The zinc homeostasis network of land plants

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 9, 2012, Pages 1553-1567

  Sinclair, Scott Aleksander ^a   Krämer, Ute ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Arabidopsis; Fe; Hyperaccumulator plant; Metal; Metal regulation; Zn

Indexed keywords

CATION; IRON; IRON REGULATED TRANSPORTER 1; IRON REGULATORY FACTOR; UNCLASSIFIED DRUG; ZINC;

ARABIDOPSIS; CHEMICAL INTERACTION; CONSERVATION BIOLOGY; HOMEOSTASIS; NONHUMAN; PHYTOCHEMISTRY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; AZETIDINECARBOXYLIC ACID; CATION TRANSPORT PROTEINS; CATIONS, DIVALENT; EMBRYOPHYTA; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; ION TRANSPORT; IRON; PLANT ROOTS; SIGNAL TRANSDUCTION; SOIL; ZINC;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; EUKARYOTA;

EID: 84864309066     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.05.016     Document Type: Review

References (185)

1. Maret W. Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals. Biometals Jan. 2009, 22(1):149-157.
2. Sriram K., Lonchyna V.A. Micronutrient supplementation in adult nutrition therapy: practical considerations. JPEN J. Parenter. Enteral. Nutr. Aug. 2009, 33(5):548-562.
3. Andreini C., Bertini I. Metalloproteomes: a bioinformatic approach. Acc. Chem. Res. 2009, 42(10):1471-14711479.
4. Fraústo da Silva J.J.R., Williams R.J.P. The Biological Chemistry of The Elements 1991, Clarendon Press, Oxford, UK.
5. Lane T.W., Morel F.M. A biological function for cadmium in marine diatoms. Proc. Natl. Acad. Sci. U. S. A. Apr. 2000, 97(9):4627-4631.
6. WHO Comparative Quantification of Health Risks: Global and Regional Burden of Diseases Attributable to Selected Major Risk Factors 2005, vol. 1-3. Organizacion Mundial de la Salud.
7. Hambidge K.M., Miller L.V., Westcott J.E., Sheng X., Krebs N.F. Zinc bioavailability and homeostasis. Am. J. Clin. Nutr. Apr. 2010, 91(5):1478S-1483S.
8. Fan M., Zhao F., Fairweather-Tait S., Poulton P., Dunham S., McGrath S. Evidence of decreasing mineral density in wheat grain over the last 160 years. J. Trace Elem. Med. Biol. Nov. 2008, 22(4):315-324.
9. Palmgren M.G., Clemens S., Williams L.E., Krämer U., Borg S., Schjørring J.K., Sanders D. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. Sep. 2008, 13(9):464-473.
10. Lee I., Seo Y., Coltrane D., Hwang S., Oh T., Marcotte E., Ronald P. Genetic dissection of the biotic stress response using a genome-scale gene network for rice. PNAS Oct. 2011, 108:18548-18553.
11. Johnson A.A.T., Kyriacou B., Callahan D.L., Carruthers L., Stangoulis J., Lombi E., Tester M. Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLoS One 2011, 6(9):e24476.
12. Alloway B.J. Soil factors associated with zinc deficiency in crops and humans. Environ. Geochem. Health Mar. 2009, 31(5):537-548.
13. Cakmak I. Enrichment of cereal grains with zinc: agronomic or genetic biofortification?. Plant Soil Nov. 2007, 302(1):1-17.
14. Hacisalihoglu G., Hart J., Wang Y., Cakmak I., Kochian L. Zinc efficiency is correlated with enhanced expression and activity of zinc-requiring enzymes in wheat. Plant Physiol. Jan. 2003, 131(2):595-602.
15. Marschner H. Mineral Nutrition of higher plants 1995, Academic Press.
16. Cousins R.J. Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. Jun. 2006, 281(34):24085-24089.
17. Eide D.J. Homeostatic and adaptive responses to zinc deficiency in Saccharomyces cerevisiae. J. Biol. Chem. Jul. 2009, 284(28):18565-18569.
18. Sinclair S.A., Sherson S.M., Jarvis R., Camakaris J., Cobbett C.S. The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytol. Mar. 2007, 174(1):39-45.
19. 2+ with genetically encoded sensors. PNAS Apr. 2011, (108):7351-7356.
20. Vinkenborg J.L., Koay M.S., Merkx M. Fluorescent imaging of transition metal homeostasis using genetically encoded sensors. Curr. Opin. Chem. Biol. Apr. 2010, 14(2):231-237.
