Coordinated gene regulation in the initial phase of salt stress adaptation.
Stress triggers complex transcriptional responses, which include both gene activation and repression. We used time-resolved reporter assays in living yeast cells to gain insights into the coordination of positive and negative control of gene expression upon salt stress. We found that the repression of "housekeeping" genes coincides with the transient activation of defense genes and that the timing of this expression pattern depends on the severity of the stress. Moreover, we identified mutants that caused an alteration in the kinetics of this transcriptional control. Loss of function of the vacuolar H(+)-ATPase (vma1) or a defect in the biosynthesis of the osmolyte glycerol (gpd1) caused a prolonged repression of housekeeping genes and a delay in gene activation at inducible loci. Both mutants have a defect in the relocation of RNA polymerase II complexes at stress defense genes. Accordingly salt-activated transcription is delayed and less efficient upon partially respiratory growth conditions in which glycerol production is significantly reduced. Furthermore, the loss of Hog1 MAP kinase function aggravates the loss of RNA polymerase II from housekeeping loci, which apparently do not accumulate at inducible genes. Additionally the Def1 RNA polymerase II degradation factor, but not a high pool of nuclear polymerase II complexes, is needed for efficient stress-induced gene activation. The data presented here indicate that the finely tuned transcriptional control upon salt stress is dependent on physiological functions of the cell, such as the intracellular ion balance, the protective accumulation of osmolyte molecules, and the RNA polymerase II turnover.
the Department of Biotechnology, Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia, 46022 Valencia, Spain.
Elena
E
Vanacloig-Pedros
the Department of Biotechnology, Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia, 46022 Valencia, Spain.
Carolina
C
Bets-Plasencia
the Department of Biotechnology, Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia, 46022 Valencia, Spain apascual@ibmcp.upv.es.
Amparo
A
Pascual-Ahuir
From the Department of Mechanisms of Plant Stress Responses, Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas, and mproft@ibmcp.upv.es.
Markus
M
Proft
D020869:Gene Expression Profiling; D015966:Gene Expression Regulation, Fungal; D017930:Genes, Reporter; D005990:Glycerol / Q000378:metabolism; D050536:Glycerol-3-Phosphate Dehydrogenase (NAD+) / Q000235:genetics* / Q000378:metabolism; D008156:Luciferases / Q000235:genetics / Q000378:metabolism; D020928:Mitogen-Activated Protein Kinases / Q000235:genetics / Q000378:metabolism; D009997:Osmotic Pressure; D006180:Proton-Translocating ATPases / Q000235:genetics* / Q000378:metabolism; D012319:RNA Polymerase II / Q000235:genetics / Q000378:metabolism; D012441:Saccharomyces cerevisiae / Q000187:drug effects / Q000235:genetics* / Q000378:metabolism; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics* / Q000378:metabolism; D054712:Salinity; D055049:Salt Tolerance / Q000235:genetics*; D015398:Signal Transduction; D012965:Sodium Chloride / Q000494:pharmacology; D013312:Stress, Physiological; D014158:Transcription, Genetic
D029701:Saccharomyces cerevisiae Proteins; D012965:Sodium Chloride; C568531:GPD1 protein, S cerevisiae; D050536:Glycerol-3-Phosphate Dehydrogenase (NAD+); D008156:Luciferases; C088589:HOG1 protein, S cerevisiae; D020928:Mitogen-Activated Protein Kinases; D012319:RNA Polymerase II; D006180:Proton-Translocating ATPases; C081687:VMA1 protein, S cerevisiae; D005990:Glycerol
Gene Expression; Glycerol; Hog1; Osmotic Stress; Saccharomyces cerevisiae; Stress Response; Transcription Regulation; Vacuolar ATPase