skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts

Abstract

Cell-cycle checkpoints and DNA repair processes protect organisms from possibly lethal mutational damage. Compared to other budding yeasts in the subphylum Saccharomycotina, we noticed that a lineage in the genus Hanseniaspora exhibited very high evolutionary rates, low Guanine–Cytosine (GC) content, small genome sizes, and lower gene numbers. To better understand Hanseniaspora evolution, we viewed 25 genomes, including 11 newly sequenced, representing 18/21 known species in the genus. Our phylogenomic analyses identify two Hanseniaspora lineages, a faster-evolving lineage (FEL), which began diversifying approximately 87 million years ago (mya), and a slower-evolving lineage (SEL), which began diversifying approximately 54 mya. Remarkably, both lineages lost genes associated with the cell cycle and genome integrity, but these losses were greater in the FEL. E.g., all species lost the cell-cycle regulator WHIskey 5 (WHI5), and the FEL lost components of the spindle checkpoint pathway (e.g., Mitotic Arrest-Deficient 1 [MAD1], Mitotic Arrest-Deficient 2 [MAD2]) and DNA-damage–checkpoint pathway (e.g., Mitosis Entry Checkpoint 3 [MEC3], RADiation sensitive 9 [RAD9]). Similarly, both lineages lost genes involved in DNA repair pathways, including the DNA glycosylase gene 3-MethylAdenine DNA Glycosylase 1 (MAG1), which is part of the base-excision repair pathway, and the DNA photolyase gene PHotoreactivation Repair deficient 1 (PHR1), whichmore » is involved in pyrimidine dimer repair. Strikingly, the FEL lost 33 additional genes, including polymerases (i.e., POLymerase 4 [POL4] and POL32) and telomere-associated genes (e.g., Repressor/activator site binding protein-Interacting Factor 1 [RIF1], Replication Factor A 3 [RFA3], Cell Division Cycle 13 [CDC13], Pbp1p Binding Protein [PBP2]). Echoing these losses, molecular evolutionary analyses reveal that, compared to the SEL, the FEL stem lineage underwent a burst of accelerated evolution, which resulted in greater mutational loads, homopolymer instabilities, and higher fractions of mutations associated with the common endogenously damaged base, 8-oxoguanine. We conclude that Hanseniaspora is an ancient lineage that has diversified and thrived, despite lacking many otherwise highly conserved cell-cycle and genome integrity genes and pathways, and may represent a novel, to our knowledge, system for studying cellular life without them.« less

