Genome-wide analysis on Chlamydomonas reinhardtii reveals the impact of hydrogen peroxide on protein stress responses and overlap with other stress transcriptomes
Abstract
Reactive oxygen species (ROS) are produced by and have the potential to be damaging to all aerobic organisms. In photosynthetic organisms, they are an unavoidable byproduct of electron transfer in both the chloroplast and mitochondrion. Here, in this paper, we employ the reference unicellular green alga Chlamydomonas reinhardtii to identify the effect of H2O2 on gene expression by monitoring the changes in the transcriptome in a time-course experiment. Comparison of transcriptomes from cells sampled immediately prior to the addition of H2O2 and 0.5 and 1 h subsequently revealed 1278 differentially abundant transcripts. Of those transcripts that increase in abundance, many encode proteins involved in ROS detoxification, protein degradation and stress responses, whereas among those that decrease are transcripts encoding proteins involved in photosynthesis and central carbon metabolism. In addition to these transcriptomic adjustments, we observe that addition of H2O2 is followed by an accumulation and oxidation of the total intracellular glutathione pool, and a decrease in photosynthetic O2 output. Additionally, we analyze our transcriptomes in the context of changes in transcript abundance in response to singlet O2 (O2*), and relate our H2O2-induced transcripts to a diurnal transcriptome, where we demonstrate enrichments of H2O2-induced transcripts early in the light phase, latemore »
- Authors:
-
- Univ. of California, Los Angeles, CA (United States). Department of Chemistry and Biochemistry; Brookhaven National Lab. (BNL), Upton, NY (United States). Biology Department
- Sorbonne Universites, UPMC Univ., Paris (France); Laboratoire de Biologie Moleculaire et Cellulaire des Eucaryotes, Institut de Biologie Physico-Chimique, Paris (France); Instituto de BioquiÂmica Vegetal y FotosiÂntesis, Consejo Superior de Investigaciones CientiÂficas (CSIC)-Universidad de Sevilla, Seville (Spain)
- Univ. of California, Los Angeles, CA (United States). Department of Chemistry and Biochemistry
- Univ. of California, Los Angeles, CA (United States). Institute for Genomics and Proteomics
- Sorbonne Universites, UPMC Univ., Paris (France); Laboratoire de Biologie Moleculaire et Cellulaire des Eucaryotes, Institut de Biologie Physico-Chimique, Paris (France)
- Univ. of California, Los Angeles, CA (United States). Department of Chemistry and Biochemistry; Univ. of California, Los Angeles, CA (United States). Institute for Genomics and Proteomics
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1335416
- Report Number(s):
- BNL-111999-2016-JA
Journal ID: ISSN 0960-7412
- Grant/Contract Number:
- SC0012704; FD02-04ER15529
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Volume: 84; Journal Issue: 5; Journal ID: ISSN 0960-7412
- Publisher:
- Society for Experimental Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; algae; H2O2; RNA-seq; transcriptome; oxidative stress; stress responses; redox signaling; reactive oxygen species
Citation Formats
Blaby, Ian K., Blaby-Haas, Crysten E., Pérez-Pérez, María Esther, Schmollinger, Stefan, Fitz-Gibbon, Sorel, Lemaire, Stéphane D., and Merchant, Sabeeha S. Genome-wide analysis on Chlamydomonas reinhardtii reveals the impact of hydrogen peroxide on protein stress responses and overlap with other stress transcriptomes. United States: N. p., 2015.
Web. doi:10.1111/tpj.13053.
Blaby, Ian K., Blaby-Haas, Crysten E., Pérez-Pérez, María Esther, Schmollinger, Stefan, Fitz-Gibbon, Sorel, Lemaire, Stéphane D., & Merchant, Sabeeha S. Genome-wide analysis on Chlamydomonas reinhardtii reveals the impact of hydrogen peroxide on protein stress responses and overlap with other stress transcriptomes. United States. https://doi.org/10.1111/tpj.13053
Blaby, Ian K., Blaby-Haas, Crysten E., Pérez-Pérez, María Esther, Schmollinger, Stefan, Fitz-Gibbon, Sorel, Lemaire, Stéphane D., and Merchant, Sabeeha S. Mon .
