Role and influence of mycorrhizal fungi on radiocesium accumulation by plants

This review summarizes current knowledge on the contribution of mycorrhizal fungi to radiocesium immobilization and plant accumulation. These root symbionts develop extended hyphae in soils and readily contribute to the soil-to-plant transfer of some nutrients. Available data show that ecto-mycorrhizal (ECM) fungi can accumulate high concentration of radiocesium in their extraradical phase while radiocesium uptake and accumulation by arbuscular mycorrhizal (AM) fungi is limited. Yet, both ECM and AM fungi can transport radiocesium to their host plants, but this transport is low. In addition, mycorrhizal fungi could thus either store radiocesium in their intraradical phase or limit its root-to-shoot translocation. The review discusses the impact of soil characteristics, and fungal and plant transporters on radiocesium uptake and accumulation in plants, as well as the potential role of mycorrhizal fungi in phytoremediation strategies.     

Effect of potassium and phosphorus on the transport of radiocesium by arbuscular mycorrhizal fungi

Potassium, a chemical analogue of cesium, and phosphorus, an essential macronutrient transported by arbuscular mycorrhizal fungi (AMF), have been suggested to influence the transport of radiocesium by AMF. However, no study investigated the effects of increasing concentrations of both elements on the importance of this transport. Here, the arbuscular mycorrhizal-plant (AM-P) in vitro culture system associating Medicago truncatula plantlets with Glomus intraradices was used to evaluate this effect.Using three concentrations of K (0, 1, 10 mM) and two concentrations of P (30 and 3000 μM) added to a compartment only accessible to the AMF, we demonstrated that K and P individually and in combination significantly influenced radiocesium transport by AMF. Whilst increased concentration of K decreased the amount of radiocesium transported, the opposite was observed for P. Although the exact mechanisms involved need to be assessed, both elements were identified as important factors influencing the transport of radiocesium by AMF.     

Environmental processes affecting plant root uptake of radioactive trace elements and variability of transfer factor data: a review

Soil-to-plant transfer factors are commonly used to estimate the food chain transfer of radionuclides. Their definition assumes that the concentration of a radionuclide in a plant relates linearly solely to its average concentration in the rooting zone of the soil. However, the large range of transfer factors reported in the literature shows that the concentration of a radionuclide in a soil is not the only factor influencing its uptake by a plant. With emphasis on radiocesium and -strontium, this paper reviews the effects of competition with major ions present in the soil-plant system, the effects of rhizosphere processes and soil micro-organisms on bioavailability, the factors influencing transport to and uptake by roots and the processes affecting long-term uptake rates. Attention is given to summarizing the results of recent novel electrophysiological and genetic techniques which provide a physiologically based understanding of the processes involved in the uptake and translocation of radiocesium and -strontium by plants.     

The role of fungi in the transfer and cycling of radionuclides in forest ecosystems

Fungi are one of the most important components of forest ecosystems, since they determine to a large extent the fate and transport processes of radionuclides in forests. They play a key role in the mobilization, uptake and translocation of nutrients and are likely to contribute substantially to the long-term retention of radiocesium in organic horizons of forest soil. This paper gives an overview of the role of fungi regarding the transfer and cycling of nutrients and radionuclides, with special emphasis on mycorrhizal symbiosis. Common definitions of transfer factors, soil-fungus and soil-green plant, including their advantages and limitations. are reviewed. Experimental approaches to quantify the bioavailability of radionuclides in soil and potential long-term change are discussed.     

Radiocesium contamination behavior and its effect on potassium absorption in tropical or subtropical plants

The accumulation and long-term decline of radiocesium contamination in tropical plant species was studied through measurements of gamma-ray spectra from pomegranate (Punica granatum) and chili pepper (Capsicum fructescens) trees. The plants were originally grown at a (137)Cs contaminated site (where a radiological accident occurred in the city of Goiania, Brazil, in 1987), and transplanted to uncontaminated soil, so that the main source of contamination of the new leaves and fruits would be the fraction of the available radiocesium in the body of the plants. Measurements of (137)Cs and (40)K concentrations along the roots, main trunk, twigs, leaves and fruits before and after the transplant process of both plant species indicated a direct competition between Cs and K ions, suggesting that these elements could have a common accumulation mechanism. Cesium transfer factors from soil to pomegranate, green and red chili pepper fruits were evaluated as 0.4 +/- 0.1, 0.06 +/- 0.01 and 0.05 +/- 0.01, respectively. Biological half-life values due to (137)Cs translocation from the tree reservoir (BHL(T)) were calculated as 0.30 years for pomegranate, 0.12 years and 0.07 years for red and green peppers, respectively.     

