Biofortification of green bean (Phaseolus vulgaris L.) and lettuce (Lactuca sativa L.) with iodine in a plant-calcareous sandy soil system irrigated with water containing KI

Highlights

• The plant growth was stimulated at iodine concentration of 0.10 and 0.25 mg/L

• Iodine in concentration of 0.50 mg/L hampered the growth of bean and lettuce plants

• Iodine concentration changed in the order of root > leaves > stem > pods

• Maximum concentration of I in edible parts were 1.8 (bean) and 5.6 (lettuce) mg/kg

• Essential element transport in lettuce was stimulated at all iodine concentrations

Abstract

Uptake and translocation of iodine by green bean (Phaseolus vulgaris L.) and lettuce (Lactuca sativa L.) were investigated in a calcareous sandy soil-plant system. These plants were cultivated in calcareous sandy soil in presence of irrigation water with the iodine concentrations of 0.10, 0.25 and 0.50 mg/L. The growth of these plants was stimulated at the two lower iodine concentrations of 0.10 and 0.25 mg/L, but hampered at 0.50 mg/L. In lettuce the highest iodine dosage resulted in smaller leaf surface and higher number of leaves, nearly with the same biomass production. In the edible parts of green bean and lettuce plants irrigated with 0.25 mg/L iodine containing water, the iodine concentration levels amounted to 0.6 and 5.2 mg/kg dry weight (DW), respectively. In lettuce, the uptake and translocation of selected essential elements (P, Mg, Mn, Fe, Cu, Zn, B) were also stimulated (20-260%) by iodine treatment; however, in fresh bean pods this phenomenon was negligible. Considering the iodine level and moisture content of the fresh lettuce leaves and fresh bean pods, the consumption of 100 g fresh vegetable covers about 66%, 3% of the recommended dietary allowance (150 μg).

Introduction

Iodine is an essential component of the thyroid hormones, which regulate many metabolic processes and play a dominant role in the early growth and development of most organs, especially the brain (Fuge and Johnson, 2015). Consequently, if iodine deficiency is severe enough to affect thyroid hormone synthesis it can result in hypothyroidism and brain damage (Andersson et al. 2007; Denage et al., 2002). The WHO recommended daily iodine intake for the age groups: 0-5 years, 6-12 years, and 13 and above years, is 90 μg, 120 μg and 150 μg, respectively, while in case of pregnant and lactating women it is 250 μg (WHO 2004). In some countries iodine intake is insufficient, while in other countries like in the USA and Canada the intake generally exceeds the recommended value (Zimmermann & Boelaert 2015). Iodine is not an essential element for terrestrial plants, and its concentration in typical land plants and food crops amounts to only 0.07-10 mg/kg (Robertson et al. 2003). The main intervention strategy for iodine deficiency monitoring and prevention is “universal” salt iodization (Andersson et al. 2007). It implies that all salt products intended for human consumption, including that used in processed foods, and for animal feeding, are iodized. Iodine can be added to table salt as potassium iodide, potassium iodate or sodium iodide. Potassium salts are the most frequently used compounds, and iodate is more preferred due to its higher stability and lower solubility than that of iodide. The iodized table salt as a simple prophylaxis tool has been successfully introduced in several countries in spite of possible iodine losses during transportation, storage or cooking itself (Kapusta-Duch et al. 2017; Rana & Raghuvanshi 2013) Another possibility to eliminate the iodine deficiency is the consumption of iodized oils, like the most commonly used Lipiodol, a poppy seed oil containing 40% iodine per weight (Azizi 2007; Wolff 2001). In addition to these relatively efficient and extensively applied methods, many different experiments have been carried out in various countries e.g., production of bread fortified with iodine, application of iodized drinking water or iodized sugar (Andersson et al. 2007). However, the efficiency and applicability of these experiments are not comparable with that of the iodized table salts. Indirect iodization of food materials has been receiving widespread attention due to adoption of new policies by many countries to reduce the salt consumption to 5 g/day, so as to tackle hypertension and cardiovascular diseases. One way of achieving adequate iodization is through iodine fortification of animal fodder and food derived from animal sources. The alternative way is through iodine fortification of edible plants by application of irrigation water containing iodine.

On basis of literature studies the agronomic biofortification of crops with iodine appears to be a promising way to increase the iodine intake of the population (Azizi 2007). Approximately 80% of the iodine in the human body and animals originates from plants, and nearly 99% of this iodine is bioavailable and can be easily assimilated (Gonzali et al. 2017). Therefore, plant-based foods with increased iodine content offer an attractive and cost-effective approach to reduce iodine deficiency.

