Physiological Aspects of Radionuclide Absorption by Plant Roots

Radioactive pollutants of soils can be classified into two groups with respect to their potential for uptake by higher plant roots. First, there are those which are radioactive isotopes of elements which are known to be either biologically essential or chemically (and presumably physiologically) analogous to essential elements. Members of this group of significance to the root uptake pathway include nuclides of Co, Zn, Mn, Fe, K, Rb, Cs, Ra and Sr. The second group comprises nuclides of elements for which organisms exhibit no known requirement. Particularly prominent members of this group are those 'artificial' radionuclides belonging to the transuranium series, which include Pu, Am, Np and Cm. As a broad rule the degree of plant uptake of the latter elements (which are all exclusively radioactive, possessing no stable isotopes) is many times less than that of the elements in the first group, which exhibit suites of stable and radioactive nuclear species. The outstanding exception to this rule, however, is the element technetium (Tc). This was the first element to be created artificially by man, in 1937, and exhibits two nuclides, one of which ("Tc) is of considerable environmental significance due to its 200000 year half-life and its remarkably high degree of bioaccumulation (see Table 7-14).

While the actinides Pu, Am, Np and Cm are critically important to assessments of the exposure of humans to environmental sources of radioactivity due to their highly hazardous a emissions, the role which the plant root absorption pathway plays in this exposure is relatively small. A conservative estimate of the degree to which plants will incorporate Pu from soil, for instance, is 10% (ie, a soil-to-plant transfer factor of

0.1) (Dahlman et al., 1976) although it can be seen from Table 7-14 that TF values for this element are commonly six orders of magnitude lower than this. In practice the predominant pathway of plant contamination by actinide elements is usually direct contamination due to the deposition and resuspension processes covered in the previous section. In a summary of data collected on plant root uptake from contaminated sites up to 30 years after nuclear weapons testing Dahlman et al. (1976) concluded that the vast majority of these elements remained within the soil, associated at least in part with humic substances. Concentration ratios (soil-to-plant transfer factors) were invariably < 1 in unamended soils and showed a very high degree of variability (up to eight orders of magnitude - see Fig. 7-12). Interestingly, the addition of artificial chelating agents such as DTPA increased the root uptake of Pu in these studies, probably by increasing the fraction of monomeric Pu in the soils and thereby enhancing its physico-chemical mobility. The chelation potential of a number of natural and artificial organic compounds for the actinides was investigated in a study by Bulman (1983) who concluded that both plant root and animal gut absorption of actinide elements may be enhanced by a variety of these compounds. However, the absolute absorption of the transuranics by biological tissues is still relatively low as compared with that of several other radionuclides for which the root uptake pathway is considerably more significant.

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Fig. 7-12. Concentration ratios (ie, soil-to-plant transfer factors) for plutonium and americium at various sites associated with the US nuclear programme. Key to sites: NTS, Nevada test site; SR, Savannah River, South Carolina; OR, Oak Ridge, Tennessee; RF, Rocky Flats, Colorado; NTS, Enewetak Atoll, South Pacific (from Dahlman et al., 1976).

The most extensively studied radionuclides with respect to biological incorporation and the contamination of food chains are l37Cs and 90Sr. The elements Cs and Sr, respectively, belong to groups I and II of the periodic table and as such share common physico-chemical properties with K and Ca. As analogues of these elements 137Cs and 90Sr are readily incorporated by biological tissues and so, historically, the ex istence of these nuclides within the environment as a result of weapons testing and accidental releases from the nuclear industry has resulted in a very large section of the radioecological literature being devoted to them.

137Cs and 90Sr are fundamentally different in their behaviour in soils. l37Cs shows a very high degree of attachment and 'fixation' to soil mineral materials (particularly within the clay fraction - see Cremers et al., 1988) whereas 90Sr remains relatively mobile and hence available for uptake by plant roots. In the case of 137Cs the relative proportion of clayey material within a contaminated soil, and particularly its mineralogy, will strongly determine the degree of soil-to-plant transfer of the nuclide (Bell et al., 1988). Despite the theoretical possibility of its existence as non-exchangeable carbonates, sulphates, phosphates, silicates and sesquioxides, however, most studies have determined that considerably more than 90% of radiostrontium is in exchangeable forms (Francis, 1978). The common factor which strongly affects the plant uptake of each of these nuclides is the similarity, in physiological terms, between the radioions which exist in the environment at 'carrier-free' concentrations and the relatively highly abundant nutrient analogues, which may be present in the soil environment at concentrations many orders of magnitude greater than the radioions themselves. The potential for the control of 137Cs and 90Sr uptake by K and Ca is therefore great although it must not be forgotten in the case of elements such as Cs and Sr that stable isotopes (133Cs and 88Sr) also exist in the natural environment at concentrations considerably greater than those of their radioactive counterparts.

