Iron uptake, translocation, and regulation in higher plants

For all plants to survive and grow, iron is necessary. The reduction strategy-I of nongraminaceous plants and the chelation strategy-II of graminaceous plants are two different ways that higher plants have evolved to obtain iron, which is only marginally soluble, from the rhizosphere. Both techniques’ essential molecular elements, such as transporters, enzymes and chelators, have been elucidated. Many of these elements are now believed to also work inside the plant to promote internal iron transport. Also being clarified are the transporters involved in intracellular iron trafficking. The bulk of the genes that encode these components are transcriptionally regulated in response to iron availability.

Iron is essential for the survival and proliferation of all plants. Higher plants have developed two distinct strategies to acquire iron, which is only slightly soluble, from the rhizosphere: the reduction strategy of nongraminaceous plants and the chelation strategy of graminaceous plants. Key molecular components-including transporters, enzymes, and chelators-have been clarified for both strategies, and many of these components are now thought to also function inside the plant to facilitate internal iron transport. Transporters for intracellular iron trafficking are also being clarified. A majority of genes encoding these components are transcriptionally regulated in response to iron availability. Recent research has uncovered central transcription factors, cis-acting elements, and molecular mechanisms regulating these genes. Manipulation of these molecular components has produced transgenic crops with enhanced tolerance to iron deficiency or with increased iron content in the edible parts.

The application of 57Fe Mössbauer spectroscopy in the investigation of iron uptake and translocation in plants

The quest for selective Cs+ transport in plants

The aim of this review article is to explore and establish the current status of 2-deoxy-2-fluoro-D-glucose (FDG) applications in plant imaging. In the present article, we review the previous literature on its experimental merits to formulate a consistent and inclusive picture of FDG applications in plant-imaging research. 2-deoxy-2-fluoro-D-glucose is a [18F]fluorine-labeled glucose analog in which C-2 hydroxyl group has been replaced by a positron-emitting [18F] radioisotope. As FDG is a positron-emitting radiotracer, it could be used in in vivo imaging studies. FDG mimics glucose chemically and structurally. Its uptake and distribution are found to be similar to those of glucose in animal models. FDG is commonly used as a radiotracer for glucose in medical diagnostics and in vivo animal imaging studies but rarely in plant imaging. Tsuji et al. (2002) first reported FDG uptake and distribution in tomato plants. Later, Hattori et al. (2008) described FDG translocation in intact sorghum plants and suggested that it could be used as a tracer for photoassimilate translocation in plants. These findings raised interest among other plant scientists, which has resulted in a recent surge of articles involving the use of FDG as a tracer in plants. There have been seven studies describing FDG-imaging applications in plants. These studies describe FDG applications ranging from monitoring radiotracer translocation to analyzing solute transport, root uptake, photoassimilate tracing, carbon allocation, and glycoside biosynthesis. Fatangare et al. (2015) recently characterized FDG metabolism in plants; such knowledge is crucial to understanding and validating the application of FDG in plant imaging research. Recent FDG studies significantly advance our understanding of FDG translocation and metabolism in plants but also raise new questions. Here, we take a look at all the previous results to form a comprehensive picture of FDG translocation, metabolism, and applications in plants. In conclusion, we summarize current knowledge, discuss possible implications and limitations of previous studies, point to open questions in the field, and comment on the outlook for FDG applications in plant imaging.

