Cesium accumulation in nodules is involved in mitigating cesium transfer to shoot
AbstractRadiocesium (137Cs) transfer from soil to crops is largely regulated by soil potassium (K) levels owing to the chemical similarity between K and cesium (Cs). However, the mitigation of Cs translocation in soybean through soil K is lower than in other crops, highlighting the importance of clarifying soybean-specific Cs translocation mechanisms. Although root nodule symbiosis has been proposed to alter nutrient transport systems, its impact on Cs dynamics remains unclear. We hypothesized that Cs translocation mechanisms are altered under root nodule symbiosis. To elucidate these mechanisms, we conducted field experiments using three soybean genotypes with different nodulation abilities and analyzed their elemental distribution patterns. Additionally, hydroponic experiments using inoculated soybeans were conducted to investigate 137Cs distribution. We found that Cs concentrations were consistently higher in nodules than in other organs. Radioisotope imaging also showed predominant 137Cs accumulation in nodules. Covariance analysis revealed that Cs translocation to shoot was lower in genotypes with higher nodule formation under the same soil exchangeable K conditions. Furthermore, increased nodule formation, especially nodule number, was associated with reduced Cs translocation to shoot. These results suggest that nodules contribute to suppressing Cs translocation to shoot and provide new insights into Cs dynamics under root nodule symbiosis.
Similar content being viewed by others
Nodulation number tempers the relative importance of stochastic processes in the assembly of soybean root-associated communities
Article
Open access
28 August 2023
Genetically optimizing soybean nodulation improves yield and protein content
Article
09 May 2024
Integrated single-nucleus and spatial transcriptomics captures transitional states in soybean nodule maturation
Article
13 April 2023
IntroductionThe hydrogen explosions at TEPCO’s Fukushima Daiichi Nuclear Power Plant in 2011 resulted in the release and deposition of radioactive substances, including radiocesium (137Cs), onto agricultural fields. Crops cultivated in decontaminated fields remain at risk of radioactive substances transfer to edible plant parts1. The transfer of 137Cs from soil to plants has become a significant environmental and agricultural concern due to its long half-life (ca. 30.2 years). Potassium (K) fertilization has been shown to effectively reduce cesium (Cs) uptake in various crops, including soybean, wheat, and rice2,3,4. For rice and soybean cultivation, maintaining exchangeable K concentrations in soils (over 25 mg K2O per 100 g soil) through cultivation has been recommended5,6. This mitigation strategy is based on the chemical similarity between Cs+ and K+, thereby elevating soil K concentrations competitively inhibiting Cs uptake. It is well known that Cs is primarily taken up and translocated via K transport systems in plants. The high-affinity K⁺ transporter family KUP/HAK/KT has been reported to be involved in Cs⁺ transport7. In the case of Arabidopsis thaliana, AtHAK5 has been identified as a key transporter contributing to increased Cs uptake under K-deficient conditions8. In rice, OsHAK1 has also been associated with Cs transport9,10. While the role of the soybean homolog GmHAK5 in K uptake and distribution in root was evaluated11, the function of this transporter for Cs remains poorly understood. Regarding other Cs transport pathways, the Arabidopsis inward-rectifying K+ channel AKT1 has been suggested to be involved in Cs transport, although its role appears to be limited12,13. Cs is also absorbed and distributed primarily in voltage-insensitive cation channels under K-sufficient conditions14.Under equivalent soil K concentrations, soybean exhibits high Cs transfer to seeds compared with other crops, such as wheat and maize15,16. Even among leguminous species, soybean tends to accumulate more 137Cs than peanut17. It is considered that the higher Cs accumulation in soybean seed is due to high K demand. Additionally, the structural characteristics of soybean seeds facilitate Cs translocation into the edible portions18. Soybean continues to absorb K from soil until the full seed stage, and it has been reported that the ability of soybean to discriminate between K and 137Cs declines from the flowering stage to seed development, resulting in increased 137Cs uptake during this period4. K fertilization is highly effective to reduce Cs uptake and improve the production in soybean; however, due to the economic cost of fertilizers, continuous K application may not be a sustainable strategy to mitigate 137Cs transfer from soil to plant. Therefore, other mitigation strategies in addition to K fertilization should be explored for effective risk management of Cs transfer in soybean.To better understand Cs transfer, several studies have investigated the role of nonexchangeable K19, Cs adsorption to soil mineral nutrients20, and the effects of cattle manure application21. While these studies focus on soil-based countermeasures, it is also necessary to explore plant-specific strategies for reducing Cs transfer. One potential approach in soybean is the use of symbiotic microorganisms. Soybean establishes symbiotic relationships with rhizobia and arbuscular mycorrhizal (AM) fungi, which primarily enhance nitrogen and phosphorus acquisition. The role of AM fungi in Cs transfer from soil to shoot remains inconsistent, with some studies showing Cs delivery to host plants from soil22, while others report limiting its movement to shoot due to its retention within fungal hyphae23,24. Nodules, which share evolutionarily conserved common signaling pathways with AM fungi symbiosis25, are reportedly more sensitive to salinity and heavy metal stress than roots or whole plants26. In terms of the role of K in nodules, it is presumed to contribute to intercellular potential regulation, cell expansion, and energy supply27,28. In rhizobia, a positive relationship between K levels and nitrogenase activity has been reported29. These limited studies suggest that K plays a critical role in both nodule tissues and rhizobia. However, while the mechanisms of K uptake and distribution in nodules are not yet fully understood, the involvement of Cs in nodules remains even more obscure. Furthermore, both nodule formation and Cs transfer are inherently influenced by soil nutrient conditions. In particular, soil nitrogen and phosphorus conditions have been suggested to play a role in nodule formation and Cs dynamics30,31,32,33. Thus, it is necessary to investigate how nodules affect Cs transfer under various soil conditions.This study aimed to reveal the effects of nodules on the mechanism of Cs transfer to shoot. To achieve this goal, we conducted field experiments in 2021 and 2024 using three soybean genotypes with different nodulation abilities, under various fertilization treatments, to investigate the dynamics of monovalent cations in each plant organ and soil. We also attempted to conduct a spatial analysis of 137Cs in root and nodule tissue to investigate the 137Cs distribution pattern. We