The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis.
Identifieur interne : 002646 ( PubMed/Curation ); précédent : 002645; suivant : 002647The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis.
Auteurs : Stephan Wagner [Allemagne] ; Smrutisanjita Behera [Italie] ; Sara De Bortoli [Italie] ; David C. Logan [France] ; Philippe Fuchs [Allemagne] ; Luca Carraretto [Italie] ; Enrico Teardo [Italie] ; Laura Cendron [Italie] ; Thomas Nietzel [Allemagne] ; Magdalena Fü L [Allemagne] ; Fabrizio G. Doccula [Italie] ; Lorella Navazio [Italie] ; Mark D. Fricker [Royaume-Uni] ; Olivier Van Aken [Australie] ; Iris Finkemeier [Allemagne] ; Andreas J. Meyer [Allemagne] ; Ildik Szab [Italie] ; Alex Costa [Italie] ; Markus Schwarzl Nder [Allemagne]Source :
- The Plant cell [ 1532-298X ] ; 2015.
Descripteurs français
- KwdFr :
- ADN bactérien (génétique), Arabidopsis (génétique), Arabidopsis (métabolisme), Calcium, Cytosol (métabolisme), Fractions subcellulaires (métabolisme), Liaison aux protéines, Mitochondries (métabolisme), Mitochondries (ultrastructure), Motifs EF Hands, Mutagenèse par insertion (génétique), Phylogénie, Plant (métabolisme), Protéines d'Arabidopsis (métabolisme), Protéines de liaison au calcium (métabolisme), Racines de plante (métabolisme), Racines de plante (ultrastructure), Respiration cellulaire, Signalisation du calcium, Similitude de séquences d'acides aminés, Transport de protéines.
- MESH :
- génétique : ADN bactérien, Arabidopsis, Mutagenèse par insertion.
- métabolisme : Arabidopsis, Cytosol, Fractions subcellulaires, Mitochondries, Plant, Protéines d'Arabidopsis, Protéines de liaison au calcium, Racines de plante.
- ultrastructure : Calcium, Liaison aux protéines, Mitochondries, Motifs EF Hands, Phylogénie, Racines de plante, Respiration cellulaire, Signalisation du calcium, Similitude de séquences d'acides aminés, Transport de protéines.
English descriptors
- KwdEn :
- Arabidopsis (genetics), Arabidopsis (metabolism), Arabidopsis Proteins (metabolism), Calcium, Calcium Signaling, Calcium-Binding Proteins (metabolism), Cell Respiration, Cytosol (metabolism), DNA, Bacterial (genetics), EF Hand Motifs, Mitochondria (metabolism), Mitochondria (ultrastructure), Mutagenesis, Insertional (genetics), Phylogeny, Plant Roots (metabolism), Plant Roots (ultrastructure), Protein Binding, Protein Transport, Seedlings (metabolism), Sequence Homology, Amino Acid, Subcellular Fractions (metabolism).
- MESH :
- chemical , genetics : DNA, Bacterial.
- chemical , metabolism : Arabidopsis Proteins, Calcium-Binding Proteins.
- genetics : Arabidopsis, Mutagenesis, Insertional.
- metabolism : Arabidopsis, Cytosol, Mitochondria, Plant Roots, Seedlings, Subcellular Fractions.
- ultrastructure : Mitochondria, Plant Roots.
- chemical : Calcium, Calcium Signaling, Cell Respiration, EF Hand Motifs, Phylogeny, Protein Binding, Protein Transport, Sequence Homology, Amino Acid.
Abstract
Plant organelle function must constantly adjust to environmental conditions, which requires dynamic coordination. Ca(2+) signaling may play a central role in this process. Free Ca(2+) dynamics are tightly regulated and differ markedly between the cytosol, plastid stroma, and mitochondrial matrix. The mechanistic basis of compartment-specific Ca(2+) dynamics is poorly understood. Here, we studied the function of At-MICU, an EF-hand protein of Arabidopsis thaliana with homology to constituents of the mitochondrial Ca(2+) uniporter machinery in mammals. MICU binds Ca(2+) and localizes to the mitochondria in Arabidopsis. In vivo imaging of roots expressing a genetically encoded Ca(2+) sensor in the mitochondrial matrix revealed that lack of MICU increased resting concentrations of free Ca(2+) in the matrix. Furthermore, Ca(2+) elevations triggered by auxin and extracellular ATP occurred more rapidly and reached higher maximal concentrations in the mitochondria of micu mutants, whereas cytosolic Ca(2+) signatures remained unchanged. These findings support the idea that a conserved uniporter system, with composition and regulation distinct from the mammalian machinery, mediates mitochondrial Ca(2+) uptake in plants under in vivo conditions. They further suggest that MICU acts as a throttle that controls Ca(2+) uptake by moderating influx, thereby shaping Ca(2+) signatures in the matrix and preserving mitochondrial homeostasis. Our results open the door to genetic dissection of mitochondrial Ca(2+) signaling in plants.
