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

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

doi:10.1371/journal.pbio.3000255

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

Journal Article · Tue May 21 00:00:00 EDT 2019 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.3000255· OSTI ID:1630352

; Opulente, Dana A.; Kominek, Jacek;

;

; Libkind, Diego; DeVirgilio, Jeremy; Hulfachor, Amanda Beth; Kurtzman, Cletus P.;

;

; Kamoun, ed., Sophien

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.

View Journal Article

Cite

Export

Save

Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

Contributing Organization:: 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

Grant/Contract Number:: BER DE-FC02-07ER64494 and DE-SC0018409; SC0018409; FC02-07ER64494

OSTI ID:: 1630352

Alternate ID(s):: OSTI ID: 1556080

Journal Information:: PLoS Biology (Online), Journal Name: PLoS Biology (Online) Vol. 17 Journal Issue: 5; ISSN 1545-7885

Publisher:: Public Library of Science (PLoS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 73 works

Citation information provided by
Web of Science

References (148)

Phylogenomics Philippe, Hervé; Delsuc, Frédéric; Brinkmann, Henner Annual Review of Ecology, Evolution, and Systematics, Vol. 36, Issue 1 https://doi.org/10.1146/annurev.ecolsys.35.112202.130205	journal	December 2005
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
The Gene Ontology (GO) database and informatics resource Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh036	journal	January 2004
Whole Genome Analysis of 132 Clinical Saccharomyces cerevisiae Strains Reveals Extensive Ploidy Variation Zhu, Yuan O.; Sherlock, Gavin; Petrov, Dmitri A. G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 8 https://doi.org/10.1534/g3.116.029397	journal	June 2016
Lighter: fast and memory-efficient sequencing error correction without counting Song, Li; Florea, Liliana; Langmead, Ben Genome Biology, Vol. 15, Issue 11 https://doi.org/10.1186/s13059-014-0509-9	journal	November 2014
ploidyNGS: visually exploring ploidy with Next Generation Sequencing data Augusto Corrêa dos Santos, Renato; Goldman, Gustavo Henrique; Riaño-Pachón, Diego Mauricio Bioinformatics, Vol. 33, Issue 16 https://doi.org/10.1093/bioinformatics/btx204	journal	April 2017
Genome Sequence of the Native Apiculate Wine Yeast Hanseniaspora vineae T02/19AF Giorello, F. M.; Berna, L.; Greif, G. Genome Announcements, Vol. 2, Issue 3 https://doi.org/10.1128/genomeA.00530-14	journal	May 2014
Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data Shen, Xing-Xing; Zhou, Xiaofan; Kominek, Jacek G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 12 https://doi.org/10.1534/g3.116.034744	journal	September 2016
Anaphase-Promoting Complex 7 is a Prognostic Factor in Human Colorectal Cancer Kim, Ik Yong; Kwon, Hye Yeon; Park, Kwang Hwa Annals of Coloproctology, Vol. 33, Issue 4 https://doi.org/10.3393/ac.2017.33.4.139	journal	August 2017
IME1, a positive regulator gene of meiosis in S. cerevisiae Kassir, Yona; Granot, David; Simchen, Giora Cell, Vol. 52, Issue 6 https://doi.org/10.1016/0092-8674(88)90427-8	journal	March 1988
Evolution of networks and sequences in eukaryotic cell cycle control Cross, Frederick R.; Buchler, Nicolas E.; Skotheim, Jan M. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1584 https://doi.org/10.1098/rstb.2011.0078	journal	December 2011
The Evolution of Low Mutation Rates in Experimental Mutator Populations of Saccharomyces cerevisiae McDonald, Michael J.; Hsieh, Yu-Ying; Yu, Yen-Hsin Current Biology, Vol. 22, Issue 13 https://doi.org/10.1016/j.cub.2012.04.056	journal	July 2012
Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Weinert, T. A.; Kiser, G. L.; Hartwell, L. H. Genes & Development, Vol. 8, Issue 6 https://doi.org/10.1101/gad.8.6.652	journal	March 1994
Mad1 contribution to spindle assembly checkpoint signalling goes beyond presenting Mad2 at kinetochores Heinrich, S.; Sewart, K.; Windecker, H. EMBO reports, Vol. 15, Issue 3 https://doi.org/10.1002/embr.201338114	journal	January 2014
