Teardo, E.; Department of Biology, University of Padova, Padova, Italy, CNR Institute of Neuroscience, Padova, Italy, Department of Biomedical Sciences, University of Padua, Padova, Italy
Carraretto, L.; Department of Biology, University of Padova, Padova, Italy
Wagner, S.; Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany
Formentin, E.; Department of Biology, University of Padova, Padova, Italy
Behera, S.; Department of Biosciences, University of Milan, Milan, Italy
De Bortoli, S.; Department of Biology, University of Padova, Padova, Italy
Larosa, Véronique ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Fuchs, P.; Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany
Lo Schiavo, F.; Department of Biology, University of Padova, Padova, Italy
Raffaello, A.; Department of Biomedical Sciences, University of Padova, Padova, Italy
Rizzuto, R.; Department of Biomedical Sciences, University of Padova, Padova, Italy
Costa, A.; Department of Biosciences, University of Milan, Milan, Italy, Institute of Biophysics, Consiglio Nazionale delle Ricerche, Milan, Italy
Schwarzländer, M.; Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany
Szabò, I.; Department of Biology, University of Padova, Padova, Italy, CNR Institute of Neuroscience, Padova, Italy, Department of Biomedical Sciences, University of Padua, Padova, Italy
Akerman KE, Moore AL (1983) Phosphate dependent, ruthenium red insensitive Ca2+ uptake in mung bean mitochondria. Biochem Biophys Res Commun 114: 1176–1181
Antony AN, Paillard M, Moffat C, Juskeviciute E, Correnti J, Bolon B, Rubin E, Csordás G, Seifert EL, Hoek JB, Hajnóczky G (2016) MICU1 regulation of mitochondrial Ca2+ uptake dictates survival and tissue regeneration. Nat Commun 7: 10955
Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot (Lond) 103: 581–597
Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, et al (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476: 341–345
Behera S, Kudla J (2013) High-resolution imaging of cytoplasmic Ca2+ dynamics in Arabidopsis roots. Cold Spring Harb Protoc 2013: 669–672
Bick AG, Calvo SE, Mootha VK (2012) Evolutionary diversity of the mitochondrial calcium uniporter. Science 336: 886
Braun CJ, Lachnit C, Becker P, Henkes LM, Arrigoni C, Kast SM, Moroni A, Thiel G, Schroeder I (2014) Viral potassium channels as a robust model system for studies of membrane-protein interaction. Biochim Biophys Acta 1838: 1096–1103
Braun HP, Binder S, Brennicke A, Eubel H, Fernie AR, Finkemeier I, Klodmann J, König AC, Kühn K, Meyer E, et al (2014) The life of plant mitochondrial complex I. Mitochondrion 19: 295–313
Carnieri EG, Martins IS, Vercesi AE (1987) The mechanism and biological role of calcium transport by plant mitochondria. Braz J Med Biol Res 20: 635–638
Carraretto L, Formentin E, Teardo E, Checchetto V, Tomizioli M, Morosinotto T, Giacometti GM, Finazzi G, Szabó I (2013) A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants. Science 342: 114–118
Carraretto L, Teardo E, Checchetto V, Finazzi G, Uozumi N, Szabò I (2016) Ion channels in plant bioenergetic organelles chloroplast and mitochondria: from molecular identification to function. Mol Plant 9: 371–395
Chaudhuri D, Sancak Y, Mootha VK, Clapham DE (2013) MCU encodes the pore conducting mitochondrial calcium currents. eLife 2: e00704
Curtis MD, Grossniklaus U (2003) A Gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462–469
de Longevialle AF, Meyer EH, Andrés C, Taylor NL, Lurin C, Millar AH, Small ID (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell 19: 3256–3265
De Marchi U, Checchetto V, Zanetti M, Teardo E, Soccio M, Formentin E, Giacometti GM, Pastore D, Zoratti M, Szabò I (2010) ATP-sensitive cation-channel in wheat (Triticum durum Desf.): identification and characterization of a plant mitochondrial channel by patch-clamp. Cell Physiol Biochem 26: 975–982
De Stefani D, Patron M, Rizzuto R (2015) Structure and function of the mitochondrial calcium uniporter complex. Biochim Biophys Acta 1853: 2006–2011