21. Lichten L.A., Cousins R.J. Mammalian zinc transporters: nutritional and physiologic regulation. Annu. Rev. Nutr. Aug. 2009, 29(1):153-176.
22. Eide D.J. Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta (BBA) - Mol. Cell Res. Jul. 2006, 1763(7):711-722.
23. MacDiarmid C.W., Milanick M.A., Eide D.J. Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock. J. Biol. Chem. Apr. 2003, 278(17):15065-15072.
24. Gaither L., Eide D. Eukaryotic zinc transporters and their regulation. Biometals 2001, 14(3):251-270.
25. Arrivault S., Senger T., Krämer U. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J. Jun. 2006, 46(5):861-879.
26. Hussain D., Haydon M., Sherson S., Jarvis R., Camakaris J., Cobbett C.S. P-Type ATPase heavy metal transporters with roles in essential zinc homeostasis in arabidopsis. Plant Cell May 2004, 16(5):1327-1339.
27. Cakmak I. Tansley review No. 111 - possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 2000, 146(2):185-205.
28. Verbruggen N., Hermans C., Schat H. Molecular mechanisms of metal hyperaccumulation in plants. New Phytol. Mar. 2009, 181(4):759-776.
29. Krämer U. Metal hyperaccumulation in plants. Annu. Rev. Plant Biol. 2010, 61:517-534.
30. Krämer U., Talke I.N., Hanikenne M. Transition metal transport. FEBS Lett. May 2007, 581(12):2263-2272.
31. Clemens S., Palmgren M., Kraemer U. A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 2002, 7(7):309-315.
32. von Wirén N., Marschner H., Romheld V. Roots of iron-efficient maize also absorb phytosiderophore-chelated zinc. Plant Physiol. Aug. 1996, 111(4):1119-1125.
33. Freisinger E. Plant MTs-long neglected members of the metallothionein superfamily. Dalton Trans. 2008, (47):6663.
34. Ren Y., Liu Y., Chen H., Li G., Zhang X., Zhao J. Type 4 metallothionein genes are involved in regulating Zn ion accumulation in late embryo and in controlling early seedling growth in Arabidopsis. Plant Cell Environ. Oct. 2011, 35(4):770-789.
35. Klatte M., Schuler M., Wirtz M., Fink-Straube C., Hell R., Bauer P. The analysis of Arabidopsis Nicotianamine Synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol. May 2009, 150(1):257-271.
36. Haydon M.J., Kawachi M., Wirtz M., Stefan H., Hell R., Krämer U. Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell Feb. 2012, 24:724-737.
37. Deinlein U., Weber M., Schmidt H., Rensch S., Trampczynska A., Hansen T.H., Husted S., Schjoerring J.K., Talke I.N., Krämer U., Clemens S. Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in Zn hyperaccumulation. Plant Cell Feb. 2012, 24:708-723.
38. Song W.Y., Choi K.S., Kim D.Y., Geisler M., Park J., Vincenzetti V., Schellenberg M., Kim S.H., Lim Y.P., Noh E.W., Lee Y., Martinoia E. Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. Plant Cell Aug. 2010, 22(7):2237-2252.
39. Hanikenne M., Talke I.N., Haydon M.J., Lanz C., Nolte A., Motte P., Kroymann J., Weigel D., Krämer U. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature Apr. 2008, 453(7193):391-395.
40. Küpper H., Lombi E., Zhao F., McGrath S. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 2000, 212(1):75-84.
41. Erenoglu E.B., Kutman U.B., Ceylan Y., Yildiz B., Cakmak I. Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat. New Phytol. Oct. 2010, 189(2):438-448.
42. van Bel A.J.E., Furch A.C.U., Hafke J.B., Knoblauch M., Patrick J.W. (Questions)n on phloem biology. 2. Mass flow, molecular hopping, distribution patterns and macromolecular signalling. Plant Sci. Oct. 2011, 181(4):325-330.
43. Turgeon R., Shmuel S. Phloem transport: cellular pathways and molecular trafficking. Annu. Rev. Plant Biol. 2009, 60:207-221.
44. Heazlewood J.L., Tonti-Filippini J.S., Gout A.M., Day D.A., Whelan J., Millar A.H. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell Online Jan. 2004, 16(1):241-256.
45. Kleffmann T., Russenberger D., von Zychlinski A., Christopher W., Sjölander K., Gruissem W., Baginsky S. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. Mar. 2004, 14(5):354-362.
46. Eide D.J. The molecular biology of metal ion transport in Saccharomyces cerevisiae. Annu. Rev. Nutr. 1998, 18:441-469.
