Minor Isozymes Tailor Yeast Metabolism to Carbon Availability

Bradley, Patrick H.; Gibney, Patrick A.; Botstein, David; Troyanskaya, Olga G.; Rabinowitz, Joshua D.; McCue, ed., Lee Ann

doi:10.1128/mSystems.00170-18

Title: Minor Isozymes Tailor Yeast Metabolism to Carbon Availability

Journal Article · Tue Feb 26 00:00:00 UTC 2019 · mSystems

DOI: https://doi.org/10.1128/mSystems.00170-18 · OSTI ID:1496504

; Gibney, Patrick A.; Botstein, David; Troyanskaya, Olga G.; Rabinowitz, Joshua D.; McCue, ed., Lee Ann

ABSTRACT Isozymes are enzymes that differ in sequence but catalyze the same chemical reactions. Despite their apparent redundancy, isozymes are often retained over evolutionary time, suggesting that they contribute to fitness. We developed an unsupervised computational method for identifying environmental conditions under which isozymes are likely to make fitness contributions. This method analyzes published gene expression data to find specific experimental perturbations that induce differential isozyme expression. In yeast, we found that isozymes are strongly enriched in the pathways of central carbon metabolism and that many isozyme pairs show anticorrelated expression during the respirofermentative shift. Building on these observations, we assigned function to two minor central carbon isozymes, aconitase 2 ( ACO2 ) and pyruvate kinase 2 ( PYK2 ). ACO2 is expressed during fermentation and proves advantageous when glucose is limiting. PYK2 is expressed during respiration and proves advantageous for growth on three-carbon substrates. PYK2 ’s deletion can be rescued by expressing the major pyruvate kinase only if that enzyme carries mutations mirroring PYK2 ’s allosteric regulation. Thus, central carbon isozymes help to optimize allosteric metabolic regulation under a broad range of potential nutrient conditions while requiring only a small number of transcriptional states. IMPORTANCE Gene duplication is one of the main evolutionary paths to new protein function. Typically, duplicated genes either accumulate mutations and degrade into pseudogenes or are retained and diverge in function. Some duplicated genes, however, show long-term persistence without apparently acquiring new function. An important class of isozymes consists of those that catalyze the same reaction in the same compartment, where knockout of one isozyme causes no known functional defect. Here we present an approach to assigning specific functional roles to seemingly redundant isozymes. First, gene expression data are analyzed computationally to identify conditions under which isozyme expression diverges. Then, knockouts are compared under those conditions. This approach revealed that the expression of many yeast isozymes diverges in response to carbon availability and that carbon source manipulations can induce fitness phenotypes for seemingly redundant isozymes. A driver of these fitness phenotypes is differential allosteric enzyme regulation, indicating isozyme divergence to achieve more-optimal control of metabolism.

View Journal Article

Cite

Export

Save

Research Organization:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0002077; SC0018420

OSTI ID:: 1496504

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 1 Vol. 4; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (93)

