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Ion homeostasis in the Chloroplast

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Plastid Biology

Part of the book series: Advances in Plant Biology ((AIPB,volume 5))

Abstract

The chloroplast is an organelle of high demand for macro- and micro-nutrient ions, which are required for the maintenance of the photosynthetic process. To avoid deficiency while preventing excess, homeostasis mechanisms must be tightly regulated. Here, we describe the needs for nutrient ions in the chloroplast and briefly highlight their functions in the chloroplastidial metabolism. We further discuss the impact of nutrient deficiency on chloroplasts and the acclimation mechanisms that evolved to preserve the photosynthetic apparatus. We finally present what is known about import and export mechanisms for these ions. Whenever possible, a comparison between cyanobacteria, algae and plants is provided to add an evolutionary perspective to the description of ion homeostasis mechanisms in photosynthesis.

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Abbreviations

Arabidopsis:

Arabidopsis thaliana

ABC:

ATP-binding-cassette

APS:

Adenosine 5′-phosphosulfate

ATP:

Adénosine-5′-triphosphate

ATPS:

ATP Sulfurylase

CaM:

Calmodulin

CAS:

Calcium-sensing protein

Chl:

Chlorophyll

CPA2:

Cation/proton antiporters 2

CuRE:

Copper responsive element

Cytc 6 :

Cytochrome c 6

CytOx:

Cytochrome c oxidase

Chlamydomonas:

Chlamydomonas reinhardtii

Ery-4-P:

Erythrose 4-phosphate

Fe/S:

Iron/Sulfur cluster

FD:

Ferredoxin

Glu-6-P:

Glucose 6-phosphate

GOGAT:

Glutamate synthase

GPT:

Glucose 6-phosphate/phosphate translocator

GS:

Glutamine synthetase

GSH:

Glutathione

GUN:

Genomes uncoupled

ISC:

Iron-sulfur cluster

LHC:

Light harvesting complex

NADK:

NAD kinase

NAP:

Non intrinsic ABC protein

NIF:

NItrogenase fixation

NiR:

Nitrite reductase

NR:

Nitrate reductase

OEC:

Oxygen-evolving complex

OEP:

Outer envelop proteins

PC:

Plastocyanin

PEP:

Phosphoenolpyruvate

Pi:

Inorganic orthophosphate

PNPase:

Ribonuclease polynucleotide phosphorylase

PPT:

Phosphoenolpyruvate/phosphate translocator

PSI:

Photosystem I

PSII:

Photosystem II

PTOX:

Plastoquinol terminal oxidase

Pyr:

Pyruvate

Rib-5-P:

Ribulose 5-phosphate

ROS:

Reactive oxygen species

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase

SOD:

Superoxide dismutase

SUF:

Sulfur fixation

TIC:

Translocon at the Inner envelope membrane of Chloroplast

TOC:

Translocon at the Outer envelope membrane of Chloroplast

TP:

Triose phosphate

TPT:

Triose phosphate translocator (TPT)

XPT:

Xylulose 5-phosphate/phosphate translocator

Xyl-5-P:

Xylulose 5-phosphate

References

  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

    PubMed  CAS  Google 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 283:15932–15945

    PubMed  CAS  PubMed Central  Google 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 17:1233–1251

    PubMed  CAS  PubMed Central  Google Scholar 

  4. Abdel-Ghany SE, Burkhead JL, Gogolin KA, Andrés-Colás N, Bodecker JR, Puig S, Peñarrubia L, Pilon M (2005) AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7. FEBS Lett 579:2307–2312

    PubMed  CAS  Google Scholar 

  5. Accardi A, Walden M, Nguitragool W, Jayaram H, Williams C, Miller C (2005) Separate ion pathways in a Cl−/H+ exchanger. J Gen Physiol 126:563–570

    PubMed  CAS  PubMed Central  Google Scholar 

  6. Adhikari ND, Orler R, Chory J, Froehlich JE, Larkin RM (2009) Porphyrins promote the association of GENOMES UNCOUPLED 4 and a Mg-chelatase subunit with chloroplast membranes. J Biol Chem 284:24783–24796

    PubMed  CAS  PubMed Central  Google Scholar 

  7. Adhikari ND, Froehlich JE, Strand DD, Buck SM, Kramer DM, Larkin RM (2011) GUN4-porphyrin complexes bind the ChlH/GUN5 subunit of Mg-Chelatase and promote chlorophyll biosynthesis in Arabidopsis. Plant Cell 23:1449–1467

    PubMed  CAS  PubMed Central  Google Scholar 

  8. Allen MD, Kropat J, Tottey S, Del Campo JA, Merchant SS (2007) Manganese deficiency in chlamydomonas results in loss of photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol 143:263–277

    PubMed  CAS  PubMed Central  Google Scholar 

  9. Allmer J, Naumann B, Markert C, Zhang M, Hippler M (2006) Mass spectrometric genomic data mining: novel insights into bioenergetic pathways in Chlamydomonas reinhardtii. Proteomics 6:6207–6220

    PubMed  CAS  Google Scholar 

  10. Alvarez JM, Vidal EA, Gutiérrez RA (2012) Integration of local and systemic signaling pathways for plant N responses. Curr Opin Plant Biol 15:185–191

    PubMed  CAS  Google Scholar 

  11. Amtmann A, Armengaud P (2009) Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis. Curr Opin Plant Biol 12:275–283

    PubMed  CAS  Google Scholar 

  12. Andaluz S, López-Millán AF, De Las Rivas J, Aro EM, Abadía J, Abadía A (2006) Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth Res 89:141–155

    PubMed  CAS  Google Scholar 

  13. Anderson JM, Charbonneau H, Jones HP, McCann RO, Cormier MJ (1980) Characterization of the plant nicotinamide adenine dinucleotide kinase activator protein and its identification as calmodulin. Biochemistry 19:3113–3120

    PubMed  CAS  Google Scholar 

  14. Andrews SC, Robinson AK, Rodrı́guez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237

    PubMed  CAS  Google Scholar 

  15. Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239

    PubMed  CAS  Google Scholar 

  16. Aran M, Ferrero D, Wolosiuk A, Mora-García S, Wolosiuk RA (2011) ATP and Mg2+ promote the reversible oligomerization and aggregation of chloroplast 2-Cys peroxiredoxin. J Biol Chem 286:23441–23451

    PubMed  CAS  PubMed Central  Google Scholar 

  17. Arosio P, Ingrassia R, Cavadini P (2009) Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim Biophys Acta 1790:589–599

    PubMed  CAS  Google Scholar 

  18. Ashley MK, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436

    PubMed  CAS  Google Scholar 

  19. Bailey S et al (2008) Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim Biophys Acta 1777:269–276

    PubMed  CAS  Google Scholar 

  20. Balandin T, Castresana C (2002) AtCOX17, an Arabidopsis homolog of the yeast copper chaperone COX17. Plant Physiol 129:1852–1857

    PubMed  CAS  PubMed Central  Google Scholar 

  21. Balk J, Pilon M (2011) Ancient and essential: the assembly of iron-sulfur clusters in plants. Trends Plant Sci 16:218–226

    PubMed  CAS  Google Scholar 

  22. Balsera M, Goetze TA, Kovács-Bogdán E, Schürmann P, Wagner R, Buchanan BB, Soll J, Bölter B (2009) Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca2+ and a stromal regulatory disulfide bridge. J Biol Chem 284:2603–2616

    PubMed  CAS  Google Scholar 

  23. Banci L, Bertini I, Ciofi-Baffoni S, Kandias NG, Robinson NJ, Spyroulias GA, Su XC, Tottey S, Vanarotti M (2006) The delivery of copper for thylakoid import observed by NMR. Proc Natl Acad Sci U S A 103:8320–8325

    PubMed  CAS  PubMed Central  Google Scholar 

  24. Banci L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, Palumaa P (2010) Affinity gradients drive copper to cellular destinations. Nature 465:645–648

    PubMed  CAS  Google Scholar 

  25. Barrero-Gil J, Rodríguez-Navarro A, Benito B (2007) Cloning of the PpNHAD1 transporter of Physcomitrella patens, a chloroplast transporter highly conserved in photosynthetic eukaryotic organisms. J Exp Bot 58:2839–2849

    PubMed  CAS  Google Scholar 

  26. Benning C (2010) The anionic chloroplast membrane lipids: phosphatidylglycerol and sulfoquinovosyldiacylglycerol. In: Rebeiz CA et al (eds) The chloroplast. Springer, Netherlands, pp 171–184

    Google Scholar 

  27. Berkowitz GA, Wu W (1993) Magnesium, potassium flux and photosynthesis. Magnes Res 6:257–265

    PubMed  CAS  Google Scholar 

  28. Bernal M, Testillano PS, Alfonso M, Carmen Risueño Md, Picorel R, Yruela I (2007) Identification and subcellular localization of the soybean copper P1B-ATPase GmHMA8 transporter. J Struct Biol 158:46–58

    PubMed  CAS  Google Scholar 

  29. Bernal M et al (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24:738–761

    PubMed  CAS  PubMed Central  Google Scholar 

  30. Bi Y-M, Wang R-L, Zhu T, Rothstein S (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8:281

    PubMed  PubMed Central  Google Scholar 

  31. Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745

    PubMed  CAS  Google Scholar 

  32. Blindauer CA (2008) Zinc-handling in cyanobacteria: an update. Chem Biodivers 5:1990–2013

    PubMed  CAS  Google Scholar 

  33. Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748

    PubMed  CAS  Google Scholar 

  34. Bölter B, Soll J (2001) Ion channels in the outer membranes of chloroplasts and mitochondria: open doors or regulated gates? EMBO J 20:935–940

    PubMed  PubMed Central  Google Scholar 

  35. Boyd PW, Ellwood MJ (2010) The biogeochemical cycle of iron in the ocean. Nat Geosci 3:675–682

    CAS  Google Scholar 

  36. Brand JJ, Becker DW (1984) Evidence for direct roles of calcium in photosynthesis. J Bioenerg Biomembr 16:239–249

    PubMed  CAS  Google Scholar 

  37. Briat JF, Ravet K, Arnaud N, Duc C, Boucherez J, Touraine B, Cellier F, Gaymard F (2010) New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann Bot 105:811–822

