Availability of iodine in food

The largest reservoir of iodine is in the sea; from there is mobilized to terrestrial areas through volatile chemical forms produced by marine seaweed or by marine aerosols carried by winds which explains why remote soil from the ocean are usually short of iodine and therefore plants grow in these soils would have low concentration of the element (^{Zimmermann, 2009}).

Iodine is not considered as an essential element for terrestrial plants, although several studies showed that these absorb and accumulate iodine (Mackowiak and Grossl, 1999; ^{Zhu et al., 2003}). This apparent non-essentiality explains why iodine is not contemplated in mineral fertilization programs of crops, despite the fact that it has been shown that the contribution of inorganic iodine salts can increase stress tolerance in plants (^{Leyva et al., 2011}; ^{Gupta et al., 2015}). Not to include fertilizers with iodine for crops causes that the content of this element in plant and animal foods depends exclusively on the natural availability of the element in soil and water. For this reason, to date, the main source of iodine for most of the world's population is the contribution of inorganic salts (iodide and potassium iodate: KI and KIO₃) in table salt, adding 20 to 40 mg of iodine per kg of salt following the guidelines from WHO/UNICEF/International Council for the Control of iodine Deficiency Disorders (WHO, 2007; ^{FAO, 2009}; ^{Zimmermann, 2009}).

Availability of iodine in the soil

The available iodine concentration in the soil is in function of the distance to the ocean as well as soil composition from mother material. Mountainous areas, valleys and plains from the interior of continents show low concentrations of iodine (^{Aston and Brazier, 1979}). It has been noted that iodine is unique among the elements in consideration to its geochemical behavior. Most elements available in the soil come from the erosion of the lithosphere, and generally this is not the case for iodine (^{Fuge and Johnson, 1986}). This element shows a wide range of soil concentrations from <0.1 to 150 mg kg^-1. It is considered that iodine concentration in soil is generally higher than that found in soil bedrock. Geochemical agree on the above because the largest supply of iodine in the soil comes from the atmosphere which in turn this receives it from marine environment (^{Fuge, 2013}).

Among the edaphic factors that modify the availability and iodine absorption in soil are: amount of organic matter, which allows higher iodine absorption by plants, especially when it is in the form of iodate (IO₃^-) (^{Seki et al., 1984}). This effect seems to depend on the ability of humic substances to adsorb iodine (process apparently mediated by microorganisms) decreasing its volatilization (^{Bostock, 2003}), although in the absence of organic matter seems to be great iodine volatilization activity as CH₃I through microbial activity (^{Amachi et al., 2003}). This fact may partly explain the apparent negative relationship between clay content of the soil and iodine uptake by plants, while soil pH does not appear to exert any effect in the range of 5.4 to 7.6 (^{Shinonaga et al., 2001}).

Iodine content in plants

Iodine concentration normally found in plant tissue ranges from 0.1 to 1 µg g^-1, reaching up to 3 µg g^-1 or more (^{Benton Jones, 1998}). In a study conducted by ^{Shinonaga et al. (2001)} established that iodine concentration in grain cereal from inland agricultural areas in Europe was particularly low, with values of 0.002 to 0.03 µg g^-1, compared to soils near the ocean. Little is known about how this element is accumulated in terrestrial plants, however, in a research conducted in pumpkin plants was deduced through a study with electron microscopy that the inorganic and organic iodine applied directly to the substrate, most of iodine accumulated in the root, while another small portion was transported to the aerial parts to be stored in the chloroplasts (^{Weng et al., 2008a}), fact that may partly explain its role of inducing tolerance to certain types of stress since a significant volume of the antioxidant cellular machinery is found in chloroplasts.

Fertilization with iodine for biofortification in soilless crop systems

Iodine content in plants generally increases when applying iodine as iodide, iodate or other chemical forms (^{Weng et al., 2008b}). The best results were obtained by applying iodine compounds in the nutrient solution or foliar spraying. In each plant species the results are variable in the sense that the response is modified versus the concentration and the distribution changes in plants organs. For example, in a study conducted in spinach under hydroponics different chemical forms of iodine as acid iodine acetic, iodide and iodate were applied and proved that concentrations greater than 0 and up to 1 mg L^-1, iodine absorption rate increased linearly against the concentration, maintaining a concentration ratio of 1:1 in roots and leaves. The following accumulation order was shown with the different iodine forms CH₂ICOO-> I-> IO₃^-.

Additionally it was found that even with these low concentrations there was an increase in biomass (^{Weng et al., 2008c}). Meanwhile ^{Blasco et al. (2008)} demonstrated that applying iodine concentrations ≤5.1 mg L^-1 iodide (I^-) in hydroponic lettuce obtained an adequate accumulation of foliar iodine, which was 900 µg^-1 g dry tissue, amount that is sufficient to meet the daily demand for iodine intake in humans (150 µg day^-1) (^{Charlton et al., 2013}) when consumed between 17 and 200 g of fresh tissue of lettuce per week, as this concentration does not exceed the maximum recommended amount which is 2 mg per day. However at concentrations above 5.1 mg L^-1 iodide a significant reduction in biomass was present, thing that did not happen applying the same concentrations of iodate.

