Copper homeostasis

New Phytologist

Volumn 182, Issue 4, 2009, Pages 799-816

  Burkhead, Jason L ^a   Gogolin Reynolds, Kathryn A ^a   Abdel Ghany, Salah E ^a   Cohu, Christopher M ^a   Pilon, Marinus ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Copper (Cu); Deficiency; Homeostasis; Metallochaperone; Photosynthesis; Regulation; Small RNA; Transport

Indexed keywords

COPPER;

BIOACCUMULATION; BIOAVAILABILITY; COPPER; ELECTRON; GENE EXPRESSION; GROWTH RATE; HOMEOSTASIS; NUTRIENT AVAILABILITY; PHOTOAUTOTROPHY; PHYTOTOXICITY; PROTEIN; RNA; ROOT SYSTEM;

CHEMISTRY; HOMEOSTASIS; METABOLISM; PHOTOSYNTHESIS; PLANT; PLANT ROOT; REVIEW; SOIL;

COPPER; HOMEOSTASIS; PHOTOSYNTHESIS; PLANT ROOTS; PLANTS; SOIL;

EID: 65549144746     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.02846.x     Document Type: Review

References (164)

1. Abdel-Ghany SE. 2009. Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes. Planta 229 : 767 779.
2. Abdel-Ghany SE, Pilon M. 2008. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. Journal of Biological Chemistry 283 : 15932 15945.
3. Abdel-Ghany SE, Burkhead JL, Gogolin KA, Andrés-Colás N, Bodecker JR, Puig S, Peñarrubia L, Pilon M. 2005b. AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7. FEBS Letters 579 : 2307 2312. (Pubitemid 40569496)
4. Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T. 2005a. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17 : 1233 1251. (Pubitemid 43142139)
5. Alaoui-Sossé I, Genet P, Vinit-Dunand F, Toussaint ML, Epron D, Badot PM. 2004. Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Science 166 : 1213 1218. (Pubitemid 38473382)
6. 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. Journal of Experimental Botany 59 : 815 825.
7. Andrés-Colás 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. The Plant Journal 45 : 225 236.
8. Angelini R, Tisi A, Rea G, Chen MM, Botta M, Federico R, Cona A. 2008. Involvement of polyamine oxidase in wound healing. Plant Physiology 146 : 162 77.
9. Arguello JM, Eren E, Gonzalez-Guerrero M. 2007. The structure and function of heavy metal transport P(1B)-ATPases. Biometals 20 : 233 248. (Pubitemid 46776570)
10. Arnesano F, Banci L, Benvenuti M, Bertini I, Calderone V, Mangani S, Viezzoli MS. 2003. The evolutionarily conserved trimeric structure of CutA1 proteins suggests a role in signal transduction. Journal of Biological Chemistry 278 : 45999 46006. (Pubitemid 37432748)
11. Arnesano F, Banci L, Bertini I, Ciofi-Baffoni S, Molteni E, Huffman DL O'Halloran TV. 2002. Metallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Research 12 : 255 271. (Pubitemid 34162992)
12. Arnon DI. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidse in Beta vulgaris. Plant Physiology 24 : 1 15.
13. Arnon DI, Stout PR. 1939. The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiology 14 : 371 375.
14. 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 Molecular Biology 65 : 343 355. (Pubitemid 47414564)
15. Badarau A, Firbank SJ, Waldron KJ, Yanagisawa S, Robinson NJ, Banfield MJ, Dennison C. 2008. FutA2 is a ferric binding protein from Synechocystis PCC 6803. Journal of Biological Chemistry 283 : 12520 12527.
16. Balandin T, Castresana C. 2002. AtCOX17, an Arabidopsis homolog of the yeast copper chaperone COX17. Plant Physiology 129 : 1852 1857.