found that Cs levels were higher in nodules than in other plant organs and increased nodule formation was potentially associated with suppressing Cs translocation to shoot. Our findings suggest that nodules may play a key role in mitigating Cs transfer in addition to K fertilization, providing a potential strategy for 137Cs risk management in leguminous crops.Materials and methodsPlant materials and growth conditionsThree soybean (Glycine max (L.) Merrill) genotypes with different nodulation abilities [a normal nodulating genotype (Enrei), a hyper-nodulating genotype (En-b0-1), and a non-nodulating genotype (En1282), all derived from Enrei as described by Hamaguchi et al.34] were cultivated in a field at Hokkaido University in 2021 and 2024. These fields were established in 1914, with four fertilizer treatments, namely, complete fertilization (+ NPK), without nitrogen (− N), without phosphorus (− P), and without potassium (− K), applied continuously for over 100 years35. Soil type is categorized as gray lowland soil. In the − N, − P, − K, and + NPK treatments, each plot size was 5.25 × 15.80 m. Moreover, the N, P, and K fertilizers were applied as ammonium sulfate, superphosphate, and potassium sulfate, respectively (100 kg N, P2O5, K2O ha−1). Three seeds were sown at 70 cm × 20 cm intervals and then thinned to two plants per hill. Plant organs (leaf, petiole, stem, pod, seed, and root) and bulk soil (the 0–15 cm soil in the inter-row space) were sampled at the flowering and maturity stages with three replications. Plant samples at the flowering stage were divided into leaf, petiole, stem, root, and nodule. Plant samples were then dried at 80 °C for 1 week, and their dry weights were measured. These dried plant samples were ground for mineral analysis. Soil samples were air-dried and passed through a sieve with a 2 mm diameter for mineral analysis.Measurement of plant mineralPlant samples were digested in 2 mL of 61% (w/v) HNO3 (EL grade; Kanto Chemical, Tokyo, Japan) at 107.5 °C in a DigiPREP apparatus (SCP Science, Canada). After approximately 1.5 h, about 0.5 mL of H2O2 (EL grade; Kanto Chemical, Tokyo, Japan) was added, following by further digestion for another 15 min. The digested solution was cooled and filled with 10 mL with 2% HNO3 in Milli-Q water. Cs, K, sodium (Na), and rubidium (Rb) were analyzed using inductively coupled plasma mass spectrometry (ICP-MS) (ELAN DRC-e; Perkin Elmer, Waltham, MA, USA). To determine δ15N in leaves, plant samples were weighed into tin capsules and analyzed using an isotope ratio mass spectrometer (Integra2, sercon, UK). The δ15N values were reported relative to atmospheric N2.Measurement of soil mineralFor the soil exchangeable cation, soil was extracted with 1 M ammonium acetate at a soil/solution ratio of 1:20, shaken for 1 h and filtered using an Advantec® quantitative filter paper No. 5C (Toyo Roshi Co., Ltd., Tokyo, Japan). The filtrates were measured using ICP-MS (ELAN DRC-e; PerkinElmer, Waltham, MA, USA) to determine the concentration of soil exchangeable cation. Total nitrogen concentration in soil samples was determined by Kjeldahl digestion. Available phosphorus concentrations were measured using the Bray II method36. Soil pH (soil/Milli-Q water = 1:5, w/v) was measured with a pH meter (HORIBA Ltd., Kyoto, Japan).Spatial imaging of 137Cs in root and nodule tissuesTo study the distribution of 137Cs in the nodules and roots, germinated soybean (Glycine max cv. Enrei) seeds were cultivated hydroponically in 3-L plastic containers while aerating and inoculated with Bradyrhizobium japonicum USDA110 (obtained from the National Agriculture and Food Research Organization, NARO, Japan) at a concentration of 1 × 107 colony-forming units mL−1. The solution was an N-free half-strength modified Hoagland’s nutrient solution (3 mM K, 2 mM Ca, 1 mM P, 0.5 mM S, 0.5 mM Mg). The nutrient solution inoculated with rhizobia was replaced every 3 days. At 18 days after the start of hydroponic cultivation, 3.7 kBq mL−1 137Cs was added to the nutrient solution immediately after 18 days of hydroponic cultivation without any pre-treatment, and the plants and rhizobia were allowed to absorb it for 24 h. After washing the root with pure water, the root with attached nodules was cut into approximately 1 cm pieces and immediately frozen by submerging in liquid nitrogen. Thereafter, the roots and sliced sections were prepared according to a previously described method37,38. Each sample was embedded in an embedding medium, covered with an adhesive film (Cryo-Film transfer kit, Finetec, Tokyo, Japan), and sliced with a cryostat into serial sections of 5 µm thickness at − 20 °C. A BAS IP TR imaging plate (GE Healthcare) was stuck to the frozen section on the side directly opposite the attached film. The imaging plate (IP) with the samples was kept in the freezer at − 80 °C for 6 days. The image on the IP was scanned with an FLA5000 image analyzer (Fujifilm, Tokyo, Japan) at a resolution of 10 µm.Statistical analysesTo compare dry weight and elemental distribution of plant organs, a three-way analysis of variance (ANOVA) was first performed to evaluate the effects of organ, fertilizer treatment, and genotype in R (version 4.4.1). However, strong effects of treatment and genotype masked organ-specific differences. To address this, a one-way ANOVA was subsequently conducted for organs within each treatment–genotype combination, followed by Tukey’s multiple comparison analysis. To assess effects of treatment and genotype by year, a two-way ANOVA was conducted, with Tukey’s multiple comparison analysis applied when interactions were significant. Regarding correlation analysis, we used the Spearman’s rank correlation to accommodate potential nonlinearity and non-normality. An analysis of covariance (ANCOVA) was conducted in Python (version 3.9.18) using the statsmodels library (version 0.14.0). Least‐squares means (LS‐means) for each genotype were calculated at the overall mean of covariates, and pairwise t-tests were then performed on those LS-means. False discovery rate correction was applied using the two-stage Benjamini–Hochberg method (BH).ResultsSoil chemical properties under different fertilization treatmentsTo clarify the effect of nodule formation on cation transfer from soil to soybean, we investigated three soybean genotypes with different nodulation abilities (normal nodulating genotype: Enrei; hyper-nodulating genotype: En-b0-1; and non-nodulating genotype: En1282) grown under various fertilization treatments. Compared with the + NPK treatment, soil exchangeable K concentrations were significantly reduced under − K treatment consistently across both years and growth stages (Supplementary Table S1). Meanwhile, soil exchangeable Cs was highest under − K treatment. Soil exchangeable K was higher and Cs was lower in the − N and − P treatments than in the + NPK treatment. Other exchangeable monovalent cations in soil showed similar trends to Cs. Available phosphorus in soil was lowest under − P treatment, and soil total nitrogen tended to be lowest under − N treatment. Soil pH was significantly increased under − N treatment.Growth of genotypes with different nodulation abilities