"Genome-wide analysis on Chlamydomonas reinhardtii reveals the impact of hydrogen peroxide on protein stress responses and overlap with other stress transcriptomes". United States. https://doi.org/10.1111/tpj.13053. https://www.osti.gov/servlets/purl/1335416.
@article{osti_1335416,
title = {Genome-wide analysis on Chlamydomonas reinhardtii reveals the impact of hydrogen peroxide on protein stress responses and overlap with other stress transcriptomes},
author = {Blaby, Ian K. and Blaby-Haas, Crysten E. and Pérez-Pérez, María Esther and Schmollinger, Stefan and Fitz-Gibbon, Sorel and Lemaire, Stéphane D. and Merchant, Sabeeha S.},
abstractNote = {Reactive oxygen species (ROS) are produced by and have the potential to be damaging to all aerobic organisms. In photosynthetic organisms, they are an unavoidable byproduct of electron transfer in both the chloroplast and mitochondrion. Here, in this paper, we employ the reference unicellular green alga Chlamydomonas reinhardtii to identify the effect of H2O2 on gene expression by monitoring the changes in the transcriptome in a time-course experiment. Comparison of transcriptomes from cells sampled immediately prior to the addition of H2O2 and 0.5 and 1 h subsequently revealed 1278 differentially abundant transcripts. Of those transcripts that increase in abundance, many encode proteins involved in ROS detoxification, protein degradation and stress responses, whereas among those that decrease are transcripts encoding proteins involved in photosynthesis and central carbon metabolism. In addition to these transcriptomic adjustments, we observe that addition of H2O2 is followed by an accumulation and oxidation of the total intracellular glutathione pool, and a decrease in photosynthetic O2 output. Additionally, we analyze our transcriptomes in the context of changes in transcript abundance in response to singlet O2 (O2*), and relate our H2O2-induced transcripts to a diurnal transcriptome, where we demonstrate enrichments of H2O2-induced transcripts early in the light phase, late in the light phase and 2 h prior to light. In conclusion, on this basis several genes that are highlighted in this work may be involved in previously undiscovered stress remediation pathways or acclimation responses.},
doi = {10.1111/tpj.13053},
journal = {The Plant Journal},
number = 5,
volume = 84,
place = {United States},
year = {Mon Dec 07 00:00:00 EST 2015},
month = {Mon Dec 07 00:00:00 EST 2015}
}
Web of Science
Works referenced in this record:
Reactive oxygen species and transcript analysis upon excess light treatment in wild-type Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein
journal, January 2011
- Alboresi, Alessandro; Dall'Osto, Luca; Aprile, Alessio
- BMC Plant Biology, Vol. 11, Issue 1
A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli.
journal, December 1992
- Almiron, M.; Link, A. J.; Furlong, D.
- Genes & Development, Vol. 6, Issue 12b
REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction
journal, June 2004
- Apel, Klaus; Hirt, Heribert
- Annual Review of Plant Biology, Vol. 55, Issue 1
Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant
journal, November 2013
- Blaby, I. K.; Glaesener, A. G.; Mettler, T.
- The Plant Cell, Vol. 25, Issue 11
The Chlamydomonas genome project: a decade on
journal, October 2014
- Blaby, Ian K.; Blaby-Haas, Crysten E.; Tourasse, Nicolas
- Trends in Plant Science, Vol. 19, Issue 10
Systems Biology Approach in Chlamydomonas Reveals Connections between Copper Nutrition and Multiple Metabolic Steps
journal, April 2011
- Castruita, Madeli; Casero, David; Karpowicz, Steven J.
- The Plant Cell, Vol. 23, Issue 4
Degradation of oxidized proteins by the 20S proteasome
journal, March 2001
- Davies, Kelvin J. A.