Recently, hydroponic (Kato et al. 2013; Landini et al. 2011; Li et al. 2016; Voogt et al. 2010; Weng et al., 2008a, 2008b, 2008c; Zhu et al. 2003; Zhu et al. 2004) pot (Blasco et al. 2008; Blasco et al. 2012; Caffagni et al. 2011; Dai et al. 2006; Hong et al. 2008; Hong et al., 2009a, 2009b; Voogt et al. 2014; Weng et al., 2008a, 2008b, 2008c) and field (Lawson et al. 2015; Smoleń et al. 2011) experiments have been carried out to produce iodine-enriched crops, by applying iodine containing nutrient solutions or irrigation water, as well as solid fertilizers (e.g. algal-based). In addition to the iodine dosage, the chemical forms of iodine (iodide or iodate) were also investigated. For these experiments, different vegetables were selected such as lettuce, Lactuca sativa L.(Blasco et al. 2008; Blasco et al. 2012; Hong et al. 2008; Lawson et al. 2015; Voogt et al. 2010); spinach, Spinacia oleracea L. (Dai et al. 2006; Weng et al., 2008a, 2008b, 2008c; Zhu et al. 2003; Zhu et al. 2004); pakchoi, Brassica chinensis L. (Hong et al., 2009a, 2009b); cabbage, B. oleracea var. capitata (Weng et al., 2008a, 2008b, 2008c); Chinese cabbage, B. chinesis L. (Hong et al. 2008); tomato, Solanum lycopersicum L. (Caffagni et al. 2011; Hong et al. 2008; Landini et al. 2011); strawberry, Fragaria ananassa (Li et al. 2016); pepper, Capsicum annuum L. (Hong et al., 2009a, 2009b); cucumber, Cucumis sativus L. (Voogt et al. 2014); carrot, Daucus carota L.var. sativus (Hong et al. 2008); celery, Apium graveolens L. var. dulce (Mill.) DC. (Hong et al., 2009a, 2009b); radish, Raphanus sativus L. (Hong et al., 2009a, 2009b; Lawson et al. 2015); potato, Solanum tuberosum L. (Caffagni et al. 2011); rice, Oryza sativa L. (Kato et al. 2013); barley, Hordeum vulgare L. wheat, Triticum aestivum L.; ryegrass, Lolium perenne L.; buckwheat, Fagopyrum esculentum; flax, Linum usitatissimum L.; tobacco, Nicotiana tabacum L. (Hong et al. 2007, Hong et al., 2009a, 2009b; Umaly & Poel 1971; Xie et al. 2007; Yu et al. 2011). All research groups determined the concentration of iodine in different plant parts, however, only a few of them studied the effect of iodine on the accumulation of macro- and micro elements (Smoleń et al. 2011; Smoleń and Sady, 2012; Smoleń et al. 2014; Krzepiłko et al. 2016).

On basis of literature related to biofortification of different plants with iodine the following observations were made:

• Low concentration of iodine has been found to enhance plant growth in plants like barley, ryegrass, tomato, buckwheat, flax, strawberry, tobacco (Hong et al. 2007; Hong et al., 2009a, 2009b; Umaly & Poel 1971; Xie et al. 2007; Yu et al. 2011). However, over a certain threshold concentration (e.g. 25 mg/kg and 1 mg/L in case of fertilizer and hydroponic technology, respectively), iodine becomes toxic, resulting in negative biomass production (Hong et al., 2009a, 2009b; Weng et al., 2008a, 2008b, 2008c).

• Iodide is more detrimental to plant growth as compared to iodate due to higher uptake (Blasco et al. 2008).

• Iodine concentration decreased along the uptake pathway, with roots having the maximum concentration and fruits or leaves having the minimum concentration. Iodine transport occurs mainly through the xylem (Hong et al., 2009a, 2009b; Li et al. 2016; Weng et al., 2008a, 2008b, 2008c), but phloem transport was also observed in lettuce and tomato (Landini et al. 2011; Smoleń et al. 2014).

• Leafy vegetables like lettuce (Blasco et al. 2008; Blasco et al. 2012; Hong et al. 2008; Lawson et al. 2015; Voogt et al. 2010), spinach (Dai et al. 2006; Weng et al., 2008a, 2008b, 2008c; Zhu et al. 2003; Zhu et al. 2004), and Chinese cabbage (Hong et al. 2008) have high translocation rates due to their larger leaf surface area and thus accumulate high amounts of iodine in the leaves. This makes them ideal candidates for biofortification with iodine. However, some fruits (strawberry, tomato) and tuber vegetables (potato) can also store high amount of iodine (Caffagni et al. 2011; Landini et al. 2011; Li et al. 2016).

• Iodine at a concentration range of 0.05-1.0 mg/L was found to have a minimal effect on the macro- and micro-elements concentration in spinach and lettuce (Smoleń and Sady, 2012; Smoleń et al. 2014; Krzepiłko et al. 2016).

We studied the uptake and translocation of iodine in a leafy vegetable, lettuce and a fruit vegetable, green bean in a pot-soil system with calcareous sandy soil. Irrigation water containing KI at concentration of 0.10, 0.25 and 0.50 mg/L was added to the soil. The iodine concentration of different plant parts and the iodine distribution within the plants was investigated by inductively coupled plasma mass spectrometer (ICP-MS) following their microwave-assisted (MW) acid digestion. In addition to these measurements, the effect of iodine on plant growth, morphological and anatomical features of plants, as well as the uptake and translocation of selected essential elements (P, Mg, K, Fe, Mn, Cu, Zn, B) was also studied.