Use of Iodine to Biofortify and Promote Growth and Stress Tolerance in Crops

Abstract

Iodine is not considered essential for land plants; however, in some aquatic plants, iodine plays a critical role in antioxidant metabolism. In humans, iodine is essential for the metabolism of the thyroid and for the development of cognitive abilities, and it is associated with lower risks of developing certain types of cancer. Therefore, great efforts are made to ensure the proper intake of iodine to the population, for example, the iodization of table salt. In the same way, as an alternative, the use of different iodine fertilization techniques to biofortify crops is considered an adequate iodine supply method. Hence, biofortification with iodine is an active area of research, with highly relevant results. The agricultural application of iodine to enhance growth, environmental adaptation, and stress tolerance in plants has not been well explored, although it may lead to the increased use of this element in agricultural practice and thus contribute to the biofortification of crops. This review systematically presents the results published on the application of iodine in agriculture, considering different environmental conditions and farming systems in various species and varying concentrations of the element, its chemical forms, and its application method. Some studies report beneficial effects of iodine, including better growth, and changes in the tolerance to stress and antioxidant capacity, while other studies report that the applications of iodine cause no response or even have adverse effects. We suggested different assumptions that attempt to explain these conflicting results, considering the possible interaction of iodine with other trace elements, as well as the different physicochemical and biogeochemical conditions that give rise to the distinct availability and the volatilization of the element.

Iodine dynamics

The oceans are the largest reservoirs of bioavailable iodine on the planet; from there, the element is distributed into the atmosphere and land areas (Fuge, 1996; Venturi, 2011). The second most important reservoir of iodine is the soil, which has a higher content than does its parent material as a result of the activity of the living organisms (Muramatsu and Yoshida, 1999). Approximately 4 × 10¹¹ g year⁻¹ of iodine volatilize from the ocean into the atmosphere (Miyake and Tsunogai, 1963; Amachi, 2008), with an estimated of 1.14–3.17 × 10¹¹ g year⁻¹ that volatilizes as CH₃I (Moore and Groszko, 1999). In the atmosphere, iodine reaches concentrations of 5–20 ng m⁻³ in gaseous forms and 1–5 ng m⁻³ as particulate iodine (Moyers and Duce, 1972). This atmospheric iodine, in the form of I₂ and organoiodine compounds (CH₃I and iodinated humic acids), reacts photochemically with O₃ and forms radicals (I₂O₂, I₂O₃, and I₂O₄) that become transformed into I₂O₅. This compound forms particles with a nanometric dimension that induces condensed nuclei for cloud formation (Saunders and Plane, 2005). Iodine in the form of gas and aerosol is carried by the wind and rain to land areas, where it is found in soils mainly in the form of iodide (I⁻) and iodate (). In rainwater, the iodine appears at concentration of 2 μg L⁻¹ (Bowley, 2013). Once found on land, iodine is distributed in different ways: it is again mobilized by volatilization into the atmosphere by abiotic and biotic processes, fixed in soil and biomass, or dragged to the ocean through water streams (Whitehead, 1984; Moreda-Piñeiro et al., 2011; Saunders et al., 2012; Fuge and Johnson, 2015; Figure 1).

Figure 1

The distribution of iodine between different terrestrial compartments occurs with the significant participation of microbiological processes (Amachi et al., 2003; Amachi, 2008). From a physiological perspective, it is assumed that the flux of iodine among different organisms is valuable as a source of antioxidant potential (Crockford, 2009; Venturi, 2011), as well as by the metabolic value of the compounds resulting from the reaction between the amino acid tyrosine and iodine, such as thyroxine (T4) and its derivatives (T2 and T3; Eales, 1997; Heyland and Moroz, 2005). From an ecological standpoint, the iodine flux between the different layers of the Earth, ecological compartments, and organisms may be considered part of the global system of energy dissipation (Karnani and Annila, 2009).

Among the biological processes of iodine mobilization, one receiving close attention involves iodine metabolism by seaweeds of the genus Laminaria (Leblanc et al., 2006), which volatilize iodine through the production of molecular iodine (I₂) and organoiodine compounds (CH₃I and CH₂I₂; Moore and Groszko, 1999; Carpenter et al., 2000; Leblanc et al., 2006; Jones et al., 2010), coupling the process with the antioxidant metabolism to reduce oxidative stress (Küpper et al., 2008; Nitschke et al., 2013). It has been shown that one iodoperoxidase enzyme dependent on vanadium (V-IPO) is critical in this antioxidant system (Figure 2).

Figure 2

The I⁻ that is absorbed from seawater reacts with H₂O₂, (catalyzed by V-IPO) to produce hypoiodous acid (HIO; Küpper et al., 1998). The oxidative process is named peroxide-dependent diffusion (PDD) and occurs in macroalgae, bacteria, and animals outside of the chordates (Miller and Heyland, 2013). The resulting HIO may (i) diffuse into the cytoplasm to be accumulated, (ii) react to form volatile organoiodine compounds, or (iii) react in the apoplast with I⁻ to produce I₂, which can also migrate to the cytoplasm and be stored or volatilized (McFiggans et al., 2004; Leblanc et al., 2006). Figure 2 partially explains the value of iodine as an antioxidant. Iodide may be a source of reduction potential to the cellular system, once oxidized it can be used for metabolic purposes, stored at an intracellular iodine pool or, to avoid excessive accumulation, dissipated by means of volatile organoiodine compounds or I₂ sublimation.

It has not been proven that iodine plays a central antioxidant role in land plants as in the Laminaria macroalgae, although it has been reported that in the presence of iodine, crop plants increase their antioxidant levels (Gupta et al., 2015). It is assumed that during their evolution, land plants decreased their dependency on iodine as an inorganic antioxidant, developing a whole new series of organic antioxidants (such as ascorbic acid, polyphenols, and carotenoids) in response to the low concentration of available iodine in the emerged areas (Venturi, 2011). Notwithstanding the apparent non-dependency on iodine, higher plants absorb iodine through their roots and leaves, and dissipate it (Barry and Chamberlain, 1963; Whitehead, 1979; Amiro and Johnston, 1989) using halogen methyltransferases not dependent on vanadium (Landini et al., 2012). Similar to iodine, the vanadium is an element of low bioavailability in land areas (Cappuyns and Swennen, 2014); thus it is possible that iodine oxidases have evolved as a dependent on one-carbon metabolism. However, the question of whether vanadium is essential for plants, coupled with the possibility that plant responses to iodine occur under a context of low bioavailability of vanadium has not been fully resolved (Pilbeam and Drihem, 2007). Additionally, marine photosynthetic organisms, algae, and diatoms synthesize analogs to thyroxine (Heyland and Moroz, 2005; Crockford, 2009), and the land plants have transthyretin-like proteins with sequence homology to transthyretin (TTR), the protein for thyroxine transport (Eneqvist et al., 2003; Pessoa et al., 2010); thus, it is possible that iodine may have metabolic functions that are not yet understood in land plants. In animals, the evolutionary strategy to address the low iodine availability in land areas is different: animals are still dependent on iodine as an indispensable element, and iodine is stored in vertebrates in the follicular tissue of the thyroid. In other groups, such as invertebrates and prochordates, iodine is accumulated in other tissues or specific proteins (Eales, 1997). Animal organisms obtain iodine mostly from food intake and, to a lesser extent, through the absorption from drinking water and from gas exchange during breathing (Vought et al., 1970; Whitehead, 1984; Fuge and Johnson, 2015).

Iodine and human health

According to the World Health Organization (WHO), iodine deficiency (Figure 3) is among the most common nutritional deficiencies, along with those of iron (Fe), zinc (Zn), and vitamin A (Burlingame, 2013; Prasad, 2013).

Figure 3

From the perspective of human health, iodine is one of the most studied elements because of its metabolic importance and because of the complexity associated with the factors that induce its deficiency. Iodine deficiency occurs in many regions of the planet; the irregular distribution of iodine on the Earth's crust is considered as a primal factor (FAO, 2009). An estimated 2 × 10⁹ people ingest an insufficient amount of iodine (Mottiar, 2013), causing the so-called iodine deficiency disorders (IDDs). IDDs refer to illnesses associated with low iodine consumption (Zimmermann et al., 2008).

The best-known IDD due to its prominent symptom is goiter. Nevertheless, the presence of less tangible IDDs has been observed in recent decades, such as an adverse impact on physical and cognitive development in children, and on productivity in adults (Lazarus et al., 2012); it has also been associated with a higher incidence of fetal death, miscarriages, and congenital anomalies (Zimmermann, 2009). On the other hand, it was recently demonstrated that iodine is capable of acting as an antioxidant and as an antiproliferative of malignant cells (Funahashi et al., 2001; García-Solís et al., 2005; Aranda et al., 2013; Anguiano and Aceves, 2011). The daily requirement of iodine, according to the Recommended Dietary Allowances (RDA; World Health Organization, 2007; Andersson et al., 2012), is among 90 and 200 μg day⁻¹.

Foods contain different quantities of iodine depending on their origin, individual characteristics, conservation, and preparation. A comprehensive study of the literature (Fordyce, 2003) indicated that the geometric mean iodine concentration in foods is 87 μg kg⁻¹, a small amount when considering the daily requirements previously mentioned. Data separation by food type is provided in Table 1.

Except for the sea fishes, nearly all foods have a low iodine content. The data presented in Table 1 may vary depending on the site where the foods are collected or produced, but clearly show the need to increase the iodine amount in foods. As an example: it has been suggested that lettuce must contain 50–100 μg of iodine per 100 g of fresh weight (Lawson et al., 2015), that is, values several times higher than those shown in Table 1.

Numerous attempts to mitigate the deficit in the consumption of iodine have been made, mainly since the 1920s through the universal iodization of table salt (de Caffarelli, 1997; Zimmermann, 2009; Charlton et al., 2013). However, throughout the years it has been shown that this technique alone is insufficient to ensure the total requirement of iodine (de Benoist et al., 2008), partly because the iodine of table salt is unstable and is subject to many losses by volatilization (Mottiar and Altosaar, 2011). In this regard, the consumption of iodine in organic forms such as seaweed and biofortified foods and yeast, is considered more appropriate (Funahashi et al., 2001; Weng et al., 2008a; Kopeć et al., 2015) because those organic sources are more stable than inorganic ones.

The maximum recommended dietary dose of iodine ranges from 1000 μg day⁻¹ (Pennington, 1990) in a daily basis, to 2000 μg day⁻¹ by not more than 3 weeks (Backer and Hollowell, 2000). Iodine toxicities are not common under normal conditions (Gupta and Gupta, 1998), and humans appear to have a high tolerance to iodine doses <2000 μg day⁻¹ (Bulloch, 2014). Frequently, the toxicity by iodine occurs by genetic or physiological predisposition (Rose et al., 2002) or by the use of iodine-based products as disinfectants (Backer and Hollowell, 2000) and medications (Bulloch, 2014).

Therefore, it is necessary to promote the use of techniques, such as the biofortification of crops, to achieve an adequate iodine intake from foods, either as a complement or as an alternative to the inorganic sources of iodine as the table salt.

Iodine applications in agricultural crops

There have been numerous studies on the application of iodine in various plant species with the purpose of biofortifying crops. The results reported in the literature are variable according to the applied concentration, chemical form used and adopted production system (Tables 2–4). An overview is presented on the absorption, transport and volatilization of iodine in plants, followed by summaries reporting the concentrations and chemical forms of iodine that are used in different production systems.

Absorption and metabolism of iodine

Iodine is an element that can be absorbed by the root and in aerial structures both by the stomata and by the cuticular waxes with high degree of unsaturation and great capacity to take iodine (Shaw et al., 2007; Tschiersch et al., 2009), both in dissolved form and in gas form as I₂ and CH₃I. The impact of the differences among species in the profile and quantity of cuticular waxes on leaf iodine absorption has not been verified. This information may be relevant considering that the cuticular waxes interacting with iodine can be alternatives for the pre- and post-harvest biofortification of fruits and seeds.

