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Research ArticleLARGE-SCALE BIOLOGY ARTICLE
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Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism

Stefan Schmollinger, Timo Mühlhaus, Nanette R. Boyle, Ian K. Blaby, David Casero, Tabea Mettler, Jeffrey L. Moseley, Janette Kropat, Frederik Sommer, Daniela Strenkert, Dorothea Hemme, Matteo Pellegrini, Arthur R. Grossman, Mark Stitt, Michael Schroda, Sabeeha S. Merchant
Stefan Schmollinger
aDepartment of Chemistry and Biochemistry, University of California, Los Angeles, California 90095
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  • ORCID record for Stefan Schmollinger
Timo Mühlhaus
bMolecular Biotechnology and Systems Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany
cMax Planck Institute of Molecular Plant Physiology, D-14476 Potsdam-Golm, Germany
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Nanette R. Boyle
aDepartment of Chemistry and Biochemistry, University of California, Los Angeles, California 90095
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Ian K. Blaby
aDepartment of Chemistry and Biochemistry, University of California, Los Angeles, California 90095
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David Casero
dDepartment of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, California 90095
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Tabea Mettler
cMax Planck Institute of Molecular Plant Physiology, D-14476 Potsdam-Golm, Germany
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Jeffrey L. Moseley
eDepartment of Plant Biology, Carnegie Institution for Science, Stanford, California 94305
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Janette Kropat
aDepartment of Chemistry and Biochemistry, University of California, Los Angeles, California 90095
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Frederik Sommer
bMolecular Biotechnology and Systems Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany
cMax Planck Institute of Molecular Plant Physiology, D-14476 Potsdam-Golm, Germany
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Daniela Strenkert
aDepartment of Chemistry and Biochemistry, University of California, Los Angeles, California 90095
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Dorothea Hemme
bMolecular Biotechnology and Systems Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany
cMax Planck Institute of Molecular Plant Physiology, D-14476 Potsdam-Golm, Germany
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Matteo Pellegrini
dDepartment of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, California 90095
fInstitute of Genomics and Proteomics, University of California, Los Angeles, California 90095
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Arthur R. Grossman
eDepartment of Plant Biology, Carnegie Institution for Science, Stanford, California 94305
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Mark Stitt
cMax Planck Institute of Molecular Plant Physiology, D-14476 Potsdam-Golm, Germany
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Michael Schroda
bMolecular Biotechnology and Systems Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany
cMax Planck Institute of Molecular Plant Physiology, D-14476 Potsdam-Golm, Germany
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Sabeeha S. Merchant
aDepartment of Chemistry and Biochemistry, University of California, Los Angeles, California 90095
fInstitute of Genomics and Proteomics, University of California, Los Angeles, California 90095
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  • ORCID record for Sabeeha S. Merchant
  • For correspondence: merchant@chem.ucla.edu

Published April 2014. DOI: https://doi.org/10.1105/tpc.113.122523

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  • © 2014 American Society of Plant Biologists. All rights reserved.

Abstract

Nitrogen (N) is a key nutrient that limits global primary productivity; hence, N-use efficiency is of compelling interest in agriculture and aquaculture. We used Chlamydomonas reinhardtii as a reference organism for a multicomponent analysis of the N starvation response. In the presence of acetate, respiratory metabolism is prioritized over photosynthesis; consequently, the N-sparing response targets proteins, pigments, and RNAs involved in photosynthesis and chloroplast function over those involved in respiration. Transcripts and proteins of the Calvin-Benson cycle are reduced in N-deficient cells, resulting in the accumulation of cycle metabolic intermediates. Both cytosolic and chloroplast ribosomes are reduced, but via different mechanisms, reflected by rapid changes in abundance of RNAs encoding chloroplast ribosomal proteins but not cytosolic ones. RNAs encoding transporters and enzymes for metabolizing alternative N sources increase in abundance, as is appropriate for the soil environmental niche of C. reinhardtii. Comparison of the N-replete versus N-deplete proteome indicated that abundant proteins with a high N content are reduced in N-starved cells, while the proteins that are increased have lower than average N contents. This sparing mechanism contributes to a lower cellular N/C ratio and suggests an approach for engineering increased N-use efficiency.

  • Glossary

    GS
    Gln synthetase
    GOGAT
    Glu oxoglutarate amidotransferase
    TAG
    triacylglycerol
    LC-MS/MS
    liquid chromatography–tandem mass spectrometry
    RPKM
    reads per kilobase of gene model per million reads
    PSII
    photosystem II
    PSI
    photosystem I
    Fv/Fm
    quantum efficiency of PSII
    TPIC
    triose phosphate isomerase
    ACCase
    acetyl-CoA carboxylase
    FAS
    fatty acid synthase
    NUE
    nitrogen use efficiency
    TAP
    Tris-acetate-phosphate
    • Received December 31, 2013.
    • Revised March 19, 2014.
    • Accepted March 29, 2014.
    • Published April 18, 2014.
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    Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism
    Stefan Schmollinger, Timo Mühlhaus, Nanette R. Boyle, Ian K. Blaby, David Casero, Tabea Mettler, Jeffrey L. Moseley, Janette Kropat, Frederik Sommer, Daniela Strenkert, Dorothea Hemme, Matteo Pellegrini, Arthur R. Grossman, Mark Stitt, Michael Schroda, Sabeeha S. Merchant
    The Plant Cell Apr 2014, 26 (4) 1410-1435; DOI: 10.1105/tpc.113.122523

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    Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism
    Stefan Schmollinger, Timo Mühlhaus, Nanette R. Boyle, Ian K. Blaby, David Casero, Tabea Mettler, Jeffrey L. Moseley, Janette Kropat, Frederik Sommer, Daniela Strenkert, Dorothea Hemme, Matteo Pellegrini, Arthur R. Grossman, Mark Stitt, Michael Schroda, Sabeeha S. Merchant
    The Plant Cell Apr 2014, 26 (4) 1410-1435; DOI: 10.1105/tpc.113.122523
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