Isotope technique including radioisotopes and stable isotopes is useful and potent tool for various scientific areas. Especially, enriched stable isotopes are indispensable tools for researchers in biological systems (Sturup et al. 2008). Stable isotope ratios are usually used in examining the biogeochemical cycling of light elements such as carbon(C), oxygen (O), nitrogen (N) and sulphur (S) in the environment. Thermal ionization mass spectrometry (TIMS) for the isotope analysis has been the most standard technique for many years. However, for TIMS analysis, time for sample preparation is needed because sample need to ensure efficient ionization. On the other hand, ICP-MS analysis has some advantages that sample preparation is simple and high sample throughput for isotope experiments where a large amount of samples need to be analyzed (Sturup et al. 2008). The disadvantage to resolve in isotope analysis using ICP-MS is spectroscopic interferences in the process of analysis. It is therefore needed to be resolved these interferences. When plant physiologists investigate mineral absorption mechanisms in roots of plant, evaluation of symplastic mineral absorption capacity in roots cell in kinetics and time course experiments is very important because mineral translocation in shoots is mainly contributed to capacity of symplastic absorption in roots. In these experiments, radioisotopes methods are mainly used for element uptake in plants. Radioisotopes in solute were the most useful markers used in nutrient uptake and translocation in plants because they are chemically similar to the solute and can be distinguished from non-labeled solutes already contained in the roots (Davenport 2007). However, there are limitations to this method, including radioisotope administrative restriction and the restricted half-life of the radioisotope. Isotope tracer experiments, using a stable isotope, are very similar to those using a radioisotope on element to analyse plant mechanisms (Sturup et al. 2008). Accurate and precise determination of mineral isotope ratios is required for analysis of enriched stable isotopes. Inductive coupled plasma mass spectrometry (ICP-MS) has now become the effective and potent technique for enriched stable isotope tracer experiments due to increased availability. Therefore, the application of enriched stable isotopes in various biological systems increased rapidly.

The ability of a quadrupole-based ICP-MS with an octopole collision cell to obtain precise and accurate measurements of isotope ratios of magnesium, calcium and potassium was evaluated. Hydrogen and helium were used as collision/reaction gases for ICP-MS isotope ratio measurements of calcium and potassium in order to avoid isobaric interference with the analyte ions from (mainly) argon ions 40Ar+ and argon hydride ions 40Ar1H+. Mass discrimination factors determined for the isotope ratios 25Mg/24Mg, 40Ca/44Ca and 39K/41K under optimized experimental conditions varied between 0.044 and 0.075. The measurement precisions for 25Mg/24Mg, 40Ca/44Ca and 39K/41K were found to be 0.09%, 0.43% and 1.4%, respectively. This analytical method that uses ICP-QMS with a collision cell to obtain isotope ratio measurements of magnesium, calcium and potassium was used in routine mode to characterize biological samples (nutrient solution and small amounts of digested plant samples). The mass spectrometric technique was employed to study the dynamics of nutrient uptake and translocation in barley plants at different root temperatures (10 degrees C and 20 degrees C) using enriched stable isotopes (25Mg, 44Ca and 41K) as tracers. For instance, the mass spectrometric results of tracer experiments demonstrated enhanced 25Mg and 44Ca uptake and translocation into shoots at a root temperature of 20 degrees C 24 h after isotope spiking. In contrast, results obtained from 41K tracer experiments showed the highest 41K contents in plants spiked at a root temperature of 10 degrees C.

Despite the usually high abundance of iron (Fe) in soils, the low solubility of Fe‐bearing minerals restricts the available Fe pools in most aerobic soils to levels that are far below those required for microbial or plant growth. To acquire the necessary amounts of Fe from the environment, organisms have evolved mechanisms that enhance the solubility and dissolution rate of Fe(iii) oxyhydroxides prevailing in aerobic soils. Chemically, these mechanisms are based on weakening of the Fe–O bond by reduction, chelation and protonation. Physiologically, two distinct and in all known cases mutually exclusive strategies can be distinguished: the excretion of siderophores capable of solubilizing external ferric Fe and subsequent uptake of the ferric siderophore complex; and reduction of Fe(iii) prior to uptake of the more soluble Fe2+ ion. With the exception of graminaceous species, in which Fe uptake is based on the former mechanism, the latter strategy is found in all cormophytes and certain algae, yeast and bacteria. In higher plants, the increase in their capacity to convert extracellular ferric to ferrous Fe is part of a series of physiological and morphological events that act in concert to achieve appropriate internal levels of Fe. It is this amalgam of features that determines the Fe efficiency of a species or cultivar that in turn affects the yield of economically important plants and the natural distribution of species. Adaptive changes to limited Fe availability have been studied at the molecular, physiological and whole‐plant level. This review summarises current knowledge of the components of reduction‐based Fe uptake in plants and presents an integrated view of the present understanding of mechanisms that control the rate and extent of Fe absorption by roots.