SSP1, a gene necessary for proper completion of meiotic divisions and spore formation in Saccharomyces cerevisiae. Nag, D. K.; Koonce, M. P.; Axelrod, J. Molecular and Cellular Biology, Vol. 17, Issue 12 https://doi.org/10.1128/MCB.17.12.7029	journal	December 1997
CDK Activity Antagonizes Whi5, an Inhibitor of G1/S Transcription in Yeast Costanzo, Michael; Nishikawa, Joy L.; Tang, Xiaojing Cell, Vol. 117, Issue 7 https://doi.org/10.1016/j.cell.2004.05.024	journal	June 2004
GOATOOLS: A Python library for Gene Ontology analyses Klopfenstein, D. V.; Zhang, Liangsheng; Pedersen, Brent S. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-28948-z	journal	July 2018
Biopython: freely available Python tools for computational molecular biology and bioinformatics Cock, P. J. A.; Antao, T.; Chang, J. T. Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp163	journal	March 2009
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Relations between chemical structure and biological activity in peptides Sneath, P. H. A. Journal of Theoretical Biology, Vol. 12, Issue 2 https://doi.org/10.1016/0022-5193(66)90112-3	journal	November 1966
DNA-damage repair; the good, the bad, and the ugly Hakem, Razqallah The EMBO Journal, Vol. 27, Issue 4 https://doi.org/10.1038/emboj.2008.15	journal	February 2008
Comprehensive Analysis of Hypermutation in Human Cancer Campbell, Brittany B.; Light, Nicholas; Fabrizio, David Cell, Vol. 171, Issue 5 https://doi.org/10.1016/j.cell.2017.09.048	journal	November 2017
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Evolution of high mutation rates in experimental populations of E. coli Sniegowski, Paul D.; Gerrish, Philip J.; Lenski, Richard E. Nature, Vol. 387, Issue 6634 https://doi.org/10.1038/42701	journal	June 1997
Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi Katinka, Michaël D.; Duprat, Simone; Cornillot, Emmanuel Nature, Vol. 414, Issue 6862 https://doi.org/10.1038/35106579	journal	November 2001
DNA Damage Response Genes and the Development of Cancer Metastasis Broustas, Constantinos G.; Lieberman, Howard B. Radiation Research, Vol. 181, Issue 2 https://doi.org/10.1667/RR13515.1	journal	February 2014
Oenological Impact of the Hanseniaspora/Kloeckera Yeast Genus on Wines—A Review Martin, Valentina; Valera, Maria; Medina, Karina Fermentation, Vol. 4, Issue 3 https://doi.org/10.3390/fermentation4030076	journal	September 2018
Remarkably ancient balanced polymorphisms in a multi-locus gene network Hittinger, Chris Todd; Gonçalves, Paula; Sampaio, José Paulo Nature, Vol. 464, Issue 7285 https://doi.org/10.1038/nature08791	journal	February 2010
The anaphase-promoting complex: a key factor in the regulation of cell cycle Castro, Anna; Bernis, Cyril; Vigneron, Suzanne Oncogene, Vol. 24, Issue 3 https://doi.org/10.1038/sj.onc.1207973	journal	January 2005
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
An Introduction to Sequence Similarity (“Homology”) Searching Pearson, William R. Current Protocols in Bioinformatics, Vol. 42, Issue 1 https://doi.org/10.1002/0471250953.bi0301s42	journal	June 2013
Functional Characterization of the S. cerevisiae Genome by Gene Deletion and Parallel Analysis Winzeler, E. A. Science, Vol. 285, Issue 5429 https://doi.org/10.1126/science.285.5429.901	journal	August 1999
Genome-scale approaches to resolving incongruence in molecular phylogenies Rokas, Antonis; Williams, Barry L.; King, Nicole Nature, Vol. 425, Issue 6960 https://doi.org/10.1038/nature02053	journal	October 2003
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
Comparative genomics of biotechnologically important yeasts Riley, Robert; Haridas, Sajeet; Wolfe, Kenneth H. Proceedings of the National Academy of Sciences, Vol. 113, Issue 35 https://doi.org/10.1073/pnas.1603941113	journal	August 2016
