Cell Biology of Copper

  • Christopher M. Cohu
  • Marinus PilonEmail author
Part of the Plant Cell Monographs book series (CELLMONO, volume 17)


The transition metal, copper (Cu), is an essential micronutrient for normal plant growth and development. Copper is a cofactor of proteins involved in photosynthesis, respiration, ethylene perception, removal of superoxide radicals, and cell wall modification. The biochemical reactions catalyzed by most Cu enzymes in plants are known. However, in many cases we are not yet sure about the biological function of these Cu proteins. Copper delivery to Cu proteins has evolved with a set of evolutionarily conserved transporters and metallo-chaperones. Analysis of Cu transporter and metallo-chaperone loss of function mutants has increased our understanding of the localization and biological function of many Cu delivery mechanisms and target Cu proteins. Studies examining the regulation of Cu transporters, metallo-chaperones, and Cu proteins have revealed an elegant system to regulate Cu homeostasis. Copper in excess is toxic while Cu deficiency can lead to decreased photosynthetic activity and reproductive success. To avoid Cu deficiency or toxicity symptoms in a sub-optimal environment, plants are capable of directing Cu delivery based on their needs via regulation of Cu proteins and delivery systems. For many Cu proteins, a network of Cu microRNAs, under the control of a SPL7 transcription factor, orchestrates the prioritization of Cu delivery based on Cu availability.


Amine Oxidase Ethylene Receptor Ascorbate Oxidase Thylakoid Lumen Endomembrane System 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Work in the author’s laboratory was supported by grants from the U.S. National Science Foundation to MP (NSF-IBN-0418993; NSF-IOS-0847442). We apologize to colleagues whose work could not be cited due to space limitations.


  1. Abdel-Ghany SE (2009) Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes. Planta 229:767–779PubMedCrossRefGoogle Scholar
  2. 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 283:15932–15945PubMedCrossRefGoogle Scholar
  3. Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251PubMedCrossRefGoogle Scholar
  4. An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825PubMedCrossRefGoogle Scholar
  5. Andrés-Colas N, Sancenon V, Rodriguez-Navarro S, Mayo S, Thiele DJ, Ecker JR, Puig S, Penarrubia L (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45:225–236PubMedCrossRefGoogle Scholar
  6. Angelini R, Tisi A, Rea G, Chen MM, Botta M, Federico R, Cona A (2008) Involvement of polyamine oxidase in wound healing. Plant Physiol 146:162–177PubMedCrossRefGoogle Scholar
  7. Arguello JM (2003) Identification of ion-selectivity determinants in heavy-metal transport P 1B-type ATPases. J Membrane Biol 195:93–108CrossRefGoogle Scholar
  8. Arguello JM, Eren E, Gonzalez-Guerrero M (2007) The structure and function of heavy metal transport P(1B)-ATPases. Biometals 20:233–248PubMedCrossRefGoogle Scholar
  9. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedCrossRefGoogle Scholar
  10. Attallah CV, Welchen E, Pujol C, Bonnard G, Gonzalez DH (2007) Characterization of Arabidopsis thaliana genes encoding functional homologues of the yeast metal chaperone Cox19p, involved in cytochrome c oxidase biogenesis. Plant Mol Biol 65:343–355PubMedCrossRefGoogle Scholar
  11. Axelsen KB, Palmgren MG (2001) Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126:696–706PubMedCrossRefGoogle Scholar
  12. Balandin T, Castresana C (2002) AtCOX17, an Arabidopsis homolog of the yeast copper chaperone COX17. Plant Physiol 129:1852–1857PubMedCrossRefGoogle Scholar
  13. Bao W, O’Malley DM, Whetten R, Sederoff RR (1993) A laccase associated with lignification in Loblolly Pine xylem. Science 260:672–674PubMedCrossRefGoogle Scholar
  14. Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628PubMedCrossRefGoogle Scholar
  15. Bernal M, Ramiro MV, Cases R, Picorel R, Yruela I (2006) Excess copper effect on growth, chloroplast ultrastructure, oxygen-evolution activity and chlorophyll fluorescence in Glycine max cell suspensions. Physiol Planta 127:312–325CrossRefGoogle Scholar
