Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data

Panchy, Nicholas L.; Lloyd, John P.; Shiu, Shin-Han

doi:10.1186/s12864-020-6554-8

Title: Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data

Journal Article · Thu Feb 13 00:00:00 EST 2020 · BMC Genomics

DOI:https://doi.org/10.1186/s12864-020-6554-8· OSTI ID:1637519

Panchy, Nicholas L. ^[1]; Lloyd, John P. ^[2];

^[3]

Michigan State Univ., East Lansing, MI (United States); Univ. of Tennessee, Knoxville, TN (United States)
Univ. of Michigan, Ann Arbor, MI (United States)
Michigan State Univ., East Lansing, MI (United States)

Gene expression is regulated by DNA-binding transcription factors (TFs). Together with their target genes, these factors and their interactions collectively form a gene regulatory network (GRN), which is responsible for producing patterns of transcription, including cyclical processes such as genome replication and cell division. However, identifying how this network regulates the timing of these patterns, including important interactions and regulatory motifs, remains a challenging task.ResultsWe employed four in vivo and in vitro regulatory data sets to investigate the regulatory basis of expression timing and phase-specific patterns cell-cycle expression in Saccharomyces cerevisiae. Specifically, we considered interactions based on direct binding between TF and target gene, indirect effects of TF deletion on gene expression, and computational inference. We found that the source of regulatory information significantly impacts the accuracy and completeness of recovering known cell-cycle expressed genes. The best approach involved combining TF-target and TF-TF interactions features from multiple datasets in a single model. In addition, TFs important to multiple phases of cell-cycle expression also have the greatest impact on individual phases. Important TFs regulating a cell-cycle phase also tend to form modules in the GRN, including two sub-modules composed entirely of unannotated cell-cycle regulators (STE12-TEC1 and RAP1-HAP1-MSN4).ConclusionOur findings illustrate the importance of integrating both multiple omics data and regulatory motifs in order to understand the significance regulatory interactions involved in timing gene expression. This integrated approached allowed us to recover both known cell-cycles interactions and the overall pattern of phase-specific expression across the cell-cycle better than any single data set. Likewise, by looking at regulatory motifs in the form of TF-TF interactions, we identified sets of TFs whose co-regulation of target genes was important for cell-cycle expression, even when regulation by individual TFs was not. Overall, this demonstrates the power of integrating multiple data sets and models of interaction in order to understand the regulatory basis of established biological processes and their associated gene regulatory networks.

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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)

Grant/Contract Number:: SC0018409; IOS-1546617l; DEB-1655386

OSTI ID:: 1637519

Journal Information:: BMC Genomics, Vol. 21, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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References (79)

