Early transcriptional response of Saccharomyces cerevisiae to stress imposed by the herbicide 2,4-dichlorophenoxyacetic acid.

The global gene transcription pattern of the eukaryotic experimental model Saccharomyces cerevisiae in response to sudden aggression with the widely used herbicide 2,4-dichlorophenoxyacetic acid (2,4-D) was analysed. Under acute stress, 14% of the yeast transcripts suffered a greater than twofold change. The yeastract database was used to predict the transcription factors mediating the response registered in this microarray analysis. Most of the up-regulated genes in response to 2,4-D are known targets of Msn2p, Msn4p, Yap1p, Pdr1p, Pdr3p, Stp1p, Stp2p and Rpn4p. The major regulator of ribosomal protein genes, Sfp1p, is known to control 60% of the down-regulated genes, in particular many involved in the transcriptional and translational machinery and in cell division. The yeast response to the herbicide includes the increased expression of genes involved in the oxidative stress response, the recovery or degradation of damaged proteins, cell wall remodelling and multiple drug resistance. Although the protective role of TPO1 and PDR5 genes was confirmed, the majority of the responsive genes encoding multidrug resistance do not confer resistance to 2,4-D. The increased expression of genes involved in alternative carbon and nitrogen source metabolism, fatty acid beta-oxidation and autophagy was also registered, suggesting that acute herbicide stress leads to nutrient limitation.

[1]  C. Palmeira,et al.  Interactions of herbicides 2,4-D and dinoseb with liver mitochondrial bioenergetics. , 1994, Toxicology and applied pharmacology.

[2]  B. E. Watt,et al.  Mechanisms of Toxicity, Clinical Features, and Management of Acute Chlorophenoxy Herbicide Poisoning: A Review , 2000, Journal of toxicology. Clinical toxicology.

[3]  M. Carlson,et al.  Glucose repression in yeast. , 1999, Current opinion in microbiology.

[4]  W. Pratt,et al.  Regulation of Signaling Protein Function and Trafficking by the hsp90/hsp70-Based Chaperone Machinery 1 , 2003, Experimental biology and medicine.

[5]  Miguel C. Teixeira,et al.  Adaptation of Saccharomyces cerevisiae to the Herbicide 2,4-Dichlorophenoxyacetic Acid, Mediated by Msn2p- and Msn4p-Regulated Genes: Important Role of SPI1 , 2003, Applied and Environmental Microbiology.

[6]  J. C. Kapteyn,et al.  The contribution of cell wall proteins to the organization of the yeast cell wall. , 1999, Biochimica et biophysica acta.

[7]  J. Heinisch,et al.  The protein kinase C‐mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae , 1999, Molecular microbiology.

[8]  Yong-Su Jin,et al.  Saccharomyces cerevisiae Engineered for Xylose Metabolism Exhibits a Respiratory Response , 2004, Applied and Environmental Microbiology.

[9]  A. Brown,et al.  Activity of the plasma membrane H(+)-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid , 1996, Applied and environmental microbiology.

[10]  Precious G. Motshwene,et al.  LEA (late embryonic abundant)-like protein Hsp 12 (heat-shock protein 12) is present in the cell wall and enhances the barotolerance of the yeast Saccharomyces cerevisiae. , 2004, The Biochemical journal.

[11]  M. A. de la Torre-Ruiz,et al.  Regulation of the Cell Integrity Pathway by Rapamycin-sensitive TOR Function in Budding Yeast* , 2002, The Journal of Biological Chemistry.

[12]  J. Spinelli,et al.  Non-Hodgkin's lymphoma and specific pesticide exposures in men: cross-Canada study of pesticides and health. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[13]  P. Kötter,et al.  Mutants that show increased sensitivity to hydrogen peroxide reveal an important role for the pentose phosphate pathway in protection of yeast against oxidative stress , 1996, Molecular and General Genetics MGG.

[14]  Mark Johnston,et al.  Function and Regulation of Yeast Hexose Transporters , 1999, Microbiology and Molecular Biology Reviews.

[15]  Y. Tone,et al.  Nob1p is required for biogenesis of the 26S proteasome and degraded upon its maturation in Saccharomyces cerevisiae. , 2002, Genes & development.