under different soil nutrient treatmentsIn the normal nodulating genotype, shoot (combined leaf, petiole, and stem) dry weight was highest in the + NPK treatment in both 2021 and 2024, and decreased in the order of − N, − P, and − K treatment (Table 1). In contrast, both the hyper-nodulating and non-nodulating genotypes reduced shoot biomass in − N treatment. Across all genotypes and treatments, leaf dry weight was consistently the highest among organs, while nodule dry weight was the lowest (Fig. 1a,b). Under − K treatments, growth was consistently suppressed in all genotypes, with the number and dry weight of nodules being the lowest across treatments in both 2021 and 2024 (Table 1). Nodule formation showed no significant difference between the − P and + NPK treatments but was significantly increased under the − N treatment. Seed weight at maturity showed a similar tendency to shoot dry weight at the flowering stage, with a significant reduction in − K treatment observed particularly in the normal nodulating genotype. While overall biomass and yield were higher in 2021 compared to those in 2024, the effects of fertilizer treatments and genotypes were largely consistent across years.Table 1 Plant growth at flowering stage and maturity stage.Full size tableFig. 1Plant growth per organ at flowering stage. (a, b) Each organ dry weight of soybean genotypes at flowering stage in 2021 (a) and 2024 (b). For each genotype and treatment, statistical analyses were performed as one-way ANOVA with Tukey’s multiple comparisons test for each plant organ. Dots represent distinct biological replicates for each treatment (n = 3), and bars indicate mean ± SE. Different letters indicate statistically significant differences (P < 0.05) as determined by Tukey’s multiple comparisons test. “n.s.” indicates no significant differences among plant organs (P > 0.05).Full size imageElemental distribution within plant in field experimentA two-way ANOVA was conducted for shoot Cs and K concentrations to evaluate the effects of genotype and treatment on the elemental distribution to shoot. Significant effects on shoot Cs concentration were observed only in 2021. Cs levels in the hyper-nodulating genotype tended to be lower compared with those in the normal and non-nodulating genotypes, particularly in − K and + NPK treatment (Table 2). Across all genotypes, shoot Cs concentration was highest in − K and lowest in − N treatment. Shoot K concentrations consistently decreased in the − K treatment in both years across all genotypes. To investigate elemental distribution among organs, soybean samples at the flowering stage were separated into leaves, petioles, stems, roots, and nodules. In the normal nodulating genotype grown in 2021, Cs concentrations were highest in nodules across all treatments compared with those in other organs, with particularly pronounced accumulation in − K and + NPK treatment (Fig. 2a). A similar tendency was observed in the hyper-nodulating genotype, which also exhibited significantly increased concentrations of Cs in nodules under these treatments. Although one-way ANOVA detected no significant differences under –N, –P, and + NPK treatment in 2024, Cs concentrations tended to be higher in nodules (Fig. 2b). In 2021, nodules had significantly higher K concentrations than other organs in the − K treatment in both the normal and hyper-nodulating genotypes (Fig. 2c). However, this trend was not observed in 2024, showing no consistent distribution pattern (Fig. 2d). For Cs concentrations in shoot, leaves were the primary organ of Cs allocation. In contrast, K concentrations were significantly higher in petioles than in leaves in all treatments except − K in both years. At maturity, seed Cs concentrations increased in the − K treatment, while seed K concentrations decreased (Table 2). For other monovalent cations of organs at the flowering stage, Na significantly accumulated in roots in all genotypes in both 2021 and 2024 (Supplementary Fig. S1). In the − K treatment, Na concentration increased in nodules but remained lower than that in roots. Rb tended to be more concentrated in nodules than in other organs in the normal nodulating and hyper-nodulating genotypes in 2021. A similar tendency was also observed in the normal nodulating genotype under the − K treatment in 2024.Table 2 Elemental concentration in shoot and seed.Full size tableFig. 2Cs and K concentrations in each soybean organ. (a, b) Concentration of Cs in each organ at flowering stage in 2021 (a) and 2024 (b). (c, d) Concentration of K in each organ at flowering stage in 2021 (c) and 2024 (d). Statistical analyses were conducted using one-way ANOVA followed by Tukey’s multiple comparisons test to evaluate differences among plant organs within each genotype and treatment. Dots represent distinct biological replicates for each treatment (n = 3), and bars indicate mean ± SE. Different letters indicate statistically significant differences (P < 0.05) as determined by Tukey’s multiple comparisons test. “n.s.” indicates no significant differences among plant organs (P > 0.05).Full size imageDistribution ratios among organs were calculated to evaluate the effect of nodules on the elemental distribution within plant. The proportion of Cs distributed to nodules was highest in the − N treatment in both 2021 and 2024 (Supplementary Fig. S2). Compared with the normal nodulating genotype, the hyper-nodulating genotype showed higher Cs proportions allocated to nodules across all treatments. K exhibited similar distribution patterns to Cs in both years. Spearman’s rank correlation coefficient (r) between the proportion of Cs allocated to nodules and that allocated to shoot was significantly negative (r = − 0.77, P < 0.005) (Supplementary Fig. S3). Similar patterns were observed for K (r = − 0.66, P < 0.005). In contrast, Na was predominantly distributed to roots across all treatments, and increased allocation to nodules did not result in the change of shoot Na level (Supplementary Figs. S2 and S3). Rb showed a distribution pattern similar to those of Cs and K (Supplementary Fig. S2), and a negative correlation was observed between nodule and shoot allocation ratios (r = − 0.70, P < 0.005) (Supplementary Fig. S3).Spatial localization of 137Cs in root systemAlthough high concentrations of stable Cs in nodules were observed in field experiments, it is also necessary to confirm the distribution pattern of 137Cs. A transverse section (Fig. 3a) and its corresponding autoradiograph (Fig. 3b) were superimposed to generate Fig. 3c. According to the overlaid image, a strong signal was observed in the nodule, particularly in the infection zone. In contrast, the signal in the main and lateral roots was very weak. These observations suggest that 137Cs is taken up and accumulated in the nodule at 24 h after the start of absorption.Fig. 3137Cs autoradiography in a soybean root and nodule after 24 h of 137Cs absorption. (a) Transverse section of the soybean root including the root nodule, (b) Autoradiograph of (a) showing the localization of 137Cs. (c) Superimposed image of (a) and (b) after the black color in (b) was converted to white. Bar, 1 mm.Full size imageRelationship