Kinetic and Allosteric Consequences of Mutations in the Subunit and Domain Interfaces and the Allosteric Site of Yeast Pyruvate Kinase Fenton, Aron W.; Blair, James B. Archives of Biochemistry and Biophysics, Vol. 397, Issue 1 https://doi.org/10.1006/abbi.2001.2634	journal	January 2002
Regulation of Pyruvate Kinase M Gene Expression Yamada, Kazuya; Noguchi, Tamio Biochemical and Biophysical Research Communications, Vol. 256, Issue 2 https://doi.org/10.1006/bbrc.1999.0228	journal	March 1999
The allosteric regulation of pyruvate kinase Mattevi, Andrea; Bolognesi, Martino; Valentini, Giovanna FEBS Letters, Vol. 389, Issue 1 https://doi.org/10.1016/0014-5793(96)00462-0	journal	June 1996
Gene Knockouts, in vivo Site-Directed Mutagenesis and Other Modifications Using the Delitto Perfetto System in Saccharomyces cerevisiae Stuckey, Samantha; Storici, Francesca Laboratory Methods in Enzymology: Cell, Lipid and Carbohydrate https://doi.org/10.1016/B978-0-12-420067-8.00008-8	book	January 2013
Targeted deletion of a yeast enolase structural gene. Identification and isolation of yeast enolase isozymes. McAlister, L.; Holland, M. J. Journal of Biological Chemistry, Vol. 257, Issue 12 https://doi.org/10.1016/S0021-9258(18)34554-X	journal	June 1982
Origin of the duplicated regions in the yeast genomes Piškur, Jure Trends in Genetics, Vol. 17, Issue 6 https://doi.org/10.1016/S0168-9525(01)02308-3	journal	June 2001
Yeast genome evolution in the post-genome era Seoighe, Cathal; Wolfe, Kenneth H. Current Opinion in Microbiology, Vol. 2, Issue 5 https://doi.org/10.1016/S1369-5274(99)00015-6	journal	October 1999
Riboneogenesis in Yeast Clasquin, Michelle F.; Melamud, Eugene; Singer, Alexander Cell, Vol. 145, Issue 6 https://doi.org/10.1016/j.cell.2011.05.022	journal	June 2011
Separation and quantitation of water soluble cellular metabolites by hydrophilic interaction chromatography-tandem mass spectrometry Bajad, Sunil U.; Lu, Wenyun; Kimball, Elizabeth H. Journal of Chromatography A, Vol. 1125, Issue 1, p. 76-88 https://doi.org/10.1016/j.chroma.2006.05.019	journal	August 2006
Pyruvate Kinase Triggers a Metabolic Feedback Loop that Controls Redox Metabolism in Respiring Cells Grüning, Nana-Maria; Rinnerthaler, Mark; Bluemlein, Katharina Cell Metabolism, Vol. 14, Issue 3 https://doi.org/10.1016/j.cmet.2011.06.017	journal	September 2011
Analytical strategies for LC–MS-based targeted metabolomics Lu, Wenyun; Bennett, Bryson D.; Rabinowitz, Joshua D. Journal of Chromatography B, Vol. 871, Issue 2 https://doi.org/10.1016/j.jchromb.2008.04.031	journal	August 2008
Regulation of Yeast Pyruvate Kinase by Ultrasensitive Allostery Independent of Phosphorylation Xu, Yi-Fan; Zhao, Xin; Glass, David S. Molecular Cell, Vol. 48, Issue 1 https://doi.org/10.1016/j.molcel.2012.07.013	journal	October 2012
Rocking cell metabolism: revised functions of the key glycolytic regulator PKM2 in cancer Chaneton, Barbara; Gottlieb, Eyal Trends in Biochemical Sciences, Vol. 37, Issue 8 https://doi.org/10.1016/j.tibs.2012.04.003	journal	August 2012
Introduction to Information Retrieval Manning, Christopher D.; Raghavan, Prabhakar; Schutze, Hinrich https://doi.org/10.1017/CBO9780511809071	book	January 2008
Metabolomic Analysis via Reversed-Phase Ion-Pairing Liquid Chromatography Coupled to a Stand Alone Orbitrap Mass Spectrometer Lu, Wenyun; Clasquin, Michelle F.; Melamud, Eugene Analytical Chemistry, Vol. 82, Issue 8 https://doi.org/10.1021/ac902837x	journal	April 2010
The control of pyruvate kinase of Escherichia coli. Binding of substrate and allosteric effectors to the enzyme activated by fructose 1,6-bisphosphate Waygood, E. Bruce; Mort, John S.; Sanwal, B. D. Biochemistry, Vol. 15, Issue 2 https://doi.org/10.1021/bi00647a006	journal	January 1976