The RNA polymerase II core promoter — the gateway to transcription Juven-Gershon, Tamar; Hsu, Jer-Yuan; Theisen, Joshua WM Current Opinion in Cell Biology, Vol. 20, Issue 3 https://doi.org/10.1016/j.ceb.2008.03.003	journal	June 2008
Transcription factor binding predicts histone modifications in human cell lines Benveniste, Dan; Sonntag, Hans-Joachim; Sanguinetti, Guido Proceedings of the National Academy of Sciences, Vol. 111, Issue 37 https://doi.org/10.1073/pnas.1412081111	journal	September 2014
Driving the Cell Cycle Through Metabolism Cai, Ling; Tu, Benjamin P. Annual Review of Cell and Developmental Biology, Vol. 28, Issue 1 https://doi.org/10.1146/annurev-cellbio-092910-154010	journal	November 2012
Translational control of lipogenic enzymes in the cell cycle of synchronous, growing yeast cells Blank, Heidi M.; Perez, Ricardo; He, Chong The EMBO Journal, Vol. 36, Issue 4 https://doi.org/10.15252/embj.201695050	journal	December 2016
Widespread evidence of cooperative DNA binding by transcription factors in Drosophila development Kazemian, Majid; Pham, Hannah; Wolfe, Scot A. Nucleic Acids Research, Vol. 41, Issue 17 https://doi.org/10.1093/nar/gkt598	journal	July 2013
Cyclebase 3.0: a multi-organism database on cell-cycle regulation and phenotypes Santos, Alberto; Wernersson, Rasmus; Jensen, Lars Juhl Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1092	journal	November 2014
Identification of cell cycle–regulated genes periodically expressed in U2OS cells and their regulation by FOXM1 and E2F transcription factors Grant, Gavin D.; Brooks, Lionel; Zhang, Xiaoyang Molecular Biology of the Cell, Vol. 24, Issue 23 https://doi.org/10.1091/mbc.e13-05-0264	journal	December 2013
Quiescent Saccharomyces cerevisiae forms telomere hyperclusters at the nuclear membrane vicinity through a multifaceted mechanism involving Esc1, the Sir complex, and chromatin condensation Laporte, Damien; Courtout, Fabien; Tollis, Sylvain Molecular Biology of the Cell, Vol. 27, Issue 12 https://doi.org/10.1091/mbc.e16-01-0069	journal	June 2016
Disentangling the Many Layers of Eukaryotic Transcriptional Regulation Lelli, Katherine M.; Slattery, Matthew; Mann, Richard S. Annual Review of Genetics, Vol. 46, Issue 1 https://doi.org/10.1146/annurev-genet-110711-155437	journal	December 2012
HAP1 and ROX1 form a regulatory pathway in the repression of HEM13 transcription in Saccharomyces cerevisiae. Keng, T. Molecular and Cellular Biology, Vol. 12, Issue 6 https://doi.org/10.1128/MCB.12.6.2616	journal	June 1992
Predicting Gene Expression from Sequence: A Reexamination Yuan, Yuan; Guo, Lei; Shen, Lei PLoS Computational Biology, Vol. 3, Issue 11 https://doi.org/10.1371/journal.pcbi.0030243	journal	November 2007
RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: A negative feedback circuit Xie, Y.; Varshavsky, A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 6 https://doi.org/10.1073/pnas.071022298	journal	March 2001
ChIP-chip: considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments Buck, Michael J.; Lieb, Jason D. Genomics, Vol. 83, Issue 3 https://doi.org/10.1016/j.ygeno.2003.11.004	journal	March 2004
HAP1 and ROX1 form a regulatory pathway in the repression of HEM13 transcription in Saccharomyces cerevisiae Keng, T. Molecular and Cellular Biology, Vol. 12, Issue 6 https://doi.org/10.1128/mcb.12.6.2616-2623.1992	journal	June 1992
DNA-dependent formation of transcription factor pairs alters their binding specificity Jolma, Arttu; Yin, Yimeng; Nitta, Kazuhiro R. Nature, Vol. 527, Issue 7578 https://doi.org/10.1038/nature15518	journal	November 2015
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.08.063	journal	September 2016
ChIP–seq and beyond: new and improved methodologies to detect and characterize protein–DNA interactions S., Furey, Terrence The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/mp8k-zj63	text	January 2012
Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana Zou, C.; Sun, K.; Mackaluso, J. D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 36 https://doi.org/10.1073/pnas.1103202108	journal	August 2011
Transcriptional regulatory code of a eukaryotic genome Harbison, Christopher T.; Gordon, D. Benjamin; Lee, Tong Ihn Nature, Vol. 431, Issue 7004 https://doi.org/10.1038/nature02800	journal	September 2004
