Transcriptome analysis reveals the oxidative stress response in Saccharomyces cerevisiae

The oxidation stress tolerance of Saccharomyces cerevisiae was improved by global transcription machinery engineering in our previous work. To explore the global perturbation induced by the mutant transcription factor Taf25, an RNA-Seq based gene expression analysis was conducted. Compared to the control strain, a total of 1006 genes with significantly differential expression levels were identified in the mutant strain taf25-3 upon oxidation stress. Fifteen transcription factor-encoding genes were determined, most of which displayed consistent up-regulated signature expressions in response to the challenge of 2 mM H2O2. Based on GO and KEGG enrichment analysis, the identified genes were involved in many metabolic pathways including carbon metabolism, fatty acid degradation, peroxisomal, and synthesis of several amino acids. The genes related to MAP kinase and cAMP-dependent protein kinase A (PKA) signaling pathways were also enriched significantly. The results suggested that the MAP kinase and PKA signaling pathways could be involved in mediation of yeast tolerance against oxidation stress, especially the mating regulation module in MAP kinase which could be reprogrammed by mutation of transcription factor Taf25 in yeast.

[1]  W. Cleland,et al.  Insight into the carboxyl transferase domain mechanism of pyruvate carboxylase from Rhizobium etli. , 2009, Biochemistry.

[2]  Z. Xue,et al.  Specialization of function among aldehyde dehydrogenases: the ALD2 and ALD3 genes are required for beta-alanine biosynthesis in Saccharomyces cerevisiae. , 2003, Genetics.

[3]  S. Hohmann.  Osmotic Stress Signaling and Osmoadaptation in Yeasts , 2002, Microbiology and Molecular Biology Reviews.

[4]  Nobuhiro Suzuki,et al.  Enhanced Tolerance to Environmental Stress in Transgenic Plants Expressing the Transcriptional Coactivator Multiprotein Bridging Factor 1c1[w] , 2005, Plant Physiology.

[5]  Hussein Mansour,et al.  Age Related Changes in NAD+ Metabolism Oxidative Stress and Sirt1 Activity in Wistar Rats , 2011, PloS one.

[6]  C. Rodrigues-Pousada,et al.  The S. cerevisiae Yap1 and Yap2 transcription factors share a common cadmium‐sensing domain , 2007, FEBS letters.

[7]  W. Huber,et al.  which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets , 2011 .

[8]  M. Frith,et al.  Incorporating sequence quality data into alignment improves DNA read mapping , 2010, Nucleic acids research.

[9]  S. Kuge,et al.  YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. , 1994, The EMBO journal.

[10]  Z. L. Liu,et al.  Comparative transcriptome profiling analyses during the lag phase uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as key regulatory genes in genomic adaptation to the lignocellulose derived inhibitor HMF for Saccharomyces cerevisiae , 2010, BMC Genomics.

[11]  B. Ylstra,et al.  Gene expression microarray analysis of heat stress in the soil invertebrate Folsomia candida , 2010, Insect molecular biology.

[12]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[13]  B. Williams,et al.  Mapping and quantifying mammalian transcriptomes by RNA-Seq , 2008, Nature Methods.

[14]  D. Šuput,et al.  Achieving the Balance between ROS and Antioxidants: When to Use the Synthetic Antioxidants , 2013, Oxidative medicine and cellular longevity.

[15]  E. Shumay,et al.  Successful expression of a functional yeast G-protein-coupled receptor (Ste2) in mammalian cells. , 2005, Biochemical and biophysical research communications.

[16]  Markus J. Tamás,et al.  Characterization of the DNA-binding motif of the arsenic-responsive transcription factor Yap8p. , 2008, Biochemical Journal.

[17]  T. Miyake,et al.  Mutations in the histone fold domain of the TAF12 gene show synthetic lethality with the TAF1 gene lacking the TAF N-terminal domain (TAND) by different mechanisms from those in the SPT15 gene encoding the TATA box-binding protein (TBP). , 2003, Nucleic acids research.

[18]  T. Bagnyukova,et al.  Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues. , 2005, The international journal of biochemistry & cell biology.

[19]  R. Edwards,et al.  A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. , 1999, The Plant journal : for cell and molecular biology.

[20]  P. Becker,et al.  Histone acetylation: a switch between repressive and permissive chromatin , 2002, EMBO reports.

