Skip to main content
SpringerLink
Log in

The mitochondrial copper chaperone COX19 influences copper and iron homeostasis in arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

The mitochondrial metallochaperone COX19 influences iron and copper responses highlighting a role of mitochondria in modulating metal homeostasis in Arabidopsis.

Abstract

The mitochondrial copper chaperone COX19 participates in the biogenesis of cytochrome c oxidase (COX) in yeast and humans. In this work, we studied the function of COX19 in Arabidopsis thaliana, using plants with either decreased or increased COX19 levels. A fusion of COX19 to the red fluorescent protein localized to mitochondria in vivo, suggesting that Arabidopsis COX19 is a mitochondrial protein. Silencing of COX19 using an artificial miRNA did not cause changes in COX activity levels or respiration in plants grown under standard conditions. These amiCOX19 plants, however, showed decreased expression of the low-copper responsive miRNA gene MIR398b and an induction of the miR398 target CSD1 relative to wild-type plants. Plants with increased COX19 levels, instead, showed induction of MIR398b and other low-copper responsive genes. In addition, global transcriptional changes in rosettes of amiCOX19 plants resembled those observed under iron deficiency. Phenotypic analysis indicated that the roots of amiCOX19 plants show altered growth responses to copper excess and iron deficiency. COX activity levels and COX-dependent respiration were lower in amiCOX19 plants than in wild-type plants under iron deficiency conditions, suggesting that COX19 function is particularly important for COX assembly under iron deficiency. The results indicate that the mitochondrial copper chaperone COX19 has a role in regulating copper and iron homeostasis and responses in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

amiRNA:

Artificial miRNA

AOX:

Alternative oxidase

BCS:

Bathocuproine disulphonate

BN:

Blue native

CLSM:

Confocal laser scanning microscopy

COX:

Cytochrome c oxidase

GFP:

Green fluorescent protein

mRFP:

Modified red fluorescent protein

MS:

Murashige and Skoog

SHAM:

Salicyl-hydroxamic acid

SOD:

Superoxide dismutase

VDAC:

Voltage dependent anion channel

References

  • Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrés-Colás N, Sancenón V, Rodríguez-Navarro S, Mayo S, Thiele DJ, Ecker JR et al (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45:225–236

    Article  CAS  PubMed  Google Scholar 

  • Attallah CV, Welchen E, Gonzalez DH (2007a) The promoters of Arabidopsis thaliana genes AtCOX17-1 and—2, encoding a copper chaperone involved in cytochrome c oxidase biogenesis, are preferentially active in roots and anthers and induced by biotic and abiotic stress. Physiol Plant 1290:123–134

    Article  CAS  Google Scholar 

  • Attallah CV, Welchen E, Pujol C, Bonnard G, Gonzalez DH (2007b) Characterization of Arabidopsis thaliana genes encoding functional homologues of the yeast metal chaperone Cox19p, involved in cytochrome c oxidase biogenesis. Plant Mol Biol 65:343–355

    Article  CAS  PubMed  Google Scholar 

  • Attallah CV, Welchen E, Martin AP, Spinelli SV, Bonnard G, Palatnik JF, Gonzalez DH (2011) Plants contain two SCO proteins that are differentially involved in cytochrome c oxidase function and copper and redox homeostasis. J Exp Bot 62:4281–4294

    Article  CAS  PubMed  Google Scholar 

  • Aznar A, Chen NW, Rigault M, Riache N, Joseph D, Desmaële D et al (2014) Scavenging iron: a novel mechanism of plant immunity activation by microbial siderophores. Plant Physiol 164:2167–2183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beauclair L, Yu A, Bouché N (2010) microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62:454–462

    Article  CAS  PubMed  Google Scholar 

  • Bode M, Woellhaf MW, Bohnert M, van der Laan M, Sommer F, Jung M et al (2015) Redox-regulated dynamic interplay between Cox19 and the copper-binding protein Cox11 in the intermembrane space of mitochondria facilitates biogenesis of cytochrome c oxidase. Mol Biol Cell 26:2385–2401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brumbarova T, Bauer P, Ivanov R (2015) Molecular mechanisms governing Arabidopsis iron uptake. Trends Plant Sci 20:124–133

    Article  CAS  PubMed  Google Scholar 

  • Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    Article  CAS  PubMed  Google Scholar 

  • Castaings L, Caquot A, Loubet S, Curie C (2016) The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Sci Rep 6:37222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charrier B, Champion A, Henry Y, Kreis M (2002) Expression profiling of the whole Arabidopsis shaggy-like kinase multigene family by real-time reverse transcriptase-polymerase chain reaction. Plant Physiol 130:577–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Barak P (1982) Iron nutrition of plants in calcareous soils. Adv Agron 35:217–240

