DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Identification of regulatory network hubs that control lipid metabolism in Chlamydomonas reinhardtii

Abstract

Microalgae-based biofuels are promising sources of alternative energy, but improvements throughout the production process are required to establish them as economically feasible. One of the most influential improvements would be a significant increase in lipid yields, which could be achieved by altering the regulation of lipid biosynthesis and accumulation. Chlamydomonas reinhardtii accumulates oil (triacylglycerols, TAG) in response to nitrogen (N) deprivation. Although a few important regulatory genes have been identified that are involved in controlling this process, a global understanding of the larger regulatory network has not been developed. In order to uncover this network in this species, a combined omics (transcriptomic, proteomic and metabolomic) analysis was applied to cells grown in a time course experiment after a shift from N-replete to N-depleted conditions. Changes in transcript and protein levels of 414 predicted transcription factors (TFs) and transcriptional regulators (TRs) were monitored relative to other genes. The TF and TR genes were thus classified by two separate measures: up-regulated versus down-regulated and early response versus late response relative to two phases of polar lipid synthesis (before and after TAG biosynthesis initiation). Lipidomic and primary metabolite profiling generated compound accumulation levels that were integrated with the transcript dataset and TF profilingmore » to produce a transcriptional regulatory network. In conclusion, evaluation of this proposed regulatory network led to the identification of several regulatory hubs that control many aspects of cellular metabolism, from N assimilation and metabolism, to central metabolism, photosynthesis and lipid metabolism.« less

Authors:
 [1];  [1];  [2];  [1];  [3];  [4];  [4];  [5];  [1]
  1. Washington State Univ., Pullman, WA (United States)
  2. New Mexico State Univ., Las Cruces, NM (United States)
  3. Donald Danforth Plant Science Center, St. Louis, MO (United States); National Center of Biomedical Analysis, Beijing (China)
  4. Michigan State Univ., East Lansing, MI (United States)
  5. Donald Danforth Plant Science Center, St. Louis, MO (United States); Univ. of North Carolina, Chapel Hill, NC (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Advanced Biofuel Systems (CABS); Washington State Univ., Pullman, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1343282
Grant/Contract Number:  
SC0001295
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Volume: 66; Journal Issue: 15; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; biofuel; Chlamydomonas reinhardtii; metabolomics; network analysis; proteomics; regulatory hubs; RNA-seq; transcription factors; transcriptional regulators