Systematic determination of genetic network architecture Tavazoie, Saeed; Hughes, Jason D.; Campbell, Michael J. Nature Genetics, Vol. 22, Issue 3 https://doi.org/10.1038/10343	journal	July 1999
Evolution of genetic redundancy Nowak, Martin A.; Boerlijst, Maarten C.; Cooke, Jonathan Nature, Vol. 388, Issue 6638 https://doi.org/10.1038/40618	journal	July 1997
Molecular evidence for an ancient duplication of the entire yeast genome Wolfe, Kenneth H.; Shields, Denis C. Nature, Vol. 387, Issue 6634 https://doi.org/10.1038/42711	journal	June 1997
Backup without redundancy: genetic interactions reveal the cost of duplicate gene loss Ihmels, Jan; Collins, Sean R.; Schuldiner, Maya Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100127	journal	January 2007
Increased glycolytic flux as an outcome of whole‐genome duplication in yeast Conant, Gavin C.; Wolfe, Kenneth H. Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100170	journal	January 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
Global analysis of protein localization in budding yeast Huh, Won-Ki; Falvo, James V.; Gerke, Luke C. Nature, Vol. 425, Issue 6959 https://doi.org/10.1038/nature02026	journal	October 2003
Metabolic network analysis of the causes and evolution of enzyme dispensability in yeast Papp, Balázs; Pál, Csaba; Hurst, Laurence D. Nature, Vol. 429, Issue 6992 https://doi.org/10.1038/nature02636	journal	June 2004
Proteome survey reveals modularity of the yeast cell machinery Gavin, Anne-Claude; Aloy, Patrick; Grandi, Paola Nature, Vol. 440, Issue 7084 https://doi.org/10.1038/nature04532	journal	January 2006
Gene duplication and the adaptive evolution of a classic genetic switch Hittinger, Chris Todd; Carroll, Sean B. Nature, Vol. 449, Issue 7163 https://doi.org/10.1038/nature06151	journal	October 2007
Escape from adaptive conflict after duplication in an anthocyanin pathway gene Des Marais, David L.; Rausher, Mark D. Nature, Vol. 454, Issue 7205 https://doi.org/10.1038/nature07092	journal	June 2008
Principles of transcriptional control in the metabolic network of Saccharomyces cerevisiae Ihmels, Jan; Levy, Ronen; Barkai, Naama Nature Biotechnology, Vol. 22, Issue 1 https://doi.org/10.1038/nbt918	journal	November 2003
Ultrasensitive regulation of anapleurosis via allosteric activation of PEP carboxylase Xu, Yi-Fan; Amador-Noguez, Daniel; Reaves, Marshall Louis Nature Chemical Biology, Vol. 8, Issue 6 https://doi.org/10.1038/nchembio.941	journal	April 2012
Exposing the fitness contribution of duplicated genes DeLuna, Alexander; Vetsigian, Kalin; Shoresh, Noam Nature Genetics, Vol. 40, Issue 5 https://doi.org/10.1038/ng.123	journal	April 2008
An integrated approach to characterize genetic interaction networks in yeast metabolism Szappanos, Balázs; Kovács, Károly; Szamecz, Béla Nature Genetics, Vol. 43, Issue 7 https://doi.org/10.1038/ng.846	journal	May 2011
Modular epistasis in yeast metabolism Segrè, Daniel; DeLuna, Alexander; Church, George M. Nature Genetics, Vol. 37, Issue 1 https://doi.org/10.1038/ng1489	journal	December 2004
Transcription control reprogramming in genetic backup circuits Kafri, Ran; Bar-Even, Arren; Pilpel, Yitzhak Nature Genetics, Vol. 37, Issue 3 https://doi.org/10.1038/ng1523	journal	February 2005
Multiple knockout analysis of genetic robustness in the yeast metabolic network Deutscher, David; Meilijson, Isaac; Kupiec, Martin Nature Genetics, Vol. 38, Issue 9 https://doi.org/10.1038/ng1856	journal	August 2006