47. Krämer U., Clemens S. Chapter 9: functions and homeostasis of zinc, copper, and nickel in plants. Topics in Current Genetics 2006, vol. 14:216-271. Springer-Verlag, Berlin/Heidelberg. M.J. Tamas, E. Martinoia (Eds.).
48. Haas C.E., Rodionov D.A., Kropat J., Malasarn D., Merchant S.S., de Crécy-Lagard V. A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genomics 2009, 10(1):470.
49. Krämer U., Cotter-Howells J.D., Charnock J.M., Baker A.J.M., Smith J.A.C. Free histidine as a metal chelator in plants that accumulate nickel. Nature Feb. 1996, 379(6566):635-638.
50. Salt D.E., Prince R.C., Baker A.J.M., Raskin I., Pickering I.J. Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ. Sci. Technol. Mar. 1999, 33(5):713-717.
51. Stephan U.W., Scholz G., Rudolph A. Distribution of nicotianamine, a presumed symplast iron transporter, in different organs of sunflower and of a tomato wild type and its mutant chloronerva. Biochem. Physiol. Pflanzen 1989, 186(2):81-88.
52. Trampczynska A., Böttcher C., Clemens S. The transition metal chelator nicotianamine is synthesized by filamentous fungi. FEBS Lett. May 2006, 580(13):3173-3178.
53. Haydon M.J., Cobbett C.S. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol. Feb. 2007, 143(4):1705-1719.
54. Tennstedt P., Peisker D., Bottcher C., Trampczynska A., Clemens S. Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol. Dec. 2008, 149(2):938-948.
55. Shanmugam V., Lo J.-C., Wu C.-L., Wang S.-L., Lai C.-C., Connolly E.L., Huang J.-L., Yeh K.-C. Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana - the role in zinc tolerance. New Phytol. Jan. 2011, 190(1):125-137.
56. Mathys W. The role of malate, oxalate, and mustard oil glucosides in the evolution of zinc resistance in herbage plants. Physiol. Plant. 1977, 40:130-136.
57. Harmens H., Den Hartog P., Ten Bookum W., Verkleij J. lncreased zinc tolerance in Silene vulgaris (Moench) Garcke is not due to lncreased production of phytochelatins. Plant Physiol. Mar. 1993, 103:1305-1309.
58. Sarret G., Samitou-Laprade P., Bert V., Proux O., Hazemann J.L., Traverse A., Marcus M.A., Manceau A. Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol. Nov. 2002, 130(4):1815-1826.
59. Haydon M.J., Cobbett C.S. Transporters of ligands for essential metal ions in plants. New Phytol. May 2007, 174(3):499-506.
60. Castaldi P., Lauro G., Senette C., Deiana S. Role of the Ca-pectates on the accumulation of heavy metals in the root apoplasm. Plant Physiol. Biochem. Dec. 2010, 48(12):1008-1014.
61. Bloss T., Clemens S., Nies D. Characterization of the ZAT1p zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta Mar. 2002, 214(5):783-791.
62. Schaaf G., Ludewig U., Erenoglu B.E., Mori S., Kitahara T., von Wirén N. ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J. Biol. Chem. Jan. 2004, 279(10):9091-9096.
63. Grotz N., Fox T., Connolly E., Park W., Guerinot M., Eide D. Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(12):7220-7224.
64. van der Zaal B., Neuteboom L., Pinas J., Chardonnens A., Schat H., Jac V., Hooykaas P. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. Feb. 1999, 119:11047-11041055.
65. Belouchi A., Cellier M., Kwan T., Saini H.S., Leroux G., Gros P. The macrophage-specific membrane protein Nramp controlling natural resistance to infections in mice has homologues expressed in the root system of plants. Plant Mol. Biol. Dec. 1995, 29(6):1181-1196.
66. Thomine S., Wang R., Ward J.M., Crawford N.M., Schroeder J.I. 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. Apr. 2000, 97(9):4991-4996.
67. Curie C., Panaviene Z., Loulergue C., Dellaporta S.L., Briat J.F., Walker E.L. Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature Jan. 2001, 409(6818):346-349.
68. Cobbett C.S., Hussain D., Haydon M.J. Structural and functional relationships between type 1B heavy metal-transporting P-type ATPases in Arabidopsis. New Phytol. Aug. 2003, 159(2):315-321.
69. Song W., Martinoia E., Lee J., Kim D., Kim D., Vogt E., Shim D., Choi K., Hwang I., Lee Y. A novel family of cys-rich membrane proteins mediates cadmium resistance in Arabidopsis. Plant Physiol. Jun. 2004, 135(2):1027-1039.
