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The Lack of Mitochondrial Thioredoxin TRXo1 Affects In Vivo Alternative Oxidase Activity and Carbon Metabolism under Different Light Conditions.

Identifieur interne : 000073 ( Main/Exploration ); précédent : 000072; suivant : 000074

The Lack of Mitochondrial Thioredoxin TRXo1 Affects In Vivo Alternative Oxidase Activity and Carbon Metabolism under Different Light Conditions.

Auteurs : Igor Florez-Sarasa [Allemagne, Espagne] ; Toshihiro Obata [Allemagne, États-Unis] ; Nï Stor Fernï Ndez Del-Saz [Espagne, Chili] ; Jean-Philippe Reichheld [France] ; Etienne H. Meyer [Allemagne] ; Manuel Rodriguez-Concepcion [Espagne] ; Miquel Ribas-Carbo [Espagne] ; Alisdair R. Fernie [Allemagne]

Source :

RBID : pubmed:31318380

Descripteurs français

English descriptors

Abstract

The alternative oxidase (AOX) constitutes a nonphosphorylating pathway of electron transport in the mitochondrial respiratory chain that provides flexibility to energy and carbon primary metabolism. Its activity is regulated in vitro by the mitochondrial thioredoxin (TRX) system which reduces conserved cysteines residues of AOX. However, in vivo evidence for redox regulation of the AOX activity is still scarce. In the present study, the redox state, protein levels and in vivo activity of the AOX in parallel to photosynthetic parameters were determined in Arabidopsis knockout mutants lacking mitochondrial trxo1 under moderate (ML) and high light (HL) conditions, known to induce in vivo AOX activity. In addition, 13C- and 14C-labeling experiments together with metabolite profiling were performed to better understand the metabolic coordination between energy and carbon metabolism in the trxo1 mutants. Our results show that the in vivo AOX activity is higher in the trxo1 mutants at ML while the AOX redox state is apparently unaltered. These results suggest that mitochondrial thiol redox systems are responsible for maintaining AOX in its reduced form rather than regulating its activity in vivo. Moreover, the negative regulation of the tricarboxylic acid cycle by the TRX system is coordinated with the increased input of electrons into the AOX pathway. Under HL conditions, while AOX and photosynthesis displayed similar patterns in the mutants, photorespiration is restricted at the level of glycine decarboxylation most likely as a consequence of redox imbalance.