In radioecology the occurrence of different radioisotopes of the same element is commonly encountered. A case in point was the simultaneous deposition of 137Cs (a fission product) and 134Cs (an activation product) from the Chernobyl plume during

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Isotopic Mass

Fig. 7-13. Relative effect of isotopic mass on reaction kinetics, expressed as ]/m2/mt (where m2 and m, are the masses of the nuclides plotted and the most common stable nuclide of the same element, respectively). Biological fractionation is only likely to be important for elements with atomic masses less than ~ 20, especially in the case of deuterium and tritium.

its passage over western Europe in 1986. Initial observations indicated that soil-to-plant transfer factors for deposited 137Cs were lower than for 134Cs and gave rise to speculations that some differential plant uptake of the two nuclides was occurring.

Partial fractionation of isotopes of the same element is known to occur in kinetic systems due to differences in mass. The extent to which this is likely to hold true for a particular pair of isotopes can be estimated using the relationship developed by Bigeleisen (1949) which states that the relative effect of the mass difference of two isotopes on the overall reaction kinetics is equal to the square root of the ratio of the two masses (^m2/m{ - see Bowen, 1979). This relationship is plotted in Fig. 7-13 which indicates that for elements of mass number > 20 the kinetic discrimination between isotopes during reactions, such as those involved during the passage of ions across plant root membranes, would be expected to be negligible. This was tested by Mills (previously unpublished) who examined the uptake of 137Cs and 134Cs by two upland plant species (Calluna vulgaris and Festuca ovina) and found no evidence of discrimination between the two isotopes (Fig. 7-14). By implication a similar lack of discrimination between radioisotopes of Cs and its naturally occurring non-radioactive isotope (133Cs) would be expected.

Fig. 7-14. Relative uptake of 134Cs and 137Cs by two common upland plant species, Festuca ovina and Calluna vulgaris. The solid line in each case is a plot of unity, showing that there is effectively zero discrimination between these two radionuclides during plant uptake (from Mills, previously unpublished).

Of more relevance to the uptake of radionuclides by plants is the question of discrimination between radionuclides and their nutrient analogues. Indeed, the question of whether the physiological mechanisms of ion uptake within the root can discriminate between the radioion and its analogue has been central to the elucidation of the environmental behaviour of 137Cs and 90Sr since the late 1950s. Comar et al. (1957) devised a measure of the degree of discrimination by plants between strontium and calcium which they termed the 'observed ratio' (OR), defined as:

ORsr/c*

A value < 1 implies that calcium is taken up preferentially whereas a value > 1 implies that strontium is taken up preferentially; a value of unity indicates zero discrimination between the two elements. The biggest source of error in applying such ratios to the field situation is the difficulty in determining an accurate [Sr]soil/[Ca]soil ratio, which reflects the extreme difficulty of relating data on the chemical extractability of a radionuclide within a soil to its actual bioavailability. As a result much of the literature evidence on this topic is based on solution culture experiments in which it has been consistently shown that ORSl/Ca values tend to be greater than unity in roots whereas in stems, leaves and seeds the reverse is true. This seems to reflect the preferential translocation of Ca to the above-ground organs of plants, although as the rate of transpiration of a plant decreases Ca transport appears to be diminished in favour of Sr movement. In relation to the highly mobile K and its analogue Cs, however, the absolute degree of internal translocation of both Sr and Ca is low with both elements existing largely as immobile complexes with glucuronic acids (Mortensen and Mar-cusiu, 1963) and pectates (Myttenaere and Masset, 1965).