Authors:
ORCiD logo; ; ; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ; ; ; ; ORCiD logo; ORCiD logo;
Publication Date:
Research Org.:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
Contributing Org.:
Advanced Computing Center for Research and Education at Vanderbilt University, the Center for High-Throughput Computing at UW-Madison, and the UW Biotechnology Center DNA Sequencing Facility
OSTI Identifier:
1630352
Alternate Identifier(s):
OSTI ID: 1556080
Grant/Contract Number:  
BER DE-FC02-07ER64494 and DE-SC0018409; SC0018409; FC02-07ER64494
Resource Type:
Published Article
Journal Name:
PLoS Biology (Online)
Additional Journal Information:
Journal Name: PLoS Biology (Online) Journal Volume: 17 Journal Issue: 5; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Steenwyk, Jacob L., Opulente, Dana A., Kominek, Jacek, Shen, Xing-Xing, Zhou, Xiaofan, Labella, Abigail L., Bradley, Noah P., Eichman, Brandt F., Čadež, Neža, Libkind, Diego, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, and Kamoun, ed., Sophien. Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts. United States: N. p., 2019. Web. https://doi.org/10.1371/journal.pbio.3000255.
Steenwyk, Jacob L., Opulente, Dana A., Kominek, Jacek, Shen, Xing-Xing, Zhou, Xiaofan, Labella, Abigail L., Bradley, Noah P., Eichman, Brandt F., Čadež, Neža, Libkind, Diego, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, & Kamoun, ed., Sophien. Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts. United States. https://doi.org/10.1371/journal.pbio.3000255
Steenwyk, Jacob L., Opulente, Dana A., Kominek, Jacek, Shen, Xing-Xing, Zhou, Xiaofan, Labella, Abigail L., Bradley, Noah P., Eichman, Brandt F., Čadež, Neža, Libkind, Diego, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, and Kamoun, ed., Sophien. Tue . "Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts". United States. https://doi.org/10.1371/journal.pbio.3000255.
@article{osti_1630352,
title = {Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts},
author = {Steenwyk, Jacob L. and Opulente, Dana A. and Kominek, Jacek and Shen, Xing-Xing and Zhou, Xiaofan and Labella, Abigail L. and Bradley, Noah P. and Eichman, Brandt F. and Čadež, Neža and Libkind, Diego and DeVirgilio, Jeremy and Hulfachor, Amanda Beth and Kurtzman, Cletus P. and Hittinger, Chris Todd and Rokas, Antonis and Kamoun, ed., Sophien},
abstractNote = {Cell-cycle checkpoints and DNA repair processes protect organisms from possibly lethal mutational damage. Compared to other budding yeasts in the subphylum Saccharomycotina, we noticed that a lineage in the genus Hanseniaspora exhibited very high evolutionary rates, low Guanine–Cytosine (GC) content, small genome sizes, and lower gene numbers. To better understand Hanseniaspora evolution, we viewed 25 genomes, including 11 newly sequenced, representing 18/21 known species in the genus. Our phylogenomic analyses identify two Hanseniaspora lineages, a faster-evolving lineage (FEL), which began diversifying approximately 87 million years ago (mya), and a slower-evolving lineage (SEL), which began diversifying approximately 54 mya. Remarkably, both lineages lost genes associated with the cell cycle and genome integrity, but these losses were greater in the FEL. E.g., all species lost the cell-cycle regulator WHIskey 5 (WHI5), and the FEL lost components of the spindle checkpoint pathway (e.g., Mitotic Arrest-Deficient 1 [MAD1], Mitotic Arrest-Deficient 2 [MAD2]) and DNA-damage–checkpoint pathway (e.g., Mitosis Entry Checkpoint 3 [MEC3], RADiation sensitive 9 [RAD9]). Similarly, both lineages lost genes involved in DNA repair pathways, including the DNA glycosylase gene 3-MethylAdenine DNA Glycosylase 1 (MAG1), which is part of the base-excision repair pathway, and the DNA photolyase gene PHotoreactivation Repair deficient 1 (PHR1), which is involved in pyrimidine dimer repair. Strikingly, the FEL lost 33 additional genes, including polymerases (i.e., POLymerase 4 [POL4] and POL32) and telomere-associated genes (e.g., Repressor/activator site binding protein-Interacting Factor 1 [RIF1], Replication Factor A 3 [RFA3], Cell Division Cycle 13 [CDC13], Pbp1p Binding Protein [PBP2]). Echoing these losses, molecular evolutionary analyses reveal that, compared to the SEL, the FEL stem lineage underwent a burst of accelerated evolution, which resulted in greater mutational loads, homopolymer instabilities, and higher fractions of mutations associated with the common endogenously damaged base, 8-oxoguanine. We conclude that Hanseniaspora is an ancient lineage that has diversified and thrived, despite lacking many otherwise highly conserved cell-cycle and genome integrity genes and pathways, and may represent a novel, to our knowledge, system for studying cellular life without them.},
doi = {10.1371/journal.pbio.3000255},
journal = {PLoS Biology (Online)},
number = 5,
volume = 17,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1371/journal.pbio.3000255

Citation Metrics:
Cited by: 15 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Phylogenomics
journal, December 2005


QUAST: quality assessment tool for genome assemblies
journal, February 2013


The Gene Ontology (GO) database and informatics resource
journal, January 2004

  • Gene Ontology Consortium,
  • Nucleic Acids Research, Vol. 32, Issue 90001
  • DOI: 10.1093/nar/gkh036

Whole Genome Analysis of 132 Clinical Saccharomyces cerevisiae Strains Reveals Extensive Ploidy Variation
journal, June 2016

  • Zhu, Yuan O.; Sherlock, Gavin; Petrov, Dmitri A.
  • G3: Genes|Genomes|Genetics, Vol. 6, Issue 8
  • DOI: 10.1534/g3.116.029397

Lighter: fast and memory-efficient sequencing error correction without counting
journal, November 2014


ploidyNGS: visually exploring ploidy with Next Generation Sequencing data
journal, April 2017