Systematic screen for human disease genes in yeast Steinmetz, Lars M.; Scharfe, Curt; Deutschbauer, Adam M. Nature Genetics, Vol. 31, Issue 4 https://doi.org/10.1038/ng929	journal	July 2002
A comprehensive strategy enabling high-resolution functional analysis of the yeast genome Breslow, David K.; Cameron, Dale M.; Collins, Sean R. Nature Methods, Vol. 5, Issue 8 https://doi.org/10.1038/nmeth.1234	journal	July 2008
The metabolic background is a global player in Saccharomyces gene expression epistasis Alam, Mohammad Tauqeer; Zelezniak, Aleksej; Mülleder, Michael Nature Microbiology, Vol. 1, Issue 3 https://doi.org/10.1038/nmicrobiol.2015.30	journal	February 2016
Turning a hobby into a job: How duplicated genes find new functions Conant, Gavin C.; Wolfe, Kenneth H. Nature Reviews Genetics, Vol. 9, Issue 12 https://doi.org/10.1038/nrg2482	journal	December 2008
The regulatory utilization of genetic redundancy through responsive backup circuits Kafri, R.; Levy, M.; Pilpel, Y. Proceedings of the National Academy of Sciences, Vol. 103, Issue 31 https://doi.org/10.1073/pnas.0604883103	journal	July 2006
Yeast metabolic and signaling genes are required for heat-shock survival and have little overlap with the heat-induced genes Gibney, P. A.; Lu, C.; Caudy, A. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 46 https://doi.org/10.1073/pnas.1318100110	journal	October 2013
Statistical significance for genomewide studies Storey, J. D.; Tibshirani, R. Proceedings of the National Academy of Sciences, Vol. 100, Issue 16, p. 9440-9445 https://doi.org/10.1073/pnas.1530509100	journal	July 2003
Dihydroxyacetone Kinases in Saccharomyces cerevisiae Are Involved in Detoxification of Dihydroxyacetone Molin, Mikael; Norbeck, Joakim; Blomberg, Anders Journal of Biological Chemistry, Vol. 278, Issue 3 https://doi.org/10.1074/jbc.M203030200	journal	October 2002
Genomic Expression Programs in the Response of Yeast Cells to Environmental Changes Gasch, Audrey P.; Spellman, Paul T.; Kao, Camilla M. Molecular Biology of the Cell, Vol. 11, Issue 12 https://doi.org/10.1091/mbc.11.12.4241	journal	December 2000
Coordinated regulation of sulfur and phospholipid metabolism reflects the importance of methylation in the growth of yeast Hickman, Mark J.; Petti, Allegra A.; Ho-Shing, Olivia Molecular Biology of the Cell, Vol. 22, Issue 21 https://doi.org/10.1091/mbc.E11-05-0467	journal	November 2011
Homeostatic Adjustment and Metabolic Remodeling in Glucose-limited Yeast Cultures Brauer, Matthew J.; Saldanha, Alok J.; Dolinski, Kara Molecular Biology of the Cell, Vol. 16, Issue 5 https://doi.org/10.1091/mbc.e04-11-0968	journal	May 2005
Coordination of Growth Rate, Cell Cycle, Stress Response, and Metabolic Activity in Yeast Brauer, Matthew J.; Huttenhower, Curtis; Airoldi, Edoardo M. Molecular Biology of the Cell, Vol. 19, Issue 1 https://doi.org/10.1091/mbc.e07-08-0779	journal	January 2008
Growth-limiting Intracellular Metabolites in Yeast Growing under Diverse Nutrient Limitations Boer, Viktor M.; Crutchfield, Christopher A.; Bradley, Patrick H. Molecular Biology of the Cell, Vol. 21, Issue 1 https://doi.org/10.1091/mbc.e09-07-0597	journal	January 2010
Missing value estimation methods for DNA microarrays Troyanskaya, O.; Cantor, M.; Sherlock, G. Bioinformatics, Vol. 17, Issue 6 https://doi.org/10.1093/bioinformatics/17.6.520	journal	June 2001
Genome-wide discovery of transcriptional modules from DNA sequence and gene expression Segal, E.; Yelensky, R.; Koller, D. Bioinformatics, Vol. 19, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/btg1038	journal	July 2003
