Essential transition metal homeostasis in plants

Current Opinion in Plant Biology

Volumn 12, Issue 3, 2009, Pages 347-357

  Pilon, Marinus ^a   Cohu, Christopher M ^a   Ravet, Karl ^b   Abdel Ghany, Salah E ^c   Gaymard, Frederic ^b  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b CNRS   (France)

^c Zagazig University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; IRON; MANGANESE; TRANSITION ELEMENT; ZINC;

HOMEOSTASIS; METABOLISM; PHYSIOLOGY; PLANT; REVIEW;

COPPER; HOMEOSTASIS; IRON; MANGANESE; PLANTS; TRANSITION ELEMENTS; ZINC;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CHLAMYDOMONAS;

EID: 66949132548     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2009.04.011     Document Type: Review

References (65)

1. Hänsch R, Mendel RR: Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol, this issue, doi:10.1016/j.pbi.2009.05.006.
2. In: Lippard S.J., and Berg J.M. (Eds). Principles of Bioinorganic Chemistry (1994), University Science Books
3. Puig S, Lola Peñarrubia: Placing metal micronutrients in context: transport and distribution in plants. Curr Opin Plant Biol, this issue, doi:10.1016/j.pbi.2009.04.008.
4. Delhaize E., Gruber B.D., Pittman J.K., White R.G., Leung H., Miao Y., Jiang L., Ryan P.R., and Richardson A.E. A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J 51 (2007) 198-210
5. Peiter E., Montanini B., Gobert A., Pedas P., Husted S., Maathuis F.J.M., Blaudez D., Chalot M., and Sanders D. A secretory pathway-localized cation diffusion facilitor confers plant manganese tolerance. Proc Natl Acad Sci U S A 104 (2007) 8532-8537
6. 2+ pump affects root growth through the secretory process. Plant Phys 147 (2008) 1675-1689
7. Mills R.F., Doherty M.L., Lopéz-Marqués R.L., Weimar T., Dupree P., Palmgreen M.G., Pittman J.K., and Williams L.E. ECA3, a golgi-localized P2A-type ATPase, plays a crucial role in manganese Nutrition in Arabidopsis. Plant Phys 146 (2008) 116-128
8. Su Z., Chai M.F., Lu P.L., An R., Chen J., and Wang X.C. AtMTM1, a novel mitochondrial protein, may be involved in activation of the manganese-containing superoxide dismutase in Arabidopsis. Planta 226 (2007) 1031-1039
9. Morgan M.J., Lehmann M., Schwarzländer M., Baxter C.J., Sienkiewicz-Porzucek A., Williams T.C.R., Schauer N., Fernie A.R., Fricker M.D., Ratcliffe R.G., et al. Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxilic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol 147 (2008) 101-114
10. Andreas Helmersson A., Sara von Arnold S., and Bozhkov P.V. The level of free intracellular zinc mediates programmed cell death/cell survival decisions in plant embryos. Plant Physiol 147 (2008) 1158-1167. Zn was known to participate in the regulation of programmed cell death in a number of mammalian systems. The authors show that Zn (low Zn) also participates in the cellular decision to undergo apoptosis. A Zn sensitive probe was used to demonstrate low Zn levels in cells that will undergo programmed cell death. This process is required for correct embryonic patterning.
11. Desbrosses-Fonrouge A.G., Voigt K., Schröder A., Arrivault S., Thomine S., and Krämer U. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579 (2005) 4165-4174
12. Arrivault S., Senger T., and 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 46 (2006) 861-879
13. Haydon M.J., and Cobbett C.S. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol 143 (2007) 1705-1719
14. Hussain D., Haydon M.J., Wang Y., Wong E., Sherson S.M., Young J., Camakaris J., Harper J.F., and Cobbett C.S. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16 (2004) 1327-1339
15. Mills R.F., Francini A., Ferreira da Rocha P.S., Baccarini P.J., Aylett M., Krijger G.C., and Williams L.E. The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579 (2005) 783-791
16. Eren E., Kennedy D.C., Maroney M.J., and Argüello J.M. A novel regulatory metal binding domain is present in the C terminus of Arabidopsis Zn2+-ATPase HMA2. J Biol Chem 281 (2006) 33881-33891
17. Waters B.M., and Grusak M.A. Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1/ysl3. New Phytol 177 (2008) 389-405
18. Eren E., Gonzalez-Guerrero M., Kaufman B.M., and Argüello J.M. Novel Zn2+ coordination by the regulatory N-terminus metal binding domain of Arabidopsis thaliana Zn2+-ATPase HMA2. Biochemistry 46 (2007) 7754-7764. The Zn binding capacity of the N-terminal metal-binding domain of HMA2 is characterized. Mutants without efficient Zn binding or lacking the N-terminal domain still transport Zn. Possibly the N-terminal domain has a regulatory role in controlling the ATPase activity of the transporter.