  • Augusto Corrêa dos Santos, Renato; Goldman, Gustavo Henrique; Riaño-Pachón, Diego Mauricio
  • Bioinformatics, Vol. 33, Issue 16
  • DOI: 10.1093/bioinformatics/btx204

Genome Sequence of the Native Apiculate Wine Yeast Hanseniaspora vineae T02/19AF
journal, May 2014


Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data
journal, September 2016

  • Shen, Xing-Xing; Zhou, Xiaofan; Kominek, Jacek
  • G3: Genes|Genomes|Genetics, Vol. 6, Issue 12
  • DOI: 10.1534/g3.116.034744

Anaphase-Promoting Complex 7 is a Prognostic Factor in Human Colorectal Cancer
journal, August 2017

  • Kim, Ik Yong; Kwon, Hye Yeon; Park, Kwang Hwa
  • Annals of Coloproctology, Vol. 33, Issue 4
  • DOI: 10.3393/ac.2017.33.4.139

IME1, a positive regulator gene of meiosis in S. cerevisiae
journal, March 1988


Evolution of networks and sequences in eukaryotic cell cycle control
journal, December 2011

  • Cross, Frederick R.; Buchler, Nicolas E.; Skotheim, Jan M.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1584
  • DOI: 10.1098/rstb.2011.0078

The Evolution of Low Mutation Rates in Experimental Mutator Populations of Saccharomyces cerevisiae
journal, July 2012


Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair.
journal, March 1994

  • Weinert, T. A.; Kiser, G. L.; Hartwell, L. H.
  • Genes & Development, Vol. 8, Issue 6
  • DOI: 10.1101/gad.8.6.652

Mad1 contribution to spindle assembly checkpoint signalling goes beyond presenting Mad2 at kinetochores
journal, January 2014


SSP1, a gene necessary for proper completion of meiotic divisions and spore formation in Saccharomyces cerevisiae.
journal, December 1997

  • Nag, D. K.; Koonce, M. P.; Axelrod, J.
  • Molecular and Cellular Biology, Vol. 17, Issue 12
  • DOI: 10.1128/MCB.17.12.7029

CDK Activity Antagonizes Whi5, an Inhibitor of G1/S Transcription in Yeast
journal, June 2004


GOATOOLS: A Python library for Gene Ontology analyses
journal, July 2018


Biopython: freely available Python tools for computational molecular biology and bioinformatics
journal, March 2009


Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Relations between chemical structure and biological activity in peptides
journal, November 1966


DNA-damage repair; the good, the bad, and the ugly
journal, February 2008


Comprehensive Analysis of Hypermutation in Human Cancer
journal, November 2017


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Evolution of high mutation rates in experimental populations of E. coli
journal, June 1997

  • Sniegowski, Paul D.; Gerrish, Philip J.; Lenski, Richard E.
  • Nature, Vol. 387, Issue 6634
  • DOI: 10.1038/42701

Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi
journal, November 2001

  • Katinka, Michaël D.; Duprat, Simone; Cornillot, Emmanuel
  • Nature, Vol. 414, Issue 6862
  • DOI: 10.1038/35106579

DNA Damage Response Genes and the Development of Cancer Metastasis
journal, February 2014

  • Broustas, Constantinos G.; Lieberman, Howard B.
  • Radiation Research, Vol. 181, Issue 2
  • DOI: 10.1667/RR13515.1

Oenological Impact of the Hanseniaspora/Kloeckera Yeast Genus on Wines—A Review
journal, September 2018


Remarkably ancient balanced polymorphisms in a multi-locus gene network
journal, February 2010

  • Hittinger, Chris Todd; Gonçalves, Paula; Sampaio, José Paulo
  • Nature, Vol. 464, Issue 7285
  • DOI: 10.1038/nature08791

The anaphase-promoting complex: a key factor in the regulation of cell cycle
journal, January 2005


MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

An Introduction to Sequence Similarity (“Homology”) Searching
journal, June 2013


Genome-scale approaches to resolving incongruence in molecular phylogenies
journal, October 2003

  • Rokas, Antonis; Williams, Barry L.; King, Nicole
  • Nature, Vol. 425, Issue 6960
  • DOI: 10.1038/nature02053