Defining transcription modules using large-scale gene expression data Ihmels, J.; Bergmann, S.; Barkai, N. Bioinformatics, Vol. 20, Issue 13 https://doi.org/10.1093/bioinformatics/bth166	journal	March 2004
A scalable method for integration and functional analysis of multiple microarray datasets Huttenhower, C.; Hibbs, M.; Myers, C. Bioinformatics, Vol. 22, Issue 23 https://doi.org/10.1093/bioinformatics/btl492	journal	September 2006
Exploring the functional landscape of gene expression: directed search of large microarray compendia Hibbs, M. A.; Hess, D. C.; Myers, C. L. Bioinformatics, Vol. 23, Issue 20 https://doi.org/10.1093/bioinformatics/btm403	journal	August 2007
Cross-hybridization modeling on Affymetrix exon arrays Kapur, Karen; Jiang, Hui; Xing, Yi Bioinformatics, Vol. 24, Issue 24 https://doi.org/10.1093/bioinformatics/btn571	journal	November 2008
ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking Wilkerson, Matthew D.; Hayes, D. Neil Bioinformatics, Vol. 26, Issue 12 https://doi.org/10.1093/bioinformatics/btq170	journal	April 2010
Correlated Asymmetry of Sequence and Functional Divergence Between Duplicate Proteins of Saccharomyces cerevisiae Kim, Seong-Ho; Yi, Soojin V. Molecular Biology and Evolution, Vol. 23, Issue 5 https://doi.org/10.1093/molbev/msj115	journal	March 2006
Functional Divergence for Every Paralog Soria, Patricia S.; McGary, Kriston L.; Rokas, Antonis Molecular Biology and Evolution, Vol. 31, Issue 4 https://doi.org/10.1093/molbev/msu050	journal	January 2014
SGD: Saccharomyces Genome Database Cherry, J. Nucleic Acids Research, Vol. 26, Issue 1 https://doi.org/10.1093/nar/26.1.73	journal	January 1998
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Edgar, R. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.207	journal	January 2002
The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases Caspi, R.; Foerster, H.; Fulcher, C. A. Nucleic Acids Research, Vol. 36, Issue Database https://doi.org/10.1093/nar/gkm900	journal	December 2007
Genetic robustness and functional evolution of gene duplicates Plata, Germán; Vitkup, Dennis Nucleic Acids Research, Vol. 42, Issue 4 https://doi.org/10.1093/nar/gkt1200	journal	November 2013
Pyruvate kinase (Pyk1) levels influence both the rate and direction of carbon flux in yeast under fermentative conditions Crimmins, Kay; Francois, Jean; Booth, Ian R. Microbiology, Vol. 147, Issue 2 https://doi.org/10.1099/00221287-147-2-391	journal	February 2001
Correlation between transcript profiles and fitness of deletion mutants in anaerobic chemostat cultures of Saccharomyces cerevisiae Tai, S. L.; Snoek, I.; Luttik, M. A. H. Microbiology, Vol. 153, Issue 3 https://doi.org/10.1099/mic.0.2006/002873-0	journal	March 2007
Yeast cells can access distinct quiescent states Klosinska, M. M.; Crutchfield, C. A.; Bradley, P. H. Genes & Development, Vol. 25, Issue 4 https://doi.org/10.1101/gad.2011311	journal	February 2011
Metabolic functions of duplicate genes in Saccharomyces cerevisiae Kuepfer, L. Genome Research, Vol. 15, Issue 10 https://doi.org/10.1101/gr.3992505	journal	September 2005
Iterative signature algorithm for the analysis of large-scale gene expression data Bergmann, Sven; Ihmels, Jan; Barkai, Naama Physical Review E, Vol. 67, Issue 3 https://doi.org/10.1103/PhysRevE.67.031902	journal	March 2003
Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response Marks, Virginia D.; Ho Sui, Shannan J.; Erasmus, Daniel FEMS Yeast Research, Vol. 8, Issue 1 https://doi.org/10.1111/j.1567-1364.2007.00338.x	journal	February 2008
The molecular genetics of hexose transport in yeasts Boles, Eckhard; Hollenberg, Cornelis P. FEMS Microbiology Reviews, Vol. 21, Issue 1 https://doi.org/10.1111/j.1574-6976.1997.tb00346.x	journal	August 1997
