- Open Access
Zn Uptake and Translocation in Rice Plants
© The Author(s) 2011
Received: 16 February 2011
Accepted: 25 April 2011
Published: 7 May 2011
Zinc (Zn) is an essential micronutrient with numerous cellular functions in plants, and its deficiency represents one of the most serious problems in human nutrition worldwide. Zn deficiency causes a decrease in plant growth and yield. On the other hand, Zn could be toxic if excess amounts are accumulated. Therefore, the uptake and transport of Zn must be strictly regulated. In this review, the dominant fluxes of Zn in soil–root–shoot translocation in rice plants (Oryza sativa) are described, including Zn uptake from soils in the form of Zn2+ and Zn-DMA at the root surface, and Zn translocation to shoots. Knowledge of these fluxes could be helpful to formulate genetic and physiologic strategies to address the widespread problem of Zn-limited crop growth.
Zinc in biology
The variety of roles that zinc (Zn) plays in cellular processes is a good example of the diverse biological utility of metal ions. Zn is involved in protein, nucleic acid, carbohydrate, and lipid metabolism. In addition, Zn is critical to the control of gene transcription and the coordination of other biological processes regulated by proteins containing DNA-binding Zn-finger motifs (Rhodes and Klug 1993), RING fingers, and LIM domains (Vallee and Falchuk 1993). Several molecules associated with DNA and RNA synthesis are also Zn metalloenzymes, such as RNA polymerases (Wu et al. 1992), reverse transcriptases, and transcription factors (Wu and Wu 1989). Zn is a non-redox-active ion and is therefore targeted to transcription factors and other enzymes involved in DNA metabolism, as the use of redox-active metal ions for these tasks could lead to radical reactions and nucleic acid damage. However, these processes must be tightly regulated to ensure that the correct amount of Zn is present at all times. Although it is an essential nutrient, Zn could be toxic if it accumulates in excess. The precise cause of Zn toxicity is unknown, but the metal may bind to inappropriate intracellular ligands, or compete with other metal ions for enzyme active sites or transporter proteins. In order to play such diverse roles in cells, and because it cannot passively diffuse across cell membranes, Zn must be transported into the intracellular compartments of the cell where it is required for these Zn-dependent processes. A group of proteins called Zn transporters is dedicated to the transport of Zn across biological membranes.
Studies of Zn uptake in biology are critical because Zn is essential for all organisms, including humans (Hambidge 2000). As Zn plays multiple roles in plant biochemical and physiological processes, even slight deficiency causes a decrease in growth, yield, and Zn content of edible plant parts. Zn deficiency is a serious agricultural problem as around one half of the cereal-growing soils in the world contain low Zn in the soil (Graham and Welch 1996; Cakmak et al. 1999). In soil, Zn is present in various forms. Among the total soil Zn content, Zn primary minerals constitute around 15%, Zn organic matter complexes around 45%, outer-sphere complexes around 20%, Zn-sorbed phosphate around 10%, and Zn-sorbed iron oxyhydroxides around 10% (Sarret et al. 2004). The solubility and availability of Zn is determined by various factors like high CaCO3, high pH, high clay soils, low organic matter, low soil moisture, and high iron and aluminum oxides (Cakmak 2008).In low Zn soils, the Zn uptake may be enhanced by the exudation of low-molecular-weight compounds like malate and mugineic acid family phytosiderophores (Arnold et al. 2010; Cakmak et al. 1994; Peng et al. 2009; Suzuki et al. 2006; Walter et al. 1994; Widodo et al. 2010; Zhang et al. 1989).
Food Zn content is very important for human health as the artificial supplementation of foods with essential minerals is often difficult to achieve, particularly in developing countries. Therefore, it has been suggested that increased levels of Zn in staple foods, e.g., rice may play a role in reducing Zn deficiency (Ruel and Bouis 1998; Graham et al. 1999; Welch and Graham 1999). Therefore, it is essential to understand the molecular mechanism through which plants mobilize, take up, translocate, and store Zn.