Mycorrhizal association of maritime pine, Pinus pinaster, with Rhizopogon roseolus has contrasting effects on the uptake from soil and root-to-shoot transfer of 137Cs, 85Sr and 95mTc

The beneficial role of mycorrhizal association on plant nutrition and water supply is well-known, however, very little information exists with respect to the availability of radionuclides. We have measured the effect of controlled mycorrhizal association on the root uptake from soil and accumulation in leaves of three radionuclides. The radionuclides have contrasting chemical and biological properties: Cs is strongly adsorbed on soil, has no biological role and is a close analogue of potassium; Sr is less strongly adsorbed on soil and behaves very similarly to calcium; and Tc is very mobile in soil as pertechnetate, but immobilised when reduced to Tc(IV), it is also considered to be easily assimilated by biological systems. We found that mycorrhizal association had no effect on root-to-needle transfer of Cs, but increased root uptake and that this increase could not be explained by improved potassium nutrition. In contrast, the symbiotic relation decreased Tc soil-to-needle transfer, but this resulted from complex dynamics of root uptake and rapid immobilisation of Tc in soil. No effect of mycorrhizal association on Sr, like its stable analogue Ca, was observed. The addition of a phytotoxic metal, Cu, inhibited mycorrhizal association, thus eliminating the effects observed for non-contaminated plant-fungus couples, but had no additional effect on radionuclide dynamics.     

Selenium bioavailability and uptake as affected by four different plants in a loamy clay soil with particular attention to mycorrhizae inoculated ryegrass

The aim of this study was to investigate the influence of plant species, especially of their rhizosphere soil, and of inoculation with an arbuscular mycorrhizal (AM) fungus on the bioavailability of selenium and its transfer in soil-plant systems. A pot experiment was performed with a loamy clay soil and four plant species: maize, lettuce, radish and ryegrass, the last one being inoculated or not with an arbuscular mycorrhizal fungus (Glomus mosseae). Plant biomass and Se concentration in shoots and roots were estimated at harvest. Se bioavailability in rhizosphere and unplanted soil was evaluated using sequential extractions. Plant biomass and selenium uptake varied with plant species. The quantity of rhizosphere soil also differed between plants and was not proportional to plant biomass. The highest plant biomass, Se concentration in plants, and soil to plant transfer factor were obtained with radish. The lowest Se transfer factors were obtained with ryegrass. For the latter, mycorrhizal inoculation did not significantly affect plant growth, but reduced selenium transfer from soil to plant by 30%. In unplanted soil after 65 days aging, more than 90% of added Se was water-extractable. On the contrary, Se concentration in water extracts of rhizosphere soil represented less than 1% and 20% of added Se for ryegrass and maize, respectively. No correlation was found between the water-extractable fraction and Se concentration in plants. The speciation of selenium in the water extracts indicated that selenate was reduced, may be under organic forms, in the rhizosphere soil.     

An overview of BORIS: Bioavailability of Radionuclides in Soils

The ability to predict the consequences of an accidental release of radionuclides relies mainly on the level of understanding of the mechanisms involved in radionuclide interactions with different components of agricultural and natural ecosystems and their formalisation into predictive models. Numerous studies and databases on contaminated agricultural and natural areas have been obtained, but their use to enhance our prediction ability has been largely limited by their unresolved variability. Such variability seems to stem from incomplete knowledge about radionuclide interactions with the soil matrix, soil moisture, and biological elements in the soil and additional pollutants, which may be found in such soils. In the 5th European Framework Programme entitled Bioavailability of Radionuclides in Soils (BORIS), we investigated the role of the abiotic (soil components and soil structure) and biological elements (organic compounds, plants, mycorrhiza, and microbes) in radionuclide sorption/desorption in soils and radionuclide uptake/release by plants. Because of the importance of their radioisotopes, the bioavailability of three elements, caesium, strontium, and technetium has been followed. The role of one additional non-radioactive pollutant (copper) has been scrutinised in some cases. Role of microorganisms (e.g., K(d) for caesium and strontium in organic soils is much greater in the presence of microorganisms than in their absence), plant physiology (e.g., changes in plant physiology affect radionuclide uptake by plants), and the presence of mycorrhizal fungi (e.g., interferes with the uptake of radionuclides by plants) have been demonstrated. Knowledge acquired from these experiments has been incorporated into two mechanistic models CHEMFAST and BIORUR, specifically modelling radionuclide sorption/desorption from soil matrices and radionuclide uptake by/release from plants. These mechanistic models have been incorporated into an assessment model to enhance its prediction ability by introducing the concept of bioavailability factor for radionuclides.     