19. Wu C.C., Rice W.J., and Stokes D.L. Structure of a copper pump suggests a regulatory role for its metal-binding domain. Structure 16 (2008) 976-985
20. Talke I.N., Hanikenne M., and Krämer 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 142 (2006) 148-167. Transcript profiling was used to identify genes involved in Zn homeostasis in two closely related plants: the non-accumulator A. thaliana and the Zn/Cd hyper accumulator A. halleri. Samples were taken from roots and shoots of plants grown on different Zn regimes. The study identified a number of Zn-regulated transporters in A. thaliana. The same genes functioned in the hyperaccumulator, but the expression pattern differed. Genes that are involved in Zn acquisition on low Zn in the root of the non-accumulator were constitutively expressed in the root of the hyperaccumulator.
21. Hanikenne M., Talke I.N., Haydon M.J., Lanz C., Nolte A., Motte P., Kroymann J., Weigel D., and Krämer U. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453 (2008) 391-395. The Zn/Cd hyperaccumulator A. halleri expresses the HMA4 transporter, that is required for root to shoot transport, to much higher levels than A. thaliana, a closely related non-accumulator. High expression and thus activity of HMA4 is caused by alterations in cis-acting elements as well as the presence of three instead of one gene copy. These findings provide insight into the evolution of hyperaccumulation.
22. Busi M.V., Maliandi M.V., Valdez H., Clemente M., Zabaleta E.J., Araya A., and Gomez-Casati D.F. Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe-S proteins and induces oxidative stress. Plant J 48 (2006) 873-882. In the Arabidopsis frataxin mutant, the activities of mitochondrial Fe-S cluster-dependent proteins are reduced, showing that frataxin is involved in Fe-S cluster assembly. Additional phenotypes are associated with this mutation, like an increase in superoxide production and activation of oxidative stress related genes. Thus, frataxin is also involved in protection against oxidative stress.
23. Ravet K., Touraine B., Boucherez J., Briat J.F., Gaymard F., and Cellier F. Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57 (2009) 400-412. The characterization of an Arabidopsis mutant devoided of ferritins has shown that this protein does not constitute an iron source metabolism and does not provide iron to the plastidial Fe-S cluster machinery. This work revealed that ferritin's main function is to protect the cell against free iron reactivity with oxygen leading to ROS production.
24. Frazzon A.P., Ramirez M.V., Warek U., Balk J., Frazzon J., Dean D.R., and Winkel B.S. Functional analysis of Arabidopsis genes involved in mitochondrial iron-sulfur cluster assembly. Plant Mol Biol 64 (2007) 225-240. A knockout mutant in the NFS2 (mtNiFS) gene encoding the mitochondrial cysteine desulfurase is lethal. Silenced plants for mtNiFS exhibited a number of striking phenotypes, including chlorosis and developmental abnormalities.
25. 2 assimilation were severely impaired. On the contrary, mitochondrial Fe-S proteins and respiration were not affected. These results suggest that mitochondrial and chloroplastic Fe-S cluster assembly operate independently.
26. 2). In vitro reconstitution of the ferredoxin iron-sulfur cluster in the presence of the CpNifS-CpSufE complex was 20-fold higher than that of CpNifS alone.
27. Xu X.M., and Möller S.G. AtSufE is an essential activator of plastidic and mitochondrial desulfurases in Arabidopsis. EMBO J 25 (2006) 900-909. AtSufE1 localizes to both plastids and mitochondria and activates both mtNiFS and cpNiFS. A mutant in AtSufE1 gene is embryo lethal, and this phenotype was rescued only when AtSufE1 was expressed in both plastidic and mitochondrial compartments. AtSufE1 acts, therefore, as an essential component of both plastidic and mitochondrial Fe-S cluster biogenesis machinery.
28. Kumánovics A., Chen O.S., Li L., Bagley D., Adkins E.M., Lin H., Dingra N.N., Outten C.E., Keller G., Winge D., et al. Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial iron-sulfur cluster synthesis. J Biol Chem 283 (2008) 10276-10286