Higher plants take up Zn from the rhizosphere via transporters, and molecular aspects of this phenomenon are now being clarified. In the Arabidopsis thaliana genome, a large number of cation transporters potentially involved in metal ion homeostasis have been identified (Maser et al. 2001). Several members of the Zn-regulated transporters in the iron (Fe)-regulated transporter-like protein (ZIP) gene family (Guerinot 2000) have been characterized and shown to be involved in metal uptake and transport in plants (Eide et al. 1996; Korshunova et al. 1999; Vert et al. 2001, 2002; Connolly et al. 2002). The ZIP proteins are predicted to have eight transmembrane domains, with their amino- and carboxyl-terminal ends situated on the outer surface of the plasma membrane (Guerinot 2000). These proteins vary considerably in overall length due to a variable region between the transmembrane domains (TM) TM-3 and TM-4, which is predicted to be on the cytoplasmic side, providing a potential metal-binding domain rich in histidine residues. The most-conserved region of these proteins lies in a variable region that has been predicted to form an amphipathic helix, containing a fully conserved histidine that may form part of an intramembranous metal-binding site involved in transport (Guerinot 2000). The transport function is disabled when the conserved histidines or certain adjacent residues are replaced by mutation (Rogers et al. 2000).
ZIP1, ZIP3, and ZIP4 from Arabidopsis restore Zn uptake to the yeast (Saccharomyces cerevisiae) Zn-uptake mutant, Δzrt1Δzrt2, and have been proposed to play a role in Zn transport (Grotz et al. 1998; Guerinot 2000). ZIP1 and ZIP3 are expressed in roots in response to Zn deficiency, suggesting that they transport Zn from the soil to the plant, while ZIP4 is expressed in both roots and shoots, suggesting that it transports Zn intracellularly or between plant tissues (Grotz et al. 1998; Guerinot 2000). ZIP2 and ZIP4 rescue yeast mutants deficient in copper (Cu) transport, and ZIP4 is up-regulated in Cu-deficient roots (Wintz et al. 2003). Yeast Zrt1 and Zrt2 are high- and low-affinity Zn transporters, respectively (Eide 1998; Guerinot 2000). The proposed role of ZIP transporters in Zn nutrition has been further supported by the characterization of homologs from several plant species. For example, GmZIP1 has been identified in soybean (Glycine max; Moreau et al. 2002), and functional complementation of Δzrt1Δzrt2 yeast cells showed that GmZIP1 is highly selective for Zn, but not for Fe or manganese (Mn). GmZIP1 is expressed specifically in nodules, but not in roots, stems, or leaves, and the protein is localized to the peribacteroid membrane, suggesting a role in symbiosis. In barley, Zn transporters are induced by low pH (Pedas and Husted 2009).
Furthermore, we have produced transgenic rice plants over-expressing OsZIP4 under the control of the CaMV 35S promoter (Ishimaru et al. 2007). Compared to control plants, Zn concentration in 35S-OsZIP4 transgenic plants was higher in roots and lower in shoots, suggesting that OsZIP4 expression driven by the 35S promoter in the 35S-OsZIP4 root may be involved in xylem unloading and reducing the Zn transport to shoots. Northern blot analysis revealed that transcripts of OsZIP4 expression driven by the CaMV 35S promoter were detected in roots and shoots of 35S-OsZIP4 transgenic plants, but endogenous OsZIP4 transcripts were rare in roots, and abundant in shoots. Microarray analysis revealed that the genes expressed in shoots of 35S-OsZIP4 transgenic plants coincided with those induced in shoots of Zn-deficient plants. Similar results were reported for OsZIP5 overexpression plants, which accumulated more Zn in roots, whereas the shoot Zn accumulation decreased. The OsZIP5OX plants were sensitive to Zn excess, while the Oszip5 knock out plants were tolerant to Zn excess. OsZIP1 and OsZIP3 are primarily associated with Zn uptake in roots and Zn homeostasis in shoots (Ramesh et al. 2003). OsZIP4 is involved in the translocation of Zn, particularly into vascular bundles and meristem (Ishimaru et al. 2005).
Contribution of MAs to Zn uptake and translocation
Recently, we showed that the expression of NASHOR2, a NAS gene in barley (Herbik et al. 1999), and HvNAAT-B was elevated in Zn-deficient barley shoots, but that the expression of IDS2 and IDS3 was not detected in Zn-deficient shoots (Suzuki et al. 2006). However, the expression of HvNAS1, HvNAAT-A, HvNAAT-B, IDS2, and IDS3 was elevated in both Zn- and Fe-deficient roots, while the expression of these genes was not observed in Fe-deficient shoots (Suzuki et al. 2006). Therefore, we suggest that Zn deficiency induces DMA synthesis in barley shoots, while both Zn and Fe deficiency induce MAs synthesis and secretion in barley roots.