- Biochimie, Vol. 83, Issue 3-4
The Peroxiredoxin and Glutathione Peroxidase Families in Chlamydomonas reinhardtii
journal, May 2008
- Dayer, Régine; Fischer, Beat B.; Eggen, Rik I. L.
- Genetics, Vol. 179, Issue 1
20S proteasome activity is modified via S-glutathionylation based on intracellular redox status of the yeast Saccharomyces cerevisiae: Implications for the degradation of oxidized proteins
journal, September 2014
- Demasi, Marilene; Hand, Adrian; Ohara, Erina
- Archives of Biochemistry and Biophysics, Vol. 557
Target of rapamycin (TOR): balancing the opposing forces of protein synthesis and degradation
journal, February 1999
- Dennis, Patrick B.; Fumagalli, Stefano; Thomas, George
- Current Opinion in Genetics & Development, Vol. 9, Issue 1
Hydrogen peroxide–induced gene expression in Arabidopsis thaliana
journal, March 2000
- Desikan, Radhika; Neill, Steven J.; Hancock, John T.
- Free Radical Biology and Medicine, Vol. 28, Issue 5
Regulation of the Arabidopsis Transcriptome by Oxidative Stress
journal, September 2001
- Desikan, Radhika; A. -H. -Mackerness, Soheila; Hancock, John T.
- Plant Physiology, Vol. 127, Issue 1
STAR: ultrafast universal RNA-seq aligner
journal, October 2012
- Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix
- Bioinformatics, Vol. 29, Issue 1
Role of the iron mobilization and oxidative stress regulons in the genomic response of yeast to hydroxyurea
journal, December 2005
- Dubacq, Caroline; Chevalier, Anne; Courbeyrette, Régis
- Molecular Genetics and Genomics, Vol. 275, Issue 2
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
Oxidative stress induced by the photosensitizers neutral red (type I) or rose bengal (type II) in the light causes different molecular responses in Chlamydomonas reinhardtii
journal, March 2005
- Fischer, Beat B.; Krieger-Liszkay, Anja; Eggen, Rik I. L.
- Plant Science, Vol. 168, Issue 3
Function and regulation of the glutathione peroxidase homologous gene GPXH/GPX5 in Chlamydomonas reinhardtii
journal, August 2009
- Fischer, Beat B.; Dayer, Régine; Schwarzenbach, Yvonne
- Plant Molecular Biology, Vol. 71, Issue 6
Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications
journal, April 2009
- Foyer, Christine H.; Noctor, Graham
- Antioxidants & Redox Signaling, Vol. 11, Issue 4
Genome wide analysis of common and specific stress responses in adult drosophila melanogaster
journal, September 2004
- Girardot, Fabrice; Monnier, Véronique; Tricoire, Hervé
- BMC Genomics, Vol. 5, Issue 1
RNA-Seq Analysis of Sulfur-Deprived Chlamydomonas Cells Reveals Aspects of Acclimation Critical for Cell Survival
journal, June 2010
- González-Ballester, David; Casero, David; Cokus, Shawn
- The Plant Cell, Vol. 22, Issue 6
The Path to Triacylglyceride Obesity in the sta6 Strain of Chlamydomonas reinhardtii
journal, February 2014
- Goodenough, Ursula; Blaby, Ian; Casero, David
- Eukaryotic Cell, Vol. 13, Issue 5
Hydrogen peroxide: a Jekyll and Hyde signalling molecule
journal, October 2011
- Gough, D. R.; Cotter, T. G.
- Cell Death & Disease, Vol. 2, Issue 10
Vitamin E Protects against Photoinhibition and Photooxidative Stress in Arabidopsis thaliana
journal, October 2005
- Havaux, Michel; Eymery, Françoise; Porfirova, Svetlana
- The Plant Cell, Vol. 17, Issue 12
The GreenCut: re-evaluation of physiological role of previously studied proteins and potential novel protein functions
journal, July 2013
- Heinnickel, Mark L.; Grossman, Arthur R.