DOI: 10.1105/tpc.15.00509
PubMed: 26530087
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<author><name sortKey="Fu L, Magdalena" sort="Fu L, Magdalena" uniqKey="Fu L M" first="Magdalena" last="Fü L">Magdalena Fü L</name>
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<author><name sortKey="Doccula, Fabrizio G" sort="Doccula, Fabrizio G" uniqKey="Doccula F" first="Fabrizio G" last="Doccula">Fabrizio G. Doccula</name>
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<author><name sortKey="Meyer, Andreas J" sort="Meyer, Andreas J" uniqKey="Meyer A" first="Andreas J" last="Meyer">Andreas J. Meyer</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis.</title>
<author><name sortKey="Wagner, Stephan" sort="Wagner, Stephan" uniqKey="Wagner S" first="Stephan" last="Wagner">Stephan Wagner</name>
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<author><name sortKey="Behera, Smrutisanjita" sort="Behera, Smrutisanjita" uniqKey="Behera S" first="Smrutisanjita" last="Behera">Smrutisanjita Behera</name>
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<country xml:lang="fr">Italie</country>
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<author><name sortKey="De Bortoli, Sara" sort="De Bortoli, Sara" uniqKey="De Bortoli S" first="Sara" last="De Bortoli">Sara De Bortoli</name>
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<country xml:lang="fr">Italie</country>
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<author><name sortKey="Logan, David C" sort="Logan, David C" uniqKey="Logan D" first="David C" last="Logan">David C. Logan</name>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Université d'Angers, INRA, Agrocampus Ouest, UMR 1345 Institut de Recherche en Horticulture et Semences, F-49045 Angers</wicri:regionArea>
</affiliation>
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<author><name sortKey="Fuchs, Philippe" sort="Fuchs, Philippe" uniqKey="Fuchs P" first="Philippe" last="Fuchs">Philippe Fuchs</name>
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<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn</wicri:regionArea>
</affiliation>
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<author><name sortKey="Carraretto, Luca" sort="Carraretto, Luca" uniqKey="Carraretto L" first="Luca" last="Carraretto">Luca Carraretto</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Biology, University of Padova, 35121 Padova</wicri:regionArea>
</affiliation>
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<author><name sortKey="Teardo, Enrico" sort="Teardo, Enrico" uniqKey="Teardo E" first="Enrico" last="Teardo">Enrico Teardo</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Biology, University of Padova, 35121 Padova</wicri:regionArea>
</affiliation>
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<author><name sortKey="Cendron, Laura" sort="Cendron, Laura" uniqKey="Cendron L" first="Laura" last="Cendron">Laura Cendron</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Biology, University of Padova, 35121 Padova</wicri:regionArea>
</affiliation>
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<author><name sortKey="Nietzel, Thomas" sort="Nietzel, Thomas" uniqKey="Nietzel T" first="Thomas" last="Nietzel">Thomas Nietzel</name>
<affiliation wicri:level="1"><nlm:affiliation>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Fu L, Magdalena" sort="Fu L, Magdalena" uniqKey="Fu L M" first="Magdalena" last="Fü L">Magdalena Fü L</name>
<affiliation wicri:level="1"><nlm:affiliation>Plant Proteomics Group, Max-Planck-Institute for Plant Breeding Research, 50829 Cologne, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Plant Proteomics Group, Max-Planck-Institute for Plant Breeding Research, 50829 Cologne</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Doccula, Fabrizio G" sort="Doccula, Fabrizio G" uniqKey="Doccula F" first="Fabrizio G" last="Doccula">Fabrizio G. Doccula</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biosciences, University of Milan, 20133 Milan, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Biosciences, University of Milan, 20133 Milan</wicri:regionArea>
</affiliation>
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<author><name sortKey="Navazio, Lorella" sort="Navazio, Lorella" uniqKey="Navazio L" first="Lorella" last="Navazio">Lorella Navazio</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Biology, University of Padova, 35121 Padova</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Fricker, Mark D" sort="Fricker, Mark D" uniqKey="Fricker M" first="Mark D" last="Fricker">Mark D. Fricker</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom.</nlm:affiliation>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Plant Sciences, University of Oxford, Oxford OX1 3RB</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Van Aken, Olivier" sort="Van Aken, Olivier" uniqKey="Van Aken O" first="Olivier" last="Van Aken">Olivier Van Aken</name>
