Keywords

Introduction

Strontium (symbol Sr, atomic no. 38) is a natural and commonly occurring alkaline earth metal (lying in group IIa, period 5, sandwiched vertically between calcium and barium). The mineral was discovered in 1790 by Adair Crawford and William Cruickshank at Strontian (Scotland). Sr ore is usually found in nature in the form of minerals like celestite (SrSO4), and strontianite (SrCO3); however, it can form a variety of compounds, which are either water soluble or not. Naturally occurring stable (non-radioactive) Sr exists in four stable isotopes, viz.84Sr, 86Sr, 87Sr and 88Sr (ATSDR 2004a; Therapeutic Goods Administration 2014; Qi et al. 2015). Furthermore, some 30 radioactive strontium isotopes are known, the most important one being 90Sr, which is formed during nuclear weapons explosions or in nuclear reactors and was released into the environment by fallouts following accidents like Chernobyl Nuclear Power Plant (NPP) in 1986 and Fukushima NPP in 2011 (Sanzharova et al. 2005; Lipscy et al. 2013). 90Sr is a β-radiation emitter with a radioactive half-life of 28.8 years and hazardous to health as it resembles calcium and creates metabolic imbalance (Merz et al. 2016). The radioactive decay through β emission of 90Sr subsequently produces 90Y (yttrium) and 90Zr (zirconium). Once absorbed inside the body, 90Sr causes bone cancer, leukaemia and softening of tissues situated around the bone and bone marrow and has lasting effects (ATSDR 2004b). Because of high toxicity and capability to be readily involved in geochemical and biological migration processes, 90Sr is a particularly hazardous radionuclide (Sanzharova et al. 2005). However, strontium also finds application in treating and preventing diseases like postmenopausal osteoporosis and resultant bone fractures (O’Donnell et al. 2008; Bolland and Grey 2014; Nakano 2016), but the use has been somewhat reduced due to significant safety concerns, particularly the risk of using Sr with patients having a history of ischemic heart disease or venous thromboembolism (Sowa et al. 2014; www.tga.gov.au/alert/strontium-ranelateprotos-and-risk-adverse-events-0; accessed on: 1 Mar 2016). Humans get exposed to radionuclides either directly or indirectly by diverse pathways like consumption of contaminated food or water (Ruttenber et al. 1984; Fowler et al. 1987; Eisenbud and Gesell 1997; Arora et al. 2008). 90Sr, due to rather high solubility in water, once inside the body, gets deposited in bones and teeth (Volkle et al. 1989). Similarly, 90Sr also gets accumulated within plants depending on factors like soil properties, climate, biosphere, and particular species and populations (subspecies, cultivars) etc. (Yablokov et al. 2008).

90Sr in Soil: Its Behaviour and Consequences

Varying meteorological conditions enhance airborne transport of radioactive aerosols from one place to another followed by deposition from atmosphere to soil. After precipitation, the fate of 90Sr is affected by different physico-chemical processes in soil-water-plant compartments (Ehlken and Kirchner 2002). The global precipitation rate varies strongly but has a significant correlation with levels of 90Sr in soil and grass (Bolsunovsky and Dementyev 2011). 90Sr has a greater mobility and migrates faster downward into the soil (especially in mineral (sandy) and organic soils) as compared to other radionuclides like 241Am (Americium), 239+240Pu (Plutonium) and 137Cs (Cesium) (Gastberger et al. 2000; Solovitch-Vella et al. 2007; Chawla et al. 2010). Soil particles are a very important reservoir of 90Sr in the terrestrial environment (Lee and Clark 2005). Sr is also known to compete with its macrohomologue calcium for exchange sites in minerals (Strebl et al. 2007). Five to tenfold increased mobility and bioavailability of 90Sr has been observed in the non-remediated ecosystems close to Chernobyl (Warner and Harrison 1993). This increase in 90Sr with passage of time may be attributed to the ion-exchange mechanism by soil components and the relatively high concentrations of the radionuclide within the soil (Maskalchuk et al. 2014). Therefore, 90Sr distribution in ecosystems includes transfer into the food chain and entering the human body. Next to 137Cs, 90Sr has the potential to significantly contribute to internal ingestion dose (Gupta et al. 2016a).