There is no information to indicate how much of the element that has been taken up by the plants comes from the soil and how much from the atmosphere, but it is known that the absorption of iodine in gas form can be significant (Barry and Chamberlain, 1963; Nakamura and Ohmomo, 1984; Whitehead, 1984). In opposite Tsukada et al. (2008) estimated the atmospheric contribution to the iodine uptake of rice to be only 0.2%. The direct atmospheric contribution would be expected to be higher in regions near the sea and lower in continental areas; however, the evidence indicates that the volatilization of iodine that is fixed in the soil may also be an important factor in iodine transfer to organisms (Whitehead, 1984; Fuge and Johnson, 2015).

Once the iodine is absorbed, it is transported through the xylem, finding that its redistribution through the phloem is low (Herrett et al., 1962); thus it accumulates in greater amounts in leaves than in fruits and seeds. However, in lettuce plants treated with iodine by leaf spray Smoleń et al. (2014a) found evidence of iodine transport from leaves to the roots. In wheat plants, even when iodine was applied by foliar spraying, the mobility from the leaves to the grains (termed the translocation factor) was very low (0.2–1.1%), but this value appears to be cumulative, i.e., iodine moves from the leaves to the grain with each application event (Hurtevent et al., 2013). The observed translocation factors for radish, potato, and bean range from 0.8 to 2.6%, 0.1 to 2.3%, and 0.1 to 2.6%, respectively (Henner et al., 2013). On the other hand, the iodine transfer factor (ITF) refers to the element that is absorbed by the root, and is defined as the ratio of the iodine concentration in the plant tissues to its concentration in the substrate. ITF is higher in leafy crops such as spinach (ITF ≥ 2.0), than in fruits such as tomatoes and nectarines, or cereal grains (0.0005 ≤ ITF ≤ 0.02; Shinonaga et al., 2001; Lawson, 2014). For example, starting with a soil concentration of 48 mg kg⁻¹, the distribution of the iodine that is absorbed by a rice plant (dry weight) is as follows: 53 mg kg⁻¹ in the root, 16 mg kg⁻¹ in the leaves, and 0.034 mg kg⁻¹ in the polished grain (Tsukada et al., 2008).

When iodine is applied to plants as it is reduced to I⁻ by the action of an iodate reductase, which responds to the availability of iodine in the medium (Kato et al., 2013). This reductase activity also occurs in microorganisms (Amachi, 2008), but the magnitude of the microbial contribution in the soil process is unknown. In soils is more efficient taken up by plants compared to I⁻ (Lawson et al., 2015), and in soilless cultures the application of I⁻ induces toxicity more easily in plants than does (Borst Pauwels, 1962; Umaly and Poel, 1971; Muramatsu et al., 1983; Zhu et al., 2003). The lower toxicity of could be explained by the iodate as an alternative substrate to other abundant enzymes, such as nitrate reductase (Barber and Notton, 1990), or by the activation of iodate reductase through inducing other responses associated with redox signaling and iodine metabolism in plants, in addition to the reduction of .

Since is more thermodynamically stable than I⁻, it is hypothesized that it is the most likely form to be available in agricultural soils. However, because the I⁻/ ratio depends on biological activity, it is not limited strictly to a thermodynamic balance (Kaplan et al., 2014), as shown in Figure 4. This fact makes it difficult to predict the pattern of iodine speciation in a particular soil.

Figure 4

Plants absorb iodine as I⁻ through ionic channels and chloride transporters that are energized by proton pumps (White and Broadley, 2009); therefore, there may occur interference scenarios with other anions such as nitrate, thiocyanate, and perchlorate (Voogt and Jackson, 2010). The identity of the I⁻ transporters is not firmly established, but their activity can presumably be shared by several families of transporters and anion channels (White and Broadley, 2009; Landini et al., 2012). Among these are the Na:K/Cl cotransporters belonging to the CCC family of genes (Colmenero-Flores et al., 2007), which directly regulate the concentration of ions in the root xylem (Shabala, 2013; Wegner, 2014; Fricke, 2015). Another group is the gene family of CLC Cl⁻-channels permeable to I⁻ (Roberts, 2006; Barbier-Brygoo et al., 2011). Currently, the CLC genes have been linked to osmotic stress tolerance (Ma et al., 2016; Nguyen et al., 2016), stomatal movement, nutrient transport, and heavy metal tolerance (Zifarelli and Pusch, 2010).

Once absorbed, transported, and accumulated in different plant organs, iodine is not stable; plants volatilize iodine as methyl iodide (CH₃I) using the enzymes halide ion methyltransferase (HMT) and halide/thiol methyltransferase (HTMT), with methyl transferase activity dependent on S-adenosylmethionine (SAM; Redeker et al., 2004; Itoh et al., 2009). The affinity of these methyl-halide transferase enzymes to iodine is much greater than that observed in other halogens or ions such as thiocyanate (Takekawa and Nakamura, 2012). Volatilization can be faster as iodine increases its concentration in the substrate (Itoh et al., 2009), and occurs in all organs; in rice, the iodine foliar concentration decreases exponentially with a half-life of 14 days (Nakamura et al., 1986). Therefore, the action of methyltransferases continuously reduces the iodine store present in plants (Landini et al., 2012). It has been noted that iodine is a phytotoxic element per se to the plants and that volatilization is a detoxification mechanism (Saini et al., 1995) or a by-product of the methyltransferase activity reactions that occur in plants (Redeker et al., 2004). An alternative explanation is that the iodine is toxic only depending on the environmental context: for example, under conditions of high solubilization or little fixation, as previously mentioned (Yuita, 1994); when a deficiency of some elements such as Fe or Cu (perhaps vanadium) occurs; or merely as a result of the intrinsic differences between plant species to metabolize iodine (Saini et al., 1995).

There is little information about the differences between vegetable species and the environmental factors that affect the activity of enzymes that dissipate iodine, but it is known that the activity increases with temperature and changes in different developmental phases, peaking during the reproductive stage (Muramatsu and Yoshida, 1995; Redeker et al., 2004). This activity is also positively associated with the iodine absorption rate of the nutrient solution and the irradiance; in addition, the stomata partially regulate the flow of iodine from the mesophyll into the atmosphere (Amiro and Johnston, 1989). It has been reported that in bacteria, the iodine volatilization activity increases under stress (Li et al., 2012, 2014). This metabolic activity of iodine volatilization by plants contributes to the overall activity of volatilization that occurs in soils and inland waters and is part of the global flow of iodine. In soils, both I⁻ as are volatilized as HI, HIO₃, and HIO₄ (Sheppard et al., 1994). In soil-plant systems, the emission of iodine into the atmosphere occurs both by abiotic soil components and by plants and soil microorganisms (Ban-nai et al., 2006), but the total activity increases with the presence of vegetation (Muramatsu and Yoshida, 1995). The estimated amount of iodine that is volatilized for soil-plant system range from 0.28 to 0.62 kg ha⁻¹ season⁻¹, with an average of 0.40 kg ha⁻¹ season⁻¹ (Redeker et al., 2002). If we consider this value alongside the global average iodine content in soil (2.6 mg kg⁻¹; Watts et al., 2010), and consider that topsoil represents 1.5 × 10⁶ kg ha⁻¹, then without exogenous iodine inputs the volatilization activity will exhaust the soil iodine reservoir in 9 years.

The success of the biofortification of crops depends on more than the iodine application technique (Sheppard et al., 1994; Fuge and Johnson, 2015). Iodine is a dynamic element that is under constant turnover by living organisms, including plants and humans (Küpper et al., 2011), as well as by the ecological systems components (Kaplan et al., 2014). The ideal effort would pay direct attention not only to plants but also to the entire system of which they are a part. Iodine is metabolized by the complete ecological system, possibly under an overall control scheme that is not yet well understood, and it is advisable to consider other biotic and abiotic factors as part of the biofortification strategy. For example, the role of the rhizosphere as a complex and dynamical environment where interacts the roots, microorganisms, and inorganic soil components have been little explored regarding the absorption of iodine (Terzano et al., 2015), but has proven to be an useful approach in the case of Fe and Si (Pii et al., 2015; Gattullo et al., 2016). In the same way, there is a notable absence of studies on the biofortification of cultivated fungi or the use of mycorrhizae or plant growth-promoting rhizobacteria to modify the absorption of iodine, although this approach has proven its value for other elements, such as Fe and Zn (He and Nara, 2007; Pellegrino and Bedini, 2014; Rana et al., 2015). Mycorrhizae further decrease the toxicity of certain elements to plants (Leung et al., 2013), an issue that has not been reported for iodine.

An additional point is that other factors, climatic, ecological, phytochemical, and cultural (e.g., food preparation and storage), may decrease the bioavailability or stability of iodine and avoid the correlation between iodine distribution and its presence in the human population (Stewart et al., 2003; Kotwal et al., 2007; Longvah et al., 2012; Zia et al., 2015).

Speciation and complexation of iodine in soil

The iodine content of soil is the result of the complex dynamic balance of three processes: incorporation from the atmosphere, fixation, and volatilization, resulting in an enormous range of variation of iodine contents in the soil, from <0.1 to 150 mg (kg soil)⁻¹ (Moreda-Piñeiro et al., 2011). The interaction of iodine with soil organic and inorganic components increases the fixation, decreases the rate of volatilization, and reduces its bioavailability. The complexation of iodine with organic matter, metal oxides and clays causes a strong fixation of iodine in soil and modifies the concentration of water-soluble iodine available to plants (Whitehead, 1974). The soluble iodine content of soils is usually <10% of the total iodine fixed in soil. The availability of soluble iodine is higher with a low oxidoreductive potential (Eh) (with I⁻ as the dominant chemical form of iodine) and lower under oxidizing conditions (with as the most abundant form; Fuge and Johnson, 2015).

The Eh of soil changes the iodine speciation, which is expressed as the dynamic ratio []/[I⁻] (Figure 4). In the soil, organic matter, flooding, excessive irrigation and inorganic sources of reductor potential, such as the sulfides, Fe⁺², and FeS induce low Eh, for which the expected form of iodine would be I⁻, generated from the reaction + 6e⁻ + 6H⁺ → I⁻ + H₂O¹. This reaction can be developed abiotically with and organic matter producing HIO and I₂, the latter of which is reduced to I- (Steinberg et al., 2008). By contrast, under high Eh (e.g., low amount of organic matter or low water content in the soil pores), will be the most abundant form. The difference between and I⁻ is that the former is less subjected to volatilization (Guido-Garcia et al., 2015).

It has been observed in experiments on different types of soil that tends to be more adsorbed to soil components than I⁻, also showing less leaching and toxicity toward crops (Hong et al., 2012; Lawson et al., 2015). In soils with >10% organic matter, it has been observed that the humic substances can fix the I⁻ and from aerosols and rain, whereas in soil with <6% organic matter, the is adsorbed to metal oxides [Fe(OH)₃, Al(OH)₃, Mn₄O₂]. With a low pH, or with the Eh to the reducing side, these same metals act as reducers and accelerate the I⁻ reaction with organic matter (Bowley, 2013). In acidic soils (pH < 7), the balance between chemical species of iodine leans toward I⁻; while under pH > 7, the predominant form is . The ITF values for cereal grains do not change in the pH interval 5.4–7.6 (Shinonaga et al., 2001), however, toward the extremes of pH (pH < 5 and pH > 8), more adsorption of I⁻ and will occur (Yoshida et al., 1992; Dai et al., 2009), probably decreasing the bioavailability of iodine for plants.

Among the different physicochemical factors that modify the availability and immobilization of iodine in the soil, the amount of organic matter is the most widely studied (Whitehead, 1978; Sheppard and Thibault, 1992; Yu et al., 1996; Dai et al., 2006). Humified soil matter has been identified as an important reservoir that decreases the iodine dissipation rate (Shetaya et al., 2012) through the formation of covalent bonds between carbon atoms and iodine (Stavber et al., 2008). This reaction mechanism of iodine with organic matter is an electrophilic substitution of H by iodine in a phenolic ring (Reiller et al., 2006). Soil microbes can accelerate this process through the action of laccase enzymes that oxidizes I⁻ to I₂ and HOI (Shimamoto et al., 2011; Seki et al., 2013), which in a subsequent step are incorporated into organic matter.