Citation Formats

Gargouri, Mahmoud, Park, Jeong -Jin, Holguin, F. Omar, Kim, Min -Jeong, Wang, Hongxia, Deshpande, Rahul R., Shachar-Hill, Yair, Hicks, Leslie M., and Gang, David R. Identification of regulatory network hubs that control lipid metabolism in Chlamydomonas reinhardtii. United States: N. p., 2015. Web. doi:10.1093/jxb/erv217.
Gargouri, Mahmoud, Park, Jeong -Jin, Holguin, F. Omar, Kim, Min -Jeong, Wang, Hongxia, Deshpande, Rahul R., Shachar-Hill, Yair, Hicks, Leslie M., & Gang, David R. Identification of regulatory network hubs that control lipid metabolism in Chlamydomonas reinhardtii. United States. https://doi.org/10.1093/jxb/erv217
Gargouri, Mahmoud, Park, Jeong -Jin, Holguin, F. Omar, Kim, Min -Jeong, Wang, Hongxia, Deshpande, Rahul R., Shachar-Hill, Yair, Hicks, Leslie M., and Gang, David R. Thu . "Identification of regulatory network hubs that control lipid metabolism in Chlamydomonas reinhardtii". United States. https://doi.org/10.1093/jxb/erv217. https://www.osti.gov/servlets/purl/1343282.
@article{osti_1343282,
title = {Identification of regulatory network hubs that control lipid metabolism in Chlamydomonas reinhardtii},
author = {Gargouri, Mahmoud and Park, Jeong -Jin and Holguin, F. Omar and Kim, Min -Jeong and Wang, Hongxia and Deshpande, Rahul R. and Shachar-Hill, Yair and Hicks, Leslie M. and Gang, David R.},
abstractNote = {Microalgae-based biofuels are promising sources of alternative energy, but improvements throughout the production process are required to establish them as economically feasible. One of the most influential improvements would be a significant increase in lipid yields, which could be achieved by altering the regulation of lipid biosynthesis and accumulation. Chlamydomonas reinhardtii accumulates oil (triacylglycerols, TAG) in response to nitrogen (N) deprivation. Although a few important regulatory genes have been identified that are involved in controlling this process, a global understanding of the larger regulatory network has not been developed. In order to uncover this network in this species, a combined omics (transcriptomic, proteomic and metabolomic) analysis was applied to cells grown in a time course experiment after a shift from N-replete to N-depleted conditions. Changes in transcript and protein levels of 414 predicted transcription factors (TFs) and transcriptional regulators (TRs) were monitored relative to other genes. The TF and TR genes were thus classified by two separate measures: up-regulated versus down-regulated and early response versus late response relative to two phases of polar lipid synthesis (before and after TAG biosynthesis initiation). Lipidomic and primary metabolite profiling generated compound accumulation levels that were integrated with the transcript dataset and TF profiling to produce a transcriptional regulatory network. In conclusion, evaluation of this proposed regulatory network led to the identification of several regulatory hubs that control many aspects of cellular metabolism, from N assimilation and metabolism, to central metabolism, photosynthesis and lipid metabolism.},
doi = {10.1093/jxb/erv217},
journal = {Journal of Experimental Botany},
number = 15,
volume = 66,
place = {United States},
year = {Thu May 28 00:00:00 EDT 2015},
month = {Thu May 28 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 80 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Nitrate Signaling by the Regulatory Gene NIT2 in Chlamydomonas
journal, November 2007

  • Camargo, Antonio; Llamas, Ángel; Schnell, Rogene A.
  • The Plant Cell, Vol. 19, Issue 11
  • DOI: 10.1105/tpc.106.045922

Differential Regulation of the Chlamydomonas Nar1 Gene Family by Carbon and Nitrogen
journal, October 2006


Error and attack tolerance of complex networks
journal, July 2000

  • Albert, Réka; Jeong, Hawoong; Barabási, Albert-László
  • Nature, Vol. 406, Issue 6794
  • DOI: 10.1038/35019019

Three Acyltransferases and Nitrogen-responsive Regulator Are Implicated in Nitrogen Starvation-induced Triacylglycerol Accumulation in Chlamydomonas
journal, March 2012

  • Boyle, Nanette R.; Page, Mark Dudley; Liu, Bensheng
  • Journal of Biological Chemistry, Vol. 287, Issue 19
  • DOI: 10.1074/jbc.M111.334052

The FHA domain
journal, December 2001


Comprehensive Comparison of iTRAQ and Label-free LC-Based Quantitative Proteomics Approaches Using Two Chlamydomonas reinhardtii Strains of Interest for Biofuels Engineering
journal, December 2011

  • Wang, Hongxia; Alvarez, Sophie; Hicks, Leslie M.
  • Journal of Proteome Research, Vol. 11, Issue 1
  • DOI: 10.1021/pr2008225

Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability
journal, April 2001

  • Fukuzawa, H.; Miura, K.; Ishizaki, K.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 9
  • DOI: 10.1073/pnas.081593498

The PHD finger, a nuclear protein-interaction domain
journal, January 2006


ABA-Dependent and -Independent G-Protein Signaling in Arabidopsis Roots Revealed through an iTRAQ Proteomics Approach
journal, July 2011

  • Alvarez, Sophie; Hicks, Leslie M.; Pandey, Sona
  • Journal of Proteome Research, Vol. 10, Issue 7
  • DOI: 10.1021/pr2001786

Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene
journal, September 2007

  • Karaba, A.; Dixit, S.; Greco, R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 39
  • DOI: 10.1073/pnas.0707294104

Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants
journal, January 2004


Mapping and quantifying mammalian transcriptomes by RNA-Seq
journal, May 2008

  • Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth
  • Nature Methods, Vol. 5, Issue 7, p. 621-628
  • DOI: 10.1038/nmeth.1226

An ancient light-harvesting protein is critical for the regulation of algal photosynthesis
journal, November 2009

  • Peers, Graham; Truong, Thuy B.; Ostendorf, Elisabeth
  • Nature, Vol. 462, Issue 7272
  • DOI: 10.1038/nature08587

High quality metabolomic data for Chlamydomonas reinhardtii
journal, January 2008


A Galactoglycerolipid Lipase Is Required for Triacylglycerol Accumulation and Survival Following Nitrogen Deprivation in Chlamydomonas reinhardtii
journal, November 2012

  • Li, Xiaobo; Moellering, Eric R.; Liu, Bensheng
  • The Plant Cell, Vol. 24, Issue 11
  • DOI: 10.1105/tpc.112.105106

Gametogenesis in the Chlamydomonas reinhardtii minus Mating Type Is Controlled by Two Genes, MID and MTD1
journal, April 2007


Detection and interpretation of metabolite–transcript coresponses using combined profiling data
journal, June 2011


Evidence for cross-pathway regulation of metabolic gene expression in plants.
journal, May 1995

  • Guyer, D.; Patton, D.; Ward, E.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 11
  • DOI: 10.1073/pnas.92.11.4997

Phytozome: a comparative platform for green plant genomics
journal, November 2011

  • Goodstein, David M.; Shu, Shengqiang; Howson, Russell
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr944

Exploiting diversity and synthetic biology for the production of algal biofuels
journal, August 2012

  • Georgianna, D. Ryan; Mayfield, Stephen P.
  • Nature, Vol. 488, Issue 7411
  • DOI: 10.1038/nature11479

Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA
journal, December 2003


Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation
journal, November 1998


Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response
journal, May 2005

  • Nikiforova, Victoria J.; Daub, Carsten O.; Hesse, Holger
  • Journal of Experimental Botany, Vol. 56, Issue 417
  • DOI: 10.1093/jxb/eri179

Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses
journal, November 2008

  • Saibo, Nelson J. M.; Lourenço, Tiago; Oliveira, Maria Margarida
  • Annals of Botany, Vol. 103, Issue 4
  • DOI: 10.1093/aob/mcn227

Molybdoenzymes and molybdenum cofactor in plants
journal, August 2002

  • Mendel, R. R.
  • Journal of Experimental Botany, Vol. 53, Issue 375
  • DOI: 10.1093/jxb/erf038

Cysteine modification of a specific repressor protein controls the translational status of nucleus-encoded LHCII mRNAs in Chlamydomonas
journal, August 2009

  • Wobbe, L.; Blifernez, O.; Schwarz, C.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 32
  • DOI: 10.1073/pnas.0900670106

Physiology of starch storage in the monocellular alga Chlamydomonas reinhardtii
journal, January 1990


Transcriptome analysis of Chlamydomonas reinhardtii during the process of lipid accumulation
journal, April 2013


Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii
journal, May 2012

  • Fan, Jilian; Yan, Chengshi; Andre, Carl
  • Plant and Cell Physiology, Vol. 53, Issue 8
  • DOI: 10.1093/pcp/pcs082

Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth
journal, November 2013

  • Trentacoste, E. M.; Shrestha, R. P.; Smith, S. R.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 49
  • DOI: 10.1073/pnas.1309299110

Changes in Transcript Abundance in Chlamydomonas reinhardtii following Nitrogen Deprivation Predict Diversion of Metabolism
journal, October 2010