The Role of Altered Nucleotide Excision Repair and UVB-Induced DNA Damage in Melanomagenesis Budden, Timothy; Bowden, Nikola International Journal of Molecular Sciences, Vol. 14, Issue 1 https://doi.org/10.3390/ijms14011132	journal	January 2013
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Analysis of Low Molecular Weight Carbohydrates in Food and Beverages: A Review Martínez Montero, C.; Rodríguez Dodero, M. C.; Guillén Sánchez, D. A. Chromatographia, Vol. 59, Issue 1-2 https://doi.org/10.1365/s10337-003-0134-3	journal	January 2004
A damage-responsive DNA binding protein regulates transcription of the yeast DNA repair gene PHR1. Sebastian, J.; Sancar, G. B. Proceedings of the National Academy of Sciences, Vol. 88, Issue 24 https://doi.org/10.1073/pnas.88.24.11251	journal	December 1991
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
Gene prediction with a hidden Markov model and a new intron submodel Stanke, M.; Waack, S. Bioinformatics, Vol. 19, Issue Suppl 2 https://doi.org/10.1093/bioinformatics/btg1080	journal	September 2003
Kloeckera taiwanica sp. nov., an ascomycetous apiculate yeast species isolated from mushroom fruiting bodies Chang, C. -F.; Huang, L. -Y.; Chen, S. -F. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 6 https://doi.org/10.1099/ijs.0.034231-0	journal	August 2011
Prevalent mutator genotype identified in fungal pathogen Candida glabrata promotes multi-drug resistance Healey, Kelley R.; Zhao, Yanan; Perez, Winder B. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11128	journal	March 2016
POL32 , a subunit of the Saccharomyces cerevisiae DNA polymerase δ, defines a link between DNA replication and the mutagenic bypass repair pathway Huang, Meng-Er; de Calignon, Alix; Nicolas, Alain Current Genetics, Vol. 38, Issue 4 https://doi.org/10.1007/s002940000149	journal	November 2000
Systematic Identification of Pathways That Couple Cell Growth and Division in Yeast Jorgensen, P. Science, Vol. 297, Issue 5580 https://doi.org/10.1126/science.1070850	journal	June 2002
Selection-Driven Gene Loss in Bacteria Koskiniemi, Sanna; Sun, Song; Berg, Otto G. PLoS Genetics, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pgen.1002787	journal	June 2012
Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells Hartwell, Leland Cell, Vol. 71, Issue 4 https://doi.org/10.1016/0092-8674(92)90586-2	journal	November 1992
nQuire: a statistical framework for ploidy estimation using next generation sequencing Weiß, Clemens L.; Pais, Marina; Cano, Liliana M. BMC Bioinformatics, Vol. 19, Issue 1 https://doi.org/10.1186/s12859-018-2128-z	journal	April 2018
A beginner's guide to eukaryotic genome annotation Yandell, Mark; Ence, Daniel Nature Reviews Genetics, Vol. 13, Issue 5 https://doi.org/10.1038/nrg3174	journal	April 2012
Gene finding in novel genomes Korf, Ian BMC Bioinformatics, Vol. 5, Issue 1 https://doi.org/10.1186/1471-2105-5-59	journal	May 2004
Simplicity and Complexity of Microsporidian Genomes Keeling, Patrick J.; Slamovits, Claudio H. Eukaryotic Cell, Vol. 3, Issue 6 https://doi.org/10.1128/EC.3.6.1363-1369.2004	journal	December 2004
Costs and Benefits of High Mutation Rates: Adaptive Evolution of Bacteria in the Mouse Gut Giraud, A. Science, Vol. 291, Issue 5513 https://doi.org/10.1126/science.1056421	journal	March 2001
The MaSuRCA genome assembler Zimin, Aleksey V.; Marçais, Guillaume; Puiu, Daniela Bioinformatics, Vol. 29, Issue 21 https://doi.org/10.1093/bioinformatics/btt476	journal	August 2013
A Rapid Bootstrap Algorithm for the RAxML Web Servers Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques Systematic Biology, Vol. 57, Issue 5 https://doi.org/10.1080/10635150802429642	journal	October 2008
ABySS: A parallel assembler for short read sequence data Simpson, J. T.; Wong, K.; Jackman, S. D. Genome Research, Vol. 19, Issue 6 https://doi.org/10.1101/gr.089532.108	journal	February 2009
Yeast Cbk1 and Mob2 Activate Daughter-Specific Genetic Programs to Induce Asymmetric Cell Fates Colman-Lerner, Alejandro; Chin, Tina E.; Brent, Roger Cell, Vol. 107, Issue 6 https://doi.org/10.1016/S0092-8674(01)00596-7	journal	December 2001