The migration of 90Sr in the solid phase of the soil–soil solution–plant system is computed by a concentration factor (CF) defined as CF = [90Sr]p/[90Sr]s, where [90Sr]p and [90Sr]s are the equilibrium specific activities of 90Sr in plant and soil, respectively, expressed in Bq kg−1 (Sanzharova et al. 2005). The CF depends on a number of parameters like the properties of soil, plant and calcium (macrohomologue of Sr) (1983). Maskalchuk et al. (2014) derived an equation to estimate the migration of 90Sr from soil to plants, which includes key characteristics of soil, content of exchangeable Ca2+ and fraction of exchangeable 90Sr2+ in soil and an exchange selectivity coefficient for the 90Sr2+–Ca2+ cation pair. The model suggests reduction of 90Sr migration in the soil–plant system by liming (in case of acidic soils; depending on the cation-exchange capacity of the soil in question) and also by introducing soil sorbents with high sorption potential like organozeolites (Maskalchuk et al. 2014). Thus, long-term soil uptake of 90Sr is strongly influenced by the pedological and agronomic characteristics of the soil and agricultural practices (Koranda and Robison 1978).

Claus et al. (1990) reported a 90Sr transfer factor (TF; mean value 0.18) in ten rye fields with podzolic soils near Bremen, Germany, correlated positively with organic content of soil and negatively with Ca and P content. Further, Rabideau et al. (2005) performed real-time performance studies and consequent modelling of a permeable reactive barrier constructed of a natural zeolite material at the West Valley Demonstration Project in western New York State. Changes in soil temperature and moisture content have a considerable impact on the oxidation states (speciation) and consequently, the geochemical forms of 90Sr in soil (Kovacheva et al. 2014). The concept of “effective half-life” as an indicator of long-term decay kinetics of a radionuclide in an environmental compartment (soil/water/plant) is also being reviewed recently (Corcho-Alvarado et al. 2016). The effective half-life may be expressed as close to ecological half-life and is calculated by using a regression analysis of the specific activity (expressed in mBq kg−1 dry weight of soil), assuming that the specific activity in the environmental compartment decreases exponentially with time. The effective half-life integrates all processes that potentially affect the activity and decay of the radionuclides in the compartment including physical radioactive decay (Prӧhl et al. 2006; IAEA 2009).

Limited data are available on distribution of artificial radionuclides in meadow soils. However, radionuclide behaviour in the forest environment is becoming an important area of research in radioecology. Pourcelot et al. (2007) pointed out that 90Sr activity concentrations in milk samples from cows that grazed in Alpine pastures are more elevated and show lower variability than that in soil and grass samples from the same area. Lukšienė et al. (2015) studied the spatial distribution of 90Sr and other artificial radionuclide activity and concentration in the top layer (0–10 cm) of undisturbed meadow soils in Chernobyl NPP fallout affected areas of Lithuania . Therefore, milk might be a more sensitive indicator of 90Sr contamination than soil or grass samples (Pourcelot et al. 2007; Kamenova-Totzeva et al. 2017). As early as in 1959, Lee (1959) reported estimated 90Sr in soil, runoff and wheat. Gustafson (1959) reported 90Sr accumulation of radioactivity in the kernels of Thatcher wheat which was about one-tenth of that in leaves and stems. Subsequently, Menzel (1960) found that only a small portion of 90Sr (10%) deposited on cultivated soils were removed in runoff. Other than small plants (crops, etc.) seasonal and multi-year dynamics of Chernobyl-derived 90Sr accumulation in woods are investigated by Shcheglov and Tsvetnova (2004).

Seasonal variation is more regular and predictable than multiyear variation (Fellows et al. 2009). The multi-year dynamics of 90Sr within the plant body depends on type of landscape, kinetics of plant-available forms of 90Sr and irreversible fixation of 90Sr in the root-abundant soil layer (Shcheglov and Tsvetnova 2004). Mahmoud and El-Hemamy (2005) studied the leakage pattern and consequent hydrological and geological effect of leaking of old (functional since 1961) underground settling tanks at the Egyptian Atomic Energy Authority (EAEA) Inshas site, where the tanks contained 90Sr among other radionuclides. The migration of 90Sr through the unsaturated zone (soil between tank and aquifer) was observed, that depends on soil type, thickness of the unsaturated zone, water velocity and retardation factor, which is a function of the specific distribution coefficient of 90Sr (Mahmoud and El-Hemamy 2005). These studies may be termed as “mini radiological fallouts” as compared to Chernobyl and Fukushima (Maloshtan et al. 2017).