In solution culture experiments both strontium and caesium show hyperbolic absorption isotherms with respect to the external concentration of the element. Figure 7-15 (a) shows an example of a typical uptake isotherm for Sr while Shaw and Bell (1989) have demonstrated a similar isotherm for Cs. Baker (1981) has referred to such plant uptake responses as 'accumulator' functions and has identified these as being typical of the absorption of elements over which plants can exert some degree of physiological control. Typically, the nutrient elements, including K and Ca, exhibit such isotherms and it can be postulated from the similarity in the uptake patterns of K and Cs on the one hand and Ca and Sr on the other that the radioions share, to some extent, the same uptake mechanisms as the nutrient ions. This has several important implications. Firstly, the direct competition for uptake sites between radioions and nutrient ions means that the external (soil) concentration of one is increased at the expense of the uptake of the other; as the nutrient ions in question are vastly more abundant in soils than radioions it is K and Ca which will be effective in competitively excluding Cs and Sr, respectively. Secondly, the kinetics of this competition are concentration-dependent, so the assumption of first order kinetic movements of

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Fig. 7-15. (a) Hyperbolic absorption isotherm for strontium uptake in wheat (Triticum aestivum). This gives rise to the negative and non-linear relationship between the transfer factor and external concentration of strontium shown in (b) (from Hewamanna, previously unpublished).

radioions into plant tissues, as embodied in the transfer factor concept, are invalid. The result of this is that any increase in a competing ion's concentration in the medium bathing the root will result in a non-linear depression in radioion uptake, whether the competing ion is a stable nuclide of the radioisotope (see, for example, Fig. 7-15(b)) or an analogue with its own chemical identity (Whicker, 1983). Indeed, Jones et al. (1991) determined that, aside from the external ionic environment, the nutritional status of the plant per se may have the same effect.

Shaw and Bell (1991) examined this effect in the case of competition between radiocaesium and the K+ and NH4+ ions during root uptake by wheat (Triticum aestivum). These authors formalised the observed relationships in terms of classical Michaelis - Menten kinetics which necessitates the assumption that each of these ions is taken up by identical sites associated with the root plasmalemma. Lembrechts et al. (1990) found a similar negative and non-linear relationship between the concentration of Ca either in soil or in solution culture and the degree of radiostrontium uptake by lettuce {Lactuca sativa). The principle of competitive exclusion of a radionuclide by an ion analogue may be exploited, with varying degrees of success, as a post-con tamination countermeasure designed to reduce the transmission of radionuclides to either human or animal populations via the soil plant pathway (Shaw, 1993). Applications of fertilisers containing either K or Ca may be more or less effective in reducing Cs and Sr uptake by plants, depending largely on the buffering characteristics of the soil in question (Nisbet, 1993). Generally these treatments are aimed at reducing the fractional molar ratio of the radionuclide with respect to the nutrient analogue so that competition between the two ions will favour the exclusion of the radioion.

Cline and Hungate (1960) applied the concept of the observed ratio to the question of discrimination between the Cs+ and K+ ions. These authors noticed that in bean plants (Viciafaba) the OR was non-constant when the K+ concentration in a nutrient solution was increased, implying that some concentration-dependent effect was altering the degree of selectivity which the plant roots were able exert over these two ions. More recently, Shaw et al. (1992) have identified a critical threshold concentration of K+ below which classical competition kinetics appear to describe adequately the antagonism between the two ions, but above which selectivity of the uptake mechanism is apparently 'switched' in favour of the K+ ion. The exact identity of the uptake machanism is still a matter of debate but may be a pore in the plasmalemma which is able to accommodate several similar ions synchronously in single file (Tester, 1988); any selectivity between Cs and K uptake must be exerted at this level. At present it is clear that the long running question of whether and how plants discriminate between these ions still awaits a final answer, though the implications of the operation of such a mechanism are evidently important. Seasonal variation in the activities of the K+ and Ca2+ ions in soil solutions will cause a variable degree of inhibition of radiocaesium and radiostrontium uptake and this may to some extent explain the degree of variability seen in the soil-to-plant transfer factors for these groups of nuclides.