Cs uptake by four plant species and Cs-K relations in the soil-plant system as affected by Ca(OH)2 application to an acid soil

Three rates of Ca(OH)₂ were applied to an acid soil and the ¹³⁴Cs uptake by radish, cucumber, soybean and sunflower plants was studied. The ¹³⁴Cs concentration in all plant species was reduced from 1.6-fold in the sunflower seeds to 6-fold in the soybean vegetative parts at the higher Ca(OH)₂ rate. Potassium (K) concentration in plants was also reduced, but less effectively. The significantly decreased ¹³⁴Cs-K soil to plant distribution factors (D.F.) clearly suggest a stronger effect of soil liming on ¹³⁴Cs than on K plant uptake. This observation was discussed in terms of ionic interactions in the soil matrix and within the plants. The results also indicated that the increased Ca²⁺ concentration in the exchange phase and in the soil solution along with the improved root activity, due to the soil liming, enhanced the immobilization of ¹³⁴Cs in the soil matrix and consequently lowered the ¹³⁴Cs availability for plant uptake.     

Yield and arsenate uptake of arbuscular mycorrhizal tomato colonized by Glomus mosseae BEG167 in As spiked soil under glasshouse conditions

A glasshouse pot experiment was conducted to study the effect of arbuscular mycorrhizal (AM) colonization by Glomus mosseae BEG167 on the yield and arsenate uptake of tomato plants in soil experimentally contaminated with five As levels (0, 25, 50, 75 and 150 mg kg(-1)). Mycorrhizal colonization (50-70% of root length) was little affected by As application and declined only in soil amended with 150 mg As kg(-1). Mycorrhizal colonization increased plant biomass at As application rates of 25, 50 and 75 mg kg(-1). Shoot As concentration increased with increasing As addition up to 50 mg kg(-1) but decreased with mycorrhizal colonization at As addition rates of 75 and 150 mg kg(-1). Shoot As uptake increased with mycorrhizal colonization at most As addition levels studied, but tended to decrease with addition of 150 mg As kg(-1). Total P uptake by mycorrhizal plants was elevated at As rates of 25, 50 and 75 mg kg(-1), and more P was allocated to the roots of mycorrhizal plants. Mycorrhizal plants had higher shoot and root P/As ratios at higher As application rates than did non-mycorrhizal controls. The soil of inoculated treatments had higher available As than uninoculated controls, and higher pH values at As addition levels of 25, 50 and 75 mg kg(-1). Mycorrhizal colonization may have increased plant resistance to potential As toxicity at the highest level of As contamination studied. Mycorrhizal tomato plants may have potential for phytoextraction of As from moderately contaminated soils or phytostabilization of more highly polluted sites.     

Uranium uptake by hydroponically cultivated crop plants

Hydroponicaly cultivated plants were grown on medium containing uranium. The appropriate concentrations of uranium for the experiments were selected on the basis of a standard ecotoxicity test. The most sensitive plant species was determined to be Lactuca sativa with an EC₅₀ value about 0.1 mM. Cucumis sativa represented the most resistant plant to uranium (EC₅₀ = 0.71 mM). Therefore, we used the uranium in a concentration range from 0.1 to 1 mM.Twenty different plant species were tested in hydroponic solution supplemented by 0.1 mM or 0.5 mM uranium concentration. The uranium accumulation of these plants varied from 0.16 mg/g DW to 0.011 mg/g DW. The highest uranium uptake was determined for Zea mays and the lowest for Arabidopsis thaliana. The amount of accumulated uranium was strongly influenced by uranium concentration in the cultivation medium. Autoradiography showed that uranium is mainly localized in the root system of the plants tested. Additional experiments demonstrated the possibility of influencing the uranium uptake from the cultivation medium by amendments. Tartaric acid was able to increase uranium uptake by Brassica oleracea and Sinapis alba up to 2.8 times or 1.9 times, respectively. Phosphate deficiency increased uranium uptake up to 4.5 times or 3.9 times, respectively, by Brassica oleracea and S. alba. In the case of deficiency of iron or presence of cadmium ions we did not find any increase in uranium accumulation.     

