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Multiomics resolution of molecular events during a day in the life of Chlamydomonas.

Identifieur interne : 000153 ( Main/Exploration ); précédent : 000152; suivant : 000154

Multiomics resolution of molecular events during a day in the life of Chlamydomonas.

Auteurs : Daniela Strenkert [États-Unis] ; Stefan Schmollinger [États-Unis] ; Sean D. Gallaher [États-Unis] ; Patrice A. Salomé [États-Unis] ; Samuel O. Purvine [États-Unis] ; Carrie D. Nicora [États-Unis] ; Tabea Mettler-Altmann [Allemagne] ; Eric Soubeyrand [États-Unis] ; Andreas P M. Weber [Allemagne] ; Mary S. Lipton [États-Unis] ; Gilles J. Basset [États-Unis] ; Sabeeha S. Merchant [États-Unis]

Source :

RBID : pubmed:30659148

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English descriptors

Abstract

The unicellular green alga Chlamydomonas reinhardtii displays metabolic flexibility in response to a changing environment. We analyzed expression patterns of its three genomes in cells grown under light-dark cycles. Nearly 85% of transcribed genes show differential expression, with different sets of transcripts being up-regulated over the course of the day to coordinate cellular growth before undergoing cell division. Parallel measurements of select metabolites and pigments, physiological parameters, and a subset of proteins allow us to infer metabolic events and to evaluate the impact of the transcriptome on the proteome. Among the findings are the observations that Chlamydomonas exhibits lower respiratory activity at night compared with the day; multiple fermentation pathways, some oxygen-sensitive, are expressed at night in aerated cultures; we propose that the ferredoxin, FDX9, is potentially the electron donor to hydrogenases. The light stress-responsive genes PSBS, LHCSR1, and LHCSR3 show an acute response to lights-on at dawn under abrupt dark-to-light transitions, while LHCSR3 genes also exhibit a later, second burst in expression in the middle of the day dependent on light intensity. Each response to light (acute and sustained) can be selectively activated under specific conditions. Our expression dataset, complemented with coexpression networks and metabolite profiling, should constitute an excellent resource for the algal and plant communities.

