Skip to main content
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian
  • Log in
  • My Cart

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses

New Research In

Physical Sciences

Featured Portals

  • Physics
  • Chemistry
  • Sustainability Science

Articles by Topic

  • Applied Mathematics
  • Applied Physical Sciences
  • Astronomy
  • Computer Sciences
  • Earth, Atmospheric, and Planetary Sciences
  • Engineering
  • Environmental Sciences
  • Mathematics
  • Statistics

Social Sciences

Featured Portals

  • Anthropology
  • Sustainability Science

Articles by Topic

  • Economic Sciences
  • Environmental Sciences
  • Political Sciences
  • Psychological and Cognitive Sciences
  • Social Sciences

Biological Sciences

Featured Portals

  • Sustainability Science

Articles by Topic

  • Agricultural Sciences
  • Anthropology
  • Applied Biological Sciences
  • Biochemistry
  • Biophysics and Computational Biology
  • Cell Biology
  • Developmental Biology
  • Ecology
  • Environmental Sciences
  • Evolution
  • Genetics
  • Immunology and Inflammation
  • Medical Sciences
  • Microbiology
  • Neuroscience
  • Pharmacology
  • Physiology
  • Plant Biology
  • Population Biology
  • Psychological and Cognitive Sciences
  • Sustainability Science
  • Systems Biology
Research Article

Characterization of systemic genomic instability in budding yeast

Nadia M. V. Sampaio, View ORCID ProfileV. P. Ajith, Ruth A. Watson, Lydia R. Heasley, Parijat Chakraborty, View ORCID ProfileAline Rodrigues-Prause, Ewa P. Malc, View ORCID ProfilePiotr A. Mieczkowski, View ORCID ProfileKoodali T. Nishant, and View ORCID ProfileJuan Lucas Argueso
PNAS November 10, 2020 117 (45) 28221-28231; first published October 26, 2020; https://doi.org/10.1073/pnas.2010303117
Nadia M. V. Sampaio
aDepartment of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO 80523;
bCell and Molecular Biology Graduate Program, Colorado State University, Fort Collins, CO 80523;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
V. P. Ajith
cSchool of Biology, Indian Institute of Science Education and Research, 695551 Thiruvananthapuram, Trivandrum, India;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for V. P. Ajith
Ruth A. Watson
aDepartment of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO 80523;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lydia R. Heasley
aDepartment of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO 80523;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Parijat Chakraborty
cSchool of Biology, Indian Institute of Science Education and Research, 695551 Thiruvananthapuram, Trivandrum, India;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Aline Rodrigues-Prause
aDepartment of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO 80523;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Aline Rodrigues-Prause
Ewa P. Malc
dDepartment of Genetics, University of North Carolina, Chapel Hill, NC 27599
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Piotr A. Mieczkowski
dDepartment of Genetics, University of North Carolina, Chapel Hill, NC 27599
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Piotr A. Mieczkowski
Koodali T. Nishant
cSchool of Biology, Indian Institute of Science Education and Research, 695551 Thiruvananthapuram, Trivandrum, India;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Koodali T. Nishant
Juan Lucas Argueso
aDepartment of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO 80523;
bCell and Molecular Biology Graduate Program, Colorado State University, Fort Collins, CO 80523;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Juan Lucas Argueso
  • For correspondence: lucas.argueso@colostate.edu
  1. Edited by Daniel E. Gottschling, Calico Life Sciences, South San Francisco, CA, and approved September 28, 2020 (received for review June 15, 2020)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Significance

Mutations are generally thought to accumulate independently and gradually over many generations. Here, we combined complementary experimental approaches in budding yeast to track the appearance of chromosomal changes resulting in loss-of-heterozygosity. In contrast to the prevailing model, our results provide evidence for the existence of a path for nonindependent accumulation of multiple chromosomal alteration events over a few generations. These results are analogous to recent reports of bursts of genomic instability in human cells. The experimental model we describe provides a system to further dissect the fundamental biological processes underlying such punctuated bursts of mutation accumulation.