A yellow stripe 1 (YS1) gene important for the uptake of Fe3+-MAs has been identified in maize (Curie et al. 2001). ZmYS1 functionally complements yeast strains that are defective in Fe uptake on media containing Fe3+-MAs, but not on media containing Fe3+ citrate, suggesting that ZmYS1 is a MAs-dependent Fe transporter (Curie et al. 2001). ZmYS1 has a broad specificity for metals and ligands, and can transport MAs-bound metals, including Zn, Cu, and nickel (Schaaf et al. 2004, Murata et al. 2006). On the other hand, Roberts et al. (2004) reported that ZmYS1 transported Fe3+- and Cu-MAs, but not Zn-MAs.
Our search for YS1 homologs in the O. sativa L. ssp. japonica (cv. Nipponbare) rice genomic database identified 18 putative OsYSLs that exhibit 36–76% sequence similarity to YS1 (Koike et al. 2004). The phloem-specific expression of OsYSL2 suggests that it is involved in the phloem transport of Fe. OsYSL2 transports Fe2+-NA and Mn2+-NA, but did not transport Fe3+-MAs. These results suggest that OsYSL2 is a rice metal-NA transporter that is responsible for phloem transport of Fe and Mn. OsYSL15 and OsYSL18 transports Fe (III)-DMA (Aoyama et al. 2009; Inoue et al. 2009).
Until now, a Zn-NA transporter or Zn-MAs transporter involved in Zn translocation has not been identified in rice plants. However, the ZmYS1-transport Zn-MAs. NA, and DMA were synthesized in Zn-deficient shoots, and rice plants have 18 putative OsYSLs. These data suggest the existence of Zn-NA or Zn-MAs transporters for Zn translocation in rice shoots.
Zn translocation of Zn2+ and Zn-DMA
Recently, we showed that Zn-deficient barley roots absorb more Zn-DMA than Zn2+ (Suzuki et al. 2006). In contrast, less Zn-DMA than Zn2+ was absorbed from the roots of Zn-deficient rice. These findings are correlated with a change in the amount of MAs secreted under Zn deficiency. In barley, MAs secretion is increased by Zn deficiency, and this contributes to the absorption of Zn from the soil. However, in rice, the level of DMA secretion was slightly reduced (Suzuki et al. 2008b); therefore, rice may prefer to absorb Zn2+ rather than Zn-DMA.
Moreover, we also showed that the amount of endogenous DMA in rice shoots increase due to Zn deficiency, corresponding to the increased expression of OsNAS3, OsNAAT1, and OsDMAS1 in Zn-deficient shoots (Suzuki et al. 2008a, b). In accordance with the dramatic increase in OsNAAT1 expression in Zn-deficient shoots, the amount of endogenous NA in shoots was remarkably reduced by Zn deficiency. In contrast to the increase in MAs secretion caused by Zn deficiency in barley, the amount of DMA secreted from rice roots slightly decrease. Furthermore, our PETIS experiment clearly show that more 62Zn is translocated to the newest leaf when 62Zn-DMA is supplied compared to the conditions when 62Zn2+ was supplied, while the opposite tendency was observed at the bottom of the leaf sheath (Suzuki et al. 2008a, b), suggesting that Zn-DMA is the preferred form for long-distance transport of Zn in Zn-deficient rice.
An appreciation for the importance of Zn in molecular biology, structural biology, and nutritional sciences has grown rapidly over the past 15 years (Berg and Shi 1996). However, many questions about the mechanisms that Zn uses in plants still remain, such as the Zn efflux system, Zn homeostasis inside the cell, and transcriptional and posttranscriptional regulation. Further studies will enable us to clarify the mechanism of Zn transport and to manipulate the distribution of Zn to produce crops that can tolerate stress due to Zn deficiency, as well as enhance the Zn content of food crop seeds.