KEGG as a reference resource for gene and protein annotation
journal, October 2015

  • Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1070

Comparative genomics of biotechnologically important yeasts
journal, August 2016

  • Riley, Robert; Haridas, Sajeet; Wolfe, Kenneth H.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 35
  • DOI: 10.1073/pnas.1603941113

The Role of Altered Nucleotide Excision Repair and UVB-Induced DNA Damage in Melanomagenesis
journal, January 2013

  • Budden, Timothy; Bowden, Nikola
  • International Journal of Molecular Sciences, Vol. 14, Issue 1
  • DOI: 10.3390/ijms14011132

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


A damage-responsive DNA binding protein regulates transcription of the yeast DNA repair gene PHR1.
journal, December 1991

  • Sebastian, J.; Sancar, G. B.
  • Proceedings of the National Academy of Sciences, Vol. 88, Issue 24
  • DOI: 10.1073/pnas.88.24.11251

SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Gene prediction with a hidden Markov model and a new intron submodel
journal, September 2003


Kloeckera taiwanica sp. nov., an ascomycetous apiculate yeast species isolated from mushroom fruiting bodies
journal, August 2011

  • Chang, C. -F.; Huang, L. -Y.; Chen, S. -F.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 6
  • DOI: 10.1099/ijs.0.034231-0

Prevalent mutator genotype identified in fungal pathogen Candida glabrata promotes multi-drug resistance
journal, March 2016

  • Healey, Kelley R.; Zhao, Yanan; Perez, Winder B.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11128

POL32 , a subunit of the Saccharomyces cerevisiae DNA polymerase δ, defines a link between DNA replication and the mutagenic bypass repair pathway
journal, November 2000

  • Huang, Meng-Er; de Calignon, Alix; Nicolas, Alain
  • Current Genetics, Vol. 38, Issue 4
  • DOI: 10.1007/s002940000149

Systematic Identification of Pathways That Couple Cell Growth and Division in Yeast
journal, June 2002


Selection-Driven Gene Loss in Bacteria
journal, June 2012


nQuire: a statistical framework for ploidy estimation using next generation sequencing
journal, April 2018


A beginner's guide to eukaryotic genome annotation
journal, April 2012

  • Yandell, Mark; Ence, Daniel
  • Nature Reviews Genetics, Vol. 13, Issue 5
  • DOI: 10.1038/nrg3174

Simplicity and Complexity of Microsporidian Genomes
journal, December 2004


The MaSuRCA genome assembler
journal, August 2013


A Rapid Bootstrap Algorithm for the RAxML Web Servers
journal, October 2008

  • Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques
  • Systematic Biology, Vol. 57, Issue 5
  • DOI: 10.1080/10635150802429642

ABySS: A parallel assembler for short read sequence data
journal, February 2009


Yeast Cbk1 and Mob2 Activate Daughter-Specific Genetic Programs to Induce Asymmetric Cell Fates
journal, December 2001


PAML 4: Phylogenetic Analysis by Maximum Likelihood
journal, April 2007


Functional profiling of the Saccharomyces cerevisiae genome
journal, July 2002


The NumPy Array: A Structure for Efficient Numerical Computation
journal, March 2011

  • van der Walt, Stéfan; Colbert, S. Chris; Varoquaux, Gaël
  • Computing in Science & Engineering, Vol. 13, Issue 2
  • DOI: 10.1109/MCSE.2011.37

The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell
journal, May 2010


MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013

  • Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1183

Coevolution with viruses drives the evolution of bacterial mutation rates
journal, December 2007

  • Pal, Csaba; Maciá, María D.; Oliver, Antonio
  • Nature, Vol. 450, Issue 7172
  • DOI: 10.1038/nature06350

Tyrosyl-DNA phosphodiesterase (Tdp1) participates in the repair of Top2-mediated DNA damage
journal, June 2006

  • Nitiss, K. C.; Malik, M.; He, X.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 24
  • DOI: 10.1073/pnas.0603455103

A review on SNP and other types of molecular markers and their use in animal genetics
journal, May 2002

  • Vignal, Alain; Milan, Denis; SanCristobal, Magali
  • Genetics Selection Evolution, Vol. 34, Issue 3
  • DOI: 10.1186/1297-9686-34-3-275