70. Wang K., Zhou B., Kuo Y.M., Zemansky J. A novel member of a zinc transporter family is defective in acrodermatitis enteropathica. Am. J. Hum. Genet. 2002, 71:66-73.
71. Colangelo E.P., Guerinot M.L. Put the metal to the petal: metal uptake and transport throughout plants. Curr. Opin. Plant Biol. Jun. 2006, 9(3):322-330.
72. Vert G. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell Jun. 2002, 14(6):1223-1233.
73. Varotto C., Maiwald D., Pesaresi P., Jahns P., Salamini F., Leister D. The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J. Sep. 2002, 31(5):589-599.
74. Henriques R., Jasik J., Klein M., Martinoia E., Feller U., Schell J., Pais M., Koncz C. Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol. Biol. 2002, 50(4):587-597.
75. Robinson N.J., Procter C.M., Connolly E.L., Guerinot M.L. A ferric-chelate reductase for iron uptake from soils. Nature Feb. 1999, 397(6721):694-697.
76. Connolly E.L. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell Jun. 2002, 14(6):1347-1357.
77. Kerkeb L., Mukherjee I., Chatterjee I., Lahner B., Salt D.E., Connolly E.L. Iron-induced turnover of the Arabidopsis IRON-regulated transporter1 metal transporter requires lysine residues. Plant Physiol. Apr. 2008, 146(4):1964-1973.
78. Barberon M., Zelazny E., Robert S., Conéjéro G., Curie C., Friml J., Vert G. Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl. Acad. Sci. Aug. 2011, 108(32):E450-E458.
79. Gitan R.S., Eide D.J. Zinc-regulated ubiquitin conjugation signals endocytosis of the yeast ZRT1 zinc transporter. Biochem. J. Mar. 2000, 346:329-336.
80. Vert G.A. Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol. May 2003, 132(2):796-804.
81. Becher M., Talke I.N., Krall L., Krämer U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. Dec. 2003, 37(2):251-268.
82. Fukao Y., Ferjani A., Tomioka R., Nagasaki N., Kurata R., Nishimori Y., Fujiwara M., Maeshima M. iTRAQ analysis reveals mechanisms of growth defects due to excess zinc in Arabidopsis. Plant Physiol. Apr. 2011, 155(4):1893-1907.
83. Colangelo E., Guerinot M. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell Dec. 2004, 16(12):3400-3412.
84. Vert G., Briat J.F., Curie C. Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant J. Apr. 2001, 26(2):181-189.
85. Vert G., Barberon M., Zelazny E., Séguéla M., Briat J.-F., Curie C. Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta May 2009, 229(6):1171-1179.
86. Talke I., Hanikenne M., Kramer U. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol. Jul. 2006, 142(1):148-167.
87. van de Mortel J.E., Almar Villanueva L., Schat H., Kwekkeboom J., Coughlan S., Moerland P.D., Ver Loren van Themaat E., Koornneef M., Aarts M.G.M. Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol. Sep. 2006, 142(3):1127-1147.
88. Lin Y.-F., Liang H.-M., Yang S.-Y., Boch A., Clemens S., Chen C.-C., Wu J.-F., Huang J.-L., Yeh K.-C. Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol. Apr. 2009, 182(2):392-404.
89. Assunção A.G.L., Herrero E., Lin Y.-F., Huettel B., Talukdar S., Smaczniak C., Immink R.G.H., van Eldik M., Fiers M., Schat H., Aarts M.G.M. Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proc. Natl. Acad. Sci. 2010, 107(22):10296-10301.
90. Wintz H., Fox T., Wu Y., Feng V., Chen W., Chang H., Zhu T., Vulpe C. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J. Biol. Chem. 2003, 278(48):47644-47653.
91. Seigneurin-Berny D., Gravot A., Auroy P. HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J. Biol. Chem. Feb 2006, 281.
92. Kim Y.-Y., Choi H., Segami S., Cho H.-T., Martinoia E., Maeshima M., Lee Y. AtHMA1 contributes to the detoxification of excess Zn(II) in Arabidopsis. Plant J. Jun. 2009, 58(5):737-753.
93. 2+/heavy metal pump. J. Biol. Chem. Feb. 2008, 283(15):9633-9641.
94. 1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett. Mar. 2004, 561(1):22-28.
95. 1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol. Dec. 2008, 149(2):894-904.