Seed Zn localization
Rice genotypes differ greatly in Zn use efficiency and grain Zn contents and this aspect has been investigated by various researchers (Graham et al. 1999; Nagarathna et al. 2010; Neue, et al. 1998; Refuerzo et al. 2009; Wissuwa et al. 2006; Wissuwa et al. 2008; Yang et al. 1998). Rice grain Zn concentrations ranged from 15.9 to 58.4 mg kg−1 (Graham et al. 1999), suggesting ample variation for this trait that might be exploited through conventional breeding. Another study revealed that native soil Zn status is the dominant factor to determine grain Zn concentrations followed by genotype and fertilizer. Depending on soil Zn status, grain Zn concentrations could range from 8 to 47 mg kg−1 in a single genotype (Wissuwa et al., 2006; Wissuwa et al., 2008).
Various groups have already demonstrated the potential to increase the Zn concentration of rice grains. Traditional breeding, maker-assisted breeding, and plant transformation techniques and a combination of these techniques can be further exploited to mitigate the Zn deficiency in plants and humans.
This study was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Green Technology Project IP-5003). We thank Dr. Tomoko Nozoye and Dr. Motofumi Suzuki for valuable discussion.
- Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, Kakei Y, et al. OsYSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol. 2009;70:681–92.PubMedPubMed CentralView ArticleGoogle Scholar
- Arnold T, Kirk GJD, Wissuwa M, Frei M, Zhao FJ, Mason TFD, et al. Evidence for the mechanisms of zinc uptake by rice using isotope fractionation. Plant Cell Environ. 2010;33:370–81.PubMedView ArticleGoogle Scholar
- Bashir K, Ishimaru Y, Nishizawa NK. Iron uptake and loading into rice grains. Rice. 2010;3:122–30.View ArticleGoogle Scholar
- Bashir K, Nishizawa NK. Deoxymugineic Acid synthase; a gene important for Fe-Acquisition and homeostasis. Plant Signal Behav. 2006;1:290–2.PubMedPubMed CentralView ArticleGoogle Scholar
- Bashir K, Inoue H, Nagasaka S, Takahashi M, Nakanishi H, Mori S, et al. Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J Biol Chem. 2006;281:32395–402.PubMedView ArticleGoogle Scholar
- Berg JM, Shi Y. The galvanization of biology: a growing appreciation for the roles of zinc. Science. 1996;271:1081–5.PubMedView ArticleGoogle Scholar
- Cakmak I. Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil. 2008;302:1–17.View ArticleGoogle Scholar
- Cakmak I, Kalayci M, Ekiz H, Braun HJ, Yilmaz A. Zinc deficiency as an actual problem in plant and human nutrition in Turkey: a NATO-Science for Stability Project. Field Crops Res. 1999;60:175–88.View ArticleGoogle Scholar
- Cakmak I, Gulut KY, Marschner H, Graham RD. Effect of zinc and iron deficiency on phytosiderophore release in wheat genotypes differing in zinc deficiency. J Plant Nutr. 1994;17:1–17.View ArticleGoogle Scholar
- Connolly EL, Fett JP, Guerinot ML. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell. 2002;14:1347–57.PubMedPubMed CentralView ArticleGoogle Scholar
- Curie C, Panavience Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL. Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature. 2001;409:346–9.PubMedView ArticleGoogle Scholar
- Eide D, Broderius M, Fett J, Guerinot ML. A novel iron regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA. 1996;93:5624–8.PubMedPubMed CentralView ArticleGoogle Scholar
- Eide D. The molecular biology of metal ion transport in Saccharomyces cerevisiae. Annu Rev Nutr. 1998;18:441–69.PubMedView ArticleGoogle Scholar
- Graham R, Senadhira D, Beebe S, Iglesias C, Monasterio I. Breeding for micronutrient density in edible portions of staple food crops: conventional approaches. Field Crops Res. 1999;60:57–80.View ArticleGoogle Scholar
- Graham RD, Welch RM. Breeding for staple-food crops with high micronutrient density: working Papers on Agricultural Strategies for Micronutrients, No.3. Washington DC: International Food Policy Institute; 1996.Google Scholar
- 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 USA. 1998;95:7220–4.PubMedPubMed CentralView ArticleGoogle Scholar
