Iodine (I) is readily taken up by plants if available [1
], which is important to both agronomy and radioecology because, although I is not an essential element for plants, food crops are a major conduit for the entry of I to human foodchains. Stable I (127
I) is an essential trace element for humans whilst the radioisotopes 131
I and 129
I can be significant radioactive contaminants of the environment [2
]. About two hundred million people worldwide suffer from I deficiency disorders (IDD), with an at risk population potentially in excess of one billion [3
]. It has been estimated that around 44% of children and adults in Europe have a mild iodine deficiency [4
]. Low I intake from food crops is partly responsible for IDD and thus, as for many other trace elements [3
], to redress deficiencies it is potentially useful to understand the agronomy of 127
I in the soil-crop system. The iodized-salt enrichment diet has reduced I deficiency in some areas but there are still areas with a significant level of IDD.
The toxicologically important radioisotopes 131
I and 129
I, which are both fission products, can be a significant component of releases of radioactivity to the environment, and, as isotopes of an essential element, tend to accumulate in animals if they are present in food. 131
I has a short-half life (eight days), is quite a high energy β/γ emitter and is primarily of concern as a food contaminant in the immediate aftermath of releases from accidents or from fall-out from above-ground nuclear weapons detonation. 129
I has a long half-life (15.7 × 106
years) and has been of importance in accidental releases, but it is a major, and potentially mobile, constituent of high and medium level nuclear waste [2
], and is released into the marine environment from nuclear-fuel reprocessing plants [5
I has the potential to be drawn upwards through soil profiles from repositories [6
] and to be transferred from sea to land [5
], provoking interest in its transfer characteristics from soil-to-plants during assessments of nuclear waste repositories and marine releases.
The transfer of I from soils-to-plants is possible because its isotopes can be both available in soil and taken up by plants. In fact, in comparison to many other nutrients and radionuclides, I isotopes are highly available in many soils with, for example, compilations of soil-solution distribution coefficients (Kd
) for radionuclides suggesting that 129
I is amongst the least strongly adsorbed isotopes in a range of soils [7
]. There is little sorption of 129
I on clay minerals and any sorption is primarily to organic matter [6
]. I is more labile under anoxic than oxic soil conditions. For example, the flooding of paddy soils has long been known to produce the “Akagare” phenomenon in rice, which results from I toxicity caused by large increases in availability brought on by anoxia [8
]. It is also clear that there can be significant changes in I mobility between the water-table and the vadose zone in soils [6
]. In many soils I−
are the most common ionic forms, with I−
most likely to be taken up by plants [1
] because they have substantial capacity for the uptake of the chemically similar Cl−
]. Overall, although soil-to-plant transfer factors can be quite low from, for example, Andosols with high anion exchange capacities [10
], hydroponic experiments show that plants can take up large quantities of I if it is available to them [1
] and most soils produce transfers to crops that can contribute significantly to food I content and to radiocontamination if 127
I or 131/129
I are available in the soil.
It has been suggested, based on a limited number of species, that inter-species differences exist in the plant uptake of I under comparative conditions (e.g., [10
]) and concentrations of almost all elements across different plant species do not simply reflect soil availability, i.e.
