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The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis.

Identifieur interne : 002646 ( PubMed/Curation ); précédent : 002645; suivant : 002647

The 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 :

RBID : pubmed:26530087

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English descriptors

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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<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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<name sortKey="Navazio, Lorella" sort="Navazio, Lorella" uniqKey="Navazio L" first="Lorella" last="Navazio">Lorella Navazio</name>
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<nlm:affiliation>Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom.</nlm:affiliation>
<country xml:lang="fr">Royaume-Uni</country>
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<name sortKey="Finkemeier, Iris" sort="Finkemeier, Iris" uniqKey="Finkemeier I" first="Iris" last="Finkemeier">Iris Finkemeier</name>
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<name sortKey="Costa, Alex" sort="Costa, Alex" uniqKey="Costa A" first="Alex" last="Costa">Alex Costa</name>
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<nlm:affiliation>Department of Biosciences, University of Milan, 20133 Milan, Italy Institute of Biophysics, Consiglio Nazionale delle Ricerche, 20133 Milan, Italy.</nlm:affiliation>
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<wicri:regionArea>Department of Biosciences, University of Milan, 20133 Milan, Italy Institute of Biophysics, Consiglio Nazionale delle Ricerche, 20133 Milan</wicri:regionArea>
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<name sortKey="Behera, Smrutisanjita" sort="Behera, Smrutisanjita" uniqKey="Behera S" first="Smrutisanjita" last="Behera">Smrutisanjita Behera</name>
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<nlm:affiliation>Department of Biosciences, University of Milan, 20133 Milan, Italy.</nlm:affiliation>
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<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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<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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<nlm:affiliation>Université d'Angers, INRA, Agrocampus Ouest, UMR 1345 Institut de Recherche en Horticulture et Semences, F-49045 Angers, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<name sortKey="Fuchs, Philippe" sort="Fuchs, Philippe" uniqKey="Fuchs P" first="Philippe" last="Fuchs">Philippe Fuchs</name>
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<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>
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<name sortKey="Carraretto, Luca" sort="Carraretto, Luca" uniqKey="Carraretto L" first="Luca" last="Carraretto">Luca Carraretto</name>
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<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>
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<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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<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>
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<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>
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<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>
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<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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<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>
</author>
<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>
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<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>
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<name sortKey="Szab, Ildik" sort="Szab, Ildik" uniqKey="Szab I" first="Ildik" last="Szab">Ildik Szab</name>
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<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>
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</analytic>
<series>
<title level="j">The Plant cell</title>
<idno type="eISSN">1532-298X</idno>
<imprint>
<date when="2015" type="published">2015</date>
</imprint>
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<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>
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<Language>eng</Language>
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<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2015</Year>
<Month>11</Month>
<Day>03</Day>
</ArticleDate>
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<Country>United States</Country>
<MedlineTA>Plant Cell</MedlineTA>
<NlmUniqueID>9208688</NlmUniqueID>
<ISSNLinking>1040-4651</ISSNLinking>
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<Chemical>
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<NameOfSubstance UI="D004269">DNA, Bacterial</NameOfSubstance>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C000610965">MICU protein, Arabidopsis</NameOfSubstance>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C036483">T-DNA</NameOfSubstance>
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<Chemical>
<RegistryNumber>SY7Q814VUP</RegistryNumber>
<NameOfSubstance UI="D002118">Calcium</NameOfSubstance>
</Chemical>
</ChemicalList>
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