17. 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. Physiologia Plantarum 127 : 312 325. (Pubitemid 43799966)
18. Bernal M, Roncel M, Ortega JM, Picorel R, Yruela I. 2004. Copper effect on cytochrome b of photosystem II under photoinhibitory conditions. Physiologia Plantarum 120 : 686 694. (Pubitemid 38414169)
19. 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. Journal of Structural Biology 158 : 46 58. (Pubitemid 46441895)
20. Bonnet E, Wuyts J, Rouze P, Van de Peer Y. 2004. Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proceedings of the National Academy of Sciences, USA 101 : 11511 11516. (Pubitemid 39038378)
21. Borrelly GPM, Rondet SAM, Tottey S, Robinson NJ. 2004. Chimeras of P1-type ATPases and their transcriptional regulators: contributions of a cytosolic amino-terminal domain to metal-specificity. Molecular Microbiology 53 : 217 227. (Pubitemid 38901392)
22. Bovy A, de Vrieze G, Borrias M, Weisbeek P. 1992. Transcriptional regulation of the plastocyanin and cytochrome c553 genes from the cyanobacterium Anabaena species PCC 7937. Molecular Microbiology 11 : 1506 1513.
23. Bowler C, Van Montagu M, Inze D. 1992. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43 : 83 116.
24. Boyd RS. 2007. The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant and Soil 293 : 153 176. (Pubitemid 46761293)
25. Briat JF, Curie C, Gaymard F. 2007. Iron utilization and metabolism in plants. Current Opinion in Plant Biolology 10 : 276 282. (Pubitemid 46722691)
26. Buhtz A, Springer F, Chappell L, Baulcombe, DC, Kehr J. 2008. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant Journal 53 : 739 749.
27. Burkhead J, Abdel-Ghany S, Morrill J, Pilon-Smits EAH, Pilon M. 2003. The Arabidopsis thaliana CUTA gene encodes an evolutionarily conserved copper binding chloroplast protein. Plant Journal 34 : 856 867. (Pubitemid 36796933)
28. 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. Journal of Experimental Botany 57 : 2563 2569. (Pubitemid 44290290)
29. Cardon G, Hohmann S, Klein J, Nettesheim K, Saedler H, Huijser P. 1999. Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237 : 91 104. (Pubitemid 29406201)
30. Carr HS, Winge DR. 2003. Assembly of cytochrome c oxidase within the mitochondrion. Accounts of Chemical Research 36 : 309 316.
31. Carroll MC, Girouard JB, Ulloa JL, Subramaniam JR, Wong PC, Valentine JS, Culotta VC. 2004. Mechanisms for activating Cu- and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proceedings of the National Academy of Sciences, USA 101 : 5964 5969. (Pubitemid 38520511)
32. Chapman DJ, Schopf JW. 1983. Biological and biochemical effects of the development of an aerobic environment. In : Schopf JW, ed. Earth's earliest biosphere: its origin and evolution. Princeton, NJ, USA : Princeton University Press, 302 320.
33. Chen YF, Randlett MD, Findell JL, Schaller GE. 2002. Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. Journal of Biological Chemistry 277 : 19861 19866.
34. Chen Y, Shi J, Tian G, Zheng S, Lina Q. 2004. Fe deficiency induces Cu uptake and accumulation in Commelina communis. Plant Science 166 : 1371 1377. (Pubitemid 38473400)
35. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL. 2006. Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18 : 412 421. (Pubitemid 43951302)
36. 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 Physiology 139 : 425 436. (Pubitemid 43951625)
37. Cobbett C, Goldsbrough P. 2002. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 53 : 159 182. (Pubitemid 36257491)
38. Cohu CM, Pilon M. 2007. Regulation of superoxide dismutase expression by copper availability. Physiologia Plantarum 129 : 747 755. (Pubitemid 46426505)
39. 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 : 319 324.