The association of iodine and organic matter is not permanent; it is known that iodine in soil is subjected to absorption and desorption processes. Under reducing conditions, such as those in rice paddy fields, soil suffers high iodine desorption promoted by low Eh (−0.1 V), the addition of straw or glucose, root exudates, and microbial metabolism. The desorbed iodine is volatilized by organic matter (especially with a low level of humification), either directly by abiotic halogenation or by the intervention of haloperoxidases of microorganisms (Wever, 2012; Leri and Ravel, 2015). The initial reaction with organic matter is faster for I⁻ and slower for , but after a time of ~60 days or more, both forms participate in a process of transformation in volatile organoiodine compounds, occurring in the presence of organic matter in the soil, with or without the participation of microorganisms (Yamaguchi et al., 2010). Volatilization is dependent on both Eh and pH, with the lowest levels of volatilization in oxic alkaline soils, where the most abundant form of iodine is the non-volatile ; in contrast, in waterlogged and organic soils occur higher rates of volatilization resulting from the predominance of I⁻ that is oxidized to I₂ and CH₃I. It has been suggested that in inland areas, the contribution of atmospheric iodine depends significantly on the volatilization of the iodine in the soil (Fuge and Johnson, 2015).

Impact on productivity and yield

The use of iodine in the nutrient solution in concentrations from 10⁻⁶ M (equivalent to 0.13 mg L⁻¹) in soilless culture typically produces an increase in biomass in leafy vegetables, such as Chinese cabbage, spinach, and lettuce (Borst Pauwels, 1961; Whitehead, 1973; Weng et al., 2003, 2008c; Zhu et al., 2003; Dai et al., 2004b; Blasco et al., 2013). The iodine concentration can be increased to 10⁻⁵ M (equivalent to 1.3 mg L⁻¹), to produce biofortified leafy vegetables using I⁻, , or iodoacetic acid (CH₂ICOOH⁻; Weng et al., 2008c). While Lehr et al. (1958) obtained higher yields of tomato when applying 2 mg L⁻¹ KI, Hageman et al. (1942) could not observe any effect on the biomass of tomato when applying 3.2 × 10⁻⁵ M KI (equivalent to 4 mg L⁻¹). Meanwhile, in tomato, Kiferle et al. (2013) used high concentrations of 1 to 5 × 10⁻³ M of KI and 0.5 to 2 × 10⁻³ M KIO₃ in the nutrient solution once a week (eight times, starting with the fruit set of the first cluster), obtaining remarkable results, with an accumulation of iodine in the fruit of up to 10 mg of iodine per kg of fresh weight of fruit with little phytotoxicity. In strawberry plants, iodine increases plant biomass and fruit quality (Li et al., 2016). On the other hand, a decrease in biomass has been reported in tomato and potato (Caffagni et al., 2011), as well as in carrot (Smoleń et al., 2014b) and in Opuntia (García-Osuna et al., 2014), although in other plants where the vegetative reserve organs are also harvested, such as onion, iodine seems to have no effect on the weight of the plant (Dai et al., 2004b). Moreover, in rice, decreases in weight (Mackowiak and Grossl, 1999) and plant height (Singh et al., 2012) occur when applying potassium iodide. This negative effect does not seem to be general for grasses, considering that null or positive effects on biomass have been reported in wheat and corn (Borst Pauwels, 1961; Mao et al., 2014). Furthermore, when iodine is applied to the soil where plants are growing, the results are either mixed, showing positive, null, and negative effects (Dai et al., 2004b), or, as in tomato, are less efficient in terms of iodine bioaccumulation in the fruits compared to the soilless system (Caffagni et al., 2012).

It has also been observed that the effect of the application of iodine on biomass was directly dependent on the amount applied. Globally, the average concentration of iodine in the soil is 2.6 mg kg⁻¹ (Watts et al., 2010). Contributions of up to 10 mg (kg soil)⁻¹ promote plant growth, whereas values greater than 50 mg (kg soil)⁻¹, which are used to increase the iodine concentration significantly in plant tissues, produce varying results depending on the plant species (Cui et al., 2003; Lawson, 2014). In some species, such as Chinese cabbage, the application of more than 25 mg (kg soil)⁻¹ decreases the plant biomass (Hong et al., 2008). On the other hand, iodine concentrations higher than 100 μM in the nutrient solution revealed an adverse effects on rice biomass (Mackowiak and Grossl, 1999; Singh et al., 2012), and in lettuce the same negative effect was observed by adding 40 μM of iodine (Blasco et al., 2008; Table 2). In strawberry plants, iodine in nutrient solution at concentrations of up to 1.97 × 10⁻⁶ M (0.25 mg L⁻¹) of I⁻ and 2.86 × 10⁻⁶ M (0.50 mg L⁻¹) of increased the plant biomass and iodine concentration in fruits (Li et al., 2016). Thresholds for beneficial concentrations and toxicity of iodine are different between species, as a result of the inherent variability found among species and of the specific interaction of each plant species with edaphic, climatic, and biotic variables (Hageman et al., 1942; Mackowiak et al., 2005; Caffagni et al., 2012).

The results in the literature indicate that neither the chemical species applied nor the form of iodine application (i.e., fertigation, foliar spray, nutrient solution) has a consistent effect between different crops (Tables 3, 4). It has been reported that the application of iodine as is favorable to that of I⁻, especially for the synthesis of antioxidant compounds (Leyva et al., 2011; Blasco et al., 2013), although in some species such as strawberry, clover, and perennial ryegrass, I⁻ is more efficient than (Whitehead, 1973; Li et al., 2016). In lettuce, KIO₃ applied to the soil at up to 7.5 kg ha⁻¹ IO₃ is more effective than KI, as it gave a better result in terms of biofortification (50–100 μg I per 100 g FW) and does not affect biomass negatively. In contrast, by leaf spraying the best result was obtained when applying KI at 0.5 kg ha⁻¹ iodide (Lawson et al., 2015). The above indicates that each species will respond in a different way and under the context of the culture system. The difference between and I⁻ becomes more complicated in the case of cultivation in soil due to the different stability, residuality, and form of interaction of each chemical species with biotic and abiotic soil components (Dai et al., 2004a, 2009). A possible alternative for the biofortification of crops grown in soil is the use of marine algae applied to soil (Fuge and Johnson, 2015), or mixtures of marine algae and diatomite, with the algae being the source of iodine and diatomite an adsorbent that provides a constant supply of the element. The mixture achieves a good result in terms of the biofortification of different crop species (Weng et al., 2013, 2014). A second alternative would be the application of iodine in plantlets, using enriched peat, perhaps iodine complexed with biopolymers or porous materials, or leaf spray. This biofortification technique in the pre-transplanting stage has worked well in case of cucumber biofortified with selenium (Businelli et al., 2015).

Considering the form of iodine application (Table 4), biofortification has been successful with the application of 5% KIO₃ solution, dripped into irrigation canals (Cao et al., 1994; Ren et al., 2008). Other authors suggest the use of fertigation as a means of iodine application because their results show that adding iodine to the soil increases its absorption by plants (Ujowundu et al., 2010; Kiferle et al., 2013) especially if it is applied together with humic substances or organic acids (Smoleń et al., 2015a,c). The application of iodine through fertigation has shown other positive effects, such as increased biomass in leafy vegetables (Dai et al., 2004b). Foliar spray is another effective method of biofortification of plants with iodine; in lettuce (Smoleń et al., 2014a) and alfalfa (Altınok et al., 2003) this method was more efficient than the application of iodine in the nutrient solution (Figure 5).

Figure 5

Antioxidant content

Iodine applications have shown mixed effects on the antioxidant potential in several crop species, depending on the sources of iodine, concentration, and type of application. In a study of soybean grown in containers with soil and compost, it was found that the KIO₃ at concentrations of 20, 40, and 80 μM increased the enzyme activities of SOD and APX (Gupta et al., 2015). In tomato, it was reported that applying at 7.88 μM increased the content of ascorbic acid and total phenolic compounds (Smoleń et al., 2015c). Similarly, an increase was reported in the content of ascorbic acid in Opuntia ficus-indica, grown in soil under low tunnels by applying 10⁻⁴ M KIO₃ and KI by fertigation (García-Osuna et al., 2014). In Ipomoea aquatica, I⁻ induced a higher amount of ascorbic acid, while and iodoacetic acid (CH₂ICOO⁻) had the opposite effect (Weng et al., 2008c). Whereas, in tomato grown in sand, I⁻ at a concentration of 4 mg L⁻¹ (3.2 × 10⁻⁵ M) decreased the concentration of ascorbic acid in the foliage of plants (Hageman et al., 1942).

Blasco and collaborators have extensively studied the impact of iodine on antioxidant metabolism in lettuce grown in hydroponics. In their first study, it was found that the application of KI increases the accumulation of phenols and ascorbic acid, as well as the antioxidant potential (Blasco et al., 2008). Subsequently they reported that the application of KI (20, 40, and 80 μM) and KIO₃ (20 μM) increased the concentration of ascorbic acid and the enzymatic activity of catalase (CAT) but decreased the GSH concentration and activity of SOD. The APX activity was increased more effectively by KIO₃ than by KI (Blasco et al., 2011). The positive effect occurred even when applying low concentration (<40 μM) of KIO₃, increasing the activity of enzymatic antioxidants, such as superoxide dismutase (SOD) and ascorbate peroxidase (APX), as well as that of non-enzymatic antioxidants such as glutathione (GSH) and ascorbic acid (AA) (Leyva et al., 2011). In a more recent study, they found an increase in the antioxidant response and a greater accumulation of total phenolic compounds using KIO₃ at concentrations of 20 and 40 μM (Blasco et al., 2013).

As shown in Table 3, most of the cited studies used as a source of iodine KI or KIO₃. There are more reports of negative effects when applying KI, while there are more reports of positive effects when applying KIO₃, especially in the generation of antioxidant compounds. The difference in effects between the chemical forms of iodine is possible related to the function of as growth promoter by inducing reductase activity in the root (Kato et al., 2013), while the iodide reduction ability perhaps modifies the redox balance and cell-associated methyltransferase metabolism, making more likely metabolic adjustments that slow the growth and yield. Unfortunately, there is not much research on the effect of iodine on the metabolic processes of plants. In lettuce, the application of iodide and iodate (20, 40, and 80 μM) altered N metabolism and photorespiration. Positive effects were observed on biomass and N uptake with the use of iodate, whereas iodide decreased plant biomass and N concentration (Blasco et al., 2010). In marine plants, iodide does not cause these effects because it is rapidly oxidized by the V-IPO enzyme (Küpper et al., 1998), which has not been found active in land plants (Pilbeam and Drihem, 2007).

On the other hand, the possibility that many of the effects that have been observed when applying iodine modify the behavior and profile of the plant microbiome should not be ignored. Bacteria and fungi dissipate halogens with a metabolic system that includes a V-IPO enzyme (Wever, 2012; Fournier et al., 2014). It is possible that the response of the plant microbiome and, indirectly, the responses of plants to iodine application depend on the characteristics of the soil and irrigation water, including the concentrations of vanadium, sulfur, and organic matter. The importance of the microbiome as a possible determinant of plant responses to iodine has been poorly explored, but its significance has become evident regarding the adaptability and susceptibility of plants to stress (Porras-Alfaro and Bayman, 2011; Berg et al., 2014).

Stress tolerance

Most of the factors that induce stress increase the concentration of reactive oxygen species (ROS) at the cellular level. Consequently, the induction of antioxidants is considered an important facet of the adaptive responses leading to stress tolerance in plants (Gill and Tuteja, 2010). It has been proposed that iodine was one of the first (inorganic) antioxidants, that allowed the organisms to resist oxidative stress once the atmospheric O₂ concentration began to increase after the origin of oxygenic photosynthesis (Crockford, 2009; Küpper et al., 2011; Venturi, 2011). This function of iodine was proven in marine algae, where the element inactivates superoxide (), hydroxyl (OH^.), singlet oxygen (¹O₂), and hydrogen peroxide (H₂O₂) (Küpper et al., 2008). In some studies, it was found that iodine increased the amount of antioxidants and allowed greater resistance to certain types of abiotic stress, such as salinity and heavy metals (Leyva et al., 2011; Gupta et al., 2015). The treatment of soybean and sunflower seeds with a dry dressing of iodine and calcium carbonate reduced physiological deterioration under high temperature and humidity. Treated seeds exhibited lower levels of membrane damage, reflected in better germination and seedling growth [Dey(née Pathak) and Mukherjee, 1984]. The short-term pre-treatment of oilseed rape seeds with iodine considerably improved the survival of individuals in deterioration tests (Powell et al., 2005). Seed deterioration is primarily associated with oxidative stress (Sun and Leopold, 1995); therefore the above studies demonstrate the induction of tolerance by iodine, functioning perhaps as an antioxidant. Analogous results were obtained by pretreating peanut seeds with zinc, leading to the improvement in the response to the pathogen Aspergillus niger (Jajda and Thakkar, 2012).

