Abstract
Many metals are known to be essential for plants while others are not. Large amounts of essential or non-essential metals can be toxic. The availability of metals in soil can vary, both temporally and spatially. How do roots acquire, store and distribute each required metal while avoiding either toxicity or deficiency? What genes determine these responses?
This account considers iron, copper and zinc. Progress in the isolation, functional analysis and metallo-regulation of genes encoding metallothionein-like proteins and root surface metal reductases is described. This article is not a broad review but presents some of our recent findings in the context of related research.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Anderson G J, Lesuisse E, Dancis A, Roman D G, Labbe P and Klausner R D 1992 Ferric iron reduction and iron assimilation in Saccharomyces cerevisiae. J. Inorg. Biochem. 47, 249–255.
Apel K, Bohlmann H and Reinmannphilipp U 1990 Leaf thionins, a novel class of putative defense factors. Physiol. Plant. 80, 315–321.
Askwith C, Eide D, Van Ho A, Bernhard P S, Li L, Davis-Kaplan S, Sipe D M and Kaplan J 1994 The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferous iron uptake. Cell 76, 403–410.
Bagg A and Neilands J B 1987 Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol. Rev. 51, 509–518.
Bernhard W R and Kagi J H R 1987 Purification and characterization of atypical cadmium-binding polypeptide from Zea mays. In Metallothionein II. Proceedings of the Second International meeting on Metallothionein and other low molecular weight metal-binding proteins, Zurich, 1985. Eds. J H R Kägi and Kojima. pp 309–315. Birkhäuser Verlag, Basel.
Brown N L, Rouch D A and Lee B T O 1992 Copper-resistance mechanisms in bacteria. Plasmid 27, 41–51.
Buchanan-Wollaston V 1994 Isolation of cDNA clones for genes that are expressed during leaf senescence in Brassica napus — identification of a gene encoding a senescence-specific metallothionein-like protein. Plant Physiol. 105, 839–846.
Buckhout T J, Bell P F, Luster D G and Chaney R L 1989 Iron-stress induced redox activity in tomato (Lycopersicum esculentum Mill.) is localized on the plasma membrane. Plant Physiol. 90, 151–156.
Cakmak I, van de Wetering D A, Marschner H and Bienfait H F 1987 Involvement of superoxide radical in extracellular ferric reduction by iron-deficient bean roots. Plant Physiol. 85, 310–314.
Chang C, Kwok S F, Bleecker A B and Meyerowitz E M 1993 Arabidopsis ethylene-response gene ETR1: Similarity of product to two-component regulators. Science 262, 539–544.
Chang C 1996 The ethylene signal transduction pathway in Arabidopsis: an emerging paradigm? Trends Biochem. Sci. 21, 129–133.
Chen Y, Saari J T and Kang Y J 1995 Copper deficiency increases metallothionein-I mRNA content selectively in rat liver. Nutr. Biochem. 6, 572–576.
Culotta V C, Howard W R and Liu X F 1994 CRS5 encodes a metallothionein-like protein in Saccharomyces cerevisiae. J. Biol. Chem. 269, 25295–25302.
Dameron C T, Winge D R, George G N, Sansones M, Hu S and Hamer D 1991 A copper-thiolate polynuclear cluster in the ACE1 transcription factor. Proc. Natl. Acad. Sci. USA 88, 6127–6131.
Dancis A, Roman D G, Anderson G J, Hinnebusch A G and Klausner R D 1992 Ferric reductase of Saccharomyces cerevisiae: molecular characterization, role in iron uptake, and transcriptional control by iron. Proc. Natl. Acad. Sci. USA 89, 3869–3873.
Dancis A, Yuan D S, Haile D, Askwith C, Eide D, Moehle C, Kaplan J and Klausner R D 1994 Molecular characterization of a copper transport protein in S. cerevisiae: An unexpected role for copper in iron transport. Cell 76, 393–402.
De Framond A J 1991 A metallothionein-like gene from maize (Zea mays). FEBS Lett. 290, 103–106.
De Miranda J R, Thomas M A, Thurman D A and Tomsett A B 1990 Metallothionein genes from the flowering plant Mimulus guttatus. FEBS Lett. 260, 277–280.
De Silva D M, Askwith C C, Eide D and Kaplan J 1995 The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase. J. Biol. Chem. 270, 1098–1101.
Ecker J R 1995 The ethylene signal-transduction pathway in plants. Science 268, 667–675.