DOI: 10.1093/pcp/pcz123
PubMed: 31318380


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<div type="abstract" xml:lang="en">The alternative oxidase (AOX) constitutes a nonphosphorylating pathway of electron transport in the mitochondrial respiratory chain that provides flexibility to energy and carbon primary metabolism. Its activity is regulated in vitro by the mitochondrial thioredoxin (TRX) system which reduces conserved cysteines residues of AOX. However, in vivo evidence for redox regulation of the AOX activity is still scarce. In the present study, the redox state, protein levels and in vivo activity of the AOX in parallel to photosynthetic parameters were determined in Arabidopsis knockout mutants lacking mitochondrial trxo1 under moderate (ML) and high light (HL) conditions, known to induce in vivo AOX activity. In addition, 13C- and 14C-labeling experiments together with metabolite profiling were performed to better understand the metabolic coordination between energy and carbon metabolism in the trxo1 mutants. Our results show that the in vivo AOX activity is higher in the trxo1 mutants at ML while the AOX redox state is apparently unaltered. These results suggest that mitochondrial thiol redox systems are responsible for maintaining AOX in its reduced form rather than regulating its activity in vivo. Moreover, the negative regulation of the tricarboxylic acid cycle by the TRX system is coordinated with the increased input of electrons into the AOX pathway. Under HL conditions, while AOX and photosynthesis displayed similar patterns in the mutants, photorespiration is restricted at the level of glycine decarboxylation most likely as a consequence of redox imbalance.</div>
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<Year>2019</Year>
<Month>Nov</Month>
<Day>01</Day>
</PubDate>
</JournalIssue>
<Title>Plant & cell physiology</Title>
<ISOAbbreviation>Plant Cell Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>The Lack of Mitochondrial Thioredoxin TRXo1 Affects In Vivo Alternative Oxidase Activity and Carbon Metabolism under Different Light Conditions.</ArticleTitle>
<Pagination>
<MedlinePgn>2369-2381</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1093/pcp/pcz123</ELocationID>
<Abstract>
<AbstractText>The alternative oxidase (AOX) constitutes a nonphosphorylating pathway of electron transport in the mitochondrial respiratory chain that provides flexibility to energy and carbon primary metabolism. Its activity is regulated in vitro by the mitochondrial thioredoxin (TRX) system which reduces conserved cysteines residues of AOX. However, in vivo evidence for redox regulation of the AOX activity is still scarce. In the present study, the redox state, protein levels and in vivo activity of the AOX in parallel to photosynthetic parameters were determined in Arabidopsis knockout mutants lacking mitochondrial trxo1 under moderate (ML) and high light (HL) conditions, known to induce in vivo AOX activity. In addition, 13C- and 14C-labeling experiments together with metabolite profiling were performed to better understand the metabolic coordination between energy and carbon metabolism in the trxo1 mutants. Our results show that the in vivo AOX activity is higher in the trxo1 mutants at ML while the AOX redox state is apparently unaltered. These results suggest that mitochondrial thiol redox systems are responsible for maintaining AOX in its reduced form rather than regulating its activity in vivo. Moreover, the negative regulation of the tricarboxylic acid cycle by the TRX system is coordinated with the increased input of electrons into the AOX pathway. Under HL conditions, while AOX and photosynthesis displayed similar patterns in the mutants, photorespiration is restricted at the level of glycine decarboxylation most likely as a consequence of redox imbalance.</AbstractText>
<CopyrightInformation>� The Author(s) 2019. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Florez-Sarasa</LastName>
<ForeName>Igor</ForeName>
<Initials>I</Initials>
<AffiliationInfo>
<Affiliation>Max-Planck-Institut f�r Molekulare Pflanzenphysiologie, Am M�hlenberg 1, Potsdam-Golm, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB Bellaterra, Barcelona, Spain.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Obata</LastName>
<ForeName>Toshihiro</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Max-Planck-Institut f�r Molekulare Pflanzenphysiologie, Am M�hlenberg 1, Potsdam-Golm, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>University of Nebraska Lincoln, 1901 Vine Street, Lincoln, NE, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Del-Saz</LastName>
<ForeName>Nï Stor Fernï Ndez</ForeName>
<Initials>NSFN</Initials>
<AffiliationInfo>
<Affiliation>Grup de Recerca en Biologia de les Plantes en Condicions Mediterranies, Departament de Biologia, Universitat de les Illes Balears, Carretera de Valldemossa Km 7.5, Palma de Mallorca, Spain.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Departamento de Bot�nica, Facultad de Ciencias Naturales y Oceanogr�ficas, Universidad de Concepci�n, Concepci�n, Chile.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Reichheld</LastName>
<ForeName>Jean-Philippe</ForeName>
<Initials>JP</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire G�nome et D�veloppement des Plantes, CNRS, Perpignan F, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Meyer</LastName>
<ForeName>Etienne H</ForeName>
<Initials>EH</Initials>
<AffiliationInfo>