90Sr in Water: Uptake and Interactions

Environmental 90Sr deposited on soil and vegetation likely gets transported into freshwater ecosystems because of washout by spring high waters. Some reports of 90Sr in the food chain and accumulation records are available on Russian, Belorussian and Ukrainian water bodies in post-Chernobyl accident, where the speed of vertical migration of 90Sr was around 2–4 cm year−1 (Outola et al. 2009; Saxen and Koskelainen 2002; Fesenko et al. 2011). The vertical migration in soil resulted in higher absorption of 90Sr in plants having deep root systems (Yablokov et al. 2008) finally leading to increased internal irradiation exposures of people in the contaminated territories (Yablokov et al. 2008).

The concentration of radionuclides in non-human biota is usually defined by biota-to-water concentration ratio (CR) (IAEA 2014) and used to subsequently estimate radiation dose to organisms or humans. For aquatic organisms especially for fishes, CR is usually defined as the ratio between the radionuclide concentration in the fish muscle (as mostly consumed) and the concentration in the surrounding water (Yankovich et al. 2010). For environmental risk assessment, CRmuscle values can be converted to CRwhole-organism using conversion coefficients (Yankovich et al. 2010). However, calculating the conversion factor is difficult, hence predicting the elements/radionuclides (like Sr/90Sr), that accumulate in tissues other than muscle. Sr uptake mechanism resembles the ions of Ca (Kryshev 2006; Outola et al. 2009), with Ca+2 and Sr+2 competing for receptor sites on biological membranes (Van Leeuwen and Koster 2004). According to Saxen and Koskelainen (2002), 95% of 90Sr accumulates in fish skeleton, scales and fins and only 2–5% accumulates in muscles.

Although the CR may ideally be defined as the concentration equilibrium of radionuclides in organisms with its surrounding media, practically, radionuclides in the environment and in organisms vary in a dynamic manner (Batlle et al. 2016). Moreover, to evaluate risk assessment, data on spatio-temporal variation (like data from various sites, longitudinal variation, etc.) must be considered (Avila et al. 2013; Beresford et al. 2016). Hence, it is very difficult accurately predicting risks related to radionuclide contamination from water to aquatic organisms in case of 90Sr. The Fukushima Daiichi NPP (FDNPP) liquid release has given us insight of what may happen to seawater and marine biota after such an accident. Marine mussels (Septifer virgatus) provide an important animal system to assess the status of 90Sr uptake and accumulation in marine biota on a spatio-temporal basis (Karube et al. 2016). Nelson (1962) studied 90Sr concentration in freshwater clams and their shells; the study may be used as indicators of the 90Sr contamination of their environment and helpful in predicting the concentrations within the organisms. Studies on the dispersion of 90Sr from FDNPP site along the Pacific coast of eastern Japan (north direction by coastal current) and radiostrontium activity in coastal areas have revealed the environmental aspects related to aquatic ecosystems human safety assessments (Fujimoto et al. 2015; Castrillejo et al. 2016; Konovalenko et al. 2016). Fujimoto et al. (2015) reported correlation of fish contamination by beta emitting radionuclides and their concentration in marine water in and around Fukushima FDNPP harbour. The investigations include Japanese rockfish (Sebastes cheni), brown hakeling (Physiculus maximowiczi) and fat greenling (Hexagrammos otakii).

However, according to the study by Tomilin et al. (1987), the accumulation of radiostrontium in mammals is surprisingly low as evident from experiments being conducted on pigs fed with contaminated mine water to their food ratio as a salt additive. Degteva et al. (1994) accounted the dose received by individuals residing on the adjoining banks of Techa river (Russia) and its flood plains due to release of fission products (primarily 90Sr) from the plutonium production facility “Mayak” from 1949 to 1956. The medium dose to the red bone marrow was about 250 mSv and the mean dose about 400 mSv (Degteva et al. 1994, 1996, 2000). Yablokov et al. (2008) studied the secondary 90Sr contamination of freshwater ecosystems and found that the vertical migration velocity of 90Sr in flood plains, lowland moors, peat bogs, etc. is about 2–4 cm year−1, where plants play a major role in absorption and subsequent taking it to the surface again. This soil to surface transfer leads to a persisting activity in the upper soil horizons and consequently to doses of internal irradiation in the contaminated territories. Delistraty and Van Verst (2009) measured the tissue radiostrontium levels in water bird which are compared to upland birds from two time periods (1971–1990 vs. 1991–2009) and different locations (on-site and off-site). On-site median concentration of 90Sr in bones of water birds was significantly higher than those in on-site upland birds (1991–2009) and on-site median concentrations in 1971–1990 were significantly higher than those in 1991–2009 for 90Sr in water bird muscle (Delistraty and Van Verst 2009). Median concentrations of 90Sr in bone were significantly higher than those in muscle for both avian groups (water and upland) and both locations. This study undoubtedly proves that the absorption mechanism of 90Sr in the body is very similar to calcium (Delistraty and Van Verst 2009).