  16. Bernal M, Testillano PS, Alfonso M, del Carmen Risueño M, Picorel R, Yruela I (2007) Identification and subcellular localization of the soybean copper P1B-ATPase GmHMA8 transporter. J Struc Biol 158:46–58CrossRefGoogle Scholar
  17. Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Ann Rev Plant Physiol Plant Mol Biol 43:83–116CrossRefGoogle Scholar
  18. Briat JF, Curie C, Gaymard F (2007) Iron utilization and metabolism in plants. Curr Opin Plant Biol 10:276–282PubMedCrossRefGoogle Scholar
  19. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749PubMedCrossRefGoogle Scholar
  20. Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V, Torabinejad J, Wu Y (2006) Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot 57:2563–2569PubMedCrossRefGoogle Scholar
  21. Cardon G, Hohmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237:91–104PubMedCrossRefGoogle Scholar
  22. Carr HS, Winge DR (2003) Assembly of cytochrome c oxidase within the mitochondrion. Acc Chem Res 36:309–316PubMedCrossRefGoogle Scholar
  23. Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem 277:19861–19866PubMedCrossRefGoogle Scholar
  24. Chen Y, Shi J, Tian G, Zheng S, Lina Q (2004) Fe deficiency induces Cu uptake and accumulation in Commelina communis. Plant Sci 166:1371–1377CrossRefGoogle Scholar
  25. Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li HM, Jinn TL (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139:425–436PubMedCrossRefGoogle Scholar
  26. 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 1757:730–741PubMedCrossRefGoogle Scholar
  27. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annl Rev Plant Biol 53:159–182CrossRefGoogle Scholar
  28. Cobine PA, Ojeda LD, Rigby KM, Winge DR (2004) Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J Biol Chem 279:14447–14455PubMedCrossRefGoogle Scholar
  29. Cohu CM, Pilon M (2007) Regulation of superoxide dismutase expression by copper availability. Physiol Planta 129:747–755CrossRefGoogle Scholar
  30. Colman PM, Freeman HC, Guss JM, Murata M, Norris VA, Ramshaw JAM, Venkatappa MP (1978) X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution. Nature 272:319–324CrossRefGoogle Scholar
  31. Culotta VC, Klomp LWJ, Strain J, Casareno RLB, Krems B, Gitlin JD (1997) The copper chaperone for superoxide dismutase. J Biol Chem 272:23469–23472PubMedCrossRefGoogle Scholar
  32. Dancis A, Yuan DS, Haile D, Askwith C, Eide D, Moehle C, Kaplan J, Klausner RD (1994) Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport. Cell 76:393–402PubMedCrossRefGoogle Scholar
  33. Dean JFD, Eriksson K-EL (1994) Laccase and the deposition of lignin in vascular plants. Holzforschung 48:21–33CrossRefGoogle Scholar
  34. DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis yellow stripe-like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414PubMedCrossRefGoogle Scholar
  35. Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138:778–789PubMedCrossRefGoogle Scholar
  36. Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417PubMedCrossRefGoogle Scholar
  37. Eisses JF, Kaplan JH (2005) The mechanism of copper uptake mediated by human CTR1, a mutational analysis. J Biol Chem 280:37159–37168PubMedCrossRefGoogle Scholar
  38. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, Inc, Sunderland, MAGoogle Scholar
  39. Frebort I, Sebela M, Svendsen I, Hirota S, Endo M, Yamauchi O, Bellelli A, Lemr K, Pec P (2000) Molecular mode of interaction of plant amine oxidase with the mechanism-based inhibitor 2-butyne-1, 4-diamine. European J Biochem 267:1423–1433CrossRefGoogle Scholar
  40. Gavnholt B, Larsen K (2002) Molecular biology of plant laccases in relation to lignin formation. Physiol Planta 116:273–280CrossRefGoogle Scholar
  41. González-Guerrero M, Argüello JM (2008) Mechanism of Cu+-transporting ATPases: soluble Cu+ chaperones directly transfer Cu+ to transmembrane transport sites. Proc Natl Acad Sci USA 105:5992–5997PubMedCrossRefGoogle Scholar
  42. Guo WJ, Bundithya W, Goldsbrough PB (2003) Characterization of the Arabidopsis metallothionein gene family: tissue specific expression and induction during senescence and in response to copper. New Phytol 159:369–381CrossRefGoogle Scholar
  43. Guo WJ, Meetam M, Goldsbrough PB (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 146:1697–1706PubMedCrossRefGoogle Scholar
  44. Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14PubMedGoogle Scholar