    Article  CAS  Google Scholar 

  • Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochim Biophys Acta 1757:730–741

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Cobine PA, Pierrel F, Winge DR (2006) Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim Biophys Acta 1763:759–772

    Article  CAS  PubMed  Google Scholar 

  • Colombatti F, Gonzalez DH, Welchen E (2014) Plant mitochondria under pathogen attack: a sigh of relief or a last breath? Mitochondrion 19:238–244

    Article  CAS  PubMed  Google Scholar 

  • Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drazkiewicz M, Skórzyńska-Polit E, Krupa Z (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. Biometals 17:379–387

    Article  CAS  PubMed  Google Scholar 

  • Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417

    Article  CAS  PubMed  Google Scholar 

  • Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629

    Article  CAS  PubMed  Google Scholar 

  • Fourcroy P, Tissot N, Gaymard F, Briat JF, Dubos C (2016) Facilitated Fe nutrition by phenolic compounds excreted by the Arabidopsis ABCG37/PDR9 transporter requires the IRT1/FRO2 high-affinity root Fe(2+) transport system. Mol Plant 9:485–488

    Article  CAS  PubMed  Google Scholar 

  • Garcia L, Welchen E, Gonzalez DH (2014) Mitochondria and copper homeostasis in plants Mitochondrion 19: 269–274

  • Garcia L, Welchen E, Gey U, Arce AL, Steinebrunner I, Gonzalez DH (2016) The cytochrome c oxidase biogenesis factor AtCOX17 modulates stress responses in Arabidopsis. Plant Cell Environ 39:628–644

    Article  CAS  PubMed  Google Scholar 

  • García MJ, Lucena C, Romera FJ, Alcántara E, Pérez-Vicente R (2010) Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J Exp Bot 61:3885–3899

    Article  CAS  PubMed  Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80

    Article  PubMed  PubMed Central  Google Scholar 

  • Gruber BD, Giehl RF, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong J, Connolly EL (2009) Iron uptake mechanisms in plants: functions of the FRO family of ferric reductases. Plant Sci 176:709–714

    Article  CAS  Google Scholar 

  • Katari MS, Nowicki SD, Aceituno FF, Nero D, Kelfer J, Thompson LP et al (2010) VirtualPlant: a software platform to support systems biology research. Plant Physiol 152:500–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khalimonchuk O, Winge DR (2008) Function and redox state of mitochondrial localized cysteine-rich proteins important in the assembly of cytochrome c oxidase. Biochim Biophys Acta 1783:618–628

    Article  CAS  PubMed  Google Scholar 

  • Kumar RK, Chu HH, Abundis C, Vasques K, Rodriguez DC, Chia JC et al (2017) Iron-nicotianamine transporters are required for proper long distance iron signaling. Plant Physiol 175:1254–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leary SC, Cobine PA, Kaufman BA, Guercin GH, Mattman A, Palaty J et al (2007) The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis. Cell Metab 5:9–20

    Article  CAS  PubMed  Google Scholar 

  • Leary SC, Winge DR, Cobine PA (2009) “Pulling the plug” on cellular copper: the role of mitochondria in copper export. Biochim Biophys Acta 1793:146–153

    Article  CAS  PubMed  Google Scholar 

  • Leary SC, Cobine PA, Nishimura T, Verdijk RM, de Krijger R, de Coo R et al (2013) COX19 mediates the transduction of a mitochondrial redox signal from SCO1 that regulates ATP7A-mediated cellular copper efflux. Mol Biol Cell 24:683–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682

    Article  CAS  PubMed  Google Scholar 

  • Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E et al (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23:1815–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2011) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22:2219–2236

    Article  CAS  Google Scholar 

  • Longen S, Bien M, Bihlmaier K, Kloeppel C, Kauff F, Hammermeister M et al (2009) Systematic analysis of the twin Cx9C protein family. J Mol Biol 393:356–368

    Article  CAS  PubMed  Google Scholar 

  • Mai HJ, Pateyron S, Bauer P (2016) Iron homeostasis in Arabidopsis thaliana: transcriptomic analyses reveal novel FIT-regulated genes, iron deficiency marker genes and functional gene networks. BMC Plant Biol 16:211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mansilla N, Garcia L, Gonzalez DH, Welchen E (2015) AtCOX10, a protein involved in haem o synthesis during cytochrome c oxidase biogenesis, is essential for plant embryogenesis and modulates the progression of senescence. J Exp Bot 66:6761–6775

    Article  CAS  PubMed  Google Scholar 

  • Mansilla N, Racca S, Gras DE, Gonzalez DH, Welchen E (2018) The complexity of mitochondrial Complex IV: an update of cytochrome c oxidase biogenesis in plants. Int J Mol Sci 19:662