The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine
journal, May 2013

  • Yoshida, Kentaro; Schuenemann, Verena J.; Cano, Liliana M.
  • eLife, Vol. 2
  • DOI: 10.7554/eLife.00731

Hanseniaspora uvarum from Winemaking Environments Show Spatial and Temporal Genetic Clustering
journal, January 2016

  • Albertin, Warren; Setati, Mathabatha E.; Miot-Sertier, Cécile
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01569

OrthoDB: a hierarchical catalog of animal, fungal and bacterial orthologs
journal, November 2012

  • Waterhouse, Robert M.; Tegenfeldt, Fredrik; Li, Jia
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1116

Autorepression of Rfx1 Gene Expression: Functional Conservation from Yeast to Humans in Response to DNA Replication Arrest
journal, November 2005


Copy Number Variation in Fungi and Its Implications for Wine Yeast Genetic Diversity and Adaptation
journal, February 2018


Genome Sequences of Three Species of Hanseniaspora Isolated from Spontaneous Wine Fermentations: TABLE 1 
journal, November 2016


Survival and Growth of Yeast without Telomere Capping by Cdc13 in the Absence of Sgs1, Exo1, and Rad9
journal, August 2010


PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
journal, July 2006

  • Suyama, M.; Torrents, D.; Bork, P.
  • Nucleic Acids Research, Vol. 34, Issue Web Server
  • DOI: 10.1093/nar/gkl315

A Population Genomics Approach to Assessing the Genetic Basis of Within-Host Microevolution Underlying Recurrent Cryptococcal Meningitis Infection
journal, February 2017

  • Rhodes, Johanna; Beale, Mathew A.; Vanhove, Mathieu
  • G3: Genes|Genomes|Genetics, Vol. 7, Issue 4
  • DOI: 10.1534/g3.116.037499

Comprehensive variation discovery in single human genomes
journal, October 2014

  • Weisenfeld, Neil I.; Yin, Shuangye; Sharpe, Ted
  • Nature Genetics, Vol. 46, Issue 12
  • DOI: 10.1038/ng.3121

Structure of the DASH/Dam1 complex shows its role at the yeast kinetochore-microtubule interface
journal, May 2018


Rate, molecular spectrum, and consequences of human mutation
journal, January 2010


MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects
journal, December 2011


Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
journal, November 2018


Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi
journal, May 2016

  • Medina, Edgar M.; Turner, Jonathan J.; Gordân, Raluca
  • eLife, Vol. 5
  • DOI: 10.7554/eLife.09492

Precise estimates of mutation rate and spectrum in yeast
journal, May 2014

  • Zhu, Y. O.; Siegal, M. L.; Hall, D. W.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
  • DOI: 10.1073/pnas.1323011111

Role of mutator alleles in adaptive evolution
journal, June 1997

  • Taddei, F.; Radman, M.; Maynard-Smith, J.
  • Nature, Vol. 387, Issue 6634
  • DOI: 10.1038/42696

An Improved General Amino Acid Replacement Matrix
journal, April 2008


Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection
journal, February 2006

  • Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki
  • Molecular Systems Biology, Vol. 2, Article No. 2006.0008
  • DOI: 10.1038/msb4100050

Genome-scale mutational signatures of aflatoxin in cells, mice, and human tumors
journal, July 2017


Checkpoint Adaptation Precedes Spontaneous and Damage-Induced Genomic Instability in Yeast
journal, March 2001


Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi
journal, May 2010

  • Slot, J. C.; Rokas, A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 22
  • DOI: 10.1073/pnas.0914418107

Evidence That Mutation Is Universally Biased towards AT in Bacteria
journal, September 2010


A Gip1p–Glc7p phosphatase complex regulates septin organization and spore wall formation
journal, November 2001

  • Tachikawa, Hiroyuki; Bloecher, Andrew; Tatchell, Kelly
  • The Journal of Cell Biology, Vol. 155, Issue 5
  • DOI: 10.1083/jcb.200107008

The functional spectrum of low-frequency coding variation
journal, January 2011


The Mechanisms of UV Mutagenesis
journal, January 2011

  • Ikehata, Hironobu; Ono, Tetsuya
  • Journal of Radiation Research, Vol. 52, Issue 2
  • DOI: 10.1269/jrr.10175