De Stefani D, Raffaello A, Teardo E, Szabò I, Rizzuto R (2011) A fortykilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476: 336–340
Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322: 1380–1384
Deniaud A, Liguori L, Blesneac I, Lenormand JL, Pebay-Peyroula E (2010) Crystallization of the membrane protein hVDAC1 produced in cell-free system. Biochim Biophys Acta 1798: 1540–1546
Dieter P, Marmé D (1980) Ca2+ transport in mitochondrial and microsomal fractions from higher plants. Planta 150: 1–8
Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61: 593–620
Fester T, Hause G (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15: 373–379
Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442–446
Foskett JK, Philipson B (2015) The mitochondrial Ca2+ uniporter complex. J Mol Cell Cardiol 78: 3–8
Hanson JB, Malhotra SS, Stoner CD (1965) Action of calcium on corn mitochondria. Plant Physiol 40: 1033–1040
Herdean A, Teardo E, Nilsson AK, Pfeil BE, Johansson ON, Ünnep R, Nagy G, Zsiros O, Dana S, Solymosi K, et al (2016) A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat Commun 7: 11654
Hess P, Tsien RW (1984) Mechanism of ion permeation through calcium channels. Nature 309: 453–456
Hille B (1978) Ionic channels in excitable membranes. Current problems and biophysical approaches. Biophys J 22: 283–294
Huang G, Vercesi AE, Docampo R (2013) Essential regulation of cell bioenergetics in Trypanosoma brucei by the mitochondrial calcium uniporter. Nat Commun 4: 2865
Huang S, Millar AH (2013) Succinate dehydrogenase: the complex roles of a simple enzyme. Curr Opin Plant Biol 16: 344–349
Huang S, Van Aken O, Schwarzländer M, Belt K, Millar AH (2016) Roles of mitochondrial reactive oxygen species in cellular signalling and stress response in plants. Plant Physiol 171: 1551–1559
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755
Jardim-Messeder D, Caverzan A, Rauber R, de Souza Ferreira E, Margis-Pinheiro M, Galina A (2015) Succinate dehydrogenase (mitochondrial complex II) is a source of reactive oxygen species in plants and regulates development and stress responses. New Phytol 208: 776–789
Jia L (2011) Is reactive oxygen species (ROS) the underlying factor for inhibited root growth in Osspr1? Plant Signal Behav 6: 1024–1025
Karniely S, Pines O (2005) Single translation–dual destination: mechanisms of dual protein targeting in eukaryotes. EMBO Rep 6: 420–425
Kirichok Y, Krapivinsky G, Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427: 360–364
Klodmann J, Senkler M, Rode C, Braun HP (2011) Defining the protein complex proteome of plant mitochondria. Plant Physiol 157: 587–598
Kmiecik P, Leonardelli M, Teige M (2016) Novel connections in plant organellar signalling link different stress responses and signalling pathways. J Exp Bot 67: 3793–3807
Kovács-Bogdán E, Sancak Y, Kamer KJ, Plovanich M, Jambhekar A, Huber RJ, Myre MA, Blower MD, Mootha VK (2014) Reconstitution of the mitochondrial calcium uniporter in yeast. Proc Natl Acad Sci USA 111: 8985–8990
Larosa V, Coosemans N, Motte P, Bonnefoy N, Remacle C (2012) Reconstruction of a human mitochondrial complex I mutation in the unicellular green alga Chlamydomonas. Plant J 70: 759–768
Lee CP, Eubel H, O’Toole N, Millar AH (2008) Heterogeneity of the mitochondrial proteome for photosynthetic and non-photosynthetic Arabidopsis metabolism. Mol Cell Proteomics 7: 1297–1316
Lepple-Wienhues A, Cahalan MD (1996) Conductance and permeation of monovalent cations through depletion-activated Ca2+ channels (ICRAC) in Jurkat T cells. Biophys J 71: 787–794
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 25: 402–408
Logan CV, Szabadkai G, Sharpe JA, Parry DA, Torelli S, Childs AM, Kriek M, Phadke R, Johnson CA, Roberts NY, et al; UK10K Consortium (2014) Loss-of-function mutations in MICU1 cause a brain and muscle disorder linked to primary alterations in mitochondrial calcium signaling. Nat Genet 46: 188–193
Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133: 21–24
Logan DC, Leaver CJ (2000) Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. J Exp Bot 51: 865–871