PAML 4: Phylogenetic Analysis by Maximum Likelihood Yang, Z. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm088	journal	April 2007
Functional profiling of the Saccharomyces cerevisiae genome Giaever, Guri; Chu, Angela M.; Ni, Li Nature, Vol. 418, Issue 6896 https://doi.org/10.1038/nature00935	journal	July 2002
The NumPy Array: A Structure for Efficient Numerical Computation van der Walt, Stéfan; Colbert, S. Chris; Varoquaux, Gaël Computing in Science & Engineering, Vol. 13, Issue 2 https://doi.org/10.1109/MCSE.2011.37	journal	March 2011
Genomic content of a novel yeast species Hanseniaspora gamundiae sp. nov. from fungal stromata (Cyttaria) associated with a unique fermented beverage in Andean Patagonia, Argentina Čadež, Neža; Bellora, Nicolas; Ulloa, Ricardo PLOS ONE, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pone.0210792	journal	January 2019
The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell Junier, T.; Zdobnov, E. M. Bioinformatics, Vol. 26, Issue 13 https://doi.org/10.1093/bioinformatics/btq243	journal	May 2010
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
Coevolution with viruses drives the evolution of bacterial mutation rates Pal, Csaba; Maciá, María D.; Oliver, Antonio Nature, Vol. 450, Issue 7172 https://doi.org/10.1038/nature06350	journal	December 2007
Extensive Copy Number Variation in Fermentation-Related Genes AmongSaccharomyces cerevisiaeWine Strains Steenwyk, Jacob; Rokas, Antonis G3 Genes\|Genomes\|Genetics, Vol. 7, Issue 5 https://doi.org/10.1534/g3.117.040105	journal	May 2017
Tyrosyl-DNA phosphodiesterase (Tdp1) participates in the repair of Top2-mediated DNA damage Nitiss, K. C.; Malik, M.; He, X. Proceedings of the National Academy of Sciences, Vol. 103, Issue 24 https://doi.org/10.1073/pnas.0603455103	journal	June 2006
A review on SNP and other types of molecular markers and their use in animal genetics Vignal, Alain; Milan, Denis; SanCristobal, Magali Genetics Selection Evolution, Vol. 34, Issue 3 https://doi.org/10.1186/1297-9686-34-3-275	journal	May 2002
The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine Yoshida, Kentaro; Schuenemann, Verena J.; Cano, Liliana M. eLife, Vol. 2 https://doi.org/10.7554/eLife.00731	journal	May 2013
Hanseniaspora uvarum from Winemaking Environments Show Spatial and Temporal Genetic Clustering Albertin, Warren; Setati, Mathabatha E.; Miot-Sertier, Cécile Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01569	journal	January 2016
OrthoDB: a hierarchical catalog of animal, fungal and bacterial orthologs Waterhouse, Robert M.; Tegenfeldt, Fredrik; Li, Jia Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1116	journal	November 2012
Autorepression of Rfx1 Gene Expression: Functional Conservation from Yeast to Humans in Response to DNA Replication Arrest Lubelsky, Y.; Reuven, N.; Shaul, Y. Molecular and Cellular Biology, Vol. 25, Issue 23 https://doi.org/10.1128/MCB.25.23.10665-10673.2005	journal	November 2005
Copy Number Variation in Fungi and Its Implications for Wine Yeast Genetic Diversity and Adaptation Steenwyk, Jacob L.; Rokas, Antonis Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00288	journal	February 2018
Genome Sequences of Three Species of Hanseniaspora Isolated from Spontaneous Wine Fermentations: TABLE 1 Sternes, Peter R.; Lee, Danna; Kutyna, Dariusz R. Genome Announcements, Vol. 4, Issue 6 https://doi.org/10.1128/genomeA.01287-16	journal	November 2016
Survival and Growth of Yeast without Telomere Capping by Cdc13 in the Absence of Sgs1, Exo1, and Rad9 Ngo, Hien-Ping; Lydall, David PLoS Genetics, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pgen.1001072	journal	August 2010
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments Suyama, M.; Torrents, D.; Bork, P. Nucleic Acids Research, Vol. 34, Issue Web Server https://doi.org/10.1093/nar/gkl315	journal	July 2006