Evolution of the angiosperms: calibrating the family tree
journal, November 2001

  • Wikström, Niklas; Savolainen, Vincent; Chase, Mark W.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 268, Issue 1482
  • DOI: 10.1098/rspb.2001.1782

Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines
journal, May 2009

  • Keightley, P. D.; Trivedi, U.; Thomson, M.
  • Genome Research, Vol. 19, Issue 7
  • DOI: 10.1101/gr.091231.109

Control-FREEC: a tool for assessing copy number and allelic content using next-generation sequencing data
journal, December 2011


ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes
journal, June 2015


Sucrose Utilization in Budding Yeast as a Model for the Origin of Undifferentiated Multicellularity
journal, August 2011


Genomic evidence reveals a radiation of placental mammals uninterrupted by the KPg boundary
journal, August 2017

  • Liu, Liang; Zhang, Jin; Rheindt, Frank E.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 35
  • DOI: 10.1073/pnas.1616744114

The DNA damage response: putting checkpoints in perspective
journal, November 2000

  • Zhou, Bin-Bing S.; Elledge, Stephen J.
  • Nature, Vol. 408, Issue 6811
  • DOI: 10.1038/35044005

Structure of the MIND Complex Defines a Regulatory Focus for Yeast Kinetochore Assembly
journal, November 2016


Genome measures used for quality control are dependent on gene function and ancestry
journal, October 2014


Mutational landscape of yeast mutator strains
journal, January 2014

  • Serero, Alexandre; Jubin, Claire; Loeillet, Sophie
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 5
  • DOI: 10.1073/pnas.1314423111

Three new species of bipolar budding yeasts of the genus Hanseniaspora and its anamorph Kloeckera isolated in Thailand
journal, December 2009


Quality Control by DNA Repair
journal, December 1999


OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


Genome Sequence of the Wine Yeast Saccharomycodes ludwigii UTAD17
journal, November 2018

  • Tavares, Maria J.; Güldener, Ulrich; Esteves, Marcos
  • Microbiology Resource Announcements, Vol. 7, Issue 18
  • DOI: 10.1128/MRA.01195-18

Deletion of the MAG1 DNA glycosylase gene suppresses alkylation-induced killing and mutagenesis in yeast cells lacking AP endonucleases
journal, December 2001


DNA Polymerase 4 of Saccharomyces cerevisiae Is Important for Accurate Repair of Methyl-Methanesulfonate-Induced DNA Damage
journal, October 2005


Evolutionary trees from DNA sequences: A maximum likelihood approach
journal, November 1981

  • Felsenstein, Joseph
  • Journal of Molecular Evolution, Vol. 17, Issue 6
  • DOI: 10.1007/BF01734359

Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts
journal, September 2004

  • Hittinger, C. T.; Rokas, A.; Carroll, S. B.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 39
  • DOI: 10.1073/pnas.0404319101

In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the Design and Analysis of de novo Genome Sequencing Studies
journal, September 2016

  • Zhou, Xiaofan; Peris, David; Kominek, Jacek
  • G3: Genes|Genomes|Genetics, Vol. 6, Issue 11
  • DOI: 10.1534/g3.116.034249

Accelerated Profile HMM Searches
journal, October 2011


trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


Efficient de novo assembly of large genomes using compressed data structures
journal, December 2011


Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Expression of the yeast PHR1 gene is induced by DNA-damaging agents.
journal, September 1990

  • Sebastian, J.; Kraus, B.; Sancar, G. B.
  • Molecular and Cellular Biology, Vol. 10, Issue 9
  • DOI: 10.1128/MCB.10.9.4630

Natural yeast flora of different varieties of grapes used for wine making in India
journal, December 2009


Factors driving metabolic diversity in the budding yeast subphylum
journal, March 2018


Genomic insights into the evolutionary origin of Myxozoa within Cnidaria
journal, November 2015

  • Chang, E. Sally; Neuhof, Moran; Rubinstein, Nimrod D.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 48
  • DOI: 10.1073/pnas.1511468112

BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler
journal, December 2012


Approximate Likelihood Calculation on a Phylogeny for Bayesian Estimation of Divergence Times
journal, February 2011


Gene duplication and co-evolution of G1/S transcription factor specificity in fungi are essential for optimizing cell fitness
journal, May 2017