Loro G, Drago I, Pozzan T, Schiavo FL, Zottini M, Costa A (2012) Targeting of Cameleons to various subcellular compartments reveals a strict cytoplasmic/mitochondrial Ca2+ handling relationship in plant cells. Plant J 71: 1–13
Love J, Dodd AN, Webb AA (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16: 956–966
Mallilankaraman K, Cárdenas C, Doonan PJ, Chandramoorthy HC, Irrinki KM, Golenár T, Csordás G, Madireddi P, Yang J, Müller M, et al (2012) MCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism. Nat Cell Biol 14: 1336–1343
Mammucari C, Gherardi G, Zamparo I, Raffaello A, Boncompagni S, Chemello F, Cagnin S, Braga A, Zanin S, Pallafacchina G, et al (2015) The mitochondrial calcium uniporter controls skeletal muscle trophism in vivo. Cell Reports 10: 1269–1279
Lee Y, Min CK, Kim TG, Song HK, Lim Y, Kim D, Shin K, Kang M, Kang JY, Youn HS, et al (2015) Structure and function of the N-terminal domain of the human mitochondrial calcium uniporter. EMBO Rep 16: 1318–1333
Martins IS, Vercesi AE (1985) Some characteristics of Ca2+ transport in plant mitochondria. Biochem Biophys Res Commun 129: 943–948
McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181: 275–294
Meng Q, Chen Y, Zhang M, Chen Y, Yuan J, Murray SC (2015) Molecular characterization and phylogenetic analysis of Zm MCUs in maize. Biologia 70: 599–605
Millar AH, Eubel H, Jänsch L, Kruft V, Heazlewood JL, Braun HP (2004) Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol Biol 56: 77–90
Murphy E, Pan X, Nguyen T, Liu J, Holmström KM, Finkel T (2014) Unresolved questions from the analysis of mice lacking MCU expression. Biochem Biophys Res Commun 449: 384–385
Nomura H, Shiina T (2014) Calcium signaling in plant endosymbiotic organelles: mechanism and role in physiology. Mol Plant 7: 1094–1104
Oxenoid K, Dong Y, Cao C, Cui T, Sancak Y, Markhard AL, Grabarek Z, Kong L, Liu Z, Ouyang B, et al (2016) Architecture of the mitochondrial calcium uniporter. Nature 533: 269–273
Pan X, Liu J, Nguyen T, Liu C, Sun J, Teng Y, Fergusson MM, Rovira II, Allen M, Springer DA, et al (2013) The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter. Nat Cell Biol 15: 1464–1472
Patron M, Checchetto V, Raffaello A, Teardo E, Vecellio Reane D, Mantoan M, Granatiero V, Szabò I, De Stefani D, Rizzuto R (2014) MICU1 and MICU2 finely tune the mitochondrial Ca2+ uniporter by exerting opposite effects on MCU activity. Mol Cell 53: 726–737
Paupe V, Prudent J, Dassa EP, Rendon OZ, Shoubridge EA (2015) CCDC90A (MCUR1) is a cytochrome c oxidase assembly factor and not a regulator of the mitochondrial calcium uniporter. Cell Metab 21: 109–116
Perocchi F, Gohil VM, Girgis HS, Bao XR, McCombs JE, Palmer AE, Mootha VK (2010) MICU1 encodes a mitochondrial EF hand protein required for Ca2+ uptake. Nature 467: 291–296
Petrungaro C, Zimmermann KM, Küttner V, Fischer M, Dengjel J, Bogeski I, Riemer J (2015) The Ca2+-dependent release of the Mia40-induced MICU1-MICU2 dimer from MCU regulates mitochondrial Ca2+ uptake. Cell Metab 22: 721–733
Plovanich M, Bogorad RL, Sancak Y, Kamer KJ, Strittmatter L, Li AA, Girgis HS, Kuchimanchi S, De Groot J, Speciner L, et al (2013) MICU2, a paralog of MICU1, resides within the mitochondrial uniporter complex to regulate calcium handling. PLoS One 8: e55785
Prudent J, Popgeorgiev N, Bonneau B, Thibaut J, Gadet R, Lopez J, Gonzalo P, Rimokh R, Manon S, Houart C, et al (2013) Bcl-wav and the mitochondrial calcium uniporter drive gastrula morphogenesis in zebrafish. Nat Commun 4: 2330
Pu X, Lv X, Tan T, Fu F, Qin G, Lin H (2015) Roles of mitochondrial energy dissipation systems in plant development and acclimation to stress. Ann Bot (Lond) 116: 583–600
Quan X, Nguyen TT, Choi SK, Xu S, Das R, Cha SK, Kim N, Han J, Wiederkehr A, Wollheim CB, et al (2015) Essential role of mitochondrial Ca2+ uniporter in the generation of mitochondrial pH gradient and metabolism-secretion coupling in insulin-releasing cells. J Biol Chem 290: 4086–4096