Effect of copper-tolerant rhizosphere bacteria on mobility of copper in soil and copper accumulation by Elsholtzia splendens

The role of rhizosphere bacteria in facilitating the solubility of copper (Cu) in contaminated soil and Cu accumulation in plant were studied. The bacteria strains were isolated from the rhizosphere of Elsholtzia splendens, a Cu accumulator growing on Tonglu Mountain copper mines. After the sandy soils containing 237 mg kg(-1) were incubated with the bacteria strains, it was indicated that rhizosphere microbes played an important role in influencing the availability of water-soluble Cu in soils. Soils had greater concentrations of water-extractable Cu compared with axenic soils inoculated with different bacterial strains. Further evidence for bacterial facilitation of increased solubility of Cu in the soil was obtained using the antibiotic ampicillin (0.1 mg g(-1)). There were 36% decreases in Cu concentration in the presence of bacterial strain MS12 and ampicillin together compared with bacterial inoculation alone. Different bacterial strains had different abilities on soil water-soluble Cu. To achieve the highest rates of plant Cu accumulation, it was necessary for bacteria to be present in the rhizosphere of E. splendens. Inoculated plants supplied with 20 micromol L(-1) CuSO4 had significantly greater concentrations of Cu in shoots and roots than uninoculated plants and bacterial strain MS2 was the most effective strain in promoting plant Cu uptake. There were 2.2-fold and 2.5-fold increases in Cu accumulation in the shoots and roots of plants inoculated with strain MS2 compared to axenic controls. Furthermore, when ampicillin and the bacterial strains were added together to the nutrient solution, the Cu concentrations in roots and shoots of ampicillin-treated plants were lower than those in inoculated plants. When ampicillin was added to the nutrient solution, Cu accumulation was inhibited by about 24-44% in shoots and 20-44% in roots. The above results provided a new insight into the phytoremediation of Cu-contaminated soil.     

Cs and K in fruiting bodies of different fungal species collected in a single forest in southern Poland

Fruiting bodies of fungi belonging to more than 70 species were collected within a few thousand square meter area of one forest during 2006 and 2007. The soil profile was collected to check the cumulative deposition of ¹³⁷Cs, which was relatively high, equal to 64 ± 2 kBq/m² (calculated for October 2006). The majority of this activity was in the first 6 cm. Fruitbodies were analyzed for radiocesium and ⁴⁰K by means of gamma-spectrometry. The highest ¹³⁷Cs activity was 54.1 ± 0.7 kBq/kg (dry weight) for a sample of Lactarius helvus collected in 2006. The results for 2006 were higher than those for 2007. In a few cases the traces of short-lived (T_1/2 = 2.06 a) ¹³⁴Cs were still found in samples. The importance of mycorrhizal fungi for radiocesium accumulation is confirmed. The differences in activity among the species are discussed in relation to observations and predictions from previous studies, where the change in relative accumulation between fruiting bodies of different species was at least partially explained by the differences in the depth of the mycelium localization in a litter/soil system. It is concluded that in some cases, such as Boletus edulis and Xerocomus badius, this prediction is fulfilled and therefore this explanation confirmed.     