The Saccharomyces cerevisiae PCD1 Gene Encodes a Peroxisomal Nudix Hydrolase Active toward Coenzyme A and Its Derivatives
journal, August 2000

  • Cartwright, Jared L.; Gasmi, Lakhdar; Spiller, David G.
  • Journal of Biological Chemistry, Vol. 275, Issue 42
  • DOI: 10.1074/jbc.M005015200

The base excision repair pathway
journal, October 1995


Non-randomness of Ammo-acid Changes in the Evolution of Homologous Proteins
journal, July 1967


Informed and automated k-mer size selection for genome assembly
journal, June 2013


Bayesian molecular clock dating of species divergences in the genomics era
journal, December 2015

  • dos Reis, Mario; Donoghue, Philip C. J.; Yang, Ziheng
  • Nature Reviews Genetics, Vol. 17, Issue 2
  • DOI: 10.1038/nrg.2015.8

Endogenous DNA damage in humans: a review of quantitative data
journal, May 2004


Suppression of Spontaneous Chromosomal Rearrangements by S Phase Checkpoint Functions in Saccharomyces cerevisiae
journal, February 2001


Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training
journal, October 2008

  • Ter-Hovhannisyan, V.; Lomsadze, A.; Chernoff, Y. O.
  • Genome Research, Vol. 18, Issue 12
  • DOI: 10.1101/gr.081612.108

Saccharomyces Genome Database: the genomics resource of budding yeast
journal, November 2011

  • Cherry, J. M.; Hong, E. L.; Amundsen, C.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1029

Natural mismatch repair mutations mediate phenotypic diversity and drug resistance in Cryptococcus deuterogattii
journal, September 2017

  • Billmyre, R. Blake; Clancey, Shelly Applen; Heitman, Joseph
  • eLife, Vol. 6
  • DOI: 10.7554/eLife.28802

Hanseniaspora jakobsenii sp. nov., a yeast isolated from Bandji, a traditional palm wine of Borassus akeassii
journal, October 2015

  • Diawara, Bréhima; Kando, Christine; Anyogu, Amarachukwu
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 10
  • DOI: 10.1099/ijsem.0.000461

BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics
journal, December 2017

  • Waterhouse, Robert M.; Seppey, Mathieu; Simão, Felipe A.
  • Molecular Biology and Evolution, Vol. 35, Issue 3
  • DOI: 10.1093/molbev/msx319

Clade- and species-specific features of genome evolution in the Saccharomycetaceae
journal, June 2015

  • Wolfe, Kenneth H.; Armisén, David; Proux-Wera, Estelle
  • FEMS Yeast Research, Vol. 15, Issue 5
  • DOI: 10.1093/femsyr/fov035

The Sequence Alignment/Map format and SAMtools
journal, June 2009


Gene Essentiality Analyzed by In Vivo Transposon Mutagenesis and Machine Learning in a Stable Haploid Isolate of Candida albicans
journal, October 2018

  • Segal, Ella Shtifman; Gritsenko, Vladimir; Levitan, Anton
  • mBio, Vol. 9, Issue 5
  • DOI: 10.1128/mBio.02048-18

A genome-wide view of the spectrum of spontaneous mutations in yeast
journal, June 2008

  • Lynch, M.; Sung, W.; Morris, K.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 27
  • DOI: 10.1073/pnas.0803466105

Evolution by gene loss
journal, April 2016

  • Albalat, Ricard; Cañestro, Cristian
  • Nature Reviews Genetics, Vol. 17, Issue 7
  • DOI: 10.1038/nrg.2016.39

From Sugar of Grape to Alcohol of Wine: Sensorial Impact of Alcohol in Wine
journal, November 2015


Graph clustering
journal, August 2007


The Origins of Genome Architecture
journal, July 2007


Using BLOSUM in Sequence Alignments
journal, May 2008

  • Mount, D. W.
  • Cold Spring Harbor Protocols, Vol. 2008, Issue 6
  • DOI: 10.1101/pdb.top39

Lighter: fast and memory-efficient sequencing error correction without counting
journal, January 2014


    Works referencing / citing this record:

    5-fluorocytosine resistance is associated with hypermutation and alterations in capsule biosynthesis in Cryptococcus
    journal, January 2020