96. Weber M., Harada E., Vess C., Roepenack-Lahaye E.V., Clemens S. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. Dec. 2003, 37(2):269-281.
97. Ueno D., Milner M.J., Yamaji N., Yokosho K., Koyama E., Clemencia Zambrano M., Kaskie M., Ebbs S., Kochian L.V., Ma J.F. Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J. Apr. 2011, 66(5):852-862.
98. 1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant J. Jun. 2003, 35(2):164-176.
99. Verret F., Gravot A., Auroy P., Leonhardt N., David P., Nussaume L., Vavasseur A., Richaud P. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett. Oct. 2004, 576(3):306-312.
100. 1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett. Jan. 2005, 579(3):783-791.
101. Verret F., Gravot A., Auroy P., Preveral S., Forestier C., Vavasseur A., Richaud P. Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Lett. Feb. 2005, 579(6):1515-1522.
102. Wong C.K.E., Cobbett C.S. HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol. Jan. 2009, 181(1):71-78.
103. Lochlainn S.O., Bowen H.C., Fray R.G., Hammond J.P., King G.J., White P.J., Graham N.S., Broadley M.R. Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator Noccaea caerulescens. PLoS One Mar. 2011, 6(3):e17814.
104. Delhaize E., Gruber B.D., Pittman J.K., White R.G., Leung H., Miao Y., Jiang L., Ryan P.R., Richardson A.E. A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J. Jun. 2007, 51(2):198-210.
105. Montanini B., Blaudez D., Jeandroz S., Sanders D., Chalot M. Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 2007, 8(1):107.
106. Kobae Y., Uemura T., Sato M., Ohnishi M., Mimura T., Nakagawa T., Maeshima M. Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol. 2004, 45(12):1749-1758.
107. Desbrosses-Fonrouge A., Voight K., Schroder A., Arrivault S., Thomine S., Kraemer U. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett. 2005, 579(19):4165-4174.
108. Gustin J.L., Loureiro M.E., Kim D., Na G., Tikhonova M., Salt D.E. MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J. Mar. 2009, 57(6):1116-1127.
109. Assunção A.G., Pieper B., Vromans J., Lindhout P., Aarts M.G., Schat H. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator. Plant Cell Environ. Jan. 2001, 24:1-10.
110. Dräger D.B., Desbrosses-Fonrouge A.-G., Krach C., Chardonnens A.N., Meyer R.C., Saumitou-Laprade P., Krämer U. Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J. Aug. 2004, 39(3):425-439.
111. Shahzad Z., Gosti F., Frérot H., Lacombe E., Roosens N., Saumitou-Laprade P., Berthomieu P. The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet. 2010, 6(4):1000911.
112. Kawachi M., Kobae Y., Mori H., Tomioka R., Lee Y., Maeshima M. A mutant strain Arabidopsis thaliana that lacks vacuolar membrane zinc transporter MTP1 revealed the latent tolerance to excessive zinc. Plant Cell Physiol. Jun. 2009, 50(6):1156-1170.
113. Podar D., Scherer J., Noordally Z., Herzyk P., Nies D., Sanders D. Metal selectivity determinants in a family of transition metal transporters. Journal of Biological Chemistry 2011, 10.1074/jbc.M111.305649.
114. Delhaize E. Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. The Plant Cell Online May 2003, 15(5):1131-1142.
115. Peiter E., Montanini B., Gobert A., Pedas P., Husted S., Maathuis F.J., Blaudez D., Chalot M., Sanders D., Peiter E., Montanini B., Gobert A., Pedas P., Husted S., Maathuis F.J., Blaudez D., Chalot M., Sanders D. A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. PNAS 2007, 104(20):8532-8537.
116. Williams L.E., Pittman J.K., Hall J.L. Emerging mechanism of heavy metal transport in plants. BBA 2000, 1465(1-2):104-120.
117. Cailliatte R., Lapeyre B., Briat J.-F., Mari S., Curie C. The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem. J. Aug. 2009, 422(2):217-228.
118. Cailliatte R., Schikora A., Briat J.F., Mari S., Curie C. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 2010, 22(3):904-917.
119. Curie C., Alonso J.M., Le Jean M., Ecker J.R., Briat J.F. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem. J. May 2000, 347:749-755.
120. Thomine S., Lelièvre F., Debarbieux E., Schroeder J.I., Barbier-Brygoo H. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. March 2003, 34(5):685-695.
121. Lanquar V., Lelièvre F., Bolte S., Hamès C., Alcon C., Neumann D., Vansuyt G., Curie C., Schröder A., Krämer U., Barbier-Brygoo H., Thomine S. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. Dec. 2005, 24(23):4041-4051.