    Article  CAS  PubMed Central  Google Scholar 

  • Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim Biophys Acta 1763:578–594

    Article  CAS  PubMed  Google Scholar 

  • Meyer EH, Millar AH (2008) Isolation of mitochondria from plant cell culture. Methods Mol Biol 425:163–169

    Article  PubMed  Google Scholar 

  • Moore AL, Shiba T, Young L, Harada S, Kita K, Ito K (2013) Unraveling the heater: new insights into the structure of the alternative oxidase. Annu Rev Plant Biol 64:637–663

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee I, Campbell NH, Ash JS, Connolly EL (2006) Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta 223:1178–1190

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K et al (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71:2095–2100

    Article  CAS  PubMed  Google Scholar 

  • Naranjo-Arcos MA, Maurer F, Meiser J, Pateyron S, Fink-Straube C, Bauer P (2017) Dissection of iron signaling and iron accumulation by overexpression of subgroup Ib bHLH039 protein. Sci Rep 7:10911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    Article  CAS  PubMed  Google Scholar 

  • Ng S, Ivanova A, Duncan O, Law SR, Van Aken O, De Clercq I et al (2013) A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25:3450–3471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nobrega MP, Bandeira SC, Beers J, Tzagoloff A (2002) Characterization of COX19, a widely distributed gene required for expression of mitochondrial cytochrome oxidase. J Biol Chem 277:40206–40211

    Article  CAS  PubMed  Google Scholar 

  • O’Connell J (2002) The basics of RT-PCR some practical considerations. Methods Mol Biol 193:19–25

    PubMed  Google Scholar 

  • Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690

    Article  CAS  PubMed  Google Scholar 

  • Pilon M (2017) The copper microRNAs. New Phytol 213:1030–1035

    Article  CAS  PubMed  Google Scholar 

  • Puig S, Andrés-Colás N, García-Molina A, Peñarrubia L (2007) Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant Cell Environ 30:271–290

    Article  CAS  PubMed  Google Scholar 

  • Radin I, Mansilla N, Rödel G, Steinebrunner I (2015) The Arabidopsis COX11 homolog is essential for cytochrome c oxidase activity. Front Plant Sci 6:1091

    Article  PubMed  PubMed Central  Google Scholar 

  • Rigby K, Zhang L, Cobine PA, George GN, Winge DR (2007) Characterization of the cytochrome c oxidase assembly factor Cox19 of Saccharomyces cerevisiae. J Biol Chem 282:10233–10242

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Celma J, Pan IC, Li W, Lan P, Buckhout TJ, Schmidt W (2013) The transcriptional response of Arabidopsis leaves to Fe deficiency. Front Plant Sci 4:276

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Celma J, Lattanzio G, Villarroya D, Gutierrez-Carbonell E, Ceballos-Laita L, Rencoret J et al (2016) Effects of Fe deficiency on the protein profiles and lignin composition of stem tissues from Medicago truncatula in absence or presence of calcium carbonate. J Proteomics 140:1–12

    Article  CAS  PubMed  Google Scholar 

  • Sancenón V, Puig S, Mira H, Thiele DJ, Peñarrubia L (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51:577–587

    Article  PubMed  Google Scholar 

  • Sancenón V, Puig S, Mateu-Andrés I, Dorcey E, Thiele DJ, Peñarrubia L (2004) The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279:15348–15355

    Article  CAS  PubMed  Google Scholar 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084

    Article  CAS  PubMed  Google Scholar 

  • Schuler M, Keller A, Backes C, Philippar K, Lenhof HP, Bauer P (2011) Transcriptome analysis by GeneTrail revealed regulation of functional categories in response to alterations of iron homeostasis in Arabidopsis thaliana. BMC Plant Biol 11:87

    Article  PubMed  PubMed Central  Google Scholar 

  • Selinski J, Hartmann A, Deckers-Hebestreit G, Day DA, Whelan J, Scheibe R (2018) Alternative oxidase isoforms are differentially activated by tricarboxylic acid cycle intermediates. Plant Physiol 176:1423–1432

    Article  CAS  PubMed  Google Scholar 

  • Silver JD, Ritchie ME, Smyth GK (2009) Microarray background correction: maximum likelihood estimation for the normal-exponential convolution. Biostatistics 10:352–363

    Article  PubMed  Google Scholar 

  • Song Y, Zhou L, Yang S, Wang C, Zhang T, Wang J (2017) Dose-dependent sensitivity of Arabidopsis thaliana seedling root to copper is regulated by auxin homeostasis. Environ Exp Bot 139:23–30

    Article  CAS  Google Scholar 

  • Steinebrunner I, Gey U, Andres M, Garcia L, Gonzalez DH (2014) Divergent functions of the Arabidopsis mitochondrial SCO proteins: HCC1 is essential for COX activity while HCC2 is involved in the UV-B stress response. Front Plant Sci 5:87