[16]  S. Lindquist,et al.  Hsp104, Hsp70, and Hsp40 A Novel Chaperone System that Rescues Previously Aggregated Proteins , 1998, Cell.

[17]  A. R. Fernandes,et al.  Activation and significance of vacuolar H+-ATPase in Saccharomyces cerevisiae adaptation and resistance to the herbicide 2,4-dichlorophenoxyacetic acid. , 2003, Biochemical and biophysical research communications.

[18]  J. Winther,et al.  Review: Biosynthesis and function of yeast vacuolar proteases , 1996, Yeast.

[19]  Susan Lindquist,et al.  Protein disaggregation mediated by heat-shock protein Hspl04 , 1994, Nature.

[20]  A. Goffeau,et al.  Yeast multidrug resistance: The PDR network , 1995, Journal of bioenergetics and biomembranes.

[21]  W. Brandt,et al.  The LEA-like protein HSP 12 in Saccharomyces cerevisiae has a plasma membrane location and protects membranes against desiccation and ethanol-induced stress. , 2000, Biochimica et biophysica acta.

[22]  Tobias Schmelzle,et al.  Yeast Protein Kinases and the RHO1 Exchange Factor TUS1 Are Novel Components of the Cell Integrity Pathway in Yeast , 2002, Molecular and Cellular Biology.

[23]  H. Vainio,et al.  Enhanced peroxisomal beta-oxidation of fatty acids and glutathione metabolism in rats exposed to phenoxyacetic acids. , 1985, Toxicology.

[24]  C. D. S. Tomlin,et al.  The Pesticide Manual , 2003 .

[25]  F Sherman,et al.  Review: The Cct eukaryotic chaperonin subunits of Saccharomyces cerevisiae and other yeasts , 1996, Yeast.

[26]  A. Covarrubias,et al.  Highly Hydrophilic Proteins in Prokaryotes and Eukaryotes Are Common during Conditions of Water Deficit* , 2000, The Journal of Biological Chemistry.

[27]  H. Vainio,et al.  Hypolipidemia and peroxisome proliferation induced by phenoxyacetic acid herbicides in rats. , 1983, Biochemical pharmacology.

[28]  Charles E. Martin,et al.  A Novel Cytochrome b5-like Domain Is Linked to the Carboxyl Terminus of the Saccharomyces cerevisiae Δ-9 Fatty Acid Desaturase (*) , 1995, The Journal of Biological Chemistry.

[29]  K. Köhrer,et al.  Preparation of high molecular weight RNA. , 1991, Methods in enzymology.

[30]  S. Zołnierowicz,et al.  Comparison of uncoupling activities of chlorophenoxy herbicides in rat liver mitochondria. , 1990, Toxicology letters.

[31]  Rudy Pandjaitan,et al.  The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast , 1998, The EMBO journal.

[32]  K. Mauch,et al.  Determination of in vivo kinetics of the starvation-induced Hxt5 glucose transporter of Saccharomyces cerevisiae. , 2002, FEMS yeast research.

[33]  D. Koller,et al.  Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  A. Brown,et al.  Genetic manipulation of 6-phosphofructo-1-kinase and fructose 2,6-bisphosphate levels affects the extent to which benzoic acid inhibits the growth of Saccharomyces cerevisiae. , 2001, Microbiology.

[35]  L. Gustafsson,et al.  Anaerobicity Prepares Saccharomyces cerevisiae Cells for Faster Adaptation to Osmotic Shock , 2004, Eukaryotic Cell.

[36]  Miguel C. Teixeira,et al.  A proteome analysis of the yeast response to the herbicide 2,4‐dichlorophenoxyacetic acid , 2005, Proteomics.

[37]  J. Buhler,et al.  The H2O2 Stimulon in Saccharomyces cerevisiae * , 1998, The Journal of Biological Chemistry.

[38]  I. S. Pretorius,et al.  Carnitine‐dependent metabolic activities in Saccharomyces cerevisiae: three carnitine acetyltransferases are essential in a carnitine‐dependent strain , 2001, Yeast.

[39]  M. Suwalsky,et al.  Interaction of 2,4-dichlorophenoxyacetic acid (2,4-D) with cell and model membranes. , 1996, Biochimica et biophysica acta.

