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.
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