Advanced

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.

(Less)
Please use this url to cite or link to this publication:
@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},
  keyword      = {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},
  volume       = {27},
  year         = {2015},
}