Abstract

Conventional models of genome evolution are centered around the principle that mutations form independently of each other and build up slowly over time. We characterized the occurrence of bursts of genome-wide loss-of-heterozygosity (LOH) in Saccharomyces cerevisiae, providing support for an additional nonindependent and faster mode of mutation accumulation. We initially characterized a yeast clone isolated for carrying an LOH event at a specific chromosome site, and surprisingly found that it also carried multiple unselected rearrangements elsewhere in its genome. Whole-genome analysis of over 100 additional clones selected for carrying primary LOH tracts revealed that they too contained unselected structural alterations more often than control clones obtained without any selection. We also measured the rates of coincident LOH at two different chromosomes and found that double LOH formed at rates 14- to 150-fold higher than expected if the two underlying single LOH events occurred independently of each other. These results were consistent across different strain backgrounds and in mutants incapable of entering meiosis. Our results indicate that a subset of mitotic cells within a population can experience discrete episodes of systemic genomic instability, when the entire genome becomes vulnerable and multiple chromosomal alterations can form over a narrow time window. They are reminiscent of early reports from the classic yeast genetics literature, as well as recent studies in humans, both in cancer and genomic disorder contexts. The experimental model we describe provides a system to further dissect the fundamental biological processes responsible for punctuated bursts of structural genomic variation.

  • mitotic recombination
  • loss-of-heterozygosity
  • genomic instability

Footnotes

  • ↵1To whom correspondence may be addressed. Email: lucas.argueso{at}colostate.edu.
  • Author contributions: N.M.V.S. and J.L.A. designed research; N.M.V.S., V.P.A., R.A.W., L.R.H., P.C., A.R.-P., E.P.M., and J.L.A. performed research; N.M.V.S., V.P.A., R.A.W., L.R.H., P.C., P.A.M., K.T.N., and J.L.A. analyzed data; and N.M.V.S., R.A.W., and J.L.A. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2010303117/-/DCSupplemental.

Data Availability.

The data that support the findings of this study are available in the article itself and the SI Appendix, specifically in SI Appendix, Figs. S1–S6, and in Datasets S1 and S2. All genome sequencing data associated with this study are available in the Sequence Read Archive (SRA) database, https://www.ncbi.nlm.nih.gov/sra (accession no. SRP082524).

Published under the PNAS license.

