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.     

Arbuscular mycorrhizal fungi decrease radiocesium accumulation in Medicago truncatula

The role of arbuscular mycorrhizal fungi (AMF) in plant radiocesium uptake and accumulation remains ambiguous. This is probably due to the presence of other soil microorganisms, the variability of soil characteristics and plant nutritional status or the availability of its chemical analogue, potassium (K). Here, we used an in vitro culture system to study the impact of increased concentration of K on radiocesium accumulation in non K-starved mycorrhizal and non-mycorrhizal Medicago truncatula plants. In the presence of AMF radiocesium uptake decreased regardless of the concentration of K, and its translocation from root to shoot was also significantly lower. Potassium also reduced the accumulation of radiocesium in plants but to a lesser extent than mycorrhization, and without any effect on translocation. These results suggest that AMF in combination with K can play a key role in reducing radiocesium uptake and its subsequent translocation to plant shoots, thereby representing good potential for improved phytomanagement of contaminated areas.     

Accumulation of radiocesium by mushrooms in the environment: a literature review

During the last 50 years, a large amount of information on radionuclide accumulators or "sentinel-type" organisms in the environment has been published. Much of this work focused on the risks of food-chain transfer of radionuclides to higher organisms such as reindeer and man. Until the 1980s and 1990s, there were few published data on the radiocesium ((134)Cs and (137)Cs) accumulation by mushrooms. The present review of published data for (134,137)Cs accumulation by mushrooms in nature discusses the aspects that promote (134,137)Cs uptake by mushrooms and focuses on mushrooms that demonstrate a propensity for use in the environmental biomonitoring of radiocesium contamination. Transfer factors (TF, as dry weight concentration in fruiting body divided by concentration in substrate) ranged up to 24 (unitless), and aggregate transfer factors (T(ag), as Bq(137)Cs/kg dw in fruiting body divided by the aerial deposition as Bq/m(2)) ranged up to 8m(2)/kg dw.     

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.     

On the influence of soil properties on the transfer of 137Cs from two soils (Chromic Luvisol and Eutric Fluvisol) to wheat and cabbage

Two types of soils (Eutric Fluvisol and Chromic Luvisol) and two crops (wheat and cabbage) were investigated for determination of the transfer of 137Cs from soil to plant. Measurements were performed using gamma-spectrometry. Results for the soil characteristics, transfer factors of the radionuclides (TF), and conversion factors (CF) (cabbage/wheat) were obtained. The transfer of 137Cs was higher for Chromic Luvisol for both the plants. Statistically significant dependence of TF of 137Cs on its concentration in soil was established for cabbage. Dependence between K content in the soil and the transfer factor of 137Cs was not found due to the high concentrations of available K. Use of bioconcentration factor (BCF) (ratio between the activity concentration of a radionuclide in a reference plant to its concentration in another plant) is demonstrated and proposed for risk assessment studies.     

Soil- and plant-based countermeasures to reduce 137Cs and 90Sr uptake by grasses in natural meadows: the REDUP project.

The effectiveness of a set of soil- and plant-based countermeasures to reduce 137Cs and 90Sr transfer to plants was tested in natural meadows in the area affected by Chernobyl fallout. Countermeasures comprised the use of agricultural practices (disking + ploughing, liming and NPK fertilisation), addition of soil amendments and reseeding with a selection of grass species. Disking + ploughing was the most effective treatment, whereas the K fertiliser doses applied were insufficient to produce a significant increase in K concentration in soil solution. The application of some agricultural practices was economically justifiable for scenarios with a high initial transfer, such as 137Cs-contaminated organic soils. The use of soil amendments did not lead to a further decrease in transfer. Laboratory experiments demonstrated that this was because of their low radionuclide sorption properties. Finally, experiments examining the effect of plant species on radionuclide transfer showed that both transfer and biomass can depend on the plant species, indicating that those with high radionuclide root uptake should be avoided when reseeding after ploughing.     

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.     

Predicting soil-to-plant transfer of radionuclides with a mechanistic model (BioRUR)

BioRUR model has been developed for the simulation of radionuclide (RN) transfer through physical and biological compartments, based on the available information on the transfer of their nutrient analogues. The model assumes that radionuclides are transferred from soil to plant through the same pathways as their nutrient analogues, where K and Ca are the analogues of Cs and Sr, respectively. Basically, the transfer of radionuclide between two compartments is calculated as the transfer of nutrient multiplied by the ratio of concentrations of RN to nutrient, corrected by a selectivity coefficient. Hydroponic experiments showed the validity of this assumption for root uptake of Cs and Sr and reported a selectivity coefficient around 1.0 for both. However, the application of this approach to soil-to-plant transfer raises some questions on which are the effective concentrations of RN and nutrient detected by the plant uptake mechanism. This paper describes the evaluation of two configurations of BioRUR, one which simplifies the soil as an homogeneous pool, and the other which considers that some concentration gradients develop around roots and therefore ion concentrations at the root surface are different from those of the bulk soil. The results show a good fit between the observed Sr transfer and the mechanistic simulations, even when a homogeneous soil is considered. On the other hand, Cs transfer is overestimated by two orders of magnitude if the development of a decreasing K profile around roots is not taken into account.     