A Population Genomics Approach to Assessing the Genetic Basis of Within-Host Microevolution Underlying Recurrent Cryptococcal Meningitis Infection Rhodes, Johanna; Beale, Mathew A.; Vanhove, Mathieu G3: Genes\|Genomes\|Genetics, Vol. 7, Issue 4 https://doi.org/10.1534/g3.116.037499	journal	February 2017
Comprehensive variation discovery in single human genomes Weisenfeld, Neil I.; Yin, Shuangye; Sharpe, Ted Nature Genetics, Vol. 46, Issue 12 https://doi.org/10.1038/ng.3121	journal	October 2014
Structure of the DASH/Dam1 complex shows its role at the yeast kinetochore-microtubule interface Jenni, Simon; Harrison, Stephen C. Science, Vol. 360, Issue 6388 https://doi.org/10.1126/science.aar6436	journal	May 2018
Rate, molecular spectrum, and consequences of human mutation Lynch, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 3 https://doi.org/10.1073/pnas.0912629107	journal	January 2010
MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects Holt, Carson; Yandell, Mark BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-491	journal	December 2011
Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum Shen, Xing-Xing; Opulente, Dana A.; Kominek, Jacek Cell, Vol. 175, Issue 6 https://doi.org/10.1016/j.cell.2018.10.023	journal	November 2018
Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi Medina, Edgar M.; Turner, Jonathan J.; Gordân, Raluca eLife, Vol. 5 https://doi.org/10.7554/eLife.09492	journal	May 2016
Precise estimates of mutation rate and spectrum in yeast Zhu, Y. O.; Siegal, M. L.; Hall, D. W. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1323011111	journal	May 2014
Role of mutator alleles in adaptive evolution Taddei, F.; Radman, M.; Maynard-Smith, J. Nature, Vol. 387, Issue 6634 https://doi.org/10.1038/42696	journal	June 1997
An Improved General Amino Acid Replacement Matrix Le, S. Q.; Gascuel, O. Molecular Biology and Evolution, Vol. 25, Issue 7 https://doi.org/10.1093/molbev/msn067	journal	April 2008
Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki Molecular Systems Biology, Vol. 2, Article No. 2006.0008 https://doi.org/10.1038/msb4100050	journal	February 2006
Genome-scale mutational signatures of aflatoxin in cells, mice, and human tumors Huang, Mi Ni; Yu, Willie; Teoh, Wei Wei Genome Research, Vol. 27, Issue 9 https://doi.org/10.1101/gr.220038.116	journal	July 2017
Checkpoint Adaptation Precedes Spontaneous and Damage-Induced Genomic Instability in Yeast Galgoczy, D. J.; Toczyski, D. P. Molecular and Cellular Biology, Vol. 21, Issue 5 https://doi.org/10.1128/MCB.21.5.1710-1718.2001	journal	March 2001
Phylogenetic placement of Hanseniaspora-Kloeckera species using multigene sequence analysis with taxonomic implications: descriptions of Hanseniaspora pseudoguilliermondii sp. nov. and Hanseniaspora occidentalis var. citrica var. nov. Cadez, N. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 5 https://doi.org/10.1099/ijs.0.64052-0	journal	May 2006
Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi Slot, J. C.; Rokas, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 22 https://doi.org/10.1073/pnas.0914418107	journal	May 2010
A novel Nudix hydrolase for oxidized purine nucleoside triphosphates encoded by ORFYLR151c (PCD1 gene) in Saccharomyces cerevisiae Nunoshiba, T. Nucleic Acids Research, Vol. 32, Issue 18 https://doi.org/10.1093/nar/gkh868	journal	October 2004
Evidence That Mutation Is Universally Biased towards AT in Bacteria Hershberg, Ruth; Petrov, Dmitri A. PLoS Genetics, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pgen.1001115	journal	September 2010
A Gip1p–Glc7p phosphatase complex regulates septin organization and spore wall formation Tachikawa, Hiroyuki; Bloecher, Andrew; Tatchell, Kelly The Journal of Cell Biology, Vol. 155, Issue 5 https://doi.org/10.1083/jcb.200107008	journal	November 2001
The functional spectrum of low-frequency coding variation Marth, Gabor T.; Yu, Fuli; Indap, Amit R. Genome Biology, Vol. 12, Issue 9 https://doi.org/10.1186/gb-2011-12-9-r84	journal	January 2011
