Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica

Pomraning, Kyle R.; Kim, Young-Mo; Nicora, Carrie D.; Chu, Rosalie K.; Bredeweg, Erin L.; Purvine, Samuel O.; Hu, Dehong; Metz, Thomas O.; Baker, Scott E.

doi:10.1186/s12864-016-2471-2

Title: Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica

Journal Article · Thu Feb 25 00:00:00 EST 2016 · BMC Genomics

DOI:https://doi.org/10.1186/s12864-016-2471-2· OSTI ID:1618542

Pomraning, Kyle R.; Kim, Young-Mo; Nicora, Carrie D.; Chu, Rosalie K.; Bredeweg, Erin L.; Purvine, Samuel O.; Hu, Dehong; Metz, Thomas O.; Baker, Scott E.

Yarrowia lipolytica is an oleaginous ascomycete yeast that stores lipids in response to limitation of nitrogen. Furthermore, while the enzymatic pathways responsible for neutral lipid accumulation in Y. lipolytica are well characterized, regulation of these pathways has received little attention. We therefore sought to characterize the response to nitrogen limitation at system-wide levels, including the proteome, phosphoproteome and metabolome, to better understand how this organism regulates and controls lipid metabolism and to identify targets that may be manipulated to improve lipid yield.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

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

Grant/Contract Number:: SC0008744; AC05-76RL01830

OSTI ID:: 1618542

Alternate ID(s):: OSTI ID: 1249359

Report Number(s):: PNNL-SA-112784; 138; PII: 2471

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Vol. 17 Journal Issue: 1; ISSN 1471-2164

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 55 works

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References (85)