- Photosynthesis Research, Vol. 116, Issue 2-3
COPPER RESPONSE REGULATOR1–Dependent and –Independent Responses of the Chlamydomonas reinhardtii Transcriptome to Dark Anoxia
journal, September 2013
- Hemschemeier, Anja; Casero, David; Liu, Bensheng
- The Plant Cell, Vol. 25, Issue 9
Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate: Role of the Suf system during oxidative stress
journal, October 2010
- Jang, Soojin; Imlay, James A.
- Molecular Microbiology, Vol. 78, Issue 6
Role of sulfiredoxin as a regulator of peroxiredoxin function and regulation of its expression
journal, August 2012
- Jeong, Woojin; Bae, Soo Han; Toledano, Michel B.
- Free Radical Biology and Medicine, Vol. 53, Issue 3
The BAG proteins: a ubiquitous family of chaperone regulators
journal, February 2008
- Kabbage, M.; Dickman, M. B.
- Cellular and Molecular Life Sciences, Vol. 65, Issue 9
AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants
journal, July 2005
- Kang, C. H.; Jung, W. Y.; Kang, Y. H.
- Cell Death & Differentiation, Vol. 13, Issue 1
The GreenCut2 Resource, a Phylogenomically Derived Inventory of Proteins Specific to the Plant Lineage
journal, April 2011
- Karpowicz, Steven J.; Prochnik, Simon E.; Grossman, Arthur R.
- Journal of Biological Chemistry, Vol. 286, Issue 24
Response to Oxidative Stress Involves a Novel Peroxiredoxin Gene in the Unicellular Cyanobacterium Synechocystis sp. PCC 6803
journal, March 2004
- Kobayashi, Mari; Ishizuka, Tomokazu; Katayama, Mitsunori
- Plant and Cell Physiology, Vol. 45, Issue 3
CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses
journal, October 2012
- Lai, A. G.; Doherty, C. J.; Mueller-Roeber, B.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 42
Acclimation to Singlet Oxygen Stress in Chlamydomonas reinhardtii
journal, April 2007
- Ledford, Heidi K.; Chin, Brian L.; Niyogi, Krishna K.
- Eukaryotic Cell, Vol. 6, Issue 6
Glutathione synthesis
journal, May 2013
- Lu, Shelly C.
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1830, Issue 5
Zinc Deficiency Impacts CO 2 Assimilation and Disrupts Copper Homeostasis in Chlamydomonas reinhardtii
journal, February 2013
- Malasarn, Davin; Kropat, Janette; Hsieh, Scott I.
- Journal of Biological Chemistry, Vol. 288, Issue 15
The Many Faces of Glutathione in Bacteria
journal, May 2006
- Masip, Lluis; Veeravalli, Karthik; Georgiou, George
- Antioxidants & Redox Signaling, Vol. 8, Issue 5-6
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions
journal, October 2007
- Merchant, S. S.; Prochnik, S. E.; Vallon, O.
- Science, Vol. 318, Issue 5848, p. 245-250
Down-regulation of catalase activity allows transient accumulation of a hydrogen peroxide signal in Chlamydomonas reinhardtii: Hydrogen peroxide signalling in C . reinhardtii
journal, January 2013
- Michelet, Laure; Roach, Thomas; Fischer, Beat B.
- Plant, Cell & Environment, Vol. 36, Issue 6
Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress
journal, February 2004
- Mostertz, J.
- Microbiology, Vol. 150, Issue 2
Organization, function and substrates of the essential Clp protease system in plastids
journal, September 2015
- Nishimura, Kenji; van Wijk, Klaas J.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 9
Glutathione in plants: an integrated overview: Glutathione status and functions
journal, August 2011
- Noctor, Graham; Mhamdi, Amna; Chaouch, Sejir
- Plant, Cell & Environment, Vol. 35, Issue 2
Ferrous ion oxidation in presence of xylenol orange for detection of lipid hydroperoxides in plasma
book, January 1999
- Nourooz-Zadeh, Jaffar
- Methods in Enzymology
Pond Scum Genomics: The Genomes of Chlamydomonas and Ostreococcus
journal, March 2008
- Peers, Graham; Niyogi, Krishna K.