    PubMed  CAS  PubMed Central  Google Scholar 

  38. Brunswick P, Cresswell CF (1988) Nitrite uptake into intact pea chloroplasts. 1. Kinetics and relationship with nitrite assimilation. Plant Physiol 86:378–383

    PubMed  CAS  PubMed Central  Google Scholar 

  39. Brunswick P, Cresswell CF (1988) Nitrite uptake into intact pea chloroplasts. 2. Influence of electron-transport regulators, uncouplers, ATPase and anion uptake inhibitors and protein binding reagents. Plant Physiol 86:384–389

    PubMed  CAS  PubMed Central  Google Scholar 

  40. Buaboocha T, Liao B, Zielinski RE (2001) Isolation of cDNA and genomic DNA clones encoding a calmodulin-binding protein related to a family of ATPases involved in cell division and vesicle fusion. Planta 212:774–781

    PubMed  CAS  Google Scholar 

  41. Buchner P, Takahashi H, Hawkesford MJ (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773

    PubMed  CAS  Google Scholar 

  42. Bughio N, Takahashi M, Yoshimura E, Nishizawa NK, Mori S (1997) Light-dependent iron transport into isolated barley chloroplasts. Plant Cell Physiol 38:101–105

    CAS  Google Scholar 

  43. Burkhead JL, Abdel-Ghany SE, Morrill JM, Pilon-Smits EAH, Pilon M (2003) The Arabidopsis thaliana CUTA gene encodes an evolutionarily conserved copper binding chloroplast protein. Plant J 34:856–867

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  45. Busch A, Rimbauld B, Naumann B, Rensch S, Hippler M (2008) Ferritin is required for rapid remodeling of the photosynthetic apparatus and minimizes photo-oxidative stress in response to iron availability in Chlamydomonas reinhardtii. Plant J 55:201–211

    PubMed  CAS  Google Scholar 

  46. Bussemer J, Chigri F, Vothknecht UC (2009) Arabidopsis ATPase family gene 1-like protein 1 is a calmodulin-binding AAA+-ATPase with a dual localization in chloroplasts and mitochondria. FEBS J 276:3870–3880

    PubMed  CAS  Google Scholar 

  47. Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704

    PubMed  CAS  Google Scholar 

  48. Cakmak I, Hengeler C, Marschner H (1994) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. J Exp Bot 45:1251–1257

    CAS  Google Scholar 

  49. Cardol P et al (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci U S A 105:7881–7886

    PubMed  CAS  PubMed Central  Google Scholar 

  50. Castruita M et al (2011) Systems biology approach in chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23:1273–1292

    PubMed  CAS  PubMed Central  Google Scholar 

  51. Catty P, Boutigny S, Miras R, Joyard J, Rolland N, Seigneurin-Berny D (2011) Biochemical characterization of AtHMA6/PAA1, a chloroplast envelope Cu(I)-ATPase. J Biol Chem 286:36188–36197

    PubMed  CAS  PubMed Central  Google Scholar 

  52. Cavet JS, Borrelly GP, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181

    PubMed  CAS  Google Scholar 

  53. Chang C-W, Moseley JL, Wykoff D, Grossman AR (2005) The LPB1 gene is important for acclimation of Chlamydomonas reinhardtii to phosphorus and sulfur deprivation. Plant Physiol 138:319–329

    PubMed  CAS  PubMed Central  Google Scholar 

  54. Changela A, Chen K, Xue Y, Holschen J, Outten CE, O’Halloran TV, Mondragón A (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383–1387

    PubMed  CAS  Google Scholar 

  55. Chardot T, Meunier J-C (1990) Fructose-1,6-bisphosphate and calcium activate oxidized spinach (Spinacia oleracea) chloroplast fructose-1,6-bisphosphatase. Plant Sci 70:1–9

    CAS  Google Scholar 

  56. Charles SA, Halliwell B (1980) Action of calcium ions on spinach (Spinacia oleracea) chloroplast fructose bisphosphatase and other enzymes of the Calvin cycle. Biochem J 188:775–779

    PubMed  CAS  PubMed Central  Google Scholar 

  57. Chen C, Kazimir J, Cheniae GM (1995) Calcium modulates the photoassembly of photosystem II (Mn)4-clusters by preventing ligation of nonfunctional high-valency states of manganese. Biochemistry 34:13511–13526

    PubMed  CAS  Google Scholar 

  58. Chen H-C, Melis A (2004) Localization and function of SulP, a nuclear-encoded chloroplast sulfate permease in Chlamydomonas reinhardtii. Planta 220:198–210

    PubMed  CAS  Google Scholar 

  59. Chen H-C, Yokthongwattana K, Newton AJ, Melis A (2003) SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii. Planta 218:98–106

    PubMed  CAS  Google Scholar 

  60. Chen H-C, Newton AJ, Melis A (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii. Photosynth Res 84:289–296

    PubMed  CAS  Google Scholar 

  61. Chen W, Yang X, He Z, Feng Y, Hu F (2008) Differential changes in photosynthetic capacity, 77 K chlorophyll fluorescence and chloroplast ultrastructure between Zn-efficient and Zn-inefficient rice genotypes (Oryza sativa) under low zinc stress. Physiol Plant 132:89–101

    PubMed  CAS  Google Scholar 

  62. Cherif J, Derbel N, Nakkach M, Bergmann H, Jemal F, Lakhdar ZB (2010) Analysis of in vivo chlorophyll fluorescence spectra to monitor physiological state of tomato plants growing under zinc stress. J Photochem Photobiol B 101:332–339

    PubMed  CAS  Google Scholar 

  63. Chigri F, Soll J, Vothknecht UC (2005) Calcium regulation of chloroplast protein import. Plant J 42:821–831

    PubMed  CAS  Google Scholar 

  64. Chigri F, Hörmann F, Stamp A, Stammers DK, Bölter B, Soll J, Vothknecht UC (2006) Calcium regulation of chloroplast protein translocation is mediated by calmodulin binding to Tic32. Proc Natl Acad Sci U S A 103:16051–16056

    PubMed  CAS  PubMed Central  Google Scholar 

  65. 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 139:425–436

    PubMed  CAS  PubMed Central  Google Scholar 

  66. Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Annu Rev Plant Biol 31:239–298

    CAS  Google Scholar 

  67. Claus-Peter W (2011) Urea metabolism in plants. Plant Sci 180:431–438

    Google Scholar 

  68. Cobbett CS, Hussain D, Haydon MJ (2003) Structural and functional relationships between type 1B heavy metal-transporting P-type ATPases in Arabidopsis. New Phytol 159:315–321

    CAS  Google Scholar 

  69. Cohu CM, Abdel-Ghany SE, Gogolin Reynolds KA, Onofrio AM, Bodecker JR, Kimbrel JA, Niyogi KK, Pilon M (2009) Copper delivery by the copper chaperone for chloroplast and cytosolic copper/zinc-superoxide dismutases: regulation and unexpected phenotypes in an Arabidopsis mutant. Mol Plant 2:1336–1350

    PubMed  CAS  Google Scholar 

  70. Collier JL, Grossman AR (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol 174:4718–4726

    PubMed  CAS  PubMed Central  Google Scholar 

  71. Conte SS, Lloyd AM (2010) The MAR1 transporter is an opportunistic entry point for antibiotics. Plant Signal Behav 5:49–52

    PubMed  CAS  PubMed Central  Google Scholar 

  72. Conte S, Stevenson D, Furner I, Lloyd A (2009) Multiple antibiotic resistance in Arabidopsis is conferred by mutations in a chloroplast-localized transport protein. Plant Physiol 151:559–573

    PubMed  CAS  PubMed Central  Google Scholar 

  73. Cornah JE, Terry MJ, Smith AG (2003) Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci 8:224–230

    PubMed  CAS  Google Scholar 

  74. Corratgé-Faillie C, Jabnoune M, Zimmermann S, Véry AA, Fizames C, Sentenac H (2010) Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cell Mol Life Sci 67:2511–2532

    PubMed  Google Scholar 

  75. Cosentino C, Fischer-Schliebs E, Bertl A, Thiel G, Homann U (2010) Na+/H+ antiporters are differentially regulated in response to NaCl stress in leaves and roots of Mesembryanthemum crystallinum. New Phytol 186:669–680

    PubMed  CAS  Google Scholar 

  76. Daram P, Brunner S, Rausch C, Steiner C, Amrhein N, Bucher M (1999) Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell 11:2153–2166

    PubMed  CAS  PubMed Central  Google Scholar 

  77. Davies JP, Yildiz FH, Grossman A (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15:2150–2159

    PubMed  CAS  PubMed Central  Google Scholar 

  78. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939–942

    PubMed  CAS  Google Scholar 

  79. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2009) CLC-mediated anion transport in plant cells. Philos Trans R Soc Lond B Biol Sci 364:195–201

    PubMed  CAS  PubMed Central  Google Scholar 

  80. Dechorgnat J, Nguyen CT, Armengaud P, Jossier M, Diatloff E, Filleur S, Daniel-Vedele F (2011) From the soil to the seeds: the long journey of nitrate in plants. J Exp Bot 62:1349–1359

    PubMed  CAS  Google Scholar 

  81. Demmig B, Gimmler H (1983) Properties of the isolated intact chloroplast at cytoplasmic K concentrations: I. light-induced cation uptake into intact chloroplasts is driven by an electrical potential difference. Plant Physiol 73:169–174

    PubMed  CAS  PubMed Central  Google Scholar 

  82. Di Baccio D, Galla G, Bracci T, Andreucci A, Barcaccia G, Tognetti R, Sebastiani L (2011) Transcriptome analyses of Populus x euramericana clone I-214 leaves exposed to excess zinc. Tree Physiol 31:1293–1308