122. Lanquar V., Ramos M.S., Lelièvre F., Barbier-Brygoo H., Krieger-Liszkay A., Krämer U., Thomine S. Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol. Apr. 2010, 152(4):1986-1999.
123. Oomen R.J.F.J., Wu J., Lelièvre F., Blanchet S., Richaud P., Barbier-Brygoo H., Aarts M.G.M., Thomine S. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol. Nov. 2008, 181(3):637-650.
124. Mizuno T., Usui K., Horie K., Nosaka S., Mizuno N., Obata H. Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant and their Ni-transport abilities. Plant Physiol. Biochem. Aug. 2005, 43(8):793-801.
125. Harada E., Sugase K., Namba K., Iwashita T., Murata Y. Structural element responsible for the Fe(III)-phytosiderophore specific transport by HvYS1 transporter in barley. FEBS Lett. Sep. 2007, 581(22):4298-4302.
126. Lee S., Chiecko J.C., Kim S.A., Walker E.L., Lee Y., Guerinot M.L., An G. Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol. Jun. 2009, 150(2):786-800.
127. Curie C., Cassin G., Couch D., Divol F., Higuchi K., Le Jean M., Misson J., Schikora A., Czernic P., Mari S. Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann. Bot. Oct. 2008, 103(1):1-11.
128. DiDonato R.J., Roberts L.A., Sanderson T., Bosler Eisley R., Walker E.L. Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J. 2004, 39 (3):403-414.
129. Schaaf G. A putative function for the arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol. Mar. 2005, 46(5):762-774.
130. Le Jean M., Schikora A., Mari S., Briat J.F., Curie C. A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading of Fe and NA into seeds. Plant J. Dec. 2005, 44 (5):769-782.
131. Waters B.M., Chu H.H., Didonato R.J., Roberts L.A., Eisley R.B., Lahner B., Salt D.E., Walker E.L. Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol. Jun. 2006, 141(4):1446-1458.
132. Verrier P.J., Bird D., Burla B., Dassa E., Forestier C., Geisler M., Klein M. Plant ABC proteins - a unified nomenclature and updated inventory. Trends Plant Sci. Mar. 2008, 13(4):151-159.
133. Kretzschmar T., Burla B., Lee Y., Martinoia E., Nagy R. Functions of ABC transporters in plants. Essays Biochem. Sep. 2011, 50(1):145-160.
134. Park J., Song W.-Y., Ko D., Eom Y., Hansen T.H., Schiller M., Lee T.G., Martinoia E., Lee Y. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. Oct. 2011, (no-no).
135. Ricachenevsky F.K., Sperotto R.A., Menguer P.K., Sperb E.R., Lopes K.L., Fett J.P. Zinc-induced facilitator-like family in plants: lineage-specific expansion in monocotyledons and conserved genomic and expression features among rice (Oryza sativa) paralogs. BMC Plant Biol. 2011, 11:20.
136. Long T.A., Tsukagoshi H., Busch W., Lahner B., Salt D.E., Benfey P.N. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. The Plant Cell Online Aug. 2010, 22(7):2219-2236.
137. Yang T.J.W., Lin W.D., Schmidt W. Transcriptional profiling of the arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiol. Apr. 2010, 152(4):2130-2141.
138. Nozoye T., Nagasaka S., Kobayashi T., Takahashi M., Sato Y., Sato Y., Uozumi N., Nakanishi H., Nishizawa N.K. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. Feb. 2011, 286(7):5446-5454.
139. Graham R.D., Stangoulis J.C.R. Trace element uptake and distribution in plants. J. Nutr. May 2003, 133(5):1502S-1505S.
140. Suzuki M., Tsukamoto T., Inoue H., Watanabe S., Matsuhashi S., Takahashi M., Nakanishi H., Mori S., Nishizawa N.K. Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Mol. Biol. Jan. 2008, 66(6):609-617.
141. Curie C., Briat J.-F. Iron Transport and signaling in plants. Annu. Rev. Plant Biol. Jun. 2003, 54(1):183-206.
142. Ling H.Q., Pich A., Scholz G., Ganal M.W. Genetic analysis of two tomato mutants affected in the regulation of iron metabolism. Mol. Gen. Genet. Aug. 1996, 252(1):87-92.