<affiliation wicri:level="1"><nlm:affiliation>ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Finkemeier, Iris" sort="Finkemeier, Iris" uniqKey="Finkemeier I" first="Iris" last="Finkemeier">Iris Finkemeier</name>
<affiliation wicri:level="1"><nlm:affiliation>Plant Proteomics Group, Max-Planck-Institute for Plant Breeding Research, 50829 Cologne, Germany Institute for Plant Biology and Biotechnology, University of Münster, 48149 Münster, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Plant Proteomics Group, Max-Planck-Institute for Plant Breeding Research, 50829 Cologne, Germany Institute for Plant Biology and Biotechnology, University of Münster, 48149 Münster</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Meyer, Andreas J" sort="Meyer, Andreas J" uniqKey="Meyer A" first="Andreas J" last="Meyer">Andreas J. Meyer</name>
<affiliation wicri:level="1"><nlm:affiliation>Department Chemical Signalling, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Department Chemical Signalling, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Szab, Ildik" sort="Szab, Ildik" uniqKey="Szab I" first="Ildik" last="Szab">Ildik Szab</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Biology, University of Padova, 35121 Padova</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Costa, Alex" sort="Costa, Alex" uniqKey="Costa A" first="Alex" last="Costa">Alex Costa</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biosciences, University of Milan, 20133 Milan, Italy Institute of Biophysics, Consiglio Nazionale delle Ricerche, 20133 Milan, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Biosciences, University of Milan, 20133 Milan, Italy Institute of Biophysics, Consiglio Nazionale delle Ricerche, 20133 Milan</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Schwarzl Nder, Markus" sort="Schwarzl Nder, Markus" uniqKey="Schwarzl Nder M" first="Markus" last="Schwarzl Nder">Markus Schwarzl Nder</name>
<affiliation wicri:level="1"><nlm:affiliation>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany markus.schwarzlander@uni-bonn.de.</nlm:affiliation>
<country wicri:rule="url">Allemagne</country>
<wicri:regionArea>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn</wicri:regionArea>
</affiliation>
</author>
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<series><title level="j">The Plant cell</title>
<idno type="eISSN">1532-298X</idno>
<imprint><date when="2015" type="published">2015</date>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Arabidopsis (genetics)</term>
<term>Arabidopsis (metabolism)</term>
<term>Arabidopsis Proteins (metabolism)</term>
<term>Calcium</term>
<term>Calcium Signaling</term>
<term>Calcium-Binding Proteins (metabolism)</term>
<term>Cell Respiration</term>
<term>Cytosol (metabolism)</term>
<term>DNA, Bacterial (genetics)</term>
<term>EF Hand Motifs</term>
<term>Mitochondria (metabolism)</term>
<term>Mitochondria (ultrastructure)</term>
<term>Mutagenesis, Insertional (genetics)</term>
<term>Phylogeny</term>
<term>Plant Roots (metabolism)</term>
<term>Plant Roots (ultrastructure)</term>
<term>Protein Binding</term>
<term>Protein Transport</term>
<term>Seedlings (metabolism)</term>
<term>Sequence Homology, Amino Acid</term>
<term>Subcellular Fractions (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>ADN bactérien (génétique)</term>
<term>Arabidopsis (génétique)</term>
<term>Arabidopsis (métabolisme)</term>
<term>Calcium</term>
<term>Cytosol (métabolisme)</term>
<term>Fractions subcellulaires (métabolisme)</term>
<term>Liaison aux protéines</term>
<term>Mitochondries (métabolisme)</term>
<term>Mitochondries (ultrastructure)</term>
<term>Motifs EF Hands</term>
<term>Mutagenèse par insertion (génétique)</term>
<term>Phylogénie</term>
<term>Plant (métabolisme)</term>
<term>Protéines d'Arabidopsis (métabolisme)</term>
<term>Protéines de liaison au calcium (métabolisme)</term>
<term>Racines de plante (métabolisme)</term>
<term>Racines de plante (ultrastructure)</term>
<term>Respiration cellulaire</term>
<term>Signalisation du calcium</term>
<term>Similitude de séquences d'acides aminés</term>
<term>Transport de protéines</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>DNA, Bacterial</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Arabidopsis Proteins</term>
<term>Calcium-Binding Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Arabidopsis</term>
<term>Mutagenesis, Insertional</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>ADN bactérien</term>
<term>Arabidopsis</term>
<term>Mutagenèse par insertion</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Arabidopsis</term>
<term>Cytosol</term>
<term>Mitochondria</term>
<term>Plant Roots</term>
<term>Seedlings</term>
<term>Subcellular Fractions</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Arabidopsis</term>
<term>Cytosol</term>
<term>Fractions subcellulaires</term>
<term>Mitochondries</term>
<term>Plant</term>
<term>Protéines d'Arabidopsis</term>
<term>Protéines de liaison au calcium</term>
<term>Racines de plante</term>
</keywords>
<keywords scheme="MESH" qualifier="ultrastructure" xml:lang="en"><term>Mitochondria</term>