between soil minerals and plant mineralsAlthough the Cs distribution pattern within plant was clarified, a comprehensive understanding of the mineral nutrient dynamics requires not only a distribution analysis but also an investigation of nutrient uptake from the soil. We then investigated the relationship between mineral nutrients in the soil and those in soybean. A consistently significant positive correlation was observed between soil exchangeable Cs concentrations and Cs concentrations of both shoots and seeds in both 2021 and 2024 (Supplementary Fig. S4). In contrast, a significant negative correlation was found between soil exchangeable K concentrations at the flowering stage and shoot Cs concentrations in 2021 (r = − 0.74, P < 0.005), with a similar tendency observed in 2024 (r = − 0.79, P < 0.005) (Fig. 4a,b). In all three genotypes, soil exchangeable K was negatively correlated with shoot Cs. Given this strong inverse relationship, soil exchangeable K was included as a covariate when comparing shoot Cs among genotypes. To compare the effects of genotypes on shoot Cs after adjusting for soil exchangeable K, an ANCOVA (shoot Cs ~ exchangeable K + genotype) was performed for the hyper-nodulating, normal, and non-nodulating genotypes, followed by pairwise t-tests of the resulting LS-means. The exchangeable K concentrations adjusted shoot Cs concentrations of the hyper-nodulating genotype were significantly lower than that of both the normal and non-nodulating genotypes (FDR-corrected two-stage BH P < 0.05), whereas the exchangeable K concentrations adjusted shoot Cs concentrations of the normal and non-nodulating genotypes were not significantly different. At the maturity stage, significant negative correlations were found between soil exchangeable K concentrations and seed Cs concentrations in both 2021 (r = − 0.84, P < 0.005) and 2024 (r = − 0.88, P < 0.005) (Fig. 4c,d). However, ANCOVA did not show significant differences among genotypes in this relationship.Fig. 4Relationship between soybean Cs concentration and soil exchangeable K concentration. (a, b) Shoot Cs concentration at flowering stage in 2021 (a) and 2024 (b). (c, d) Seed Cs concentration at maturity stage in 2021 (c) and 2024 (d). Line types represent soybean genotypes: Enrei (solid), En-b0-1 (dotted), and En1282 (dashed). Power-law equations (y = axb) were estimated separately for each genotype. Spearman’s rank correlation coefficient (r) and corresponding two-sided P values are indicated (†P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001). When pooled across genotypes: (a) r = − 0.74, P < 0.001; (b) r = − 0.79, P < 0.001; (c) r = − 0.84, P < 0.001; (d) r = − 0.88, P < 0.001.Full size imageRelationship between nodulation and Cs translocationThe relationship between soil exchangeable K concentration and shoot Cs concentration varied among nodulation genotypes, indicating that nodule formation may influence Cs translocation to shoot. We then further investigated the relationship between nodulation traits and shoot Cs concentration at the flowering stage. Shoot Cs concentration decreased as the nodule dry weight increased (r = − 0.55, P < 0.005), and a similar negative relationship was found with nodule number (r = − 0.66, P < 0.005) (Fig. 5a,b). Shoot Cs concentration was negatively correlated with soil exchangeable K concentration (Fig. 4a,b), and both nodule number and nodule dry weight were significantly reduced under K-deficient conditions (Table 1). The relationship between nodule formation and shoot Cs concentration may be potentially confounded by soil K availability. To address this, partial correlation analysis was performed using soil exchangeable K concentration at the flowering stage as a confounding factor. While no significant relationship was found between shoot Cs concentration and nodule dry weight, a significant negative partial correlation was retained with nodule number (r = − 0.37, P < 0.01). δ15N in leaves, which is used as an indirect indicator of nitrogen fixation, showed no significant correlation with shoot Cs concentration (Supplementary Fig. S5). In contrast, a significant correlation was observed between nodule Cs concentration and leaf δ15N, and this relationship remained significant after accounting for soil exchangeable K (Supplementary Fig. S6). Similar correlation analyses were conducted for other monovalent cations in shoot. K concentration showed significantly positive correlations with both nodule dry weight and nodule number (Supplementary Fig. S7). Meanwhile, Na concentration was not significantly correlated with either trait. Rb showed a pattern similar to Cs. It was not significantly correlated with nodule dry weight but was negatively correlated with nodule number (r = − 0.49, P < 0.005). Regarding nitrogen fixation, no significant correlations were found between δ15N and other monovalent cation concentrations in leaves (Supplementary Fig. S5). For nodule monovalent cation concentrations, significant correlations were observed for Na and Rb, but not for K (Supplementary Fig. S6).Fig. 5Relationship between shoot Cs concentration and nodule formation. (a) Nodule dry weight. (b) Number of nodules. Spearman’s rank correlation coefficient (r) and corresponding two-sided P values are indicated (†P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001). Partial correlation coefficient (partial r) was calculated using soil exchangeable K concentration at flowering stage as a confounding factor (†P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001).Full size imageDiscussionRoot nodule symbiosis affects the uptake and transport systems not only for nitrogen but also for other mineral nutrients, such as K39,40. K has been suggested to play a role in maintaining ion homeostasis and nodule development and nitrogenase activity41. Our study revealed that Cs consistently accumulated at higher concentrations in nodules at the flowering stage in both 2021 and 2024, whereas K levels in nodules exhibited an inconsistent trend (Fig. 2). Moreover, 137Cs was mainly accumulated in nodules under root nodule symbiotic conditions (Fig. 3). As reported by Shinano et al.42, K is preferentially translocated to the shoot rather than Cs, possibly limiting Cs mobility and leading to Cs accumulation in the root system, particularly in nodules. Supporting this notion, Cs accumulation in nodules was significantly high under K-deficient conditions, indicating that limited K availability enhances Cs accumulation in nodules. Furthermore, 137Cs was particularly enriched in the infected cells of nodule. K is essential for rhizobia to maintain osmotic balance43. This suggests that Cs may also accumulate preferentially in bacteroids. However, Cs localization within nodules remains inconclusive due to the short-term observation and the overall K requirement of nodule tissues. To clarify this, further studies, such as merging Cs imaging with rhizobia staining or conducting experiments using artificial nodules, will be necessary. Additionally, because nutrient uptake and distribution mechanisms may differ between symbiotic and non-symbiotic conditions, results such as 137Cs imaging should be regarded as specific to the