DOI: 10.1073/pnas.1815238116
PubMed: 30659148
PubMed Central: PMC6369806


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<term>Cell Division (MeSH)</term>
<term>Chlamydomonas (genetics)</term>
<term>Chlamydomonas (metabolism)</term>
<term>DNA Replication (MeSH)</term>
<term>Gene Expression Profiling (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Genomics (methods)</term>
<term>Glycolysis (MeSH)</term>
<term>Metabolome (MeSH)</term>
<term>Metabolomics (methods)</term>
<term>NAD (metabolism)</term>
<term>Oxidation-Reduction (MeSH)</term>
<term>Photosynthesis (genetics)</term>
<term>Proteome (MeSH)</term>
<term>Proteomics (methods)</term>
<term>Signal Transduction (MeSH)</term>
<term>Transcriptome (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de profil d'expression de gènes (MeSH)</term>
<term>Chlamydomonas (génétique)</term>
<term>Chlamydomonas (métabolisme)</term>
<term>Division cellulaire (MeSH)</term>
<term>Glycolyse (MeSH)</term>
<term>Génomique (méthodes)</term>
<term>Métabolome (MeSH)</term>
<term>Métabolomique (méthodes)</term>
<term>NAD (métabolisme)</term>
<term>Oxydoréduction (MeSH)</term>
<term>Photosynthèse (génétique)</term>
<term>Protéome (MeSH)</term>
<term>Protéomique (méthodes)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Réplication de l'ADN (MeSH)</term>
<term>Transcriptome (MeSH)</term>
<term>Transduction du signal (MeSH)</term>
</keywords>
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<term>NAD</term>
</keywords>
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<term>Chlamydomonas</term>
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<term>Chlamydomonas</term>
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<term>Chlamydomonas</term>
</keywords>
<keywords scheme="MESH" qualifier="methods" xml:lang="en">
<term>Genomics</term>
<term>Metabolomics</term>
<term>Proteomics</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Chlamydomonas</term>
<term>NAD</term>
</keywords>
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<term>Génomique</term>
<term>Métabolomique</term>
<term>Protéomique</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Cell Division</term>
<term>DNA Replication</term>
<term>Gene Expression Profiling</term>
<term>Gene Expression Regulation, Plant</term>
<term>Glycolysis</term>
<term>Metabolome</term>
<term>Oxidation-Reduction</term>
<term>Proteome</term>
<term>Signal Transduction</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de profil d'expression de gènes</term>
<term>Division cellulaire</term>
<term>Glycolyse</term>
<term>Métabolome</term>
<term>Oxydoréduction</term>
<term>Protéome</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Réplication de l'ADN</term>
<term>Transcriptome</term>
<term>Transduction du signal</term>
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<front>
<div type="abstract" xml:lang="en">The unicellular green alga
<i>Chlamydomonas reinhardtii</i>
displays metabolic flexibility in response to a changing environment. We analyzed expression patterns of its three genomes in cells grown under light-dark cycles. Nearly 85% of transcribed genes show differential expression, with different sets of transcripts being up-regulated over the course of the day to coordinate cellular growth before undergoing cell division. Parallel measurements of select metabolites and pigments, physiological parameters, and a subset of proteins allow us to infer metabolic events and to evaluate the impact of the transcriptome on the proteome. Among the findings are the observations that
<i>Chlamydomonas</i>
exhibits lower respiratory activity at night compared with the day; multiple fermentation pathways, some oxygen-sensitive, are expressed at night in aerated cultures; we propose that the ferredoxin, FDX9, is potentially the electron donor to hydrogenases. The light stress-responsive genes
<i>PSBS</i>
,
<i>LHCSR1</i>
, and
<i>LHCSR3</i>
show an acute response to lights-on at dawn under abrupt dark-to-light transitions, while
<i>LHCSR3</i>
genes also exhibit a later, second burst in expression in the middle of the day dependent on light intensity. Each response to light (acute and sustained) can be selectively activated under specific conditions. Our expression dataset, complemented with coexpression networks and metabolite profiling, should constitute an excellent resource for the algal and plant communities.</div>
</front>
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<DateCompleted>
<Year>2019</Year>
<Month>04</Month>
<Day>16</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>03</Month>
<Day>09</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1091-6490</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>116</Volume>
<Issue>6</Issue>
<PubDate>
<Year>2019</Year>
<Month>02</Month>
<Day>05</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>Multiomics resolution of molecular events during a day in the life of Chlamydomonas.</ArticleTitle>
<Pagination>
<MedlinePgn>2374-2383</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1815238116</ELocationID>
<Abstract>
<AbstractText>The unicellular green alga
<i>Chlamydomonas reinhardtii</i>
displays metabolic flexibility in response to a changing environment. We analyzed expression patterns of its three genomes in cells grown under light-dark cycles. Nearly 85% of transcribed genes show differential expression, with different sets of transcripts being up-regulated over the course of the day to coordinate cellular growth before undergoing cell division. Parallel measurements of select metabolites and pigments, physiological parameters, and a subset of proteins allow us to infer metabolic events and to evaluate the impact of the transcriptome on the proteome. Among the findings are the observations that
<i>Chlamydomonas</i>
exhibits lower respiratory activity at night compared with the day; multiple fermentation pathways, some oxygen-sensitive, are expressed at night in aerated cultures; we propose that the ferredoxin, FDX9, is potentially the electron donor to hydrogenases. The light stress-responsive genes
<i>PSBS</i>