View Full Text

References

  1. ↵
    1. W. Ch. Cross,
    2. T. A. Graham,
    3. N. A. Wright
    , New paradigms in clonal evolution: Punctuated equilibrium in cancer. J. Pathol. 240, 126–136 (2016).
    OpenUrl
  2. ↵
    1. S. Turajlic,
    2. A. Sottoriva,
    3. T. Graham,
    4. C. Swanton
    , Resolving genetic heterogeneity in cancer. Nat. Rev. Genet. 20, 404–416 (2019).
    OpenUrl
  3. ↵
    1. R. Gao et al
    ., Punctuated copy number evolution and clonal stasis in triple-negative breast cancer. Nat. Genet. 48, 1119–1130 (2016).
    OpenUrlCrossRefPubMed
  4. ↵
    1. W. Cross et al.; S:CORT Consortium
    , The evolutionary landscape of colorectal tumorigenesis. Nat. Ecol. Evol. 2, 1661–1672 (2018).
    OpenUrl
  5. ↵
    1. M. G. Field et al
    ., Punctuated evolution of canonical genomic aberrations in uveal melanoma. Nat. Commun. 9, 116 (2018).
    OpenUrlCrossRefPubMed
  6. ↵
    1. M. Gerstung et al.; PCAWG Evolution & Heterogeneity Working Group; PCAWG Consortium
    , The evolutionary history of 2,658 cancers. Nature 578, 122–128 (2020).
    OpenUrlCrossRef
  7. ↵
    1. P. Liu et al
    ., An organismal CNV mutator phenotype restricted to early human development. Cell 168, 830–842.e7 (2017).
    OpenUrlCrossRef
  8. ↵
    1. S. Fogel,
    2. D. D. Hurst
    , Coincidence relations between gene conversion and mitotic recombination in Saccharomyces. Genetics 48, 321–328 (1963).
    OpenUrlFREE Full Text
  9. ↵
    1. D. D. Hurst,
    2. S. Fogel
    , Mitotic recombination and heteroallelic repair in Saccharomyces cerevisiae. Genetics 50, 435–458 (1964).
    OpenUrlFREE Full Text
  10. ↵
    1. M. Minet,
    2. A. M. Grossenbacher-Grunder,
    3. P. Thuriaux
    , The origin of a centromere effect on mitotic recombination: A study in the fission yeast Schizosaccharomyces pombe. Curr. Genet. 2, 53–60 (1980).
    OpenUrlCrossRef
  11. ↵
    1. B. A. Montelone,
    2. S. Prakash,
    3. L. Prakash
    , Spontaneous mitotic recombination in mms8-1, an allele of the CDC9 gene of Saccharomyces cerevisiae. J. Bacteriol. 147, 517–525 (1981).
    OpenUrlAbstract/FREE Full Text
  12. ↵
    1. J. E. Golin,
    2. M. S. Esposito
    , Coincident gene conversion during mitosis in saccharomyces. Genetics 107, 355–365 (1984).
    OpenUrlAbstract/FREE Full Text
  13. ↵
    1. J. E. Golin,
    2. H. Tampe
    , Coincident recombination during mitosis in saccharomyces: Distance-dependent and -independent components. Genetics 119, 541–547 (1988).
    OpenUrlAbstract/FREE Full Text
  14. ↵
    1. K. M. Freeman,
    2. G. R. Hoffmann
    , Frequencies of mutagen-induced coincident mitotic recombination at unlinked loci in Saccharomyces cerevisiae. Mutat. Res. 616, 119–132 (2007).
    OpenUrlCrossRefPubMed
  15. ↵
    1. A. Forche,
    2. P. T. Magee,
    3. A. Selmecki,
    4. J. Berman,
    5. G. May
    , Evolution in Candida albicans populations during a single passage through a mouse host. Genetics 182, 799–811 (2009).
    OpenUrlAbstract/FREE Full Text
  16. ↵
    1. A. Forche et al
    ., Rapid phenotypic and genotypic diversification after exposure to the oral host niche in Candida albicans. Genetics 209, 725–741 (2018).
    OpenUrlAbstract/FREE Full Text
  17. ↵
    1. L. R. Heasley,
    2. R. A. Watson,
    3. J. L. Argueso
    , Punctuated aneuploidization of the budding yeast genome. Genetics 216, 43–50 (2020).
    OpenUrlAbstract/FREE Full Text
  18. ↵
    1. A. Rodrigues-Prause et al
    ., A case study of genomic instability in an industrial strain of Saccharomyces cerevisiae. G3 (Bethesda) 8, 3703–3713 (2018).
    OpenUrlAbstract/FREE Full Text
  19. ↵
    1. E. L. Weiss
    , Mitotic exit and separation of mother and daughter cells. Genetics 192, 1165–1202 (2012).
    OpenUrlAbstract/FREE Full Text
  20. ↵
    1. A. Gusa,
    2. S. Jinks-Robertson