  • Miller, Rachel; Wu, Guangxi; Deshpande, Rahul R.
  • Plant Physiology, Vol. 154, Issue 4
  • DOI: 10.1104/pp.110.165159

Progress in plant metabolic engineering
journal, April 2004


The response of Chlamydomonas reinhardtii to nitrogen deprivation: a systems biology analysis
journal, February 2015

  • Park, Jeong-Jin; Wang, Hongxia; Gargouri, Mahmoud
  • The Plant Journal, Vol. 81, Issue 4
  • DOI: 10.1111/tpj.12747

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
  • DOI: 10.1105/tpc.113.122523

The SANT domain: a unique histone-tail-binding module?
journal, February 2004

  • Boyer, Laurie A.; Latek, Robert R.; Peterson, Craig L.
  • Nature Reviews Molecular Cell Biology, Vol. 5, Issue 2, p. 158-163
  • DOI: 10.1038/nrm1314

Metabolic Pathway Relationships Revealed by an Integrative Analysis of the Transcriptional and Metabolic Temperature Stress-Response Dynamics in Yeast
journal, June 2010

  • Walther, Dirk; Strassburg, Katrin; Durek, Pawel
  • OMICS: A Journal of Integrative Biology, Vol. 14, Issue 3
  • DOI: 10.1089/omi.2010.0010

Photorespiration: current status and approaches for metabolic engineering
journal, June 2010

  • Maurino, Veronica G.; Peterhansel, Christoph
  • Current Opinion in Plant Biology, Vol. 13, Issue 3
  • DOI: 10.1016/j.pbi.2010.01.006

Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant
journal, November 2013


The Evolutionary Origin of an Altruistic Gene
journal, May 2006

  • Nedelcu, Aurora M.; Michod, Richard E.
  • Molecular Biology and Evolution, Vol. 23, Issue 8
  • DOI: 10.1093/molbev/msl016

Disruption of the Arabidopsis CGI-58 homologue produces Chanarin–Dorfman-like lipid droplet accumulation in plants
journal, September 2010

  • James, Christopher N.; Horn, Patrick J.; Case, Charlene R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 41, p. 17833-17838
  • DOI: 10.1073/pnas.0911359107

Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria
journal, January 2012

  • Czarnecki, O.; Grimm, B.
  • Journal of Experimental Botany, Vol. 63, Issue 4
  • DOI: 10.1093/jxb/err437

SDG2-Mediated H3K4 Methylation Is Required for Proper Arabidopsis Root Growth and Development
journal, February 2013


The Role of bZIP Transcription Factors in Green Plant Evolution: Adaptive Features Emerging from Four Founder Genes
journal, August 2008

  • Corrêa, Luiz Gustavo Guedes; Riaño-Pachón, Diego Mauricio; Schrago, Carlos Guerra
  • PLoS ONE, Vol. 3, Issue 8
  • DOI: 10.1371/journal.pone.0002944

Structure and functions of the GNAT superfamily of acetyltransferases
journal, January 2005

  • Vetting, Matthew W.; S. de Carvalho, Luiz Pedro; Yu, Michael
  • Archives of Biochemistry and Biophysics, Vol. 433, Issue 1
  • DOI: 10.1016/j.abb.2004.09.003

Evolutionary and Temporal Dynamics of Transcriptional Regulatory Networks
book, January 2008


Analysis of Transcription Factor HY5 Genomic Binding Sites Revealed Its Hierarchical Role in Light Regulation of Development
journal, March 2007


Overlapping Photoprotective Function of Vitamin E and Carotenoids in Chlamydomonas
journal, November 2011

  • Li, Zhirong; Keasling, Jay D.; Niyogi, Krishna K.
  • Plant Physiology, Vol. 158, Issue 1
  • DOI: 10.1104/pp.111.181230

Zeaxanthin Accumulation in the Absence of a Functional Xanthophyll Cycle Protects Chlamydomonas reinhardtii from Photooxidative Stress
journal, March 2003