^{Zhu et al. (2003)} studied iodine absorption in spinach plants under hydroponic culture at concentrations of 0.127, 1.27, 6.35 and 12.7 mg L^-1 of iodide and iodate, finding that with 12.7 mg L^-1 iodide there were no negative effects on plant growth, while with the same iodate concentration occurred only a small effect on plant biomass; however low concentrations, such as 0.127 mg L^-1 of iodide and iodate resulted in adequate accumulation of this element, showing 3 and 1.8 µg I g^-1 fresh weight, which is considered adequate.

^{Voogt et al. (2010)} conducted another biofortification experiment with iodine as iodide and iodate in lettuce plants, applied very low concentrations of these chemical forms, which ranged between 0.013 and 0.129 mg L^-1, finding that none of concentrations showed toxic effect on lettuce plants and with a concentration of 0.129 mg L^-1 iodide obtained an accumulation of 0.653 and 0.764 µg I g^-1 fresh tissue, five times lower than the concentration obtained by applying iodate.

Today there is a growing interest in iodine supplementation in the food chain through uptake and accumulation of this element in plants for human consumption (^{Nestel, 2006}), the positive results described above, mainly in horticultural species on soilless systems are important and suggest that are good candidates for bio-fortification programs with iodine, however, the real challenge is crop bio-fortification in extensive soil systems, since it is what would allow a truly comprehensive coverage of the target population.

Fertilization with iodine for crop biofortification in soil

The addition of iodine to the soil allows to broaden the spectrum of plant species for biofortification (^{Cui and Song, 2003}), including also medicinal vegetables and even staple crops (Yuita, 1992) normally grown in field. In the soil can coexist various chemical forms of iodine, among the most abundant are iodate (IO₃) and iodide (I^-) (^{Borst Pauwels, 1962}). Some studies related to application of iodine to the soil have shown that plants can tolerate higher concentrations of iodate than iodide (^{Dai et al., 2006}; ^{Smolen et al., 2012}) and that very low concentrations of iodine (0.02-0.2 mg kg^-1) regardless of the form, are beneficial for different crops, especially for halophytic (^{Borst Pauwels, 1961}; ^{Dai et al., 2006}; Smolen and Sandy, 2012). ^{Dai et al. (2006)} conducted the application of iodide and potassium iodate directly to the soil to biofortify lettuce plants, noting that the highest accumulation of this element was obtained with iodate treatments.

Contrary to what happened when applying iodide and potassium iodate through hydroponics in lettuce plants and rice (Mackowiak and Grossl 1999; ^{Zhu et al., 2003}). Studies performed in rice have shown that these have the ability to reduce iodate to iodide, fact that seems to confer metabolic flexibility compared to iodine (^{Kato et al., 2013}). Moreover, ^{Weng et al. (2003)} found that when applying kelp and diatomaceous earth to the soil managed to increase the availability of iodine for vegetables. The same authors found that the iodine absorption by vegetables was a direct function of the concentration from the element in the soil, up to a limit that was different for each plant species. In a recent study ^{Weng et al. (2014)} demonstrated that it is possible to use seaweed compost incorporated into the soil as a mechanism of fertilization with iodine.

The origin of the differences in iodine or iodate absorption in soil and nutrient solutions are unknown. They are attributed in part to the substantial volatilization of Iodine from the plant-soil system to the atmosphere mediated by different microorganisms (Muramatsu et al., 1995; ^{Fuge, 1996}). However, there is evidence that the synthesis of volatile forms of iodine, called organoiodine, mainly from the chemical form iodide (^{Keppler et al., 2003}) this fact might seem contradictory since iodide is the chemical form that plants absorb more easily from the soil. Iodine content in irrigation water can be a source of this element for plants; however it is unlikely that water contains adequate levels of iodine in regions where the soil has low concentrations of the element. The application of iodine as potassium iodate in irrigation water (0.010 to 0.08 mg L^-1 for four weeks) was effective for four years to increase the concentration of iodine in soil and plants in regions from China with severe iodine deficiency (^{Jiang et al., 1998}).

In another study Caffagini et al. (2011) conducted the application of iodide and iodate through irrigation at concentrations of 500 and 1 000 mg L^-1 and 500, 1 000, 2 000 and 5 000 mg L^-1, respectively, in barley, corn, tomato and potato; finding favorable results only in tomato fruits and potato tubers reaching concentrations of 272 to 6 245 µg I per 100 g of fresh weight and from 527 to 5 375 µg I per 100 g of fresh weight respectively. Iodine concentration achieved in tomato fruits of treated plants with iodide at 500 mg L^-1 was seven times higher than that achieved with the application of iodate at 500 mg L^-1 (3 900-527 µg 100 g^-1). Similarly for potato tubers, where the achieved concentration with the application of iodide at 500 mg L^-1 was seven times higher than the concentration achieved with the application of iodate at 500 mg L^-1 (1 875 versus 272 µg I per 100 g fresh weight), which confirmed the greater ease of absorption from iodide against iodate.

