of saccharomyces cerevisiae
S. Liebman (1981)
10.3109/10409238.2012.675644
Multiple cellular mechanisms prevent chromosomal rearrangements involving repetitive DNA
Carolyn M George (2012)
10.1021/BI026705Q
Human glutathione-dependent formaldehyde dehydrogenase. Structural changes associated with ternary complex formation.
P. Sanghani (2002)
10.1159/000080593
Mismatch repair proteins: key regulators of genetic recombination
J. Surtees (2004)
10.1101/gr.091777.109
Genome structure of a Saccharomyces cerevisiae strain widely used in bioethanol production.
J. L. Argueso (2009)
J. Bacteriol
The Hawthorne deletion twenty-five years later.
I. Herskowitz (1988)
10.1021/BI0257639
Human glutathione-dependent formaldehyde dehydrogenase. Structures of apo, binary, and inhibitory ternary complexes.
P. Sanghani (2002)
10.1038/nrg3240
Genetic architectures of psychiatric disorders: the emerging picture and its implications
P. F. Sullivan (2012)
10.1128/JB.156.2.625-635.1983
The presence of a defective LEU2 gene on 2 mu DNA recombinant plasmids of Saccharomyces cerevisiae is responsible for curing and high copy number.
E. Erhart (1983)
10.1371/journal.pgen.1000410
A Fine-Structure Map of Spontaneous Mitotic Crossovers in the Yeast Saccharomyces cerevisiae
P. S. Lee (2009)
10.1038/90837
In vivo site-directed mutagenesis using oligonucleotides
F. Storici (2001)
10.1016/S0092-8674(80)80052-3
Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes
T. Petes (1980)
10.1038/nature08973
A Three-Dimensional Model of the Yeast Genome
Z. Duan (2010)
10.1016/J.DNAREP.2006.05.027
Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae.
P. Mieczkowski (2006)
10.1534/GENETICS.112.541.TEST
A Method for Gene Disruption That Allows Repeated Use of URA3 Selection in the Construction of Multiply Disrupted Yeast Strains
E. Alani (1987)
10.1038/284426A0
Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae
J. Szostak (1980)



This paper is referenced by
Investigating the Frequency of Copy Number Variations (CNVs) at Fragile Site FRA3B in Saccharomyces Cerevisiae
Samantha Bartolet (2018)
10.1007/s00294-018-0857-1
Border collies of the genome: domestication of an autonomous retrovirus-like transposon
M. Curcio (2018)
Understanding The Complexity of Human Structural Genomic Variation Through Multiple Whole Genome Sequencing Platforms
Xuefang Zhao (2017)
10.1016/j.ymben.2014.09.004
Evolution reveals a glutathione-dependent mechanism of 3-hydroxypropionic acid tolerance.
Kanchana R Kildegaard (2014)
10.1534/genetics.113.159202
The Sister Chromatid Cohesion Pathway Suppresses Multiple Chromosome Gain and Chromosome Amplification
Shay Covo (2013)
10.1371/journal.pgen.1004119
Cascades of Genetic Instability Resulting from Compromised Break-Induced Replication
Soumini Vasan (2014)
10.1101/047266
Transient structural variations alter gene expression and quantitative traits in Schizosaccharomyces pombe.
D. Jeffares (2016)
10.1534/genetics.120.303536
Punctuated Aneuploidization of the Budding Yeast Genome
L. R. Heasley (2020)
10.1534/genetics.115.181149
Stimulation of Chromosomal Rearrangements by Ribonucleotides
Hailey N Conover (2015)
10.1371/journal.pgen.1004041
Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
Jungeui Hong (2014)
10.1007/s00294-019-00976-w
Rapid and extensive karyotype diversification in haploid clinical Candida auris isolates
Gustavo Bravo Ruiz (2019)
10.1007/s10295-014-1556-7
Genomic reconstruction to improve bioethanol and ergosterol production of industrial yeast Saccharomyces cerevisiae
K. Zhang (2014)
10.1093/gbe/evu287
Accelerated Evolution of Schistosome Genes Coding for Proteins Located at the Host–Parasite Interface
G. S. Philippsen (2015)
10.1186/s13100-020-00215-x
Diverse transposable element landscapes in pathogenic and nonpathogenic yeast models: the value of a comparative perspective
P. Maxwell (2020)
Structural variations in pig genomes
Y. Paudel (2015)
10.1101/047266
Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast
D. Jeffares (2016)
10.1093/femsyr/foaa043
A glimpse of potential transposable element impact on adaptation of the industrial yeast Saccharomyces cerevisiae.
Z. Liu (2020)
Assessment of water quality, toxicity and treatment strategies downstream of NPDES oil and gas produced water discharges intended for beneficial reuse
Molly C McLaughlin (2020)
10.1016/j.dnarep.2017.02.012
Both R-loop removal and ribonucleotide excision repair activities of RNase H2 contribute substantially to chromosome stability.
Deborah A Cornelio (2017)
Stochastic gene expression, phenotypic variability and adaptation of budding yeast to environmental stresses
J. Liu (2015)
10.1101/514745
Rapid and extensive karyotype diversification in haploid clinical Candida auris isolates
Gustavo Bravo Ruiz (2019)
10.19146/PIBIC-2016-52146
Copy-number variation of xylose isomerase for efficient adaptive evolution of engineered industrial Saccharomyces cerevisiae strain
João Gabriel Ribeiro Bueno (2016)
10.1101/2020.06.25.164855
A new experimental system to study meiotic recurrent non-allelic homologous recombination in budding yeast
Hailey N. C. Sedam (2020)
10.1101/250365
The genome-wide rate and spectrum of spontaneous mutations differs between haploid and diploid yeast
N. P. Sharp (2018)
10.3390/genes10010040
Genetic Instability and Chromatin Remodeling in Spermatids
Tiphanie Cavé (2019)
10.1534/genetics.112.145805
Pathways and Mechanisms that Prevent Genome Instability in Saccharomyces cerevisiae
C. Putnam (2017)
10.1016/j.cub.2018.02.026
Evolution: Zeroing In on the Rate of Genome Doubling
N. P. Sharp (2018)
10.1534/g3.114.012922
Structures of Naturally Evolved CUP1 Tandem Arrays in Yeast Indicate That These Arrays Are Generated by Unequal Nonhomologous Recombination
Y. Zhao (2014)
10.17863/CAM.31757
Accelerated adaptation through stimulated copy number variation in Saccharomyces cerevisiae
R. Hull (2018)
10.3390/genes9110539
Genome Instability Induced by Low Levels of Replicative DNA Polymerases in Yeast
Dao-Qiong Zheng (2018)
10.1186/s12864-016-3044-0
Copy number variation contributes to cryptic genetic variation in outbreak lineages of Cryptococcus gattii from the North American Pacific Northwest
J. Steenwyk (2016)
10.1038/ncomms14061
Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast
D. Jeffares (2017)
See more
Semantic Scholar Logo Some data provided by SemanticScholar