  • Baroli, Irene; Do, An D.; Yamane, Tomoko
  • The Plant Cell, Vol. 15, Issue 4
  • DOI: 10.1105/tpc.010405

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii
journal, December 2014

  • Juergens, Matthew T.; Deshpande, Rahul R.; Lucker, Ben F.
  • Plant Physiology, Vol. 167, Issue 2
  • DOI: 10.1104/pp.114.250530

RNA Interference Silencing of a Major Lipid Droplet Protein Affects Lipid Droplet Size in Chlamydomonas reinhardtii
journal, November 2009

  • Moellering, Eric R.; Benning, Christoph
  • Eukaryotic Cell, Vol. 9, Issue 1
  • DOI: 10.1128/EC.00203-09

Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning
journal, June 2011

  • Bourgis, F.; Kilaru, A.; Cao, X.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
  • DOI: 10.1073/pnas.1106502108

Amino Acid and Adenine Cross-pathway Regulation Act through the Same 5′-TGACTC-3′ Motif in the Yeast HIS7 Promoter
journal, November 1996

  • Springer, Christoph; Künzler, Markus; Balmelli, Tiziano
  • Journal of Biological Chemistry, Vol. 271, Issue 47
  • DOI: 10.1074/jbc.271.47.29637

An analysis of variance test for normality (complete samples)
journal, December 1965


Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas
journal, December 1999

  • Wykoff, D. D.; Grossman, A. R.; Weeks, D. P.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 26
  • DOI: 10.1073/pnas.96.26.15336

Measuring Skewness: A Forgotten Statistic?
journal, July 2011


An Analysis of Variance Test for Normality (Complete Samples)
journal, December 1965

  • Shapiro, S. S.; Wilk, M. B.
  • Biometrika, Vol. 52, Issue 3/4
  • DOI: 10.2307/2333709

Progress in plant metabolic engineering
journal, July 2001

  • Broun, P.; Somerville, C.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 16
  • DOI: 10.1073/pnas.171310598

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii
text, January 2015

  • Mahmoud, Gargouri,; Yair, Shachar-Hill,; Omar, Holguin, F.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/3v8s-ma76

Structure and functions of the GNAT superfamily of acetyltransferases
journal, January 2005

  • Vetting, Matthew W.; S. de Carvalho, Luiz Pedro; Yu, Michael
  • Archives of Biochemistry and Biophysics, Vol. 433, Issue 1
  • DOI: 10.1016/j.abb.2004.09.003

Progress in plant metabolic engineering
journal, April 2004


Differential Regulation of the Chlamydomonas Nar1 Gene Family by Carbon and Nitrogen
journal, October 2006


The PHD finger, a nuclear protein-interaction domain
journal, January 2006


Essential Role for the SANT Domain in the Functioning of Multiple Chromatin Remodeling Enzymes
journal, October 2002


Transcription factors: An overview
journal, December 1997


The oxidative pentose phosphate pathway: structure and organisation
journal, June 2003


ABA-Dependent and -Independent G-Protein Signaling in Arabidopsis Roots Revealed through an iTRAQ Proteomics Approach
journal, July 2011

  • Alvarez, Sophie; Hicks, Leslie M.; Pandey, Sona
  • Journal of Proteome Research, Vol. 10, Issue 7
  • DOI: 10.1021/pr2001786

Comprehensive Comparison of iTRAQ and Label-free LC-Based Quantitative Proteomics Approaches Using Two Chlamydomonas reinhardtii Strains of Interest for Biofuels Engineering
journal, December 2011

  • Wang, Hongxia; Alvarez, Sophie; Hicks, Leslie M.
  • Journal of Proteome Research, Vol. 11, Issue 1
  • DOI: 10.1021/pr2008225

Error and attack tolerance of complex networks
journal, July 2000

  • Albert, Réka; Jeong, Hawoong; Barabási, Albert-László
  • Nature, Vol. 406, Issue 6794
  • DOI: 10.1038/35019019