root nodule symbiotic condition.Increasing exchangeable K concentration in soil has been widely regarded as the most effective strategy for reducing Cs transfer, regardless of species. We also observed a significant negative correlation between soil exchangeable K and shoot Cs concentrations in soybean (Fig. 4). However, ANCOVA showed the different relationships of different nodulation genotypes, suggesting that nodule formation influences Cs uptake at the flowering stage. In nodules, K supports ATP supply and nitrogenase activity and is positively associated with carbon and nitrogen transport44,45,46. In the hyper-nodulating genotype, increased total photosynthate allocation to nodules may result from enhanced nodulation in lateral root and reduced root elongation47. Changes in the root system may have increased carbon costs in roots and altered nutrient uptake mechanisms, potentially affecting translocation and consequently reducing Cs translocation to shoot. This suggestion is supported by the different elemental distributions in roots and nodules observed in the hyper-nodulating genotype compared with those in other genotypes (Supplementary Fig. S2). In contrast, there were no significant differences among genotypes at the maturity stage, indicating that seed Cs levels remain homeostatic despite genotypic differences in Cs uptake at the flowering stage.Furthermore, our results suggest that nodules may contribute to suppressing Cs translocation to shoot (Fig. 5). The high Cs concentrations observed in nodules (Fig. 2a,b) indicate that nodules may function as “buffer zones”. While heavy metals and alkali metals generally differ in terms of chemical properties and translocation mechanisms, nodules have been proposed to serve as buffer zones to mitigate heavy metals48,49,50. We also found that increased nodule number was associated with increased shoot K concentrations (Supplementary Fig. S7), suggesting that preferential K translocation to the shoot may have indirectly promoted Cs accumulation in nodules. Notably, δ15N, one of nitrogen fixation activity indicators, suggested that nitrogen fixation may not contribute to reduced Cs translocation to shoot (Supplementary Fig. S5). In contrast, Cs accumulation in nodules did not appear to inhibit nitrogen fixation activity (Supplementary Fig. S6). Further studies should use more quantitative indicators of nitrogen fixation activity, such as acetylene reduction assays, to examine its relationship with Cs dynamics.Elemental uptake and distribution in nodules primarily occur via two pathways, i.e. direct transport through the nodule epidermis and cortex51 and translocation from roots via vascular tissues into nodules52. Several K transporters, including HAK5, GORK, SKOR and KUP7, are expressed in the epidermal and vascular tissues53,54,55,56. Interestingly, our study found that the suppression of Cs translocation was more strongly associated with nodule number than with nodule dry weight (Fig. 5). In soybean nodules, the vascular bundles extend radially around the infected zone57,58. Therefore, the increase in the nodule number implies an expansion of the total epidermal and vascular tissue area. Treating transporter density per unit membrane area as approximately constant, this expansion broadens the expression domain of K transporters at these sites and, in turn, altering Cs translocation. Verification of this hypothesis requires functional analyses of transporters, including assessments of Cs selectivity, and spatial localization of expression in the relevant regions. As another hypothesis, our findings suggest that a single nodule does not accumulate Cs indefinitely. Soybean forms determinate nodules, where nodule development is driven by cell expansion rather than division59. To facilitate cell expansion, intercellular potential balance needs to be maintained, potentially absorbing Cs in nodules during nodule development. However, in mature nodules, an elevated intracellular potential may limit further passive Cs transport. K transporters such as GmHAK5 and LjKUP, which are expressed in nodules, have been identified, but their involvement in active Cs sequestration within nodules remains unclear60,61. To clarify these physiological mechanisms, it is necessary to investigate the subcellular localization of elements and gene expression within nodules spatiotemporally, in accordance with nodule developmental stages.For other cations, Cs+, K+, Na+ and Rb+ are chemically similar and generally exhibit competitive uptake due to overlapping parts of transport pathways7. In this study, exchangeable Na and Rb concentrations in the soil increased under K-deficient conditions, like Cs (Table S1). Regarding Rb distribution within the plant, Rb concentrations in nodules tended to increase, similar to Cs, and nodule number appeared to be associated with reduced Rb translocation to shoot (Figs. 2, S1, S2, S3 and S7). These similar dynamics of Cs and Rb suggest the involvement of a common transport mechanism. Further studies are needed to identify nodule-localized transporters responsible for Cs and Rb uptake and to clarify their ion selectivity. In contrast, Na was predominantly distributed to the roots, and no significant relationship was observed between nodule traits and Na translocation patterns (Figs. 2, S1, S2, S3 and S7). In legumes, Na taken up from the soil is retained prior to crossing the endodermis, with reduced levels in xylem vessels, thereby limiting its upward movement62. Although recent work in rice suggested that Na indirectly influences Cs transport through Na transporters63, Cs and Rb transport is thought to rely mainly on K transport systems7. This indicates that Na is likely distributed through a distinct mechanism from Cs and Rb. To elucidate differences in these distribution mechanisms, future studies of rhizobia-inoculated soybean should employ techniques such as isotope tracing and elemental mapping. Importantly, because exchangeable Na concentrations in soil differ substantially from those of Rb and Cs, potential ionic interactions and competition among these monovalent cations should be carefully considered.ConclusionOur study revealed the influence of nodules on the mechanism of Cs translocation to shoot. Through field experiments conducted using soybean genotypes with different nodulation abilities, comparison of elemental concentrations in each organ revealed that Cs was highly accumulated in nodules. Similarly, spatial mapping of 137Cs in the root system revealed that 137Cs was predominantly distributed in nodules. These results highlight the importance of nodules as key sites for Cs sequestration. This study also demonstrated a significant negative correlation between nodule number and shoot Cs concentration, suggesting that increased nodulation may suppress Cs translocation to shoot. These findings provide fundamental insights into the potential use of root nodule symbiosis as a strategy for mitigating Cs transfer to shoots. To further elucidate the mechanisms underlying Cs accumulation in nodules and its suppressed translocation to shoot, spatiotemporal analyses of elemental distribution and gene expression within nodules are needed.