    , Mitotic recombination and adaptive genomic changes in human pathogenic fungi. Genes (Basel) 10, 901 (2019).
    OpenUrl
  21. ↵
    1. A. R. Borneman et al
    ., Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet. 7, e1001287 (2011).
    OpenUrlCrossRefPubMed
  22. ↵
    1. V. Galeote et al
    ., Amplification of a Zygosaccharomyces bailii DNA segment in wine yeast genomes by extrachromosomal circular DNA formation. PLoS One 6, e17872 (2011).
    OpenUrlCrossRefPubMed
  23. ↵
    1. D. E. Lea,
    2. C. A. Coulson
    , The distribution of the numbers of mutants in bacterial populations. J. Genet. 49, 264–285 (1949).
    OpenUrlCrossRefPubMed
  24. ↵
    1. R. Laureau et al
    ., Extensive recombination of a yeast diploid hybrid through meiotic reversion. PLoS Genet. 12, e1005781 (2016).
    OpenUrlCrossRefPubMed
  25. ↵
    1. S. Keeney,
    2. J. Lange,
    3. N. Mohibullah
    , Self-organization of meiotic recombination initiation: General principles and molecular pathways. Annu. Rev. Genet. 48, 187–214 (2014).
    OpenUrlCrossRefPubMed
  26. ↵
    1. F. Pâques,
    2. J. E. Haber
    , Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349–404 (1999).
    OpenUrlAbstract/FREE Full Text
  27. ↵
    1. J. M. Cherry et al
    ., Saccharomyces Genome Database: The genomics resource of budding yeast. Nucleic Acids Res. 40, D700–D705 (2012).
    OpenUrlCrossRefPubMed
  28. ↵
    1. W. Wei et al
    ., Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc. Natl. Acad. Sci. U.S.A. 104, 12825–12830 (2007).
    OpenUrlAbstract/FREE Full Text
  29. ↵
    1. W. A. Rosche,
    2. P. L. Foster
    , Determining mutation rates in bacterial populations. Methods 20, 4–17 (2000).
    OpenUrlCrossRefPubMed
  30. ↵
    1. G. I. Lang
    , Measuring mutation rates using the Luria-Delbrück fluctuation assay. Methods Mol. Biol. 1672, 21–31 (2018).
    OpenUrl
  31. ↵
    1. E. A. Radchenko,
    2. R. J. McGinty,
    3. A. Y. Aksenova,
    4. A. J. Neil,
    5. S. M. Mirkin
    , Quantitative analysis of the rates for repeat-mediated genome instability in a yeast experimental system. Methods Mol. Biol. 1672, 421–438 (2018).
    OpenUrlCrossRefPubMed
  32. ↵
    1. S. Sarkar,
    2. W. T. Ma,
    3. G. H. Sandri
    , On fluctuation analysis: A new, simple and efficient method for computing the expected number of mutants. Genetica 85, 173–179 (1992).
    OpenUrlCrossRefPubMed
  33. ↵
    1. C. E. Smith,
    2. B. Llorente,
    3. L. S. Symington
    , Template switching during break-induced replication. Nature 447, 102–105 (2007).
    OpenUrlCrossRefPubMed
  34. ↵
    1. C. Y. Li,
    2. D. W. Yandell,
    3. J. B. Little
    , Elevated frequency of microsatellite mutations in TK6 human lymphoblast clones selected for mutations at the thymidine kinase locus. Mol. Cell. Biol. 14, 4373–4379 (1994).
    OpenUrlAbstract/FREE Full Text
  35. ↵
    1. D. Grygoryev et al
    ., Autosomal mutants of proton-exposed kidney cells display frequent loss of heterozygosity on nonselected chromosomes. Radiat. Res. 181, 452–463 (2014).
    OpenUrl
  36. ↵
    1. E. Mancera,
    2. R. Bourgon,
    3. A. Brozzi,
    4. W. Huber,
    5. L. M. Steinmetz
    , High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454, 479–485 (2008).
    OpenUrlCrossRefPubMed
  37. ↵
    1. J. St Charles,
    2. T. D. Petes
    , High-resolution mapping of spontaneous mitotic recombination hotspots on the 1.1 Mb arm of yeast chromosome IV. PLoS Genet. 9, e1003434 (2013).
    OpenUrlCrossRefPubMed
  38. ↵
    1. R. Prasad
    1. C. d’Enfert et al
    ., “Genome diversity and dynamics” in Candida albicans: Cellular and Molecular Biology, R. Prasad, Ed. (Springer International Publishing, Cham, 2017), pp. 205–232.
  39. ↵
    1. A. K. Casasent et al
    ., Multiclonal invasion in breast tumors identified by topographic single cell sequencing. Cell 172, 205–217.e12 (2018).