- The Plant Cell, Vol. 20, Issue 3
Dps/Dpr ferritin-like protein: insights into the mechanism of iron incorporation and evidence for a central role in cellular iron homeostasis in Streptococcus suis: Iron incorporation by Streptococcus suis Dps/Dpr
journal, July 2005
- Pulliainen, Arto T.; Kauko, Anni; Haataja, Sauli
- Molecular Microbiology, Vol. 57, Issue 4
A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: Application to redox profiling during Arabidopsis rosette development
journal, April 2007
- Queval, Guillaume; Noctor, Graham
- Analytical Biochemistry, Vol. 363, Issue 1
H2O2-Activated Up-Regulation of Glutathione in Arabidopsis Involves Induction of Genes Encoding Enzymes Involved in Cysteine Synthesis in the Chloroplast
journal, March 2009
- Queval, Guillaume; Thominet, Dorothée; Vanacker, Hélène
- Molecular Plant, Vol. 2, Issue 2
Conditional Depletion of the Chlamydomonas Chloroplast ClpP Protease Activates Nuclear Genes Involved in Autophagy and Plastid Protein Quality Control
journal, May 2014
- Ramundo, Silvia; Casero, David; Mühlhaus, Timo
- The Plant Cell, Vol. 26, Issue 5
Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism
journal, April 2014
- Schmollinger, Stefan; Mühlhaus, Timo; Boyle, Nanette R.
- The Plant Cell, Vol. 26, Issue 4
Chemistry and biology of vitamin E
journal, January 2005
- Schneider, Claus
- Molecular Nutrition & Food Research, Vol. 49, Issue 1
Spatial H2O2 Signaling Specificity: H2O2 from Chloroplasts and Peroxisomes Modulates the Plant Transcriptome Differentially
journal, July 2014
- Sewelam, Nasser; Jaspert, Nils; Van Der Kelen, Katrien
- Molecular Plant, Vol. 7, Issue 7
Photosynthetic electron flow affects H2O2 signaling by inactivation of catalase in Chlamydomonas reinhardtii
journal, September 2008
- Shao, Ning; Beck, Christoph F.; Lemaire, Stéphane D.
- Planta, Vol. 228, Issue 6
Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese
journal, March 2011
- Sobota, J. M.; Imlay, J. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
A nuclear gene of Chlamydomonas reinhardtii, Tba1, encodes a putative oxidoreductase required for translation of the chloroplast psbA mRNA: Translational activator of D1 protein
journal, March 2005
- Somanchi, Aravind; Barnes, Dwight; Mayfield, Stephen P.
- The Plant Journal, Vol. 42, Issue 3
Hydrogen Peroxide: A Signaling Messenger
journal, March 2006
- Stone, James R.; Yang, Suping
- Antioxidants & Redox Signaling, Vol. 8, Issue 3-4
Resistance of Photosynthesis to Hydrogen Peroxide in Algae
journal, September 1995
- Takeda, Toru; Yokota, Akiho; Shigeoka, Shigeru
- Plant and Cell Physiology, Vol. 36, Issue 6
Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues
journal, March 1969
- Tietze, Frank
- Analytical Biochemistry, Vol. 27, Issue 3
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
journal, May 2010
- Trapnell, Cole; Williams, Brian A.; Pertea, Geo
- Nature Biotechnology, Vol. 28, Issue 5
Impact of Oxidative Stress on Ascorbate Biosynthesis in Chlamydomonas via Regulation of the VTC2 Gene Encoding a GDP-l-galactose Phosphorylase
journal, March 2012
- Urzica, Eugen I.; Adler, Lital N.; Page, M. Dudley
- Journal of Biological Chemistry, Vol. 287, Issue 17
Systems and Trans -System Level Analysis Identifies Conserved Iron Deficiency Responses in the Plant Lineage
journal, October 2012
- Urzica, Eugen I.; Casero, David; Yamasaki, Hiroaki
- The Plant Cell, Vol. 24, Issue 10
A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco
journal, December 2003
- Vandenabeele, S.; Van Der Kelen, K.; Dat, J.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 26
Hydrogen Peroxide-Induced Gene Expression across Kingdoms: A Comparative Analysis
journal, January 2008
- Vandenbroucke, K.; Robbens, S.; Vandepoele, K.