Data availability
Raw data were generated at Hokkaido University. Derived data supporting the findings of this study are available from Kazuki Murashima on request.
ReferencesShinano, T. Mitigation of radioactive contamination from farmland environment and agricultural products. MESE 2, 454–461 (2016).Article
Google Scholar
Zhu, Y. & Smolders, E. Plant uptake of radiocaesium: A review of mechanisms, regulation and application. J. Exp. Bot. 51, 1635–1645 (2000).Article
CAS
PubMed
Google Scholar
Fujimura, S. et al. Theoretical model of the effect of potassium on the uptake of radiocesium by rice. J. Environ. Radioact. 138, 122–131 (2014).Article
CAS
PubMed
Google Scholar
Matsunami, H., Uchida, T., Kobayashi, H., Ota, T. & Shinano, T. Comparative dynamics of potassium and radiocesium in soybean with different potassium application levels. J. Environ. Radioact. 233, 106609. https://doi.org/10.1016/j.jenvrad.2021.106609 (2021).Article
CAS
PubMed
Google Scholar
MAFF, NARO & NIAES. Factors and Countermeasure of Soybean with High Radioactive Cesium Concentration. Investigation of Factors and Result of Trial Examination. https://www.maff.go.jp/j/kanbo/joho/saigai/pdf/youin_daizu_3.pdf (2015).Kato, N. et al. Potassium fertilizer and other materials as countermeasures to reduce radiocesium levels in rice: Results of urgent experiments in 2011 responding to the Fukushima Daiichi Nuclear Power Plant accident. Soil Sci. Plant Nutr. 61, 179–190 (2015).Article
CAS
Google Scholar
White, P. J. & Broadley, M. R. Tansley Review No. 113: Mechanisms of caesium uptake by plants. New Phytol. 147, 241–256 (2000).Article
CAS
Google Scholar
Qi, Z. et al. The high affinity K+ transporter AtHAK5 plays a physiological role in planta at very low K+ concentrations and provides a caesium uptake pathway in Arabidopsis. J. Exp. Bot. 59, 595–607 (2008).Article
CAS
PubMed
Google Scholar
Rai, H. et al. Cesium uptake by rice roots largely depends upon a single gene, HAK1, which encodes a potassium transporter. Plant Cell Physiol. 58, 1486–1493 (2017).Article
ADS
CAS
PubMed
Google Scholar
Nieves-Cordones, M. et al. Production of low-Cs+ rice plants by inactivation of the K+ transporter OsHAK1 with the CRISPR-Cas system. Plant J. 92, 43–56 (2017).Article
ADS
CAS
PubMed
Google Scholar
Chao, M. et al. Structural features and expression regulation analysis of potassium transporter gene GmHAK5 in soybean (Glycine max L.). Plant Growth Regul. 102, 471–483 (2024).Article
CAS
Google Scholar
Broadley, M. R., Escobar-Gutierrez, A. J., Bowen, H. C., Willey, N. J. & White, P. J. Influx and accumulation of Cs+ by the akt1 mutant of Arabidopsis thaliana (L.) Heynh. lacking a dominant K+ transport system. J. Exp. Bot. 52, 839–844 (2001).Article
CAS
PubMed
Google Scholar
Adams, E., Miyazaki, T., Saito, S., Uozumi, N. & Shin, R. Cesium inhibits plant growth primarily through reduction of potassium influx and accumulation in Arabidopsis. Plant Cell Physiol. 60, 63–76 (2019).Article
ADS
CAS
PubMed
Google Scholar
Kanter, U., Hauser, A., Michalke, B., Dräxl, S. & Schäffner, A. R. Caesium and strontium accumulation in shoots of Arabidopsis thaliana: genetic and physiological aspects. J. Exp. Bot. 61, 3995–4009 (2010).Article
CAS
PubMed
PubMed Central
Google Scholar
Hirayama, T., Takeuchi, M., Nakayama, H. & Nihei, N. Effects of decreasing radiocesium transfer from the soil to soybean plants and changing the seed nutrient composition by the increased application of potassium fertilizer. Bull. Fukushima Agric. Technol. Centre (Jpn. Engl. Abstr.) 9, 1–10 (2018).
Google Scholar
IAEA. Environmental Transfer of Radionuclides in Japan Following the Accident at the Fukushima Daiichi Nuclear Power Plant: Report of Working Group 4 Transfer Processes and Data for Radiological Impact Assessment Subgroup 2 on Fukushima Data (IAEA, 2020).