Evans I M, Gatehouse L N, Gatehouse J A, Robinson N J and Croy R R D 1990 A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Lett. 262, 29–32.
Evans K M, Gatehouse J.A, Lindsay W P, Shi J, Tommey A M and Robinson N J 1992 Expression of the pea metallothionein-like gene PsMT A in Escherichia coli and Arabidopsis thaliana and analysis of trace metal ion accumulation: Implications for PsMT A function. Plant Mol. Biol. 20, 1019–1028.
Foley R C and Singh K B 1994 Isolation of a Vicia faba metallothionein-like gene: expression in foliar trichomes. Plant Mol. Biol. 26, 435–444.
Fortham-Skelton A P et al. Plant Molec. Biol., in press.
Georgatsu E and Alexandraki D 1994 Two distinctly regulated genes are required for ferric reduction, the first step of iron uptake in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 3065–3073.
Grill E, Winnacker E L and Zenk M H 1985 Phytochelatins: The principle heavy-metal complexing peptides of higher plants. Science 230, 674–676.
Groom Q J, Torres M A, Fordham-Skelton A P, Hammond-Kosack K E, Robinson N J and Jones J D G 1996 rbohA, a rice homologue of the mammalian SP91phox respiratory burst oxidase gene. Plant J. 10, 515–522.
Grusak M A, Welch R M and Kochian L V 1990 Physiological characterisation of a single-gene mutant of Pisum sativum exhibiting excess iron accumulation. Plant Physiol. 93, 976–981.
Hamer D H 1986 Metallothionein. Annu. Rev. Biochem. 55, 913–951.
Hassett R and Kosman D J 1995 Evidence for Cu (II) reduction as a component of copper uptake by Saccharomyces cerevisiae. J. Biol. Chem. 270, 128–134.
Hofmann T, Kells D I C and Lane B G 1984 Partial amino acid sequence of the wheat germ Ec protein. Comparison with another protein very rich in half-cystine and glycine: wheat germ agglutinin. Can. J. Biochem. Cell Biol. 62, 908–913.
Huckle J W, Morby A P, Turner J S and Robinson N J 1993 Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol. Microbiol. 7, 177–187.
Itzhaki H, Maxson J M and Woodson W R 1994 An ethylene-responsive enhancer element is involved in the senescence-related expression of the carnation glutathione S-transferase (GST1) gene. Proc. Natl. Acad. Sci. USA 91, 8925–8929.
Jungmann J, Reins H-A, Lee J, Romeo A, Hassett R, Kosman D and Jentsch S 1993 MAC1, a nuclear regulatory protein related to Cu-dependent transcription factors is involved in Cu/Fe utilization and stress resistance in yeast. EMBO J. 12, 5051–5056.
Kakimoto T 1996 CKH, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274, 982–985.
Kanamura K, Kashiwagi S and Mizuno T 1994 A copper-transporting P-type ATPse found in the thylakoid membrane of the Synechococcus species PCC 7942. Mol. Microbiol. 13, 369–377.
Kawashima I, Inokuchi Y, Chino M, Kimura M, and Shimizu N 1991 Isolation of a gene for a metallothionein-like protein from soybean. Plant Cell Physiol. 32, 913–916.
Kawashima I, Kennedy T D, Chino M and Lane B G 1992 Wheat Ec metallothionein genes. Eur. J. Biochem. 209, 971–976.
Kieber J J, Rothenberg M, Roman G, Feldmann K A and Ecker J R 1993 CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427–441.
Kille P, Winge D R, Harwood J L and Kay J 1991 A plant metallothionein produced in E. coli. FEBS Lett. 295, 171–175.
Klemsdal S S, Hughes W, Lönneborg A, Aalen R B and Olsen O A 1991 Primary structure of a novel barley gene differentially expressed in immature aleurone layers. Mol. Gen. Genet. 228, 9–16.
Lamb C J 1994 Plant disease resistance genes in signal perception and transduction. Cell 76, 419–422.
Lane B, Kajioka R and Kennedy T 1987 The wheat-germ Ec protein is a zinc-containing metallothionein. Biochem. Cell Biol. 65, 1001–1005.
Ledger S E and Gardner R C 1994 Cloning and expression of five cDNAs for genes differentially expressed during fruit development of kiwifruit (Actinidia deliciosa var. deliciosa). Plant Mol. Biol. 25, 877–886.