143. Herbik A., Giritch A., Horstmann C., Becker R., Balzer H., Baumlein H., Stephan U. Iron and copper nutrition-dependent changes in protein expression in a tomato wild type and the nicotianamine-free mutant chloronerva. Plant Physiol. 1996, 111(2):533-540.
144. Takahashi M., Terada Y., Nakai I., Yoshimura E., Mori S., Nishizawa N.K. Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell Jun. 2003, 15(6):1263-1280.
145. Gendre D., Czernic P., Conéjéro G., Pianelli K., Briat J.-F., Lebrun M., Mari S. TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J. Nov. 2006, 49(1):1-15.
146. von Wirén N., Klair S., Bansal S., Briat J., Khodr H., Shioiri T., Leigh R., Hider R. Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol. Mar. 1999, 119(3):1107-1114.
147. Rellán-Alvarez R., Abadía J., Alvarez-Fernández A. Formation of metal-nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. A study by electrospray ionization time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. May 2008, 22(10):1553-1562.
148. Kerkeb L., Kraemer U. The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol. Jan. 2003, 131(2):716-724.
149. Persans M.W., Yan X., Patnoe J.M., Kramer U., Salt D.E. Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Halacsy). Plant Physiol. 1999, 121:117-1126.
150. Ma J.F., Ueno D., Zhao F.-J., McGrath S.P. Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta Mar. 2005, 220(5):731-736.
151. Küpper H., Mijovilovich A., Meyer-Klaucke W., Kroneck P.M.H. Tissue- and age-dependent differences in the complexation of cadmium and zinc in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by x-ray absorption spectroscopy/zinc hyperaccumulator Thlaspi caerulescens. Plant Physiol. 2004, 134 (2):748-757.
152. Cobbett C., Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. Jun. 2002, 53(1):159-182.
153. Clay N., Adio A., Denoux C., Jander J., Ausubel F. Glucosinolate metabolites required for an arabidopsis innate immune response. Science Dec. 2008, 323:1-7.
154. Rouhier N., Lemaire S.D., Jaquot J.-P. The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins andglutathionylation. Annu. Rev. Plant Biol. Jun. 2008, 59(1):143-166.
155. Shanmugam V., Tsednee M., Yeh K.-C. ZINC TOLERANCE INDUCED BY IRON 1 reveals the importance of glutathione in the cross-homeostasis between zinc and iron in Arabidopsis thaliana. Plant J. Nov. 2011, 60(6):1006-1017.
156. Guo W.J., Meetam M., Goldsbrough P.B. Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol. Apr. 2008, 146(4):1697-1706.
157. Roosens N.H.C.J., Willems G., Saumitou-Laprade P. Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends Plant Sci. May 2008, 13(5):208-215.
158. Hassinen V.H., Tuomainen M., Peräniemi S., Schat H., Kärenlampi S.O., Tervahauta A.I. Metallothioneins 2 and 3 contribute to the metal-adapted phenotype but are not directly linked to Zn accumulation in the metal hyperaccumulator, Thlaspi caerulescens. J. Exp. Bot. Nov. 2008, 60(1):187-196.
159. Zhao H., Eide D.J. Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Mol. Cell. Biol. Sep. 1997, 17(9):5044-5052.
160. Zhao H., Butler E., Rodgers J., Spizzo T., Duesterhoeft S., Eide D. Regulation of zinc homeostasis in yeast by binding of the ZAP1 transcriptional activator to zinc-responsive promoter elements. J. Biol. Chem. Oct. 1998, 273(44):28713-28720.
161. Ishimaru Y. OsZIP4, a novel zinc-regulated zinc transporter in rice. J. Exp. Bot. Nov. 2005, 56(422):3207-3214.
162. Pedas P., Schjoerring J.K., Husted S. Identification and characterization of zinc-starvation-induced ZIP transporters from barley roots. Plant Physiol. Biochem. May 2009, 47(5):377-383.
163. Hammond J.P., Bowen H.C., White P.J., Mills V., Pyke K.A., Baker A.J.M., Whiting S.N., May S.T., Broadley M.R. A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol. Apr. 2006, 170(2):239-260.
164. Abdel-Ghany S.E., Muller-Moule P., Niyogi K.K., Pilon M., Shikanai T. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. The Plant Cell Online Apr. 2005, 17(4):1233-1251.
165. Liu T.-Y., Chang C.-Y., Chiou T.-J. The long-distance signaling of mineral macronutrients. Curr. Opin. Plant Biol. Jun. 2009, 12(3):312-319.
166. Forde B.G. Local and long-range signaling pathways regulating plant responses to nitrate. Annu. Rev. Plant Biol. Jun. 2002, 53(1):203-224.