Google Scholar
Kubo, K. et al. Comparative study of radioactive cesium transfer from soil to peanut and soybean. Soil Sci. Plant Nutr. 67, 707–715 (2021).Article
CAS
Google Scholar
Nihei, N. et al. The concentration distributions of Cs in soybean seeds. Radioisotopes 66, 235–242 (2017).Article
CAS
Google Scholar
Kurokawa, K. et al. Advanced approach for screening soil with a low radiocesium transfer to brown rice in Fukushima based on exchangeable and nonexchangeable potassium. Sci. Total Environ. 743, 140458. https://doi.org/10.1016/j.scitotenv.2020.140458 (2020).Article
CAS
PubMed
Google Scholar
Ogasawara, S. et al. Phytoavailability of 137Cs and stable Cs in soils from different parent materials in Fukushima, Japan. J. Environ. Radioact. 198, 117–125 (2019).Article
CAS
PubMed
Google Scholar
Suzuki, M. et al. Effects of cattle manure compost application on crop growth and soil-to-crop transfer of cesium in a physically radionuclide-decontaminated field. Sci. Total Environ. 908, 167939. https://doi.org/10.1016/j.scitotenv.2023.167939 (2024).Article
CAS
PubMed
Google Scholar
Dupré De Boulois, H., Voets, L., Delvaux, B., Jakobsen, I. & Declerck, S. Transport of radiocaesium by arbuscular mycorrhizal fungi to Medicago truncatula under in vitro conditions. Environ. Microbiol. 8, 1926–1934 (2006).Article
Google Scholar
Joner, E. J. et al. No significant contribution of arbuscular mycorrhizal fungi to transfer of radiocesium from soil to plants. Appl. Environ. Microbiol. 70, 6512–6517 (2004).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Dupré De Boulois, H. et al. Role and influence of mycorrhizal fungi on radiocesium accumulation by plants. J. Environ. Radioact. 99, 785–800 (2008).Article
PubMed
Google Scholar
Ivanov, S. et al. Rhizobium–legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc. Natl. Acad. Sci. U.S.A. 109, 8316–8321 (2012).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Fedorova, E. E. et al. Potassium content diminishes in infected cells of Medicago truncatula nodules due to the mislocation of channels MtAKT1 and MtSKOR/GORK. J. Exp. Bot. 72, 1336–1348 (2020).Article
PubMed Central
Google Scholar
Cakmak, I., Hengeler, C. & Marschner, H. Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J. Exp. Bot. 45, 1245–1250 (1994).Article
CAS
Google Scholar
Ragel, P., Raddatz, N., Leidi, E. O., Quintero, F. J. & Pardo, J. M. Regulation of K+ nutrition in plants. Front. Plant Sci. https://doi.org/10.3389/fpls.2019.00281 (2019).Article
PubMed
PubMed Central
Google Scholar
Gober, J. W. & Kashket, E. R. K+ regulates bacteroid-associated functions of Bradyrhizobium. Proc. Natl. Acad. Sci. U.S.A. 84, 4650–4654 (1987).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Gyuricza, V., Dupré de Boulois, H. & Declerck, S. Effect of potassium and phosphorus on the transport of radiocesium by arbuscular mycorrhizal fungi. J. Environ. Radioact. 101, 482–487 (2010).Article
CAS
PubMed
Google Scholar
ten Hoopen, F. et al. Competition between uptake of ammonium and potassium in barley and Arabidopsis roots: molecular mechanisms and physiological consequences. J. Exp. Bot. 61, 2303–2315 (2010).Article
PubMed
PubMed Central
Google Scholar
Xia, X., Ma, C., Dong, S., Xu, Y. & Gong, Z. Effects of nitrogen concentrations on nodulation and nitrogenase activity in dual root systems of soybean plants. Soil Sci. Plant Nutr. 63, 470–482 (2017).Article
CAS
Google Scholar
Mirriam, A. et al. Role of phosphorus and inoculation with Bradyrhizobium in enhancing soybean production. Adv. Agric. 2023, 3231623. https://doi.org/10.1155/2023/3231623 (2023).Article
Google Scholar
Hamaguchi, H. et al. Nitrogen fertilization affects yields and storage compound contents in seeds of field-grown soybeans cv Enrei (Glycine max L) and its super-nodulating mutant En-b0–1 through changing N2 fixation activity of the plants. Soil Soil Sci. Plant Nutr. 66, 299–307 (2020).Article
CAS
Google Scholar
Watanabe, T., Urayama, M., Shinano, T., Okada, R. & Osaki, M. Application of ionomics to plant and soil in fields under long-term fertilizer trials. SpringerPlus 4, 781. https://doi.org/10.1186/s40064-015-1562-x (2015).Article
CAS
PubMed
PubMed Central
Google Scholar
Bray, R. H. & Kurtz, L. T. determination of total, organic, and available forms of phosphorus in soils. Soil Sci. 59, 39–46 (1945).Article
ADS
CAS
Google Scholar
Kawamoto, T. Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch. Histol. Cytol. 66, 123–143 (2003).Article
PubMed
Google Scholar
Kobayashi, N. I., Tanoi, K., Hirose, A. & Nakanishi, T. M. Characterization of rapid intervascular transport of cadmium in rice stem by radioisotope imaging. J. Exp. Bot. 64, 507–517 (2013).Article
CAS
PubMed
Google Scholar
Udvardi, M. & Poole, P. S. Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol. 64, 781–805 (2013).Article
CAS
PubMed
Google Scholar
Ma, Y., Xiao, C., Liu, J. & Ren, G. Nutrient-dependent regulation of symbiotic nitrogen fixation in legumes. Hortic. Res. 12, uhae321. https://doi.org/10.1093/hr/uhae321 (2025).Article
CAS
PubMed
Google Scholar
Li, Y. et al. Metal nutrition and transport in the process of symbiotic nitrogen fixation. Plant Commun. 5, 100829. https://doi.org/10.1016/j.xplc.2024.100829 (2024).Article
CAS
PubMed
PubMed Central
Google Scholar
Shinano, T. et al. Varietal difference in radiocesium uptake and transfer from radiocesium deposited soils in the genus Amaranthus. Soil Sci. Plant Nutr. 60, 809–817 (2014).Article
CAS
Google Scholar
Domínguez-Ferreras, A., Muñoz, S., Olivares, J., Soto, M. J. & Sanjuán, J. Role of potassium uptake systems in Sinorhizobium meliloti osmoadaptation and symbiotic performance. J. Bacteriol. 191, 2133–2143 (2009).Article
PubMed
PubMed Central
Google Scholar
Mengel, K., Haghparast, M.-R. & Koch, K. The effect of potassium on the fixation of molecular nitrogen by root nodules of Vicia faba. Plant Physiol. 54, 535–538 (1974).Article
CAS
PubMed
PubMed Central
Google Scholar
Lynd, J. Q., Odell, G. V. Jr. & McNew, R. W. Soil potassium effects on nitrogenase activity with associated nodule components of hairy vetch at anthesis. J. Plant Nutr. 4, 303–318 (1981).Article
CAS
Google Scholar
Cao, H.-R. et al. Carbon-nitrogen trading in symbiotic nodules depends on magnesium import. Curr. Biol. 32, 4337–4349 (2022).Article
CAS
PubMed
Google Scholar