While Cs and Sr are important because of their global distributions and because of their ability to mimic biologically essential elements, "Tc is of special radio-ecological interest because of its extraordinary mobility and ability to concentrate in plants despite being an 'artificial' element (Wildung et al., 1977) (an excellent review of the environmental behaviour of this element is given by the collection of papers edited by Desmet and Myttenaere, 1986). The element Tc is considered to be 'extinct' on earth; its introduction into our environment over the last 50 years has provided a particularly interesting problem for radioecologists because, as well as being a novel element in the sense that biological systems have had no previous contact with it during their evolution, it has no stable isotopes. Two radionuclides of Tc exist: 99mTc, an activation product, is relatively unimportant as an environmental contaminant because of its short (~ 6 h) half life, whereas "Tc, a fission product of 238U, is long lived (~ 200000 years). The environmental behaviour of this element is complex as a result of its existence in several oxidation states.

Under oxic conditions Tc7+ predominates and the most stable chemical species of "Tc is TCO4 ; in well aerated soils, therefore, the pertechnetate anion is considered to be the most important chemical form of Tc (Sparkes and Long, 1988). In a similar manner to the N03~ ion, TcO^ is highly mobile in the mainly negatively charged soil environment and incorporation of this anion by plant roots can be very considerable (Wildung et al., 1977; see also Table 7-14). Over the longer term, however, reduction of "Tc may occur, especially in association with microorganisms in anaerobic soil microaggregates, but also as a result of complexation with organic matter. Unfortunately, the reaction kinetics involved are so slow that it has been estimated (Van Loon, 1986) that 90% immobilisation of "Tc in a contaminated soil may take as long as 30 to 40 years (this compares with an immobilisation time for radiocaesium in most agricultural soils of less than one year). It has been shown that even over one cropping season the vast majority of "Tc within a soil will be incorporated by wheat and other crops (Grogan et al., 1987), so the principal means of loss of this radionuclide from soils in agricultural ecosystems is likely to be the removal of harvested crop tissues.

Despite the extensive use of 99mTc as a tracer in medical studies the plant physiological behaviour of Tc has only recently been elucidated. Lembrechts et al. (1985) determined that free TcO^ occurs within the cells of spinach leaves, implying that Tc is transported across the plasmalemma and into the cytosol in this form (as a result the root uptake of Tc is subject to a considerable degree of antagonism from N03" and other anions - Van Loon, 1986). Reduction of Tc7+, however, appears to take place within the cell and Lembrechts et al. (1985) also determined that up to ten discrete Tc bio-organic complexes were present in spinach leaf homogenates, 80 to 90% of which had molecular weights of < 6 kD. In a further study Lembrechts and Desmet (1986) argued that the reduction of Tc04~ to Tc5+ is mediated by ferredoxin within chloroplasts and that the incorporation of Tc within plant tissues was therefore effected as the result of photosynthetic reduction. Stable Tc5+ complexes appear to be formed in vivo by ligand exchange with complexing agents such as thiol compounds (Lembrechts and Desmet, 1989); having been incorporated by plant tissues, however, the bioavailability of Tc to animals via absorption in the gastrointestinal tract appears to be reduced (Garten et al., 1986).

While present knowledge of the ion absorption and metabolism of individual radionuclides such as I37Cs, 90Sr and "Tc is considerable there is still a major requirement for a reliable generic approach to the quantification of plant uptake of radionuclides based on mechanistic principles which can be applied equally to nuclides of widely differing chemical and physiological characteristics. Models such as SPADE (Thorne and Coughtrey, 1983), ECOSYS (Prohl et al., 1988) and RUINS (Crout et al., 1990) have made important headway on this problem in the last decade, recognising some of the complex features of the soil-to-plant transfer of radionuclides which are omitted or forgotten in a simplistic transfer factor approach. A mechanistic model for soil-to-plant transfer of radiocaesium in grassland, based on the soil chemical behaviour of the nuclide, was produced by Kirk and Staunton (1989) in the wake of the Chernobyl accident but this does not account for plant growth or seasonal physiological effects and apparently remains untested. Desmet et al. (1991) have recently highlighted the importance of both speciation of radionuclides within the soil to their bioavailability to the plant and the effects of growth rate on the build up of radioactivity in plant tissues across a growing season. Both of these factors need to be addressed in future if a 'definitive' model for radionuclide accumulation is to be produced.

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