    PubMed  CAS  Google Scholar 

  83. Diédhiou CJ, Golldack D (2006) Salt-dependent regulation of chloride channel transcripts in rice. Plant Sci 170:793–800

    Google Scholar 

  84. Drummond RSM, Tutone A, Li YC, Gardner RC (2006) A putative magnesium transporter AtMRS2-11 is localized to the plant chloroplast envelope membrane system. Plant Sci 170:78–89

    CAS  Google Scholar 

  85. Dunkley TP et al (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci U S A 103:6518–6523

    PubMed  CAS  PubMed Central  Google Scholar 

  86. Duy D, Soll J, Philippar K (2007) Solute channels of the outer membrane: from bacteria to chloroplasts. Biol Chem 388:879–889

    PubMed  CAS  Google Scholar 

  87. Duy D, Wanner G, Meda AR, von Wirén N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19:986–1006

    PubMed  CAS  PubMed Central  Google Scholar 

  88. Duy D, Stübe R, Wanner G, Philippar K (2011) The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol 155:1709–1722

    PubMed  CAS  PubMed Central  Google Scholar 

  89. Eitinger T, Suhr J, Moore L, Smith JA (2005) Secondary transporters for nickel and cobalt ions: theme and variations. Biometals 18:399–405

    PubMed  CAS  Google Scholar 

  90. Elias M, Archibald JM (2009) Sizing up the genomic footprint of endosymbiosis. Bioessays 31:1273–1279

    PubMed  CAS  Google Scholar 

  91. Eriksson M, Moseley JL, Tottey S, Del Campo JA, Quinn J, Kim Y, Merchant S (2004) Genetic dissection of nutritional copper signaling in Chlamydomonas distinguishes regulatory and target genes. Genetics 168:795–807

    PubMed  CAS  PubMed Central  Google Scholar 

  92. Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1386

    PubMed  CAS  PubMed Central  Google Scholar 

  93. Fang Z, Mi F, Berkowitz GA (1995) Molecular and physiological analysis of a thylakoid K+ channel protein. Plant Physiol 108:1725–1734

    PubMed  CAS  PubMed Central  Google Scholar 

  94. Fernández E, Galván A (2007) Inorganic nitrogen assimilation in Chlamydomonas. J Exp Bot 58:2279–2287

    PubMed  Google Scholar 

  95. Ferrario-Méry S, Bouvet M, Leleu O, Savino G, Hodges M, Meyer C (2005) Physiological characterisation of Arabidopsis mutants affected in the expression of the putative regulatory protein PII. Planta 223:28–39

    PubMed  Google Scholar 

  96. Ferrario-Méry S, Meyer C, Hodges M (2008) Chloroplast nitrite uptake is enhanced in Arabidopsis PII mutants. FEBS Lett 582:1061–1066

    PubMed  Google Scholar 

  97. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    PubMed  CAS  Google Scholar 

  98. Ferro M, Salvi D, Riviere-Rolland H, Vermat T, Seigneurin-Berny D, Grunwald D, Garin J, Joyard J, Rolland N (2002) Integral membrane proteins of the chloroplast envelope: identification and subcellular localization of new transporters. Proc Natl Acad Sci U S A 99:11487–11492

    PubMed  CAS  PubMed Central  Google Scholar 

  99. Ferro M, Salvi D, Brugière S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2:325–345

    PubMed  CAS  Google Scholar 

  100. Ferro M et al (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9:1063–1084

    PubMed  CAS  PubMed Central  Google Scholar 

  101. Finney LA, O’Halloran TV (2003) Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300:931–936

    PubMed  CAS  Google Scholar 

  102. Flügge U-I, Häusler RE, Ludewig F, Fischer K (2003) Functional genomics of phosphate antiport systems of plastids. Physiol Plant 118:475–482

    Google Scholar 

  103. Flügge UI, Häusler RE, Ludewig F, Gierth M (2011) The role of transporters in supplying energy to plant plastids. J Exp Bot 62:2381–2392

    PubMed  Google Scholar 

  104. Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA, Phinney BS (2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J Proteome Res 2:413–425

    PubMed  Google Scholar 

  105. Fukada-Tanaka S, Inagaki Y, Yamaguchi T, Saito N, Iida S (2000) Colour-enhancing protein in blue petals. Nature 407:581

    PubMed  CAS  Google Scholar 

  106. Furumoto T et al (2011) A plastidial sodium-dependent pyruvate transporter. Nature 476:472–475

    PubMed  CAS  Google Scholar 

  107. Garcia-Molina A, Andrés-Colás N, Perea-García A, Del Valle-Tascón S, Peñarrubia L, Puig S (2011) The intracellular Arabidopsis COPT5 transport protein is required for photosynthetic electron transport under severe copper deficiency. Plant J 65:848–860

    PubMed  CAS  Google Scholar 

  108. Gebert M, Meschenmoser K, Svidová S, Weghuber J, Schweyen R, Eifler K, Lenz H, Weyand K, Knoop V (2009) A root-expressed magnesium transporter of the MRS2/MGT gene family in Arabidopsis thaliana allows for growth in low-Mg2+ environments. Plant Cell 21:4018–4030

    PubMed  CAS  PubMed Central  Google Scholar 

  109. Geelen D, Lurin C, Bouchez D, Frachisse JM, Lelièvre F, Courtial B, Barbier-Brygoo H, Maurel C (2000) Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content. Plant J 21:259–267

    PubMed  CAS  Google Scholar 

  110. Gertz M, Seelert H, Dencher NA, Poetsch A (2007) Interactions of rotor subunits in the chloroplast ATP synthase modulated by nucleotides and by Mg2+. Biochim Biophys Acta 1774:566–574

    PubMed  CAS  Google Scholar 

  111. Glass ADM et al (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

    PubMed  CAS  Google Scholar 

  112. González-Ballester D, Camargo A, Fernández E (2004) Ammonium transporter genes in Chlamydomonas: the nitrate-specific regulatory gene Nit2 is involved in Amt1;1 expression. Plant Mol Biol 56:863–878

    PubMed  Google Scholar 

  113. González-Ballester D, Pollock SV, Pootakham W, Grossman AR (2008) The central role of a SNRK2 kinase in sulfur deprivation responses. Plant Physiol 147:216–227

    PubMed  PubMed Central  Google Scholar 

  114. González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22:2058–2084

    PubMed  PubMed Central  Google Scholar 

  115. Gordon T, Lea PJ, Rosenberg C, Trinchnat JC (2001) Nodule formation and function. In: Lea PJ, Morot-Gaudry J-F (eds) Plant nitrogen. Springer, Berlin, pp 101–146

    Google Scholar 

  116. Gray JC (2003) Chloroplast-to-nucleus signalling: a role for Mg-protoporphyrin. Trends Genet 19:526–529

    PubMed  CAS  Google Scholar 

  117. Grossman AR, González-Ballester D, Shibagaki N, Pootakham W, Moseley J (2010) Responses to macronutrient deprivation. In: Pareek A, Sopory SK, Bohnert HJ (eds) Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer, Netherlands, pp 307–348

    Google Scholar 

  118. Grove GN, Brudvig GW (1998) Calcium binding studies of photosystem II using a calcium-selective electrode. Biochemistry 37:1532–1539

    PubMed  CAS  Google Scholar 

  119. Guo B, Irigoyen S, Fowler TB, Versaw WK (2008) Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues. Plant Signal Behav 3:784–790

    PubMed  PubMed Central  Google Scholar 

  120. Guo B, Jin Y, Wussler C, Blancaflor EB, Motes CM, Versaw WK (2008) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol 177:889–898

    PubMed  CAS  Google Scholar 

  121. Haas CE, Rodionov DA, Kropat J, Malasarn D, Merchant SS, de Crecy-Lagard V (2009) A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genomics 10:470

    PubMed  PubMed Central  Google Scholar 

  122. Hammond JP et al (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132:578–596

    PubMed  CAS  PubMed Central  Google Scholar 

  123. Han S, Tang R, Anderson LK, Woerner TE, Pei ZM (2003) A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 425:196–200

    PubMed  CAS  Google Scholar 

  124. 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 Cyanidioschizon merolae. Plant Physiol 137:428–446

    PubMed  CAS  PubMed Central  Google Scholar 

  125. Hanikenne M, Merchant SS, Hamel P (2009) Transition metal nutrition: a balance between deficiency and toxicity. In: Stern D, Harris EH (eds) The Chlamydomonas. Organellar and metabolic processes, vol 2. Elsevier, Amsterdam, pp 333–399

    Google Scholar 

  126. Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    PubMed  Google Scholar 

  127. Harada H, Kuromori T, Hirayama T, Shinozaki K, Leigh RA (2004) Quantitative trait loci analysis of nitrate storage in Arabidopsis leading to an investigation of the contribution of the anion channel gene, AtCLC-c, to variation in nitrate levels. J Exp Bot 55:2005–2014

    PubMed  CAS  Google Scholar 

  128. Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565

    PubMed  CAS  Google Scholar 

  129. Hawkesford MJ (2008) Uptake, distribution and subcellular transport of sulfate. In: Hell R et al (eds) Sulfur metabolism in phototrophic organisms. Springer, Netherlands, pp 15–30

    Google Scholar 

  130. Haydon MJ, Bell LJ, Webb AAR (2011) Interactions between plant circadian clocks and solute transport. J Exp Bot 62:2333–2348

    PubMed  CAS  Google Scholar 

  131. Hechenberger M, Schwappach B, Fischer WN, Frommer WB, Jentsch TJ, Steinmeyer K (1996) A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption. J Biol Chem 271:33632–33638

    PubMed  CAS  Google Scholar 

  132. Heiber T, Steinkamp T, Hinnah S, Schwarz M, Flügge UI, Weber A, Wagner R (1995) Ion channels in the chloroplast envelope membrane. Biochemistry 34:15906–15917

    PubMed  CAS  Google Scholar 

  133. Hell R, Wirtz M (2008) Metabolism of cysteine in plants and phototrophic bacteria. In: Hell R et al (eds) Sulfur metabolism in phototrophic organisms. Springer, Netherlands, pp 59–91