B lineage--specific interactions of an immunoglobulin enhancer with cellular factors in vivo Ephrussi, A.; Church, G.; Tonegawa, S. Science, Vol. 227, Issue 4683 https://doi.org/10.1126/science.3917574	journal	January 1985
3-Amino-2-piperidone in the urine of patients with hyperornithinemia Oberholzer, Victor G.; Briddon, Anthony Clinica Chimica Acta, Vol. 87, Issue 3 https://doi.org/10.1016/0009-8981(78)90186-9	journal	August 1978
Yarrowia lipolytica: A model and a tool to understand the mechanisms implicated in lipid accumulation Beopoulos, Athanasios; Chardot, Thierry; Nicaud, Jean-Marc Biochimie, Vol. 91, Issue 6 https://doi.org/10.1016/j.biochi.2009.02.004	journal	June 2009
Magnetic Bead Processor for Rapid Evaluation and Optimization of Parameters for Phosphopeptide Enrichment Ficarro, Scott B.; Adelmant, Guillaume; Tomar, Maria N. Analytical Chemistry, Vol. 81, Issue 11 https://doi.org/10.1021/ac9004452	journal	June 2009
The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. Kudla, B.; Caddick, M. X.; Langdon, T. The EMBO Journal, Vol. 9, Issue 5 https://doi.org/10.1002/j.1460-2075.1990.tb08250.x	journal	May 1990
Glutamate synthase levels in Neurospora crassa mutants altered with respect to nitrogen metabolism. Dunn-Coleman, N. S.; Robey, E. A.; Tomsett, A. B. Molecular and Cellular Biology, Vol. 1, Issue 2 https://doi.org/10.1128/MCB.1.2.158	journal	February 1981
Stb3 Binds to Ribosomal RNA Processing Element Motifs That Control Transcriptional Responses to Growth in Saccharomyces cerevisiae Liko, Dritan; Slattery, Matthew G.; Heideman, Warren Journal of Biological Chemistry, Vol. 282, Issue 36 https://doi.org/10.1074/jbc.M704762200	journal	July 2007
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
Data, information, knowledge and principle: back to metabolism in KEGG Kanehisa, Minoru; Goto, Susumu; Sato, Yoko Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1076	journal	November 2013
Two different, adjacent and divergent zinc finger binding sites are necessary for CREA-mediated carbon catabolite repression in the proline gene cluster of Aspergillus nidulans. Cubero, B.; Scazzocchio, C. The EMBO Journal, Vol. 13, Issue 2 https://doi.org/10.1002/j.1460-2075.1994.tb06275.x	journal	January 1994
Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation Swaney, Danielle L.; Beltrao, Pedro; Starita, Lea Nature Methods, Vol. 10, Issue 7 https://doi.org/10.1038/nmeth.2519	journal	June 2013
Improving Production of Malonyl Coenzyme A-Derived Metabolites by Abolishing Snf1-Dependent Regulation of Acc1 Shi, Shuobo; Chen, Yun; Siewers, Verena mBio, Vol. 5, Issue 3 https://doi.org/10.1128/mBio.01130-14	journal	May 2014
Lipid particle composition of the yeast Yarrowia lipolytica depends on the carbon source Athenstaedt, Karin; Jolivet, Pascale; Boulard, Céline PROTEOMICS, Vol. 6, Issue 5, p. 1450-1459 https://doi.org/10.1002/pmic.200500339	journal	March 2006
The PhosphoGRID Saccharomyces cerevisiae protein phosphorylation site database: version 2.0 update Sadowski, I.; Breitkreutz, B. -J.; Stark, C. Database, Vol. 2013, Issue 0 https://doi.org/10.1093/database/bat026	journal	January 2013
Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Oliphant, A. R.; Brandl, C. J.; Struhl, K. Molecular and Cellular Biology, Vol. 9, Issue 7 https://doi.org/10.1128/MCB.9.7.2944	journal	July 1989
DtaRefinery, a Software Tool for Elimination of Systematic Errors from Parent Ion Mass Measurements in Tandem Mass Spectra Data Sets Petyuk, Vladislav A.; Mayampurath, Anoop M.; Monroe, Matthew E. Molecular & Cellular Proteomics, Vol. 9, Issue 3 https://doi.org/10.1074/mcp.M900217-MCP200	journal	December 2009
Saccharomyces cerevisiae Yak1p protein kinase autophosphorylates on tyrosine residues and phosphorylates myelin basic protein on a C-terminal serine residue Kassis, Shouki; Melhuish, Tiffany; Annan, Roland S. Biochemical Journal, Vol. 348, Issue 2 https://doi.org/10.1042/bj3480263	journal	May 2000
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801 https://doi.org/10.1021/ac061133r	journal	November 2006
Structural basis for the inhibition of the eukaryotic ribosome Garreau de Loubresse, Nicolas; Prokhorova, Irina; Holtkamp, Wolf Nature, Vol. 513, Issue 7519 https://doi.org/10.1038/nature13737	journal	September 2014
How Saccharomyces Responds to Nutrients Zaman, Shadia; Lippman, Soyeon Im; Zhao, Xin Annual Review of Genetics, Vol. 42, Issue 1 https://doi.org/10.1146/annurev.genet.41.110306.130206	journal	December 2008
UniPROBE: an online database of protein binding microarray data on protein-DNA interactions Newburger, D. E.; Bulyk, M. L. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn660	journal	January 2009
Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter-specific recognition by the Aspergillus nidulans GATA factor AreA Ravagnani, Adriana; Gorfinkiel, Lisette; Langdon, Timothy The EMBO Journal, Vol. 16, Issue 13 https://doi.org/10.1093/emboj/16.13.3974	journal	July 1997
Engineering lipid overproduction in the oleaginous yeast Yarrowia lipolytica Qiao, Kangjian; Imam Abidi, Syed Hussain; Liu, Hongjuan Metabolic Engineering, Vol. 29, p. 56-65 https://doi.org/10.1016/j.ymben.2015.02.005	journal	May 2015
Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi Lavoie, Hugo; Hogues, Hervé; Whiteway, Malcolm Current Opinion in Microbiology, Vol. 12, Issue 6 https://doi.org/10.1016/j.mib.2009.09.015	journal	December 2009
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Recognition of nitrogen-responsive upstream activation sequences of Saccharomyces cerevisiae by the product of the GLN3 gene. Blinder, D.; Magasanik, B. Journal of Bacteriology, Vol. 177, Issue 14 https://doi.org/10.1128/JB.177.14.4190-4193.1995	journal	July 1995
Glycogen Synthase Kinase-3 (GSK3): Inflammation, Diseases, and Therapeutics Jope, Richard S.; Yuskaitis, Christopher J.; Beurel, Eléonore Neurochemical Research, Vol. 32, Issue 4-5 https://doi.org/10.1007/s11064-006-9128-5	journal	August 2006
Fatty acid biosynthesis in microorganisms being used for Single Cell Oil production Ratledge, Colin Biochimie, Vol. 86, Issue 11 https://doi.org/10.1016/j.biochi.2004.09.017	journal	November 2004
Regulation of lipid accumulation in oleaginous micro-organisms Ratledge, C. Biochemical Society Transactions, Vol. 30, Issue 6, p. 1047-1050 https://doi.org/10.1042/bst0301047	journal	November 2002
Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species Sitepu, Irnayuli R.; Sestric, Ryan; Ignatia, Laura Bioresource Technology, Vol. 144 https://doi.org/10.1016/j.biortech.2013.06.047	journal	September 2013
The genetics of polyamine synthesis in Neurospora crassa Pitkin, John; Davis, Rowland H. Archives of Biochemistry and Biophysics, Vol. 278, Issue 2 https://doi.org/10.1016/0003-9861(90)90275-4	journal	May 1990
Salmonella modulates metabolism during growth under conditions that induce expression of virulence genes Kim, Young-Mo; Schmidt, Brian J.; Kidwai, Afshan S. Molecular BioSystems, Vol. 9, Issue 6 https://doi.org/10.1039/c3mb25598k	journal	January 2013
Target-Decoy Search Strategy for Mass Spectrometry-Based Proteomics Elias, Joshua E.; Gygi, Steven P. Methods in Molecular Biology https://doi.org/10.1007/978-1-60761-444-9_5	book	December 2009
Microscopic Analysis of Lipid Droplet Metabolism and Dynamics in Yeast Wolinski, Heimo; Kohlwein, Sepp D. Membrane Trafficking https://doi.org/10.1007/978-1-59745-261-8_11	book	January 2008
Accumulation of High-Value Lipids in Single-Cell Microorganisms: A Mechanistic Approach and Future Perspectives Garay, Luis A.; Boundy-Mills, Kyria L.; German, J. Bruce Journal of Agricultural and Food Chemistry, Vol. 62, Issue 13 https://doi.org/10.1021/jf4042134	journal	March 2014
Oily yeasts as oleaginous cell factories Ageitos, Jose Manuel; Vallejo, Juan Andres; Veiga-Crespo, Patricia Applied Microbiology and Biotechnology, Vol. 90, Issue 4 https://doi.org/10.1007/s00253-011-3200-z	journal	April 2011
Physiology and genetics of the dimorphic fungus Yarrowia lipolytica Barth, Gerold; Gaillardin, Claude FEMS Microbiology Reviews, Vol. 19, Issue 4, p. 219-237 https://doi.org/10.1111/j.1574-6976.1997.tb00299.x	journal	April 1997
A Library of Yeast Transcription Factor Motifs Reveals a Widespread Function for Rsc3 in Targeting Nucleosome Exclusion at Promoters Badis, Gwenael; Chan, Esther T.; van Bakel, Harm Molecular Cell, Vol. 32, Issue 6 https://doi.org/10.1016/j.molcel.2008.11.020	journal	December 2008
Polyamine Metabolism and Growth of Neurospora Strains Lacking Cis-Acting Control Sites in the Ornithine Decarboxylase Gene Pitkin, J.; Perriere, M.; Kanehl, A. Archives of Biochemistry and Biophysics, Vol. 315, Issue 1 https://doi.org/10.1006/abbi.1994.1484	journal	November 1994
An evolutionary and functional assessment of regulatory network motifs Mazurie, Aurélien; Bottani, Samuel; Vergassola, Massimo Genome Biology, Vol. 6, Issue 4, p. R35 https://doi.org/10.1186/gb-2005-6-4-r35	journal	January 2005
Self-made frits for nanoscale columns in proteomics Maiolica, Alessio; Borsotti, Dario; Rappsilber, Juri PROTEOMICS, Vol. 5, Issue 15 https://doi.org/10.1002/pmic.200402010	journal	October 2005
Isolation and characterization of two crude oil-degrading yeast strains, Yarrowia lipolytica PG-20 and PG-32, from the Persian Gulf Hassanshahian, Mehdi; Tebyanian, Hamid; Cappello, Simone Marine Pollution Bulletin, Vol. 64, Issue 7 https://doi.org/10.1016/j.marpolbul.2012.04.020	journal	July 2012