A microarray-assisted screen for potential Hap1 and Rox1 target genes inSaccharomyces cerevisiae Ter Linde, Jos� J. M.; Steensma, H. Yde Yeast, Vol. 19, Issue 10 https://doi.org/10.1002/yea.879	journal	January 2002
Network motifs: theory and experimental approaches Alon, Uri Nature Reviews Genetics, Vol. 8, Issue 6 https://doi.org/10.1038/nrg2102	journal	June 2007
Cell-Cycle Control of Gene Expression in Budding and Fission Yeast Bähler, Jürg Annual Review of Genetics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.genet.39.110304.095808	journal	December 2005
Spatial reorganization of telomeres in long-lived quiescent cells Guidi, Micol; Ruault, Myriam; Marbouty, Martial Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0766-2	journal	September 2015
Cell cycle-dependent transcription in yeast: promoters, transcription factors, and transcriptomes Wittenberg, Curt; Reed, Steven I. Oncogene, Vol. 24, Issue 17 https://doi.org/10.1038/sj.onc.1208606	journal	April 2005
Predicting expression patterns from regulatory sequence in Drosophila segmentation Segal, Eran; Raveh-Sadka, Tali; Schroeder, Mark Nature, Vol. 451, Issue 7178 https://doi.org/10.1038/nature06496	journal	January 2008
Rap1 relocalization contributes to the chromatin-mediated gene expression profile and pace of cell senescence Platt, J. M.; Ryvkin, P.; Wanat, J. J. Genes & Development, Vol. 27, Issue 12 https://doi.org/10.1101/gad.218776.113	journal	June 2013
High-resolution DNA-binding specificity analysis of yeast transcription factors Zhu, C.; Byers, K. J. R. P.; McCord, R. P. Genome Research, Vol. 19, Issue 4 https://doi.org/10.1101/gr.090233.108	journal	January 2009
Reconciling conflicting models for global control of cell-cycle transcription Cho, Chun-Yi; Motta, Francis C.; Kelliher, Christina M. Cell Cycle, Vol. 16, Issue 20 https://doi.org/10.1080/15384101.2017.1367073	journal	August 2017
Gene regulatory networks and the role of robustness and stochasticity in the control of gene expression MacNeil, L. T.; Walhout, A. J. M. Genome Research, Vol. 21, Issue 5 https://doi.org/10.1101/gr.097378.109	journal	February 2011
Feedback Loops of the Mammalian Circadian Clock Constitute Repressilator Pett, J. Patrick; Korenčič, Anja; Wesener, Felix PLOS Computational Biology, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pcbi.1005266	journal	December 2016
High Functional Overlap Between MluI Cell-Cycle Box Binding Factor and Swi4/6 Cell-Cycle Box Binding Factor in the G1/S Transcriptional Program in Saccharomyces cerevisiae Bean, James M.; Siggia, Eric D.; Cross, Frederick R. Genetics, Vol. 171, Issue 1 https://doi.org/10.1534/genetics.105.044560	journal	June 2005
Dynamic Regulation of Transcription Factors by Nucleosome Remodeling Li, Ming; Sen, Payel; Olufemi, Lola Biophysical Journal, Vol. 106, Issue 2 https://doi.org/10.1016/j.bpj.2013.11.498	journal	January 2014
Transcription factors: from enhancer binding to developmental control Spitz, François; Furlong, Eileen E. M. Nature Reviews Genetics, Vol. 13, Issue 9 https://doi.org/10.1038/nrg3207	journal	August 2012
YeTFaSCo: a database of evaluated yeast transcription factor sequence specificities de Boer, C. G.; Hughes, T. R. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr993	journal	November 2011
Systematic identification of yeast cell cycle transcription factors using multiple data sources Wu, Wei-Sheng; Li, Wen-Hsiung BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-522	journal	December 2008
Data mining in bioinformatics using Weka Frank, E.; Hall, M.; Trigg, L. Bioinformatics, Vol. 20, Issue 15 https://doi.org/10.1093/bioinformatics/bth261	journal	April 2004
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
Collaborative Competition Mechanism for Gene Activation In Vivo Miller, Joanna A.; Widom, Jonathan Molecular and Cellular Biology, Vol. 23, Issue 5 https://doi.org/10.1128/mcb.23.5.1623-1632.2003	journal	March 2003
Predicting Gene Expression from Sequence Beer, Michael A.; Tavazoie, Saeed Cell, Vol. 117, Issue 2 https://doi.org/10.1016/S0092-8674(04)00304-6	journal	April 2004
Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Schmitt, A. P.; McEntee, K. Proceedings of the National Academy of Sciences, Vol. 93, Issue 12 https://doi.org/10.1073/pnas.93.12.5777	journal	June 1996
Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors Berger, Michael F.; Bulyk, Martha L. Nature Protocols, Vol. 4, Issue 3 https://doi.org/10.1038/nprot.2008.195	journal	March 2009
Global Prediction of Tissue-Specific Gene Expression and Context-Dependent Gene Networks in Caenorhabditis elegans Chikina, Maria D.; Huttenhower, Curtis; Murphy, Coleen T. PLoS Computational Biology, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pcbi.1000417	journal	June 2009
Genomewide mechanisms of chronological longevity by dietary restriction in budding yeast Campos, Sergio E.; Avelar-Rivas, J. Abraham; Garay, Erika Aging Cell, Vol. 17, Issue 3 https://doi.org/10.1111/acel.12749	journal	March 2018
Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters Koranda, Manfred; Schleiffer, Alexander; Endler, Lukas Nature, Vol. 406, Issue 6791 https://doi.org/10.1038/35017589	journal	July 2000
Predictive Models of Spatial Transcriptional Response to High Salinity Uygun, Sahra; Seddon, Alexander E.; Azodi, Christina B. Plant Physiology, Vol. 174, Issue 1 https://doi.org/10.1104/pp.16.01828	journal	April 2017
Comprehensive Identification of Cell Cycle–regulated Genes of the Yeast Saccharomyces cerevisiae by Microarray Hybridization Spellman, Paul T.; Sherlock, Gavin; Zhang, Michael Q. Molecular Biology of the Cell, Vol. 9, Issue 12 https://doi.org/10.1091/mbc.9.12.3273	journal	December 1998
Control of cell cycle transcription during G1 and S phases Bertoli, Cosetta; Skotheim, Jan M.; de Bruin, Robertus A. M. Nature Reviews Molecular Cell Biology, Vol. 14, Issue 8 https://doi.org/10.1038/nrm3629	journal	July 2013
An Integrative Multi-Network and Multi-Classifier Approach to Predict Genetic Interactions Pandey, Gaurav; Zhang, Bin; Chang, Aaron N. PLoS Computational Biology, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pcbi.1000928	journal	September 2010
A Machine Learning Approach for Identifying Novel Cell Type–Specific Transcriptional Regulators of Myogenesis Busser, Brian W.; Taher, Leila; Kim, Yongsok PLoS Genetics, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pgen.1002531	journal	March 2012
The TEA Transcription Factor Tec1 Links TOR and MAPK Pathways to Coordinate Yeast Development Brückner, Stefan; Kern, Sandra; Birke, Raphael Genetics, Vol. 189, Issue 2 https://doi.org/10.1534/genetics.111.133629	journal	August 2011
Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth Zhu, Gefeng; Spellman, Paul T.; Volpe, Tom Nature, Vol. 406, Issue 6791 https://doi.org/10.1038/35017581	journal	July 2000
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang Cell, Vol. 165, Issue 5 https://doi.org/10.1016/j.cell.2016.04.038	journal	May 2016
Feedback Loops of the Mammalian Circadian Clock Constitute Repressilator Pett, J. Patrick; Korencic, Anja; Wesener, Felix Charité - Universitätsmedizin Berlin https://doi.org/10.17169/refubium-24578	text	January 2016
ChIP–seq and beyond: new and improved methodologies to detect and characterize protein–DNA interactions Furey, Terrence S. Nature Reviews Genetics, Vol. 13, Issue 12 https://doi.org/10.1038/nrg3306	journal	October 2012
Cell cycle regulation by feed‐forward loops coupling transcription and phosphorylation Csikász‐Nagy, Attila; Kapuy, Orsolya; Tóth, Attila Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2008.73	journal	January 2009
Cell cycle population effects in perturbation studies O'Duibhir, Eoghan; Lijnzaad, Philip; Benschop, Joris J. Molecular Systems Biology, Vol. 10, Issue 6 https://doi.org/10.15252/msb.20145172	journal	June 2014
Overcome Support Vector Machine Diagnosis Overfitting Han, Henry; Jiang, Xiaoqian Cancer Informatics, Vol. 13s1 https://doi.org/10.4137/cin.s13875	journal	January 2014
Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF Iyer, Vishwanath R.; Horak, Christine E.; Scafe, Charles S. Nature, Vol. 409, Issue 6819 https://doi.org/10.1038/35054095	journal	January 2001
The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). Martínez-Pastor, M. T.; Marchler, G.; Schüller, C. The EMBO Journal, Vol. 15, Issue 9 https://doi.org/10.1002/j.1460-2075.1996.tb00576.x	journal	May 1996
Gene regulatory networks and the role of robustness and stochasticity in the control of gene expression MacNeil, L. T.; Walhout, A. J. M. Genome Research https://doi.org/10.1101/gr.97378.109	journal	March 2011
