Promoters maintain their relative activity levels under different growth conditions

Abstract

Most genes change expression levels across conditions, but it is unclear which of these changes represents specific regulation and what determines their quantitative degree. Here, we accurately measured activities of ~900 S. cerevisiae and ~1800 E. coli promoters using fluorescent reporters. We show that in both organisms 60-90% of promoters change their expression between conditions by a constant global scaling factor that depends only on the conditions and not on the promoter's identity. Quantifying such global effects allows precise characterization of specific regulation-promoters deviating from the global scale line. These are organized into few functionally related groups that also adhere to scale lines and preserve their relative activities across conditions. Thus, only several scaling factors suffice to accurately describe genome-wide expression profiles across conditions. We present a parameter-free passive resource allocation model that quantitatively accounts for the global scaling factors. It suggests that many changes in expression across conditions result from global effects and not specific regulation, and provides means for quantitative interpretation of expression profiles.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 84

1. 1.

   Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000 ) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25–29

   Not in our library10.1038/75556

2. 2.

   Badis G, Chan ET, van Bakel H, Pena-Castillo L, Tillo D, Tsui K, Carlson CD, Gossett AJ, Hasinoff MJ, Warren CL, Gebbia M, Talukder S, Yang A, Mnaimneh S, Terterov D, Coburn D, Li Yeo A, Yeo ZX, Clarke ND, Lieb JD (2008 ) A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol Cell 32: 878–887

   Not in our library10.1016/j.molcel.2008.11.020

3. 3.

   Bakel H Van, Holstege FCP (2008 ) A tutorial for DNA microarray expression profiling. Cell Evaluating: 22–28, Available at: http://download.cell.com/images/edimages/etbr/VANBAKEL.PDF

   Not in our library

4. 4.

   Balázsi G, Oltvai ZN (2007 ) A pitfall in series of microarrays: the position of probes affects the cross-correlation of gene expression profiles. Methods Mol Biol (Clifton, NJ) 377: 153–162

   Not in our library10.1007/978-1-59745-390-5_9

5. 5.

   Bammler T, Beyer RP, Bhattacharya S, Boorman GA, Boyles A, Bradford BU, Bumgarner RE, Bushel PR, Chaturvedi K, Choi D, Cunningham ML, Deng S, Dressman HK, Fannin RD, Farin FM, Freedman JH, Fry RC, Harper A, Humble MC, Hurban P (2005 ) Standardizing global gene expression analysis between laboratories and across platforms. Nat Meth 2: 351–356

   Not in our library10.1038/nmeth754

6. 6.

   Benjamini Y, Hochberg Y (1995 ) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol 57: 289–300

   Not in our library

7. 7.

   Boer VM, de Winde JH, Pronk JT, Piper MDW (2003 ) The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. J Biol Chem 278: 3265–3274

   Not in our library10.1074/jbc.m209759200

8. 8.

   Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, Gresham D, Boer VM, Troyanskaya OG, Botstein D (2008 ) Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol Biol Cell 19: 352–367

   Not in our library10.1091/mbc.e07-08-0779

9. 9.

   Bremer H, Dennis P (1987 ) Modulation of chemical composition and other parameters of the cell by growth rate. Escherichia coli and Salmonella. Available at: http://ctbp.ucsd.edu/qbio/beemer96.pdf [Accessed 7 November 2011]

   Not in our library

10. 10.

    Broach JR (2012 ) Nutritional control of growth and development in yeast. Genetics 192: 73–105

    Not in our library10.1534/genetics.111.135731

11. 11.

    Bronstein I, Fortin J, Stanley PE, Stewart GS, Kricka LJ (1994 ) Chemiluminescent and bioluminescent reporter gene assays. Anal Biochem 219: 169–181

    Not in our library10.1006/abio.1994.1254

12. 12.
    Growth control of the eukaryote cell: a systems biology study in yeast · 2007

    No notice
13. 13.

    Chechik G, Oh E, Rando O, Weissman J, Regev A, Koller D (2008 ) Activity motifs reveal principles of timing in transcriptional control of the yeast metabolic network. Nat Biotechnol 26: 1251–1259

    Not in our library10.1038/nbt.1499

14. 14.

    Churchill GA (2002 ) Fundamentals of experimental design for cDNA microarrays. Nat Genet 32(Suppl): 490–495

    Not in our library10.1038/ng1031

15. 15.

    Cormack BP, Valdivia RH, Falkow S (1996 ) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33–38

    Not in our library10.1016/0378-1119(95)00685-0

16. 16.

    Costenoble R, Picotti P, Reiter L, Stallmach R, Heinemann M, Sauer U, Aebersold R (2011 ) Comprehensive quantitative analysis of central carbon and amino-acid metabolism in Saccharomyces cerevisiae under multiple conditions by targeted proteomics. Mol Syst Biol 7: 464

    Not in our library10.1038/msb.2010.122

17. 17.

    Cox RS, Surette MG, Elowitz MB (2007 ) Programming gene expression with combinatorial promoters. Mol Syst Biol 3: 145

    Not in our library10.1038/msb4100187

18. 18.

    De Godoy LMF, Olsen J V, Cox J, Nielsen ML, Hubner NC, Fröhlich F, Walther TC, Mann M (2008 ) Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455: 1251–1254

    Not in our library10.1038/nature07341

19. 19.