- Molecular Biology and Evolution, Vol. 25, Issue 3
Phosphoprotein SAK1 is a regulator of acclimation to singlet oxygen in Chlamydomonas reinhardtii
journal, May 2014
- Wakao, Setsuko; Chin, Brian L.; Ledford, Heidi K.
- eLife, Vol. 3
Fenton's reagent revisited
journal, April 1975
- Walling, Cheves
- Accounts of Chemical Research, Vol. 8, Issue 4
GSH1, which encodes gamma-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation.
journal, September 1994
- Wu, A. L.; Moye-Rowley, W. S.
- Molecular and Cellular Biology, Vol. 14, Issue 9
Retained duplicate genes in green alga Chlamydomonas reinhardtii tend to be stress responsive and experience frequent response gains
journal, January 2015
- Wu, Guangxi; Hufnagel, David E.; Denton, Alisandra K.
- BMC Genomics, Vol. 16, Issue 1
Roles of xanthophyll carotenoids in protection against photoinhibition and oxidative stress in the cyanobacterium Synechococcus sp. strain PCC 7002
journal, December 2010
- Zhu, Yuehui; Graham, Joel E.; Ludwig, Marcus
- Archives of Biochemistry and Biophysics, Vol. 504, Issue 1
Photosynthetic electron flow affects H2O2 signaling by inactivation of catalase in Chlamydomonas reinhardtii
journal, September 2008
- Shao, Ning; Beck, Christoph F.; Lemaire, Stéphane D.
- Planta, Vol. 228, Issue 6
Function and regulation of the glutathione peroxidase homologous gene GPXH/GPX5 in Chlamydomonas reinhardtii
journal, August 2009
- Fischer, Beat B.; Dayer, Régine; Schwarzenbach, Yvonne
- Plant Molecular Biology, Vol. 71, Issue 6
The GreenCut: re-evaluation of physiological role of previously studied proteins and potential novel protein functions
journal, July 2013
- Heinnickel, Mark L.; Grossman, Arthur R.
- Photosynthesis Research, Vol. 116, Issue 2-3
A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: Application to redox profiling during Arabidopsis rosette development
journal, April 2007
- Queval, Guillaume; Noctor, Graham
- Analytical Biochemistry, Vol. 363, Issue 1
Oxidative stress induced by the photosensitizers neutral red (type I) or rose bengal (type II) in the light causes different molecular responses in Chlamydomonas reinhardtii
journal, March 2005
- Fischer, Beat B.; Krieger-Liszkay, Anja; Eggen, Rik I. L.
- Plant Science, Vol. 168, Issue 3
The Chlamydomonas genome project: a decade on
journal, October 2014
- Blaby, Ian K.; Blaby-Haas, Crysten E.; Tourasse, Nicolas
- Trends in Plant Science, Vol. 19, Issue 10
Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese
journal, March 2011
- Sobota, J. M.; Imlay, J. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses
journal, October 2012
- Lai, A. G.; Doherty, C. J.; Mueller-Roeber, B.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 42
A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco
journal, December 2003
- Vandenabeele, S.; Van Der Kelen, K.; Dat, J.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 26
Mononuclear Iron Enzymes Are Primary Targets of Hydrogen Peroxide Stress
journal, March 2012
- Anjem, Adil; Imlay, James A.