    Google Scholar 

  134. Hell R, Khan M, Wirtz M (2010) Cellular biology of sulfur and its functions in plants. In: Hell R, Mendel R-R (eds) Cell biology of metals and nutrients. Springer, Berlin/Heidelberg, pp 243–279

    Google Scholar 

  135. Hermans C, Verbruggen N (2005) Physiological characterization of Mg deficiency in Arabidopsis thaliana. J Exp Bot 56:2153–2161

    PubMed  CAS  Google Scholar 

  136. Hermans C, Bourgis F, Faucher M, Strasser RJ, Delrot S, Verbruggen N (2005) Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves. Planta 220:541–549

    PubMed  CAS  Google Scholar 

  137. Hermans C, Vuylsteke M, Coppens F, Craciun A, Inzé D, Verbruggen N (2010) Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol 187:119–131

    PubMed  CAS  Google Scholar 

  138. Hermans C, Vuylsteke M, Coppens F, Cristescu SM, Harren FJ, Inzé D, Verbruggen N (2010) Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol 187:132–144

    PubMed  CAS  Google Scholar 

  139. Higuchi M, Ozaki H, Matsui M, Sonoike K (2009) A T-DNA insertion mutant of AtHMA1 gene encoding a Cu transporting ATPase in Arabidopsis thaliana has a defect in the water-water cycle of photosynthesis. J Photochem Photobiol B 94:205–213

    PubMed  CAS  Google Scholar 

  140. Hill KL, Merchant S (1995) Coordinate expression of coproporphyrinogen oxidase and cytochrome c 6 in the green alga Chlamydomonas reinhardtii in response to changes in copper availability. EMBO J 14:857–865

    PubMed  CAS  PubMed Central  Google Scholar 

  141. 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 117:1227–1234.

    PubMed  CAS  PubMed Central  Google Scholar 

  142. Hirai MY et al (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280:25590–25595

    PubMed  CAS  Google Scholar 

  143. Hoefgen R, Nikiforova VJ (2008) Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol Plant 132:190–198

    PubMed  CAS  Google Scholar 

  144. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008:420747

    PubMed  PubMed Central  Google Scholar 

  145. Hsieh MH, Lam HM, van de Loo FJ, Coruzzi G (1998) A PII-like protein in Arabidopsis, putative role in nitrogen sensing. Proc Natl Acad Sci U S A 95:13965–13970

    PubMed  CAS  PubMed Central  Google Scholar 

  146. Huang L, Berkelman T, Franklin AE, Hoffman NE (1993) Characterization of a gene encoding a Ca2+-ATPase-like protein in the plastid envelope. Proc Natl Acad Sci U S A 90:10066–10070

    PubMed  CAS  PubMed Central  Google Scholar 

  147. Huber SC, Maury W (1980) Effects of magnesium on intact chloroplasts: I. EVIDENCE FOR ACTIVATION OF (SODIUM) POTASSIUM/PROTON EXCHANGE ACROSS THE CHLOROPLAST ENVELOPE. Plant Physiol 65:350–354

    PubMed  CAS  PubMed Central  Google Scholar 

  148. Husted S, Laursen KH, Hebbern CA, Schmidt SB, Pedas P, Haldrup A, Jensen PE (2009) Manganese deficiency leads to genotype-specific changes in fluorescence induction kinetics and state transitions. Plant Physiol 150:825–833

    PubMed  CAS  PubMed Central  Google Scholar 

  149. Irigoyen S, Karlsson PM, Kuruvilla J, Spetea C, Versaw WK (2011) The sink-specific plastidic phosphate transporter PHT4;2 influences starch accumulation and leaf size in Arabidopsis. Plant Physiol 157:1765–1777

    PubMed  CAS  PubMed Central  Google Scholar 

  150. Irihimovitch V, Yehudai-Resheff S (2008) Phosphate and sulfur limitation responses in the chloroplast of Chlamydomonas reinhardtii. FEMS Microbiol Lett 283:1–8

    PubMed  CAS  Google Scholar 

  151. 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. Proc Natl Acad Sci U S A 105:10619–10624

    PubMed  CAS  PubMed Central  Google Scholar 

  152. Jin SH, Huang JQ, Li XQ, Zheng BS, Wu JS, Wang ZJ, Liu GH, Chen M (2011) Effects of potassium supply on limitations of photosynthesis by mesophyll diffusion conductance in Carya cathayensis. Tree Physiol 31:1142–1151

    PubMed  CAS  Google Scholar 

  153. Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269:1863–1865

    PubMed  CAS  Google Scholar 

  154. Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704

    PubMed  CAS  PubMed Central  Google Scholar 

  155. Katoh H, Hagino N, Grossman AR, Ogawa T (2001) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183:2779–2784

    PubMed  CAS  PubMed Central  Google Scholar 

  156. Kawamura Y, Takahashi M, Arimura G, Isayama T, Irifune K, Goshima N, Morikawa H (1996) Determination of levels of NO3 −, NO2 −, and NO4 − ions in leaves of various plants by capillary electrophoresis. Plant Cell Physiol 37:878–880

    Google Scholar 

  157. Khan MS et al (2010) Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. Plant Cell 22:1216–1231

    PubMed  CAS  PubMed Central  Google Scholar 

  158. Kim YY, Choi H, Segami S, Cho HT, Martinoia E, Maeshima M, Lee Y (2009) AtHMA1 contributes to the detoxification of excess Zn(II) in Arabidopsis. Plant J 58:737–753

    PubMed  CAS  Google Scholar 

  159. Kim T-H, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591

    PubMed  CAS  PubMed Central  Google Scholar 

  160. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjölander K, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14:354–362

    PubMed  CAS  Google Scholar 

  161. Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet 25:185–192

    PubMed  CAS  Google Scholar 

  162. Knappe S, Flugge UI, Fischer K (2003) Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol 131:1178–1190

    PubMed  CAS  PubMed Central  Google Scholar 

  163. Knoop V, Groth-Malonek M, Gebert M, Eifler K, Weyand K (2005) Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily. Mol Genet Genomics 274:205–216

    PubMed  CAS  Google Scholar 

  164. Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    PubMed  CAS  Google Scholar 

  165. Kobayashi Y, Kanesaki Y, Tanaka A, Kuroiwa H, Kuroiwa T, Tanaka K (2009) Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc Natl Acad Sci U S A 106:803–807

    PubMed  CAS  PubMed Central  Google Scholar 

  166. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    PubMed  CAS  Google Scholar 

  167. Krämer U, Clemens S (2005) Functions and homeostasis of zinc, copper, and nickel in plants. In: Tamás M, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification. Springer, Berlin, pp 216–271

    Google Scholar 

  168. Kreimer G, Melkonian M, Latzko E (1985) An electrogenic uniport mediates light-dependent Ca2+ influx into intact spinach chloroplasts. FEBS Lett 180:253–258

    CAS  Google Scholar 

  169. Kreimer G, Melkonian M, Holtum JA, Latzko E (1988) Stromal free calcium concentration and light-mediated activation of chloroplast fructose-1,6-bisphosphatase. Plant Physiol 86:423–428

    PubMed  CAS  PubMed Central  Google Scholar 

  170. Krieger A, Rutherford AW, Vass I, Hideg E (1998) Relationship between activity, D1 loss, and Mn binding in photoinhibition of photosystem II. Biochemistry 37:16262–16269

    PubMed  CAS  Google Scholar 

  171. Kronzucker HJ, Britto DT (2010) Sodium transport in plants: a critical review. New Phytol 189:54–81

    Google Scholar 

  172. Kropat J, Oster U, Rüdiger W, Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci U S A 94:14168–14172

    PubMed  CAS  PubMed Central  Google Scholar 

  173. Kropat J, Oster U, Rüdiger W, Beck CF (2000) Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24:523–531

    PubMed  CAS  Google Scholar 

  174. Kropat J, Tottey S, Birkenbihl RP, Depège 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 U S A 102:18730–18735

    PubMed  CAS  PubMed Central  Google Scholar 

  175. 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. Eukaryot Cell 1:736–757.

    PubMed  CAS  PubMed Central  Google Scholar 

  176. Laganowsky A, Gómez SM, Whitelegge JP, Nishio JN (2009) Hydroponics on a chip: analysis of the Fe deficient Arabidopsis thylakoid membrane proteome. J Proteomics 72:397–415

    PubMed  CAS  Google Scholar 

  177. Lam HM, Coschigano K, Oliveira IC, M-O R, Coruzzi G (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:569–593

    PubMed  CAS  Google Scholar 

  178. Lambertz C, Hemschemeier A, Happe T (2010) Anaerobic expression of the ferredoxin-encoding FDX5 gene of Chlamydomonas reinhardtii is regulated by the Crr1 transcription factor. Eukaryotic Cell 9:1747–1754

    PubMed  CAS  PubMed Central  Google Scholar 

  179. Lancien M, Gadal P, Hodges M (2000) Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation. Plant Physiol 123:817–824

    PubMed  CAS  PubMed Central  Google Scholar 

  180. Lane TW, Morel FM (2000) Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii. Plant Physiol 123:345–352

    PubMed  CAS  PubMed Central  Google Scholar 

  181. Lanquar V et al (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051

    PubMed  CAS  PubMed Central  Google Scholar 

  182. Lanquar V, Ramos MS, Lelièvre F, Barbier-Brygoo H, Krieger-Liszkay A, Krämer U, Thomine S (2010) Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol 152:1986–1999

    PubMed  CAS  PubMed Central  Google Scholar 

  183. Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906

    PubMed  CAS  Google Scholar 

  184. Larkum AWD (1968) Ionic relations of chloroplasts in vivo. Nature 218:447

    CAS  Google Scholar 

  185. Laudenbach DE, Reith ME, Straus NA (1988) Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bacteriol 170:258–265

    PubMed  CAS  PubMed Central  Google Scholar 

  186. Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol 97:1–13

    CAS  Google Scholar 

  187. Léon S, Touraine B, Ribot C, Briat JF, Lobréaux S (2003) Iron-sulphur cluster assembly in plants: distinct NFU proteins in mitochondria and plastids from Arabidopsis thaliana. Biochem J 371:823–830

