Abstract
Regulation of gene expression by the Hog1 stress-activated protein kinase is essential for proper cell adaptation to osmostress. Hog1 coordinates an extensive transcriptional program through the modulation of transcription. To identify systematically novel components of the transcriptional machinery required for osmostress-mediated gene expression, we performed an exhaustive genome-wide genetic screening, searching for mutations that render cells osmosensitive at high osmolarity and that are associated with reduced expression of osmoresponsive genes. The SAGA and Mediator complexes were identified as putative novel regulators of osmostress-mediated transcription. Interestingly, whereas Mediator is essential for osmostress gene expression, the requirement for SAGA is different depending on the strength of the extracellular osmotic conditions. At mild osmolarity, SAGA mutants show only very slight defects on RNA polymerase II (Pol II) recruitment and gene expression, whereas at severe osmotic conditions, SAGA mutants show completely impaired RNA Pol II recruitment and transcription of osmoresponsive genes. Thus, our results define an essential role for Mediator in osmostress gene expression and a selective role for SAGA under severe osmostress. Our results indicate that the requirement for a transcriptional complex to regulate a promoter might be determined by the strength of the stimuli perceived by the cell through the regulation of interactions between transcriptional complexes.
MeSH Terms
Gene Expression Regulation, Fungal
Macromolecular Substances
Mitogen-Activated Protein Kinases/genetics,metabolism
Osmolar Concentration
Osmotic Pressure
Promoter Regions, Genetic
RNA Polymerase II/metabolism
Saccharomyces cerevisiae/cytology,physiology
Saccharomyces cerevisiae Proteins/genetics,metabolism
Trans-Activators/genetics,metabolism
Transcription Factors/genetics,metabolism
Transcription, Genetic
Chemicals
Macromolecular Substances
SAGA complex, S cerevisiae
Saccharomyces cerevisiae Proteins
Trans-Activators
Transcription Factors
HOG1 protein, S cerevisiae
Mitogen-Activated Protein Kinases
RNA Polymerase II
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Zapater Meritxell
Cell Signaling Unit, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Dr. Aiguader 88, E-08003 Barcelona, Spain.
Sohrmann Marc
Peter Matthias
Posas Francesc
de Nadal Eulàlia
References (31)
31 references, click to expand
-
Simultaneous recruitment of coactivators by Gcn4p stimulates multiple steps of transcription in vivo.
Mol Cell Biol. 2005 Jul;25(13):5626-38
PMID: 15964818
-
Mediator and the mechanism of transcriptional activation.
Trends Biochem Sci. 2005 May;30(5):235-9
PMID: 15896740
-
Genome-wide location of the coactivator mediator: Binding without activation and transient Cdk8 interaction on DNA.
Mol Cell. 2006 Apr 21;22(2):179-92
PMID: 16630888
-
The stress-activated Hog1 kinase is a selective transcriptional elongation factor for genes responding to osmotic stress.
Mol Cell. 2006 Jul 21;23(2):241-50
PMID: 16857590
-
Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions.
Mol Cell. 2007 Jan 12;25(1):31-42
PMID: 17218269
-
Redundant roles for the TFIID and SAGA complexes in global transcription.
Nature. 2000 Jun 8;405(6787):701-4
PMID: 10864329
-
Derepression of DNA damage-regulated genes requires yeast TAF(II)s.
EMBO J. 2000 Aug 1;19(15):4091-100
PMID: 10921889
-
Regulation of the Sko1 transcriptional repressor by the Hog1 MAP kinase in response to osmotic stress.
EMBO J. 2001 Mar 1;20(5):1123-33
PMID: 11230135
-
Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation.
Physiol Rev. 2001 Apr;81(2):807-69
PMID: 11274345
-
Stress-induced map kinase Hog1 is part of transcription activation complexes.
Mol Cell. 2001 Apr;7(4):767-77
PMID: 11336700
-
Systematic genetic analysis with ordered arrays of yeast deletion mutants.
Science. 2001 Dec 14;294(5550):2364-8
PMID: 11743205
-
Osmotic stress signaling and osmoadaptation in yeasts.
Microbiol Mol Biol Rev. 2002 Jun;66(2):300-72
PMID: 12040128
-
Hog1 kinase converts the Sko1-Cyc8-Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress.
Mol Cell. 2002 Jun;9(6):1307-17
PMID: 12086627
-
Dealing with osmostress through MAP kinase activation.
EMBO Rep. 2002 Aug;3(8):735-40
PMID: 12151331
-
Targeting the MEF2-like transcription factor Smp1 by the stress-activated Hog1 mitogen-activated protein kinase.
Mol Cell Biol. 2003 Jan;23(1):229-37
PMID: 12482976
-
Osmostress-induced transcription by Hot1 depends on a Hog1-mediated recruitment of the RNA Pol II.
EMBO J. 2003 May 15;22(10):2433-42
PMID: 12743037
-
Independent recruitment in vivo by Gal4 of two complexes required for transcription.
Mol Cell. 2003 May;11(5):1301-9
PMID: 12769853
-
FunSpec: a web-based cluster interpreter for yeast.
BMC Bioinformatics. 2002 Nov 13;3:35
PMID: 12431279
-
The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes.
Nature. 2004 Jan 22;427(6972):370-4
PMID: 14737171
-
A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae.
Mol Cell. 2004 Feb 27;13(4):573-85
PMID: 14992726
-
Molecular architecture of the S. cerevisiae SAGA complex.
Mol Cell. 2004 Jul 23;15(2):199-208
PMID: 15260971
-
MAP kinase-mediated stress relief that precedes and regulates the timing of transcriptional induction.
Cell. 2004 Aug 6;118(3):351-61
PMID: 15294160
-
Global position and recruitment of HATs and HDACs in the yeast genome.
Mol Cell. 2004 Oct 22;16(2):199-209
PMID: 15494307
-
Yeast SKO1 gene encodes a bZIP protein that binds to the CRE motif and acts as a repressor of transcription.
Nucleic Acids Res. 1992 Oct 25;20(20):5271-8
PMID: 1437546
-
ACR1, a yeast ATF/CREB repressor.
Mol Cell Biol. 1992 Dec;12(12):5394-405
PMID: 1448073
-
Dissecting the regulatory circuitry of a eukaryotic genome.
Cell. 1998 Nov 25;95(5):717-28
PMID: 9845373
-
Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme.
Nature. 1999 Jun 10;399(6736):609-13
PMID: 10376605
-
MAP kinases and the adaptive response to hypertonicity: functional preservation from yeast to mammals.
Am J Physiol Renal Physiol. 2004 Dec;287(6):F1102-10
PMID: 15522988
-
When the stress of your environment makes you go HOG wild.
Science. 2004 Nov 26;306(5701):1511-2
PMID: 15567851
-
SAGA unveiled.
Trends Biochem Sci. 2005 Jan;30(1):7-10
PMID: 15653319
-
Activator-specific recruitment of Mediator in vivo.
Nat Struct Mol Biol. 2006 Feb;13(2):117-20
PMID: 16429153