Modelling 137Cs uptake in plants from undisturbed soil monoliths

A model predicting 137Cs uptake in plants was applied on data from artificially contaminated lysimeters. The lysimeter data involve three different crops (beans, ryegrass and lettuce) grown on five different soils between 3 and 5 years after contamination and where soil solution composition was monitored. The mechanistic model predicts plant uptake of 137Cs from soil solution composition. Predicted K concentrations in the rhizosphere were up to 50-fold below that in the bulk soil solution whereas corresponding 137Cs concentration gradients were always less pronounced. Predictions of crop 137Cs content based on rhizosphere soil solution compositions were generally closer to observations than those based on bulk soil solution composition. The model explained 17% (beans) to 91% (lettuce) of the variation in 137Cs activity concentrations in the plants. The model failed to predict the 137Cs activity concentration in ryegrass where uptake of the 5-year-old 137Cs from 3 soils was about 40-fold larger than predicted. The model generally underpredicted crop 137Cs concentrations at soil solution K concentration below about 1.0 mM. It is concluded that 137Cs uptake can be predicted from the soil solution composition at adequate K nutrition but that significant uncertainties remain when soil solution K is below 1 mM.     

Soil organic horizons as a major source for radiocesium biorecycling in forest ecosystems

Here we review some of the main processes and key parameters affecting the mobility of radiocesium in soils of semi-natural areas. We further illustrate them in a collection of soil surface horizons which largely differ in their organic matter contents. In soils, specific retention of radiocesium occurs in a very small number of sorbing sites, which are the frayed edge sites (FES) born out of weathered micaceous minerals. The FES abundance directly governs the mobility of trace Cs in the rhizosphere and thus its transfer from soil to plant. Here, we show that the accumulation of organic matter in topsoils can exert a dilution of FES-bearing minerals in the thick humus of some forest soils. Consequently, such accumulation significantly contributes to increasing 137Cs soil-to-plant transfer. Potassium depletion and extensive exploration of the organic horizons by plant roots can further enhance the contamination hazard. As humus thickness depends on both ecological conditions and forest management. our observations support the following ideas: (1) forest ecosystems can be classified according to their sensitivity to radiocesium bio-recycling, (2) specific forest management could be searched to decrease such bio-recycling.     

Diffusive gradient in thin FILMS (DGT) compared with soil solution and labile uranium fraction for predicting uranium bioavailability to ryegrass

The usefulness of uranium concentration in soil solution or recovered by selective extraction as unequivocal bioavailability indices for uranium uptake by plants is still unclear. The aim of the present study was to test if the uranium concentration measured by the diffusive gradient in thin films (DGT) technique is a relevant substitute for plant uranium availability in comparison to uranium concentration in the soil solution or uranium recovered by ammonium acetate. Ryegrass (Lolium perenne L. var. Melvina) is grown in greenhouse on a range of uranium spiked soils. The DGT-recovered uranium concentration (C_DGT) was correlated with uranium concentration in the soil solution or with uranium recovered by ammonium acetate extraction. Plant uptake was better predicted by the summed soil solution concentrations of UO₂²⁺, uranyl carbonate complexes and UO₂PO₄⁻. The DGT technique did not provide significant advantages over conventional methods to predict uranium uptake by plants.     

Radiocesium storage in soil microbial biomass of undisturbed alpine meadow soils and its relation to 137Cs soil-plant transfer

This study focuses on radiocesium storage in soil microbial biomass of undisturbed alpine meadow sites and its relation to the soil-to-plant transfer. Soil and plant samples were taken in August 1999 from an altitude transect (800-1600m.a.s.l.) at Gastein valley, Austria. Soil samples were subdivided into 3-cm layers for analyses of total, K(2)SO(4)-extractable and microbially stored (137)Cs. Microbial biomass was measured by the fumigation extraction method, and fungal biomass was quantified using ergosterol as biomarker molecule. In general, the quantity of (137)Cs stored in the living soil microbial biomass was relatively small. At the high-altitude meadows, showing high amounts of fungal biomass, microbially stored (137)Cs amounted to 0.64+/-0.14kBqm(-2) which corresponds to about 1.2-2.7% of the total (137)Cs soil inventory. At lower altitudes, microbial (137)Cs content was distinctly smaller and in most cases not measurable at all using the fumigation extraction method. However, a positive correlation between the observed soil-to-plant aggregated transfer factor, microbially stored (137)Cs and fungal biomass was found, which indicates a possible role of fungal biomass in the storage and turnover of (137)Cs in soils and in the (137)Cs uptake by plants.     