The Mechanisms of UV Mutagenesis Ikehata, Hironobu; Ono, Tetsuya Journal of Radiation Research, Vol. 52, Issue 2 https://doi.org/10.1269/jrr.10175	journal	January 2011
Evolution of the angiosperms: calibrating the family tree Wikström, Niklas; Savolainen, Vincent; Chase, Mark W. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 268, Issue 1482 https://doi.org/10.1098/rspb.2001.1782	journal	November 2001
Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines Keightley, P. D.; Trivedi, U.; Thomson, M. Genome Research, Vol. 19, Issue 7 https://doi.org/10.1101/gr.091231.109	journal	May 2009
Control-FREEC: a tool for assessing copy number and allelic content using next-generation sequencing data Boeva, Valentina; Popova, Tatiana; Bleakley, Kevin Bioinformatics, Vol. 28, Issue 3 https://doi.org/10.1093/bioinformatics/btr670	journal	December 2011
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes Mirarab, Siavash; Warnow, Tandy Bioinformatics, Vol. 31, Issue 12 https://doi.org/10.1093/bioinformatics/btv234	journal	June 2015
Sucrose Utilization in Budding Yeast as a Model for the Origin of Undifferentiated Multicellularity H. Koschwanez, John; R. Foster, Kevin; W. Murray, Andrew PLoS Biology, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pbio.1001122	journal	August 2011
Genomic evidence reveals a radiation of placental mammals uninterrupted by the KPg boundary Liu, Liang; Zhang, Jin; Rheindt, Frank E. Proceedings of the National Academy of Sciences, Vol. 114, Issue 35 https://doi.org/10.1073/pnas.1616744114	journal	August 2017
The DNA damage response: putting checkpoints in perspective Zhou, Bin-Bing S.; Elledge, Stephen J. Nature, Vol. 408, Issue 6811 https://doi.org/10.1038/35044005	journal	November 2000
Structure of the MIND Complex Defines a Regulatory Focus for Yeast Kinetochore Assembly Dimitrova, Yoana N.; Jenni, Simon; Valverde, Roberto Cell, Vol. 167, Issue 4 https://doi.org/10.1016/j.cell.2016.10.011	journal	November 2016
Genome measures used for quality control are dependent on gene function and ancestry Wang, Jing; Raskin, Leon; Samuels, David C. Bioinformatics, Vol. 31, Issue 3 https://doi.org/10.1093/bioinformatics/btu668	journal	October 2014
Mutational landscape of yeast mutator strains Serero, Alexandre; Jubin, Claire; Loeillet, Sophie Proceedings of the National Academy of Sciences, Vol. 111, Issue 5 https://doi.org/10.1073/pnas.1314423111	journal	January 2014
Three new species of bipolar budding yeasts of the genus Hanseniaspora and its anamorph Kloeckera isolated in Thailand Jindamorakot, Sasitorn; Ninomiya, Shinya; Limtong, Savitree FEMS Yeast Research, Vol. 9, Issue 8 https://doi.org/10.1111/j.1567-1364.2009.00568.x	journal	December 2009
High Frequency of Hypermutable Pseudomonas aeruginosa in Cystic Fibrosis Lung Infection Oliver, A. Science, Vol. 288, Issue 5469 https://doi.org/10.1126/science.288.5469.1251	journal	May 2000
Synergism between yeast nucleotide and base excision repair pathways in the protection against DNA methylation damage Xiao, W.; Chow, Barbara L. Current Genetics, Vol. 33, Issue 2 https://doi.org/10.1007/s002940050313	journal	March 1998
Quality Control by DNA Repair Lindahl, T. Science, Vol. 286, Issue 5446 https://doi.org/10.1126/science.286.5446.1897	journal	December 1999
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes Li, L. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.1224503	journal	September 2003
Genome Sequence of the Wine Yeast Saccharomycodes ludwigii UTAD17 Tavares, Maria J.; Güldener, Ulrich; Esteves, Marcos Microbiology Resource Announcements, Vol. 7, Issue 18 https://doi.org/10.1128/MRA.01195-18	journal	November 2018
Deletion of the MAG1 DNA glycosylase gene suppresses alkylation-induced killing and mutagenesis in yeast cells lacking AP endonucleases Xiao, Wei; Chow, Barbara L.; Hanna, Michelle Mutation Research/DNA Repair, Vol. 487, Issue 3-4 https://doi.org/10.1016/S0921-8777(01)00113-6	journal	December 2001