    Article  PubMed  PubMed Central  Google Scholar 

  • Strodtkötter I, Padmasree K, Dinakar C, Speth B, Niazi PS, Wojtera J et al (2009) Induction of the AOX1D isoform of alternative oxidase in A. thaliana T-DNA insertion lines lacking isoform AOX1A is insufficient to optimize photosynthesis when treated with antimycin A. Mol Plant 2:284–297

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by down-regulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    Article  CAS  PubMed  Google Scholar 

  • Tan YF, O’Toole N, Taylor NL, Millar AH (2010) Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol 152:747–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Team R (2013) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. http://www.r-projectorg/

  • Timón-Gómez A, Nývltová E, Abriata LA, Vila AJ, Hosler J, Barrientos A (2018) Mitochondrial cytochrome c oxidase biogenesis: recent developments. Semin Cell Dev Biol 76:163–178

    Article  CAS  PubMed  Google Scholar 

  • Tomassi AH, Gagliardi D, Cambiagno DA, Manavella PA (2017) Nonradioactive detection of small RNAs using digoxigenin-labeled probes. Methods Mol Biol 1640:199–210

    Article  CAS  PubMed  Google Scholar 

  • Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanlerberghe GC, Robson CA, Yip JY (2002) Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol 129:1829–1842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vigani G, Briat JF (2016) Impairment of respiratory chain under nutrient deficiency in plants: does it play a role in the regulation of iron and sulfur responsive genes? Front Plant Sci 6:1185

    Article  PubMed  PubMed Central  Google Scholar 

  • Vigani G, Maffi D, Zocchi G (2009) Iron availability affects the function of mitochondria in cucumber roots. New Phytol 182:127–136

    Article  CAS  PubMed  Google Scholar 

  • Vigani G, Bohic S, Faoro F, Vekemans B, Vincze L, Terzano R (2018) Cellular fractionation and nanoscopic X-ray fluorescence imaging analyses reveal changes of zinc distribution in leaf cells of iron-deficient plants. Front Plant Sci 9:1112

    Article  PubMed  PubMed Central  Google Scholar 

  • Waters BM, McInturf SA, Stein RJ (2012) Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. J Exp Bot 63:5903–5918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wittig I, Braun HP, Schägger H (2006) Blue native PAGE. Nat Protoc 1:418–428

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai Y (2009) SQUAMOSA Promoter Binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143:1–9

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants from Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, Argentina); Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina); and Universidad Nacional del Litoral (UNL, Argentina). EW, MAP and DHG are members of CONICET. LG and NM are fellows of the same Institution. NO was an undergraduate fellow of UNL. We thank Javier Palatnik for sending us the MIR398b reporter line and the pNB47 vector, Agustín Arce for help with microarray analysis, Iris Steinebrunner for help with CLSM, María Rosa Marano for the use of laboratory space, reagents and equipment during the work of LG in Rosario, and Pablo Manavella for the labeled miRNA probes.

Author information

Author notes

  1. Lucila Garcia and Natanael Mansilla contributed equally to this work.

Authors and Affiliations

  1. Instituto de Agrobiotecnología del Litoral (CONICET-UNL), Cátedra de Biología Celular y Molecular, Facultad de Bioquímica y Ciencias Biológicas, Centro Científico Tecnológico CONICET Santa Fe, Universidad Nacional del Litoral, Colectora Ruta Nac. Nº 168 km 0, Paraje el Pozo s/n, 3000, Santa Fe, Argentina

    Lucila Garcia, Natanael Mansilla, Natacha Ocampos, Elina Welchen & Daniel H. Gonzalez

  2. Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Ocampo y Esmeralda s/n, 2000, Rosario, Argentina

    Lucila Garcia

  3. Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI-CONICET), Universidad Nacional de Rosario, Suipacha 570, 2000, Rosario, Argentina

    María A. Pagani

Authors
  1. Lucila Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Natanael Mansilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natacha Ocampos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María A. Pagani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elina Welchen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Daniel H. Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DHG, EW and LG conceived and designed the experiments; LG, NM and NO performed the experiments and analyzed the data; MAP performed the ICP-MS determination of metal content; DHG wrote the paper; EW and LG contributed with the writing of the paper; all authors read and approved the final manuscript.

Corresponding author

Correspondence to Daniel H. Gonzalez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garcia, L., Mansilla, N., Ocampos, N. et al. The mitochondrial copper chaperone COX19 influences copper and iron homeostasis in arabidopsis. Plant Mol Biol 99, 621–638 (2019). https://doi.org/10.1007/s11103-019-00840-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00840-y

Keywords

Search

Navigation