<term>Plant Roots</term>
</keywords>
<keywords scheme="MESH" type="chemical" xml:lang="en"><term>Calcium</term>
<term>Calcium Signaling</term>
<term>Cell Respiration</term>
<term>EF Hand Motifs</term>
<term>Phylogeny</term>
<term>Protein Binding</term>
<term>Protein Transport</term>
<term>Sequence Homology, Amino Acid</term>
</keywords>
<keywords scheme="MESH" qualifier="ultrastructure" xml:lang="fr"><term>Calcium</term>
<term>Liaison aux protéines</term>
<term>Mitochondries</term>
<term>Motifs EF Hands</term>
<term>Phylogénie</term>
<term>Racines de plante</term>
<term>Respiration cellulaire</term>
<term>Signalisation du calcium</term>
<term>Similitude de séquences d'acides aminés</term>
<term>Transport de protéines</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en">Plant organelle function must constantly adjust to environmental conditions, which requires dynamic coordination. Ca(2+) signaling may play a central role in this process. Free Ca(2+) dynamics are tightly regulated and differ markedly between the cytosol, plastid stroma, and mitochondrial matrix. The mechanistic basis of compartment-specific Ca(2+) dynamics is poorly understood. Here, we studied the function of At-MICU, an EF-hand protein of Arabidopsis thaliana with homology to constituents of the mitochondrial Ca(2+) uniporter machinery in mammals. MICU binds Ca(2+) and localizes to the mitochondria in Arabidopsis. In vivo imaging of roots expressing a genetically encoded Ca(2+) sensor in the mitochondrial matrix revealed that lack of MICU increased resting concentrations of free Ca(2+) in the matrix. Furthermore, Ca(2+) elevations triggered by auxin and extracellular ATP occurred more rapidly and reached higher maximal concentrations in the mitochondria of micu mutants, whereas cytosolic Ca(2+) signatures remained unchanged. These findings support the idea that a conserved uniporter system, with composition and regulation distinct from the mammalian machinery, mediates mitochondrial Ca(2+) uptake in plants under in vivo conditions. They further suggest that MICU acts as a throttle that controls Ca(2+) uptake by moderating influx, thereby shaping Ca(2+) signatures in the matrix and preserving mitochondrial homeostasis. Our results open the door to genetic dissection of mitochondrial Ca(2+) signaling in plants.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26530087</PMID>
<DateCreated><Year>2015</Year>
<Month>12</Month>
<Day>15</Day>
</DateCreated>
<DateCompleted><Year>2016</Year>
<Month>09</Month>
<Day>26</Day>
</DateCompleted>
<DateRevised><Year>2017</Year>
<Month>02</Month>
<Day>20</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-298X</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>27</Volume>
<Issue>11</Issue>
<PubDate><Year>2015</Year>
<Month>Nov</Month>
</PubDate>
</JournalIssue>
<Title>The Plant cell</Title>
<ISOAbbreviation>Plant Cell</ISOAbbreviation>
</Journal>
<ArticleTitle>The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis.</ArticleTitle>
<Pagination><MedlinePgn>3190-212</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1105/tpc.15.00509</ELocationID>
<Abstract><AbstractText>Plant organelle function must constantly adjust to environmental conditions, which requires dynamic coordination. Ca(2+) signaling may play a central role in this process. Free Ca(2+) dynamics are tightly regulated and differ markedly between the cytosol, plastid stroma, and mitochondrial matrix. The mechanistic basis of compartment-specific Ca(2+) dynamics is poorly understood. Here, we studied the function of At-MICU, an EF-hand protein of Arabidopsis thaliana with homology to constituents of the mitochondrial Ca(2+) uniporter machinery in mammals. MICU binds Ca(2+) and localizes to the mitochondria in Arabidopsis. In vivo imaging of roots expressing a genetically encoded Ca(2+) sensor in the mitochondrial matrix revealed that lack of MICU increased resting concentrations of free Ca(2+) in the matrix. Furthermore, Ca(2+) elevations triggered by auxin and extracellular ATP occurred more rapidly and reached higher maximal concentrations in the mitochondria of micu mutants, whereas cytosolic Ca(2+) signatures remained unchanged. These findings support the idea that a conserved uniporter system, with composition and regulation distinct from the mammalian machinery, mediates mitochondrial Ca(2+) uptake in plants under in vivo conditions. They further suggest that MICU acts as a throttle that controls Ca(2+) uptake by moderating influx, thereby shaping Ca(2+) signatures in the matrix and preserving mitochondrial homeostasis. Our results open the door to genetic dissection of mitochondrial Ca(2+) signaling in plants.</AbstractText>
<CopyrightInformation>© 2015 American Society of Plant Biologists. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wagner</LastName>
<ForeName>Stephan</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-5369-7911</Identifier>
<AffiliationInfo><Affiliation>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Behera</LastName>