Genetic regulation of nitrogen metabolism in the fungi. Marzluf, G. A. Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 1 https://doi.org/10.1128/.61.1.17-32.1997	journal	January 1997
DREME: motif discovery in transcription factor ChIP-seq data Bailey, Timothy L. Bioinformatics, Vol. 27, Issue 12 https://doi.org/10.1093/bioinformatics/btr261	journal	May 2011
DAnTE: a statistical tool for quantitative analysis of -omics data Polpitiya, A. D.; Qian, W. -J.; Jaitly, N. Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn217	journal	May 2008
Nitrogen Catabolite Repression of DAL80 Expression Depends on the Relative Levels of Gat1p and Ure2p Production in Saccharomyces cerevisiae Cunningham, Thomas S.; Andhare, Roopa; Cooper, Terrance G. Journal of Biological Chemistry, Vol. 275, Issue 19 https://doi.org/10.1074/jbc.275.19.14408	journal	May 2000
Regulation of nitrogen assimilation in Saccharomyces cerevisiae: roles of the URE2 and GLN3 genes. Courchesne, W. E.; Magasanik, B. Journal of Bacteriology, Vol. 170, Issue 2 https://doi.org/10.1128/JB.170.2.708-713.1988	journal	February 1988
The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors Beck, Thomas; Hall, Michael N. Nature, Vol. 402, Issue 6762 https://doi.org/10.1038/45287	journal	December 1999
The pathway of arginine breakdown in Saccharomyces cerevisiae Middelhoven, W. J. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 93, Issue 3 https://doi.org/10.1016/0304-4165(64)90349-6	journal	December 1964
Disruption of the MIG1 gene enhances lipid biosynthesis in the oleaginous yeast Yarrowia lipolytica ACA-DC 50109 Wang, Zhi-Peng; Xu, Hong-Mei; Wang, Guang-Yuan Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1831, Issue 4 https://doi.org/10.1016/j.bbalip.2012.12.010	journal	April 2013
Recent Advances in Nitrogen Regulation: a Comparison between Saccharomyces cerevisiae and Filamentous Fungi Wong, Koon Ho; Hynes, Michael J.; Davis, Meryl A. Eukaryotic Cell, Vol. 7, Issue 6 https://doi.org/10.1128/EC.00076-08	journal	April 2008
Sch9 regulates ribosome biogenesis via Stb3, Dot6 and Tod6 and the histone deacetylase complex RPD3L Huber, Alexandre; French, Sarah L.; Tekotte, Hille The EMBO Journal, Vol. 30, Issue 15 https://doi.org/10.1038/emboj.2011.221	journal	July 2011
Stb3 Plays a Role in the Glucose-Induced Transition from Quiescence to Growth in Saccharomyces cerevisiae Liko, Dritan; Conway, Michael K.; Grunwald, Douglas S. Genetics, Vol. 185, Issue 3 https://doi.org/10.1534/genetics.110.116665	journal	April 2010
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research Conesa, A.; Gotz, S.; Garcia-Gomez, J. M. Bioinformatics, Vol. 21, Issue 18 https://doi.org/10.1093/bioinformatics/bti610	journal	August 2005
Comprehensive Metabolomic, Lipidomic and Microscopic Profiling of Yarrowia lipolytica during Lipid Accumulation Identifies Targets for Increased Lipogenesis Pomraning, Kyle R.; Wei, Siwei; Karagiosis, Sue A. PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0123188	journal	April 2015
Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production Tai, Mitchell; Stephanopoulos, Gregory Metabolic Engineering, Vol. 15, p. 1-9 https://doi.org/10.1016/j.ymben.2012.08.007	journal	January 2013
Quantitative phosphoproteomics identifies filaggrin and other targets of ionizing radiation in a human skin model: Phosphoproteomics on irradiated skin Yang, Feng; Waters, Katrina M.; Webb-Robertson, Bobbie-Jo Experimental Dermatology, Vol. 21, Issue 5 https://doi.org/10.1111/j.1600-0625.2012.01470.x	journal	April 2012
MASIC: A software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC–MS(/MS) features Monroe, Matthew E.; Shaw, Jason L.; Daly, Don S. Computational Biology and Chemistry, Vol. 32, Issue 3 https://doi.org/10.1016/j.compbiolchem.2008.02.006	journal	June 2008
Phosphorylation of ATP-Citrate Lyase by Nucleoside Diphosphate Kinase Wagner, Paul D.; Vu, Ngoc-Diep Journal of Biological Chemistry, Vol. 270, Issue 37 https://doi.org/10.1074/jbc.270.37.21758	journal	September 1995
Biochemical activities during lipid accumulation inCandida curvata Evans, Christopher T.; Ratledge, Colin Lipids, Vol. 18, Issue 9 https://doi.org/10.1007/BF02534674	journal	September 1983
Genome evolution in yeasts Dujon, Bernard; Sherman, David; Fischer, Gilles Nature, Vol. 430, Issue 6995 https://doi.org/10.1038/nature02579	journal	July 2004
Hyperornithinaemia- hyperammonaemia- homocitrullinuria syndrome is caused by mutations in a gene encoding a mitochondrial ornithine transporter Camacho, Jose A.; Obie, Cassandra; Biery, Barbara Nature Genetics, Vol. 22, Issue 2 https://doi.org/10.1038/9658	journal	June 1999
Transcriptomic Analyses during the Transition from Biomass Production to Lipid Accumulation in the Oleaginous Yeast Yarrowia lipolytica Morin, Nicolas; Cescut, Julien; Beopoulos, Athanasios PLoS ONE, Vol. 6, Issue 11, Article No. e27966 https://doi.org/10.1371/journal.pone.0027966	journal	November 2011