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.     

Incorporating soil structure and root distribution into plant uptake models for radionuclides: toward a more physically based transfer model

Most biosphere and contamination assessment models are based on uniform soil conditions, since single coefficients are used to describe the transfer of contaminants to the plant. Indeed, physical and chemical characteristics and root distribution are highly variable in the soil profile. These parameters have to be considered in the formulation of a more realistic soil-plant transfer model for naturally structured soils. The impact of monolith soil structure (repacked and structured) on Zn and Mn uptake by wheat was studied in a controlled tracer application (dye and radioactive) experiment. We used Brilliant Blue and Sulforhodamine B to dye flow lines and 65Zn and 54Mn to trace soil distribution and plant uptake of surface-applied particle-reactive contaminants. Spatial variation of the soil water content during irrigation and plant growth informs indirectly about tracer and root location in the soil profile. In the structured monolith, a till pan at a depth of 30 cm limited vertical water flow and root penetration into deeper soil layers and restricted tracers to the upper third of the monolith. In the repacked monolith, roots were observed at all depths and fingering flow allowed for the fast appearance of all tracers in the outflow. These differences between the two monoliths are reflected by significantly higher 54Mn and 65Zn uptake in wheat grown on the structured monolith. The higher uptake of Mn can be modelled on the basis of radionuclide and root distribution as a function of depth and using a combination of preferential flow and rooting. The considerably higher uptake of Zn requires transfer factors which account for variable biochemical uptake as a function of location.     

Spatial variability of fallout-90Sr in soil and vegetation of an alpine pasture

According to the soil-to-plant transfer concept generally used in dose assessment modeling, the plant uptake of a radionuclide should depend linearly on its concentration in the soil. In order to validate this concept for (90)Sr in a semi-natural ecosystem, plant and soil samples were taken at 100 plots of a 100 x 100 m(2) area within an alpine pasture near Berchtesgaden, Germany. At three plots, the vertical distribution of (90)Sr in the soil was determined in addition. A statistically significant correlation between the soil and plant concentration of (90)Sr was not detectable (Spearman correlation coefficient R=-0.116, p>0.05) within the range of the Sr-concentration covered (15-548 Bq kg(-1) dry soil and 17-253 Bq kg(-1) dry plant material). Thus, the prerequisite of the soil-to-plant transfer concept was not fulfilled for (90)Sr at this site. Organic carbon and total nitrogen were also determined in the soil samples. Both elements were highly correlated (R=0.912, p<0.001), their ratio being C/N=10.9+/-0.7. While C was positively correlated with the (90)Sr concentrations in the soil (R=0.342, p<0.001), negative correlations were observed for the plant concentrations (R=-0.286, p<0.01) and the concentration ratios (R=-0.444, p<0.001) of (90)Sr. These results are compared with those recently obtained for (137)Cs by Bunzl et al. (J Environ Radioactiv 48 (2000) 145).     

Radionuclide transfer from soil to fruit

The available literature on the transfer of radionuclides from soil to fruit has been reviewed with the aim of identifying the main variables and processes affecting the behaviour of radionuclides in fruit plants. Where available, data for transfer of radionuclides from soil to other components of fruit plant have also been collected, to help in understanding the processes of translocation and storage in perennial plants. Soil-to-fruit transfer factors were derived from agricultural ecosystems, both from temperate and subtropical or tropical zones. Aggregated transfer factors have also been collected from natural or semi-natural ecosystems. The data concern numerous fruits and various radionuclides. Soil-to-fruit transfer is nuclide specific. The variability for a given radionuclide is first of all ascribable to the different properties of soils. Fruit plant species are very heterogeneous, varying from woody trees and shrubs to herbaceous plants. In temperate areas the soil-to-fruit transfer is higher in woody trees for caesium and in shrubs for strontium. Significant differences between the values obtained in temperate and subtropical and tropical regions do not necessarily imply that they are ascribable to climate. Transfer factors for caesium are higher in subtropical and tropical fruits, while those for strontium, as well as for plutonium and americium, in the same fruits, are lower; these results can be interpreted taking into account different soil characteristics.     

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.     

Predicting the transfer of radiocaesium from organic soils to plants using soil characteristics

A model predicting plant uptake of radiocaesium based on soil characteristics is described. Three soil parameters required to determine radiocaesium bioavailability in soils are estimated in the model: the labile caesium distribution coefficient (kd1), K+ concentration in the soil solution [mK] and the soil solution-->plant radiocaesium concentration factor (CF, Bq kg-1 plant/Bq dm-3). These were determined as functions of soil clay content, exchangeable K+ status, pH, NH4+ concentration and organic matter content. The effect of time on radiocaesium fixation was described using a previously published double exponential equation, modified for the effect of soil organic matter as a non-fixing adsorbent. The model was parameterised using radiocaesium uptake data from two pot trials conducted separately using ryegrass (Lolium perenne) on mineral soils and bent grass (Agrostis capillaris) on organic soils. This resulted in a significant fit to the observed transfer factor (TF, Bq kg-1 plant/Bq kg-1 whole soil) (P < 0.001, n = 58) and soil solution K+ concentration (mK, mol dm-3) (P < 0.001, n = 58). Without further parameterisation the model was tested against independent radiocaesium uptake data for barley (n = 71) using a database of published and unpublished information covering contamination time periods of 1.2-10 years (transfer factors ranged from 0.001 to 0.1). The model accounted for 52% (n = 71, P < 0.001) of the observed variation in log transfer factor.     