,
<i>LHCSR1</i>
, and
<i>LHCSR3</i>
show an acute response to lights-on at dawn under abrupt dark-to-light transitions, while
<i>LHCSR3</i>
genes also exhibit a later, second burst in expression in the middle of the day dependent on light intensity. Each response to light (acute and sustained) can be selectively activated under specific conditions. Our expression dataset, complemented with coexpression networks and metabolite profiling, should constitute an excellent resource for the algal and plant communities.</AbstractText>
<CopyrightInformation>Copyright © 2019 the Author(s). Published by PNAS.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Strenkert</LastName>
<ForeName>Daniela</ForeName>
<Initials>D</Initials>
<Identifier Source="ORCID">0000-0002-3420-1332</Identifier>
<AffiliationInfo>
<Affiliation>Institute for Genomics and Proteomics, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schmollinger</LastName>
<ForeName>Stefan</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Institute for Genomics and Proteomics, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
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<LastName>Gallaher</LastName>
<ForeName>Sean D</ForeName>
<Initials>SD</Initials>
<Identifier Source="ORCID">0000-0002-9773-6051</Identifier>
<AffiliationInfo>
<Affiliation>Institute for Genomics and Proteomics, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
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<LastName>Salomé</LastName>
<ForeName>Patrice A</ForeName>
<Initials>PA</Initials>
<Identifier Source="ORCID">0000-0003-4452-9064</Identifier>
<AffiliationInfo>
<Affiliation>Institute for Genomics and Proteomics, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Purvine</LastName>
<ForeName>Samuel O</ForeName>
<Initials>SO</Initials>
<Identifier Source="ORCID">0000-0002-2257-2400</Identifier>
<AffiliationInfo>
<Affiliation>Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory (PNNL), US Department of Energy, Richland, WA 99352.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Nicora</LastName>
<ForeName>Carrie D</ForeName>
<Initials>CD</Initials>
<Identifier Source="ORCID">0000-0003-2461-9548</Identifier>
<AffiliationInfo>
<Affiliation>Biological Sciences Divison, PNNL, US Department of Energy, Richland, WA 99352.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Mettler-Altmann</LastName>
<ForeName>Tabea</ForeName>
<Initials>T</Initials>
<Identifier Source="ORCID">0000-0002-9161-4889</Identifier>
<AffiliationInfo>
<Affiliation>Institute of Plant Biochemistry, Cluster of Excellence on Plant Science, Heinrich Heine University, 40225 Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Soubeyrand</LastName>
<ForeName>Eric</ForeName>
<Initials>E</Initials>
<Identifier Source="ORCID">0000-0003-2970-3183</Identifier>
<AffiliationInfo>
<Affiliation>Center for Plant Science Innovation, University of Nebraska, Lincoln, NE 68588.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Weber</LastName>
<ForeName>Andreas P M</ForeName>
<Initials>APM</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Biochemistry, Cluster of Excellence on Plant Science, Heinrich Heine University, 40225 Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lipton</LastName>
<ForeName>Mary S</ForeName>
<Initials>MS</Initials>
<AffiliationInfo>
<Affiliation>Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory (PNNL), US Department of Energy, Richland, WA 99352.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Basset</LastName>
<ForeName>Gilles J</ForeName>
<Initials>GJ</Initials>
<Identifier Source="ORCID">0000-0001-5275-9797</Identifier>
<AffiliationInfo>
<Affiliation>Center for Plant Science Innovation, University of Nebraska, Lincoln, NE 68588.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Merchant</LastName>
<ForeName>Sabeeha S</ForeName>
<Initials>SS</Initials>
<AffiliationInfo>
<Affiliation>Institute for Genomics and Proteomics, University of California, Los Angeles, CA 90095; sabeeha@chem.ucla.edu.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
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<Month>01</Month>
<Day>18</Day>
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<MeshHeading>
<DescriptorName UI="D002455" MajorTopicYN="N">Cell Division</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002696" MajorTopicYN="N">Chlamydomonas</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D004261" MajorTopicYN="N">DNA Replication</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020869" MajorTopicYN="N">Gene Expression Profiling</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D023281" MajorTopicYN="Y">Genomics</DescriptorName>
<QualifierName UI="Q000379" MajorTopicYN="N">methods</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006019" MajorTopicYN="N">Glycolysis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055442" MajorTopicYN="N">Metabolome</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055432" MajorTopicYN="Y">Metabolomics</DescriptorName>
<QualifierName UI="Q000379" MajorTopicYN="N">methods</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009243" MajorTopicYN="N">NAD</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010084" MajorTopicYN="N">Oxidation-Reduction</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010788" MajorTopicYN="N">Photosynthesis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020543" MajorTopicYN="N">Proteome</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D040901" MajorTopicYN="Y">Proteomics</DescriptorName>
<QualifierName UI="Q000379" MajorTopicYN="N">methods</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059467" MajorTopicYN="N">Transcriptome</DescriptorName>
</MeshHeading>
</MeshHeadingList>
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<Keyword MajorTopicYN="Y">cell division</Keyword>
<Keyword MajorTopicYN="Y">chloroplast</Keyword>
<Keyword MajorTopicYN="Y">histone expression</Keyword>
<Keyword MajorTopicYN="Y">photobioreactor</Keyword>
<Keyword MajorTopicYN="Y">systems biology</Keyword>
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