In soil and water, plants are the first links in the transfer chain of 90Sr from the environment to human food (Moyen and Roblin 2010). Vose and Koontz (1959) have compared the Ca and 90Sr absorption by different species of clover and grass grown in pots in three distinct soil types to distinguish species differences in uptaking strontium from the soil.

Metal Uptake by Plants: General Account

Metals in soil exist as a range of chemical species in a dynamic equilibrium; however, because of various factors like soil properties, solubility, ionic potential, biological constituents, etc. only a fraction of soil metal is readily available for plant uptake (Wenzel et al. 2003; Mitra et al. 2014). Therefore, plant-based remediation of contaminated soil (phytoremediation) can either be direct (where plants take up or absorb the metals through roots and subsequently translocate to the upper part of the plant) and rhizoremediation (where pollutants are confined to the rhizosphere only after transformation of the material either by enzymatic or root specific microbial actions) (Kuiper et al. 2004; Reboreda and Cacador 2008). Secretion of root exudates into the soil matrix plays a crucial role in heavy metal availability and uptake by plants (Mitra et al. 2014). However, the plant cell wall is functionally important in controlling metals uptake into the cytosol by immobilizing ions by providing histidyl groups, and extracellular carbohydrates such as callose and mucilage (Manara 2012). Admission of metals into plant tissue typically occurs through the root cellular membrane, where metals are directed towards the xylem through apoplast (Salt and Rauser 1995). Roots have high affinity chemical receptors to transport the ions into cells (Salt and Kramer 2000).

Effective reduction of heavy metals (HMs) in cytological active areas like cytoplasm and plasmids in the cells is mainly performed by common HM transporters involved in transportation to vacuole or in exclusion at plasma membrane. These HM transporters thereby help in reducing the levels of toxicity exerted by HMs as free radicals or indirect inducers of ROS in the sites (Inouhe et al. 2015). There are substantial evidences that many hyperaccumulator plants for various HMs are prevailed for these transportation mechanisms via xylem transport systems rather than their different detoxification mechanisms in the cells (Hossain et al. 2012; Socha and Guerinot 2014; Inouhe et al. 2015).

Strontium in Plants

Russell (1965) clarified the interactions of a typical vascular plant and radionuclide, which occurs at two levels: the first level is the aerial or shoot portion and the second level is the soil-root zone or rhizosphere of the plant. Accumulation of radionuclides by these two modes is interrelated, because radionuclides reaching the aerial part like foliage and shoot of the plant will ultimately be shed by the plant and eventually reach the soil (Russell 1965). However, two modes of radionuclide entry into plants are usually difficult to separate in practical scenario.

Significant portions of radionuclide solutions deposited on the leaf surfaces may get entry into the edible parts of plants (as for example, more than 40% of the cesium radioisotope in radishes) (Tukey et al. 1961; Oestling et al. 1989; Fortunati et al. 2004). Uptake of 90Sr is also evident on leaf surfaces as it gets precipitated from atmospheric mist and contacting the leaf (cuticle and epidermis) (Fortunati et al. 2004). Both active and passive transport occurs for 90Sr uptake via leaf epidermis, where it remains, as translocation from leafs to other plant parts is not common (Liu et al. 2016). According to Comar and Wasserman (1964), foliar uptake of Sr bears a non-specific competition with all the alkaline earth metals as compared to calcium alone for binding to sites on exchange compounds in case of passive transport, or on receptors in case of active transport. 90Sr soil to root uptake depends on various physico-chemical factors of the soil components and the water-soluble form of the radionuclide (Fig. 1). Once the metal enters the body of the plant, it may get accumulated within the leaf tissues, while the accumulation of the metal in seeds and fruits is usually low (Asgari and Cornelis 2015). Even roots show lower activity in 90Sr accumulation and translocation as compared to shoots (Wang et al. 2017). Willey (2014) has reported similar findings where plants showed more Sr in green shoots than woody parts, which is probably due to higher activity and flow of nutrients in green parts of the plants.