More research is needed on the potential of iodine to induce tolerance to stress. The adoption of the use of iodine by the commercial agricultural sector will be fastest if the application of the element is presented to producers and companies as an alternative to mitigate damage from biotic and abiotic stresses and to promote plant growth. The advantage of this approach is that it is more attractive from an economic standpoint, reaching in parallel the goal of crop biofortification. To our knowledge, there are no published studies on the impact of iodine on plant pathogens, although it was reported that iodine is effective (0.7 mg L⁻¹) in killing fungi in recirculating water in soilless cultures (Runia, 1995). The problem with the direct use of iodine as a microbicide is that it rapidly induces resistance and forces the use of higher concentrations than are suitable for plants and beneficial microorganisms (Mackowiak et al., 2005). Instead we considered the possibility that iodine is an inductor of tolerance to certain pathogens by activating or by modifying the plant's defense systems through redox signals or through chemical changes in the cuticle (Shaw et al., 2007), which is essential for the induction of systemic acquired resistance (SAR; Xia et al., 2009). The same modifications on cuticular waxes induced by iodine may change the pattern of interactions of plants with pathogens, such as germination and the formation of appressoria (Gniwotta et al., 2005; Silva-Moreno et al., 2016). If it is shown that iodine has this function, the element could be applied as a tool to control crop pathogens.

Interactions with other elements

The conversion of iodine in its different chemical species, the mobilization and metabolism, depends on the factors that modify Eh and pH. Iodine per se has a significant impact on the redox state of the system that absorbs the element (Venturi, 2011); therefore, it interacts with other chemical components of the system, such as organic compounds and metal ions (Fe, Cu, Mn, V), modifying the oxidation state and bioavailability (Hageman et al., 1942). These components in turn give rise to changes in the chemical form, bioavailability and rate of volatilization of iodine in the biomass, water, and soil (Whitehead, 1984), as well as possible changes in the bioavailability of other elements (Terzano et al., 2015).

An iodine biofortification program must occur ideally in absence of restrictions on other mineral elements (White and Broadley, 2009). The interactions between mineral elements can be either synergistic or antagonistic. Synergisms refer to the increased absorption, transport, uptake or metabolism of an element in the presence of iodine. Antagonisms occur when any of the listed activities is diminished in the presence of iodine. In lettuce, it was found that the soil application of KI (0.5–2.0 kg ha⁻¹) and leaf spraying with KIO₃ (0.02–2 kg ha⁻¹) do not substantially change the mineral composition of lettuce. From a statistical point of view, there occurred significant changes in plants in both macronutrients N, P, K, Mg, Ca, S, and Na, and microelements B, Cu, Fe, Mn, Zn, and Mo, including Al, Cd, and Pb, but the changes were not significant from a functional point of view (Smoleń et al., 2011). It has been verified in hydroponics that the combined application of KIO₃ and in lettuce plants does not affect the biomass or mineral composition, showing a synergistic effect resulting in the increased absorption of both elements in the leaves (Smoleń et al., 2014a). The above does not seem to cause any significant antagonism between iodine and other elements, at least for lettuce. However, in a more recent study of the same crop (Smoleń et al., 2015b), a negative correlation was found between the contents of iodine and of K, Mg, Ca, S, Na, B, Cu, Fe, Mn, Zn, Cd, and Pb. Moreover, an increase in P, K, Mg, and Fe was reported when applying KIO₃, along with an increase in Cu and Mn when using KI in Opuntia ficus-indica (García-Osuna et al., 2014). Unfortunately for other species there is little information about the impact of iodine on other mineral elements (Smoleń et al., 2014a).

In biofortification experiments with tomato, where iodine was applied in a range of 10⁻⁶–10⁻⁵ M, a positive correlation was found between iodine concentration and Cu and Mn in leaves (Hageman et al., 1942). In lettuce, applying KI to the soil and KIO₃ by leaf spray produced the same effect on Mn but not on Cu (Smoleń et al., 2011).

Bacteria living in iodine-rich groundwater have proteins called IoxA, which are capable of oxidizing I⁻ to I₂. These proteins have been characterized as multicopper oxidases, i.e., oxidases with several Cu cofactors (Suzuki et al., 2012; Shiroyama et al., 2015). Another possible explanation regarding the relationship between copper and iodine has to do with the ability of copper oxidases to oxidize I⁻ to I₂ or HOI (Xu, 1996). It is possible that a greater amount of iodine present in plant tissues induces increased activity in the systems that dissipate the element, such as copper oxidases and possibly other oxidases with Fe and Mn (Klebanoff, 1982; Schlorke et al., 2016). This increased activity could induce changes in the concentration of Cu, Fe, and Mn in tissues that actively dissipate iodine.

Hageman et al. (1942) proposed that changes in the mineral composition of plants that occur when applying iodine relate to a redox phenomenon, explaining that the oxidation of I⁻ to I₂ provides a reducing potential of −0.535 V. Iodate may cause a similar effect by the induction of reductase activity in the root (Kato et al., 2013). This redox effect of iodine will have a more or less impact on the bioavailability of other elements depending on the complexity and number of components in the interaction. There are fewer of these components in soilless production systems but much more in a soil system with interacting biological, organic and inorganic components in both the exchange matrix and soil solution (Jones, 1998). It is possible that these differences in the complexity of interactions between the components of each production system (soil and soilless) could help to explain the diversity of results obtained with iodine application in crops. The study of ionome in plants might be used to deal with this complexity, as a tool for explain and predict the nutritional profile, considering both essential as non-essential elements. This approach has been successful in the case of iron (Pii et al., 2015; Gattullo et al., 2016), but so far has not been used with iodine.

Conclusions

The dynamic behavior of iodine is modified by multiple environmental factors that change its flow rate and mobilization among different compartments of the ecosystems. It is necessary to consider more closely the microbial contribution to these flows and to the functions of iodine in ecological systems, in addition to their mere presence or potential role in crop plants.

The variability of the effects of iodine, when applied to crops, can be partially explained when considering the possible impact on N metabolism, photorespiration, and one-carbon metabolism. Additionally, it is necessary to consider interactions with other elements, such as Fe, Mn, Cu, and V, either directly in the plant metabolism or indirectly through the microbiome of the plant.

In general, the effect of iodine is positive on the growth of plants. Good results are obtained regarding biofortification when applied to the soil as KIO₃ in concentrations of 7.5 kg ha⁻¹, 10 mg (kg soil)⁻¹ in pots, or 10⁻⁶–10⁻⁵ M in the nutrient solution. Leaf spray with KI at 0.5 kg ha⁻¹ gave good results. With higher concentrations, the response is variable: negative, neutral, or positive, depending on the plant species.

Positive results have been obtained when applying 10⁻³ M iodine in the nutrient solution but only when doing so on a weekly basis. The use of seaweed applied to the soil also increased the availability of iodine. More research is needed on the use of biopolymers to form complex with iodine to enhance bioavailability and decrease volatilization in soil and pots and on the potential of iodine to induce a higher stress tolerance.

References

• 1

  AltınokS.Sozudogru-OkS.HalilovaH. (2003). Effect of iodine treatments on forage yields of alfalfa. Commun. Soil Sci. Plant Anal.34, 55–64. 10.1081/CSS-120017415

  • CrossRef
  • Google Scholar

• 2

  AmachiS. (2008). Microbial contribution to global iodine cycling: volatilization, accumulation, reduction, oxidation, and sorption of iodine. Microbes Environ.23, 269–276. 10.1264/jsme2.ME08548

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 3

  AmachiS.KasaharaM.HanadaS.KamagataY.ShinoyamaH.FujiiT.et al. (2003). Microbial participation in iodine volatilization from soils. Environ. Sci. Technol.37, 3885–3890. 10.1021/es0210751

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 4

  AmiroB. D.JohnstonF. L. (1989). Volatilization of iodine from vegetation. Atmos. Environ.23, 533–538. 10.1016/0004-6981(89)90002-4

  • CrossRef
  • Google Scholar

• 5

  AnderssonM.KarumbunathanV.ZimmermannM. B. (2012). Global iodine status in 2011 and trends over the past decade. J. Nutr.142, 744–750. 10.3945/jn.111.149393

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 6

  AnguianoB.AcevesC. (2011). Iodine in mammary and prostate pathologies. Curr. Chem. Biol.5, 177–182. 10.2174/187231311796765049

  • CrossRef
  • Google Scholar

• 7

  ArandaN.SosaS.DelgadoG.AcevesC.AnguianoB. (2013). Uptake and antitumoral effects of iodine and 6-iodolactone in differentiated and undifferentiated human prostate cancer cell lines. Prostate73, 31–41. 10.1002/pros.22536

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 8

  BackerH.HollowellJ. (2000). Use of iodine for water disinfection: iodine toxicity and maximum recommended dose. Environ. Health Perspect.108, 679–684. 10.1289/ehp.00108679

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 9

  Ban-naiT.MuramatsuY.AmachiS. (2006). Rate of iodine volatilization and accumulation by filamentous fungi through laboratory cultures. Chemosphere65, 2216–2222. 10.1016/j.chemosphere.2006.05.047

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 10

  BarberM. J.NottonB. A. (1990). Spinach nitrate reductase : effects of ionic strength and ph on the full and partial enzyme activities. Plant Physiol.93, 537–540. 10.1104/pp.93.2.537

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 11

  Barbier-BrygooH.De AngeliA.FilleurS.FrachisseJ.-M.GambaleF.ThomineS.et al. (2011). Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu. Rev. Plant Biol.62, 25–51. 10.1146/annurev-arplant-042110-103741

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 12

  BarryP. J.ChamberlainA. C. (1963). Deposition of iodine onto plant leaves from air. Health Phys.9, 1149–1157. 10.1097/00004032-196312000-00011

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 13

  BergG.GrubeM.SchloterM.SmallaK. (2014). Unraveling the plant microbiome: looking back and future perspectives. Front. Microbiol.5:148. 10.3389/fmicb.2014.00148

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 14

  BlascoB.LeyvaR.RomeroL.RuizJ. M. (2013). Iodine effects on phenolic metabolism in lettuce plants under salt stress. J. Agric. Food Chem.61, 2591–2596. 10.1021/jf303917n

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 15

  BlascoB.RiosJ. J.CervillaL. M.Sánchez-RodrigezE.RuizJ. M.RomeroL. (2008). Iodine biofortification and antioxidant capacity of lettuce: potential benefits for cultivation and human health. Ann. Appl. Biol.152, 289–299. 10.1111/j.1744-7348.2008.00217.x

  • CrossRef
  • Google Scholar

• 16

  BlascoB.RiosJ. J.CervillaL. M.Sánchez-RodríguezE.Rubio-WilhelmiM. M.RosalesM. A.et al. (2010). Photorespiration process and nitrogen metabolism in lettuce plants (Lactuca sativa L.): induced changes in response to iodine biofortification. J. Plant Growth Regul.29, 477–486. 10.1007/s00344-010-9159-7

  • CrossRef
  • Google Scholar

• 17

  BlascoB.RíosJ. J.LeyvaR.CervillaL. M.Sánchez-RodríguezE.Rubio-WilhelmiM. M.et al. (2011). Does iodine biofortification affect oxidative metabolism in lettuce plants?Biol. Trace Elem. Res.142, 831–842. 10.1007/s12011-010-8816-9

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 18

  Borst PauwelsG. W. F. H. (1961). Iodine as a micronutrient for plants. Plant Soil14, 377–392. 10.1007/BF01666295

  • CrossRef
  • Google Scholar

• 19

  Borst PauwelsG. W. F. H. (1962). An investigation into the effects of iodide and iodate on plant growth. Plant Soil16, 284–292. 10.1007/BF01381340

  • CrossRef
  • Google Scholar

• 20

  BowleyH. (2013). Iodine Dynamics In The Terrestrial Environment. dissertation/Ph.D. thesis, University of Nottingham, Nottingham. Available online at: http://eprints.nottingham.ac.uk/13241/1/Iodine_dynamics_in_the_terrestrial_environment_-_Hannah_Bowley.pdf (Accessed January 31, 2016).