Ito, S. et al. Real-time ananlysis of translocation of photosynthates to nodules in soybean plants using 11CO2 with a positron-emitting tracer imaging system (PETIS). Radioisotope (Jpn. Engl. Abstr.) 59, 145–154 (2010).CAS
Google Scholar
Chen, W.-M., Wu, C.-H., James, E. K. & Chang, J.-S. Metal biosorption capability of Cupriavidus taiwanensis and its effects on heavy metal removal by nodulated Mimosa pudica. J. Hazard. Mater. 151, 364–371 (2008).Article
CAS
PubMed
Google Scholar
Wani, P. A., Khan, Md. S. & Zaidi, A. Effect of metal-tolerant plant growth-promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch. Environ. Contam. Toxicol. 55, 33–42 (2008).Article
CAS
PubMed
Google Scholar
Guo, J. & Chi, J. Effect of Cd-tolerant plant growth-promoting rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr in Cd-contaminated soil. Plant Soil 375, 205–214 (2014).Article
CAS
Google Scholar
Slatni, T., Krouma, A., Gouia, H. & Abdelly, C. Importance of ferric chelate reductase activity and acidification capacity in root nodules of N2-fixing common bean (Phaseolus vulgaris L.) subjected to iron deficiency. Symbiosis 47, 35–42 (2009).Article
CAS
Google Scholar
Roy, S. et al. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell 32, 15–41 (2020).Article
CAS
PubMed
Google Scholar
Gaymard, F. et al. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647–655 (1998).Article
CAS
PubMed
Google Scholar
Han, M., Wu, W., Wu, W.-H. & Wang, Y. Potassium transporter KUP7 is involved in K+ acquisition and translocation in Arabidopsis root under K+-limited conditions. Mol. Plant 9, 437–446 (2016).Article
CAS
PubMed
Google Scholar
Qin, Y.-J., Wu, W.-H. & Wang, Y. ZmHAK5 and ZmHAK1 function in K+ uptake and distribution in maize under low K+ conditions. J. Integr. Plant Biol. 61, 691–705 (2019).Article
CAS
PubMed
Google Scholar
Drain, A. et al. Functional characterization and physiological roles of the single Shaker outward K+ channel in Medicago truncatula. Plant J. 102, 1249–1265 (2020).Article
ADS
CAS
PubMed
Google Scholar
Guinel, F. C. Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types. Botany 87, 1117–1138 (2009).Article
Google Scholar
Livingston, D., Tuong, T., Nogueira, M. & Sinclair, T. Three-dimensional reconstruction of soybean nodules provides an update on vascular structure. Am. J. Bot. 106, 507–513 (2019).Article
PubMed
PubMed Central
Google Scholar
Crespi, M. & Gálvez, S. Molecular mechanisms in root nodule development. J. Plant Growth Regul. 19, 155–166 (2000).Article
CAS
PubMed
Google Scholar
Desbrosses, G., Kopka, C., Ott, T. & Udvardi, M. K. Lotus japonicus LjKUP Is induced late during nodule development and encodes a potassium transporter of the plasma membrane. MPMI 17, 789–797 (2004).Article
CAS
PubMed
Google Scholar
Liu, J. et al. Investigate the effect of potassium on nodule symbiosis and uncover an HAK/KUP/KT member, GmHAK5, strongly responsive to root nodulation in soybean. J. Plant Biol. 65, 459–471 (2022).Article
CAS
Google Scholar
Iqbal, M. S., Clode, P. L., Malik, A. I., Erskine, W. & Kotula, L. Salt tolerance in mungbean is associated with controlling Na and Cl transport across roots, regulating Na and Cl accumulation in chloroplasts and maintaining high K in root and leaf mesophyll cells. Plant Cell Environ. 47, 3638–3653 (2024).Article
CAS
PubMed
Google Scholar
Kanno, S. et al. Rice Na+ absorption mediated by OsHKT2;1 affected Cs+ translocation from root to shoot under low K+ environments. Front. Plant Sci. https://doi.org/10.3389/fpls.2024.1477223 (2024).Article
PubMed
PubMed Central
Google Scholar
Download referencesAcknowledgementsThis work was financially supported by the Japan Science and Technology Agency (JST), project no. JPMJSP2119 “Support for Pioneering Research Initiated by the Next Generation (SPRING)”. Additional support was provided by JSPS KAKENHI Grant-in-Aid for Scientific Research B (23K21251); JSPS KAKENHI Grant-in-Aid for Scientific Research C (26511006); Kuribayashi Scholarship Academic Foundation. Bradyrhizobium japonicum USDA110 and soybean seed (En1282 and En-b0-1) was kindly provided by the National Agriculture and Food Research Organization (NARO; formerly NIAS), Japan.Author informationAuthors and AffiliationsGraduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, JapanKazuki Murashima, Hayato Maruyama, Toshihiro Watanabe & Takuro ShinanoFaculty of Food and Agricultural Sciences, Fukushima University, Fukushima, 960-1248, JapanNaoto NiheiRIKEN CSRS, Tsukuba, Ibaraki, 305-0074, JapanNao OkumaAuthorsKazuki MurashimaView author publicationsSearch author on:PubMed Google ScholarNaoto NiheiView author publicationsSearch author on:PubMed Google ScholarNao OkumaView author publicationsSearch author on:PubMed Google ScholarHayato MaruyamaView author publicationsSearch author on:PubMed Google ScholarToshihiro WatanabeView author publicationsSearch author on:PubMed Google ScholarTakuro ShinanoView author publicationsSearch author on:PubMed Google ScholarContributionsK.M.: Writing—original draft, visualization, methodology, investigation, statistical analysis. N.O.: Statistical analysis, writing—review & editing. N.N.: Investigation, writing—review & editing. H.M., T.W., & T.S.: Investigation, supervision, resources, writing—review & editing. All authors have read and agreed to the published version of the manuscript.Corresponding authorCorrespondence to
Takuro Shinano.Ethics declarations
Competing interests
The authors declare no competing interests.
Additional informationPublisher’s noteSpringer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.Supplementary InformationSupplementary Information.Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Reprints and permissionsAbout this articleCite this articleMurashima, K., Nihei, N., Okuma, N. et al. Cesium accumulation in nodules is involved in mitigating cesium transfer to shoot.
Sci Rep 15, 44449 (2025). https://doi.org/10.1038/s41598-025-28137-9Download citationReceived: 04 July 2025Accepted: 07 November 2025Published: 24 December 2025Version of record: 24 December 2025DOI: https://doi.org/10.1038/s41598-025-28137-9Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy shareable link to clipboard
Provided by the Springer Nature SharedIt content-sharing initiative
KeywordsCesiumNodulePotassiumRadioisotope imagingRoot nodule symbiosis More