- Journal of Biological Chemistry, Vol. 287, Issue 19
The Many Faces of Glutathione in Bacteria
journal, May 2006
- Masip, Lluis; Veeravalli, Karthik; Georgiou, George
- Antioxidants & Redox Signaling, Vol. 8, Issue 5-6
Global Transcriptional Responses of Fission Yeast to Environmental Stress
journal, January 2003
- Chen, Dongrong; Toone, W. Mark; Mata, Juan
- Molecular Biology of the Cell, Vol. 14, Issue 1
H2O2-Activated Up-Regulation of Glutathione in Arabidopsis Involves Induction of Genes Encoding Enzymes Involved in Cysteine Synthesis in the Chloroplast
journal, March 2009
- Queval, Guillaume; Thominet, Dorothée; Vanacker, Hélène
- Molecular Plant, Vol. 2, Issue 2
Resistance of Photosynthesis to Hydrogen Peroxide in Algae
journal, September 1995
- Takeda, Toru; Yokota, Akiho; Shigeoka, Shigeru
- Plant and Cell Physiology, Vol. 36, Issue 6
Regulation of the Arabidopsis Transcriptome by Oxidative Stress
journal, September 2001
- Desikan, Radhika; A. -H. -Mackerness, Soheila; Hancock, John T.
- Plant Physiology, Vol. 127, Issue 1
Pond Scum Genomics: The Genomes of Chlamydomonas and Ostreococcus
journal, March 2008
- Peers, Graham; Niyogi, Krishna K.
- The Plant Cell, Vol. 20, Issue 3
RNA-Seq Analysis of Sulfur-Deprived Chlamydomonas Cells Reveals Aspects of Acclimation Critical for Cell Survival
journal, June 2010
- González-Ballester, David; Casero, David; Cokus, Shawn
- The Plant Cell, Vol. 22, Issue 6
Transcriptome and Physiological Responses to Hydrogen Peroxide of the Facultatively Phototrophic Bacterium Rhodobacter sphaeroides
journal, October 2005
- Zeller, T.; Moskvin, O. V.; Li, K.
- Journal of Bacteriology, Vol. 187, Issue 21
GSH1, Which Encodes γ-Glutamylcysteine Synthetase, Is a Target Gene for yAP-1 Transcriptional Regulation
journal, September 1994
- Wu, Ai Ling; Moye-Rowley, W. Scott
- Molecular and Cellular Biology, Vol. 14, Issue 9
Reactive oxygen species and transcript analysis upon excess light treatment in wild-type Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein
journal, January 2011
- Alboresi, Alessandro; Dall'Osto, Luca; Aprile, Alessio
- BMC Plant Biology, Vol. 11, Issue 1
Retained duplicate genes in green alga Chlamydomonas reinhardtii tend to be stress responsive and experience frequent response gains
journal, January 2015
- Wu, Guangxi; Hufnagel, David E.; Denton, Alisandra K.
- BMC Genomics, Vol. 16, Issue 1
Clinical holding of children and young people
book, November 2009
- Brenner, Maria; Noctor, Colman
- Developing Practical Skills for Nursing Children and Young People
The Peroxiredoxin and Glutathione Peroxidase Families in Chlamydomonas reinhardtii
journal, May 2008
- Dayer, Régine; Fischer, Beat B.; Eggen, Rik I. L.
- Genetics, Vol. 179, Issue 1
Works referencing / citing this record:
Proteome evolution under non-substitutable resource limitation
journal, November 2018
- Tamminen, Manu; Betz, Alexander; Pereira, Aaron Louis
- Nature Communications, Vol. 9, Issue 1
Chloroplast function revealed through analysis of GreenCut2 genes
journal, March 2017
- Fristedt, Rikard
- Journal of Experimental Botany, Vol. 68, Issue 9
Proteome evolution under non-substitutable resource limitation
text, January 2018
- Tamminen, Manu; Betz, Alexander; Pereira, Aaron L.
- ETH Zurich
Proteome evolution under non-substitutable resource limitation
text, January 2018
- Tamminen, Manu; Betz, Alexander; Pereira, Aaron L.
- ETH Zurich