Mining iron: Iron uptake and transport in plants

Methylglycinediacetic acid (MGDA) is a readily biodegradable complexing agent in compliance with Organization for Economic Cooperation and Development standards. In the present study, the use of MGDA for iron (Fe) and arsenic (As) bioavailability and uptake by rice plants (Oryza sativa L.) was investigated. The highest plant biomass was observed at pH 7, and the growth of rice seedlings decreased significantly (p < 0.05) with increasing pH of the nutrient solution. This might be due to Fe deficiency to the plant at alkaline pH. When rice seedlings were grown with different concentrations of MGDA (0.1, 0.25, 0.5, 1.0, 2.5, and 5 mM), the highest plant biomass was observed at 0.25 mM MGDA, while further increases of the ligand concentration decreased the plant growth. Fe concentrations on rice root surfaces decreased gradually with increasing MGDA concentrations in the growing medium, while Fe concentrations in rice roots and shoots increased with increasing MGDA concentrations up to 0.25 mM and then decreased gradually. This indicates that the concentration of the chelating ligand influences Fe uptake in the plant. Arsenic concentrations on rice root surfaces decreased, while As concentrations in roots and shoots increased with the addition of MGDA in the growing medium, indicating that the ligand enhanced As bioavailability and uptake in rice. The mechanism behind the MGDA effect on Fe and As uptake in plant is likely to be due to that Fe exists mostly in insoluble particulate forms [e.g., ferric oxide (Fe2O3), ferric hydroxide (Fe(OH)3) and ferric oxyhydroxide (FeOOH)] at neutral or alkaline pH, and the soluble [e.g., ferric ion (Fe3+), iron hydroxide ion (Fe(OH)2+) and iron dihydroxide ion ()] and apparently soluble (colloidal) fractions of Fe are increased at moderate concentrations of the ligand that increases Fe bioavailability. Since arsenate [As(V)] binds to the insoluble Fe-oxides/hydroxides, the binding sites for As(V) decreases with the increase of the soluble fractions of Fe by the ligand, which slightly increased As uptake in rice plants.

Iron uptake and translocation in plants are important processes for both plant and human nutrition, whereas relatively little is known about the molecular mechanisms of iron transport within the plant body. Several reports have shown that yellow stripe 1 (YS1) and YS1-like (YSL) transporters mediate metal-phytosiderophore uptake and/or metal-nicotianamine translocation. Among the 18 YSL genes in rice (OsYSLs), OsYSL18 is predicted to encode a polypeptide of 679 amino acids containing 13 putative transmembrane domains. An OsYSL18-green fluorescent protein (GFP) fusion was localized to the plasma membrane when transiently expressed in onion epidermal cells. Electrophysiological measurements using Xenopus laevis oocytes showed that OsYSL18 transports iron(III)–deoxymugineic acid, but not iron(II)–nicotianamine, zinc(II)–deoxymugineic acid, or zinc(II)–nicotianamine. Reverse transcriptase PCR analysis revealed more OsYSL18 transcripts in flowers than in shoots or roots. OsYSL18 promoter-β-glucuronidase (GUS) analysis revealed that OsYSL18 was expressed in reproductive organs including the pollen tube. In vegetative organs, OsYSL18 was specifically expressed in lamina joints, the inner cortex of crown roots, and phloem parenchyma and companion cells at the basal part of every leaf sheath. These results suggest that OsYSL18 is an iron-phytosiderophore transporter involved in the translocation of iron in reproductive organs and phloem in joints.