An ancient light-harvesting protein is critical for the regulation of algal photosynthesis
journal, November 2009

  • Peers, Graham; Truong, Thuy B.; Ostendorf, Elisabeth
  • Nature, Vol. 462, Issue 7272
  • DOI: 10.1038/nature08587

Exploiting diversity and synthetic biology for the production of algal biofuels
journal, August 2012

  • Georgianna, D. Ryan; Mayfield, Stephen P.
  • Nature, Vol. 488, Issue 7411
  • DOI: 10.1038/nature11479

Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene
journal, September 2007

  • Karaba, A.; Dixit, S.; Greco, R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 39
  • DOI: 10.1073/pnas.0707294104

Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth
journal, November 2013

  • Trentacoste, E. M.; Shrestha, R. P.; Smith, S. R.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 49
  • DOI: 10.1073/pnas.1309299110

Evidence for cross-pathway regulation of metabolic gene expression in plants.
journal, May 1995

  • Guyer, D.; Patton, D.; Ward, E.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 11
  • DOI: 10.1073/pnas.92.11.4997

Amino Acid and Adenine Cross-pathway Regulation Act through the Same 5′-TGACTC-3′ Motif in the Yeast HIS7 Promoter
journal, November 1996

  • Springer, Christoph; Künzler, Markus; Balmelli, Tiziano
  • Journal of Biological Chemistry, Vol. 271, Issue 47
  • DOI: 10.1074/jbc.271.47.29637

Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation
journal, November 1998


Measuring Skewness: A Forgotten Statistic?
journal, July 2011


Metabolic Pathway Relationships Revealed by an Integrative Analysis of the Transcriptional and Metabolic Temperature Stress-Response Dynamics in Yeast
journal, June 2010

  • Walther, Dirk; Strassburg, Katrin; Durek, Pawel
  • OMICS: A Journal of Integrative Biology, Vol. 14, Issue 3
  • DOI: 10.1089/omi.2010.0010

Detection and interpretation of metabolite–transcript coresponses using combined profiling data
journal, June 2011


Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA
journal, December 2003


Molybdoenzymes and molybdenum cofactor in plants
journal, August 2002

  • Mendel, R. R.
  • Journal of Experimental Botany, Vol. 53, Issue 375
  • DOI: 10.1093/jxb/erf038

Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response
journal, May 2005

  • Nikiforova, Victoria J.; Daub, Carsten O.; Hesse, Holger
  • Journal of Experimental Botany, Vol. 56, Issue 417
  • DOI: 10.1093/jxb/eri179

The Evolutionary Origin of an Altruistic Gene
journal, May 2006

  • Nedelcu, Aurora M.; Michod, Richard E.
  • Molecular Biology and Evolution, Vol. 23, Issue 8
  • DOI: 10.1093/molbev/msl016

Phytozome: a comparative platform for green plant genomics
journal, November 2011

  • Goodstein, David M.; Shu, Shengqiang; Howson, Russell
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr944

Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii
journal, May 2012

  • Fan, Jilian; Yan, Chengshi; Andre, Carl
  • Plant and Cell Physiology, Vol. 53, Issue 8
  • DOI: 10.1093/pcp/pcs082

Overlapping Photoprotective Function of Vitamin E and Carotenoids in Chlamydomonas
journal, November 2011

  • Li, Zhirong; Keasling, Jay D.; Niyogi, Krishna K.
  • Plant Physiology, Vol. 158, Issue 1
  • DOI: 10.1104/pp.111.181230

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii
journal, December 2014

  • Juergens, Matthew T.; Deshpande, Rahul R.; Lucker, Ben F.
  • Plant Physiology, Vol. 167, Issue 2
  • DOI: 10.1104/pp.114.250530

Zeaxanthin Accumulation in the Absence of a Functional Xanthophyll Cycle Protects Chlamydomonas reinhardtii from Photooxidative Stress
journal, March 2003