  45. Himelblau E, Mira H, Lin SJ, Culotta VC, Penarrubia L, Amasino RM (1998) Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis. Plant Physiol 117:1227–1234PubMedCrossRefGoogle Scholar
  46. Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR (1999) RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393PubMedCrossRefGoogle Scholar
  47. Hoopes JT, Dean JFD (2004) Ferroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipifera. Plant Physiol Biochem 42:27–33PubMedCrossRefGoogle Scholar
  48. Horng Y-C, Cobine PA, Maxfield AB, Carr HS, Winge DR (2004) Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome c oxidase. J Biol Chem 279:35334–35340PubMedCrossRefGoogle Scholar
  49. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799PubMedCrossRefGoogle Scholar
  50. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Ann Rev Plant Biol 57:19–53CrossRefGoogle Scholar
  51. Kampfenkel K, Kushnir S, Babiychuk E, Inze D, Van Montagu M (1995) Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue. J Biol Chem 270:28479–28486PubMedCrossRefGoogle Scholar
  52. Katoh S (1960) A new copper protein from Chlorella ellipsoidea. Nature 186:533–534PubMedCrossRefGoogle Scholar
  53. Kieselbach T, Hagman Å, Andersson B, Schröder WP (1998) The thylakoid lumen of the chloroplasts: isolation and characterization. J Biol Chem 273:6710–6716PubMedCrossRefGoogle Scholar
  54. Kieselbach T, Bystedt M, Hynds P, Robinson C, Schröder WP (2000) A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen. FEBS Lett 480:271–276PubMedCrossRefGoogle Scholar
  55. Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM (2003) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100:16125–16130PubMedCrossRefGoogle Scholar
  56. Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an ecletic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650PubMedCrossRefGoogle Scholar
  57. Kobayashi Y, Kuroda K, Kimura K, Southron-Francis JL, Furuzawa A, Kimura K, Iuchi S, Kobayashi M, Taylor GJ, Koyama H (2008) Amino acid polymorphisms in strictly conserved domains of a P-type ATPase HMA5 are involved in the mechanism of copper tolerance variation in Arabidopsis. Plant Physiol 148:969–980PubMedCrossRefGoogle Scholar
  58. Kropat J, Tottey S, Birkenbihl RP, Depege N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci USA 102:18730–18735PubMedCrossRefGoogle Scholar
  59. Kumar V, Dooley DM, Freeman HC, Guss JM, Harvey I, McGuirl MA, Wilce MC, Zubak VM (1996) Crystal structure of a eukaryotic (pea seedling) copper-containing amine oxidase at 2.2 A resolution. Structure 4:943–955PubMedCrossRefGoogle Scholar
  60. Kuper J, Llamas A, Hecht HJ, Mendel RR, Schwarz G (2004) Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430:803–806PubMedCrossRefGoogle Scholar
  61. Lee H, Lee JS, Bae EK, Choi YI, Noh EW (2005) Differential expression of a poplar copper chaperone gene in response to various abiotic stresses. Tree Physiol 25:395–401PubMedGoogle Scholar
  62. Li HH, Merchant S (1995) Degradation of plastocyanin in copper-deficient Chlamydomonas reinhardtii. Evidence for a protease-susceptible conformation of the apoprotein and regulated proteolysis. J Biol Chem 270:23504–23510PubMedCrossRefGoogle Scholar
  63. Liang M, Haroldsen V, Cai X, Wu Y (2006) Expression of a putative laccase gene, ZmLAC1, in maize primary roots under stress. Plant Cell Environ 29:746–753PubMedCrossRefGoogle Scholar
  64. Liao MT, Hedley MJ, Woolley DJ, Brooks RR, Nichols MA (2000) Copper uptake and translocation in chicory (Cichorium intybus L. cv Grasslands Puna) and tomato (Lycopersicon esculentum Mill. cv Rondy) plants grown in NFT system. II. The role of nicotianamine and histidine in xylem sap copper transport. Plant Soil 223:1573–5036CrossRefGoogle Scholar
  65. Linder MC, Goode CA (1991) Biochemistry of copper. Plenum Press, New YorkGoogle Scholar
  66. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY (2007) Function and regulation of human copper-transporting ATPases. Physiol Reviews 87:1011–1046CrossRefGoogle Scholar
  67. Mandal AK, Yang Y, Kertesz TM, Argüello JM (2004) Identification of the transmembrane metal binding site in Cu+-transporting PIB-type ATPases. J Biol Chem 279:54802–54807PubMedCrossRefGoogle Scholar