Enhanced lipid accumulation in the yeast Yarrowia lipolytica by over-expression of ATP:citrate lyase from Mus musculus Zhang, Huaiyuan; Zhang, Luning; Chen, Haiqin Journal of Biotechnology, Vol. 192 https://doi.org/10.1016/j.jbiotec.2014.10.004	journal	December 2014
141 Malic enzyme: A lipogenic enzyme in fungi Wynn, James P.; Kendrick, Andrew; Hamid, Adil A. Biochemical Society Transactions, Vol. 25, Issue 4 https://doi.org/10.1042/bst025s669	journal	November 1997
Essential Functions of Protein Tyrosine Phosphatases Ptp2 and Ptp3 and Rim11 Tyrosine Phosphorylation in Saccharomyces cerevisiae Meiosis and Sporulation Zhan, Xiao-Li; Hong, Yulong; Zhu, Tianqing Molecular Biology of the Cell, Vol. 11, Issue 2 https://doi.org/10.1091/mbc.11.2.663	journal	February 2000
Improving polyketide and fatty acid synthesis by engineering of the yeast acetyl-CoA carboxylase Choi, Jin Wook; Da Silva, Nancy A. Journal of Biotechnology, Vol. 187 https://doi.org/10.1016/j.jbiotec.2014.07.430	journal	October 2014
Degradation of the Transcription Factor Gcn4 Requires the Kinase Pho85 and the SCF ^CDC4 Ubiquitin–Ligase Complex Meimoun, Ariella; Holtzman, Tsvi; Weissman, Ziva Molecular Biology of the Cell, Vol. 11, Issue 3 https://doi.org/10.1091/mbc.11.3.915	journal	March 2000
Cross regulation of four GATA factors that control nitrogen catabolic gene expression in Saccharomyces cerevisiae. Coffman, J. A.; Rai, R.; Loprete, D. M. Journal of Bacteriology, Vol. 179, Issue 11 https://doi.org/10.1128/JB.179.11.3416-3429.1997	journal	June 1997
Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software Kamentsky, Lee; Jones, Thouis R.; Fraser, Adam Bioinformatics, Vol. 27, Issue 8 https://doi.org/10.1093/bioinformatics/btr095	journal	February 2011
Single cell oil production by Yarrowia lipolytica growing on an industrial derivative of animal fat in batch cultures Papanikolaou, S.; Chevalot, I.; Komaitis, M. Applied Microbiology and Biotechnology, Vol. 58, Issue 3, p. 308-312 https://doi.org/10.1007/s00253-001-0897-0	journal	March 2002
Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots Cooper, Terrance G. FEMS Microbiology Reviews, Vol. 26, Issue 3 https://doi.org/10.1111/j.1574-6976.2002.tb00612.x	journal	August 2002
Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae Conrad, Michaela; Schothorst, Joep; Kankipati, Harish Nag FEMS Microbiology Reviews, Vol. 38, Issue 2 https://doi.org/10.1111/1574-6976.12065	journal	March 2014
Improved similarity scores for comparing motifs Tanaka, Emi; Bailey, Timothy; Grant, Charles E. Bioinformatics, Vol. 27, Issue 12 https://doi.org/10.1093/bioinformatics/btr257	journal	May 2011
Distinct roles of putrescine and spermidine in the regulation of ornithine decarboxylase in Neurospora crassa. Davis, R. H.; Krasner, G. N.; DiGangi, J. J. Proceedings of the National Academy of Sciences, Vol. 82, Issue 12 https://doi.org/10.1073/pnas.82.12.4105	journal	June 1985
The Regulation of Glutamine Synthesis in Microorganisms Shapiro, B. M.; Stadtman, E. R. Annual Review of Microbiology, Vol. 24, Issue 1 https://doi.org/10.1146/annurev.mi.24.100170.002441	journal	October 1970
GCN4 protein, a positive transcription factor in yeast, binds general control promoters at all 5' TGACTC 3' sequences. Arndt, K.; Fink, G. R. Proceedings of the National Academy of Sciences, Vol. 83, Issue 22 https://doi.org/10.1073/pnas.83.22.8516	journal	November 1986
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
A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides Zhu, Zhiwei; Zhang, Sufang; Liu, Hongwei Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2112	journal	January 2012
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian Analytical Chemistry, Vol. 81, Issue 9 https://doi.org/10.1021/ac802689c	journal	May 2009
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
MS-GF+ makes progress towards a universal database search tool for proteomics Kim, Sangtae; Pevzner, Pavel A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6277	journal	October 2014
Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production Blazeck, John; Hill, Andrew; Liu, Leqian Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4131	journal	January 2014
Control of Lipid Accumulation in the Yeast Yarrowia lipolytica Beopoulos, A.; Mrozova, Z.; Thevenieau, F. Applied and Environmental Microbiology, Vol. 74, Issue 24, p. 7779-7789 https://doi.org/10.1128/AEM.01412-08	journal	October 2008
Glucose- and nitrogen sensing and regulatory mechanisms in Saccharomyces cerevisiae Rødkaer, Steven V.; Faergeman, Nils J. FEMS Yeast Research, Vol. 14, Issue 5 https://doi.org/10.1111/1567-1364.12157	journal	May 2014