  • Baroli, Irene; Do, An D.; Yamane, Tomoko
  • The Plant Cell, Vol. 15, Issue 4
  • DOI: 10.1105/tpc.010405

Nitrate Signaling by the Regulatory Gene NIT2 in Chlamydomonas
journal, November 2007

  • Camargo, Antonio; Llamas, Ángel; Schnell, Rogene A.
  • The Plant Cell, Vol. 19, Issue 11
  • DOI: 10.1105/tpc.106.045922

Analysis of Transcription Factor HY5 Genomic Binding Sites Revealed Its Hierarchical Role in Light Regulation of Development
journal, March 2007


A Galactoglycerolipid Lipase Is Required for Triacylglycerol Accumulation and Survival Following Nitrogen Deprivation in Chlamydomonas reinhardtii
journal, November 2012

  • Li, Xiaobo; Moellering, Eric R.; Liu, Bensheng
  • The Plant Cell, Vol. 24, Issue 11
  • DOI: 10.1105/tpc.112.105106

Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant
journal, November 2013


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
  • DOI: 10.1105/tpc.113.122523

The response of Chlamydomonas reinhardtii to nitrogen deprivation: a systems biology analysis
journal, February 2015

  • Park, Jeong-Jin; Wang, Hongxia; Gargouri, Mahmoud
  • The Plant Journal, Vol. 81, Issue 4
  • DOI: 10.1111/tpj.12747

High quality metabolomic data for Chlamydomonas reinhardtii
journal, January 2008


The Role of bZIP Transcription Factors in Green Plant Evolution: Adaptive Features Emerging from Four Founder Genes
journal, August 2008

  • Corrêa, Luiz Gustavo Guedes; Riaño-Pachón, Diego Mauricio; Schrago, Carlos Guerra
  • PLoS ONE, Vol. 3, Issue 8
  • DOI: 10.1371/journal.pone.0002944

SDG2-Mediated H3K4 Methylation Is Required for Proper Arabidopsis Root Growth and Development
journal, February 2013


Gametogenesis in the Chlamydomonas reinhardtii minus Mating Type Is Controlled by Two Genes, MID and MTD1
journal, April 2007


Works referencing / citing this record:

Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator
journal, June 2017

  • Ajjawi, Imad; Verruto, John; Aqui, Moena
  • Nature Biotechnology, Vol. 35, Issue 7
  • DOI: 10.1038/nbt.3865

Characterization of dysregulated lncRNA-mRNA network based on ceRNA hypothesis to reveal the occurrence and recurrence of myocardial infarction
journal, February 2018


Transcriptomic and lipidomic analysis of an EPA-containing Nannochloropsis sp. PJ12 in response to nitrogen deprivation
journal, March 2019


Comprehensive analysis of the lncRNA-associated ceRNA network identifies neuroinflammation biomarkers for Alzheimer's disease
journal, January 2019

  • Zhou, Yuanshuai; Xu, Zhongjuan; Yu, Yanzhen
  • Molecular Omics, Vol. 15, Issue 6
  • DOI: 10.1039/c9mo00129h

Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster
journal, September 2018

  • Mohorianu, Irina; Fowler, Emily K.; Dalmay, Tamas
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 285, Issue 1887
  • DOI: 10.1098/rspb.2018.1681

Intrinsic limitations in mainstream methods of identifying network motifs in biology
posted_content, February 2018

  • Fodor, James; Brand, Michael; Stones, Rebecca J.
  • bioRxiv
  • DOI: 10.1101/272401

Metabolic regulation of triacylglycerol accumulation in the green algae: identification of potential targets for engineering to improve oil yield
journal, January 2016

  • Goncalves, Elton C.; Wilkie, Ann C.; Kirst, Matias
  • Plant Biotechnology Journal, Vol. 14, Issue 8
  • DOI: 10.1111/pbi.12523

Unraveling lipid metabolism in maize with time‐resolved multi‐omics data
journal, February 2018