  • Google Scholar

• 21

  BullochM. N. (2014). Acute iodine toxicity from a suspected oral methamphetamine ingestion. Clin. Med. Insights Case Rep.7, 127–129. 10.4137/CCRep.S20086

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 22

  BurlingameB. (2013). The Role of Agriculture in Diet: Quantity versus Quality no Title. Conf. Front. Agric. Sustain. Stud. Protein Supply Chain to Improv. Diet. Qual. New York Acad. Sci. Available online at: http://www.nyas.org/Publications/Ebriefings/Detail.aspx?cid=5309dc45-a7a8-4611-90f6-dba5b2a139b6 (Accessed January 1, 2016).

  • Google Scholar

• 23

  BusinelliD.D'AmatoR.OnofriA.TedeschiniE.TeiF. (2015). Se-enrichment of cucumber (Cucumis sativus L.), lettuce (Lactuca sativa L.) and tomato (Solanum lycopersicum L. Karst) through fortification in pre-transplanting. Sci. Hortic.197, 697–704. 10.1016/j.scienta.2015.10.039

  • CrossRef
  • Google Scholar

• 24

  CaffagniA.ArruL.MeriggiP.MilcJ.PerataP.PecchioniN. (2011). Iodine fortification plant screening process and accumulation in tomato fruits and potato tubers. Commun. Soil Sci. Plant Anal.42, 706–718. 10.1080/00103624.2011.550372

  • CrossRef
  • Google Scholar

• 25

  CaffagniA.PecchioniN.MeriggiP.BucciV.SabatiniE.AcciarriN.et al. (2012). Iodine uptake and distribution in horticultural and fruit tree species. Ital. J. Agron.7:32. 10.4081/ija.2012.e32

  • CrossRef
  • Google Scholar

• 26

  CaoX.-Y.JiangX.-M.DouZ.-H.RakemanM. A.KareemA.ZangM.-L.et al. (1994). Iodination of irrigation water as a method of supplying iodine to a severely iodine-deficient population in XinJiang, China. Lancet344, 107–110. 10.1016/S0140-6736(94)91286-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 27

  CappuynsV.SwennenR. (2014). Release of vanadium from oxidized sediments: insights from different extraction and leaching procedures. Environ. Sci. Pollut. Res. Int.21, 2272–2282. 10.1007/s11356-013-2149-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 28

  CarpenterL. J.MalinG.LissP. S.KüpperF. C. (2000). Novel biogenic iodine-containing trihalomethanes and other short-lived halocarbons in the coastal east Atlantic. Global Biogeochem. Cycles14, 1191–1204. 10.1029/2000GB001257

  • CrossRef
  • Google Scholar

• 29

  CharltonK.SkeaffS. (2011). Iodine fortification: why, when, what, how, and who?Curr. Opin. Clin. Nutr. Metab. Care14, 618–624. 10.1097/MCO.0b013e32834b2b30

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 30

  CharltonK. E.JoosteP. L.SteynK.LevittN. S.GhoshA. (2013). A lowered salt intake does not compromise iodine status in Cape Town, South Africa, where salt iodization is mandatory. Nutrition29, 630–634. 10.1016/j.nut.2012.09.010

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 31

  Colmenero-FloresJ. M.MartínezG.GambaG.VázquezN.IglesiasD. J.BrumósJ.et al. (2007). Identification and functional characterization of cation-chloride cotransporters in plants. Plant J.50, 278–292. 10.1111/j.1365-313X.2007.03048.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 32

  CrockfordS. J. (2009). Evolutionary roots of iodine and thyroid hormones in cell-cell signaling. Integr. Comp. Biol.49, 155–166. 10.1093/icb/icp053

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 33

  CuiX.SangY.SongJ. (2003). [Residual of exogenous iodine in forest soils and its effect on some wild-vegetable plants]. J. Appl. Ecol.14, 1612–1616.

  • Pubmed Abstract
  • Google Scholar

• 34

  DaiJ. L.ZhangM.HuQ. H.HuangY. Z.WangR. Q.ZhuY. G. (2009). Adsorption and desorption of iodine by various Chinese soils: II. Iodide and iodate. Geoderma153, 130–135. 10.1016/j.geoderma.2009.07.020

  • CrossRef
  • Google Scholar

• 35

  DaiJ.-L.ZhangM.ZhuY.-G. (2004a). Adsorption and desorption of iodine by various Chinese soils: I. Iodate. Environ. Int.30, 525–530. 10.1016/j.envint.2003.10.007

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 36

  DaiJ. L.ZhuY. G.HuangY. Z.ZhangM.SongJ. L. (2006). Availability of iodide and iodate to spinach (Spinacia oleracea L.) in relation to total iodine in soil solution. Plant Soil289, 301–308. 10.1007/s11104-006-9139-7

  • CrossRef
  • Google Scholar

• 37

  DaiJ.-L.ZhuY.-G.ZhangM.HuangY.-Z. (2004b). Selecting iodine-enriched vegetables and the residual effect of iodate application to soil. Biol. Trace Elem. Res.101, 265–276. 10.1385/BTER:101:3:265

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 38

  de BenoistB.McLeanE.AnderssonM.RogersL. (2008). Iodine deficiency in 2007: global progress since 2003. Food Nutr. Bull.29, 195–202. 10.1177/156482650802900305

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 39

  de CaffarelliE. (1997). Iodine. Consequences of a deficiency, of excessive iodine, and value of systematic supplementation. J. Gynécol. Obstet. Biol. Reprod.26, 90–94.

  • Pubmed Abstract
  • Google Scholar

• 40

  Dey(née Pathak)G.MukherjeeR. K. (1984). Iodine treatment of soybean and sunflower seeds for controlling deterioration. Field Crop Res.9, 205–213. 10.1016/0378-4290(84)90026-1

  • CrossRef
  • Google Scholar

• 41

  EalesJ. G. (1997). Iodine metabolism and thyroid-related functions in organisms lacking thyroid follicles: are thyroid hormones also vitamins?Exp. Biol. Med.214, 302–317. 10.3181/00379727-214-44098

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 42

  EneqvistT.LundbergE.NilssonL.AbagyanR.Sauer-ErikssonA. E. (2003). The transthyretin-related protein family. Eur. J. Biochem.270, 518–532. 10.1046/j.1432-1033.2003.03408.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 43

  FAO (2009). The State of Food Insecurity in the World.Rome: Food and Agriculture Organization of the United Nations.

  • Google Scholar

• 44

  FordyceF. M. (2003). Database of the Iodine Content of Food and Diets Populated with Data from Published Literature. Commisioned Report CR/03/84N. Nottingham: British Geological Survey.

  • Google Scholar

• 45

  FournierJ.-B.RebuffetE.DelageL.GrijolR.Meslet-CladièreL.RzoncaJ.et al. (2014). The Vanadium Iodoperoxidase from the marine flavobacteriaceae species Zobellia galactanivorans reveals novel molecular and evolutionary features of halide specificity in the vanadium haloperoxidase enzyme family. Appl. Environ. Microbiol.80, 7561–7573. 10.1128/AEM.02430-14

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 46

  FrickeW. (2015). The significance of water co-transport for sustaining transpirational water flow in plants: a quantitative approach. J. Exp. Bot.66, 731–739. 10.1093/jxb/eru466

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 47

  FugeR. (1996). Geochemistry of iodine in relation to iodine deficiency diseases. Geol. Soc.113, 201–211. 10.1144/GSL.SP.1996.113.01.16

  • CrossRef
  • Google Scholar

• 48

  FugeR. (2005). Soils and iodine deficiency, in Essentials of Medical Geology, eds SelinusO.AllowayB.CentenoJ. A.FinkelmanR. B.FugeR.LindhU.SmedleyP. (New York, NY: Elsevier Academic Press), 417–433.

  • Google Scholar

• 49

  FugeR. (2013). Soils and iodine deficiency, in Essentials of Medical Geology: Revised Edition, ed SelinusO. (Dordrecht: Springer Netherlands), 417–432.

  • Google Scholar

• 50

  FugeR.JohnsonC. C. (1986). The geochemistry of iodine - a review. Environ. Geochem. Health8, 31–54. 10.1007/BF02311063

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 51

  FugeR.JohnsonC. C. (2015). Iodine and human health, the role of environmental geochemistry and diet, a review. Appl. Geochem.63, 282–302. 10.1016/j.apgeochem.2015.09.013

  • CrossRef
  • Google Scholar

• 52

  FunahashiH.ImaiT.MaseT.SekiyaM.YokoiK.HayashiH.et al. (2001). Seaweed prevents breast cancer?Jpn. J. Cancer Res.92, 483–487. 10.1111/j.1349-7006.2001.tb01119.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 53

  García-OsunaH. T.Benavides-MendozaA.Rivas-MoralesC.Morales-RubioE.Verde-StarJ.Miranda-RuvalcabaR. (2014). Iodine application increased ascorbic acid content and modified the vascular tissue in Opuntia ficus-indica. Pak. J. Bot.46, 127–134. Available online at: http://www.pakbs.org/pjbot/abstracts/46(1)/13.html

  • Google Scholar

• 54

  García-SolísP.AlfaroY.AnguianoB.DelgadoG.GuzmanR. C.NandiS.et al. (2005). Inhibition of N-methyl-N-nitrosourea-induced mammary carcinogenesis by molecular iodine (I2) but not by iodide (I-) treatment Evidence that I2 prevents cancer promotion. Mol. Cell. Endocrinol.236, 49–57. 10.1016/j.mce.2005.03.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 55

  GattulloC. E.AllegrettaI.MediciL.FijanR.PiiY.CescoS.et al. (2016). Silicon dynamics in the rhizosphere: connections with iron mobilization. J. Plant Nutr. Soil Sci.179, 409–417. 10.1002/jpln.201500535

  • CrossRef
  • Google Scholar

• 56

  GillS. S.TutejaN. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem.48, 909–930. 10.1016/j.plaphy.2010.08.016

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 57

  GniwottaF.VoggG.GartmannV.CarverT. L. W.RiedererM.JetterR. (2005). What do microbes encounter at the plant surface? Chemical composition of pea leaf cuticular waxes. Plant Physiol.139, 519–530. 10.1104/pp.104.053579

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 58

  Guido-GarciaF.LawG. T. W.LloydJ. R.LythgoeP.MorrisK. (2015). Bioreduction of iodate in sediment microcosms. Mineral. Mag.79, 1343–1351. 10.1180/minmag.2015.079.6.10

  • CrossRef
  • Google Scholar

• 59

  GuptaN.BajpaiM.MajumdarR.MishraP. (2015). Response of iodine on antioxidant levels of Glycine max L. Grown under Cd2+ stress. Adv. Biol. Res. (Rennes).9, 40–48. 10.5829/idosi.abr.2015.9.1.9183

  • CrossRef
  • Google Scholar

• 60

  GuptaU. C.GuptaS. C. (1998). Trace element toxicity relationships to crop production and livestock and human health: implications for management. Commun. Soil Sci. Plant Anal.29, 1491–1522. 10.1080/00103629809370045

  • CrossRef
  • Google Scholar

• 61

  HagemanR. H.HodgeE. S.McHargueJ. S. (1942). Effect of potassium iodide on the ascorbic acid content and growth of tomato plants. Plant Physiol.17, 465–472. 10.1104/pp.17.3.465

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 62

  HeX.NaraK. (2007). Element biofortification: can mycorrhizas potentially offer a more effective and sustainable pathway to curb human malnutrition?Trends Plant Sci.12, 331–333. 10.1016/j.tplants.2007.06.008

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 63

  HennerP.HurteventP.ThiryY.LevchukS.YoschenkoV.KashparovV. (2013). Translocation of (125)I, (75)Se and (36)Cl to edible parts of radish, potato and green bean following wet foliar contamination under field conditions. J. Environ. Radioact.124, 171–184. 10.1016/j.jenvrad.2013.05.012