<Affiliation>Max-Planck-Institut f�r Molekulare Pflanzenphysiologie, Am M�hlenberg 1, Potsdam-Golm, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rodriguez-Concepcion</LastName>
<ForeName>Manuel</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB Bellaterra, Barcelona, Spain.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ribas-Carbo</LastName>
<ForeName>Miquel</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Grup de Recerca en Biologia de les Plantes en Condicions Mediterranies, Departament de Biologia, Universitat de les Illes Balears, Carretera de Valldemossa Km 7.5, Palma de Mallorca, Spain.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Fernie</LastName>
<ForeName>Alisdair R</ForeName>
<Initials>AR</Initials>
<AffiliationInfo>
<Affiliation>Max-Planck-Institut f�r Molekulare Pflanzenphysiologie, Am M�hlenberg 1, Potsdam-Golm, Germany.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
</Article>
<MedlineJournalInfo>
<Country>Japan</Country>
<MedlineTA>Plant Cell Physiol</MedlineTA>
<NlmUniqueID>9430925</NlmUniqueID>
<ISSNLinking>0032-0781</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D024101">Mitochondrial Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>7440-44-0</RegistryNumber>
<NameOfSubstance UI="D002244">Carbon</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.-</RegistryNumber>
<NameOfSubstance UI="D010088">Oxidoreductases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.-</RegistryNumber>
<NameOfSubstance UI="C088813">alternative oxidase</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<CommentsCorrectionsList>
<CommentsCorrections RefType="CommentIn">
<RefSource>Plant Cell Physiol. 2019 Nov 1;60(11):2357-2359</RefSource>
<PMID Version="1">31504877</PMID>
</CommentsCorrections>
</CommentsCorrectionsList>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002244" MajorTopicYN="N">Carbon</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008928" MajorTopicYN="N">Mitochondria</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D024101" MajorTopicYN="N">Mitochondrial Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010084" MajorTopicYN="N">Oxidation-Reduction</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010088" MajorTopicYN="N">Oxidoreductases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010788" MajorTopicYN="N">Photosynthesis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Arabidopsis thaliana </Keyword>
<Keyword MajorTopicYN="N">Alternative oxidase</Keyword>
<Keyword MajorTopicYN="N">Carbon fluxes</Keyword>
<Keyword MajorTopicYN="N">High light</Keyword>
<Keyword MajorTopicYN="N">Mitochondrial thioredoxin</Keyword>
<Keyword MajorTopicYN="N">Oxygen-isotope fractionation</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2019</Year>
<Month>01</Month>
<Day>03</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2019</Year>
<Month>06</Month>
<Day>17</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2019</Year>
<Month>7</Month>
<Day>19</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2020</Year>
<Month>2</Month>
<Day>23</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2019</Year>
<Month>7</Month>
<Day>19</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">31318380</ArticleId>
<ArticleId IdType="pii">5535538</ArticleId>
<ArticleId IdType="doi">10.1093/pcp/pcz123</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Chili</li>
<li>Espagne</li>
<li>France</li>
<li>États-Unis</li>
</country>
<region>
<li>Catalogne</li>
<li>Nebraska</li>
</region>
<settlement>
<li>Barcelone</li>
</settlement>
</list>
<tree>
<country name="Allemagne">
<noRegion>
<name sortKey="Florez Sarasa, Igor" sort="Florez Sarasa, Igor" uniqKey="Florez Sarasa I" first="Igor" last="Florez-Sarasa">Igor Florez-Sarasa</name>
</noRegion>
<name sortKey="Fernie, Alisdair R" sort="Fernie, Alisdair R" uniqKey="Fernie A" first="Alisdair R" last="Fernie">Alisdair R. Fernie</name>
<name sortKey="Meyer, Etienne H" sort="Meyer, Etienne H" uniqKey="Meyer E" first="Etienne H" last="Meyer">Etienne H. Meyer</name>
<name sortKey="Obata, Toshihiro" sort="Obata, Toshihiro" uniqKey="Obata T" first="Toshihiro" last="Obata">Toshihiro Obata</name>
</country>
<country name="Espagne">
<region name="Catalogne">
<name sortKey="Florez Sarasa, Igor" sort="Florez Sarasa, Igor" uniqKey="Florez Sarasa I" first="Igor" last="Florez-Sarasa">Igor Florez-Sarasa</name>
</region>
<name sortKey="Del Saz, Ni Stor Ferni Ndez" sort="Del Saz, Ni Stor Ferni Ndez" uniqKey="Del Saz N" first="Nï Stor Fernï Ndez" last="Del-Saz">Nï Stor Fernï Ndez Del-Saz</name>
<name sortKey="Ribas Carbo, Miquel" sort="Ribas Carbo, Miquel" uniqKey="Ribas Carbo M" first="Miquel" last="Ribas-Carbo">Miquel Ribas-Carbo</name>
<name sortKey="Rodriguez Concepcion, Manuel" sort="Rodriguez Concepcion, Manuel" uniqKey="Rodriguez Concepcion M" first="Manuel" last="Rodriguez-Concepcion">Manuel Rodriguez-Concepcion</name>
</country>
<country name="États-Unis">
<region name="Nebraska">
<name sortKey="Obata, Toshihiro" sort="Obata, Toshihiro" uniqKey="Obata T" first="Toshihiro" last="Obata">Toshihiro Obata</name>
</region>
</country>
<country name="Chili">
<noRegion>
<name sortKey="Del Saz, Ni Stor Ferni Ndez" sort="Del Saz, Ni Stor Ferni Ndez" uniqKey="Del Saz N" first="Nï Stor Fernï Ndez" last="Del-Saz">Nï Stor Fernï Ndez Del-Saz</name>
</noRegion>
</country>
<country name="France">
<noRegion>
<name sortKey="Reichheld, Jean Philippe" sort="Reichheld, Jean Philippe" uniqKey="Reichheld J" first="Jean-Philippe" last="Reichheld">Jean-Philippe Reichheld</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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