    DeRisi JL (1997 ) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278: 680–686

    Not in our library10.1126/science.278.5338.680

20. 20.
    GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists · 2009

    No notice
21. 21.

    Edgar R (2002 ) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207–210

    Not in our library10.1093/nar/30.1.207

22. 22.

    Ehrenberg M, Kurland CG (1984 ) Costs of accuracy determined by a maximal growth rate constraint. Q Rev Biophys 17: 45–82

    Not in our library10.1017/s0033583500005254

23. 23.

    Fazio A, Jewett M (2008 ) Transcription factor control of growth rate dependent genes in Saccharomyces cerevisiae: a three factor design. BMC Available at: http://www.biomedcentral.com/1471-2164/9/341 [Accessed 7 November 2011]

    Not in our library10.1186/1471-2164-9-341

24. 24.

    Fendt S-M, Sauer U (2010 ) Transcriptional regulation of respiration in yeast metabolizing differently repressive carbon substrates. BMC Syst Biol 4: 12

    Not in our library10.1186/1752-0509-4-12

25. 25.

    Frantz S (2005 ) An array of problems. Nat Rev Drug Discov 4: 362–363

    Not in our library10.1038/nrd1746

26. 26.

    Gasch AP, Eisen MB (2002 ) Exploring the conditional coregulation of yeast gene expression through fuzzy k-means clustering. Genome Biol 3: RESEARCH0059

    Not in our library10.1186/gb-2002-3-11-research0059

27. 27.

    Gasch AP, Huang M, Metzner S, Botstein D, Elledge SJ, Brown PO (2001 ) Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol Biol Cell 12: 2987–3003

    Not in our library10.1091/mbc.12.10.2987

28. 28.
    Genomic Expression Programs in the Response of Yeast Cells to Environmental ChangesD⃞ · 2000

    Not checked
29. 29.
    Dissecting specific and global transcriptional regulation of bacterial gene expression · 2013

    Not checked
30. 30.

    Gertz J, Siggia ED, Cohen BA (2009 ) Analysis of combinatorial cis-regulation in synthetic and genomic promoters. Nature 457: 215–218

    Not in our library10.1038/nature07521

31. 31.

    Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003 ) Global analysis of protein expression in yeast. Nature 425: 737–741

    Not in our library10.1038/nature02046

32. 32.

    Haurie V, Perrot M, Mini T, Jenö P, Sagliocco F, Boucherie H (2001 ) The transcriptional activator Cat8p provides a major contribution to the reprogramming of carbon metabolism during the diauxic shift in Saccharomyces cerevisiae. J Biol Chem 276: 76–85

    Not in our library10.1074/jbc.m008752200

33. 33.

    Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA (1998 ) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717–728

    Not in our library10.1016/s0092-8674(00)81641-4

34. 34.

    Hughes JD, Estep PW, Tavazoie S, Church GM (2000 ) Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J Mol Biol 296: 1205–1214

    Not in our library10.1006/jmbi.2000.3519

35. 35.

    Huisinga KL, Pugh BF (2004 ) A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol Cell 13: 573–585

    Not in our library10.1016/s1097-2765(04)00087-5

36. 36.

    Ihmels J, Friedlander G, Bergmann S, Sarig O, Ziv Y, Barkai N (2002 ) Revealing modular organization in the yeast transcriptional network. Nat Genet 31: 370–377

    Not in our library10.1038/ng941

37. 37.

    Ingraham JL, Maaløe O, Neidhardt FC (1983 ) Growth of the Bacterial Cell Sunderland, MA: Sinauer Assoc.,

    Not in our library

38. 38.

    Islam S, Kjällquist U, Moliner A, Zajac P, Fan J-B, Lönnerberg P, Linnarsson S (2011 ) Characterization of the single-cell transcriptional landscape by highly multiplex RNA-seq. Genome Res 21: 1160–1167

    Not in our library10.1101/gr.110882.110

39. 39.

    Jacob F, Monod J (1961 ) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3: 318–356

    Not in our library10.1016/s0022-2836(61)80072-7

40. 40.

    Kalir S, McClure J, Pabbaraju K, Southward C, Ronen M, Leibler S, Surette MG, Alon U (2001 ) Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria. Science (New York, NY) 292: 2080–2083

    Not in our library10.1126/science.1058758

Cited by papers we hold 9

• De novo biosynthesis of bioactive isoflavonoids by engineered yeast cell factories · 2021
  No notice
• Deep learning suggests that gene expression is encoded in all parts of a co-evolving interacting gene regulatory structure · 2020
  No notice
• Rewiring carbon metabolism in yeast for high level production of aromatic chemicals · 2019
  No notice
• Promoter Activity Buffering Reduces the Fitness Cost of Misregulation · 2018
  Not checked
• Few regulatory metabolites coordinate expression of central metabolic genes in Escherichia coli · 2017
  No notice
• Principles of cellular resource allocation revealed by condition-dependent proteome profiling · 2017
  No notice
• Optimality and sub-optimality in a bacterial growth law · 2017
  No notice
• Hierarchy of non-glucose sugars in Escherichia coli · 2014
  No notice
• A ‘resource allocator’ for transcription based on a highly fragmented T7 RNA polymerase · 2014
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.