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Title: 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 » 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.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [5];  [6]
  1. Univ. of California, Los Angeles, CA (United States). Department of Chemistry and Biochemistry; Brookhaven National Lab. (BNL), Upton, NY (United States). Biology Department
  2. Sorbonne Universites, UPMC Univ., Paris (France); Laboratoire de Biologie Moleculaire et Cellulaire des Eucaryotes, Institut de Biologie Physico-Chimique, Paris (France); Instituto de Bioqui­mica Vegetal y Fotosi­ntesis, Consejo Superior de Investigaciones Cienti­ficas (CSIC)-Universidad de Sevilla, Seville (Spain)
  3. Univ. of California, Los Angeles, CA (United States). Department of Chemistry and Biochemistry
  4. Univ. of California, Los Angeles, CA (United States). Institute for Genomics and Proteomics
  5. Sorbonne Universites, UPMC Univ., Paris (France); Laboratoire de Biologie Moleculaire et Cellulaire des Eucaryotes, Institut de Biologie Physico-Chimique, Paris (France)
  6. 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}
}

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Proteome evolution under non-substitutable resource limitation
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