- Guerinot ML. The ZIP family of metal transporters. Biochim Biophys Acta. 2000;1465:190–8.PubMedView ArticleGoogle Scholar
- Hambidge M. Human zinc deficiency. J Nutr. 2000;130:1344S–9.PubMedGoogle Scholar
- Herbik A, Koch G, Mock HP, Dushkov D, Czihal A, Thielmann J, et al. Isolation, characterization and cDNA cloning of nicotianamine synthase from barley. A key enzyme for iron homeostasis in plants. Eur J Biochem. 1999;265:231–9.PubMedView ArticleGoogle Scholar
- Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S. Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol. 1999;119:471–9.PubMedPubMed CentralView ArticleGoogle Scholar
- Higuchi K, Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S. Analysis of transgenic rice containing barley nicotianamine synthase gene. Soil Sci Plant Nutr. 2001a;47:315–22.View ArticleGoogle Scholar
- Higuchi K, Watanabe S, Takahashi M, Kawasaki S, Nakanishi H, Nishizawa NK, et al. Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. Plant J. 2001b;25:159–67.View ArticleGoogle Scholar
- Inoue H, Higuchi K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in long-distance transport of iron and differentially regulated by iron. Plant J. 2003;36:366–81.PubMedView ArticleGoogle Scholar
- Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, et al. Rice OsYSL15 is an iron-regulated iron(iii)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem. 2009;284:3470–9.PubMedView ArticleGoogle Scholar
- Inoue H, Takahashi M, Kobayashi T, Suzuki M, Nakanishi H, Mori S, et al. Identification and localisation of the rice nicotianamine aminotransferase gene OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Mol Biol. 2008;66:193–203.PubMedView ArticleGoogle Scholar
- Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, et al. Rice metal-nicotianamine transporter, OsYSL2, is required for long distance transport of iron and manganese. Plant J. 2010;62:379–90.PubMedView ArticleGoogle Scholar
- Ishimaru Y, Masuda H, Suzuki M, Bashir K, Takahashi M, Nakanishi H, et al. Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. J Exp Bot. 2007;58:2909–15.PubMedView ArticleGoogle Scholar
- Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, et al. OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot. 2005;56:3207–14.PubMedView ArticleGoogle Scholar
- Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, et al. Rice plants take up iron as an Fe3+−phytosiderophore and as Fe2+. Plant J. 2006;45:335–46.PubMedView ArticleGoogle Scholar
- Kobayashi T, Nakanishi H, Takahashi M, Kawasaki S, Nishizawa NK, Mori S. In vivo evidence that Ids3 from Hordeum vulgare encodes a dioxygenase that converts 2′-deoxymugineic acid to mugineic acid in transgenic rice. Planta. 2001;212:864–71.PubMedView ArticleGoogle Scholar
- Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, et al. OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J. 2004;39:415–24.PubMedView ArticleGoogle Scholar
- Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB. The IRT1 protein from Arabidopsis thaliana is a metal transporter with broad specificity. Plant Mol Biol. 1999;40:37–44.PubMedView ArticleGoogle Scholar
- Lee S, Jeong HJ, Kim SA, Lee J, Guerinot ML, An G. OsZIP5 is a plasma membrane zinc transporter in rice. Plant Mol Biol. 2010;73:507–17.PubMedView ArticleGoogle Scholar
- Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, et al. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 2001;126:1646–67.PubMedPubMed CentralView ArticleGoogle Scholar
- Masuda H, Suzuki M, Morikawa KC, Kobayashi T, Nakanishi H, Takahashi M, et al. Increase in iron and zinc concentrations in rice grains via the introduction of barley genes involved in phytosiderophore synthesis. Rice. 2008;1:100–8.View ArticleGoogle Scholar
- Masuda H, Usuda K, Kobayashi T, Ishimaru Y, Kakei Y, Takahashi M, et al. Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice. 2009;2:155–66.View ArticleGoogle Scholar
- Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, et al. GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem. 2002;15:4738–46.View ArticleGoogle Scholar
- Mori S, Nishizawa NK. Methionine as a dominant precursor of phytosiderophores in Graminaceae plants. Plant Cell Physiol. 1987;28:1081–92.Google Scholar
- Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T. A specific transporter for iron(III)–phytosiderophore in barley roots. Plant J. 2006;46:563–72.PubMedView ArticleGoogle Scholar
- Nagarathna TK, Shankar AG, Udayakumar M. Assessment of genetic variation in zinc acquisition and transport to seed in diversified germplasm lines of rice (Oryza sativa L.). J Agric Tech. 2010;6:171–8.Google Scholar
- Nakanishi H, Okumura N, Umehara Y, Nishizawa NK, Chino M, Mori S. Expression of a gene specific for iron deficiency (Ids3) in the roots of Hordeum vulgare. Plant Cell Physiol. 1993;34:401–10.PubMedGoogle Scholar
- Nakanishi H, Yamaguchi H, Sasakuma T, Nishizawa NK, Mori S. Two dioxygenase genes, Ids3 and Ids2, from Hordeum vulgare are involved in the biosynthesis of muginetic acid family phytosiderophores. Plant Mol Biol. 2000;44:199–207.PubMedView ArticleGoogle Scholar
- Neue HU, Quijano C, Senadhira D, Setter T. Strategies for dealing with micronutrient disorders and salinity in lowland rice systems. Field Crops Res. 1998;56:139–55.View ArticleGoogle Scholar
- Nozoye T, Inoue H, Takahashi M, Ishimaru Y, Nakanishi H, Mori S, et al. The expression of iron homeostasis-related genes during rice germination. Plant Mol Biol. 2007;64:35–47.PubMedView ArticleGoogle Scholar
- Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, et al. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem. 2011;286(7):5446–54.PubMedPubMed CentralView ArticleGoogle Scholar
- Okumura N, Nishizawa NK, Umehara Y, Ohata T, Nakanishi H, Yamaguchi T, et al. A dioxygenase gene (Ids2) expressed under iron deficiency conditions in the roots of Hordeum vulgare. Plant Mol Biol. 1994;25:705–19.PubMedView ArticleGoogle Scholar
- Pedas P, Husted S. Zinc transport mediated by barley ZIP proteins are induced by low pH. Plant Signal Behav. 2009;4:842–5.PubMedPubMed CentralView ArticleGoogle Scholar
- Peng GX, FuSuo Z, Hoffland E. Malate exudation by six aerobic rice genotypes varying in zinc uptake efficiency. J Environ Qual. 2009;38:2315–21.View ArticleGoogle Scholar
- Ramesh SA, Shin R, Eide DJ, Schachtman DP. Defferential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiol. 2003;133:126–34.PubMedPubMed CentralView ArticleGoogle Scholar
- Refuerzo L, Mercado EF, Arceta M, Sajese AG, Gregorio G, Singh RK. QTL mapping for zinc deficiency tolerance in rice (Oryza sativa L.). Philipp J Crop Sci. 2009;34:86.Google Scholar
- Rhodes D, Klug A. Zinc fingers. Sci Am. 1993;268:56–65.PubMedView ArticleGoogle Scholar
- Roberts LA, Pierson AJ, Panaviene Z, Walker EL. Yellow stripe1. Expanded roles for the maize iron–phytosiderophore transporter. Plant Physiol. 2004;135:112–20.PubMedPubMed CentralView ArticleGoogle Scholar
- Rogers EE, Eide DJ, Guerinot ML. Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA. 2000;97:12356–60.PubMedPubMed CentralView ArticleGoogle Scholar
- Ruel MT, Bouis HE. Plant breeding: a long-term strategy for the control of zinc deficiency in vulnerable populations. Am J Clin Nutr Suppl. 1998;68:488S–94.Google Scholar
- Sarret G, Balesdent J, Bouziri L, Garnier JM, Marcus MA, Geoffroy N, et al. Zn speciation in the organic horizon of a contaminated soil by micro-X-ray fluorescence, micro- and powder-EXAFS spectroscopy, and isotopic dilution. Environ Sci Technol. 2004;38:2792–801.PubMedView ArticleGoogle Scholar
- Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wirén N. ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem. 2004;279:9091–6.PubMedView ArticleGoogle Scholar
- Suzuki M, Takahashi M, Tsukamoto T, Watanabe S, Matsuhashi S, Yazaki J, et al. Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. Plant J. 2006;48:85–97.PubMedView ArticleGoogle Scholar