    PubMed  PubMed Central  Google Scholar 

  188. Lewis NE, Marty NJ, Kathir KM, Rajalingam D, Kight AD, Daily A, Kumar TK, Henry RL, Goforth RL (2010) A dynamic cpSRP43-Albino3 interaction mediates translocase regulation of chloroplast signal recognition particle (cpSRP)-targeting components. J Biol Chem 285:34220–34230

    PubMed  CAS  PubMed Central  Google Scholar 

  189. Li L, Kaplan J (2004) A mitochondrial-vacuolar signaling pathway in yeast that affects iron and copper metabolism. J Biol Chem 279:33653–33661

    PubMed  CAS  Google Scholar 

  190. Li HH, Merchant S (1995) Degradation of plastocyanin in copper-deficient Chlamydomonas reinhardtii. J Biol Chem 270:23504–23510

    PubMed  CAS  Google Scholar 

  191. Li HM, Theg SM, Bauerle CM, Keegstra K (1990) Metal-ion-center assembly of ferredoxin and plastocyanin in isolated chloroplasts. Proc Natl Acad Sci U S A 87:6748–6752

    PubMed  CAS  PubMed Central  Google Scholar 

  192. Li L, Tutone AF, Drummond RS, Gardner RC, Luan S (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13:2761–2775

    PubMed  CAS  PubMed Central  Google Scholar 

  193. Li J, Wang DY, Li Q, Xu YJ, Cui KM, Zhu YX (2004) PPF1 inhibits programmed cell death in apical meristems of both G2 pea and transgenic Arabidopsis plants possibly by delaying cytosolic Ca2+ elevation. Cell Calcium 35:71–77

    PubMed  CAS  Google Scholar 

  194. Li L-G, Sokolov LN, Yang Y-H, Li D-P, Ting J, Pandy GK, Luan S (2008) A mitochondrial magnesium transporter functions in Arabidopsis pollen development. Mol Plant 1:675–685

    PubMed  CAS  Google Scholar 

  195. Lillo C (2008) Signalling cascades integrating light-enhanced nitrate metabolism. Biochem J 415:11–19

    PubMed  CAS  Google Scholar 

  196. Lindberg P, Melis A (2008) The chloroplast sulfate transport system in the green alga Chlamydomonas reinhardtii. Planta 228:951–961

    PubMed  CAS  Google Scholar 

  197. Linka M, Weber APM (2005) Shuffling ammonia between mitochondria and plastids during photorespiration. Trends Plant Sci 10:461–465

    PubMed  CAS  Google Scholar 

  198. Lommer M, Roy AS, Schilhabel M, Schreiber S, Rosenstiel P, LaRoche J (2010) Recent transfer of an iron-regulated gene from the plastid to the nuclear genome in an oceanic diatom adapted to chronic iron limitation. BMC genomics 11:718

    PubMed  CAS  PubMed Central  Google Scholar 

  199. Long JC, Sommer F, Allen MD, Lu SF, Merchant SS (2008) FER1 and FER2 encoding two ferritin complexes in Chlamydomonas reinhardtii chloroplasts are regulated by iron. Genetics 179:137–147

    PubMed  CAS  PubMed Central  Google Scholar 

  200. Lurin C, Geelen D, Barbier-Brygoo H, Guern J, Maurel C (1996) Cloning and functional expression of a plant voltage-dependent chloride channel. Plant Cell 8:701–711

    PubMed  CAS  PubMed Central  Google Scholar 

  201. Lutsenko S, Petris MJ (2003) Function and regulation of the mammalian copper-transporting ATPases: insights from biochemical and cell biological approaches. J Membr Biol 191:1–12

    PubMed  CAS  Google Scholar 

  202. Marcaida MJ, Schlarb-Ridley BG, Worrall JA, Wastl J, Evans TJ, Bendall DS, Luisi BF, Howe CJ (2006) Structure of cytochrome c6A, a novel dithio-cytochrome of Arabidopsis thaliana, and its reactivity with plastocyanin: implications for function. J Mol Biol 360:968–977

    PubMed  CAS  Google Scholar 

  203. Marchive C et al (2009) Abnormal physiological and molecular mutant phenotypes link chloroplast polynucleotide phosphorylase to the phosphorus deprivation response in Arabidopsis. Plant Physiol 151:905–924

    PubMed  CAS  PubMed Central  Google Scholar 

  204. Mariscal V, Rexach J, Fernández E, Galván A (2004) The plastidic nitrite transporter NAR1;1 improves nitrate use efficiency for growth in Chlamydomonas. Plant Cell Environ 27:1321–1328

    CAS  Google Scholar 

  205. Mariscal V, Moulin P, Orsel M, Miller AJ, Fernández E, Galván A (2006) Differential regulation of the Chlamydomonas Nar1 gene family by carbon and nitrogen. Protist 157:421–433

    PubMed  CAS  Google Scholar 

  206. Marmagne A et al (2007) Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and golgi membranes, respectively. J Exp Bot 58:3385–3393

    PubMed  CAS  Google Scholar 

  207. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London

    Google Scholar 

  208. Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic, London

    Google Scholar 

  209. Marten I, Deeken R, Hedrich R, Roelfsema MRG (2010) Light-induced modification of plant plasma membrane ion transport. Plant Biol (Stuttg) 12:64–79

    PubMed  CAS  Google Scholar 

  210. Mäser P et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    PubMed  PubMed Central  Google Scholar 

  211. Masuda T (2008) Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynth Res 96:121–143

    PubMed  CAS  Google Scholar 

  212. Matsushima R, Tang LY, Zhang L, Yamada H, Twell D, Sakamoto W (2011) A conserved, Mg2+-dependent exonuclease degrades organelle DNA during Arabidopsis pollen development. Plant Cell 23:1608–1624

    PubMed  CAS  PubMed Central  Google Scholar 

  213. Maury WJ, Huber SC, Moreland DE (1981) Effects of magnesium on intact chloroplasts: II. CATION SPECIFICITY AND INVOLVEMENT OF THE ENVELOPE ATPase IN (SODIUM) POTASSIUM/PROTON EXCHANGE ACROSS THE ENVELOPE. Plant Physiol 68:1257–1263

    PubMed  CAS  PubMed Central  Google Scholar 

  214. Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226:1075–1086

    PubMed  CAS  Google Scholar 

  215. Melis A, Chen H-C (2005) Chloroplast sulfate transport in green algae-genes, proteins and effects. Photosynth Res 86:299–307

    PubMed  CAS  Google Scholar 

  216. Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136

    PubMed  CAS  PubMed Central  Google Scholar 

  217. Merchant SS (2006) Trace metal utilization in chloroplasts. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Netherlands, pp 199–218

    Google Scholar 

  218. Merchant S, Bogorad L (1986) Regulation by copper of the expression of plastocyanin and cytochrome c552 in Chlamydomonas reinhardtii. Mol Cell Biol 6:462–469

    PubMed  CAS  PubMed Central  Google Scholar 

  219. Merchant S, Bogorad L (1987) Metal ion regulated gene expression: use of a plastocyanin-less mutant of Chlamydomonas reinhardtii to study the Cu(II)-dependent expression of cytochrome c-552. EMBO J 6:2531–2535

    PubMed  CAS  PubMed Central  Google Scholar 

  220. Merchant S, 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

    PubMed  CAS  Google Scholar 

  221. Mi F, Peters JS, Berkowitz GA (1994) Characterization of a chloroplast inner envelope K+ channel. Plant Physiol 105:955–964

    PubMed  CAS  PubMed Central  Google Scholar 

  222. Miller C (2006) ClC chloride channels viewed through a transporter lens. Nature 440:484

    PubMed  CAS  Google Scholar 

  223. Miller AF, Brudvig GW (1989) Manganese and calcium requirements for reconstitution of oxygen-evolution activity in manganese-depleted photosystem II membranes. Biochemistry 28:8181–8190

    PubMed  CAS  Google Scholar 

  224. Miqyass M, van Gorkom HJ, Yocum CF (2007) The PSII calcium site revisited. Photosynth Res 92:275–287

    PubMed  CAS  Google Scholar 

  225. Misson J et al (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A 102:11934–11939

    PubMed  CAS  PubMed Central  Google Scholar 

  226. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci U S A 98:2053–2058

    PubMed  CAS  PubMed Central  Google Scholar 

  227. Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A (2008) The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc Natl Acad Sci U S A 105:15184–15189

    PubMed  CAS  PubMed Central  Google Scholar 

  228. Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15:488–498

    PubMed  CAS  Google Scholar 

  229. Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervas M, Howe CJ, De La Rosa MA (2003) Photosynthesis: a new function for an old cytochrome? Nature 424:33–34

    PubMed  CAS  Google Scholar 

  230. Monachello D, Allot M, Oliva S, Krapp A, Daniel-Vedele F, Barbier-Brygoo H, Ephritikhine G (2009) Two anion transporters AtClCa and AtClCe fulfil interconnecting but not redundant roles in nitrate assimilation pathways. New Phytol 183:88–94

    PubMed  CAS  Google Scholar 

  231. Morales F, Abadía A, Abadía J (1991) Chlorophyll fluorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. Plant Physiol 97:886–893

    PubMed  CAS  PubMed Central  Google Scholar 

  232. Morales F, Cerovic ZG, Moya I (1994) Characterization of blue-green fluorescence in the mesophyll of sugar beet (Beta vulgaris L.) leaves affected by iron deficiency. Plant Physiol 106:127–133

    PubMed  CAS  PubMed Central  Google Scholar 

  233. Morcuende R et al (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    PubMed  CAS  Google Scholar 

  234. Moreno I, Norambuena L, Maturana D, Toro M, Vergara C, Orellana A, Zurita-Silva A, Ordenes VR (2008) AtHMA1 is a thapsigargin sensitive Ca2+/heavy metal pump. J Biol Chem 283:9633–9641

    PubMed  CAS  Google Scholar 

  235. Morrissey J, Baxter IR, Lee J, Li L, Lahner B, Grotz N, Kaplan J, Salt DE, Guerinot ML (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21:3326–3338

    PubMed  CAS  PubMed Central  Google Scholar 

  236. Moseley J, Quinn J, Eriksson M, Merchant S (2000) The Crd1 gene encodes a putative di-iron enzyme required for photosystem I accumulation in copper deficiency and hypoxia in Chlamydomonas reinhardtii. EMBO J 19:2139–2151.