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 64

  HerrettR. A.HatfieldH. H.CrosbyD. G.VlitosA. J. (1962). Leaf abscission induced by the iodide ion. Plant Physiol.37, 358–363. 10.1104/pp.37.3.358

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 65

  HeylandA.MorozL. L. (2005). Cross-kingdom hormonal signaling: an insight from thyroid hormone functions in marine larvae. J. Exp. Biol.208, 4355–4361. 10.1242/jeb.01877

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 66

  HongC.WengH.JilaniG.YanA.LiuH.XueZ. (2012). Evaluation of iodide and iodate for adsorption-desorption characteristics and bioavailability in three types of soil. Biol. Trace Elem. Res.146, 262–271. 10.1007/s12011-011-9231-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 67

  HongC.-L.WengH.-X.QinY.-C.YanA.-L.XieL.-L. (2008). Transfer of iodine from soil to vegetables by applying exogenous iodine. Agron. Sustain. Dev.28, 575–583. 10.1051/agro:2008033

  • CrossRef
  • Google Scholar

• 68

  HurteventP.ThiryY.LevchukS.YoschenkoV.HennerP.Madoz-EscandeC.et al. (2013). Translocation of 125I, 75Se and 36Cl to wheat edible parts following wet foliar contamination under field conditions. J. Environ. Radioact.121, 43–54. 10.1016/j.jenvrad.2012.04.013

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 69

  ItohN.TodaH.MatsudaM.NegishiT.TaniguchiT.OhsawaN. (2009). Involvement of S-adenosylmethionine-dependent halide/thiol methyltransferase (HTMT) in methyl halide emissions from agricultural plants: isolation and characterization of an HTMT-coding gene from Raphanus sativus (daikon radish). BMC Plant Biol.9:116. 10.1186/1471-2229-9-116

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 70

  JajdaH. M.ThakkarV. R. (2012). Control of Aspergillus niger infection in varieties of Arachis hypogeae L. by supplementation of zinc ions during seed germination. Arch. Phytopathol. Plant Prot.45, 1464–1478. 10.1080/03235408.2012.677312

  • CrossRef
  • Google Scholar

• 71

  JohnsonC. C. (2003). The Geochemistry of Iodine and its Application to Environmental Strategies for Reducing the Risks from Iodine Deficiency Disorders (IDD). Nottingham: British Geological Survey.

  • Google Scholar

• 72

  JonesC. E.HornsbyK. E.SommarivaR.DunkR. M.von GlasowR.McFiggansG.et al. (2010). Quantifying the contribution of marine organic gases to atmospheric iodine. Geophys. Res. Lett.37, 1–6. 10.1029/2010gl043990

  • CrossRef
  • Google Scholar

• 73

  JonesD. L. (1998). Organic acids in the rhizosphere – a critical review. Plant Soil205, 25–44. 10.1023/A:1004356007312

  • CrossRef
  • Google Scholar

• 74

  KaplanD. I.DenhamM. E.ZhangS.YeagerC.XuC.SchwehrK. A.et al. (2014). Radioiodine biogeochemistry and prevalence in groundwater. Crit. Rev. Environ. Sci. Technol.44, 2287–2335. 10.1080/10643389.2013.828273

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 75

  KarnaniM.AnnilaA. (2009). Gaia again. Biosystems95, 82–87. 10.1016/j.biosystems.2008.07.003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 76

  KatoS.WachiT.YoshihiraK.NakagawaT.IshikawaA.TakagiD.et al. (2013). Rice (Oryza sativa L.) roots have iodate reduction activity in response to iodine. Front. Plant Sci.4:227. 10.3389/fpls.2013.00227

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 77

  KiferleC.GonzaliS.HolwerdaH. T.Real IbacetaR.PerataP. (2013). Tomato fruits: a good target for iodine biofortification. Front. Plant Sci.4:205. 10.3389/fpls.2013.00205

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 78

  KlebanoffS. J. (1982). The iron-H2O2-iodide cytotoxic system. J. Exp. Med.156, 1262–1267. 10.1084/jem.156.4.1262

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 79

  KopećA.PiątkowskaE.Bieżanowska-KopećR.PyszM.KoronowiczA.Kapusta-DuchJ.et al. (2015). Effect of lettuce biofortified with iodine by soil fertilization on iodine concentration in various tissues and selected biochemical parameters in serum of Wistar rats. J. Funct. Foods14, 479–486. 10.1016/j.jff.2015.02.027

  • CrossRef
  • Google Scholar

• 80

  KotwalA.PriyaR.QadeerI. (2007). Goiter and other iodine deficiency disorders: a systematic review of epidemiological studies to deconstruct the complex web. Arch. Med. Res.38, 1–14. 10.1016/j.arcmed.2006.08.006

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 81

  KüpperF. C.CarpenterL. J.McFiggansG. B.PalmerC. J.WaiteT. J.BonebergE.-M.et al. (2008). Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc. Natl. Acad. Sci. U.S.A.105, 6954–6958. 10.1073/pnas.0709959105

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 82

  KüpperF. C.FeitersM. C.OlofssonB.KaihoT.YanagidaS.ZimmermannM. B.et al. (2011). Commemorating two centuries of iodine research: an interdisciplinary overview of current research. Angew. Chem. Int. Ed. Engl.50, 11598–11620. 10.1002/anie.201100028

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 83

  KüpperF. C.SchweigertN.Ar GallE.LegendreJ.-M.VilterH.KloaregB. (1998). Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta207, 163–171. 10.1007/s004250050469

  • CrossRef
  • Google Scholar

• 84

  LandiniM.GonzaliS.KiferleC.TonaccheraM.AgrettiP.DimidaA.et al. (2012). Metabolic engineering of the iodine content in Arabidopsis. Sci. Rep.2:338. 10.1038/srep00338

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 85

  LandiniM.GonzaliS.PerataP. (2011). Iodine biofortification in tomato. J. Plant Nutr. Soil Sci.174, 480–486. 10.1002/jpln.201000395

  • CrossRef
  • Google Scholar

• 86

  LawsonP. G. (2014). Development and Evaluation of Iodine Biofortification Strategies for Vegetables. Berlin: Logos Verlag Berlin GmbH.

  • Google Scholar

• 87

  LawsonP. G.DaumD.CzaudernaR.MeuserH.HärtlingJ. W. (2015). Soil versus foliar iodine fertilization as a biofortification strategy for field-grown vegetables. Front. Plant Sci.6:450. 10.3389/fpls.2015.00450

  • CrossRef
  • Google Scholar

• 88

  LazarusJ. H.BestwickJ. P.ChannonS.ParadiceR.MainaA.ReesR.et al. (2012). Antenatal thyroid screening and childhood cognitive function. N. Engl. J. Med.366, 493–501. 10.1056/NEJMoa1106104

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 89

  LeblancC.ColinC.CosseA.DelageL.La BarreS.MorinP.et al. (2006). Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie88, 1773–1785. 10.1016/j.biochi.2006.09.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 90

  LehrJ. J.WybengaJ. M.RosanowM. (1958). Iodine as a micronutrient for tomatoes. Plant Physiol.33, 421–427. 10.1104/pp.33.6.421

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 91

  LeriA. C.RavelB. (2015). Abiotic bromination of soil organic matter. Environ. Sci. Technol.49, 13350–13359. 10.1021/acs.est.5b03937

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 92

  LeungH.-M.WangZ.-W.YeZ.-H.YungK.-L.PengX.-L.CheungK.-C. (2013). Interactions between arbuscular mycorrhizae and plants in phytoremediation of metal-contaminated soils: a review. Pedosphere23, 549–563. 10.1016/S1002-0160(13)60049-1

  • CrossRef
  • Google Scholar

• 93

  LeyvaR.Sánchez-RodríguezE.RíosJ. J.Rubio-WilhelmiM. M.RomeroL.RuizJ. M.et al. (2011). Beneficial effects of exogenous iodine in lettuce plants subjected to salinity stress. Plant Sci.181, 195–202. 10.1016/j.plantsci.2011.05.007

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 94

  LiH.-P.DanielB.CreeleyD.GrandboisR.ZhangS.XuC.et al. (2014). Superoxide production by a manganese-oxidizing bacterium facilitates iodide oxidation. Appl. Environ. Microbiol.80, 2693–2699. 10.1128/AEM.00400-14

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 95

  LiH.-P.YeagerC. M.BrinkmeyerR.ZhangS.HoY.-F.XuC.et al. (2012). Bacterial production of organic acids enhances H2O2-dependent iodide oxidation. Environ. Sci. Technol.46, 4837–4844. 10.1021/es203683v

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 96

  LiR.LiuH.-P.HongC.-L.DaiZ.-X.LiuJ.-W.ZhouJ.et al. (2016). Iodide and iodate effects on the growth and fruit quality of strawberry. J. Sci. Food Agric.10.1002/jsfa.7719. [Epub ahead of print].

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 97

  LimchoowongN.SricharoenP.TechawongstienS.ChanthaiS. (2016). An iodine supplementation of tomato fruits coated with an edible film of the iodide-doped chitosan. Food Chem.200, 223–229. 10.1016/j.foodchem.2016.01.042

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 98

  LongvahT.TotejaG. S.BulliyyaG.RaghuvanshiR. S.JainS.RaoV.et al. (2012). Stability of added iodine in different Indian cooking processes. Food Chem.130, 953–959. 10.1016/j.foodchem.2011.08.024

  • CrossRef
  • Google Scholar

• 99

  MaQ.BaoA.-K.ChaiW.-W.WangW.-Y.ZhangJ.-L.LiY.-X.et al. (2016). Transcriptomic analysis of the succulent xerophyte Zygophyllum xanthoxylum in response to salt treatment and osmotic stress. Plant Soil402, 343–361. 10.1007/s11104-016-2809-1

  • CrossRef
  • Google Scholar

• 100

  MackowiakC. L.GrosslP. R. (1999). Iodate and iodide effects on iodine uptake and partitioning in rice (Oryza sativa L.) grown in solution culture. Plant Soil212, 133–141. 10.1023/A:1004666607330

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 101

  MackowiakC. L.GrosslP. R.CookK. L. (2005). Iodine toxicity in a plant-solution system with and without humic acid. Plant Soil269, 141–150. 10.1007/s11104-004-0401-6

  • CrossRef
  • Google Scholar

• 102

  MaoH.WangJ.WangZ.ZanY.LyonsG.ZouC. (2014). Using agronomic biofortification to boost zinc, selenium, and iodine concentrations of food crops grown on the loess plateau in China. J. Soil Sci. Plant Nutr.14, 459–470. 10.4067/s0718-95162014005000036

  • CrossRef
  • Google Scholar

• 103

  McFiggansG.CoeH.BurgessR.AllanJ.CubisonM.AlfarraM. R.et al. (2004). Direct evidence for coastal iodine particles from Laminaria macroalgae – linkage to emissions of molecular iodine. Atmos. Chem. Phys.4, 701–713. 10.5194/acp-4-701-2004

  • CrossRef
  • Google Scholar

• 104

  MillerA. E. M.HeylandA. (2013). Iodine accumulation in sea urchin larvae is dependent on peroxide. J. Exp. Biol.216, 915–926. 10.1242/jeb.077958

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 105

  MiyakeY.TsunogaiS. (1963). Evaporation of iodine from the ocean. J. Geophys. Res.68, 3989–3993. 10.1029/JZ068i013p03989

  • CrossRef
  • Google Scholar

• 106

  MooreR. M.GroszkoW. (1999). Methyl iodide distribution in the ocean and fluxes to the atmosphere. J. Geophys. Res. Ocean.104, 11163–11171. 10.1029/1998JC900073

  • CrossRef
  • Google Scholar

• 107

  Moreda-PiñeiroA.Romarís-HortasV.Bermejo-BarreraP. (2011). A review on iodine speciation for environmental, biological and nutrition fields. J. Anal. At. Spectrom.26, 2107–2152. 10.1039/C0JA00272K

  • CrossRef
  • Google Scholar

• 108

  MottiarY. (2013). Iodine biofortification through plant biotechnology. Nutrition29, 1431. 10.1016/j.nut.2013.04.009

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 109

  MottiarY.AltosaarI. (2011). Iodine sequestration by amylose to combat iodine deficiency disorders. Trends Food Sci. Technol.22, 335–340. 10.1016/j.tifs.2011.02.007