40. Culotta VC, Klomp LWJ, Strain J, Casareno RLB, Krems B, Gitlin JD. 1997. The copper chaperone for superoxide dismutase. Journal of Biological Chemistry 272 : 23469 23472. (Pubitemid 27410910)
41. 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 : 393 402. (Pubitemid 124000739)
42. 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 Journal 39 : 403 414. (Pubitemid 39040145)
43. Dong J, Kim ST, Lord EM. 2005. Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiology 138 : 778 789. (Pubitemid 43793158)
44. Dugas DV, Bartel B. 2008. Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Molecular Biology 67 : 403 417.
45. Eisses JF, Kaplan JH. 2005. The mechanism of copper uptake mediated by human CTR1, a mutational analysis. Journal of Biological Chemistry 280 : 37159 37168. (Pubitemid 41587800)
46. Epstein E, Bloom AJ. 2005. Mineral nutrition of plants: principles and perspectives, 2nd edn. Sunderland, MA, USA : Sinauer Associates, Inc.
47. Faucon MP, Shutcha N, Meerts P. 2007. Revisiting copper and cobalt concentrations in supposed hyperaccumulators from SC Africa: influence of washing and metal concentrations in soil. Plant Soil 301 : 29 36.
48. Fordham-Skelton A, Wilson J, Groom Q, Robinson N. 1997. Accumulation of metallothionein transcripts in response to iron, copper and zinc: metallothionein and metal-chelate reductase. Acta Physiologia Plantarum 19 : 451 457. (Pubitemid 28118119)
49. 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 Journal of Biochemistry 267 : 1423 1433. (Pubitemid 30143281)
50. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. 2005. A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biology 15 : 2038 2043. (Pubitemid 41654628)
51. Garrett TP, Clingeleffer DJ, Guss JM, Rogers SJ, Freeman HC. 1984. The crystal structure of poplar apoplastocyanin at 1.8-A resolution. The geometry of the copper-binding site is created by the polypeptide. Journal of Biological Chemistry 259 : 2822 2825.
52. Gavnholt B, Larsen K. 2002. Molecular biology of plant laccases in relation to lignin formation. Physiologia Plantarum 116 : 273 280. (Pubitemid 35241140)
53. + to transmembrane transport sites. Proceedings of the National Academy of Sciences, USA 105 : 5992 5997.
54. Gralla, EB, Thiele DJ, Silar P, Valentine JS. 1991. ACE1, a copper-dependent transcription factor, activates expression of the yeast copper, zinc superoxide dismutase gene. Proceedings of the National Academy of Sciences, USA 88 : 8558 8562. (Pubitemid 21915396)
55. 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 Phytologist 159 : 369 381. (Pubitemid 36900927)
56. Guo WJ, Meetam M, Goldsbrough PB. 2008. Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiology 146 : 1697 1706. (Pubitemid 352844070)
57. Halliwell B, Gutteridge JM. 1984. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochemical Journal 219 : 1 14. (Pubitemid 14171443)
58. Hanikenne M, Krämer U, Demoulin V, Baurain D. 2005. A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschyzon merolae. Plant Physiology 137 : 428 446. (Pubitemid 43136095)
59. Harrison M, Jones C, Dameron C. 1999. Copper chaperones: function, structure and copper-binding properties. Journal of Biological Inorganic Chemistry 4 : 145 153. (Pubitemid 29227787)
60. Harrison PM, Hoare RJ. 1980. Metals in biochemistry. New York, NY, USA : Chapman & Hall.
61. 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 Physiology 117 : 1227 1234. (Pubitemid 128652896)
62. 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 : 383 393. (Pubitemid 29214594)
63. Huffman DL, O'Halloran TV. 2000. Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2. Journal of Biological Chemistry 275 : 18611 18614. (Pubitemid 30422815)
64. Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML. 2008. Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proceedings of the National Academy of Sciences, USA 105 : 10619 10624.