  68. Marina M, Maiale SJ, Rossi FR, Romero MF, Rivas EI, Gárriz A, Ruiz OA, Pieckenstain FL (2008) Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava. Plant Physiol 147:2164–2178PubMedCrossRefGoogle Scholar
  69. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  70. Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochem 67:2318–2331CrossRefGoogle Scholar
  71. McCaig BC, Meagher RB, Dean JFD (2005) Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221:619–636PubMedCrossRefGoogle Scholar
  72. Mira H, Vilar M, Perez-Paya E, Penarrubia L (2001a) Functional and conformational properties of the exclusive C-domain from the Arabidopsis copper chaperone (CCH). Biochem J 357:545–549PubMedCrossRefGoogle Scholar
  73. Mira H, Martinez-Garcia F, Penarrubia L (2001b) Evidence for the plant-specific intercellular transport of the Arabidopsis copper chaperone CCH. Plant J 25:521–528PubMedCrossRefGoogle Scholar
  74. Mira H, Martínez N, Peñarrubia L (2002) Expression of a vegetative-storage-protein gene from Arabidopsis is regulated by copper, senescence and ozone. Planta 214:939–946PubMedCrossRefGoogle Scholar
  75. Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervás M, Howe CJ, De la Rosa MA (2003) A new function for an old cytochrome? Nature 424:33–34PubMedCrossRefGoogle Scholar
  76. 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 223:1178–1190PubMedCrossRefGoogle Scholar
  77. Nakamura K, Go N (2005) Function and molecular evolution of multicopper blue proteins. Cell Mol Life Sci 62:2050–2066PubMedCrossRefGoogle Scholar
  78. Nersissian AM, Valentine JS, Immoos C, Hill MG, Hart PJ, Williams G, Herrmann RG (1998) Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci 7:1915–1929PubMedCrossRefGoogle Scholar
  79. Newman SM, Eannetta NT, Yu H, Prince JP, de Vicente MC, Tanksley SD, Steffens JC (1993) Organisation of the tomato polyphenol oxidase gene family. Plant Mol Biol 21:1035–1051PubMedCrossRefGoogle Scholar
  80. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738PubMedCrossRefGoogle Scholar
  81. Paschalidis KA, Roubelakis-Angelakis KA (2005) Sites and regulation of polyamine catabolism in the tobacco plant. Correlations with cell division/expansion, cell cycle progression, and vascular development. Plant Physiol 138:2174–2184PubMedCrossRefGoogle Scholar
  82. Pesaresi P, Scharfenberg M, Weigel M, Granlund I, Schroder WP, Finazzi G, Rappaport F, Masiero S, Furini A, Jahns P, Leister D (2008) Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: revised roles of plastocyanin in photosynthetic electron flow and thylakoid redox state. Mol Plant 1:1–13 in press, out onlineCrossRefGoogle Scholar
  83. Pich A, Scholz I (1996) Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. J Exp Bot 47:41–47CrossRefGoogle Scholar
  84. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641PubMedCrossRefGoogle Scholar
  85. Pourcel L, Routaboul JM, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17:2966–2980PubMedCrossRefGoogle Scholar
  86. Puig S, Lee J, Lau M, Thiele DJ (2002) Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J Biol Chem 277:26021–26030PubMedCrossRefGoogle Scholar
  87. Puig S, Mira H, Dorcey E, Sancenon V, Andres-Colas N, Garcia-Molina A, Burkhead JL, Gogolin KA, Abdel-Ghany SE, Thiele DJ, Ecker JR, Pilon M (2007) Higher plants possess two different types of ATX1-like copper chaperones. Biochem Biophys Res Commun 354:385–390PubMedCrossRefGoogle Scholar
  88. Ranocha P, Chabannes M, Chamayou S, Danoun S, Jauneau A, Boudet AM, Goffner D (2002) Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol 129:145–155PubMedCrossRefGoogle Scholar
  89. Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving. Photosynth Res 60:111–150CrossRefGoogle Scholar
  90. Rea G, Metoui O, Infantino A, Federico R, Angelini R (2002) Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion. Plant Physiol 128:865–875PubMedCrossRefGoogle Scholar
  91. Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697PubMedCrossRefGoogle Scholar
  92. Rodriguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283:996–998PubMedCrossRefGoogle Scholar
  93. Sancenon V, Puig S, Mira H, Thiele DJ, Penarrubia L (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51:577–587PubMedCrossRefGoogle Scholar
  94. Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L (2004) The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279:15348–15355PubMedCrossRefGoogle Scholar
