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

Wagner, Stephan ; Behera, Smrutisanjita ; De Bortoli, Sara ; Logan, David C ; Fuchs, Philippe ; Carraretto, Luca ; Teardo, Enrico ; Cendron, Laura ; Nietzel, Thomas and Füßl, Magdalena , et al. (2015) In Plant Cell 27(11). p.212-3190
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... (More)

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.

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@article{e194396e-b886-41df-a641-7f82201cd6eb,
  abstract     = {{<p>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.</p>}},
  author       = {{Wagner, Stephan and Behera, Smrutisanjita and De Bortoli, Sara and Logan, David C and Fuchs, Philippe and Carraretto, Luca and Teardo, Enrico and Cendron, Laura and Nietzel, Thomas and Füßl, Magdalena and Doccula, Fabrizio G and Navazio, Lorella and Fricker, Mark D and Van Aken, Olivier and Finkemeier, Iris and Meyer, Andreas J and Szabò, Ildikò and Costa, Alex and Schwarzländer, Markus}},
  issn         = {{1040-4651}},
  keywords     = {{Arabidopsis; Arabidopsis Proteins; Calcium; Calcium Signaling; Calcium-Binding Proteins; Cell Respiration; Cytosol; DNA, Bacterial; EF Hand Motifs; Mitochondria; Mutagenesis, Insertional; Phylogeny; Plant Roots; Protein Binding; Protein Transport; Seedlings; Sequence Homology, Amino Acid; Subcellular Fractions; Journal Article; Research Support, Non-U.S. Gov't}},
  language     = {{eng}},
  number       = {{11}},
  pages        = {{212--3190}},
  publisher    = {{American Society of Plant Biologists}},
  series       = {{Plant Cell}},
  title        = {{The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis}},
  url          = {{http://dx.doi.org/10.1105/tpc.15.00509}},
  doi          = {{10.1105/tpc.15.00509}},
  volume       = {{27}},
  year         = {{2015}},
}