Raffaello A, De Stefani D, Sabbadin D, Teardo E, Merli G, Picard A, Checchetto V, Moro S, Szabò I, Rizzuto R (2013) The mitochondrial calcium uniporter is a multimer that can include a dominant-negative pore-forming subunit. EMBO J 32: 2362–2376
Rasmussen TP, Wu Y, Joiner ML, Koval OM, Wilson NR, Luczak ED, Wang Q, Chen B, Gao Z, Zhu Z, et al (2015) Inhibition of MCU forces extramitochondrial adaptations governing physiological and pathological stress responses in heart. Proc Natl Acad Sci USA 112: 9129–9134
Rizzuto R, De Stefani D, Raffaello A, Mammucari C (2012) Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 13: 566–578
Sancak Y, Markhard AL, Kitami T, Kovács-Bogdán E, Kamer KJ, Udeshi ND, Carr SA, Chaudhuri D, Clapham DE, Li AA, et al (2013) EMRE is an essential component of the mitochondrial calcium uniporter complex. Science 342: 1379–1382
Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flügge UI, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131: 16–26
Senkler J, Senkler M, Eubel H, Hildebrandt T, Lengwenus C, Schertl P, Schwarzländer M, Wagner S, Wittig I, Braun HP (2016) The mitochondrial complexome of Arabidopsis thaliana. Plant J, doi/10.1111/tpj.13448
Silva MA, Carnieri EG, Vercesi AE (1992) Calcium transport by corn mitochondria: evaluation of the role of phosphate. Plant Physiol 98: 452–457
Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signalling: an emerging field. J Exp Bot 63: 1525–1542
Sweetlove LJ, Taylor NL, Leaver CJ (2007) Isolation of intact, functional mitochondria from the model plant Arabidopsis thaliana. Methods Mol Biol 372: 125–136
Szabò I, Zoratti M (2014) Mitochondrial channels: ion fluxes and more. Physiol Rev 94: 519–608
Talavera K, Nilius B (2006) Biophysics and structure-function relationship of T-type Ca2+ channels. Cell Calcium 40: 97–114
Teardo E, Carraretto L, De Bortoli S, Costa A, Behera S, Wagner R, Lo Schiavo F, Formentin E, Szabò I (2015) Alternative splicing-mediated targeting of the Arabidopsis GLUTAMATE RECEPTOR3.5 to mitochondria affects organelle morphology. Plant Physiol 167: 216–227
Teardo E, Formentin E, Segalla A, Giacometti GM, Marin O, Zanetti M, Lo Schiavo F, Zoratti M, Szabò I (2011) Dual localization of plant glutamate receptor AtGLR3.4 to plastids and plasmamembrane. Biochim Biophys Acta 1807: 359–367
Tsukagoshi H (2016) Control of root growth and development by reactive oxygen species. Curr Opin Plant Biol 29: 57–63
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606–616
Vais H, Mallilankaraman K, Mak DO, Hoff H, Payne R, Tanis JE, Foskett JK (2016) EMRE is a matrix Ca2+ sensor that governs gatekeeping of the mitochondrial Ca2+ uniporter. Cell Reports 14: 403–410
Vais H, Tanis JE, Müller M, Payne R, Mallilankaraman K, Foskett JK (2015) MCUR1, CCDC90A, is a regulator of the mitochondrial calcium uniporter. Cell Metab 22: 533–535
van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390: 287–289
Vecellio Reane D, Vallese F, Checchetto V, Acquasaliente L, Butera G, De Filippis V, Szabò I, Zanotti G, Rizzuto R, Raffaello A (2016) A MICU1 splice variant confers high sensitivity to the mitochondrial Ca2+ uptake machinery of skeletal muscle. Mol Cell 64: 760–773
Virolainen E, Blokhina O, Fagerstedt K (2002) Ca2+-induced high amplitude swelling and cytochrome c release from wheat (Triticum aestivum L.) mitochondria under anoxic stress. Ann Bot (Lond) 90: 509–516
Wagner S, Behera S, De Bortoli S, Logan DC, Fuchs P, Carraretto L, Teardo E, Cendron L, Nietzel T, Füßl M, et al (2015) The EF-hand Ca2+ binding protein MICU choreographs mitochondrial Ca2+ dynamics in Arabidopsis. Plant Cell 27: 3190–3212
Wagner S, De Bortoli S, Schwarzländer M, Szabò I (2016) Regulation of mitochondrial calcium in plants versus animals. J Exp Bot 67: 3809–3829
Weber AP, Linka N (2011) Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62: 53–77
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621–2632
Zottini M, Zannoni D (1993) The use of Fura-2 fluorescence to monitor the movement of free calcium ions into the matrix of plant mitochondria (Pisum sativum and Helianthus tuberosus). Plant Physiol 102: 573–578