, there are significant inter-taxa differences in uptake under the same conditions of availability [11
]. It seems likely, therefore, that there might be inter-taxa differences in the concentration to which plants take up I, and that these might be useful to understanding the agronomy of I. There are, however, few data on this phenomenon and no studies that have attempted to link these differences to recent phylogenies of angiosperms (flowering plants), nor to compare them to inter-varietal differences. The understanding of the phylogeny (evolutionary relationships) of angiosperms has been transformed in recent years by molecular and computer methodologies, resulting in new phylogenies for angiosperms (e.g., [12
]). Given that many phenotypes can be affected by phylogeny, angiosperm phylogenies specifically for use in comparative biological experiments have been published [13
]. These have now been used to analyze inter-species differences in the concentrations to which plants concentrate numerous elements [11
], and to establish that there is a significant influence of angiosperm phylogeny on plant mineralogy, including that of crop plants. Such analyses require quite large databases of inter-species comparisons, often produced by collating data from a variety of sources through, for example, Residual Maximum Likelihood (REML) analysis. Here we utilize techniques successfully used to investigate inter-species differences of other elements to construct a database of relative I concentrations following root exposure in 103 angiosperm species, analyze their differences using a recently published phylogenetic hierarchy for the angiosperms, compare them to inter-varietal differences in two species, and assess their influence on I concentrations in food crops. The usefulness of the results to predicting the transfer of I isotopes from soils to plants in agricultural and radioecological contexts is then discussed.
and Figure 1
indicate that there is a wide range of I concentrations between plant species. They confirm the existence of inter-species differences in I concentrations of sufficient magnitude to support previous suggestions that crop species might be as important as soil type in determining I concentrations in crop plants [21
]. For elements in which there are very small phylogenetic influences above the species level there is very little variance attributable to taxonomic levels above the species. Table 2
shows that there is a phylogenetic influence on inter-species differences in iodine concentration, especially for Genera within Families. Figure 4
indicates that inter-varietal differences in I concentrations do occur, strengthening the assertion that there is nothing especially significant about the species as a taxonomic unit to describe inter-taxa differences in I concentrations in plants. These observations suggest, for the first time, (a) that angiosperm phylogeny influences the I concentrations of plants; (b) that the species is not an independent sampling unit for I concentrations in plants; and (c) that it might be possible to make general predictions of relative I concentrations in food crops based on phylogeny. If correct, such insights are potentially useful for understanding the agricultural chemistry and food toxicology of I.
The validity of the general insights above, however, depends on a number of assumptions about the relative mean concentrations reported in Table 1
. First, a high proportion of the data in Table 1
are from experiments with 125
I. There is no evidence of discrimination between I isotopes during plant uptake and 125
I has previously been used as a proxy for other I isotopes in uptake experiments [22
], so we assume that the data for 125
I are very likely to represent the behavior of I isotopes of more agricultural and toxicological significance. Second, it is likely that the acute exposures to I used to generate much of the data in Table 1
will not produce exactly the same relative mean concentrations in plants as chronic exposures. However, much nutrient uptake takes place during the exponential phase of growth when our plants were exposed so we assume that our observations will approximate inter-species differences that might be found following chronic exposures. Nevertheless the data in Table 1
may be more directly relevant to acute exposures to 129
I (which can be radioecologically significant, for example, during pulsed movement up through soil profiles [6
]) than to long-term uptake of 127
I. And third, it is important to acknowledge that the relative mean concentrations between plant species reported in Table 1
might not be the same under all environmental conditions, i.e.
, there might be an interaction between environment and inter-species differences. Despite these assumptions, it is notable that similar observations to those we make above for I have been reported for numerous other elements using a variety of isotopes, exposure times and environmental regimes [11
]. Thus, given that it is the most taxonomically wide-ranging database yet reported for inter-species differences in plant I concentrations and that it is compatible with results for other elements, Table 1
provides a basis for initiating assessments of the influence of phylogeny on I concentrations in plants. There have been detailed studies of the translocation of I in plants and its partitioning between plant parts [22
], which clearly affect I concentrations in food stuffs. As the data in Table 1
focuses on green shoots in toto
, phylogenetic influences identified might provide background concentrations upon which internal partitioning is imposed.
If there is no effect of phylogeny on inter-species differences in uptake then, as is approximately the case for N and P [16
], there will be no variance associated with taxonomic levels above the species. This is not the case for I and we conclude that Table 1
and Table 2
show that there is an influence of phylogeny on differences in I concentrations between plant species. This gives further support to the assertion that particular taxa of plants have characteristic mineralogies and that a phylogenetic perspective on plant contribution to the transfer of elements in the soil-crop system might be useful [16
]. A phylogenetic influence also means that plant species are not independent sampling units for I, i.e.