  95. Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wiren N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem 279:9091–9096PubMedCrossRefGoogle Scholar
  96. Schnell DJ (1998) Protein targeting to the thylakoid membrane. Ann Rev Plant Physiol Plant Mol Biol 49:97–126CrossRefGoogle Scholar
  97. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365PubMedCrossRefGoogle Scholar
  98. Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892PubMedCrossRefGoogle Scholar
  99. Shikanai T, Müller-Moulé P, Munekage Y, Niyogi KK, Pilon M (2003) PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15:1333–1346PubMedCrossRefGoogle Scholar
  100. Smeekens S, Bauerle C, Hageman J, Keegstra K, Weisbeek P (1986) The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell 46:365–375PubMedCrossRefGoogle Scholar
  101. Sterjiades R, Dean JFD, Eriksson K-EL (1992) Laccase from Sycamore maple (Acer pseudoplatanus) polymerizes monolignols. Plant Physiol 99:1162–1168PubMedCrossRefGoogle Scholar
  102. Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065PubMedCrossRefGoogle Scholar
  103. Tabata K, Kashiwagi S, Mori H, Ueguchi C, Mizuno T (1997) Cloning of a cDNA encoding a putative metal-transporting P-type ATPase from Arabidopsis thaliana. Biochim Biophys Acta 1326:1–6PubMedCrossRefGoogle Scholar
  104. Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15:1263–1280PubMedCrossRefGoogle Scholar
  105. Thipyapong P, Joel DM, Steffens JC (1997) Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiol 113:707–718PubMedGoogle Scholar
  106. Vorst O, Kock P, Lever A, Weterings B, Weisbeek P, Smeekens S (1993) The promoter of the Arabidopsis thaliana plastocyanin gene contains a far upstream enhancer-like element involved in chloroplast-dependent expression. Plant J 4:933–945PubMedCrossRefGoogle Scholar
  107. Waters BM, Grusak MA (2008) Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3. New Phytol 177:389–405PubMedGoogle Scholar
  108. Waters BM, Chu HH, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458PubMedCrossRefGoogle Scholar
  109. Weigel M, Varotto C, Pesaresi P, Finazzi G, Rappaport F, Salamini F, Leister D (2003) Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 278:31286–31289PubMedCrossRefGoogle Scholar
  110. Welch RM, Norvell WA, Schaefer SC, Shaff JE, Kochian LV (1993) Induction of iron(III) and copper(II) reduction in pea roots by Fe and Cu status: does the root-cell plasmalemma Fe(III)-chelate reductase perform a general role in regulation of cation uptake. Planta 190:555–561CrossRefGoogle Scholar
  111. Welchen E, Chan RL, Gonzalez DH (2004) The promoter of the Arabidopsis nuclear gene COX5b–1, encoding subunit 5b of the mitochondrial cytochrome c oxidase, directs tissue-specific expression by a combination of positive and negative regulatory elements. J Exp Bot 55:1997–2004PubMedCrossRefGoogle Scholar
  112. Williams LE, Mills RF (2005) P(1B)-ATPases: an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502PubMedCrossRefGoogle Scholar
  113. Wintz H, Fox T, Wu YY, Feng V, Chen W, Chang HS, Zhu T, Vulpe C (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653PubMedCrossRefGoogle Scholar
  114. Woeste KE, Kieber JJ (2000) A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12:443–455PubMedCrossRefGoogle Scholar
  115. Yamamoto A, Bhuiyan MN, Waditee R, Tanaka Y, Esaka M, Oba K, Jagendorf AT, Takabe T (2005) Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. J Exp Bot 56:1785–1796PubMedCrossRefGoogle Scholar
  116. 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 282:16369–16378PubMedCrossRefGoogle Scholar
  117. Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter-binding protein-like 7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361PubMedCrossRefGoogle Scholar
  118. Yruela I, Pueyo JJ, Alonso PJ, Picorel R (1996) Photoinhibition of photosystem II from higher plants. Effect of copper inhibition. J Biol Chem 271:27408–27415PubMedCrossRefGoogle Scholar
  119. Zhou J, Goldsbrough PB (1994) Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–884PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Biology DepartmentColorado State UniversityFort CollinsUSA

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