167. Engineer C.B., Kranz R.G. Reciprocal leaf and root expression of AtAmt1.1 and root architectural changes in response to nitrogen starvation. Plant Physiol. 2006, 143(1):236-250.
168. Lin S.I., Chiang S.F., Lin W.Y., Chen J.W., Tseng C.Y., Wu P.C., Chiou T.J. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol. Apr. 2008, 147(2):732-746.
169. Pant B.D., Buhtz A., Kehr J., Scheible W.-R. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. Mar. 2008, 53(5):731-738.
170. Péret B., De Rybel B., Casimiro I., Benková E., Swarup R., Laplaze L., Beeckman T., Bennett M.J. Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 2009, 14 (7):399-408.
171. Svistoonoff S., Creff A., Reymond M., Sigoillot-Claude C., Ricaud L., Blanchet A., Nussaume L., Desnos T. Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. May 2007, 39(6):792-796.
172. Jain A., Poling M.D., Karthikeyan A.S., Blakeslee J.J., Peer W.A., Titapiwatanakun B., Murphy A.S., Raghothama K.G. Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in arabidopsis. Plant Physiol. Mar. 2007, 144(1):232-247.
173. Yousfi S., Wissal M., Mahmoudi H., Abdelly C., Gharsalli M. Effect of salt on physiological responses of barley to iron deficiency. Plant Physiol. Biochem. May 2007, 45(5):309-314.
174. Giehl R.F.H., Lima J.E., von Wiren N. Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell Jan. 2012, 24:33-49.
175. Gruszak M., Pezeshigi S. Shoot-to-root signal transmission regulates root Fe. Plant Physiol. Mar. 1996, 110:329-334.
176. Enomoto Y., Hodoshima H., Shimada H., Shoji K., Yoshihara T., Goto F. Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots. Planta Oct. 2007, 227(1):81-89.
177. Kim S.A., Punshon T., Lanzirotti A., Li L., Alonso J.M., Ecker J.R., Kaplan J., Guerinot M.L. Localization of iron in arabidopsis seed requires the vacuolar membrane transporter VIT1. Science Nov. 2006, 314(5803):1295-1298.
178. Filatov V., Dowdle J., Smirnoff N., Ford-Lloyd B., Newbury H.J., Macnair M.R. A quantitative trait loci analysis of Zinc hyperaccumulation in Arabidopsis halleri. New Phytol. May 2007, 174(3):580-590.
179. Pilon M., Cohu C.M., Ravet K., Abdel-Ghany S.E., Gaymard F. Essential transition metal homeostasis in plants. Curr. Opin. Plant Biol. Jun. 2009, 12(3):347-357.
180. 2+-ATPase HMA2. Biochemistry Jul. 2007, 46(26):7754-7764.
181. Baekgaard L., Mikkelsen M.D., Sorensen D.M., Hegelund J.N., Persson D.P., Mills R.F., Yang Z., Husted S., Andersen J.P., Buch-Pedersen M.J., Schjoerring J.K., Williams L.E., Palmgren M.G. A combined zinc/cadmium sensor and zinc/cadmium export regulator in a heavy metal pump. J. Biol. Chem. Oct. 2010, 285(41):31243-31252.
182. Leitenmaier B., Witt A., Witzke A., Stemke A., Meyer-Klaucke W., Kroneck P.M.H., Küpper H. Biochemical and biophysical characterisation yields insights into the mechanism of a Cd/Zn transporting ATPase purified from the hyperaccumulator plant Thlaspi caerulescens. Biochim. Biophys. Acta Oct. 2011, 1808(10):2591-2599.
183. Young L.W., Westcott N.D., Attenkofer K., Reaney M.J.T. A high-throughput determination of metal concentrations in whole intact Arabidopsis thaliana seeds using synchrotron-based X-ray fluorescence spectroscopy. J. Synchrotron Radiat. Jul. 2006, 13(4):304-313.
184. Chu H.H., Chiecko J., Punshon T., Lanzirotti A., Lahner B., Salt D.E., Walker E.L. Successful reproduction requires the function of Arabidopsis YELLOW STRIPE-LIKE1 and YELLOW STRIPE-LIKE3 metal-nicotianamine transporters in both vegetative and reproductive structures. Plant Physiol. Sep. 2010, 154(1):197-210.
185. Punshon T., Guerinot M.L., Lanzirotti A. Using synchrotron X-ray fluorescence microprobes in the study of metal homeostasis in plants. Ann. Bot. Dec. 2008, 103(5):665-672.