Lesuisse E, Crichton R R and Labbe P 1990 Iron reductases in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Acta 1038, 253–259
Levine A, Tenhaken R, Dixon R and Lamb C 1994 H2O2 from the oxidative burst orchestrates the plant hypersensive disease resistance response. Cell 79, 583–593.
Mehdy M C 1994 Active oxygen species in plant defense against pathogens. Plant Physiol. 105, 467–472.
Moisyadi S and Stiles J I 1995 A cDNA encoding a metallothionein I-like protein from coffee leaves (Coffea arabica). Plant Physiol. 107, 295–296.
Montgomery J, Goldman S, Deikman J, Margossian L and Fischer R L 1993 Identification of an ethylene-responsive region in the promoter of a fruit ripening gene. Proc. Nat. Acad. Sxi. USA 90, 5939–5943.
Morby A.P, Turner J S, Huckle J W and Robinson N J 1993 SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA: identification of a Zn inhibited DNA-protein complex. Nucleic Acids Res. 21, 921–925.
Nielson K B and Winge D R 1983 Order of metal binding in metallothionein. J. Biol. Chem. 58, 13063–13069.
Nielson K B and Winge D R 1984 Preferential binding of copper to the β domain of metallothionein. J. Biol. Chem. 259, 4941–4946.
Okumura N, Nishizawa N-K, Umehara Y and Mori S 1991 An iron deficiency-specific cDNA from barley roots having two homologous cysteine-rich MT domains. Plant Mol. Biol. 17, 531–533.
Okumura N, Nishizawa N-K, Umehara Y, Ohata T and Mori S 1992 Iron deficiency specific cDNA (Ids1) with two homologous cysteine rich MT domains from the roots of barley. J. Plant Nutr. 15, 2157–2172.
Olafson R W, McCubbin W D and Kay C M 1988 Primary and-secondary-structural analysis of a unique prokaryotic metallothionein from a Synechococcus sp. cyanobacterium. Biochem. J. 251, 691–699.
Parkinson J S and Kofoid E C 1992 Communication modules in bacterial signalling proteins. Annu. Rev. Genet. 26, 71–112.
Phung L T, Ajlani G and Haselkorn R 1994 P-type ATPase from the cyanobacterium Synechococcus 7942 related to the human Menkes and Wilson disease gene products. Proc. Nat. Acad. Sci. USA 91, 9651–9654.
Rauser W E and Curvetto N R 1980 Metallothionein occurs in roots of Agrostis tolerant to excess copper: Nature 287, 563–564.
Robinson N J, Barton K, Naranjo C M, Sillerund J O, Trewhella J, Watt K and Jackson P J 1987 Characterization of metal binding peptides from cadmium resistant plant cells. In Metallothionein II. Proceedings of the Second International meeting on Metallothionein and other low molecular weight metal-binding proteins, Zurich 1985. Eds. J H R Kägi and Kojima. pp 323–327. Birkhäuser Verlag, Basel.
Robinson N J, Evans I M, Mulcrone J, Bryden J and Tommey A M 1992 Genes with similarity to metallothionein genes and copper, zinc ligands in Pisum sativum L. Plant Soil 146, 291–298.
Robinson N J, Tommey A M, Kuske C and Jackson P J 1993 Plant metallothioneins. Biochem. J. 295, 1–10.
Robinson N J, Wilson J R and Turner J S 1996 Expression of the type 2 metallothiinein-like gene MT2 from Arabidopsis thaliana in Zn2+-metallothionein-deficient Synechococcus PCC 7942: putative role for MT2 in Zn2+ metabolism. Plant Mol. Biol. 30, 1169–1179.
Romera F J and Alcantara E 1994 Iron-deficiency stress response in cucumber (Cucumis sativus L.) roots. A possible role for ethylene? Plant Physiol. 105, 1133–1138.
Romera F J, Welch R M, Norvell W A and Schaefer S C 1996a Iron requirement for and effects of promoters and inhibitors of ethylene action on stimulation of Fe(III)-chelate reductase in roots of strategy I species. BioMetals 9, 45–50.
Romera F J, Welch R M, Norvell W A, Schaefer S C and Kochian L V 1996b Ethylene involvement in the over-expression of Fe(III)-chelate reductase by roots of El07 pea [Pisum sativum L. (brz, brz)] and chloronerva tomato (Lycopersicon esculentum L.) mutant genotypes. BioMetals 9, 38–44.