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Regulation of Nitrogen Metabolism by GATA Zinc Finger Transcription Factors in Yarrowia lipolytica

Journal Article · Wed Feb 15 00:00:00 EST 2017 · mSphere · OSTI ID:1618542

Pomraning, Kyle R.; Bredeweg, Erin L.; Baker, Scott E.; +1 more

Leucine Biosynthesis Is Involved in Regulating High Lipid Accumulation in Yarrowia lipolytica

Journal Article · Wed Jul 05 00:00:00 EDT 2017 · mBio · OSTI ID:1618542

Kerkhoven, Eduard J.; Kim, Young-Mo; Wei, Siwei; +11 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Yarrowia lipolytica
lipid
proteome
metabolome
phosphorylation
phosphoproteome
nitrogen regulation
beta-oxidation
ribosome biogenesis
translation

Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica [Supplementary Data] Pomraning, Kyle; Kim, Young-Mo; Nicora, Carrie https://doi.org/10.6084/m9.figshare.c.3631478 The current record is supplemented by this dataset	dataset	February 2016
Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica [Supplemental Data] Pomraning, Kyle; Kim, Young-Mo; Nicora, Carrie https://doi.org/10.6084/m9.figshare.c.3631478.v1 The current record is supplemented by this dataset	dataset	February 2016
Additional file 1: of Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica [Supplemental Data] Pomraning, Kyle; Kim, Young-Mo; Nicora, Carrie https://doi.org/10.6084/m9.figshare.c.3631478_d1 The current record is supplemented by this dataset	dataset	February 2016
Additional file 1: of Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica Pomraning, Kyle; Kim, Young-Mo; Nicora, Carrie https://doi.org/10.6084/m9.figshare.c.3631478_d1.v1 The current record is supplemented by this dataset	dataset	February 2016
Additional file 2: of Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica Pomraning, Kyle; Nicora, Carrie; Chu, Rosalie https://doi.org/10.6084/m9.figshare.c.3631478_d2.v1 The current record is supplemented by this dataset	dataset	February 2016