65. Jones-Rhoades MW, Bartel DP. 2004. Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA. Molecular Cell 14 : 787 799. (Pubitemid 38780852)
66. Jones-Rhoades MW, Bartel DP, Bartel B. 2006. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57 : 19 53. (Pubitemid 44061017)
67. 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. Journal of Biological Chemistry 270 : 28479 28486.
68. Kanamaru K, Kashiwagi S, Mizuno T. 1994. A copper-transporting P-type ATPase found in the thylakoid membrane of the cyanobacterium Synechococcus species PCC7942. Molecular Microbiology 13 : 369 377. (Pubitemid 24225507)
69. Katoh S. 1960. A new copper protein from Chlorella ellipsoidea. Nature 186 : 533 534.
70. 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. Proceedings of the National Academy of Sciences, USA 100 : 16125 16130. (Pubitemid 38021125)
71. Kliebenstein DJ, Monde RA, Last RL 1998. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology 118 : 637 650. (Pubitemid 128652956)
72. 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. Proceedings of the National Academy of Sciences, USA 102 : 18730 18735. (Pubitemid 43011294)
73. 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 Å resolution. Structure 4 : 943 955. (Pubitemid 26324706)
74. 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 : 803 806. (Pubitemid 39071353)
75. Küpper H, Šetlík I, Šetliková E, Ferimazova N, Spiller M, Küpper FC. 2003. Copper-induced inhibition of photosynthesis: limiting steps of in vivo copper chlorophyll formation in Scenedesmus quadricauda. Functional Plant Biology 30 : 1187 1196. (Pubitemid 38184754)
76. Kurepa J, Hérouart D, Van Montagu M, Inzé D. 1997. Differential expression of CuZn- and Fe-superoxide dismutase genes of tobacco during development, oxidative stress, and hormonal treatments. Plant and Cell Physiology 38 : 463 470. (Pubitemid 127467262)
77. La Fontaine S, Quinn JM, Nakamoto SS, Page MD, Göhre V, Moseley JL, Kropat J, Merchant S. 2002. Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryotic Cell 1 : 736 757. (Pubitemid 36557733)
78. 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 Physiology 25 : 395 401. (Pubitemid 40466274)
79. 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. Journal of Biological Chemistry 270 : 23504 23510.
80. Li H-M, Theg SM, Bauerle CM, Keegstra K. 1990. Metal-ion-center assembly of ferredoxin and plastocyanin in isolated chloroplasts. Proceedings of the National Academy of Sciences, USA 87 : 6748 6752. (Pubitemid 20351558)
81. Linder MC, Goode CA. 1991. Biochemistry of copper. New York, NY, USA : Plenum Press.
82. Lippard SJ, Berg JM. 1994. Principles of bioinorganic chemistry. New York, NY, USA : University Science Books.
83. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY 2007. Function and regulation of human copper-transporting ATPases. Physiological Reviews 87 : 1011 1046. (Pubitemid 47084675)
84. Magnani, D, Solioz M. 2007. How bacteria handle copper. In : Nies, DH, Silver S, eds. Bacterial transition metal homeostasis. Heidelberg, Germany : Springer, 259 285.
85. +-transporting PIB-type ATPases. Journal of Biological Chemistry 279 : 54802 54807. (Pubitemid 40053225)
86. 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 Physiology 147 : 2164 2178.
87. Marschner H. 1995. Mineral nutrition of higher plants. London, UK : Academic Press.
88. Mayer AM. 2006. Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67 : 2318. (Pubitemid 44527933)
89. 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 : 619 636. (Pubitemid 41003879)
90. 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. Biochimica et Biophysica Acta 1763 : 587 594. (Pubitemid 44189540)
91. 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 : 939 946. (Pubitemid 36059260)
92. Mira H, Martinez-Garcia F, Penarrubia L. 2001b. Evidence for the plant-specific intercellular transport of the Arabidopsis copper chaperone CCH. Plant Journal, 25 : 521 528. (Pubitemid 32442251)
93. 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). Biochemical Journal 357 : 545 549. (Pubitemid 32701793)
94. Misra KC. 2000. Understanding mineral deposits. Dordrecht, the Netherlands : Kluwer Academic Publishers.
95. Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervás M, Howe CJ, De La Rosa MA. 2003. Photosynthesis: a new function for an old cytochrome? Nature 424 : 33 34.