Rost B and Sander C 1993 Prediction of protein structure at better than 70% accuracy. J. Mol. Biol. 232, 584–599.
Rost B and Sander C 1994 Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19, 55–72.
Shewry P R and Tatham A S 1990 The prolamin storage proteins of cereal seeds — structure and evolution. Biochem. J. 267, 1–12.
Shi J, Lindsay W P, Huckle J W, Morby A P and Robinson N J 1992 Cyanobacterial metallothionein gene expressed in Escherichia coli. FEBS Lett. 303, 159–163.
Silver S, Nucifora G and Phung L T 1993 Human Menkes X-chromosome disease and the staphylococcal cadmium-resistance ATPase: a remarkable similarity in protein sequences. Mol. Microbiol. 10, 7–12.
Snowden K C and Gardner R C 1993 Five genes induced by aluminium in wheat (Triticum aestivum L.) roots. Plant Physiol. 103, 855–861.
Thiele D J 1992 Metal-regulated transcription in eukaryotes. Nucleic Acids Res. 20, 1183–1191.
Tommey A M, Shi J, Lindsay W P, Urwin P E and Robinson N J 1991 Expression of the pea gene PsMTa in E. coli. FEBS Lett. 292, 48–52.
Turner J S, Morby A P, Whitton B A, Gupta A and Robinson N J 1993 Construction of Zn2+/Cd2+ hypersensitive cyanobacteri al mutants lacking a functional metallothionein locus. J. Biol. Chem. 68, 4494–4498.
Turner J S, Glands P D, Samson A C R and Robinson N J 1996 Zn2+-sensing by the cyanobacterial metallothionein repressor SmtB: different motifs mediate metal-induced protein-DNA dissociation. Nucleic Acids Res. 24, 3714–3721.
Uknes S, Dincher S, Friedrich L, Negrotto D, Williams S, Thompson-Taylor H, Potter S, Ward E and Ryals J 1993 Regulation of pathogenesis-related protein-la gene expression in tobacco. Plant Cell 5, 159–169.
Weig A and Komor E 1995 Isolation of a class II metallothionein cDNA (accession no. L02306) from Ricinus communis L. Plant Physiol. PGR95-066.
Welch R M and LaRue T A 1990 Physiological characteristics of Fe accumulation in the ‘bronze’ mutant of Pisum sativum L. cv’ sparkle’ E107 (brz, brz). Plant Physiol. 93, 723–729.
Welch R M, Norvell W A, Schaefer S C, Shaff J E and Kochian L V 1993 Induction of iron (III) and copper (II) reduction in pea (Pisum sativum L.) roots by Fe and Cu status: Does the root-cell plasmalemma Fe(III)-chelate reductase perform a general role in regulating cation uptake? Planta 190, 555–561.
Yamagchi-Iwai Y, Dancis A and Klausner R 1995 AFT1 a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J. 14, 1231–1239.
Yi Y and Guerinot D 1996 Genetic evidence that induction of root Fe (III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J. 10, 835–844.
Yuan D S, Stearman R, Dancis A, Dunn T, Beller T and Klausner R D 1995 The Menkes-Wilson-disease gene homolog in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc. Natl. Acad. Sci. USA 92, 2632–2636.
Zarembinski T I and Theologis A 1994 Ethylene biosynthesis and action: a case of conservation. Plant Mol. Biol. 26, 1579–1597.
Zhou J and Goldsbrough P B 1994 Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6, 875–884.
Zhou J and Goldsbrough P B 1995 Structure, organization and expression of the metallothionein gene family in Arabidopsis. Mol. Gen. Genet. 248, 318–328.
Author information
Authors and Affiliations
Editor information
Rights and permissions
Copyright information
© 1997 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Robinson, N.J., Wilson, J.R., Turner, J.S., Fordham-Skelton, A.P., Groom, Q.J. (1997). Metal-gene-interactions in roots: metallothionein-like genes and iron reductases. In: Anderson, H.M., Barlow, P.W., Clarkson, D.T., Jackson, M.B., Shewry, P.R. (eds) Plant Roots - From Cells to Systems. Developments in Plant and Soil Sciences, vol 73. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5696-7_12
Download citation
DOI: https://doi.org/10.1007/978-94-011-5696-7_12
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-010-6402-6
Online ISBN: 978-94-011-5696-7
eBook Packages: Springer Book Archive