    OpenUrlCrossRef
  40. ↵
    1. M. A. McMurray,
    2. D. E. Gottschling
    , An age-induced switch to a hyper-recombinational state. Science 301, 1908–1911 (2003).
    OpenUrlAbstract/FREE Full Text
  41. ↵
    1. J. R. Veatch,
    2. M. A. McMurray,
    3. Z. W. Nelson,
    4. D. E. Gottschling
    , Mitochondrial dysfunction leads to nuclear genome instability via an iron-sulfur cluster defect. Cell 137, 1247–1258 (2009).
    OpenUrlCrossRefPubMed
  42. ↵
    1. A. Raj,
    2. A. van Oudenaarden
    , Nature, nurture, or chance: Stochastic gene expression and its consequences. Cell 135, 216–226 (2008).
    OpenUrlCrossRefPubMed
  43. ↵
    1. C. D. Putnam et al
    ., A genetic network that suppresses genome rearrangements in Saccharomyces cerevisiae and contains defects in cancers. Nat. Commun. 7, 11256 (2016).
    OpenUrlCrossRef
  44. ↵
    1. M. P. Andersen,
    2. Z. W. Nelson,
    3. E. D. Hetrick,
    4. D. E. Gottschling
    , A genetic screen for increased loss of heterozygosity in Saccharomyces cerevisiae. Genetics 179, 1179–1195 (2008).
    OpenUrlAbstract/FREE Full Text
  45. ↵
    1. R. J. Craven,
    2. P. W. Greenwell,
    3. M. Dominska,
    4. T. D. Petes
    , Regulation of genome stability by TEL1 and MEC1, yeast homologs of the mammalian ATM and ATR genes. Genetics 161, 493–507 (2002).
    OpenUrlAbstract/FREE Full Text
  46. ↵
    1. A. Serero,
    2. C. Jubin,
    3. S. Loeillet,
    4. P. Legoix-Né,
    5. A. G. Nicolas
    , Mutational landscape of yeast mutator strains. Proc. Natl. Acad. Sci. U.S.A. 111, 1897–1902 (2014).
    OpenUrlAbstract/FREE Full Text
  47. ↵
    1. J. Liu,
    2. J. M. François,
    3. J. P. Capp
    , Gene expression noise produces cell-to-cell heterogeneity in eukaryotic homologous recombination rate. Front. Genet. 10, 475 (2019).
    OpenUrlCrossRef
  48. ↵
    1. M. Petljak et al
    ., Characterizing mutational signatures in human cancer cell lines reveals episodic APOBEC mutagenesis. Cell 176, 1282–1294.e20 (2019).
    OpenUrlCrossRefPubMed
  49. ↵
    1. J. Xia et al
    ., Bacteria-to-human protein networks reveal origins of endogenous DNA damage. Cell 176, 127–143.e24 (2019).
    OpenUrlCrossRef
  50. ↵
    1. A. N. Nguyen Ba et al
    ., High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast. Nature 575, 494–499 (2019).
    OpenUrlCrossRef
  51. ↵
    1. A. Jariani et al
    ., A new protocol for single-cell RNA-seq reveals stochastic gene expression during lag phase in budding yeast. eLife 9, e55320 (2020).
    OpenUrl
  52. ↵
    1. J. L. Argueso et al
    ., Genome structure of a Saccharomyces cerevisiae strain widely used in bioethanol production. Genome Res. 19, 2258–2270 (2009).
    OpenUrlAbstract/FREE Full Text
  53. ↵
    1. A. Morrison,
    2. J. B. Bell,
    3. T. A. Kunkel,
    4. A. Sugino
    , Eukaryotic DNA polymerase amino acid sequence required for 3′–5′ exonuclease activity. Proc. Natl. Acad. Sci. U.S.A. 88, 9473–9477 (1991).
    OpenUrlAbstract/FREE Full Text
  54. ↵
    1. F. M. Ausubel et al
    ., Eds., Current Protocols in Molecular Biology (John Wiley & Sons, 2003).
  55. ↵
    1. H. Zhang et al
    ., Gene copy-number variation in haploid and diploid strains of the yeast Saccharomyces cerevisiae. Genetics 193, 785–801 (2013).
    OpenUrlAbstract/FREE Full Text
  56. ↵
    1. A. L. Goldstein,
    2. J. H. McCusker
    , Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541–1553 (1999).
    OpenUrlCrossRefPubMed
  57. ↵
    1. F. Winston,
    2. C. Dollard,
    3. S. L. Ricupero-Hovasse
    , Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11, 53–55 (1995).
    OpenUrlCrossRefPubMed
  58. ↵
    1. B. M. Hall,
    2. C. X. Ma,
    3. P. Liang,
    4. K. K. Singh
    , Fluctuation analysis CalculatOR: A web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 25, 1564–1565 (2009).
    OpenUrlCrossRefPubMed