DNA Polymerase 4 of Saccharomyces cerevisiae Is Important for Accurate Repair of Methyl-Methanesulfonate-Induced DNA Damage Sterling, Catherine H.; Sweasy, Joann B. Genetics, Vol. 172, Issue 1 https://doi.org/10.1534/genetics.105.049254	journal	October 2005
Evolutionary trees from DNA sequences: A maximum likelihood approach Felsenstein, Joseph Journal of Molecular Evolution, Vol. 17, Issue 6 https://doi.org/10.1007/BF01734359	journal	November 1981
Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts Hittinger, C. T.; Rokas, A.; Carroll, S. B. Proceedings of the National Academy of Sciences, Vol. 101, Issue 39 https://doi.org/10.1073/pnas.0404319101	journal	September 2004
In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the Design and Analysis of de novo Genome Sequencing Studies Zhou, Xiaofan; Peris, David; Kominek, Jacek G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 11 https://doi.org/10.1534/g3.116.034249	journal	September 2016
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
Efficient de novo assembly of large genomes using compressed data structures Simpson, J. T.; Durbin, R. Genome Research, Vol. 22, Issue 3 https://doi.org/10.1101/gr.126953.111	journal	December 2011
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Expression of the yeast PHR1 gene is induced by DNA-damaging agents. Sebastian, J.; Kraus, B.; Sancar, G. B. Molecular and Cellular Biology, Vol. 10, Issue 9 https://doi.org/10.1128/MCB.10.9.4630	journal	September 1990
Natural yeast flora of different varieties of grapes used for wine making in India Chavan, Pradnya; Mane, Sarika; Kulkarni, Girish Food Microbiology, Vol. 26, Issue 8 https://doi.org/10.1016/j.fm.2009.05.005	journal	December 2009
Factors driving metabolic diversity in the budding yeast subphylum Opulente, Dana A.; Rollinson, Emily J.; Bernick-Roehr, Cleome BMC Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12915-018-0498-3	journal	March 2018
Genomic insights into the evolutionary origin of Myxozoa within Cnidaria Chang, E. Sally; Neuhof, Moran; Rubinstein, Nimrod D. Proceedings of the National Academy of Sciences, Vol. 112, Issue 48 https://doi.org/10.1073/pnas.1511468112	journal	November 2015
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler Luo, Ruibang; Liu, Binghang; Xie, Yinlong GigaScience, Vol. 1, Issue 1 https://doi.org/10.1186/2047-217X-1-18	journal	December 2012
Approximate Likelihood Calculation on a Phylogeny for Bayesian Estimation of Divergence Times Reis, M. d.; Yang, Z. Molecular Biology and Evolution, Vol. 28, Issue 7 https://doi.org/10.1093/molbev/msr045	journal	February 2011
Gene duplication and co-evolution of G1/S transcription factor specificity in fungi are essential for optimizing cell fitness Hendler, Adi; Medina, Edgar M.; Kishkevich, Anastasiya PLOS Genetics, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pgen.1006778	journal	May 2017
The Saccharomyces cerevisiae PCD1 Gene Encodes a Peroxisomal Nudix Hydrolase Active toward Coenzyme A and Its Derivatives Cartwright, Jared L.; Gasmi, Lakhdar; Spiller, David G. Journal of Biological Chemistry, Vol. 275, Issue 42 https://doi.org/10.1074/jbc.M005015200	journal	August 2000
The base excision repair pathway Seeberg, Erling; Eide, Lars; Bjørås, Magnar Trends in Biochemical Sciences, Vol. 20, Issue 10 https://doi.org/10.1016/S0968-0004(00)89086-6	journal	October 1995
Non-randomness of Ammo-acid Changes in the Evolution of Homologous Proteins Epstein, Charles J. Nature, Vol. 215, Issue 5099 https://doi.org/10.1038/215355a0	journal	July 1967
Informed and automated k-mer size selection for genome assembly Chikhi, R.; Medvedev, P. Bioinformatics, Vol. 30, Issue 1 https://doi.org/10.1093/bioinformatics/btt310	journal	June 2013
Bayesian molecular clock dating of species divergences in the genomics era dos Reis, Mario; Donoghue, Philip C. J.; Yang, Ziheng Nature Reviews Genetics, Vol. 17, Issue 2 https://doi.org/10.1038/nrg.2015.8	journal	December 2015
Endogenous DNA damage in humans: a review of quantitative data De Bont, R. Mutagenesis, Vol. 19, Issue 3 https://doi.org/10.1093/mutage/geh025	journal	May 2004