- Suzuki M, Morikawa KC, Nakanishi H, Takahashi M, Saigusa M, Mori S, et al. Transgenic rice lines that include barley genes have increased tolerance to low iron availability in a calcareous paddy soil. Soil Sci Plant Nutr. 2008a;54:77–85.View ArticleGoogle Scholar
- Suzuki M, Tsukamoto T, Inoue H, Watanabe S, Matsuhashi S, Takahashi M, et al. Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Mol Biol. 2008b;66:609–17.View ArticleGoogle Scholar
- Takahashi M, Nozoye T, Kitajima B, Fukuda N, Hokura N, Terada Y, et al. In vivo analysis of metal distribution and expression of metal transporters in rice seed during germination process by microarray and X-ray Fluorescence Imaging of Fe, Zn, Mn, and Cu. Plant Soil. 2009;325:39–51.View ArticleGoogle Scholar
- Takahashi M, Yamaguchi H, Nakanishi H, Shioiri T, Nishizawa NK, Mori S. Cloning two genes for nicotianamine aminotransferase, a criticalenzyme in iron acquisition (strategy II) in graminaceous plants. Plant Physiol. 1999;121:947–56.PubMedPubMed CentralView ArticleGoogle Scholar
- Usuda K, Wada Y, Ishimaru Y, Kobayashi T, Takahashi M, Nakanishi H, et al. Genetically engineered rice containing larger amounts of nicotianamine to enhance the antihypertensive effect. Plant Biotech J. 2009;7:87–95.View ArticleGoogle Scholar
- Vallee BL, Falchuk KH. The biochemical basis of zinc physiology. Physiol Rev. 1993;73:79–118.PubMedGoogle Scholar
- Vert G, Briatt JF, Curie C. Arabidopsis IRT2 gene encodes a root periphery iron transporter. Plant J. 2001;26:181–9.PubMedView ArticleGoogle Scholar
- Vert G, Grotz N, DeÂdaldeÂchamp F, Gaymard F, Guerinot ML, Briat JF, et al. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell. 2002;14:1223–33.PubMedPubMed CentralView ArticleGoogle Scholar
- Walter A, Romheld V, Marschner H, Mori S. Is the release of phytosiderophores in zinc-deficient wheat plants a response to impaired iron utilization? Physiol Plant. 1994;92:493–500.View ArticleGoogle Scholar
- Welch RM, Graham RD. A new paradigm for world agriculture: meeting human needs: productive, sustainable, nutritious. Field Crops Res. 1999;60:1–10.View ArticleGoogle Scholar
- Welch RM. Micronutrient nutrition of plants. Crit Rev Plant Sci. 1995;14:49–82.View ArticleGoogle Scholar
- Widodo, Broadley MR, Rose T, Frei M, Tanaka JP, Yoshihashi T, et al. Response to zinc deficiency of two rice lines with contrasting tolerance is determined by root growth maintenance and organic acid exudation rates, and not by zinc-transporter activity. New Phytol. 2010;186:400–14.PubMedView ArticleGoogle Scholar
- Wintz H, Fox T, Wu YY, Feng V, Chen W, Chang HS, et al. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem. 2003;28:47644–53.View ArticleGoogle Scholar
- Wissuwa M, Ismail AM, Graham RD. Rice grain zinc concentrations as affected by genotype, native soil-zinc availability, and zinc fertilization. Plant Soil. 2008;306:37–48.View ArticleGoogle Scholar
- Wissuwa M, Ismail AM, Yanagihara S. Effects of zinc deficiency on rice growth and genetic factors contributing to tolerance. Plant Physiol. 2006;142:731–41.PubMedPubMed CentralView ArticleGoogle Scholar
- Wu YF, Huang JW, Sinclair BR, Powers L. The structure of the zinc sites of Escherichia coli DNA-dependent RNA polymerase. J Biol Chem. 1992;267:25560–7.PubMedGoogle Scholar
- Wu YF, Wu WC. Zinc in DNA replication and transcription. Annu Rev Nutr. 1989;7:251–72.View ArticleGoogle Scholar
- Yang X, Huang J, Jiang Y, Zhang HS. Cloning and functional identification of two members of the ZIP (Zrt, Irt-like protein) gene family in rice (Oryza sativa L.). Mol Biol Rep. 2009;36:281–7.PubMedView ArticleGoogle Scholar
- Yang X, Ye ZQ, Shi CH, Zhu ML, Graham RD. Genotypic differences in concentrations of iron, manganese, copper, and zinc in polished rice grains. J Plant Nutr. 1998;21:1453–62.View ArticleGoogle Scholar
- Zhang F, Romheld V, Marschner H. Effect of zinc deficiency in wheat on the release of zinc and iron mobilizing root exudates. Pflanzenernahr Bodenk. 1989;152:205–10.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution and reproduction in any medium, provided the original author(s) and source are credited.