Log in using your username and password

Forgot your user name or password?

Log in through your institution

You may be able to gain access using your login credentials for your institution. Contact your library if you do not have a username and password.
If your organization uses OpenAthens, you can log in using your OpenAthens username and password. To check if your institution is supported, please see this list. Contact your library for more details.

Purchase access

You may purchase access to this article. This will require you to create an account if you don't already have one.

Subscribers, for more details, please visit our Subscriptions FAQ.

Please click here to log into the PNAS submission website.

PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Characterization of systemic genomic instability in budding yeast
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Characterization of systemic genomic instability in budding yeast
Nadia M. V. Sampaio, V. P. Ajith, Ruth A. Watson, Lydia R. Heasley, Parijat Chakraborty, Aline Rodrigues-Prause, Ewa P. Malc, Piotr A. Mieczkowski, Koodali T. Nishant, Juan Lucas Argueso
Proceedings of the National Academy of Sciences Nov 2020, 117 (45) 28221-28231; DOI: 10.1073/pnas.2010303117

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
Characterization of systemic genomic instability in budding yeast
Nadia M. V. Sampaio, V. P. Ajith, Ruth A. Watson, Lydia R. Heasley, Parijat Chakraborty, Aline Rodrigues-Prause, Ewa P. Malc, Piotr A. Mieczkowski, Koodali T. Nishant, Juan Lucas Argueso
Proceedings of the National Academy of Sciences Nov 2020, 117 (45) 28221-28231; DOI: 10.1073/pnas.2010303117
Digg logo Reddit logo Twitter logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley
Proceedings of the National Academy of Sciences: 117 (45)
Table of Contents

Submit

Sign up for Article Alerts

Article Classifications

  • Biological Sciences
  • Genetics

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Materials and Methods
    • Data Availability.
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Surgeons hands during surgery
Inner Workings: Advances in infectious disease treatment promise to expand the pool of donor organs
Despite myriad challenges, clinicians see room for progress.
Image credit: Shutterstock/David Tadevosian.
Setting sun over a sun-baked dirt landscape
Core Concept: Popular integrated assessment climate policy models have key caveats
Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Double helix
Journal Club: Noncoding DNA shown to underlie function, cause limb malformations
Using CRISPR, researchers showed that a region some used to label “junk DNA” has a major role in a rare genetic disorder.
Image credit: Nathan Devery.
Steamboat Geyser eruption.
Eruption of Steamboat Geyser
Mara Reed and Michael Manga explore why Yellowstone's Steamboat Geyser resumed erupting in 2018.
Listen
Past PodcastsSubscribe
Multi-color molecular model
Enzymatic breakdown of PET plastic
A study demonstrates how two enzymes—MHETase and PETase—work synergistically to depolymerize the plastic pollutant PET.
Image credit: Aaron McGeehan (artist).

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Librarians
  • Press
  • Site Map
  • PNAS Updates

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490