96. 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.
97. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15 : 473 497.
98. Murphy A, Taiz L. 1995. A new vertical mesh transfer technique for metal-tolerance studies in Arabidopsis. Plant Physiology 108 : 29 38.
99. Nagae M, Nakata M, Takahashi Y. 2008. Identification of negative cis-acting elements in response to copper in the chloroplastic iron superoxide dismutase gene of the moss Barbula unguiculata. Plant Physiology 146 : 1687 1696. (Pubitemid 352844069)
100. Nakamura K, Go N. 2005. Function and molecular evolution of multicopper blue proteins. Cellular and Molecular Life Science 62 : 2050 2066. (Pubitemid 41291662)
101. Navari-Izzo F, Cestone B, Cavallini A, Natali L, Giordani T, Quartacci MF. 2006. Copper excess triggers phospholipase D activity in wheat roots. Phytochemistry 67 : 1232 1242. (Pubitemid 43913902)
102. Pant BD, Buhtz A, Kehr J, Scheible WR. 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant Journal 53 : 731 8.
103. 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 Physiology 138 : 2174 2184. (Pubitemid 43733560)
104. Pena MM, Koch KA, Thiele DJ. 1998. Dynamic regulation of copper uptake and detoxification genes in Saccharomyces cerevisiae. Molecular and Cellular Biology 18 : 2514 2523. (Pubitemid 28183421)
105. Pena MM, Puig S, Thiele DJ. 2000. Characterization of the Saccharomyces cerevisiae high affinity copper transporter Ctr3. Journal of Biological Chemistry 275 : 33244 33251.
106. Pesaresi P, Scharfenberg M, Weigel M, Granlund I, Schroder WP, Finazzi G, Rappaport F, Masiero S, Furini A, Jahns P et al. 2009. Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: revised roles of plastocyanin in photosynthetic electron flow and thylakoid redox state. Molecular Plant 2 : 236 248.
107. Phung LT, Ajlani G, Haselkorn R. 1994. P-type ATPase from the cyanobacterium Synechococcus 7942 related to the human Menkes and Wilson disease gene products. Proceedings of the National Academy of Sciences, USA 91 : 9651 9654. (Pubitemid 24297973)
108. Pich A, Scholz I. 1996. Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. Journal of Experimental Botany 47 : 41 47. (Pubitemid 2615912)
109. Pierrel F, Cobine PA, Winge DR. 2007. Metal ion availability in mitochondria. Biometals. 20 : 675 682. (Pubitemid 46776567)
110. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH. 2003. The function of ascorbate oxidase in tobacco. Plant Physiology 132 : 1631 1641. (Pubitemid 36872910)
111. 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 2980.
112. Puig S, Mira H, Dorcey E, Sancenon V, Andres-Colas N, Garcia-Molina A, Burkhead JL, Gogolin KA, Abdel-Ghany SE, Thiele DJ et al. 2007. Higher plants possess two different types of ATX1-like copper chaperones. Biochemical and Biophysical Research Communications 354 : 385 390. (Pubitemid 46161338)
113. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O' Halloran TV. 1999. Undetectable intercellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284 : 805 808. (Pubitemid 29291346)
114. 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 Physiology 128 : 865 875. (Pubitemid 34243824)
115. Reeves RO, Baker AJM, 2000. Metal accumulating plants. In : Raskin I, Ensey BD, eds. Phytoremediation of toxic metals: using plants to clean up the environment. New York, NY, USA : Wiley & Sons.