One way to avoid the complexity of the phenomena of absorption and transport of iodine when applied to the soil, is to apply it through foliar spraying as iodide and iodate (^{Zanirato and Mayerle, 2009}), finding good results when compared to soil applications (^{Lawson et al., 2015}). In another recent study ^{Tonacchera et al. (2013)} achieved to increase iodine concentration in potato, carrot, tomato and lettuce applying iodine as foliar spray. The results indicated that the edible parts of the plants reached up to 30% of the recommended daily intake (RDA) of iodine without affecting other aspects of food quality.

Mechanisms of iodine absorption and transport

Marine plants are immersed in a medium rich in iodine, therefore constitute the simplest model to study the phenomenon of iodine absorption. According to the proposed mechanism Küper et al. (1998), iodine absorption in brown algae occurs through the pass of iodide present in the apoplast through the cell wall through enzyme iodine peroxidase dependent of vanadium (V-IPO) (^{Truesdale et al., 1995}; Colin et al., 2003; ^{Winter and Moore, 2009}) which catalyzes the oxidation of iodide to hypoiodous acid (HIO), as shown in reaction 1:

Additionally hypoiodous acid can react spontaneously with iodide maintaining equilibrium of reaction in aqueous medium as shown in reaction 2 (^{Truesdale et al., 1995}).

When algae are subject to low levels of oxidative stress, I₂ formed in the reaction (2) can cross the cell membrane, subjected to a reduction in the cytoplasm and then stored as iodide in the vacuole, where will be mobilized at times of oxidative stress. Instead, when algae are subjected to a high level of oxidative stress I₂ will volatilize into the atmosphere (Le Blanc et al., 2006; ^{Kupper et al., 2008}). The same fate may suffer HIO, because it can accumulate in vacuoles or react with organic compounds forming mainly methyl iodide (CH₃I) which will volatilize (Le Barre et al., 2008) (Figure 2).

Figure 2 Diagram of the absorption and volatilization mechanism of iodine by marine plants; (Modified from Le Blanc et al., 2006). 

^{Weng et al., (2013)} performed a series of experiments with cabbage plants and concluded that the iodine absorption through the root occurs in a different way to that observed in marine plants. In cabbage iodide transport occurs via coupled transporters to a proton bomb, thus through anion channels and the same has been observed in other terrestrial species (^{White and Broadley, 2009}). By contrast, in marine plants it seems to operate only the mechanism associated to proton pump (^{Weng et al., 2013}). Subsequent mobilization of iodine from the root to the stems and leaves occurs through the xylem (Herret et al., 1962; Mackowiak and Grossl, 1999; ^{Zhu et al., 2003}; ^{Kato et al., 2013}) but as it occurs with other elements seems to be a subsequent redistribution of iodine via phloem (^{Landini et al., 2011}).

The assimilation and transport processes of iodine start to elucidate and it promises to obtain great benefit in terms of nutritional quality of vegetables. However, even in the absence of such knowledge a practical way to quantify iodine uptake by plants is the so-called transfer factor (TF) which is calculated by the following equation:

The disadvantage of this factor (TF) is that it does not indicate anything about the factors that modify it, however, if the goal is to detect soil types or management factors that increase the uptake of iodine or decrease its loss by volatilization, then TF will be very useful as an indicator. For example Cl^- has a high TF, due to its flow in the plant shows high correlation with xylem water flow, it has been calculated a TF = 785 value for Cl^- in Lolium perene (Ashworth and Shaw, 2006). In contrast TF values for iodine are usually very low: 0.00034 for forage (^{IAEA, 1994}), 0.0005-.02 for cereals in Austria (^{Shinonaga et al., 2001}), 0.024-0.19 for corn, beets and pumpkin (^{Sheppard et al., 1993}) and 0.01-0.03 for radishes and lettuce (^{Kashparov et al., 2005}).

However, it has been reported that it is possible to significantly increase TF of iodine, by increasing the concentration of this element in the soil. ^{Dai et al. (2004)} obtained that when applying iodine at a concentration of 5 mg kg^-1, TF from edible parts of different vegetables increased from 0.1 to 10. The values increased in the following order carrot =onion <celery <spinach outbreak < spinach leaf. Because of the problems described above, and not only to uneven distribution of iodine in the soil, have been proposed application techniques to apply iodine to soil, water or foliar spray and has been proven the effectiveness of these practices to achieve improved iodine concentration in the main plants for human consumption.