title: The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis.
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.
authors.affiliation: Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.
authors.forename: Stephan
authors.identifier: http://orcid.org/0000-0001-5369-7911
authors.initials: S
authors.lastname: Wagner
authors.affiliation: Department of Biosciences, University of Milan, 20133 Milan, Italy.
authors.forename: Smrutisanjita
authors.identifier: http://orcid.org/0000-0001-8749-6130
authors.initials: S
authors.lastname: Behera
authors.affiliation: Department of Biology, University of Padova, 35121 Padova, Italy.
authors.forename: Sara
authors.identifier: http://orcid.org/0000-0003-3797-6966
authors.initials: S
authors.lastname: De Bortoli
authors.affiliation: Université d'Angers, INRA, Agrocampus Ouest, UMR 1345 Institut de Recherche en Horticulture et Semences, F-49045 Angers, France.
authors.forename: David C
authors.identifier: http://orcid.org/0000-0002-8980-240X
authors.initials: DC
authors.lastname: Logan
authors.affiliation: Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.
authors.forename: Philippe
authors.identifier: http://orcid.org/0000-0001-6379-853X
authors.initials: P
authors.lastname: Fuchs
authors.affiliation: Department of Biology, University of Padova, 35121 Padova, Italy.
authors.forename: Luca
authors.initials: L
authors.lastname: Carraretto
authors.affiliation: Department of Biology, University of Padova, 35121 Padova, Italy.
authors.forename: Enrico
authors.initials: E
authors.lastname: Teardo
authors.affiliation: Department of Biology, University of Padova, 35121 Padova, Italy.
authors.forename: Laura
authors.initials: L
authors.lastname: Cendron
authors.affiliation: Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.
authors.forename: Thomas
authors.identifier: http://orcid.org/0000-0002-1934-1732
authors.initials: T
authors.lastname: Nietzel
authors.affiliation: Plant Proteomics Group, Max-Planck-Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Magdalena
authors.initials: M
authors.lastname: Füßl
authors.affiliation: Department of Biosciences, University of Milan, 20133 Milan, Italy.
authors.forename: Fabrizio G
authors.initials: FG
authors.lastname: Doccula
authors.affiliation: Department of Biology, University of Padova, 35121 Padova, Italy.
authors.forename: Lorella
authors.identifier: http://orcid.org/0000-0001-5640-108X
authors.initials: L
authors.lastname: Navazio
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom.
authors.forename: Mark D
authors.identifier: http://orcid.org/0000-0002-8942-6897
authors.initials: MD
authors.lastname: Fricker
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009, Australia.
authors.forename: Olivier
authors.identifier: http://orcid.org/0000-0003-4024-968X
authors.initials: O
authors.lastname: Van Aken
authors.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.
authors.forename: Iris
authors.identifier: http://orcid.org/0000-0002-8972-4026
authors.initials: I
authors.lastname: Finkemeier
authors.affiliation: Department Chemical Signalling, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany.
authors.forename: Andreas J
authors.identifier: http://orcid.org/0000-0001-8144-4364
authors.initials: AJ
authors.lastname: Meyer
authors.affiliation: Department of Biology, University of Padova, 35121 Padova, Italy.
authors.forename: Ildikò
authors.initials: I
authors.lastname: Szabò
authors.affiliation: Department of Biosciences, University of Milan, 20133 Milan, Italy Institute of Biophysics, Consiglio Nazionale delle Ricerche, 20133 Milan, Italy.
authors.forename: Alex
authors.identifier: http://orcid.org/0000-0002-2628-1176
authors.initials: A
authors.lastname: Costa
authors.affiliation: Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation, University of Bonn, 53113 Bonn, Germany markus.schwarzlander@uni-bonn.de.
authors.forename: Markus
authors.identifier: http://orcid.org/0000-0003-0796-8308
authors.initials: M
authors.lastname: Schwarzländer
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D002118:Calcium; D020013:Calcium Signaling; D002135:Calcium-Binding Proteins / Q000378:metabolism*; D019069:Cell Respiration; D003600:Cytosol / Q000378:metabolism; D004269:DNA, Bacterial / Q000235:genetics; D020832:EF Hand Motifs; D008928:Mitochondria / Q000378:metabolism* / Q000648:ultrastructure; D016254:Mutagenesis, Insertional / Q000235:genetics; D010802:Phylogeny; D018517:Plant Roots / Q000378:metabolism / Q000648:ultrastructure; D011485:Protein Binding; D021381:Protein Transport; D036226:Seedlings / Q000378:metabolism; D017386:Sequence Homology, Amino Acid; D013347:Subcellular Fractions / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D002135:Calcium-Binding Proteins; D004269:DNA, Bacterial; C000610965:MICU protein, Arabidopsis; C036483:T-DNA; D002118:Calcium