    PubMed  CAS  PubMed Central  Google Scholar 

  237. Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21:6709–6720.

    PubMed  CAS  PubMed Central  Google Scholar 

  238. Moseley JL, Page MD, Alder NP, Eriksson M, Quinn J, Soto F, Theg SM, Hippler M, Merchant S (2002) Reciprocal expression of two candidate di-iron enzymes affecting photosystem I and light-harvesting complex accumulation. Plant Cell 14:673–688

    PubMed  CAS  PubMed Central  Google Scholar 

  239. Moseley JL, Chang C-W, Grossman AR (2006) Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot Cell 5:26–44

    PubMed  CAS  PubMed Central  Google Scholar 

  240. Moseley JL, González-Ballester D, Pootakham W, Bailey S, Grossman AR (2009) Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses. Genetics 181:889–905

    PubMed  CAS  PubMed Central  Google Scholar 

  241. Moulin M, McCormac AC, Terry MJ, Smith AG (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci U S A 105:15178–15183

    PubMed  CAS  PubMed Central  Google Scholar 

  242. Mourioux G, Douce R (1979) Transport du sulfate à travers la double membrane limitante, ou enveloppe, des chloroplastes d’épinard. Biochimie 61:1283–1292

    PubMed  CAS  Google Scholar 

  243. 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

    PubMed  CAS  Google Scholar 

  244. Muto S, Izawa S, Miyachi S (1982) Light-induced Ca2+ uptake by intact chloroplasts. FEBS Lett 139:250–254

    CAS  Google Scholar 

  245. Nakamura A, Fukuda A, Sakai S, Tanaka Y (2006) Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). Plant Cell Physiol 47:32–42

    PubMed  CAS  Google Scholar 

  246. Naumann B, Stauber EJ, Busch A, Sommer F, Hippler M (2005) N-terminal processing of Lhca3 Is a key step in remodeling of the photosystem I-light-harvesting complex under iron deficiency in Chlamydomonas reinhardtii. J Biol Chem 280:20431–20441

    PubMed  CAS  Google Scholar 

  247. Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, Kirchhoff H, Hippler M (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7:3964–3979

    PubMed  CAS  Google Scholar 

  248. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650

    PubMed  CAS  Google Scholar 

  249. Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318

    PubMed  CAS  PubMed Central  Google Scholar 

  250. Nilsson L, Müller R, Nielsen TH (2010) Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation. Physiol Plant 139:129–143

    PubMed  CAS  Google Scholar 

  251. Nishio JN, Abadía J, Terry N (1985) Chlorophyll-proteins and electron transport during iron nutrition-mediated chloroplast development. Plant Physiol 78:296–299

    PubMed  CAS  PubMed Central  Google Scholar 

  252. Nobel PS (1969) Light-induced changes in the ionic content of chloroplasts in Pisum sativum. Biochim Biophys Acta 172:134–143

    PubMed  CAS  Google Scholar 

  253. Nomura H, Komori T, Kobori M, Nakahira Y, Shiina T (2008) Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 53:988–998

    PubMed  CAS  Google Scholar 

  254. Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759

    PubMed  CAS  Google Scholar 

  255. Nouet C, Motte P, Hanikenne M (2011) Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci 16:395–404

    PubMed  CAS  Google Scholar 

  256. O’Halloran TV, Culotta VC (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275:25057–25060

    PubMed  Google Scholar 

  257. Ohnishi J-I, Kanai R (1987) Na+-induced uptake of pyruvate into mesophyll chloroplasts of a C4 plant, Panicum miliaceum. FEBS Lett 219:347–350

    CAS  Google Scholar 

  258. Ohnishi J, Kanai R (1990) Pyruvate uptake induced by a pH jump in mesophyll chloroplasts of maize and sorghum, NADP-malic enzyme type C4 species. FEBS Lett 269:122–124

    PubMed  CAS  Google Scholar 

  259. Padan E, Venturi M, Gerchman Y, Dover N (2001) Na+/H+ antiporters. Biochim Biophys Acta 1505:144–157

    PubMed  CAS  Google Scholar 

  260. Pádua M, Cavaco AM, Aubert S, Bligny R, Casimiro A (2010) Effects of copper on the photosynthesis of intact chloroplasts: interaction with manganese. Physiol Plant 138:301–311

    PubMed  Google Scholar 

  261. Page MD, Kropat J, Hamel PP, Merchant SS (2009) Two Chlamydomonas CTR copper transporters with a novel cys-met motif are localized to the plasma membrane and function in copper assimilation. Plant Cell 21:928–943

    PubMed  CAS  PubMed Central  Google Scholar 

  262. Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199

    PubMed  CAS  Google Scholar 

  263. Pätsikkä E, Kairavuo M, Šeršen F, Aro EM, Tyystjärvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367

    PubMed  PubMed Central  Google Scholar 

  264. Peltier JB, Ytterberg AJ, Sun Q, van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279:49367–49383

    PubMed  CAS  Google Scholar 

  265. Peters JS, Berkowitz GA (1991) Studies on the system regulating proton movement across the chloroplast envelope: effects of ATPase inhibitors, Mg, and an amine anesthetic on stromal pH and photosynthesis. Plant Physiol 95:1229–1236

    PubMed  CAS  PubMed Central  Google Scholar 

  266. Petroutsos D et al (2011) The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. Plant Cell 23:2950–2963

    PubMed  CAS  PubMed Central  Google Scholar 

  267. Pilon M, Cohu CM, Ravet K, Abdel-Ghany SE, Gaymard F (2009) Essential transition metal homeostasis in plants. Curr Opin Plant Biol 12:347–357

    PubMed  CAS  Google Scholar 

  268. Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim Biophys Acta 1807:989–998

    PubMed  CAS  Google Scholar 

  269. Pontier D, Albrieux C, Joyard J, Lagrange T, Block MA (2007) Knock-out of the magnesium protoporphyrin IX methyltransferase gene in Arabidopsis. J Biol Chem 282:2297–2304

    PubMed  CAS  PubMed Central  Google Scholar 

  270. Pottosin II (1992) Single channel recording in the chloroplast envelope. FEBS Lett 308:87–90

    PubMed  CAS  Google Scholar 

  271. Pottosin II, Schönknecht G (1996) Ion channel permeable for divalent and monovalent cations in native spinach thylakoid membranes. J Membr Biol 152:223–233

    PubMed  CAS  Google Scholar 

  272. Pottosin II, Muñiz J, Shabala S (2005) Fast-activating channel controls cation fluxes across the native chloroplast envelope. J Membr Biol 204:145–156

    PubMed  CAS  Google Scholar 

  273. Puig S et al (2007) Higher plants possess two different types of ATX1-like copper chaperones. Biochem Biophys Res Commun 354:385–390

    PubMed  CAS  Google Scholar 

  274. Quinn JM, Merchant S (1995) Two copper-responsive elements associated with the Chlamydomonas Cyc6 gene function as targets for transcriptional activators. Plant Cell 7:623–638

    PubMed  CAS  PubMed Central  Google Scholar 

  275. Quinn JM, Nakamoto SS, Merchant S (1999) Induction of coproporphyrinogen oxidase in Chlamydomonas chloroplasts occurs via transcriptional regulation of Cpx1 mediated by copper response elements and increased translation from a copper deficiency- specific form of the transcript. J Biol Chem 274:14444–14454

    PubMed  CAS  Google Scholar 

  276. Quinn JM, Barraco P, Eriksson M, Merchant S (2000) Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. J Biol Chem 275:6080–6089

    PubMed  CAS  Google Scholar 

  277. Randall PJ, Bouma D (1973) Zinc deficiency, carbonic anhydrase, and photosynthesis in leaves of spinach. Plant Physiol 52:229–232

    PubMed  CAS  PubMed Central  Google Scholar 

  278. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37

    PubMed  CAS  Google Scholar 

  279. Ravet K, Touraine B, Kim SA, Cellier F, Thomine S, Guerinot ML, Briat JF, Gaymard F (2009) Post-translational regulation of AtFER2 ferritin in response to intracellular iron trafficking during fruit development in Arabidopsis. Mol Plant 2:1095−1106

    Google Scholar 

  280. Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57:400–412

    PubMed  CAS  Google Scholar 

  281. Ravet K, Danford FL, Dihle A, Pittarello M, Pilon M (2011) Spatiotemporal analysis of copper homeostasis in Populus trichocarpa reveals an integrated molecular remodeling for a preferential allocation of copper to plastocyanin in the chloroplasts of developing leaves. Plant Physiol 157:1300–1312

    PubMed  CAS  PubMed Central  Google Scholar 

  282. Reddy VS, Ali GS, Reddy AS (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852

    PubMed  CAS  Google Scholar 

  283. Remacle C, Coosemans N, Jans F, Hanikenne M, Motte P, Cardol P (2010) Knock-down of the COX3 and COX17 gene expression of cytochrome c oxidase in the unicellular green alga Chlamydomonas reinhardtii. Plant Mol Biol 74:223–233

    PubMed  CAS  Google Scholar 

  284. Renné P, Dressen U, Hebbeker U, Hille D, Flügge UI, Westhoff P, Weber APM (2003) The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J 35:316–331

    PubMed  Google Scholar 

  285. Rexach J, Fernández E, Galván A (2000) The Chlamydomonas reinhardtii Nar1 gene encodes a chloroplast membrane protein involved in nitrite transport. Plant Cell 12:1441–1453