Fig. 1
figure 1

Overview of uptake mechanism of strontium in plants

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In 1950s, a study was conducted to assess the 90Sr absorption in edible plants like wheat, rice, oats and barley. Lee (1959) studied the uptake of 90Sr into wheat (Thatcher variety) and reported that the radioactivity in the kernels was about one-tenth in comparison with that of leaves and stems; milling of those kernels yielded flour with radioactivity lower than in brans. Ichikawa et al. (1962) reported the uptake of 90Sr in rice due to root absorption from soil. Similar finding of root absorption of 90Sr by rice was corroborated by Menzel et al. (1963), showing the definite observed pattern of radionuclide accumulation by field-grown crops.

Rickard and Price (1990) pointed out a positive correlation between 90Sr concentrations in red canary grass grown near the nuclear reactor of the U.S. Department of Energy (Hanford site) in the eggshells of Canadian geese feeding on that red canary grass. This study was an important example of 90Sr bioaccumulation across the food chain. Paasikallio et al. (1994) studied the soil to plant transfer of 90Sr in different cereals and vegetables, where it was found that green leafy vegetables like lettuce and cabbage showed more accumulation, followed by cereals and tuberous vegetables (potato).

Strontium and Rhizosphere

Determining the plant-available fraction of a radionuclide is difficult considering the rhizospheric zone (Gupta et al. 2016a). The plant root-soil region is completely different from the bulk soil. Plants root exudates typically increase the richness of soil microflora (bacterial and fungal communities) by 1–4 orders of magnitude compared to the adjacent bulk soil that aids to degrade diverse pollutants (Anderson et al. 1994). The availability of metal to the plant depends upon the chemistries between soil fraction and variety of substances that a plant root exudes or releases that creates a micro-environment specific to the plants. Root exudates include: diffusates (e.g. organic or amino acids, inorganic ions, sugars, and water), excretions (e.g. bicarbonates, carbon dioxide, and protons), secretions (e.g. siderophores, mucilage, and allelopathic compounds) which help moderating soil microflora community structure to have a better variety of metabolic capabilities with unique gene pool (Hall 2002; LeDuc and Terry 2005; Mitra et al. 2014; Chatterjee et al. 2017a). As for instance, release of H+ and HCO3 − at root zone actively influences the pH in their immediate vicinity, thus increasing the accessibility of phosphorus and potassium (Gupta et al. 2016a).

Similarly, ammonium (NH4 +) mobilizes Sr on soil surface, leading to increased Sr concentration in soil solution, although it inhibits uptake by plants, like that of calcium. Thus, common ammonium fertilizers like diammonium phosphate (DAP) and NPK may act as inhibitor for the soil to plant transfer of 90Sr after a radioactive fallout in agricultural fields, acting as a countermeasure (Guillén et al. 2017).

Plant growth-promoting rhizobacteria (PGPR) perform an important role in development by reducing the physiological stress in plants, when grown in contaminated soils. By stimulating the production of plant growth regulators like indole acetic acid, gibberellic acid, cytokinins and ethylene, PGPR helps in rhizospheric colonization. This microbial colonization contributes to plant health and better response. Rhizobacteria can also secrete antibiotics, hydrocyanic acid, phosphate solubilizing substances, siderophores and 1-aminocyclopropane-1-carboxylic acid (ACC) to increase bioavailability and root absorption of different metals (Meyer 2000; Davies et al. 2001; Gupta et al. 2016a). Burd et al. (1998) reported that after adding of Kluyvera ascorbata SUD165/26 a related rhizobacteria, germination and growth of Indian mustard (Brassica juncea) seeds was increased by 50–100% in a nickel-contaminated soil.