116. Ridge P, Zhang Y, Gladyshev V. 2008. Comparative genomic analyses of copper transporters and cuproproteomes reveal evolutionary dynamics of copper utilization and its link to oxygen. PLoS ONE 3 : e1378.
117. Rizhsky L, Liang H, Mittler R. 2003. The water-water cycle is essential for chloroplast protection in the absence of stress. Journal of Biological Chemistry 278 : 38921 38925. (Pubitemid 37221792)
118. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397 : 694 697. (Pubitemid 29108388)
119. 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 : 996 998. (Pubitemid 129505221)
120. Ruiter HJ. 1969. Suspected copper deficiency in radiata pine. Plant and Soil 31 : 197 200.
121. Ruzsa SM, Scandalios JG. 2003. Altered Cu metabolism and differential transcription of Cu/ZnSod genes in a Cu/ZnSOD-deficient mutant of maize: evidence for a Cu-responsive transcription factor. Biochemistry 42 : 1508 1516. (Pubitemid 36205957)
122. 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. Journal of Biological Chemistry 279 : 15348 15355. (Pubitemid 38618933)
123. Sancenon V, Puig S, Mira H, Thiele DJ, Penarrubia L. 2003. Identification of a copper transporter family in Arabidopsis thaliana. Plant Molecular Biology 51 : 577 587. (Pubitemid 36325932)
124. +-ATPase. Journal of Biological Chemistry 281 : 11161 11166. (Pubitemid 43855541)
125. 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. Journal of Biological Chemistry 279 : 9091 9096. (Pubitemid 38295973)
126. 3- by the tomato mutant chloronerva. Biochemie und Physiologie der Pflanzen 182 : 189 194.
127. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T. 2002. Proteome map of the chloroplast lumen of Arabidopsis thaliana. Journal of Biological Chemistry 277 : 8354 8365
128. Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J et al. 2006. HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. Journal of Biological Chemistry 281 : 2882 2892. (Pubitemid 43845754)
129. Sgherri C, Quartacci MF, Navari-Izzo F. 2007. Early production of activated oxygen species in root apoplast of wheat following copper excess. Journal of Plant Physiology 164 : 1152 1160. (Pubitemid 47238517)
130. 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 1346. (Pubitemid 36715176)
131. Shingles R, Wimmers LE, McCarty RE. 2004. Copper transport across pea thylakoid membranes. Plant Physiology 135 : 145 151. (Pubitemid 38653662)
132. Stacey MG, Koh S, Becker J, Stacey G. 2002. AtOPT3, a member of the oligopeptide transporter family, is essential for embryo development in Arabidopsis. The Plant Cell 14 : 2799 2811. (Pubitemid 35326305)
133. Stephan UW, Grun M. 1989. Physiological disorders of the nicotianamine-auxotroph tomato mutant chloronerva at different levels of iron nutrition II. Iron deficiency response and heavy metal metabolism. Biochem Physiol Pflanzen 185 : 189 200.
134. Sunkar R, Zhu JK. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16 : 2001 2019. (Pubitemid 39059724)
135. Sunkar R, Girke T, Jain PK, Zhu JK. 2005. Cloning and characterization of microRNAs from rice. Plant Cell 17 : 1397 1411. (Pubitemid 43138193)
136. 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 2065. (Pubitemid 44260196)
137. 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. Biochimica et Biophysica Acta 1326 : 1 6. (Pubitemid 27226804)
138. 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 1280. (Pubitemid 36715171)
139. Tang S, Wilke BM, Changyong HC. 1999. The uptake of copper by plants dominantly growing on copper mining spoils along the Yangtze River, the People's Republic of China. Plant and Soil 209 : 225 232. (Pubitemid 29368501)
140. Thipyapong P, Joel DM, Steffens JC. 1997. Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiology 113 : 707 718. (Pubitemid 27169986)
141. Tottey S, Rich PR, Rondet SA, Robinson NJ. 2001. Two Menkes-type ATPases supply copper for photosynthesis in Synechocystis PCC 6803. Journal of Biological Chemistry 276 : 19999 20004. (Pubitemid 37411066)
142. Tottey S, Rondet SA, Borrelly GP, Robinson PJ, Rich PR, Robinson NJ. 2002. A copper metallochaperone for photosynthesis and respiration reveals metal-specific targets, interaction with an importer, and alternative sites for copper acquisition. Journal of Biological Chemistry 277 : 5490 5497.
143. Tottey S, Waldron KJ, Firbank SJ, Reale B, Bessant C, Sato K, Cheek TR, Gray J, Banfield MJ, Dennison C et al. 2008. Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 455 : 1138 1142.
144. Trindade LM, Horvath BM, Bergervoet MJE, Visser RG. 2003. Isolation of a gene encoding a copper chaperone for the copper/zinc superoxide dismutase and characterization of its promoter in potato. Plant Physiology 133 : 618 629. (Pubitemid 37325674)
145. Waldron KJ, Tottey S, Yanagisawa S, Dennison C, Robinson NJ. 2007. A periplasmic iron-binding protein contributes toward inward copper supply. Journal of Biological Chemistry 282 : 3837 3846. (Pubitemid 47084464)
146. Wang Y, Li Q, Shi J, Lin Q, Chen X, Wu W, Chen Y. 2008. Assessment of microbial activity and bacterial community composition in the rhizosphere of a copper accumulator and an non-accumulator. Soil Biology & Biochemistry 40 : 1167 1177.
147. 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 Phytologist 177 : 389 405. (Pubitemid 350295785)
148. 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 Physiology 141 : 1446 1458. (Pubitemid 44223295)
149. 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. Journal of Biological Chemistry 278 : 31286 31289. (Pubitemid 36994646)
150. 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 : 555 561.
151. 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. Journal of Experimental Botany 55 : 1997 2004. (Pubitemid 39211157)
152. Williams LE, Mills RF. 2005. P(1B)-ATPases: an ancient family of transition metal pumps with diverse functions in plants. Trends in Plant Science 10 : 491 502. (Pubitemid 41395271)
153. 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. Journal of Biological Chemistry 278 : 47644 47653. (Pubitemid 37523209)
154. Wintz H, Vulpe C. 2002. Plant copper chaperones. Biochemical Society Transactions 30 : 732 735.
155. 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 : 443 455. (Pubitemid 30186312)
156. Wu CC, Rice WJ, Stokes DL. 2008. Structure of a copper pump suggests a regulatory role for its metal-binding domain. Structure 16 : 976 985.
157. 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. Journal of Experimental Botany 56 : 1785 1796. (Pubitemid 40907142)
158. Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M. 2007. Regulation of copper homeostasis by micro-RNA in Arabidopsis. Journal of Biological Chemistry 282 : 16369 16378. (Pubitemid 47100389)
159. Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Toshiharu Shikanai T. 2009. SQUAMOSA promoter-binding protein-like 7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21 : 347 361.
160. Yruela I, Pueyo JJ, Alonso PJ, Picorel R. 1996. Photoinhibition of photosystem II from higher plants. Effect of copper inhibition. Journal of Biological Chemistry 271 : 27408 27415. (Pubitemid 26367298)
161. Zhang L, McSpadden B, Pakrasi HB, Whitmarsh J. 1992. Copper-mediated regulation of cytochrome c553 and plastocyanin in the cyanobacterium Synechocystis 6803. Journal of Biological Chemistry 267 : 19054 19059.
162. Zhou J, Goldsbrough PB. 1994. Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6 : 875 884. (Pubitemid 2112732)
163. 2+) binding to human and tomato copper chaperone for superoxide dismutase: implications for the metal ion transfer mechanism. Biochemistry 39 : 5413 5421. (Pubitemid 30257082)
164. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ. 2008. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3 : e1994.