Prevalence, Evolution, and cis -Regulation of Diel Transcription in Chlamydomonas reinhardtii Panchy, Nicholas; Wu, Guangxi; Newton, Linsey G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 12 https://doi.org/10.1534/g3.114.015032	journal	October 2014
Reconciling conflicting models for global control of cell-cycle transcription Cho, Chun-Yi; Motta, Francis C.; Kelliher, Christina M. Taylor & Francis https://doi.org/10.6084/m9.figshare.5431981	dataset	January 2017
Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast Mannhaupt, Gertrud; Schnall, Ralf; Karpov, Vadim FEBS Letters, Vol. 450, Issue 1-2 https://doi.org/10.1016/s0014-5793(99)00467-6	journal	April 1999
The Unfolded Protein Response Regulates Multiple Aspects of Secretory and Membrane Protein Biogenesis and Endoplasmic Reticulum Quality Control Ng, Davis T. W.; Spear, Eric D.; Walter, Peter Journal of Cell Biology, Vol. 150, Issue 1 https://doi.org/10.1083/jcb.150.1.77	journal	July 2000
Saccharomyces cerevisiae Genes Involved in Survival of Heat Shock Jarolim, Stefanie; Ayer, Anita; Pillay, Bethany G3: Genes\|Genomes\|Genetics, Vol. 3, Issue 12 https://doi.org/10.1534/g3.113.007971	journal	October 2013
Circular piecewise regression with applications to cell‐cycle data Rueda, Cristina; Fernández, Miguel A.; Barragán, Sandra Biometrics, Vol. 72, Issue 4 https://doi.org/10.1111/biom.12512	journal	March 2016
It's the Data! Botstein, David Molecular Biology of the Cell, Vol. 21, Issue 1 https://doi.org/10.1091/mbc.e09-07-0575	journal	January 2010
Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression Marion, R. M.; Regev, A.; Segal, E. Proceedings of the National Academy of Sciences, Vol. 101, Issue 40 https://doi.org/10.1073/pnas.0405353101	journal	September 2004
Periodic Transcription: A Cycle within a Cycle Breeden, Linda L. Current Biology, Vol. 13, Issue 1 https://doi.org/10.1016/s0960-9822(02)01386-6	journal	January 2003
DNA-dependent formation of transcription factor pairs alters their binding specificity Jolma, Arttu; Yin, Yimeng; Nitta, Kazuhiro R. Nature, Vol. 534, Issue 7607 https://doi.org/10.1038/nature18912	journal	June 2016
Dynamic regulation of transcription factors by nucleosome remodeling Li, Ming; Hada, Arjan; Sen, Payel eLife, Vol. 4 https://doi.org/10.7554/eLife.06249	journal	June 2015
Aca1 and Aca2, ATF/CREB Activators in Saccharomyces cerevisiae, Are Important for Carbon Source Utilization but Not the Response to Stress Garcia-Gimeno, M. Adelaida; Struhl, Kevin Molecular and Cellular Biology, Vol. 20, Issue 12 https://doi.org/10.1128/mcb.20.12.4340-4349.2000	journal	June 2000
A general approach to the isolation of cell cycle-regulated genes in the budding yeast, Saccharomyces cerevisiae Price, Clive; Nasmyth, Kim; Schuster, Tillman Journal of Molecular Biology, Vol. 218, Issue 3 https://doi.org/10.1016/0022-2836(91)90700-g	journal	April 1991
Transcriptional regulatory networks and the yeast cell cycle Futcher, Bruce Current Opinion in Cell Biology, Vol. 14, Issue 6 https://doi.org/10.1016/s0955-0674(02)00391-5	journal	December 2002
The Dynamics of Yeast Telomeres and Silencing Proteins through the Cell Cycle Laroche, Thierry; Martin, Sophie G.; Tsai-Pflugfelder, Monika Journal of Structural Biology, Vol. 129, Issue 2-3 https://doi.org/10.1006/jsbi.2000.4240	journal	April 2000
Comprehensive reanalysis of transcription factor knockout expression data in Saccharomyces cerevisiae reveals many new targets Reimand, Jüri; Vaquerizas, Juan M.; Todd, Annabel E. Nucleic Acids Research, Vol. 38, Issue 14 https://doi.org/10.1093/nar/gkq232	journal	April 2010
The Transcription Factors Tec1 and Ste12 Interact with Coregulators Msa1 and Msa2 To Activate Adhesion and Multicellular Development van der Felden, J.; Weisser, S.; Bruckner, S. Molecular and Cellular Biology, Vol. 34, Issue 12 https://doi.org/10.1128/mcb.01599-13	journal	April 2014
The WEKA data mining software: an update Hall, Mark; Frank, Eibe; Holmes, Geoffrey ACM SIGKDD Explorations Newsletter, Vol. 11, Issue 1 https://doi.org/10.1145/1656274.1656278	journal	November 2009
The SFP1 Gene Product of Saccharomyces cerevisiae Regulates G2/M Transitions During the Mitotic Cell Cycle and DNA-Damage Response Xu, Zhiheng; Norris, David Genetics, Vol. 150, Issue 4 https://doi.org/10.1093/genetics/150.4.1419	journal	December 1998