Uptake of 40K and 137Cs in native plants of the Marshall Islands

Uptake of 137Cs and 40K was studied in seven native plant species of the Marshall Islands. Plant and soil samples were obtained across a broad range of soil 137Cs concentrations (0.08-3900 Bq/kg) and a narrower range of 40K soil concentrations (2.3-55 Bq/kg), but with no systematic variation of 40K relative to 137Cs. Potassium-40 concentrations in plants varied little within the range of 40K soil concentrations observed. Unlike the case for 40K, 137Cs concentrations increased in plants with increasing 137Cs soil concentrations though not precisely in a proportionate manner. The best-fit relationship between soil and plant concentrations was P = aSb where a and b are regression coefficients and P and S are plant and soil concentrations, respectively. The exponent b for 40K was zero, implying plant concentrations were a single value, while b for 137Cs varied between 0.51 and 0.82, depending on the species. For both 40K and 137Cs, we observed a decreasing concentration ratio (where concentration ratio=plant concentration/soil concentration) with increasing soil concentrations. For the CR values, the best-fit relationship was of the form CR = aSb/S = aSb(-1). For the 40K CR functions, the exponent b - 1 was close to - 1 for all species. For the 137Cs CR functions, the exponent b - 1 varied from -0.19 to -0.48. The findings presented here, aswell as those by other investigators, collectively argue against the usefulness of simplistic ratio models to accurately predict uptake of either 40K or 137Cs in plants over wide ranges of soil concentration.     

(137)Cs and (90)Sr uptake by sunflower cultivated under hydroponic conditions

The (90)Sr and (137)Cs uptake by the plant Helianthus annuus L. was studied during cultivation in a hydroponic medium. The accumulation of radioactivity in plants was measured after 2, 4, 8, 16 and 32 days of cultivation. About 12% of (137)Cs and 20% of (90)Sr accumulated during the experiments. We did not find any differences between the uptake of radioactive and stable caesium and strontium isotopes. Radioactivity distribution within the plant was determined by autoradiography. (137)Cs was present mainly in nodal segments, leaf veins and young leaves. High activity of (90)Sr was localized in leaf veins, stem, central root and stomata. The influence of stable elements or analogues on the transfer behaviour was investigated. The percentage of non-active caesium and strontium concentration in plants decreased with the increasing initial concentration of Cs or Sr in the medium. The percentage of (90)Sr activity in plants decreased with increasing initial activity of the nuclide in the medium, but the activity of (137)Cs in plants increased. The influence of K(+) and NH(4)(+) on the uptake of (137)Cs and the influence of Ca(2+) on the uptake of (90)Sr was tested. The highest accumulation of (137)Cs (24-27% of the initial activity of (137)Cs) was found in the presence of 10 mM potassium and 12 mM ammonium ions. Accumulation of about 22% of initial activity of (90)Sr was determined in plants grown on the medium with 8 mM calcium ions.     

Hyperaccumulation of Pb, Zn and Cd in herbaceous grown on lead-zinc mining area in Yunnan, China

A field survey of herbaceous growing on lead-zinc mining area in Yunnan, China were conducted to identify species accumulating exceptionally large concentrations of Pb, Zn and Cd in shoots. In total, 220 plant samples of 129 species of 50 families and 220 soil samples in which the plants were growing were collected. According to accumulation concentration in plant shoots and the concentration time levels compared to plants from non-polluted environments, 21 plant samples of 16 species were chosen as best-performing specimens, 11 plant samples of 10 species for Pb, 5 plant samples of 4 species for Zn and 5 plant samples of 5 species for Cd. Sonchus asper (L.) Hill in Qilinkeng had hyperaccumulation capacity to Pb and Zn. Corydalis pterygopetala Franch in Paomaping had hyperaccumulation capacity to Zn and Cd. All 5 Cd hyperaccumulators came from Lanping lead-zinc mining area. Out of 11 Pb hyperaccumulators, 7 came from Minbingying of Huice lead-zinc mining area. The average of the concentration time levels compared to plants from non-polluted environments were higher than 10 times in all plant samples, the concentration time levels changed from 203 times to 620 times for Pb, from 50 times to 70 times for Zn and from 145 times to 330 times for Cd. Out of 21 plant samples, translocation factor changed from 0.35 to 1.90, only translocation factor of 7 plant samples were higher than 1. Enrichment coefficients of all samples were lower than 1. These plant species were primarily heavy metal hyperaccumulator, and will be used in phytoremediation of the metallic pollutants in soils after further research in accumulation mechanism.