Domestication and Divergence of Saccharomyces cerevisiae Beer Yeasts Gallone, Brigida; Steensels, Jan; Prahl, Troels Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.08.020	journal	September 2016
Suppression of Spontaneous Chromosomal Rearrangements by S Phase Checkpoint Functions in Saccharomyces cerevisiae Myung, Kyungjae; Datta, Abhijit; Kolodner, Richard D. Cell, Vol. 104, Issue 3 https://doi.org/10.1016/S0092-8674(01)00227-6	journal	February 2001
Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training Ter-Hovhannisyan, V.; Lomsadze, A.; Chernoff, Y. O. Genome Research, Vol. 18, Issue 12 https://doi.org/10.1101/gr.081612.108	journal	October 2008
Saccharomyces Genome Database: the genomics resource of budding yeast Cherry, J. M.; Hong, E. L.; Amundsen, C. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1029	journal	November 2011
Natural mismatch repair mutations mediate phenotypic diversity and drug resistance in Cryptococcus deuterogattii Billmyre, R. Blake; Clancey, Shelly Applen; Heitman, Joseph eLife, Vol. 6 https://doi.org/10.7554/eLife.28802	journal	September 2017
Hanseniaspora jakobsenii sp. nov., a yeast isolated from Bandji, a traditional palm wine of Borassus akeassii Diawara, Bréhima; Kando, Christine; Anyogu, Amarachukwu International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 10 https://doi.org/10.1099/ijsem.0.000461	journal	October 2015
Molecular evolution of the telomere-associated MAL loci of Saccharomyces. Charron, M. J.; Read, E.; Haut, S. R. Genetics, Vol. 122, Issue 2 https://doi.org/10.1093/genetics/122.2.307	journal	June 1989
BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics Waterhouse, Robert M.; Seppey, Mathieu; Simão, Felipe A. Molecular Biology and Evolution, Vol. 35, Issue 3 https://doi.org/10.1093/molbev/msx319	journal	December 2017
Clade- and species-specific features of genome evolution in the Saccharomycetaceae Wolfe, Kenneth H.; Armisén, David; Proux-Wera, Estelle FEMS Yeast Research, Vol. 15, Issue 5 https://doi.org/10.1093/femsyr/fov035	journal	June 2015
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Mismatch Repair of DNA Replication Errors Contributes to Microevolution in the Pathogenic Fungus Cryptococcus neoformans Boyce, Kylie J.; Wang, Yina; Verma, Surbhi mBio, Vol. 8, Issue 3 https://doi.org/10.1128/mBio.00595-17	journal	May 2017
Gene Essentiality Analyzed by In Vivo Transposon Mutagenesis and Machine Learning in a Stable Haploid Isolate of Candida albicans Segal, Ella Shtifman; Gritsenko, Vladimir; Levitan, Anton mBio, Vol. 9, Issue 5 https://doi.org/10.1128/mBio.02048-18	journal	October 2018
A genome-wide view of the spectrum of spontaneous mutations in yeast Lynch, M.; Sung, W.; Morris, K. Proceedings of the National Academy of Sciences, Vol. 105, Issue 27 https://doi.org/10.1073/pnas.0803466105	journal	June 2008
Evolution by gene loss Albalat, Ricard; Cañestro, Cristian Nature Reviews Genetics, Vol. 17, Issue 7 https://doi.org/10.1038/nrg.2016.39	journal	April 2016
From Sugar of Grape to Alcohol of Wine: Sensorial Impact of Alcohol in Wine Jordão, António; Vilela, Alice; Cosme, Fernanda Beverages, Vol. 1, Issue 4 https://doi.org/10.3390/beverages1040292	journal	November 2015

Similar Records

Cytogenetic damage and the radiation-induced G{sub 1}-phase checkpoint

Journal Article · Fri Mar 01 00:00:00 EST 1996 · Radiation Research · OSTI ID:1630352

Gupta, N; Haas-Kogan, D A; Israel, M A

Local chromatin structure of heterochromatin regulates repeated DNA stability, nucleolus structure, and genome integrity

Thesis/Dissertation · Mon Jan 01 00:00:00 EST 2007 · OSTI ID:1630352

Peng, Jamy C.

CCC1, putative human checkpoint gene, rescues the DNA damage-inducible G2 checkpoint in yeast

Journal Article · Thu Sep 01 00:00:00 EDT 1994 · American Journal of Human Genetics · OSTI ID:1630352

Plon, S E; Murrray, J C; Groudine, M

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (148)

Similar Records

Related Subjects