  • Abreu e. Lima, Francisco; Li, Kun; Wen, Weiwei
  • The Plant Journal, Vol. 93, Issue 6
  • DOI: 10.1111/tpj.13833

Transcriptional program for nitrogen starvation-induced lipid accumulation in Chlamydomonas reinhardtii
journal, December 2015

  • López García de Lomana, Adrián; Schäuble, Sascha; Valenzuela, Jacob
  • Biotechnology for Biofuels, Vol. 8, Issue 1
  • DOI: 10.1186/s13068-015-0391-z

Functional photosystem I maintains proper energy balance during nitrogen depletion in Chlamydomonas reinhardtii, promoting triacylglycerol accumulation
journal, April 2017

  • Gargouri, Mahmoud; Bates, Philip D.; Park, Jeong-Jin
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0774-4

Increased lipid production by heterologous expression of AtWRI1 transcription factor in Nannochloropsis salina
journal, October 2017


Recent developments in synthetic biology and metabolic engineering in microalgae towards biofuel production
journal, June 2018

  • Jagadevan, Sheeja; Banerjee, Avik; Banerjee, Chiranjib
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1181-1

Microalgae for the production of lipid and carotenoids: a review with focus on stress regulation and adaptation
journal, October 2018


Nitrogen-dependent coordination of cell cycle, quiescence and TAG accumulation in Chlamydomonas
journal, December 2019


Integration of proteome and transcriptome refines key molecular processes underlying oil production in Nannochloropsis oceanica
journal, June 2020


Understanding nitrate assimilation and its regulation in microalgae
journal, October 2015

  • Sanz-Luque, Emanuel; Chamizo-Ampudia, Alejandro; Llamas, Angel
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00899

Identification and characterization of circRNAs as competing endogenous RNAs for miRNA-mRNA in colorectal cancer
journal, January 2019


Intrinsic limitations in mainstream methods of identifying network motifs in biology
journal, April 2020


The lipid biochemistry of eukaryotic algae
journal, April 2019


Real-time iTRAQ-based proteome profiling revealed the central metabolism involved in nitrogen starvation induced lipid accumulation in microalgae
journal, April 2017

  • Rai, Vineeta; Muthuraj, Muthusivaramapandian; Gandhi, Mayuri N.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep45732

PhytoNet: comparative co-expression network analyses across phytoplankton and land plants
journal, April 2018

  • Ferrari, Camilla; Proost, Sebastian; Ruprecht, Colin
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky298

Intrinsic limitations in mainstream methods of identifying network motifs in biology
journal, April 2020


Transcriptional program for nitrogen starvation-induced lipid accumulation in Chlamydomonas reinhardtii
journal, December 2015

  • López García de Lomana, Adrián; Schäuble, Sascha; Valenzuela, Jacob
  • Biotechnology for Biofuels, Vol. 8, Issue 1
  • DOI: 10.1186/s13068-015-0391-z

Recent developments in synthetic biology and metabolic engineering in microalgae towards biofuel production
journal, June 2018

  • Jagadevan, Sheeja; Banerjee, Avik; Banerjee, Chiranjib
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1181-1

Microalgae for the production of lipid and carotenoids: a review with focus on stress regulation and adaptation
journal, October 2018


Understanding nitrate assimilation and its regulation in microalgae
journal, October 2015

  • Sanz-Luque, Emanuel; Chamizo-Ampudia, Alejandro; Llamas, Angel
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00899

iTRAQ-Based Proteomic Analysis Reveals Several Strategies to Cope with Drought Stress in Maize Seedlings
journal, November 2019

  • Jiang, Zhilei; Jin, Fengxue; Shan, Xiaohui
  • International Journal of Molecular Sciences, Vol. 20, Issue 23
  • DOI: 10.3390/ijms20235956

Identification and characterization of circRNAs as competing endogenous RNAs for miRNA-mRNA in colorectal cancer
journal, January 2019