Number of metal transporter-proteins show significant roles in homeostasis of heavy metals at root cell plasma membranes. Amid diverse group of transporter-proteins, NRAMP (natural resistance-associated macrophage protein), CDF (cation diffusion facilitator) family, ZIP (Zinc importer) families (ZRT, IRT-like Protein; [ZRT—Zinc regulated transporter, IRT—iron regulated transporter]), heavy metal ATPases (HMAs) family like P1B-ATPases, ATP-binding cassette (ABC) transporters, copper transporter (COPT) family proteins, ABC transporters of the mitochondria (ATM), multidrug resistance associated proteins (MRP), Ca2+ cation antiporter (CAX), and yellow-stripe-like (YSL) pleiotropic drug resistance (PDR) transporters are well studied (Dubey 2011; Huang et al. 2012; Gupta et al. 2013, 2016a). A ZIP family transporter with histidine-rich domain is important in activated response and uptake to divalent metal ions (Kramer et al. 2007). Nishida et al. (2008) reported that IRT1 is responsible for transportation of metals like Fe2+, Mn2+, Zn2+ and Cd2+ in root cells of A. thaliana. Internal transporters like HMAs family transporters (P1B-type ATPases) help in loading of metals like Cd and Zn from the surrounding tissues into the xylem and performing as an efflux pump (Kramer et al. 2007). Sequestration of heavy metals at vacuole level is mainly carried out by AtHMA3 transporter present in the tonoplast membrane (Manara 2012; Gupta et al. 2013). Plants have their own general tactics that use vacuolar sequestration through proton pumps like vacuolar proton-ATPase (V-ATPase) and vacuolar protonpyrophosphatase (V-PPase) to isolate metals from metabolically active cytosol and cellular organelles (Dalcorso et al. 2010).

Sr Removal from Soil: Phytoremediation Approach

Removal of 90Sr from soil is an interesting study carried out by different workers. As per the field study of Fuhrmann et al. (2002) on redroot pigweed (Amaranthus retroflexus), Indian mustard (Brassica juncea), and tepary bean (Phaseolus acutifolius) to determine the ability of extraction of 90Sr from contaminated soil, it was found that the redroot pigweed was a most potent accumulator (estimated time required for removal of 50% of 90Sr is 7 years, assuming two crops per year). Calotropis gigantea plants were also studied to remove 90Sr from soil, where Eapen et al. (2006) demonstrated 90% of the radioactivity can be removed within 24 h. Broadley et al. (2003, 2004) and Willey and Fawcett (2006) identified the efficiency of Caryophyllidae (Eudicot plants, viz. amaranth, buckwheat, chards and beets; most of them being agriculturally important plants) clades for the transfer of alkali earth metals particularly 90Sr from soil to roots.

Zheng et al. (2016) studied angiosperm Tillandsia usneoides (Bromeliaceae, known as Spanish moss, an established bio-monitor of air pollution) as a bio-indicator for 90Sr, as this plant can tolerate Sr for an elongated period and has a very high uptake ratio which has a positive correlation with concentration of Sr in solution. It was also reported that high Sr concentration inhibits chlorophyll content due to oxidative stress, while low concentration promotes chlorophyll synthesis in Spanish moss (Zheng et al. 2016). Maxwell et al. (2010) and Amano et al. (2016) reported different methodologies to determine the concentration of 90Sr in edible vegetation samples using liquid scintillation counting (LSC) and inductively coupled plasma (ICP)-mass spectrometry (MS).

Weed plants, in many a times, have been hyperaccumulators of metals or radionuclides (Wenzel et al. 1999; IAEA 2006). The soil-to-plant transfer factor accounts for the uptake of radionuclides via plant roots and represents the activity concentration ratio of the radionuclide per unit dry mass in the plant (Bq kg−1) to that in the soil, designated as Fv (IAEA 2009, 2010). Attar et al. (2016) studied the effect of ageing on the transfer of 90Sr to lettuce (Lactuca sativa) and winter wheat (Triticum aestivum) with respect to a clayey soil and semi-arid environment in Syria. Moderate accumulation of 90Sr from soil may be compensated by high biomass and fast growth (Hernandez-Allica et al. 2008). Several authors have worked on the suitability of rice, wheat, rye and oat where existing data indicates that oats may be a better accumulator of 90Sr as compared to wheat and rye (Krouglov et al. 1997; Soudek et al. 2006; Schimmack et al. 2007). In case of both rice and oats, it was also found that in the main plant where around 99% of 90Sr is stored is the non-edible over-ground parts, i.e. leaves and stems as compared to roots because roots have lower biomass (Tsukada et al. 2005; Lin et al. 2015). As per the available reports, the activity concentration in a nutrient solution of 1 Bq L−1 of 90Sr or 137Cs corresponds to ca. 2 × 10−15 Moles L−1 however, the average concentrations of chemical homologues like K, Ca, and Mg, in soil solution are in the order of 1 mMoles L−1 . Uptake and co-precipitation of radionuclides like radioactive strontium by plants is therefore affected by many soil factors, where cation exchanges reactions regulate the concentration of a competitive ion, like Sr, in soil solution. Sorption of radiostrontium is governed by reversible exchange with major cations like Ca2+. Although Sr is exchanged in preference to Ca in minerals, the preference of the same metal may get changed when organic matters are present (Chu et al. 2015).