29. Bandyopadhyay S., Gama F., Molina-Navarro M.M., Gualberto J.M., Claxton R., Naik S.G., Huynh B.H., Herrero E., Jacquot J.P., Johnson M.K., and Rouhier N. Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27 (2008) 1122-1133. In vitro studies bring evidence for the incorporation of a [2Fe-2S] cluster in the two chloroplastic monothiolglutaredoxin GrxS14 and GrxS16. [2Fe-2S] clusters on GrxS14 are transferred to apo-ferredoxin. Thus, these chloroplastic Grxs have the potential to function as scaffold proteins and may function in the storage and/or delivery of preformed Fe-S clusters or in the regulation of the chloroplastic Fe-S cluster assembly machinery.
30. Murthy N.M., Ollagnier-de-Choudens S., Sanakis Y., Abdel-Ghany S.E., Rousset C., Ye H., Fontecave M., Pilon-Smits E.A., and Pilon M. Characterization of Arabidopsis thaliana SufE2 and SufE3: functions in chloroplast iron-sulfur cluster assembly and Nad synthesis. J Biol Chem 282 (2007) 18254-18264. Like SufE1, SufE2 and SufE3 are chloroplastic activators of cysteine desulfurase. SufE3 is expressed in all plant organs, while SufE2 expression is restricted to flower. SufE3 contains a NadA additional domain that is similar to the bacterial quinolinate synthase. A highly oxygen-sensitive 4Fe-4S cluster is present in the NadA domain of SufE3, which can be reconstituted in vitro in the presence of CpNifS, cysteine and iron. Thus, additionally to the cysteine desulfurase activation, SuFE3 is involved in a crucial step of NAD biosynthesis.
31. Lill R., and Mühlenhoff U. Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77 (2008) 669-700
32. Li K., Tong W.H., Hughes R.M., and Rouault T.A. Roles of the mammalian cytosolic cysteine desulfurase, ISCS, and scaffold protein, ISCU, in iron-sulfur cluster assembly. J Biol Chem 281 (2006) 12344-12351
33. Chen S., Sanchez-Fernandez R., Lyver E.R., Dancis A., and Rea P.A. Functional characterization of AtATM1, AtATM2, and AtATM3, a subfamily of Arabidopsis half-molecule ATP-binding cassette transporters implicated in iron homeostasis. J Biol Chem 282 (2007) 21561-21571
34. Bych K., Netz D.J., Vigani G., Bill E., Lill R., Pierik A.J., and Balk J. The essential cytosolic iron-sulfur protein NBP35 acts without CFD1 partner in the green lineage. J Biol Chem PMID (2008) 18957412. In yeast and humans, the CIA (cytosolic iron-sulfur cluster assembly) machinery includes two P-loop NTPases, Cfd1 and Nbp35, which form a heteromeric complex and function as Fe-S scaffolds. In Arabidopsis, a gene encoding Npb35 homologue is present, but CFD1 is absent. When expressed in yeast, AtNBP35 binds iron dependent on the mtNiFS activity, indicating that this cytosolic machinery is dependent on the mitochondrial Fe-S cluster biogenesis machinery. In vitro, the holo-AtNBP35 was able to transfer an Fe-S cluster to an apoprotein. The disruption of AtNBP35 gene was associated with an arrest of embryo development, putting out the essential role of this cytosolic machinery, likely to be essential to transfer Fe-S clusters to cytosolic and nuclear proteins.
35. Colangelo E.P., and Guerinot M.L. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16 (2004) 3400-3412
36. Yuan Y., Wu H., Wang N., Li J., Zhao W., Du J., Wang D., and Ling H.Q. FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18 (2008) 385-397
37. Kerkeb L., Mukherjee I., Chatterjee I., Lahner B., Salt D.E., and Connolly E.L. Iron-induced turnover of the Arabidopsis iron-regulated transporter1 metal transporter requires lysine residues. Plant Physiol 146 (2008) 1964-1973
38. Kobayashi T., Ogo Y., Itai R.N., Nakanishi H., Takahashi M., Mori S., and Nishizawa N.K. The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. Proc Natl Acad Sci U S A 104 (2007) 19150-19155
39. Ogo Y., Kobayashi T., Nakanishi Itai R., Nakanishi H., Kakei Y., Takahashi M., Toki S., Mori S., and Nishizawa N.K. A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem 283 (2008) 13407-13417
40. Ogo Y., Itai R.N., Nakanishi H., Inoue H., Kobayashi T., Suzuki M., Takahashi M., Mori S., and Nishizawa N.K. Isolation and characterization of IRO2, a novel iron-regulated bHLH transcription factor in graminaceous plants. J Exp Bot 57 (2006) 2867-2878