Fermentative lifestyle in yeasts belonging to the Saccharomyces complex : Fermentative lifestyle in yeasts Merico, Annamaria; Sulo, Pavol; Piškur, Jure The FEBS Journal, Vol. 274, Issue 4 https://doi.org/10.1111/j.1742-4658.2007.05645.x	journal	January 2007
Genetic Dissection of Transcriptional Regulation in Budding Yeast Brem, R. B. Science, Vol. 296, Issue 5568 https://doi.org/10.1126/science.1069516	journal	March 2002
The Chemical Genomic Portrait of Yeast: Uncovering a Phenotype for All Genes Hillenmeyer, M. E.; Fung, E.; Wildenhain, J. Science, Vol. 320, Issue 5874 https://doi.org/10.1126/science.1150021	journal	April 2008
Exploring the Metabolic and Genetic Control of Gene Expression on a Genomic Scale DeRisi, J. L.; Iyer, Vishwanath R.; Brown, Patrick O. Science, Vol. 278, Issue 5338, p. 680-686 https://doi.org/10.1126/science.278.5338.680	journal	October 1997
A global genetic interaction network maps a wiring diagram of cellular function Costanzo, M.; VanderSluis, B.; Koch, E. N. Science, Vol. 353, Issue 6306 https://doi.org/10.1126/science.aaf1420	journal	September 2016
Systematic analysis of complex genetic interactions Kuzmin, Elena; VanderSluis, Benjamin; Wang, Wen Science, Vol. 360, Issue 6386 https://doi.org/10.1126/science.aao1729	journal	April 2018
The Ehrlich Pathway for Fusel Alcohol Production: a Century of Research on Saccharomyces cerevisiae Metabolism Hazelwood, L. A.; Daran, J. -M.; van Maris, A. J. A. Applied and Environmental Microbiology, Vol. 74, Issue 8 https://doi.org/10.1128/AEM.02625-07	journal	February 2008
Two Distinct Pathways for Trehalose Assimilation in the Yeast Saccharomyces cerevisiae Jules, M.; Guillou, V.; Francois, J. Applied and Environmental Microbiology, Vol. 70, Issue 5 https://doi.org/10.1128/AEM.70.5.2771-2778.2004	journal	May 2004
Genetic Analysis and Functional Characterization of the Streptococcus pneumoniae vic Operon Wagner, C.; Saizieu, A. d.; Schonfeld, H. -J. Infection and Immunity, Vol. 70, Issue 11 https://doi.org/10.1128/IAI.70.11.6121-6128.2002	journal	November 2002
Identification and Characterization ofMAE1, the Saccharomyces cerevisiae Structural Gene Encoding Mitochondrial Malic Enzyme Boles, Eckhard; de Jong-Gubbels, Patricia; Pronk, Jack T. Journal of Bacteriology, Vol. 180, Issue 11 https://doi.org/10.1128/JB.180.11.2875-2882.1998	journal	June 1998
Heme Levels Switch the Function of Hap1 of Saccharomyces cerevisiae between Transcriptional Activator and Transcriptional Repressor Hickman, M. J.; Winston, F. Molecular and Cellular Biology, Vol. 27, Issue 21 https://doi.org/10.1128/MCB.00887-07	journal	September 2007
Characterization of a glucose-repressed pyruvate kinase (Pyk2p) in Saccharomyces cerevisiae that is catalytically insensitive to fructose-1,6-bisphosphate. Boles, E.; Schulte, F.; Miosga, T. Journal of Bacteriology, Vol. 179, Issue 9 https://doi.org/10.1128/jb.179.9.2987-2993.1997	journal	May 1997
Expression variability of co-regulated genes differentiates Saccharomyces cerevisiae strains Carreto, Laura; Eiriz, Maria F.; Domingues, Inês BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-201	journal	April 2011
Re-evaluation of glycerol utilization in Saccharomyces cerevisiae: characterization of an isolate that grows on glycerol without supporting supplements Swinnen, Steve; Klein, Mathias; Carrillo, Martina Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-157	journal	January 2013
Broad metabolic sensitivity profiling of a prototrophic yeast deletion collection VanderSluis, Benjamin; Hess, David C.; Pesyna, Colin Genome Biology, Vol. 15, Issue 4 https://doi.org/10.1186/gb-2014-15-4-r64	journal	January 2014