[40]  P. F. Almeida,et al.  The H+-ATPase in the Plasma Membrane ofSaccharomyces cerevisiae Is Activated during Growth Latency in Octanoic Acid-Supplemented Medium Accompanying the Decrease in Intracellular pH and Cell Viability , 1998, Applied and Environmental Microbiology.

[41]  G. G. Bond,et al.  Weight of the evidence on the human carcinogenicity of 2,4-D* , 1991, Environmental health perspectives.

[42]  S. Kuhara,et al.  Response of genes associated with mitochondrial function to mild heat stress in yeast Saccharomyces cerevisiae. , 2003, Journal of biochemistry.

[43]  Miguel C. Teixeira,et al.  Saccharomyces cerevisiae resistance to chlorinated phenoxyacetic acid herbicides involves Pdr1p-mediated transcriptional activation of TPO1 and PDR5 genes. , 2002, Biochemical and biophysical research communications.

[44]  S. Schreiber,et al.  Carbon- and nitrogen-quality signaling to translation are mediated by distinct GATA-type transcription factors , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[45]  C. Grant Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions , 2001, Molecular microbiology.

[46]  J. Gancedo Yeast Carbon Catabolite Repression , 1998, Microbiology and Molecular Biology Reviews.

[47]  Miguel C. Teixeira,et al.  Yeast adaptation to 2,4-dichlorophenoxyacetic acid involves increased membrane fatty acid saturation degree and decreased OLE1 transcription. , 2005, Biochemical and biophysical research communications.

[48]  Y. Ohsumi,et al.  [Autophagy in yeast]. , 1993, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[49]  A. D. Re,et al.  Relationships of Pesticide Octanol/Water Partition Coefficients to Their Physicochemical Properties , 1993 .

[50]  M. Jia,et al.  Global expression profiling of yeast treated with an inhibitor of amino acid biosynthesis, sulfometuron methyl. , 2000, Physiological genomics.

[51]  Pooja Jain,et al.  The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae , 2005, Nucleic Acids Res..

[52]  Carsten Friis,et al.  Transcriptional profiling of extracellular amino acid sensing in Saccharomyces cerevisiae and the role of Stp1p and Stp2p , 2004, Yeast.

[53]  A. Kastaniotis,et al.  The biochemistry of peroxisomal β-oxidation in the yeast Saccharomyces cerevisiae , 2003 .

[54]  C. Li,et al.  Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[55]  A. Sols,et al.  Studies on the mechanism of the antifungal action of benzoate. , 1983, The Biochemical journal.

[56]  Jun Onodera,et al.  Autophagy Is Required for Maintenance of Amino Acid Levels and Protein Synthesis under Nitrogen Starvation* , 2005, Journal of Biological Chemistry.

[57]  J. Winderickx,et al.  From feast to famine: Adaptation to nutrient depletion in yeast , 1997 .

[58]  Ronald W. Davis,et al.  Transcriptional response of Saccharomyces cerevisiae to DNA-damaging agents does not identify the genes that protect against these agents , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[59]  P. Piper,et al.  Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives. , 2001, Microbiology.

[60]  W. Chaffin,et al.  Members of the Hsp70 family of proteins in the cell wall of Saccharomyces cerevisiae , 1996, Journal of bacteriology.

[61]  J. D. de Winde,et al.  Novel sensing mechanisms and targets for the cAMP–protein kinase A pathway in the yeast Saccharomyces cerevisiae , 1999, Molecular microbiology.

[62]  S. Cullinan,et al.  Functional Interactions between Hsp90 and the Co-chaperones Cns1 and Cpr7 in Saccharomyces cerevisiae* , 2003, Journal of Biological Chemistry.

[63]  H. Bussey,et al.  Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. , 1997, Genetics.

[64]  Mehdi Mollapour,et al.  Moderately lipophilic carboxylate compounds are the selective inducers of the Saccharomyces cerevisiae Pdr12p ATP‐binding cassette transporter , 2003, Yeast.

[65]  J. Garin,et al.  Yap1 and Skn7 Control Two Specialized Oxidative Stress Response Regulons in Yeast* , 1999, The Journal of Biological Chemistry.

[66]  F. Turano,et al.  Expression of a Glutamate Decarboxylase Homologue Is Required for Normal Oxidative Stress Tolerance in Saccharomyces cerevisiae * , 2001, The Journal of Biological Chemistry.