<ForeName>Smrutisanjita</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-8749-6130</Identifier>
<AffiliationInfo><Affiliation>Department of Biosciences, University of Milan, 20133 Milan, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>De Bortoli</LastName>
<ForeName>Sara</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-3797-6966</Identifier>
<AffiliationInfo><Affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Logan</LastName>
<ForeName>David C</ForeName>
<Initials>DC</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-8980-240X</Identifier>
<AffiliationInfo><Affiliation>Université d'Angers, INRA, Agrocampus Ouest, UMR 1345 Institut de Recherche en Horticulture et Semences, F-49045 Angers, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Fuchs</LastName>
<ForeName>Philippe</ForeName>
<Initials>P</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-6379-853X</Identifier>
<AffiliationInfo><Affiliation>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Carraretto</LastName>
<ForeName>Luca</ForeName>
<Initials>L</Initials>
<AffiliationInfo><Affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Teardo</LastName>
<ForeName>Enrico</ForeName>
<Initials>E</Initials>
<AffiliationInfo><Affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Cendron</LastName>
<ForeName>Laura</ForeName>
<Initials>L</Initials>
<AffiliationInfo><Affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Nietzel</LastName>
<ForeName>Thomas</ForeName>
<Initials>T</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-1934-1732</Identifier>
<AffiliationInfo><Affiliation>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Füßl</LastName>
<ForeName>Magdalena</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Plant Proteomics Group, Max-Planck-Institute for Plant Breeding Research, 50829 Cologne, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Doccula</LastName>
<ForeName>Fabrizio G</ForeName>
<Initials>FG</Initials>
<AffiliationInfo><Affiliation>Department of Biosciences, University of Milan, 20133 Milan, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Navazio</LastName>
<ForeName>Lorella</ForeName>
<Initials>L</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-5640-108X</Identifier>
<AffiliationInfo><Affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Fricker</LastName>
<ForeName>Mark D</ForeName>
<Initials>MD</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-8942-6897</Identifier>
<AffiliationInfo><Affiliation>Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Van Aken</LastName>
<ForeName>Olivier</ForeName>
<Initials>O</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-4024-968X</Identifier>
<AffiliationInfo><Affiliation>ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Finkemeier</LastName>
<ForeName>Iris</ForeName>
<Initials>I</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-8972-4026</Identifier>
<AffiliationInfo><Affiliation>Plant Proteomics Group, Max-Planck-Institute for Plant Breeding Research, 50829 Cologne, Germany Institute for Plant Biology and Biotechnology, University of Münster, 48149 Münster, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Meyer</LastName>
<ForeName>Andreas J</ForeName>
<Initials>AJ</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-8144-4364</Identifier>
<AffiliationInfo><Affiliation>Department Chemical Signalling, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Szabò</LastName>
<ForeName>Ildikò</ForeName>
<Initials>I</Initials>
<AffiliationInfo><Affiliation>Department of Biology, University of Padova, 35121 Padova, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Costa</LastName>
<ForeName>Alex</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-2628-1176</Identifier>
<AffiliationInfo><Affiliation>Department of Biosciences, University of Milan, 20133 Milan, Italy Institute of Biophysics, Consiglio Nazionale delle Ricerche, 20133 Milan, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Schwarzländer</LastName>
<ForeName>Markus</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-0796-8308</Identifier>
<AffiliationInfo><Affiliation>Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany markus.schwarzlander@uni-bonn.de.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2015</Year>
<Month>11</Month>
<Day>03</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>Plant Cell</MedlineTA>
<NlmUniqueID>9208688</NlmUniqueID>
<ISSNLinking>1040-4651</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D029681">Arabidopsis Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D002135">Calcium-Binding Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D004269">DNA, Bacterial</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C000610965">MICU protein, Arabidopsis</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C036483">T-DNA</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>SY7Q814VUP</RegistryNumber>
<NameOfSubstance UI="D002118">Calcium</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
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