, great care must be taken in statistical analysis of I transfer in the soil-crop system as many techniques, such as regression, make the assumption that samples from different species are independent. In contrast to the frequency distribution of relative concentrations of some elements [15
], I concentrations in plants are not normally distributed. This indicates that the parametric statistics often used in soil-crop transfer analysis must be used with care in analyses with numerous species. Normal distributions of phenotypes are often characteristic of polygenic, “quantitative”, traits. Quantitative techniques, such as the Quantitative Trait Loci analysis used to locate genes impacting on the concentration of other elements in plants [29
] might have to be used with care for analysis of the genetic factors affecting the I chemistry of crops.
Detailed analyses of the effects of phylogeny necessitate concentration values for more than 103 species but some patterns do emerge from the analysis carried out here. It seems clear that, as is the case with some other elements [16
], there is a significant difference in I concentration between Monocot and Eudicot plants. Of Orders with significant numbers of food crops the analysis reported here indicates that plants in the Poales (cereals and relatives), Asparagales (onions and relatives), and Caryophyllales (beets, amaranths, buckwheat and relatives) might have higher than average I concentrations. These Orders might worth further investigations if explanations for dietary loadings of I are being sought, particularly as some of these Orders are represented by few species in Table 1
. Further investigations might, for example, test the suggestion that at a given soil availability of I, cereal grains such as amaranths and buckwheat might provide higher I concentrations than grains such as wheat or rice. These effects might be used to expand the reported general pattern of I concentrations in foodstuffs of legumes > vegetables > fruit [31
] because they suggest that there are groups of plants with significantly higher I concentrations than legumes.
suggests that although there might be some inter-varietal differences in I concentrations in some crops, they might be small compared to inter-specific differences. This supports conclusions of previous studies with numerous varieties of clover, grasses and other herbage crops [23
]. Nevertheless, further analyses might very usefully compare the amount of variation above and below the species level in order to determine the extent to which I concentrations in plant biomass can be altered by choosing different varieties or different species. The phylogenetic effects described above have some similarity to those we have reported for Cl [18
], especially the higher than average values in the Caryophyllales. However, we found no direct correlation in relative mean values for 24 species that occur in both data sets. It might be interesting to investigate, using a dataset with more species, if this lack of correlation reflects real differences in the behavior of I and Cl.
In the database compiled here, loge
-transformed values subject to REML-modeling are approximately normally distributed. Using the IAEA recommended value and back transforming modeled values to CRs, confirms the loge
-normal distribution of I concentrations in plants and enables us to predict geometric mean CRs for different plant groups and 95% confidence intervals (Figure 2
). These suggest that significantly improved predictions of CR for radioiodine can be made by taking taxonomic group into account, with splitting the recommended CR into two, one for Monocots and one for Eudicots, bringing about a significant improvement in predicted CR very simply (Figure 2
a). Such overall predictions for groups of many species are very useful in the case of a contamination event in which many Monocots and Eudicots might be contaminated simultaneously. In different ecosystems that have different proportions of Monocots and Eudicots, the predicted CRs in Figure 2
could significantly improve predictions of overall radioiodine transfer from soils to plants.
Overall, in both agriculture and radioecology inter-taxa differences in I uptake by plants are important—in addition to iodized salt and irrigation water, it has been suggested that crop selection and/or breeding might help to provide increases in I concentration in food [31
] and predictions of radioiodine movement into foodchains use CRs for soil-to-plant transfer. The data reported here improve the understanding of inter-taxa differences in I concentrations, and by initiating investigations of the phylogenetic distribution of the diversity in I uptake, might help to identify those groups of plants with particular I concentrations thus benefitting both agricultural supply of iodine and predictions of radioiodine transfer to food, flora and fauna.