    PubMed  CAS  PubMed Central  Google Scholar 

  286. Richard CG (2003) Genes for magnesium transport. Curr Opin Plant Biol 6:263–267

    Google Scholar 

  287. Robinson NJ, Winge DR (2010) Copper metallochaperones. Annu Rev Biochem 79:537–562

    PubMed  CAS  PubMed Central  Google Scholar 

  288. Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol 188:317–327

    PubMed  CAS  PubMed Central  Google Scholar 

  289. Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160

    PubMed  Google Scholar 

  290. Roh MH, Shingles R, Cleveland MJ, McCarty RE (1998) Direct measurement of calcium transport across chloroplast inner-envelope vesicles. Plant Physiol 118:1447–1454

    PubMed  CAS  PubMed Central  Google Scholar 

  291. Rolland N, Ferro M, Seigneurin-Berny D, Garin J, Douce R, Joyard J (2003) Proteomics of chloroplast envelope membranes. Photosynth Res 78:205–230

    PubMed  CAS  Google Scholar 

  292. Roth C, Menzel G, Petetot JM, Rochat-Hacker S, Poirier Y (2004) Characterization of a protein of the plastid inner envelope having homology to animal inorganic phosphate, chloride and organic-anion transporters. Planta 218:406–416

    PubMed  CAS  Google Scholar 

  293. Rouached H, Secco D, Arpat B, Poirier Y (2011) The transcription factor PHR1 plays a key role in the regulation of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biol 11:19

    PubMed  CAS  PubMed Central  Google Scholar 

  294. Ruiz-Pavón L, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C (2008) Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: functional characterization in Escherichia coli. J Biol Chem 283:13520–13527

    Google Scholar 

  295. Rumak I, Gieczewska K, Kierdaszuk B, Gruszecki WI, Mostowska A, Mazur R, Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) magnesium ion treatment. Relationship between thylakoid membrane arrangement and stacking. Biochim Biophys Acta 1797:1736–1748

    PubMed  CAS  Google Scholar 

  296. Sagardoy R, Vazquez S, Florez-Sarasa ID, Albacete A, Ribas-Carbo M, Flexas J, Abadia J, Morales F (2010) Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol 187:145–158

    PubMed  CAS  Google Scholar 

  297. Sagasti S, Yruela I, Bernal M, Lujan MA, Frago S, Medina M, Picorel R (2011) Characterization of the recombinant copper chaperone (CCS) from the plant Glycine (G. ) max. Metallomics 3:169–175

    PubMed  CAS  Google Scholar 

  298. Sai J, Johnson CH (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14:1279–1291

    PubMed  CAS  PubMed Central  Google Scholar 

  299. Saito A, Lino T, Sonoike K, Miwa E, Higuchi K (2010) Remodeling of the major light-harvesting antenna protein of PSII protects the young leaves of barley (Hordeum vulgare L.) from photoinhibition under prolonged iron deficiency. Plant Cell Physiol 51:2013–2030

    PubMed  CAS  Google Scholar 

  300. Sánchez-Calderón L, Chacon-López A, Pérez-Torres C-A, Herrera-Estrella L (2010) Phosphorus: plant strategies to cope with its scarcity. In: Hell R, Mendel R-R (eds) Cell biology of metals and nutrients. Springer, Berlin, pp 173–198

    Google Scholar 

  301. Sandstrom S, Park YI, Oquist G, Gustafsson P (2001) CP43’, the isiA gene product, functions as an excitation energy dissipater in the cyanobacterium Synechococcus sp. PCC 7942. Photochem Photobiol 74:431–437

    PubMed  CAS  Google Scholar 

  302. Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wirén N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540

    PubMed  CAS  Google Scholar 

  303. Scheible W-R et al (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499

    PubMed  CAS  PubMed Central  Google Scholar 

  304. Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flügge U-I, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131:16–26

    PubMed  CAS  PubMed Central  Google Scholar 

  305. Seigneurin-Berny D et al (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892

    PubMed  CAS  Google Scholar 

  306. Shabala S (2003) Regulation of potassium transport in leaves: from molecular to tissue level. Ann Bot 92:627–634

    PubMed  CAS  Google Scholar 

  307. Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309–323

    PubMed  CAS  Google Scholar 

  308. Shcolnick S, Keren N (2006) Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus. Plant Physiol 141:805–810

    PubMed  CAS  PubMed Central  Google Scholar 

  309. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci U S A 97:6896–6901

    PubMed  CAS  PubMed Central  Google Scholar 

  310. Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85

    PubMed  CAS  Google Scholar 

  311. Shi H, Bencze KZ, Stemmler TL, Philpott CC (2008) A cytosolic iron chaperone that delivers iron to ferritin. Science 320:1207–1210

    PubMed  CAS  PubMed Central  Google Scholar 

  312. Shikanai T, Muller-Moule 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

    PubMed  CAS  PubMed Central  Google Scholar 

  313. Shimoni-Shor E, Hassidim M, Yuval-Naeh N, Keren N (2010) Disruption of Nap14, a plastid-localized non-intrinsic ABC protein in Arabidopsis thaliana results in the over-accumulation of transition metals and in aberrant chloroplast structures. Plant Cell Environ 33:1029–1038

    PubMed  CAS  Google Scholar 

  314. Shingles R, Roh MH, McCarty RE (1996) Nitrite transport in chloroplast inner envelope vesicles. 1. Direct measurement of proton-linked transport. Plant Physiol 112:1375–1381

    PubMed  CAS  PubMed Central  Google Scholar 

  315. Shingles R, North M, McCarty RE (2001) Direct measurement of ferrous ion transport across membranes using a sensitive fluorometric assay. Anal Biochem 296:106–113

    PubMed  CAS  Google Scholar 

  316. Shingles R, North M, McCarty RE (2002) Ferrous ion transport across chloroplast inner envelope membranes. Plant Physiol 128:1022–1030

    PubMed  CAS  PubMed Central  Google Scholar 

  317. Shingles R, Wimmers LE, McCarty RE (2004) Copper transport across pea thylakoid membranes. Plant Physiol 135:145–151

    PubMed  CAS  PubMed Central  Google Scholar 

  318. Song C-P, Guo Y, Qiu Q, Lambert G, Galbraith DW, Jagendorf A, Zhu J-K (2004) A probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 101:10211–10216

    PubMed  CAS  PubMed Central  Google Scholar 

  319. Spiller S, Terry N (1980) Limiting factors in photosynthesis: II. IRON STRESS DIMINISHES PHOTOCHEMICAL CAPACITY BY REDUCING THE NUMBER OF PHOTOSYNTHETIC UNITS. Plant Physiol 65:121–125

    PubMed  CAS  PubMed Central  Google Scholar 

  320. Stiller J (2007) Plastid endosymbiosis, genome evolution and the origin of green plants. Trends Plant Sci 12:391–396

    PubMed  CAS  Google Scholar 

  321. Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83

    PubMed  CAS  Google Scholar 

  322. Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692

    PubMed  CAS  Google Scholar 

  323. Sugiura M, Georgescu MN, Takahashi M (2007) A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant Cell Physiol 48:1022–1035

    PubMed  CAS  Google Scholar 

  324. Sun Q, Zybailov B, Majeran W, Friso G, Olinares PDB, van Wijk KJ (2009) PPDB, the plant proteomics database at Cornell. Nucl Acids Res 37:D969–D974

    PubMed  CAS  PubMed Central  Google Scholar 

  325. Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, Coupland G (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9:717–730

    PubMed  CAS  PubMed Central  Google Scholar 

  326. Suorsa M, Aro EM (2007) Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosynth Res 93:89–100

    PubMed  CAS  Google Scholar 

  327. Surek B, Kreimer G, Melkonian M, Latzko E (1987) Spinach ferredoxin is a calcium-binding protein. Planta 171:565–568

    PubMed  CAS  Google Scholar 

  328. Taira M, Valtersson U, Burkhardt B, Ludwig RA (2004) Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 16:2048–2058

    PubMed  CAS  PubMed Central  Google Scholar 

  329. Takahashi H, Asanuma W, Saito K (1999) Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform. J Exp Bot 50:1713–1714

    CAS  Google Scholar 

  330. Tanaka R, Kobayashi K, Masuda T (2011) Tetrapyrrole metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0145

    PubMed  PubMed Central  Google Scholar 

  331. Taniguchi M, Taniguchi Y, Kawasaki M, Takeda S, Kato T, Sato S, Tabata S, Miyake H, Sugiyama T (2002) Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana. Plant Cell Physiol 43:706–717

    PubMed  CAS  Google Scholar 

  332. Tapken W, Ravet K, Pilon M (2012) Plastocyanin controls the stabilization of the thylakoid Cu-transporting P-type ATPase PAA2/HMA8 in response to low copper in Arabidopsis. J Biol Chem 287:18544–18550

    PubMed  CAS  PubMed Central  Google Scholar 

  333. Tarantino D, Casagrande F, Soave C, Murgia I (2010) Knocking out of the mitochondrial AtFer4 ferritin does not alter response of Arabidopsis plants to abiotic stresses. J Plant Physiol 167:453–460

    PubMed  CAS  Google Scholar 

  334. Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9:1514–1532

    PubMed  CAS  PubMed Central  Google Scholar 

  335. Terry N, Abadia J (1986) Function of iron in chloroplasts. J Plant Nutr 9:609–646

    CAS  Google Scholar 

  336. Tester M, Blatt MR (1989) Direct measurement of K+ channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. Plant Physiol 91:249–252

    PubMed  CAS  PubMed Central  Google Scholar 

  337. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    PubMed  CAS  Google Scholar 

  338. Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci U S A 97:4991–4996

    PubMed  CAS  PubMed Central  Google Scholar 

  339. Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    PubMed  CAS  Google Scholar 

  340. Timperio AM, D’Amici GM, Barta C, Loreto F, Zolla L (2007) Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J Exp Bot 58:3695–3710

    PubMed  CAS  Google Scholar 

  341. Tottey S, Rich PR, Rondet SAM, Robinson NJ (2001) Two menkes-type ATPases supply copper for photosynthesis in Synechocystis sp. 6803. J Biol Chem 276:19999–20004