[21]  V. Lobo,et al.  Free radicals, antioxidants and functional foods: Impact on human health , 2010, Pharmacognosy reviews.

[22]  Lawrence J. Marnett,et al.  Systems Analysis of Protein Modification and Cellular Responses Induced by Electrophile Stress , 2010, Accounts of chemical research.

[23]  Xiaojun Zhang,et al.  Experimental mapping of DNA duplex shape enabled by global lineshape analyses of a nucleotide-independent nitroxide probe , 2014, Nucleic acids research.

[24]  C. Grant,et al.  Metabolic reconfiguration is a regulated response to oxidative stress , 2008, Journal of biology.

[25]  C. Rodrigues-Pousada,et al.  The Yap family and its role in stress response , 2010, Yeast.

[26]  S. Brul,et al.  Yeast adaptation to weak acids prevents futile energy expenditure , 2013, Front. Microbiol..

[27]  N. Holbrook,et al.  Oxidants, oxidative stress and the biology of ageing , 2000, Nature.

[28]  D. E. Levin,et al.  Saccharomyces cerevisiae contains four fatty acid activation (FAA) genes: an assessment of their role in regulating protein N- myristoylation and cellular lipid metabolism , 1994, The Journal of cell biology.

[29]  C. Rodrigues-Pousada,et al.  The ABC transporter proteins Pat1 and Pat2 are required for import of long‐chain fatty acids into peroxisomes of Saccharomyces cerevisiae. , 1996, The EMBO journal.

[30]  Dongrong Chen,et al.  Multiple pathways differentially regulate global oxidative stress responses in fission yeast. , 2008, Molecular biology of the cell.

[31]  Chikara Furusawa,et al.  Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. , 2009, FEMS yeast research.

[32]  I. Nookaew,et al.  A comprehensive comparison of RNA-Seq-based transcriptome analysis from reads to differential gene expression and cross-comparison with microarrays: a case study in Saccharomyces cerevisiae , 2012, Nucleic acids research.

[33]  K. Yamamoto,et al.  Identification of TATA-binding Protein-free TAFII-containing Complex Subunits Suggests a Role in Nucleosome Acetylation and Signal Transduction* , 1999, The Journal of Biological Chemistry.

[34]  Stuart K. Kim,et al.  Ethanol-response genes and their regulation analyzed by a microarray and comparative genomic approach in the nematode Caenorhabditis elegans. , 2004, Genomics.

[35]  Yoav Benjamini,et al.  Identifying differentially expressed genes using false discovery rate controlling procedures , 2003, Bioinform..

[36]  Hongwei Zhao,et al.  Improvement of oxidative stress tolerance in Saccharomyces cerevisiae through global transcription machinery engineering , 2014, Journal of Industrial Microbiology & Biotechnology.

[37]  D. Laporte.  The isocitrate dehydrogenase phosphorylation cycle: Regulation and enzymology , 1993, Journal of cellular biochemistry.

[38]  Chuan-Yun Li,et al.  KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases , 2011, Nucleic Acids Res..

[39]  C. Widmann,et al.  Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. , 1999, Physiological reviews.

[40]  J. Aitchison,et al.  Proteomics of the peroxisome. , 2006, Biochimica et biophysica acta.

[41]  K. Smolková,et al.  The Role of Mitochondrial NADPH-Dependent Isocitrate Dehydrogenase in Cancer Cells , 2012, International journal of cell biology.

[42]  Brian C. Jackson,et al.  Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. , 2013, Free radical biology & medicine.

[43]  T. Shibasaki,et al.  PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. , 2005, Physiological reviews.

[44]  Y. Inoue,et al.  Oxidative stress response in yeast: effect of glutathione on adaptation to hydrogen peroxide stress in Saccharomyces cerevisiae , 1995, FEBS letters.

[45]  D. Dignard,et al.  Structure and transcriptional control of the Saccharomyces cerevisiae POX1 gene encoding acyl-coenzyme A oxidase. , 1990, Gene.

[46]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[47]  J. Kirchner,et al.  Molecular Genetic Dissection of TAF25, an Essential Yeast Gene Encoding a Subunit Shared by TFIID and SAGA Multiprotein Transcription Factors , 2001, Molecular and Cellular Biology.