[67]  E. Lander,et al.  Remodeling of yeast genome expression in response to environmental changes. , 2001, Molecular biology of the cell.

[68]  Peter J. Coote,et al.  Evidence of a New Role for the High-Osmolarity Glycerol Mitogen-Activated Protein Kinase Pathway in Yeast: Regulating Adaptation to Citric Acid Stress , 2004, Molecular and Cellular Biology.

[69]  H. V. van Vuuren,et al.  Ammonia Regulates VID30 Expression and Vid30p Function Shifts Nitrogen Metabolism toward Glutamate Formation Especially when Saccharomyces cerevisiae Is Grown in Low Concentrations of Ammonia* , 2001, The Journal of Biological Chemistry.

[70]  I. Sá-Correia,et al.  Activation of plasma membrane ATPase of Saccharomyces cerevisiae by octanoic acid. , 1991, Journal of general microbiology.

[71]  G. Owsianik,et al.  Control of 26S proteasome expression by transcription factors regulating multidrug resistance in Saccharomyces cerevisiae , 2002, Molecular microbiology.

[72]  Miguel C. Teixeira,et al.  The herbicide 2,4-dichlorophenoxyacetic acid induces the generation of free-radicals and associated oxidative stress responses in yeast. , 2004, Biochemical and biophysical research communications.

[73]  L. Yu,et al.  Molecular cloning and mapping of the brain-abundant B1gamma subunit of protein phosphatase 2A, PPP2R2C, to human chromosome 4p16. , 2000, Genomics.

[74]  Audrey P. Gasch,et al.  The environmental stress response: a common yeast response to diverse environmental stresses , 2003 .

[75]  I. Pedruzzi,et al.  Saccharomyces cerevisiae Ras/cAMP pathway controls post‐diauxic shift element‐dependent transcription through the zinc finger protein Gis1 , 2000, The EMBO journal.

[76]  C. Sheu,et al.  Inhibitory Effects of Lipophilic Acids and Related Compounds on Bacteria and Mammalian Cells , 1975, Antimicrobial Agents and Chemotherapy.

[77]  T. Schmelzle,et al.  Activation of the RAS/Cyclic AMP Pathway Suppresses a TOR Deficiency in Yeast , 2004, Molecular and Cellular Biology.

[78]  D. Botstein,et al.  Genomic expression programs in the response of yeast cells to environmental changes. , 2000, Molecular biology of the cell.

[79]  Amber L. Mosley,et al.  Glucose-mediated Phosphorylation Converts the Transcription Factor Rgt1 from a Repressor to an Activator* , 2003, The Journal of Biological Chemistry.

[80]  M. Carlson,et al.  Sip5 interacts with both the Reg1/Glc7 protein phosphatase and the Snf1 protein kinase of Saccharomyces cerevisiae. , 2000, Genetics.

[81]  C. Michels,et al.  The Hsp90 Molecular Chaperone Complex Regulates Maltose Induction and Stability of the Saccharomyces MAL Gene Transcription Activator Mal63p* , 2003, Journal of Biological Chemistry.

[82]  C T Verrips,et al.  The role of ammonia metabolism in nitrogen catabolite repression in Saccharomyces cerevisiae. , 2000, FEMS microbiology reviews.

[83]  I. S. Mysyakina,et al.  Lipid Composition of the Arthrospores, Yeastlike Cells, and Mycelium of the Fungus Mucor hiemalis , 2001, Microbiology.

[84]  Michael N. Hall,et al.  Elucidating TOR Signaling and Rapamycin Action: Lessons from Saccharomyces cerevisiae , 2002, Microbiology and Molecular Biology Reviews.

[85]  R. Larossa,et al.  Amino acid biosynthetic enzymes as targets of herbicide action , 1984 .

[86]  J. Spinelli,et al.  Non-Hodgkin’s Lymphoma and Specific Pesticide Exposures in Men , 2001 .

[87]  Hans-Joachim Schüller,et al.  Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae , 2003, Current Genetics.

[88]  D. Klionsky,et al.  Autophagy in Yeast: Mechanistic Insights and Physiological Function , 2001, Microbiology and Molecular Biology Reviews.

[89]  A. Goffeau,et al.  Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants , 2000, FEBS letters.

[90]  Mehdi Mollapour,et al.  Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. , 2003, Molecular biology of the cell.