    PubMed  CAS  Google Scholar 

  342. Tottey S, Rondet SAM, Borrelly GPM, 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. J Biol Chem 277:5490–5497

    PubMed  Google Scholar 

  343. Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, Merchant S, Jensen PE (2003) Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci U S A 100:16119–16124

    PubMed  CAS  PubMed Central  Google Scholar 

  344. Touraine B, Boutin JP, Marion-Poll A, Briat JF, Peltier G, Lobréaux S (2004) Nfu2: a scaffold protein required for [4Fe-4S] and ferredoxin iron-sulphur cluster assembly in Arabidopsis chloroplasts. Plant J 40:101–111

    PubMed  CAS  Google Scholar 

  345. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 58:2290–2300

    Google Scholar 

  346. Tsunekawa K et al (2009) Identification and characterization of the Na+/H+ antiporter Nhas3 from the thylakoid membrane of Synechocystis sp. PCC 6803. J Biol Chem 284:16513–16521

    PubMed  CAS  PubMed Central  Google Scholar 

  347. Turner WL, Waller JC, Vanderbeld B, Snedden WA (2004) Cloning and characterization of two NAD kinases from Arabidopsis. Identification of a calmodulin binding isoform. Plant Physiol 135:1243–1255

    PubMed  CAS  PubMed Central  Google Scholar 

  348. Versaw WK, Harrison MJ (2002) A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14:1751–1766

    PubMed  CAS  PubMed Central  Google Scholar 

  349. Vidal EA, Gutiérrez RA (2008) A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol 11:521–529

    PubMed  CAS  Google Scholar 

  350. Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K (2006) Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J 48:296–306

    PubMed  CAS  Google Scholar 

  351. von der Fecht-Bartenbach J, Bogner M, Krebs M, Stierhof YD, Schumacher K, Ludewig U (2007) Function of the anion transporter AtCLC-d in the trans-Golgi network. Plant J 50:466–474

    PubMed  CAS  PubMed Central  Google Scholar 

  352. Voß B, Meinecke L, Kurz T, Al-Babili S, Beck CF, Hess WR (2011) Hemin and magnesium-protoporphyrin IX induce global changes in gene expression in Chlamydomonas reinhardtii. Plant Physiol 155:892–905

    PubMed  PubMed Central  Google Scholar 

  353. Vothknecht UC, Soll J (2005) Chloroplast membrane transport: interplay of prokaryotic and eukaryotic traits. Gene 354:99–109

    PubMed  CAS  Google Scholar 

  354. Wagner R, Aigner H, Funk C (2011) FtsH proteases located in the plant chloroplast. Physiol Plant 145:203–214

    Google Scholar 

  355. Waller JC, Dhanoa PK, Schumann U, Mullen RT, Snedden WA (2010) Subcellular and tissue localization of NAD kinases from Arabidopsis: compartmentalization of de novo NADP biosynthesis. Planta 231:305–317

    PubMed  CAS  Google Scholar 

  356. Wang X, Berkowitz GA, Peters JS (1993) K+-conducting ion channel of the chloroplast inner envelope: functional reconstitution into liposomes. Proc Natl Acad Sci U S A 90:4981–4985

    PubMed  CAS  PubMed Central  Google Scholar 

  357. Wang D, Xu Y, Li Q, Hao X, Cui K, Sun F, Zhu Y (2003) Transgenic expression of a putative calcium transporter affects the time of Arabidopsis flowering. Plant J 33:285–292

    PubMed  CAS  Google Scholar 

  358. Wang WH et al (2012) Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J Exp Bot 63:177–190

    PubMed  CAS  PubMed Central  Google Scholar 

  359. Weber A, Flügge UI (2002) Interaction of cytosolic and plastidic nitrogen metabolism in plants. J Exp Bot 53:865–874

    PubMed  CAS  Google Scholar 

  360. Weber APM, 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

    PubMed  CAS  Google Scholar 

  361. Weber A, Menzlaff E, Arbinger B, Gutensohn M, Eckerskorn C, Flügge UI (1995) The 2-oxoglutarate/malate translocator of chloroplast envelope membranes: molecular cloning of a transporter containing a 12-helix motif and expression of the functional protein in yeast cells. Biochemistry 34:2621–2627

    PubMed  CAS  Google Scholar 

  362. Weber APM, Schwacke R, Flügge U-I (2005) Solute transporters of the plastid envelope membrane. Annu Rev Plant Biol 56:133–164

    PubMed  Google Scholar 

  363. Wegner SV, Sun F, Hernandez N, He C (2011) The tightly regulated copper window in yeast. Chem Commun 47:2571–2573

    CAS  Google Scholar 

  364. 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 278:31286–31289

    PubMed  CAS  Google Scholar 

  365. Weinl S, Held K, Schlucking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–686

    PubMed  CAS  Google Scholar 

  366. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets-iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84

    PubMed  CAS  Google Scholar 

  367. Whiteman S-A, Serazetdinova L, Jones AME, Sanders D, Rathjen J, Peck SC, Maathuis FJM (2008) Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Proteomics 8:3536–3547

    PubMed  CAS  Google Scholar 

  368. Williams LE, Mills RF (2005) P(1B)-ATPases-an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502

    PubMed  CAS  Google Scholar 

  369. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    PubMed  CAS  Google Scholar 

  370. Wu W, Berkowitz GA (1991) Lidocaine and ATPase inhibitor interaction with the chloroplast envelope. Plant Physiol 97:1551–1557

    PubMed  CAS  PubMed Central  Google Scholar 

  371. Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260–1271

    PubMed  CAS  PubMed Central  Google Scholar 

  372. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139

    PubMed  CAS  PubMed Central  Google Scholar 

  373. Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci U S A 96:15336–15341

    PubMed  CAS  PubMed Central  Google Scholar 

  374. Xu XM, Møller SG (2011) Iron-sulfur clusters: biogenesis, molecular mechanisms and their functional significance. Antioxid Redox Signal 15:271–307

    PubMed  Google Scholar 

  375. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    PubMed  CAS  Google Scholar 

  376. Yamagishi A, Satoh K, Katoh S (1981) The concentrations and thermodynamic activities of cations in intact Bryopsis chloroplasts. Biochim Biophys Acta 637:252–263

    CAS  Google Scholar 

  377. 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  379. Yang T, Poovaiah BW (2000) Arabidopsis chloroplast chaperonin 10 is a calmodulin-binding protein. Biochem Biophys Res Commun 275:601–607

    PubMed  CAS  Google Scholar 

  380. Yanykin DV, Khorobrykh AA, Khorobrykh SA, Klimov VV (2010) Photoconsumption of molecular oxygen on both donor and acceptor sides of photosystem II in Mn-depleted subchloroplast membrane fragments. Biochim Biophys Acta 1797:516–523

    PubMed  CAS  Google Scholar 

  381. Yehudai-Resheff S, Zimmer SL, Komine Y, Stern DB (2007) Integration of chloroplast nucleic acid metabolism into the phosphate deprivation response in Chlamydomonas reinhardtii. Plant Cell 19:1023–1038

    PubMed  CAS  PubMed Central  Google Scholar 

  382. Yuan L, Loqué D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wirén N (2007) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19:2636–2652

    PubMed  CAS  PubMed Central  Google Scholar 

  383. Zancani M et al (2004) Evidence for the presence of ferritin in plant mitochondria. Eur J Biochem 271:3657–3664

    PubMed  CAS  Google Scholar 

  384. Zanetti M et al (2010) A novel potassium channel in photosynthetic cyanobacteria. PLoS ONE 5:e10118

    PubMed  PubMed Central  Google Scholar 

  385. Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348

    PubMed  CAS  PubMed Central  Google Scholar 

  386. Zhong L, Inesi G (1998) Role of the S3 stalk segment in the thapsigargin concentration dependence of sarco-endoplasmic reticulum Ca2+ ATPase inhibition. J Biol Chem 273:12994–12998

    PubMed  CAS  Google Scholar 

  387. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    PubMed  CAS  Google Scholar 

  388. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    PubMed  CAS  Google Scholar 

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Acknowledgments

Research in the M.H.’s laboratory is supported by the “Fonds de la Recherche Scientifique—FNRS” (grant nos. 2.4638.05, 2.4540.06, 2.4583.08 and 2.4581.10) and the “Fonds Spéciaux du Conseil de la Recherche” from the University of Liège. M.H. is a Research Associate of the FNRS. M.B. acknowledges the support of the CSIC JAE-DOC Program and Juan de la Cierva Program of the Spanish Ministry of Science and Innovation. M.B. research is supported by a grant from MCINN (AGL2011-23574) and a grant for young scientist from ARAID. The work of E.I.U. at UCLA is funded by the Division of Chemical Sciences, Geosciences and Biosciences, Office of Basic Energy Sciences of the US Department of Energy (DE-FD02-04ER15529).

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Authors and Affiliations

  1. Functional Genomics and Plant Molecular Imaging, Center for Protein Engineering (CIP), PhytoSystems, B22, Department of Life Sciences, University of Liège, Bld du Rectorat, 27, Sart Tilman, 4000, Liège, Belgium

    Marc Hanikenne

  2. Plant Nutrition Department, Estación Experimental De Aula Dei, Consejo Superior de Investigaciones Científicas (CSIC), Avda. Montañana 1005, 50059, Zaragoza, Spain

    María Bernal

  3. Department of Chemistry and Biochemistry, UCLA, Los Angeles, 90095, CA, USA

    Eugen-Ioan Urzica

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  1. Marc Hanikenne
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  2. María Bernal
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  3. Eugen-Ioan Urzica
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Correspondence to Marc Hanikenne .

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  1. Department of Plant Biology, Univeristy of California-Davis, Davis, California, USA

    Steven M. Theg

  2. Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, Paris, France

    Francis-André Wollman

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Hanikenne, M., Bernal, M., Urzica, EI. (2014). Ion homeostasis in the Chloroplast. In: Theg, S., Wollman, FA. (eds) Plastid Biology. Advances in Plant Biology, vol 5. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1136-3_17

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