Iron is an essential element needed by all organisms for growth and development. Because iron becomes toxic at higher concentrations iron is under homeostatic control. Plants face also the problem that iron in the soil is tightly bound to oxygen and difficult to access. Plants have therefore developed special mechanisms for iron uptake and regulation. During the last years key components of plant iron regulation have been identified. How these components integrate and maintain robust iron homeostasis is presently not well understood. Here we use a computational approach to identify mechanisms for robust iron homeostasis in non-graminaceous plants. In comparison with experimental results certain control arrangements can be eliminated, among them that iron homeostasis is solely based on an iron-dependent degradation of the transporter IRT1. Recent IRT1 overexpression experiments suggested that IRT1-degradation is iron-independent. This suggestion appears to be misleading. We show that iron signaling pathways under IRT1 overexpression conditions become saturated, leading to a breakdown in iron regulation and to the observed iron-independent degradation of IRT1. A model, which complies with experimental data places the regulation of cytosolic iron at the transcript level of the transcription factor FIT. Including the experimental observation that FIT induces inhibition of IRT1 turnover we found a significant improvement in the system’s response time, suggesting a functional role for the FIT-mediated inhibition of IRT1 degradation. By combining iron uptake with storage and remobilization mechanisms a model is obtained which in a concerted manner integrates iron uptake, storage and remobilization. In agreement with experiments the model does not store iron during its high-affinity uptake. As an iron biofortification approach we discuss the possibility how iron can be accumulated even during high-affinity uptake.

Purified pseudobactin inhibits the uptake of ferric iron by the roots of peas and maize plants sufficiently to reduce the synthesis of chlorophyll. This inhibition is interpreted as competitive binding, as described for synthetic chelating compounds.

Calcium (Ca) and the toxic heavy metal cadmium (Cd) are antagonistic ions competing for uptake in plants when they co-occur in soil solutions, and high Ca concentrations can reduce the uptake of Cd in plants. However, less is known about the effects of low Ca bioavailability on Cd uptake and translocation in plants. We hypothesized that low Ca availability would enhance Cd uptake and translocation in Sesbania sesban, a fast-growing shrub potentially useful for Cd removal from contaminated soils, and Brassica juncea, a well-known Cd-hyperaccumulator. The two species were grown under controlled conditions for 21 days in hydroponic nutrient solutions with either 0.2 or 2 mM Ca and 0 or 50 µM Cd in a 2 × 2 factorial experimental design. Both species had a lower relative growth rate, final root length and shoot and root biomasses at 50 µM Cd compared with growth without Cd. The negative effects of Cd on both species were exacerbated at low Ca availability. Brassica juncea had higher root Cd concentrations than S. sesban, but the shoot Cd concentrations did not differ between the two species. The low Ca concentration enhanced the uptake of Cd in the roots of both species, but Cd translocation to the shoots was low, especially at 0.2 mM Ca. We conclude that the low Ca concentration enhanced the uptake of Cd into roots of S. sesban and B. juncea and increased the phytotoxicity of Cd. The translocation of Cd to the shoots of the two species was, however, lower at 0.2 mM than at 2 mM Ca, implying that Cd removal from polluted soil cannot simply be increased by adjusting ion concentrations.

It has been well recognized that microbes can assist phytoremediation of lead (Pb) by promoting plant growth and metal uptake. However, little is known about the potential of soil inoculation with actinomycetes to enhance Pb uptake and translocation in plants, particularly in semi-arid water-deficient areas. This study was focused on exploring the resistance of a soil actinomycete strain (Streptomyces pactum Act12) to Pb and its effects on plant growth, antioxidant responses, Pb uptake and translocation in perennial ryegrass (Lolium perenne L.). Special attention was given to experimental conditions in semi-arid area in Northerwest China. A fermentation culture of Act12 was applied in powder form to soil with or without Pb treatment (0–1,000 mg kg-1), and ryegrass plants were immediately grown in this soil, in pots, for 60 days under 20% relative soil moisture. Act12 showed tolerance to up to 1,200 mg Pb L-1 in plate culture and well colonized the soil containing less than 500 mg Pb kg-1. Under Pb stress, inoculated plants had higher biomass with greater plant height and root tiller number than the uninoculated controls. Additionally, higher catalase, superoxide dismutase and peroxidase activities were detected in leaves of inoculated plants under Pb stress. Inoculating soil with Act12 significantly increased Pb concentrations and uptake in plants grown in soil containing 200 to 1,000 mg Pb kg-1. The translocation and bioconcentration factors of inoculated plants were 10.5–36.2% and 37.3–133.1% higher than uninoculated plants, respectively. Streptomyces pactum Act12 can enhance Pb phytoremediation by perennial ryegrass and its powder form facilitates the use in semi-arid areas.