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Additional file 9 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853669.v1 The current record is supplemented by this dataset	dataset	January 2020
Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.c.4856523.v1 The current record is supplemented by this collection	collection	January 2020
Additional file 9 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853669 The current record is supplemented by this dataset	dataset	January 2020
Additional file 8 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853660 The current record is supplemented by this dataset	dataset	January 2020
Additional file 12 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853630.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 10 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853621.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 6 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853648 The current record is supplemented by this dataset	dataset	January 2020
Additional file 5 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853645 The current record is supplemented by this dataset	dataset	January 2020
Additional file 4 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853642 The current record is supplemented by this dataset	dataset	January 2020
Additional file 5 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853645.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 8 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853660.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 7 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853651.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 2 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853636.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 7 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853651 The current record is supplemented by this dataset	dataset	January 2020
Additional file 11 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853627.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 6 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853648.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 1 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853633.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 11 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853627 The current record is supplemented by this dataset	dataset	January 2020
Additional file 10 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853621 The current record is supplemented by this dataset	dataset	January 2020
Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.c.4856523 The current record is supplemented by this collection	collection	January 2020
Additional file 2 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853636 The current record is supplemented by this dataset	dataset	January 2020
Additional file 3 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853639 The current record is supplemented by this dataset	dataset	January 2020
Additional file 4 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853642.v1 The current record is supplemented by this dataset	dataset	January 2020
Additional file 1 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853633 The current record is supplemented by this dataset	dataset	January 2020
Additional file 12 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853630 The current record is supplemented by this dataset	dataset	January 2020
Additional file 3 of Improved recovery of cell-cycle gene expression in Saccharomyces cerevisiae from regulatory interactions in multiple omics data Panchy, Nicholas; Lloyd, John; Shiu, Shin-Han https://doi.org/10.6084/m9.figshare.11853639.v1 The current record is supplemented by this dataset	dataset	January 2020