  • CrossRef
  • Google Scholar

• 110

  MoyersJ. L.DuceR. A. (1972). Gaseous and particulate iodine in the marine atmosphere. J. Geophys. Res.77, 5229–5238. 10.1029/JC077i027p05229

  • CrossRef
  • Google Scholar

• 111

  MuramatsuY.ChristoffersD.OhmomoY. (1983). Influence of chemical forms on iodine uptake by plant. J. Radiat. Res.24, 326–338. 10.1269/jrr.24.326

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 112

  MuramatsuY.YoshidaS. (1995). Volatilization of methyl iodide from the soil-plant system. Atmos. Environ.29, 21–25. 10.1016/1352-2310(94)00220-F

  • CrossRef
  • Google Scholar

• 113

  MuramatsuY.YoshidaS. (1999). Effects of microorganisms on the fate of iodine in the soil environment. Geomicrobiol. J.16, 85–93. 10.1080/014904599270776

  • CrossRef
  • Google Scholar

• 114

  NakamuraY.OhmomoY. (1984). Transfer of gaseous iodine to Tradescantia. J. Radiat. Res.25, 251–259. 10.1269/jrr.25.251

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 115

  NakamuraY.SumiyaM.UchidaS.OhmomoY. (1986). Transfer of gaseous iodine to rice plants. J. Radiat. Res.27, 171–182. 10.1269/jrr.27.171

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 116

  NguyenC. T.AgorioA.JossierM.DepréS.ThomineS.FilleurS. (2016). Characterization of the chloride channel-like, atclcg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol.57, 764–775. 10.1093/pcp/pcv169

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 117

  NitschkeU.DixneufS.RuthA. A.SchmidM.StengelD. B. (2013). Molecular iodine (I2) emission from two Laminaria species (Phaeophyceae) and impact of irradiance and temperature on I2 emission into air and iodide release into seawater from Laminaria digitata. Mar. Environ. Res.92, 102–109. 10.1016/j.marenvres.2013.09.006

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 118

  PearceE. N.AnderssonM.ZimmermannM. B. (2013). Global iodine nutrition: where do we stand in 2013?Thyroid23, 523–528. 10.1089/thy.2013.0128

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 119

  PellegrinoE.BediniS. (2014). Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol. Biochem.68, 429–439. 10.1016/j.soilbio.2013.09.030

  • CrossRef
  • Google Scholar

• 120

  PenningtonJ. A. (1990). A review of iodine toxicity reports. J. Am. Diet. Assoc.90, 1571–1581.

  • Pubmed Abstract
  • Google Scholar

• 121

  PessoaJ.SárkányZ.Ferreira-da-SilvaF.MartinsS.AlmeidaM. R.LiJ.et al. (2010). Functional characterization of Arabidopsis thaliana transthyretin-like protein. BMC Plant Biol.10:30. 10.1186/1471-2229-10-30

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 122

  PiiY.CescoS.MimmoT. (2015). Shoot ionome to predict the synergism and antagonism between nutrients as affected by substrate and physiological status. Plant Physiol. Biochem.94, 48–56. 10.1016/j.plaphy.2015.05.002

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 123

  PilbeamD. J.DrihemK. (2007). Vanadium, in Handbook of Plant Nutrition, eds BarkerA. V.PilbeamD. J. (Boca Raton, FL: CRC Press), 585–596.

  • Google Scholar

• 124

  Porras-AlfaroA.BaymanP. (2011). Hidden fungi, emergent properties: endophytes and microbiomes. Annu. Rev. Phytopathol.49, 291–315. 10.1146/annurev-phyto-080508-081831

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 125

  PowellA. A.CorbineauF.Franca-NetoJ.LéchappéJ.MesterhazyA.NoliE.et al. (2005). Towards the future in seed production, evaluation and improvement. Seed Sci. Technol.33, 265–281. 10.15258/sst.2005.33.2.01

  • CrossRef
  • Google Scholar

• 126

  PrasadA. S. (2013). Discovery of human zinc deficiency: its impact on human health and disease. Adv. Nutr.4, 176–190. 10.3945/an.112.003210

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 127

  RanaA.KabiS. R.VermaS.AdakA.PalM.ShivayY. S.et al. (2015). Prospecting plant growth promoting bacteria and cyanobacteria as options for enrichment of macro- and micronutrients in grains in rice–wheat cropping sequence. Cogent Food Agric.1, 1–16. 10.1080/23311932.2015.1037379

  • CrossRef
  • Google Scholar

• 128

  RedekerK. R.AndrewsJ.FisherF.SassR.CiceroneR. J. (2002). Interfield and intrafield variability of methyl halide emissions from rice paddies. Global Biogeochem. Cycles16, 72-1–72-9. 10.1029/2002GB001874

  • CrossRef
  • Google Scholar

• 129

  RedekerK. R.ManleyS. L.WalserM.CiceroneR. J. (2004). Physiological and biochemical controls over methyl halide emissions from rice plants. Global Biogeochem. Cycles18, 1–14. 10.1029/2003gb002042

  • CrossRef
  • Google Scholar

• 130

  ReillerP.Mercier-BionF.GimenezN.BarréN.MiserqueF. (2006). Iodination of humic acid samples from different origins. Radiochim. Acta94, 739–745. 10.1524/ract.2006.94.9-11.739

  • CrossRef
  • Google Scholar

• 131

  RenQ.FanJ.ZhangZ.ZhengX.DelongG. R. (2008). An environmental approach to correcting iodine deficiency: supplementing iodine in soil by iodination of irrigation water in remote areas. J. Trace Elem. Med. Biol.22, 1–8. 10.1016/j.jtemb.2007.09.003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 132

  RobertsS. K. (2006). Plasma membrane anion channels in higher plants and their putative functions in roots. New Phytol.169, 647–666. 10.1111/j.1469-8137.2006.01639.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 133

  RoseN. R.BonitaR.BurekC. L. (2002). Iodine: an environmental trigger of thyroiditis. Autoimmun. Rev.1, 97–103. 10.1016/S1568-9972(01)00016-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 134

  RuniaW. T. H. (1995). A review of possibilities for disinfection of recirculation water from soilless cultures. Acta Hortic.382, 221–229. 10.17660/ActaHortic.1995.382.25

  • CrossRef
  • Google Scholar

• 135

  SainiH. S.AttiehJ. M.HansonA. D. (1995). Biosynthesis of halomethanes and methanethiol by higher plants via a novel methyltransferase reaction. Plant Cell Environ.18, 1027–1033. 10.1111/j.1365-3040.1995.tb00613.x

  • CrossRef
  • Google Scholar

• 136

  SaundersR. W.KumarR.MacDonaldS. M.PlaneJ. M. C. (2012). Insights into the photochemical transformation of iodine in aqueous systems: humic acid photosensitized reduction of iodate. Environ. Sci. Technol.46, 11854–11861. 10.1021/es3030935

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 137

  SaundersR. W.PlaneJ. M. C. (2005). Formation pathways and composition of iodine oxide ultra-fine particles. Environ. Chem.2, 299–303. 10.1071/EN05079

  • CrossRef
  • Google Scholar

• 138

  SchlorkeD.FlemmigJ.BirkemeyerC.ArnholdJ. (2016). Formation of cyanogen iodide by lactoperoxidase. J. Inorg. Biochem.154, 35–41. 10.1016/j.jinorgbio.2015.11.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 139

  SekiM.OikawaJ.TaguchiT.OhnukiT.MuramatsuY.SakamotoK.et al. (2013). Laccase-catalyzed oxidation of iodide and formation of organically bound iodine in soils. Environ. Sci. Technol.47, 390–397. 10.1021/es303228n

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 140

  ShabalaS. (2013). Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann. Bot.112, 1209–1221. 10.1093/aob/mct205

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 141

  ShawG.ScottL. K.KinnersleyR. P. (2007). Sorption of caesium, iodine and sulphur in solution to the adaxial leaf surface of broad bean (Vicia faba L.). Environ. Exp. Bot.59, 361–370. 10.1016/j.envexpbot.2006.04.008

  • CrossRef
  • Google Scholar

• 142

  SheppardM. I.ThibaultD. H. (1992). Chemical behaviour of iodine in organic and mineral soils. Appl. Geochem.7, 265–272. 10.1016/0883-2927(92)90042-2

  • CrossRef
  • Google Scholar

• 143

  SheppardM. I.ThibaultD. H.SmithP. A.HawkinsJ. L. (1994). Volatilization: a soil degassing coefficient for iodine. J. Environ. Radioact.25, 189–203. 10.1016/0265-931X(94)90072-8

  • CrossRef
  • Google Scholar

• 144

  ShetayaW. H.YoungS. D.WattsM. J.AnderE. L.BaileyE. H. (2012). Iodine dynamics in soils. Geochim. Cosmochim. Acta77, 457–473. 10.1016/j.gca.2011.10.034

  • CrossRef
  • Google Scholar

• 145

  ShimamotoY. S.TakahashiY.TeradaY. (2011). Formation of organic iodine supplied as iodide in a soil-water system in Chiba, Japan. Environ. Sci. Technol.45, 2086–2092. 10.1021/es1032162

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 146

  ShinonagaT.GerzabekM.StreblF.MuramatsuY. (2001). Transfer of iodine from soil to cereal grains in agricultural areas of Austria. Sci. Total Environ.267, 33–40. 10.1016/S0048-9697(00)00764-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 147

  ShiroyamaK.KawasakiY.UnnoY.AmachiS. (2015). A putative multicopper oxidase, IoxA, is involved in iodide oxidation by Roseovarius sp. strain A-2. Biosci. Biotechnol. Biochem.79, 1898–905. 10.1080/09168451.2015.1052767

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 148

  Silva-MorenoE.Brito-EcheverríaJ.LópezM.RíosJ.BalicI.Campos-VargasR.et al. (2016). Effect of cuticular waxes compounds from table grapes on growth, germination and gene expression in Botrytis cinerea. World J. Microbiol. Biotechnol.32, 74. 10.1007/s11274-016-2041-4

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 149

  SinghA. K.SinghA.SinghA. K.ShamimM.VikramP.SinghS.et al. (2012). Application of potassium iodide as a new agent for screening of drought tolerance upland rice genotypes at flowering stage. Plant Knowl. J.1, 25–32. Available online at: https://search.informit.com.au/documentSummary;dn=939538551491567;res=IELENG

  • Google Scholar

• 150

  SmoleńS.KowalskaI.SadyW. (2014a). Assessment of biofortification with iodine and selenium of lettuce cultivated in the NFT hydroponic system. Sci. Hortic.166, 9–16. 10.1016/j.scienta.2013.11.011

  • CrossRef
  • Google Scholar

• 151

  SmoleńS.Ledwożyw-SmoleńI.SadyW. (2015a). The role of exogenous humic and fulvic acids in iodine biofortification in spinach (Spinacia oleracea L.). Plant Soil1–15. 10.1007/s11104-015-2785-x

  • CrossRef
  • Google Scholar

• 152

  SmoleńS.RozekR.Ledwozyw-SmolenI.StrzetelskiP. (2011). Preliminary evaluation of the nfluence of soil fertilization and foliar nutrition with iodine on the efficiency of iodine biofortification and chemical composition of lettuce. J. Elem.16, 613–622. 10.5601/jelem.2011.16.4.10

  • CrossRef
  • Google Scholar

• 153

  SmoleńS.SadyW. (2012). Influence of iodine form and application method on the effectiveness of iodine biofortification, nitrogen metabolism as well as the content of mineral nutrients and heavy metals in spinach plants (Spinacia oleracea L.). Sci. Hortic.143, 176–183. 10.1016/j.scienta.2012.06.006

  • CrossRef
  • Google Scholar

• 154

  SmoleńS.SadyW.Ledwożyw-SmoleńI.StrzetelskiP.Liszka-SkoczylasM.RożekS. (2014b). Quality of fresh and stored carrots depending on iodine and nitrogen fertilization. Food Chem.159, 316–322. 10.1016/j.foodchem.2014.03.024