41. Ogo Y., Itai R.N., Nakanishi H., Kobayashi T., Takahashi M., Mori S., and Nishizawa N.K. The rice bHLH protein OsIRO2 is an essential regulator of the genes involved in Fe uptake under Fe-deficient conditions. Plant J 51 (2007) 366-377. The rice bHLH trans-acting factor OsIRO2 is strongly induced by iron-starvation. This protein is an essential regulator of genes involved in mugineic acid synthesis and iron uptake. Interestingly, an IDE1 element is present in the OsIRO2 promoter, suggesting that the expression of this factor is under the control of IDEF1. OsIRO2 binding sites have been localized in the promoter regions of some transcription factors whose expression was downregulated in an OsIRO2 knockdown lines, suggesting that other activation steps occur downstream of OsIRO2.
42. Jeong J., Cohu C., Kerkeb L., Pilon M., Connolly E.L., and Guerinot M.L. Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci U S A 105 (2008) 10619-10624. FRO7 is a member of the ferric reductase oxidase family localized to the chloroplast. Loss-of-function mutants are iron-deficiency hypersensitive, exhibit decreased chlorophyll and chloroplastic iron contents and show alterations in photosynthesis activity and in photosynthetic complexes composition. This study provides molecular and genetic evidence for the involvement of FRO7 in chloroplast iron acquisition.
43. Duy D., Wanner G., Meda A.R., von Wiren N., Soll J., and Philippar K. PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19 (2007) 986-1006. AtPIC1 is homologous to the Synechocystis iron permease and is targeted to the inner envelope of the chloroplast. AtPIC1 complemented the iron acquisition defective fet3 fet4 and ctr1 yeast mutants, suggesting that the protein exhibited an iron transport activity. The Arabidopsis mutant pic1 grew only heterotrophically and was characterized by a chlorotic and dwarfism phenotype reminiscent of iron-deficient plants. The mutant presented a severely impaired chloroplast development, differential regulation of genes involved in iron stress, iron transport, photosynthesis and Fe-S cluster biogenesis, but to a striking overaccumulation of ferritins. This study provides evidences of an iron transport activity when PIC1 was expressed in yeast and strong deregulations observed in the mutant at the molecular, structural and physiological levels indicate that PIC1 acts directly or indirectly in the control of iron homeostasis.
44. Long J.C., Sommer F., Allen M.D., Lu S.F., and Merchant S.S. FER1 and FER2 encoding two ferritin complexes in Chlamydomonas reinhardtii chloroplasts are regulated by iron. Genetics 179 (2008) 137-147
45. Busch A., Rimbauld B., Naumann B., Rensch S., and Hippler M. 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 (2008) 201-211
46. Abdel-Ghany S.E., Müller-Moulé P., Niyogi K.K., Pilon M., and Shikanai T. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17 (2005) 1233-1251
47. Cohu C.M., and Pilon M. Regulation of superoxide dismutase expression by copper availability. Physiol Planta 129 (2007) 747-755
48. Sunkar R., Kapoor A., and Zhu J.-K. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18 (2006) 2051-2065. A firm link is established between miR398 and the regulation of the Cu/ZnSOD genes CSD1 and CSD2 in Arabidopsis, in the context of oxidative stress. miR398 targets CSD1 and CSD2 mRNA for cleavage. The authors found miR398 to be downregulated by oxidative stress treatments. Plants in which the miR398 system is de-regulated were used to establish a link between CuZnSOD content and oxidative stress tolerance. However, extreme experimental conditions had to be used to reveal phenotypic differences with the WT.
49. Yamasaki H., Abdel-Ghany S.E., Cohu C.M., Kobayashi Y., Shikanai T., and Pilon M. Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282 (2007) 16369-16378. MiR398 was found to be regulated primarily by Cu. Compared to Cu, oxidative stress had only a moderate effect on miR398 and consequently Cu/ZnSOD expression.
50. Dugas D.V., and Bartel B. Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67 (2008) 403-417. Next to Cu, Sucrose levels in tissue culture were shown to affect miR398 expression and as a consequence the miR398 targets CSD1 and CSD2. Deletion mutants and over expressors of microRNA398 genes were used to firmly link CSD1 and CSD2 regulation to miR398 in the response to Cu and sucrose. Interestingly, only mild phenotypes were reported for these plants.
51. Abdel-Ghany S.E., and Pilon M. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283 (2008) 15932-15945. Four Cu-microRNA families (miR398 and the newly identified miR397, miR408 and miR857) were shown to target the mRNAs for the Cu proteins Cu/ZnSOD, laccase and plantacyanin. Cleavage site analysis confirmed the new targets. Each of these Cu-microRNAs was upregulated on low Cu throughout the plant. The Cu-microRNA target genes were accumulated only when Cu levels were sufficient. Plastocyanin, an essential Cu protein was not downregulated on low Cu. The expression of Cu-microRNAs was observed before Cu-deficiency affected Cu delivery to Plastocyanin to the extent that photosynthesis would have been compromised.
52. Kropat J., Tottey S., Birkenbihl R.P., Depege N., Huijser P., and Merchant S. 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 (2005) 18730-18735
53. Yamasaki H., Hayashi M., Fukazawa M., Kobayashi Y., and Toshiharu Shikanai T. SPL7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21 (2009) 347-361. In plants several Cu-microRNAs and Cu-transporter genes contain multiple putative Cu-responsive elements with GTAC motifs in their promoters. In WT plants the Cu-microRNAs are expressed on low Cu. In an A. thaliana mutant for spl7 all Cu-microRNAs are de-regulated: they are no longer expressed on low Cu. Consequently, Cu/ZnSOD mRNA is not downregulated in spl7. Cu regulation of a number of metal transporters is also disturbed in spl7. The spl7 mutant shows a severe phenotype on low Cu, which indicates the importance of the AtSPL7-mediated response to low Cu for plant survival.
54. Nagae M., Nakata M., and Takahashi Y. Identification of negative cis-acting elements in response to copper in the chloroplast iron superoxide dismutase gene of the moss Barbula unguiculata. Plant Physiol 146 (2008) 1687-1696
55. Andrés-Colás N., Sancenón V., Rodríguez-Navarro S., Mayo S., Thiele D.J., Ecker J.R., Puig S., and Peñarrubia L. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45 (2006) 225-236
56. Mukherjee I., Campbell N.H., Ash J.S., and Connolly E.L. Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta 223 (2006) 1178-1190
57. Buhtz A., Springer F., Chappell L., Baulcombe D., and Kehr J. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53 (2008) 739-749
58. Chu C.C., Lee W.C., Guo W.Y., Pan S.M., Chen L.J., Li H.M., and Jinn T.L. A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139 (2005) 425-436
59. Abdel-Ghany S.E. Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes. Planta 229 (2009) 767-779
60. Uauy C., Distelfeld A., Fahima T., Blechl A., and Dubcovsky J. A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314 (2006) 1298-1301. Most wheat varieties have a low Zn and Fe content in their grains. A QTL locus that controls wheat grain Zn, Fe and protein content was cloned. The gene encodes a NAC transcription factor involved in the regulation of senescence. The locus is inactive in most cultured wheat species but expressed and active in wild ancestors. Presumably, selection for yield has resulted in loss of function of this gene.
61. Durrett T.P., Connolly E.L., and Rogers E.E. Arabidopsis cpFtsY mutants exhibit pleiotropic defects including an inability to increase iron deficiency-inducible root Fe(III) chelate reductase activity. Plant J 47 (2006) 467-479
62. Seguela M., Briat J.F., Vert G., and Curie C. Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway. Plant J 55 (2008) 289-300
63. Korenkov V., Hirschi K., Crutchfield J.D., and Wagner G.J. Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 226 (2007) 1379-1387
64. Kawachi M., Kobae Y., Mimura T., and Maeshima M. Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn(2 + )/H(+) antiporter of Arabidopsis thaliana, stimulates the transport activity. J Biol Chem 283 (2008) 8374-8383. A yeast expression system was used to study the kinetics of Zn transport of wild-type AtMTP1 as well as a mutant that lacks a cytoplasmic histidine-rich loop.
65. Gustin J.L., Loureiro M.E., Kim D., Na G., Tikhonova M., and Salt D.E. MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J 57 (2009) 1116-1127. MTP1 from the Zn hyperaccumulator Thlaspi goesingense was localized to the tonoplast and not the plasmalemma. Expression in A. thaliana indicates that the protein mediates Zn sequestration in vacuoles and tolerance. Furthermore, high MTP1 activity induces a systemic Zn deficiency response characteristic of hyperaccumulators.