On the radiocesium carbonate barrier in organics-rich sediments of Lake Juodis, Lithuania

Radiocesium vertical profiles in organics-rich sediments of running shallow eutrophic Lake Juodis (Lithuania) were studied in relation to seasonal variations of vertical profiles (in water column and sediments) of standard variables (pH, redox potential, temperature, oxygen concentrations, conductivity). It is shown that the sedimentation rate, radiocesium mobility and its vertical profiles in sediments are controlled by the vital cycle (processes of the growth, accumulation and decomposition) of green algae covering the main bottom areas of the lake. It is also shown that calcite deposits are formed in the shallow bottom areas that are oxygenated throughout the year because of the photosynthetic activity of the green algae covering the sediment. Formation of the calcite coatings on freshly accumulated organics is remarkable for causing elevated densities of sediment solids in the upper part of the respective vertical profiles. These calcite deposits behave as a barrier for radiocesium backward flux to the bottom water making the respective bottom areas a radionuclide sink. Together with the jelly-structured sediments lying below these deposits, the calcite preserves the shape of the primary radiocesium vertical profiles formed due to free-ion diffusion after the deposition event. It was determined that bottom areas anaerobic in winter are the main radiocesium source in the water column and cause characteristic radiocesium redistribution in surface sediments.     

The influence of the development of temperate fruit tree species on the potential for their uptake of radionuclides

This paper reviews the published literature that describes the phenological development of above and below ground organs of temperate fruit trees (top fruit), particularly with respect to apple (Malus domestica). Critical information is presented which is considered appropriate in developing an understanding of the potential for top fruit species to take up radionuclide contaminants from the atmosphere and the soil. Information is cited on how climatic and edaphic factors influence the growth and development of temperate fruit trees, the phenological production of their leaf area and the development and growth of their fruit and hence the potential for foliar and fruit uptake of radionuclides from the atmosphere. The study also reports on the importance of the distribution and phenological development of roots in the soil and the potential for their uptake of radionuclides from the soil. The effects of above and below ground management procedures, within temperate fruit orchards, on potential radionuclide uptake are also considered. It is concluded that the potential for the uptake of radionuclides by temperate fruit tree species will depend on a number of phenological and physiological factors. For uptake from the soil these factors include; root distribution and density in the soil profile, seasonal changes in the production and distribution of roots, and the presence and amount of water in the soil. These factors are themselves influenced by rootstock type and its growth vigour, scion type and its growth vigour, tree age, spacing of trees in the orchard, orchard management practices (presence or absence of weeds or grass under the trees) and soil type and depth. Direct uptake by the shoot, however, will be influenced by the climatic conditions at the time of exposure and the presence of foliage. Deposition and uptake are likely to change with leaf area development and the ability of radionuclides to penetrate the cuticle of the leaf changes with seasonal development. Transport of radionuclides to the fruit may also depend on the time of season, as the importance of the xylem and phloem transport routes can change with the growth and development of the fruit.     

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.     

Plant uptake and downward migration of 85Sr and 137Cs after their deposition on to flooded rice fields: lysimeter experiments with and without the addition of KCl and lime

In order to study the plant uptake and downward migration of radiostrontium and radiocesium deposited on to a flooded rice field, 85Sr and 137Cs were applied to the standing water over an acidic sandy soil in planted lysimeters. The plant uptake was quantified with the areal transfer factor (TFa, m2 kg(-1)-dry plant). Following the spiking 14 days after transplanting, the TFa values for the hulled seeds were 3.9 x 10(-4) for 85Sr and 1.4 x 10(-4) for 137Cs, whereas those for the straws were 1.3 x 10(-2) and 3.2 x 10(-4), respectively. The 137Cs TFa from the spiking at the anthesis/milky-ripe stage was several times higher than that from the earlier spiking, whereas the difference was much less in the 85Sr TFa. Such an increase in the 137Cs TFa was attributed mainly to an enhanced plant-base uptake. The addition of KCl and lime after the spiking significantly reduced the TFa values of both radionuclides. The reducing effect was greater for the later spiking. An appreciable fraction of the applied activity leached out of the lysimeter for 85Sr, whereas a negligible fraction leached for 137Cs. The leaching was remarkably increased by the KCl and lime addition for both. A conspicuous localization of 137Cs with respect to the soil surface was observed. In a batch experiment, the 137Cs concentration in the standing water decreased more rapidly than that of 85Sr, both of which were fitted to the power functions of the elapsed time. To add KCl and lime slowed such decreases to lessen the distribution coefficients (Kd) of both 85Sr and 137Cs.     

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.