Increased rates of protein evolution and asymmetric deceleration after the whole-genome duplication in yeasts Ascencio, Diana; Ochoa, Soledad; Delaye, Luis BMC Evolutionary Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12862-017-0895-1	journal	February 2017
MADS: A new and improved method for analysis of differential alternative splicing by exon-tiling microarrays Xing, Y.; Stoilov, P.; Kapur, K. RNA, Vol. 14, Issue 8 https://doi.org/10.1261/rna.1070208	journal	June 2008
Specific roles for the Ccr4-Not complex subunits in expression of the genome Azzouz, N.; Panasenko, O. O.; Deluen, C. RNA, Vol. 15, Issue 3 https://doi.org/10.1261/rna.1348209	journal	January 2009
Need-Based Up-Regulation of Protein Levels in Response to Deletion of Their Duplicate Genes DeLuna, Alexander; Springer, Michael; Kirschner, Marc W. PLoS Biology, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pbio.1000347	journal	March 2010
Coordinated Concentration Changes of Transcripts and Metabolites in Saccharomyces cerevisiae Bradley, Patrick H.; Brauer, Matthew J.; Rabinowitz, Joshua D. PLoS Computational Biology, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pcbi.1000270	journal	January 2009
Systematic Planning of Genome-Scale Experiments in Poorly Studied Species Guan, Yuanfang; Dunham, Maitreya; Caudy, Amy PLoS Computational Biology, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pcbi.1000698	journal	March 2010
Mechanisms of Cell Cycle Control Revealed by a Systematic and Quantitative Overexpression Screen in S. cerevisiae Niu, Wei; Li, Zhihua; Zhan, Wenjing PLoS Genetics, Vol. 4, Issue 7 https://doi.org/10.1371/journal.pgen.1000120	journal	July 2008
Bulk Segregant Analysis by High-Throughput Sequencing Reveals a Novel Xylose Utilization Gene from Saccharomyces cerevisiae Wenger, Jared W.; Schwartz, Katja; Sherlock, Gavin PLoS Genetics, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pgen.1000942	journal	May 2010
Profiling of Cytosolic and Peroxisomal Acetyl-CoA Metabolism in Saccharomyces cerevisiae Chen, Yun; Siewers, Verena; Nielsen, Jens PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0042475	journal	August 2012
Upon Accounting for the Impact of Isoenzyme Loss, Gene Deletion Costs Anticorrelate with Their Evolutionary Rates Jacobs, Christopher; Lambourne, Luke; Xia, Yu PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0170164	journal	January 2017
A New System for Comparative Functional Genomics of Saccharomyces Yeasts Caudy, Amy A.; Guan, Yuanfang; Jia, Yue Genetics, Vol. 195, Issue 1 https://doi.org/10.1534/genetics.113.152918	journal	July 2013

Similar Records

Evolutionary Divergence of Duplicated Hsf Genes in Populus

Journal Article · Fri May 10 00:00:00 UTC 2019 · Cells · OSTI ID:1513366

Liu, Bobin; Hu, Jianjun; Zhang, Jin

A web-based tool for the prediction of rice transcription factor function

Journal Article · Thu Jun 06 00:00:00 UTC 2019 · Database · OSTI ID:2469652

Chandran, Anil Nalini; Moon, Sunok; Yoo, Yo-Han; +6 more

Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization

Journal Article · Mon Sep 26 04:00:00 UTC 2022 · Plant Physiology (Bethesda) · OSTI ID:2422507

Noble, Jennifer A.; Bielski, Nicholas V.; Liu, Ming-Che James; +13 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
cerevisiae
duplicates
genomics
isozymes
metabolomics
paralogs
systems biology
transcriptomics
yeast

Title: Minor Isozymes Tailor Yeast Metabolism to Carbon Availability

Citation Formats

References (93)

Similar Records

Related Subjects