Strontium Exposure, Plant Responses and Phytoremediation

Irrespective of biological necessity, plants usually take up several cations present in their root region. When plants are exposed to radionuclide and ionizing radiation, cellular and molecular effects take place, involving direct damage of macromolecules or indirect radiolytic reactions producing reactive oxygen species (ROS) (Gupta et al. 2016b, 2017). Ionizing radiation can induce DNA strand breaks, lipid oxidation, or enzyme denaturation (Gupta and Walther 2014; Gupta et al. 2016a). Antioxidative defence system of plants having enzymes (e.g. superoxide dismutase (SOD) and catalase (CAT)) and metabolites (e.g. ascorbate and glutathione) controls the ROS within cellular systems (Gupta and Sandalio 2012). Plants employ complex coordinated mechanism for metal tolerance mechanisms involving both biochemical and physiological processes. To cope with toxic effects of radionuclides, plants may avoid (restricting the metal uptake) or tolerate (survive in the presence of high internal metal concentration) the stress condition (Chatterjee et al. 2017b). Avoidance mechanism of plants involves concentration reduction of metal entering into the cell by extracellular precipitation, biosorption to cell walls, reduced uptake, and/or by increased efflux (Gupta and Walther 2014; Gupta et al. 2016a). Elaborate physiological responses are also present in plants like intracellular chelation by synthesizing organic acids, amino acids, glutathione (GSH), and/or by metal-binding ligands such as phytochelatins (PCs) and metallothioneins (MTs), vacuolar compartmentalization, glyoxalase systems and up-regulation of antioxidant defence to defy the harmful effects rooted by ROS (Gupta and Sandalio 2012; Gupta et al. 2016a).

Sasmaz and Sasmaz (2009) studied Sr phytoremediation potential in Euphorbia macroclada, Verbascum cheiranthifolium and Astragalus gummifer, where they investigated the roots and shoots of the plants for distribution and accumulation of the metal. The Sr enrichment factors for root (ECR) and shoot (ECS) and mean translocation factors (TLF) of these plants were examined and the authors found that the shoots of these plant (Euphorbia macroclada, Verbascum cheiranthifolium and Astragalus gummifer) were competent Sr bioaccumulator (having high TLF) which may be used in amelioration of Sr-contaminated soil (Sasmaz and Sasmaz 2009). The probable use of coyote willow (Salix exigua) plants for phytoextraction of the soil Sr through the plant roots and into above-ground shoots is being tested by the Department of Energy (DOE), USA, to protect the environment contaminated with 90Sr (Fellows et al. 2009). The study showed that, as plants take up 90Sr from soil, the soil content of the 90Sr is also being reduced. Further, the study also pointed out that the hazard for detectable transfer of 90Sr through the food chain of herbivorous insects from willow trees grown in the Sr-contaminated soil is minor to non-existent (Fellows et al. 2009). Wang et al. (2017) studied phytoremediation of Sr-contaminated soil by Sorghum bicolor. This study examined soil microbial community-level physiological profiles (CLPPs) , where it was found that Sr-spiked soil is having enhanced soil-microbial diversity and activity with considerable augmentation in the height and the stem biomass weight of the plant (with Sr content in tissues decreased in the order of leaves > roots > stems) (Wang et al. 2017).

Conclusion

90Sr is a fission product of uranium (U) and plutonium (Pu). Anthropogenic activities led to discharge and waste disposal of Sr in many places of the world that impacted soil and groundwater. There are certain factors for implementing specific plants for restoration of radionuclide-contaminated sites , which includes relative high levels uptake potential of plants for the radioactive material and growth or high biomass production. Potential plants must amass radionuclide in the above-ground parts at a proportion which significantly exceeds the soil concentration. Several factors limit the application of plant-based techniques that affect the Sr uptake by plants, which include clay/soil particle/minerals properties, and availability of organic matters. However, phytoremediation might be the appropriate and easy technique for restoration of radionuclide-contaminated soil if selected cultivars are used. Therefore, detailed research on plants selection, manipulation of diverse transporters, and explication of anti-stress physiology factors in plants are the area which will be useful to decontaminate Sr-contaminated soil in an eco-friendly manner.