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 155

  SmoleńS.SkoczylasŁ.RakoczyR.Ledwożyw-SmolenI.KopecA.PiatkowskaE.et al. (2015b). Mineral composition of field-grown lettuce (Lactuca sativa L.) depending on the diversified fertilization with iodine and selenium compounds. Acta Sci. Pol. Hortorum Cultus14, 97–114. Available online at: http://www.acta.media.pl/pl/full/7/2015/000070201500014000060009700114.pdf

  • Google Scholar

• 156

  SmoleńS.WierzbińskaJ.SadyW.KołtonA.WiszniewskaA.Liszka-SkoczylasM. (2015c). Iodine biofortification with additional application of salicylic acid affects yield and selected parameters of chemical composition of tomato fruits (Solanum lycopersicum L.). Sci. Hortic.188, 89–96. 10.1016/j.scienta.2015.03.023

  • CrossRef
  • Google Scholar

• 157

  StavberS.JerebM.ZupanM. (2008). Electrophilic iodination of organic compounds using elemental iodine or iodides. Synthesis2008, 1487–1513. 10.1055/s-2008-1067037

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 158

  SteinbergS.KimbleG.SchmettG.EmersonD.TurnerM.RudinM. (2008). Abiotic reaction of iodate with sphagnum peat and other natural organic matter. J. Radioanal. Nucl. Chem.277, 185–191. 10.1007/s10967-008-0728-1

  • CrossRef
  • Google Scholar

• 159

  SteinnesE. (2009). Soils and geomedicine. Environ. Geochem. Health31, 523–535. 10.1007/s10653-009-9257-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 160

  StewartA. G.CarterJ.ParkerA.AllowayB. J. (2003). The illusion of environmental iodine deficiency. Environ. Geochem. Health25, 165–170. 10.1023/A:1021281822514

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 161

  StrzetelskiP.SmoleńS.RozekS.SadyW. (2010). The effect of diverse iodine fertilization on nitrate accumulation and content of selected compounds in radish plants (Raphanus sativus L.). Acta Sci. Pol. Hortorum Cultus9, 65–73. Available online at: https://www.infona.pl/resource/bwmeta1.element.dl-catalog-15502fac-cba9-4081-b367-847faf1bc05f

  • Google Scholar

• 162

  SunW. Q.LeopoldA. C. (1995). The Maillard reaction and oxidative stress during aging of soybean seeds. Physiol. Plant.94, 94–104. 10.1111/j.1399-3054.1995.tb00789.x

  • CrossRef
  • Google Scholar

• 163

  SuzukiM.EdaY.OhsawaS.KanesakiY.YoshikawaH.TanakaK.et al. (2012). Iodide oxidation by a novel multicopper oxidase from the alphaproteobacterium strain Q-1. Appl. Environ. Microbiol.78, 3941–3949. 10.1128/AEM.00084-12

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 164

  TakekawaY.NakamuraT. (2012). Rice OsHOL1 and OsHOL2 proteins have S-adenosyl-L-methionine-dependent methyltransferase activities toward iodide ions. Plant Biotechnol.29, 103–108. 10.5511/plantbiotechnology.12.0207a

  • CrossRef
  • Google Scholar

• 165

  TerzanoR.CescoS.MimmoT. (2015). Dynamics, thermodynamics and kinetics of exudates: crucial issues in understanding rhizosphere processes. Plant Soil386, 399–406. 10.1007/s11104-014-2308-1

  • CrossRef
  • Google Scholar

• 166

  TschierschJ.ShinonagaT.HeubergerH. (2009). Dry deposition of gaseous radioiodine and particulate radiocaesium onto leafy vegetables. Sci. Total Environ.407, 5685–5693. 10.1016/j.scitotenv.2009.06.025

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 167

  TsukadaH.TakedaA.TagamiK.UchidaS. (2008). Uptake and distribution of iodine in rice plants. J. Environ. Qual.37, 2243–2247. 10.2134/jeq2008.0010

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 168

  UjowunduC.UkohaA.AghaC.NwachukwuN.IgweK.KaluF. (2010). Effects of potassium iodate application on the biomass and iodine concentration of selected indigenous nigerian vegetables. Afr. J. Biotechnol.9, 7141–7147. 10.4314/ajb.v9i42

  • CrossRef
  • Google Scholar

• 169

  UmalyR. C.PoelL. W. (1971). Effects of lodine in various formulations on the growth of barley and pea plants in nutrient solution culture. Ann. Bot.35, 127–131.

  • Google Scholar

• 170

  VenturiS. (2011). Evolutionary significance of iodine. Curr. Chem. Biol.5, 155–162. 10.2174/2212796811105030155

  • CrossRef
  • Google Scholar

• 171

  VinogradovA. P.LappM. A. (1971). Use of iodine haloes to search for concealed mineralisation. Vestn. -Lemngradskii Univ. Seriia Geol. Geogr.24, 70–76.

  • Google Scholar

• 172

  VoughtR. L.BrownF. A.LondonW. T. (1970). Iodine in the environment. Arch. Environ. Heal. An Int. J.20, 516–522. 10.1080/00039896.1970.10665632

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 173

  VoogtW.HolwerdaH. T.KhodabaksR. (2010). Biofortification of lettuce (Lactuca sativa L.) with iodine: the effect of iodine form and concentration in the nutrient solution on growth, development and iodine uptake of lettuce grown in water culture. J. Sci. Food Agric.90, 906–913. 10.1002/jsfa.3902

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 174

  VoogtW.JacksonW. A. (2010). Perchlorate, nitrate, and iodine uptake and distribution in lettuce (Lactuca sativa L.) and potential impact on background levels in humans. J. Agric. Food Chem.58, 12192–12198. 10.1021/jf101227d

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 175

  WattsM. J.O'ReillyJ.MaricelliA.ColemanA.AnderE. L.WardN. I. (2010). A snapshot of environmental iodine and selenium in La Pampa and San Juan provinces of Argentina. J. Geochem. Explor.107, 87–93. 10.1016/j.gexplo.2009.11.002

  • CrossRef
  • Google Scholar

• 176

  WegnerL. H. (2014). Root pressure and beyond: energetically uphill water transport into xylem vessels?J. Exp. Bot.65, 381–393. 10.1093/jxb/ert391

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 177

  WengH.HongC.XiaT.BaoL.LiuH.LiD. (2013). Iodine biofortification of vegetable plants—An innovative method for iodine supplementation. Chin. Sci. Bull.58, 2066–2072. 10.1007/s11434-013-5709-2

  • CrossRef
  • Google Scholar

• 178

  WengH.-X.HongC.-L.YanA.-L.PanL.-H.QinY.-C.BaoL.-T.et al. (2008a). Mechanism of iodine uptake by cabbage: effects of iodine species and where it is stored. Biol. Trace Elem. Res.125, 59–71. 10.1007/s12011-008-8155-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 179

  WengH.-X.LiuH.-P.LiD.-W.YeM.PanL.XiaT.-H. (2014). An innovative approach for iodine supplementation using iodine-rich phytogenic food. Environ. Geochem. Health36, 815–828. 10.1007/s10653-014-9597-4

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 180

  WengH.-X.WengJ.-K.YanA.-L.HongC.-L.YongW.-B.QinY.-C. (2008b). Increment of iodine content in vegetable plants by applying iodized fertilizer and the residual characteristics of iodine in soil. Biol. Trace Elem. Res.123, 218–228. 10.1007/s12011-008-8094-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 181

  WengH.-X.WengJ.-K.YongW.-B.SunX.-W.ZhongH. (2003). Capacity and degree of iodine absorbed and enriched by vegetable from soil. J. Environ. Sci. (China)15, 107–111.

  • Pubmed Abstract
  • Google Scholar

• 182

  WengH.-X.YanA.-L.HongC.-L.XieL.-L.QinY.-C.ChengC. Q. (2008c). Uptake of different species of iodine by water spinach and its effect to growth. Biol. Trace Elem. Res.124, 184–194. 10.1007/s12011-008-8137-4

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 183

  WeverR. (2012). Structure and function of vanadium haloperoxidases, in Vanadium: Biochemical and Molecular Biological Approaches, ed MichibataH. (Dordrecht: Springer), 97–125.

  • Google Scholar

• 184

  WhiteP. J.BroadleyM. R. (2009). Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol.182, 49–84. 10.1111/j.1469-8137.2008.02738.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 185

  WhiteheadD. C. (1973). Uptake and distribution of iodine in grass and clover plants grown in solution culture. J. Sci. Food Agric.24, 43–50. 10.1002/jsfa.2740240108

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 186

  WhiteheadD. C. (1974). The influence of organic matter, chalk, and sesquioxides on the solubility of iodide, elemental iodine, and iodate incubated with soil. J. Soil Sci.25, 461–470. 10.1111/j.1365-2389.1974.tb01141.x

  • CrossRef
  • Google Scholar

• 187

  WhiteheadD. C. (1978). Iodine in soil profiles in relation to iron and aluminium oxides and organic matter. J. Soil Sci.29, 88–94. 10.1111/j.1365-2389.1978.tb02035.x

  • CrossRef
  • Google Scholar

• 188

  WhiteheadD. C. (1979). Iodine in the U.K. environment with particular reference to agriculture. J. Appl. Ecol.16, 269–279. 10.2307/2402746

  • CrossRef
  • Google Scholar

• 189

  WhiteheadD. C. (1984). The distribution and transformations of iodine in the environment. Environ. Int.10, 321–339. 10.1016/0160-4120(84)90139-9

  • CrossRef
  • Google Scholar

• 190

  World Health Organization (2007). Assessment of the Iodine Deficiency Disorders and Monitoring their Elimination. A Guide for Programme Managers. Geneva.

  • Google Scholar

• 191

  XiaY.GaoQ.-M.YuK.LapchykL.NavarreD.HildebrandD.et al. (2009). An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. Cell Host Microbe5, 151–165. 10.1016/j.chom.2009.01.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 192

  XuF. (1996). Catalysis of novel enzymatic iodide oxidation by fungal laccase. Appl. Biochem. Biotechnol.59, 221–230. 10.1007/BF02783566

  • CrossRef
  • Google Scholar

• 193

  YamaguchiN.NakanoM.TakamatsuR.TanidaH. (2010). Inorganic iodine incorporation into soil organic matter: evidence from iodine K-edge X-ray absorption near-edge structure. J. Environ. Radioact.101, 451–457. 10.1016/j.jenvrad.2008.06.003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 194

  YoshidaS.MuramatsuY.UchidaS. (1992). Studies on the sorption of I- (iodide) and IO3- (iodate) onto Andosols. Water Air Soil Pollut.63, 321–329. 10.1007/BF00475499

  • CrossRef
  • Google Scholar

• 195

  YuZ.WarnerJ. A.DahlgrenR. A.CaseyW. H. (1996). Reactivity of iodide in volcanic soils and noncrystalline soil constituents. Geochim. Cosmochim. Acta60, 4945–4956. 10.1016/S0016-7037(96)00305-5

  • CrossRef
  • Google Scholar

• 196

  YuitaK. (1994). Overview and dynamics of iodine and bromine in the environment, 2: iodine and bromine toxicity and environmental hazards. JARQ28, 100–111.

  • Google Scholar

• 197

  ZhuY.-G.HuangY.-Z.HuY.LiuY.-X. (2003). Iodine uptake by spinach (Spinacia oleracea L.) plants grown in solution culture: effects of iodine species and solution concentrations. Environ. Int.29, 33–37. 10.1016/S0160-4120(02)00129-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 198

  ZiaM. H.WattsM. J.GardnerA.CheneryS. R. (2015). Iodine status of soils, grain crops, and irrigation waters in Pakistan. Environ. Earth Sci.73, 7995–8008. 10.1007/s12665-014-3952-8

  • CrossRef
  • Google Scholar

• 199

  ZifarelliG.PuschM. (2010). CLC transport proteins in plants. FEBS Lett.584, 2122–2127. 10.1016/j.febslet.2009.12.042

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 200

  ZimmermannM. B. (2009). Iodine deficiency in pregnancy and the effects of maternal iodine supplementation on the offspring: a review. Am. J. Clin. Nutr.89, 668S–672S. 10.3945/ajcn.2008.26811c

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 201

  ZimmermannM. B.JoosteP. L.PandavC. S. (2008). Iodine-deficiency disorders. Lancet372, 1251–1262. 10.1016/S0140-6736(08)61005-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar