Zinc in soils, water and food crops

Accepted Manuscript Title: Zinc in soils, water and food crops Authors: Christos Noulas, Miltiadis Tziouvalekas, Theodore Karyotis PII: DOI: Reference:

S0946-672X(17)30838-6 https://doi.org/10.1016/j.jtemb.2018.02.009 JTEMB 26058

To appear in: Received date: Revised date: Accepted date:

18-10-2017 8-2-2018 8-2-2018

Please cite this article as: Noulas Christos, Tziouvalekas Miltiadis, Karyotis Theodore.Zinc in soils, water and food crops.Journal of Trace Elements in Medicine and Biology https://doi.org/10.1016/j.jtemb.2018.02.009 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Zinc in soils, water and food crops

Short/alternative title: Zn in the soil-water-plant-continuum

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Christos Noulas*, Miltiadis Tziouvalekas and Theodore Karyotis

Hellenic Agricultural Organization ‘DEMETER’. Agricultural Research General Directorate

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(N.AG.RE.F.). Institute of Industrial and Forage Crops, Department of Soil and Water Resources. Address: 1, Theophrastou Str., 41335, Larissa, Greece.

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*

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Correspoding Author: Christos Noulas

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E mail address: [email protected] (Christos Noulas) Tel: +30 2410 671 296. Fax

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+30 2410 671 321.

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Highlights:

Zinc deficiency in soil-crop systems in widespread globally.

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Zinc deficiency is common on calcareous, high pH, eroded and land-levelled soils.

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Zn in water enters from natural processes and human activities.

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Zn plays a vital role in several plant physiological functions.

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Biofortification of food crops may be an effective method for improving Zn intake in

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susceptible human populations.

Contents ABSTRACT 1. Introduction

1.1.1.

Zn content in European soils

1.1.2.

Soil conditions for Zn deficiency

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1.1. Zinc in the soil system

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1.2. Zinc in water 1.3. Zinc in food crops Zinc content in crops

1.3.2.

Biofortification with Zn and health effects

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1.3.1.

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Conclusions

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Conflict of interest

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Acknowledgements

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References

ABSTRACT

A basic knowledge of the dynamics of zinc (Zn) in soils, water and plants are important steps in achieving sustainable solutions to the problem of Zn deficiency in crops and humans. This paper aims at reviewing and discussing the relevant aspects of the role of Zn in

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the soil–water–plant agro biological system: from the origins of Zn in soils and water to soil

Zn deficiency distribution and the factors affecting soil Zn availability to plants, therefore to

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elucidate the strategies potentially help combating Zn deficiency problems in soil-planthuman continuum. This necessitates identifying the main areas of Zn-deficient soils and food

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crops and treating them with Zn amendments, mainly fertilizers in order to increase Zn

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uptake and Zn use efficiency to crops. In surface and groundwater, Zn enters the

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environment from various sources but predominately from the erosion of soil particles

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containing Zn. In plants is involved in several key physiological functions (membrane structure, photosynthesis, protein synthesis, and drought and disease tolerance) and is

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required in small but nevertheless critical contents. Several high revenue food crops such as beans, citrus, corn, rice etc are highly susceptible to Zn deficiency and biofortification is

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considered as a promising method to accumulate high content of Zn especially in grains. With the world population continuing to rise and the problems of producing extra food rich

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in Zn to provide an adequate standard of nutrition to increase, it is very important that any

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losses in production easily corrected so as Zn deficiencies are prevented.

Abbreviations: DTPA, diethylene triamine penta-acetic acid; CEC, cation exchange capacity

Keywords: Zn content; soil; water; food crops; Zn deficiency; biofortification

1. Introduction

Zinc (Zn) plays a substantial role in many biological processes and is an essential trace element for proper growth and reproduction of plants, and health of animals and humans; it

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has also been reported to cause contamination of soil, water, and food chains [1–3]. In

human beings Zn deficiency is associated to diet quality, exacerbated by Zn-deficient soils

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[4,5]. Soils vulnerable to Zn deficiency, are sandy, calcareous, saline and wetland soils, compacted and rich in organic matter with high nitrogen and phosphate levels [2]. In unfertilized and uncontaminated soil the content of Zn ranges from 10–300 mg/kg (overall

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mean of around 50–55 mg/kg) [6–8].

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Zn is also found in surface and groundwater, and enters the environment from several

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sources including mine drainage, industrial and municipal wastes, urban runoff, and mainly

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from the erosion of soil particles containing Zn [9,10]. According to Food and Agricultural

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Organization (FAO) and to World Health Organization (WHO) drinking water containing Zn > 3 mg/L tends to be opalescent, develops a greasy film when boiled, and has an undesirable

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astringent taste [11]. The recommended maximum content in irrigation water was set at 2 mg/L, since higher contents can be toxic to many plants [12] and can pollute water aquifers

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[1].

Most plants contain 30–100 mg Zn/kg dry matter whereas; contents above 300 mg/kg are

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generally toxic. Beans, citrus, grapes, maize, rice and sorghum are considered highly susceptible to Zn deficiency crops. Since crop Zn fertilizer recovery is generally low (<1%) biofortification is considered as a promising method to accumulate high Zn concentration in grains [13,14] and alleviate serious health problems in human beings [15,16]. This paper reviews the status of Zn in the soil–water–plant agro biological system and discusses the

conditions affecting Zn availability and strategies combating Zn deficiency in the soil-planthuman continuum.

Zinc in the soil system

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1.1.

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1.1.1. Zn content in European soils

The content of Zn in natural (unfertilized and uncontaminated) soil is related to the chemical

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composition of the parent rock and the extent of weathering processes [17]. In the magmatic

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rocks it ranges from 40 to 120 mg/kg whereas in the sedimentary rocks its contents vary

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from 80–120 mg/kg in argillaceous sediments and shales to only 15–30 mg/kg in sandstones

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and 10–25 mg/kg in limestones and dolomites [18].

In agricultural soils Zn is mostly unevenly distributed and its content ranges between 10–300

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mg/kg [6,7]. The range of total Zn content in soils reported in the literature tends to show an overall mean of around 50–55 mg/kg [6,8]. Other researchers indicate that typical total Zn

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contents in uncontaminated soils vary widely and can range from 10–100 mg/kg [19]. The lowest Zn values were found in sandy soils and the highest in calcareous and organic soils

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whereas some researchers indicate a mean Zn content for worldwide soils of 64 mg/kg

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(Table 1) [18,20].

“((Place Table 1 here))”

In Europe high Zn values occur in the Canary Islands (basalt), west-central Spain, the Pyrenees, the Poitou region in France, the southern Central Massif, the east part of northern

Italy, Slovenia, Sardinia, Calabria, and Lavrion in Greece. Mean contents of Zn in soils reported for several European countries vary from 7–89 mg/kg, being the lowest for Denmark and the highest for Italy [18,21]. Other sources indicate that average natural (background) level of Zn in soils in European Union ranges between 70 and 150 mg Zn/kg soil [22]. A relatively recent map compiled by Reimann et al. [23], illustrates the Zn content

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extracted by the Aqua Regia method [24] for the surface soils used in agriculture (Figure 1).

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“((Place Figure 1 here))”

Within the framework of the GEMAS project (Geochemical Mapping of Agricultural and

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Grazing Land Soil of Europe) several trace elements (among them Zn) show relatively low

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levels over sizeable zones of land in Europe that trace element deficiency is clearly

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designated. It is important to mention that on Figure 1 the effect of diffuse contamination

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remains somehow invisible at the chosen scale (continental) and sample density. At a higher

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sampling density (i.e., at local scale), mapping is needed in order to reliably detect pollution. However, soil samples from agricultural and grazing land show practically similar

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distribution patterns over Europe and very comparable element contents. This demonstrates the robustness of the low sample density geochemical mapping approach [23].

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A survey of soils in England and Wales showed a mean Zn content of 97 mg/kg (median 82.0 mg/kg) but this included contaminated soils from various sources such as metalliferous

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mining and heavy applications of sewage sludge [25]. In France, the median Zn content in soils with different soil texture was found 17.0 mg/kg for sandy soils [26], 63.5 mg/kg for loamy soils, and 132.0 mg/kg for heavy clay soils. In addition, Kabata-Pendias [27] reported for Polish soils the following mean Zn content: sandy soils 37 mg/kg, loess 60 mg/kg and loamy 75 mg/kg. In Sweden Zn contents in agricultural soils ranges from 6 to 152 mg/kg,

with mean of 65 mg/kg [28]. For German soils, according to Gorny et al. [29] the median Zn contents were 27.3 mg/kg for sandy soils, 59.2 for silty and 76.4 mg/kg for clay soils. The above examples show clear that Zn content in soils increases with clay content. Numerous studies in Greece have paid attention on soil micronutrients and trace elements during the last decades. It was observed that mean content of plant available Zn (DTPA;

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diethylene triamine penta-acetic acid) [30] in 52 cultivated organic soils in Greece (with soil organic matter 35.5%) was 6.4 mg/kg, while the respective mean content of total Zn in these

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soils was 44.2 mg/kg [31]. Another research indicated that accumulation of heavy metals in

roadside soils around the motorway connecting Athens and Thessaloniki at distances 5-10 m,

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10-50 m and 50-100 m from the road was found to the following order: Zn>Ni>Pb>Cu>Cd

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[32].

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A Zn soil test above 1.5 mg/kg using the DTPA extraction method is sufficient for most

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crops. A research carried out in surface soils of the drained lake Askuris (Greece), showed that only 5.95% of Zn was found as plant available, namely, as potentially ready to be taken

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by plants [33].

In olive orchards, the average content of Zn in 263 soil samples was 0.7 mg/kg and can be

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assumed that 82.9% of samples were at Zn deficiency levels [34]. In sandy soils of Central Greece cultivated with asparagus, mean Zn (DTPA) content due to leaching in 13 locations

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ranged from 4.76 mg/kg to 5.20 mg/kg for the surface soil samples [35]. Range and mean of total Zn contents in surface soils of certain European countries are

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compiled in Table 2 these values may be considered as background Zn contents. The highest mean Zn values were reported for some Fluvisols (alluvial deposits), Rendzinas (shallow soils over limestones) and Solonchaks (soils with salt accumulation), whereas the lowest values were for soils on glacial till, Podzols and light organic soils.

“((Place Table 2 here))”

Nevertheless, threshold values for soils are difficult to assess because except of total content in soils the bioavailability of Zn and of other trace elements depends on many other environmental variables. Moreover, eventhough some European countries (The Netherlands,

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UK) proposed alone soil quality standards, at European Union level only background values related to the application of sewage sludge in agricultural soils have been defined (EU

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Directive 86/278/EC). Recent research concluded that eventhough the vast majority of the agricultural soils in Europe can be considered safe for food production, an estimated 6.24%

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or 137,000 km2 needs local assessment and remediation actions [58].

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1.1.2. Soil conditions for Zn deficiency

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Zn deficiency in agricultural soils is considered to be the most geographically widespread

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micronutrient deficiency constraint limiting crop production (yield losses can exceed 40%) whereas, its excess in soil may be either of geological or anthropogenic origin [2,59,60]. Zn

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deficiencies tend to occur on calcareous (high pH) soils that have been leveled by machinery means for uniform application of irrigation. This is because leveling of fields, especially in

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calcareous soils removes topsoil and organic matter rich in micronutrients [2]. Moreover, deficiencies occur in soils with a low total Zn content (i.e. sandy soils) or soils which have

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relatively high available phosphorus content [59]. However, total Zn content is not a reliable index to reflect the capacity of soil to supply Zn for plant uptake. A very small part of the total soil Zn (< 1 mg/kg) is present in the soil solution that can be up taken by crops [27]. Deficiencies can also be observed in cool and wet soils during early growing seasons if temperature is rather low. Zn deficiency problems are often severe during cool wet springs

and disappear during summer. Low temperatures cause reduced microbial decomposition of organic matter which would release Zn to the crop due to poorly developed root systems. On the other hand, increased soil temperature raises Zn supply, diffusion rate from soil colloids to plant roots and increases mineralization rates from organic matter [61]. In irrigated corn fields Zn deficiencies have been found in many countries, especially in the Mediterranean

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basin, but additional research trials are required to confirm such observations. In arid and

semi-arid regions Zn deficiency of plants may occur in the upper soil layers which are drier

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compared to deeper soil layers and prohibit Zn transport to the plant roots by diffusion [62]. In these areas the application (injection) of liquid form of Zn fertilizers to the subsoil can

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increase Zn uptake by crops more than applying granular fertilizers to the surface

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apply, it will provide returns for many years [63].

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eventhough liquid fertilizers may increase production costs. Although Zn is fairly costly to

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The main causes of Zn deficiency in crops are mainly soil-related: low Zn availability (high pH, calcareous and sodic soils), low total soil Zn content (especially in sandy, sodic, and

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calcareous soils), loss of soil organic matter, presence of nitrogen, sodium, calcium, magnesium and phosphates, restricted root exploration due to soil compaction or high water

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table and climate factors [2,5,64]. Therefore, Zn deficiency to crops can occur on a range of soil types such as highly weathered soils, calcareous high pH soils (semiarid areas), sandy

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soils, and acid-leached soils with low total Zn content [65,66]. Deficiencies can also be related to soil parent material heredity as found in Northern Greece, where Zn deficiency

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was recorded in 92.8% of the studied acidic soils [67]. Plant available Zn in Crete island, Greece (n=80) ranged between 0.2 and 12.3 mg/kg due to differences of soil parent materials and farming practices [68]. It was recorded that maize is the most susceptible cereal crop, but wheat grown on calcareous soils and rice grown on flooded soils are also sensitive to Zn deficiency [69].

The relative sensitivity of various crops to Zn deficiency is compiled in Table 3. Common beans, deciduous fruit trees, grapes, hops, maize and onions, and are among the most sensitive crops to low levels of Zn [70].

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“((Place Table 3 here))”

Alkaline-calcareous soils represent an important type of agricultural soil in many countries

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with Mediterranean climates and are commonly utilized for the production of cereals. The prevention of Zn deficiency in cereals and other food crops may be alleviated by using the

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biofortification practice which is discussed later in this paper and the efficient use of Zn

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fertilizers. Zn deficiency has increased with the introduction of high yielding modern

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varieties, crop intensification and increased Zn removal [74,75].

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Zn exists in five distinct pools in soils such as water soluble, exchangeable, adsorbed, chelated or complexes of Zn. These forms differ in strength and therefore in their

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susceptibility to plant uptake, and leaching. The equilibrium among different forms is influenced by pH, concentration of Zn and other metals, particularly iron and manganese

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[76]. Adsorption mechanisms play a very important role in the soil-plant relationships of Zn by controlling its content in the soil solution. Hence, Zn is immediately available to plant

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roots, and also the amounts of labile forms can be desorbed and become available to crops.

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Adsorption of exchangeable Zn cations in soils can be described by the simple form as:

Zn2+ + M-Soil ⇆ Zn-Soil + M2+

Where M is any other divalent cation. Cation exchange, specific adsorption, binding to organic matter, chemisorption and precipitation are the mechanisms involved in the

adsorption of ions on solid surfaces (i.e. clay minerals, iron and manganese hydrous oxides, and humic organic matter) [2]. Zn as an essential micronutrient for plant growth plays an important role in the catalytic part of several enzymes [77]. In plants, enzymes either containing or activated by Zn are involved in carbohydrate metabolism, protein synthesis, maintenance of the integrity of cellular

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membranes, regulation of auxin synthesis and pollen formation. Many researchers observed

that Zn is closely related to the nitrogen metabolism pathway of plants, thus causing a

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reduction in protein synthesis for Zn deficient plants [77, 78]. Zinc deficiency significantly affects the root system including root development and therefore the absorption of water and

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plant available nutrients from soil. In agricultural soils Zn is bound to the soil complex (clay,

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organic material, etc.) depending on various physicochemical soil factors mainly pH and

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organic matter content. These factors determine the solubility of Zn contained in soil, and

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consequently, its bioavailability for uptake by plants. [78]. In acidic soils, a DTPA-extractable Zn content above 10 mg/kg is considered potentially

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harmful. As discussed earlier ‘total Zn’ content s in soils, usually fall in the range 10-300 mg/kg, with contents above 150 mg/kg regarded as high [79], and likely to result in reduced

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plant growth. Soil quality guidelines for national/regional jurisdictions vary in their consideration of bioavailability and application to different land uses. The European Union

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comprehensively considers geochemical properties, primarily soil pH and CEC, when interpreting data for providing Zn guidelines. Formerly, it was found that among other trace

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elements (Cd, Cu, Hg, Pb) Zn content in soils was well correlated (r=0.7) to agricultural activities and moderately correlated (r=0.41) to quaternary limestones, where most of the agricultural areas in Central Europe are located. The study concluded that fertilizers, manure and agrochemicals as well as the approximate distance to urban and industrial areas are important sources of these elements in European soils [80].

The LUCAS Topsoil Survey, (the survey used standard sampling and analytical procedures and the analysis of all soil samples carried out in a single laboratory, [81]) revealed that excess Zn appears in agricultural soils in more than 20 % of the NUTS regions in Europe (Classification of Territorial Units for Statistics in the European Union) by showing content s above the threshold value. However, the number of the samples which Zn content exceeded

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the higher guideline was considered small. Therefore it was concluded that Zn pollution exists only in isolated cases in the agricultural soils of the European Union and does not pose

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Zinc in water

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1.2.

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any risk to food safety on a continental scale [58].

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Water pollution by trace elements is an important factor in both geochemical cycling of trace

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elements and in environmental health. The hydrocycle of trace elements plays a significant

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role in each aquatic and terrestrial ecosystem. Especially cycling of trace metals in the oceans and their role in the photosynthetic fixation of carbon by phytoplankton is of great

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importance [82]. Ecological consequences of trace element pollution of waters are difficult to predict and to assess. The main sources of trace elements in ocean and sea basins are

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riverine fluxes, however, calculations of these values differ depending upon authors. The world average riverine fluxes of Zn to oceans and seas is estimated from 20 kt/yr [83] to 200

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kt/yr [84].

Zinc enters the water, and soil as a result of both natural processes and human activities. Most zinc is introduced into water by artificial pathways and may enter from numerous sources including mine drainage, industrial and municipal wastes, urban runoff, coal-fired power stations, burning of waste materials, but the largest input occurs from the erosion of

soil particles containing Zn [9,10]. In the EU the largest Zn discharge (28%) to the aquatic environment occurs from the manufacturing of basic industrial chemicals. Zinc may be also leached into groundwater by some mineral fertilizers and old galvanized metal pipes and well cribbings which were coated with zinc and can be dissolved by acidic waters. Estimated predicted environmental Zn contents for nine EU river basins in Germany, France and

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Belgium ranged between 1.3 to 14.6 µg Zn/L. These values were generated based on

monitoring data and using advanced methodologies in line with the recommendations made

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by the EU Scientific Committee on Human and Environmental Risks [85]. On the other hand predicted no effect contents values varied from 22.1 to 46.1 µg Zn/L. These results showed

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deterministic risk characterization ratios that were below 1 in all river basins, suggesting that

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there is no regional risk associated with current use patterns of Zn in these river basins.

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Zn is also found in drinking water in the form of salts or organic complexes. Normal levels

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of Zn in surface water and groundwater do not exceed 0.01 and 0.05 mg/L, respectively. Joint FAO/WHO committee on food additives proposed a daily dietary requirement of Zn of

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0.3 mg/kg of body weight and a provisional maximum tolerable daily intake of 1.0 mg/kg of body weight [11]. Daily human adult requirement is 15–22 mg Zn/day however; values of 5–

areas [86].

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22 mg Zn/day have been reported in studies on the average daily intake of Zn in different

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This trace element imparts an undesirable taste to water at a threshold content of around 4 mg/L (as Zn sulphate). Elevated levels of Zn in water can impart a bitter, metallic taste to

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water. Water with Zn contents exceeding 5 mg/L can has a milky appearance. Moreover, drinking water containing Zn at levels above 3 mg/L tends to be opalescent, develops a greasy film when boiled, and has an undesirable astringent taste [11]. The Council Directive 98/83/EC on the quality of water intended for human consumption Zn contents of more than 20 mg/L can cause nausea and vomiting in children under the age of 2, in people receiving

chemotherapy and people that consume large volumes of water. Although drinking-water contains Zn at contents above 0.1 mg/L, levels in tap water can be considerably higher because of the Zn used in older galvanized plumbing materials. In agriculture elevated Zn content in irrigation waters plays an important role because farmers are not obliged to apply additional Zn fertilizers to sustain plant growth. The

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recommended maximum content of Zn in irrigation water is 2.0 mg/L, since above this limit Zn is toxic to many plant species [12]. Its toxicity can be reduced at pH >6.0 and in fine

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textured or organic soils. Research carried out in Greece, Crete Island (Peza area) indicated a

maximum content of Zn in ground waters used for irrigation in greenhouses of about 0.34

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mg/L while the respective value in the area of Pylos (W. Peloponnese, Southern Greece),

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was 0.56 mg/L [34].

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When a water source has a Zn content of approximately 0.015 mg/L, it is an indication that

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the water source is fresh and unpolluted although, it is difficult to present a natural background concentration across Europe [87]. Higher Zn levels can be an indication of Zn

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pollution, from e.g. industrial processes of Zn leaching into the ground water. It has been found that long term effects of irrigation with wastewater might include pollution of ground

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water and soil with heavy metals including Zn ions [1]. It is apparent that due to geochemical differences and the different anthropogenic and a ‘natural’ sources which

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cannot be easily distinguished it is almost unattainable to determine experimentally Zn

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natural background contents at European level [87].

1.3.

1.3.1.

Zinc in food crops

Zinc content in crops

It has generally been recognized that Zn is transported in the plants either as Zn2+ or bound to organic acids. At high soil pH, it is presumably also taken up as monovalent cation (ZnOH+). Zinc accumulates in root tissues and is translocated via xylem to the shoot. Translocation of Zn to roots xylem occurs via symplast and apoplast but high levels of Zn

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have also been detected in the phloem, indicating that Zn is translocated both through xylem and phloem tissues [61]. In the aboveground plant part Zn is partially translocated from old

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leaves to developing plant organs [61]. Zn is an essential micronutrient which in plants is required in small but critical contents, and is involved in several key physiological functions

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including: membrane structure, photosynthesis, phytohormone activity, lipids and nucleic

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acids metabolism, gene expression and regulation, protein synthesis and defense against

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drought and disease. As a cofactor Zn activates different hormones (i.e. auxin) which are

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required for plant growth and development. It is essential for numerous biochemical processes, such as nucleotides production, auxin metabolism, enzyme activation and

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chlorophyll formation. It has special role in fertilization, as pollen grains have a very high concentration of Zn [88, 89]. Crops will not achieve their full yield potential and will exhibit

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stunted growth if their supply of Zn is inadequate. Visual symptoms include short internodes (i.e. in cereals) and small leaves; rosetting or whirling of (tree) leaves [90, 91]. Younger

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leaves usually affected first and may show signs of interveinal chlorosis (Figure 2a). High

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pH and high P or Mn can induce Zn deficiency [92].

“((Place Figure 2 here))”

As discussed earlier and as shown in Table 3, a wide range of food crops are affected by soil Zn deficiency including beans, deciduous fruit trees, maize, rice, and vegetables as well as

non-food crops such as cotton and flax [70]. Under Zn deficiency, losses of up to 30% in cereal grains can occur, without any obvious visual symptoms of stress (hidden deficiency) [5]. Zn allows critical physiological pathways to function normally and these pathways have important roles in photosynthesis and sugar formation, protein synthesis, fertility and seed production, growth regulation, and immunity to disease. Most plants contain between 30-100

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mg Zn/kg dry matter, with contents above 300 mg Zn/kg to be considered generally as toxic [61].

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Zn deficiency in crops occurs in most countries with Mediterranean type of climate, where alkaline-calcareous soils represent an important type of agricultural soil and are devoted

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particularly to cereal cultivation. In Central Anatolia (Turkey) for example, 65% of the soils

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contain high CaCO3 (> 20%) and the pH range from 7.5 to 8.1. These soils contain very low

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plant available Zn (0.23 mg/kg DTPA-Zn) although the total Zn content of the soils is

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relatively high (39.6–62.4 mg/kg). The low Zn availability in these soils is due to Zn being strongly sorbed onto CaCO3 and, in common with other regions of Zn-deficient soils, has

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stimulated the introduction of agronomic measures (i.e. proper fertilization) to correct Zn deficiencies [93] (Figure 2b).

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The sufficiency range of Zn contents vary between 15–70 mg Zn/kg in shoot of spring wheat [92, 94]. Zinc, in common with the other micronutrients, can affect growth when its content

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is either lower or above a critical level due to deficiency and/or toxicity problems, respectively. The lower critical content of whole plant is 15 mg Zn/kg in rice [95], and 15 to

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22 mg Zn/kg in maize and 22 mg Zn/kg groundnut. For the whole young plant, values reported include 8 mg Zn/kg for sorghum and 25 mg Zn/kg in winter wheat and chickpea. However, differences can also occur between different varieties of these crops [96]. Sufficient levels of Zn in the tissue of certain vegetables, arable and fruit crops are compiled in Table 4. It should be noted that detailed conditions on the sampling period and the

harvested plant part for each crop on which sufficiency ranges were based on must be searched on the respective individual references [92,94,97].

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“((Place Table 4 here))”

Experiments with quinoa (Chenopodium quinoa L.) conducted in two experimental locations

of Greece with different soil characteristics showed a higher Zn content in grains by all

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tested varieties in the clay soil [99] (Table 5). Also, biomass weight and plant height were more favorable in clay soils. Quinoa crop is gaining recently considerable international

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agronomic recognition due to its tolerance to abiotic stresses, the wide genetic variability and

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its high nutritional value. Its grain is an important source of minerals including Zn [99].

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“((Place Table 5 here))”

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Other important agronomic plant species include legumes (grain, pasture, and agro-forestry species) which are also among the most important crops in agriculture at European and

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worldwide level and ranked second only to the Gramineae in their importance to humans.

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These are also important sources of minerals (including Zn) when directly consumed by humans or in livestock production. The study on plant available metals carried out in hilly area of Thessaly, (Central Greece) [100] revealed differences in the uptake between annual

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plants suitable for grazing by sheep and perennial pasture crops (Table 6).

“((Place Table 6 here))”

Results indicate that metal bioavailability varied widely from element to element and according to different plant types. Plant samples showed marked difference in accumulation of metals and their uptake. Mean Zn content in annual grazing biomass was 4-fold greater than in perennial pasture whereas in both plant types Zn content was within the sufficiency

Biofortification with Zn and health effects

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1.3.2.

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ranges [100].

Recently, a new field of research has been developed on the biofortification of plant foods

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with Zn [101,102]. Biofortification is the process that aims to increase the content (‘density’)

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of micronutrients in edible portions of crop plants either through plant breeding (genetic

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biofortification) or fertilization (agronomic biofortification) [13]. This includes both

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breeding of new varieties with the genetic potential to accumulate high content of Zn in grains (for cereal crops) and the use of Zn fertilizers to increase their utilization efficiency

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and consequently grain Zn content [102]. Genetic biofortification (i.e. identify and transfer of the corresponding genes to important crops that increase their uptake capacity) is likely to

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be the most cost efficient approach, but additionally the use of fertilizers is necessary to improve Zn content in diets while the plant breeding programs are being carried out. Soil

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types, growth stage, and genotypes play also a key role in efficient use of Zn fertilizers (such as ZnSO4), therefore those factors need to be taken into account during application of

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fertilizers [60,102]. Another practice to mitigate Zn deficiency includes foliar Zn application which can increase significantly Zn content in seeds [3]. The application of foliar Zn is considered an efficient method of agronomic biofortification nevertheless there are large differences between plant species with regard to effectiveness of foliar-applied Zn. From the agronomic perspective increasing the content of Zn in seeds is a desirable quality factor.

Priming seeds in Zn containing solutions is a practical way to increase seed Zn prior to sowing and to contribute to better seedling growth. Seeds with high Zn content can sustain crop growth and increase yield through better germination, seedling vigor, and stress tolerance particularly in Zn-deficient soils [103, 104]. Additionally, biofortification of grains with Zn can bring beneficial effects for human health by helping to overcome malnutrition in

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populations with cereal-based diets [3]. Studies revealed that plant-based foods are significant sources of Zn for humans [2, 105]. An estimated 17.3% of people worldwide are

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at risk of inadequate Zn intake [106] and Zn-deficiency leads to estimated annual deaths of 433,000 children under the age of five [107]. Deficiency of Zn in humans can cause

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decreased loss of appetite, anemia, growth retardation, hypogonadism with impaired

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reproductive capacity, depressed mental function and in certain cases impaired keratosis and

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teratogenic effects [108–110]. Other severe health complications (defective immune system,

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learning capabilities, risk of infections, damage to DNA and cancer) are also reported to be associated with Zn deficiencies [111]. Infants and preschool children have lowered the

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incidence of diarrhoea and respiratory infections with increased growth in Znsupplementation [112], whereas it was found that low levels of Zn in soil are related to

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human Zn deficiency [113]. It may also have direct toxic effects when it found in excess causing gastrointestinal and immunologic problems. Elevated amounts of Zn may also

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inhibit Cu absorption and result in Cu deficiency symptoms. Through the food chain Zn is bioaccumulated resulting in higher contents in meat as compared to vegetables and fruits

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[114]. However, according to Risk Assessment Report [87] on the bioaccumulation of Zn in animals and on biomagnification (the increasing content of a substance, in the tissue of an organisms at successively higher levels in a food chain) it was concluded that the evaluation of quality standards for the protection of top predators from secondary poisoning and protection of human health from consumption of fishery products is considered to be not

relevant in the effect assessment of Zn. This was because the results of relevant studies revealed small differences in Zn levels of small mammals from control and polluted sites, indicating that the bioaccumulation potential of Zn in both herbivorous and carnivorous mammals will be low. Several factors can contribute to different Zn requirements such as differences in soil composition in different areas of the world, traditions of food preparation

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in various countries, food processing and accessibility, cultural practices and environmental

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pollution [115, 116].

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Conclusions

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Threshold values of Zn and other trace elements in soils are not easy to evaluate since apart

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of the total content in soils several other biochemical and environmental variables are involved. The main soil factors that affect the availability of Zn to the plants are those which

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control the amount of Zn in the soil solution and the most important are: Total Zn and clay content, redox potential, activity of soil microorganisms, presence of other nutrients, and

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climate conditions. The concentrations of Zn in surface waters (both marine waters and

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freshwater) are dependent on natural conditions and it is difficult to present experimentally a natural background concentration due to geochemical differences. High water Zn levels can be an indication of Zn pollution, from e.g. industrial processes of Zn leaching into the

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ground water which may seriously affect human health. Water solubility and mobility of Zn fertilizers should also be addressed, particularly in water saving environments. Yield of several important food crops (beans, citrus, fruit trees, grapes, maize, onions, pecan nuts, rice, sorghum, sweet corn etc) as well as the quality of the crop product may be decreased under Zn deficiency conditions. In future research should focus on the development of the

most efficient Zn application methods that will maximize Zn availability for plant uptake and grain accumulation. The role of different Zn sources and efficient fertilization strategies are means to eliminate Zn deficiency related health problems. Currently, biofortification of staple crops could be adopted for improving Zn intake in susceptible human populations. It includes efficient use of Zn fertilizers (agronomic biofortification) to accumulate high Zn

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content in edible plant parts whereas, our efforts should concentrate more to develop Zn

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accumulating genotypes through breading approaches (genetic biofortification).

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In this review the authors declare no conflict of interest

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Conflict of interest

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Acknowledgements

The present work was initiated within the framework of the COST Action TD1304 (Food

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and Agriculture), the Network for the Biology of Zinc (Zinc-Net).

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References

[1] A. Lebourg, T. Sterckeman, H. Ciesielski, N. Proix, Trace metal speculation in three unbuffered salt solutions used to assess their bioavailability in soil, J. Environ. Qual. 27 (1998) 584– 590.

[2] B.J. Alloway, Zinc in Soils and Crop Nutrition, second ed. IZA and IFA, Brussels, Belgium, Paris, France, 2008b. [3] I. Cakmak, Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil. 302 (2008a) 1–17. [4] I. Cakmak, M. Kalayci, H. Ekiz, H.J. Braun, Y. Kilinç, A. Yilmaz, Zinc deficiency as a

IP T

practical problem in plant and human nutrition in Turkey: a NATO-science for stability project, Field Crop Res. 60 (1999) 175–188.

SC R

[5] B.J. Alloway, Soil factors associated with zinc deficiency in crops and humans, Environ. Geochem. Health. 31 (2009) 537–548.

U

[6] K.G. Malle, Zink in der Umwelt, Acta Hydrochim. Hydrobiol. 20 (1992) 196–204

N

[7] S.A. Barber, Soil Nutrient Bioavailability: A Mechanistic Approach, second ed., John

A

Wiley & Sons, Inc., New York, 1995.

M

[8] L. Kiekens, Zinc, in: B.J. Alloway (Ed.), Heavy Metals in Soils, second ed., Blackie Academic and Professional, London, 1995, pp. 284–305.

ED

[9] U.S. Environmental Protection Agency (EPA), Ambient water quality criteria for silver, EPA-440/5-80-071. Office of Water Regulations and Standards. Criteria and Standard

PT

Division. Washington, DC., 1980a.

[10] U.S. Environmental Protection Agency (EPA), Exposure and risk assessment for zinc,

CC E

EPA 440/4-81-016. Office of Water Regulations and Standards. (WH-553) Washington, DC., 1980b.

A

[11] FAO/WHO, Evaluation of certain food additives and contaminants, Joint FAO/WHO Expert Committee on Food Additives, Cambridge University Press, Cambridge, WHO Food Additives Series, No. 17, 1982.

[12] P.F. Pratt, Quality criteria for trace elements in irrigation waters. University of California, Division of Agricultural Sciences, California Agricultural Experiment Station p. 46. 1972. [13] P.J. White, M.R. Broadley, Biofortifying crops with essential mineral elements, Trends Plant Sci. 10 (2005) 586–593.

IP T

[14] Y.H. Wang, C.Q. Zou, Z. Mirza, H. Li, Z.Z. Zhang, D.P. Li, C.L. Xu, X. Zhou, X.J.

Shi, D.T. Xie, X. He, Y. Zhang, Cost of agronomic biofortification of wheat with zinc

SC R

in China, Agron. Sust. Develop. 36 (2016) 44–51.

[15] C. Hotz, K.H. Brown, Assessment of the risk of zinc deficiency in populations and

U

options for its control, Food Nutr. Bull. 25 (2004) 94–204.

N

[16] A.J. Stein, P. Nestel, J.V. Meenakshi, M. Qaim, H.P.S. Sachdev, Z.A. Bhutta, Plant

M

Public Health Nutr. 10 (2007) 92–501.

A

breeding to control zinc deficiency in India: how cost-effective is biofortification?

[17] W. Chesworth, Geochemistry of micronutrients, in: J.J. Mortvedt, F.R. Cox, L.M.

ED

Shuman, R.M. Welch (Eds.), Micronutrients in Agriculture, second ed., Soil Sci. Soc. Am. Inc., Madison, WI., 1991 pp. 1–30.

PT

[18] A. Kabata-Pendias, H. Pendias, Trace elements in soils and plants, third ed., CRC Press, Inc., Boca Raton, Florida, USA, 2001.

CC E

[19] J. Mertens, E. Smolders, Zinc, in: B.J. Alloway (Ed.), Heavy Metals in Soils: Trace Metals and Metalloids in Soils and Their Bioavailability. Springer, Dordrecht,

A

Nederlands, 2013, pp. 465–493.

[20] A. Kabata-Pendias, H. Pendias, Biogeochemistry of trace elements, second ed., Wyd Nauk PWN. Warszawa, (in Polish), 1999.

[21] M. Angelone, C. Bini, Trace elements concentration in soils and plants of Western Europe, in: D.C. Adriano (Ed.), Biogeochemistry of trace metals. Lewis Publ., Boca Raton, 1992, pp. 19–60. [22] IZA, Chemical Safety Report, Zinc, International Zinc Association. Submitted to ECHA for REACH registration purposes, 2010.

IP T

[23] C. Reimann, A. Demetriades, M. Birke, P. Filzmoser, P. O’Connor, J. Halamic, A.

Ladenberger, and the GEMAS Project Team, Distribution of elements/parameters in

SC R

agricultural and grazing land soil of Europe, in: C. Reimann, M. Birke, A. Demetriades, P. Filzmoser, P. O’Connor (Eds.), Chemistry of Europe's agricultural soils – Part A:

U

Methodology and interpretation of the GEMAS data set. Geologisches Jahrbuch (Reihe

N

B 102), Schweizerbarth, 2014, pp. 101–472. (Chapter 11).

A

[24] ISO, 1995. Soil quality. Extraction of Trace Elements Soluble in Aqua Regia

M

[25] S.P. McGrath, P.J. Loveland, Soil Geochemical Atlas of England and Wales, Blackie Academic and Professional, Glasgow, 1992.

ED

[26] D. Baize, Teneurs totales en éléments traces métalliques dans les sols (France), INRA Editions, Paris, p. 410, 1997.

PT

[27] A. Kabata-Pendias, H. Pendias, Trace elements in soils and plants, second ed., CRC Press, Inc., Boca Raton, p. 365. Florida, USA, 1992.

CC E

[28] J.E. Eriksson, Concentrations of 61 trace elements in sewage sludge, farmyard manure, mineral fertilizers, precipitation and in oil and crops. Swedish Environmental Protection

A

Agency (EPA), Report No 5159, Stockholm, 2001a.

[29] A. Gorny, J. Uterman, W. Eckelmann, Germany, in: Heavy Metal (Trace Element) and Organic Matter Contents of European Soils. European Commission, CEN Soil Team No 30, Secretariat, Nederland’s Normalisatie-Institute (NEN) Delft, The Netherlands, 2000.

[30] W. Lindsay, W. Norvell, Development of a DTPA Soil Test Zinc, Iron, Manganese and Copper, Soil Sci. Soc. Am. J. 42 (1978) 421–428. [31] Th. Karyotis, A. Charoulis, Th. Mitsimponas, E. Vavoulidou, Nutrients and trace elements of arable soils rich in organic matter, Commun. Soil Sci. Plant Anal. 36: (2005) 403–414.

IP T

[32] Th. Karyotis, P. Papadopoulos, A. Haroulis, G. Argyropoulos, Origin and accumulation of heavy metals in roadside soils of Central Greece, Balkan Ecol. 2 (1999) 72–80.

SC R

[33] Th. Karyotis, A. Charoulis, J. Alexiou, M. Tziouvalekas, Th. Mitsimponas, A. Drosos.

Variation of Properties in Surface Soils from a Prior Lake-Bed (Lake Askuris, Greece)

U

Farmed for Over 90 Years, Commun. Soil Sci. Plant Anal. 40 (2009) 352–364.

N

[34] Th. Karyotis, G. Arampatzis, A. Panagopoulos, E. Hatzigiannakis, E. Tziritis, Aik.

A

Karyoti, J. Vrouchakis, Nutrients, trace elements and water deficit in Greek soils

M

cultivated with olive trees, Int. J. Env. Qual. 13 (2014) 9–20. [35] Th. Karyotis, Th. Mitsimponas, A. Charoulis, G. Argyropoulos, Nutrients and heavy

ED

metals in cultivated soils of the Prefecture of Larissa, Greece. Geotech. Sci. Issues, 6, (1995) 75–81. (In Greek)

PT

[36] FAO/UNESCO, Soil Map of the World, Vol. I, Legend, UNESCO, Paris, 1974. [37] A. Kabata-Pendias, Heavy metal concentrations in arable soils of Poland, Pamiet.

CC E

Pulawski, 74 (1981) 101–111. (In Polish).

[38] A. Kabata-Pendias, M. Piotrowska, Total contents of trace elements in soils of Poland,

A

Materialy IUNG, S8, Pulawy, Poland, p.47. 1971. (In Polish).

[39] C. Räutä, S. Cärstea, A. Mihäilescu, R. Lacatusu, Some aspects of pedochemical and biogeochemical research in Romania, in: I. Thornton, (Ed.), Proc. 1st Int. Symp. Geochemistry and Health, Imperial College, London, 1985, pp. 236–244.

[40] L.P. Golovina, M.N. Lysenko, T.J. Kisiel, Content and distribution of zinc in soils of Ukrainian Woodland (Polessie), Pochvovedenie, 2 (1980) 72–79. (In Russian). [41] J.N. Zborishchuk, N.G. Zyrin, Copper and zinc in the ploughed layer of soils of the European USSR, Pochvovedenie, 1 (1978) 31–36. (In Russian). [42] E. Schlichting, A.M. Elgala, Schwermetallverteilung und Tongehalte in Böden, Z.

IP T

Pflanzenern. Bodenk. 6, (1975) 563–571.

[43] J. Bäjescu, A., Chiriac, Some aspects of the distribution of copper, cobalt, zinc and

SC R

nickel in soils of the Dobrudja, Anal. Inst. Cent. Cerc. Agric. 30A (1962) 79–87. (In Romanian).

U

[44] C. Wilkins, The distribution of Mn, Fe, Cu, and Zn in topsoils and herbage of North-

N

West Pembrokeshire, J. Agric. Sci. 92 (1979) 61–68.

A

[45] J.Ch. Tjell, M.F. Hovmand, Metal concentrations in Danish arable soils, Acta Agric.

M

Scand. 28 (1978) 81–89.

[46] K. Czarnowska, B. Gworek, Heavy metals in some soils of the central and northern

ED

regions of Poland, Roczn. Glebozn. 5 (1987) 41–57. (In Polish). [47] L. Stanchev, G. Gyurov, N. Mashev, Cobalt as a trace element in Bulgarian soils, Izv.

PT

Centr. Nauch. Inst. Pochvoznan Agrotekh. “Pushkarov”, 4 (1962) 145–154. (In Bulgarian).

CC E

[48] B.E. Davies, Ed., Applied Soil Trace Elements, John Wiley & Sons, New York, p. 482, 1980

A

[49] I. Thornton, J.S. Webb, Trace elements in soils and surface waters contaminated by past metalliferous mining in parts of England, in: D.D. Hemphill (Ed.), Trace Subst. Environ. Health, Vol. 9, University of Missouri, Columbia, MO, p. 77. 1975. [50] G.M. Ivanov, C.H Cybzhitov, Microelements in steppe facies of Southern Zabaykalie, Agrokhimiya, 2 (1979) 103. (In Russian).

[51] O.J. Alikhanova, A.N. Zyrianova, V.V. Cherbar, Minor elements in soils of some regions in the western Pamirs, Pochvovedenie, 11 (1977) 54. (In Russian). [52] B.K Shakuri, Trace elements in northern Azov and cis Caucasian chernozems of the Rostov Region, Izv. Akad. Nauk Azerbaizhan. SSR, ser. Biol. Nauk. 4 (1964) 81–89. (In Russian).

IP T

[53] B. Aaby, J. Jacobsen, Changes in biotic conditions and metal deposition in the last

Denmark. Yearbook 5. 1978.

SC R

millennium as reflected in ombrotrophic peat in Draved Moses, Denmark, Geol. Surv.

[54] S. Mirchev, Zinc and copper compounding forms in Chernozems and forest soils, Pochvozn. Agrokhim. 13 (1978) 84–91. (In Bulgarian).

N

U

[55] C. Bini, M. Dall’Aglio, O. Ferretti, R. Gragnani, Background levels of microelements in

A

soils of Italy, Environ. Geochem. Health, 10 (1988) 63–69.

M

[56] A. Kabata-Pendias, K. Wiącek, Excessive uptake of heavy metals by plants from contaminated soils, Soil Sci. Ann. 36 (1985) 33–42.

ED

[57] J. Bäjescu, A. Chiriac, Trace element distribution in brun lessivé and lessivé soils, Stiinta Solului 6 (1968) 45–5. (In Romanian).

PT

[58] G. Tóth, T. Hermann, M.R. Da Silva, L. Montanarella, Heavy metals in agricultural soils of the European Union with implications for food safety, Environ. Intern. 88

CC E

(2016) 299–309.

[59] B. Singh, S.K.A. Natesan, B.K. Singh, K. Usha, Improving zinc efficiency of cereals

A

under zinc deficiency, Curr. Sci. 88 (2005) 36–44.

[60] B. Sadeghzadeh, A review of zinc nutrition and plant breeding, J. Soil Sci. Plant Nutr. 13 (4) (2013) 905–927. [61] H. Marschner, Mineral Nutrition of Higher Plants, second ed., Academic Press, London, 1995.

[62] I. Cakmak, A. Yilmaz, M. Kalayci, H. Ekiz, B. Torun, B. Erenoglu, H.J. Braun, Zn deficiency as a critical problem in wheat production in central Anatolia, Plant Soil 180 (1996) 165–172. [63] R. Holloway, Zinc as a subsoil nutrient for cereals, PhD thesis, Dept. of Agronomy and Farming Systems, University of Adelaide, Adelaide, Australia, 1996.

IP T

[64] B.J. Alloway, Zinc deficiency in wheat in Turkey, in: B.J. Alloway, (Ed.),

Micronutrient Deficiencies in Global Crop Production, Springer, Dordrecht,

SC R

Netherlands, 2008, pp. 181–200.

[65] R.E. Lucas, J.F. Davis, Relationships between pH values of organic soils and

U

availabilities of 12 plant nutrients, Soil Sci. 92 (1961) 177–182.

N

[66] P.N. Takkar, C.D. Walker, The distribution and correction of zinc deficiency, in: A.D.

A

Robson (Ed.), Zinc in Soils and Plants, Kluwer Academic Publishers, Dordrecht, The

M

Netherlands, 1993, pp. 151-165.

[67] K. Haidouti, Th. Karyotis, A. Haroulis, J. Massas, Fluctuation of micronutrients in acid

ED

Entisols in the Province of Xanthi, Proc,. of the, 5th Panhellenic Symposium of Soil Science, Xanthi, Greece, 1994, pp. 825–836. (In Greek)

PT

[68] E. Vavoulidou, A. Charoulis, K. Soulis, Th. Karyotis and V. Kavvadias, Soil Survey for Improvement of Farming Practices in Malia Municipality, Greece, Commun. Soil

CC E

Sci. Plant Anal. 40 (2009) 1020–1033.

[69] A. Mori, G.J.D. Kirk, J.S. Lee, M.J. Morete, A.K. Nanda, S.E. Johnson-Beebout, M.

A

Wissuwa, Rice Genotype Differences in Tolerance of Zinc-Deficient Soils: Evidence for the Importance of Root-Induced Changes in the Rhizosphere. Front. Plant Sci. 6 (2016), Article 1160.

[70] D.A. Horneck, D.M. Sullivan, J.S. Owen, and J.M. Hart, Soil Test Interpretation Guide, Oregon State University, Extension Service 2011.

[71] B.J. Alloway, Micronutrients and crop production: An introduction. in: B.J. Alloway, (Ed.), Micronutrient Deficiencies in Global Crop Production. Springer, Dordrecht, Netherlands, 2008, pp. 1–39. [72] D.C. Martens, D.T. Westermann, Fertilizer applications for correcting micronutrient deficiencies, in: Micronutrients in Agriculture, second edition, Soil Sci. Soc. Am.,

IP T

Madison, Wisconsin, USA, 1991, pp. 549–592.

[73] ILZRO, Zinc in crop production, International Lead Zinc Research Organization, 1975,

SC R

pp 54.

[74] N.A. Slaton, C.E. Wilson Jr., S. Ntamatungiro, R.J. Norman, D.L. Boothe, Evaluation

U

of zinc seed treatments for rice. Agron J. 93 (2001) 152–157.

N

[75] B. Sadeghzadeh, Z. Rengel, Zinc in Soils and Crop Nutrition, in: M.J. Hawkesford, P.

A

Barraclough (Eds.), The Molecular and Physiological Basis of Nutrient Use Efficiency

M

in Crops. Wiley-Blackwell, 2011, pp. 335–375.

[76] B. Mandal, L.N. Mandal, M.H. Ali, Chemistry of zinc availability in submerged soils in

ED

relation to zinc nutrition of rice crop. in: Proc., of the workshop on micronutrients, Bhubaneswar, India, 22–23 January 1992, (1993) pp 240–253.

PT

[77] N.K. Fageria, Influence of micronutrients on dry matter yield and interaction with other nutrients in annual crops. Pesq. Agropec. Bras. 37 (2002) 1765–1772.

CC E

[78] N.K. Fageria. Dry matter yield and nutrient uptake by lowland rice at different growth stages. J. Plant Nutr. 27(6) (2004) 947–958.

A

[79] R.J. Landon, (ed.), Booker tropical soil manual: a handbook for soil survey and agricultural land evaluation in the tropics and subtropics, Booker Tate Ltd; Longman, London, 1991. [80] L.R. Lado, T. Hengl, H.I. Reuter, Heavy metals in European soils: A geostatistical analysis of the FOREGS Geochemical database, Geoderma 148 (2008) 189–199.

[81] G. Tóth, A. Jones, L. Montanarella, LUCAS Topsoil Survey — methodology, data and results, EUR 26102 EN, Office for Official Publications of the European Communities, Luxembourg, 2013, p. 141. [82] A. Kabata-Pendias, A. Mukherjee, Trace Elements from Soil to Human, SpringerVerlag, Berlin, 2007, pp 561.

IP T

[83] J. Gaillardet, J. Viers, B. Dupré, Trace elements in river waters, in: J.I. Drever (Ed.), H.D. Holland, K.K. Turekian (Exec. Eds.), Treatise on geochemistry, surface and

SC R

ground water, weathering and soils. Elsevier, Amsterdam 5, 2003, pp 225–227.

[84] Y. Kitano, Water Chemistry, in: W.A. Nierenberg (Ed.), Encyclopedia of Earth system

U

science, Acad. Press, San Diego, 4, 1992, pp 449–470.

N

[85] P.A. Van Sprang, F.A.M. Verdonck, F. Van Assche, L. Regoli, K.A.C. De

A

Schamphelaere, Environmental risk assessment of zinc in European freshwaters: A

M

critical appraisal, Sci. Tot. Environ. 407 (2009) 5373–5391. [86] C.G. Elinder, Zinc, in: L. Friberg, G.F. Nordberg, V.B. Vouk (Eds.), Handbook on the

ED

toxicology of metals, second ed., Amsterdam, Elsevier Science Publishers, 1986, pp. 664–679.

PT

[87] E.C., European Union Risk Assessment Report for Zinc metal (CAS-No.: 7440-66-6, EINECS-No.: 231-175-3), (Final report, Part I, Environment), Institute for Health and

CC E

Consumer Protection - European Chemicals Bureau. 117, 2008.

[88] M.C. Begum, M. Islam, M.R. Sarkar, M.A.S. Azad, A.N. Huda, A.H. Kabir, Auxin

A

signaling is closely associated with Zn efficiency in rice (Oryza sativa L.). J Plant Interact. 11 (2016) 124–129.

[89] H.B. Chang, C.W. Lin, H.J. Huang, Zinc-induced cell death in rice (Oryza sativa L.) roots. Plant Growth Regul. 46 (2005) 261–266.

[90] R.F. Brennan, J.D. Armour, D.J. Reuter, Diagnosis of zinc deficiency, in: A.D. Robson, (Ed.), Zinc in Soils and Plants, Kluwer Academic Publishers, Dordrecht, Netherlands, 1993, pp. 167–181, 206. [91] R.F. Brennan, M.D.A. Bolland, Relative effectiveness of soil-applied zinc for four crop species, Aust. J. Exp. Agric., 42 (2002) 985–993.

in Minnesota, Univ. Minn. Extension Service, BU-05886, 2005.

IP T

[92] C.J. Rosen, R. Eliason, Nutrient management for commercial fruit and vegetable crops

SC R

[93] I. Cakmak, Zinc deficiency in wheat in Turkey, in: B. Alloway, (Ed.), Micronutrient Deficiencies in Global Crop Production, Springer, Netherlands, 2008, pp. 181–200.

U

[94] G.M. Bryson, H.A. Mills, D.N. Sasseville, J.B. Jones, A.V. Baker, Plant analysis

N

handbook III, Micro-Macro Publishing, Inc., Athens, 2014, GA.

A

[95] P.C. Srivastava, U.C. Gupta, Trace Elements in Crop Production, Science Publishers,

M

Lebanon, New Hampshire, 1996, pp. 356.

[96] B.J. Alloway, Zinc - The Vital Micronutrient for Healthy, High - Value Crops,

ED

International Zinc Association, Brussels, 2001. [97] E. Hanson, Fertilizing fruit crops. Michigan State University, Extension Bulletin E-852.

PT

1996. Available at http://www.msue.msu.edu/vanburen/e-852.htm [98] P.N. Takkar, Zinc deficiency in Indian soils and crops, Chap. 10, in: Zinc in Crop

CC E

Nutrition (2nd edn.), India Lead Zinc Information Centre, Delhi, and International Lead, Zinc Research Organisation Inc. Research Triangle Park, 1991, pp 66.

A

[99] Th. Karyotis, C. Iliadis, Ch. Noulas, Th. Mitsibonas, Preliminary Research on Seed Production and Nutrient Content for Certain Quinoa Varieties in a Saline–Sodic Soil, J. Agron. Crop Sci. 189 (2003) 1–7. [100] Th. Karyotis, M. Toulios, J. Alexiou, M. Tziouvalekas, A. Charoulis, S. Vergos, K. Tsipis, A. Drosos, V. Aretos, Th. Mitsimponas, Soils and Native Vegetation in a Hilly

and Mountainous Area in Central Greece, Commun. Soil Sci. Plant Anal. 42 (2011) 1249–1258. [101] Z. Shahzad, H. Rouached, A. Rakha, Combating Mineral Malnutrition through Iron and Zinc Biofortification of Cereals, Compreh. Rev. Food Sci. Food Saf. 13 (2014) 329–346.

IP T

[102] D. Montalvo, F. Degryse, R.C. da Silva, R. Baird, M.J. McLaughlin, Agronomic

Effectiveness of Zinc Sources as Micronutrient Fertilizer, Adv. Agron. 139 (2016)

SC R

215–267.

[103] Z. Rengel, R. Graham, Importance of seed Zn content for wheat growth on Zn

U

deficient soil, Plant Soil 173 (1995) 259–266.

N

[104] A. Yilmaz, H. Ekiz, I. Gültekin, B. Torun, H. Barut, S. Karanlik, I. Cakmak, Effect of

A

seed zinc content on grain yield and zinc concentration of wheat grown in zinc

M

deficient calcareous soils, J. Plant Nutr. 21 (1998) 2257–2264. [105] R.M. Welch, R.D. Graham, Breeding for micronutrients in staple food crops from a

ED

human nutrition perspective, J Exp. Bot. 55 (2004) 353–364. [106] K.R. Wessells, K.H. Brown, Estimating the global prevalence of zinc deficiency:

PT

results based on zinc availability in national food supplies and the prevalence of stunting, PLoS ONE 7: e50568. (2012).

CC E

[107] WHO, Global Health Risks, Mortality and Burden of Disease Attributable to Selected Major Risk, Available at

A

http://www.who.int/healthinfo/global_burden_disease/GlobalHealthRisks, 2009 (accessed 17.10.2017)

[108] E. Frossard, M. Bucher, F. Machler, A. Mozafar, R. Hurrell, Potential for increasing the content and bioavailability of Fe, Zn and Ca in plants for human nutrition, J. Sci. Food Agric. 80 (2000) 861–879.

[109] S. Cunningham-Rundles, D.F. McNeeley, A. Moon, Mechanisms of nutrient modulation of the immune response, J. Allergy Clin. Immun. 115 (2005) 1119–1128. [110] H. Suzuki, A. Asakawa. J.B. Li, M. Tsai, H. Amitani, K. Ohinata, M. Komai, A. Inui, Zinc as an Appetite Stimulator - The Possible Role of Zinc in the Progression of Diseases Such as Cachexia and Sarcopenia. Rec. Pat. Food Nutr. Agric. 3 (2011) 226 –

IP T

231.

developing countries, Proc. Nutr. Soc. 65 (2006) 51–60.

SC R

[111] R.S. Gibson, Zinc: the missing link in combating micronutrient malnutrition in

[112] J.A. Rivera, M.T. Ruel, M.C.Santizo, B. Lonnerdal, K.H. Brown, Zinc

U

supplementation improves growth of stunted rural Guatemalan infants, J. Nutr. 128

N

(1998) 556–562.

A

[113] I. Cakmak, Enrichment of fertilizers with zinc: an excellent investment for humanity

M

and crop production in India, J. Trace Elem. Med. Biol. 23 (2009) 281–289. [114] ATDSR (United States Agency for Toxic Substances and Disease Registry),

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Toxicological Profile for Zinc. U.S. Department of Health and Human Services, 2007, p. 352.

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[115] J.H. Freeland-Graves, N. Sanjeevi, J.J. Lee, Global perspectives on trace element requirements, J. Trace Elem. Med. Biol. 31 (2015) 135–141.

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[116] Q. Zaman, Z. Aslam, M. Yaseen, M.Z. Ihsan, A. Khaliq, S. Fahad, S. Bashir, P.M.A. Ramzani, M.Naeem, Zinc biofortification in rice: leveraging agriculture to moderate

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hidden hunger in developing countries, Arch. Agron. Soil Sci. 64 (2018) 147–161.

Figures: Figure 1. Distribution of total Zn in agricultural top soils in Europe: Geochemical map of high quality data within the GEMAS project (Geochemical Mapping of Agricultural and Grazing Land Soil of Europe) has produced for chemical elements (including Zn) across Europe, harmonized with respect to: (1) land-use (agricultural soil, Ap= 0-20 cm); (2) spatial

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scale (homogeneous sampling density: 1 site/2500 km2 (grid of 50×50 km); (3) sample preparation (<2mm) and (4) analytical methods (Aqua regia extractable ICP-MS 53

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elements). (5) Number of samples = 2218 [23].

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1.

Figure 2. a) Soybean Zn deficiency symptoms including whirling and interveinal chlorosis (courtesy IPNI http://www.ipni.net/), b) Effect of zinc fertilization on wheat growth in

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Central Anatolia, Turkey [4].

Tables: Table 1. Zn content concentration? (mg/kg) in different types of soils. Source: [18,20] Soil type

Abundance

SC R

IP T

64 31–61 47–61 35–75 50–100 57–100

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A

N

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Mean Light sandy Medium loamy Heavy loamy Calcareous Organic

Table 2. Soil types/units according to FAO/UNESCO [36] and Zn content concentration? (mg/kg, on dry weight basis) of surface soils in some European countries [18]. Zn

Mean Zn

Podzols (highly altered profile due to leaching) and sandy soils (coarse)

Poland Romania Russia Germany

5–220 25–188 3.5–57 40–76

24 61 31 ̶

Loess and silty soils (medium textured soils)

Poland Romania Russia Germany

17–127 ̶ 40.55 58–100

47 73 48 ̶

Loamy (medium textured) and clay (heavy textured) soils

Great Britain Poland Romania Russia Germany

̶ 13–362 37–101 9–77 40–50

Soils on glacial till

Denmark Poland

Fluvisols (percent alluvial deposits, little alternation)

Bulgaria Great Britain Poland Russia

U

N

70 67.5 75 35 ̶

[37,38] [39] [40,41] [42] [37,38] [43] [40] [44] [37,38] [39] [40,41] [42]

̶ 19–52

28 40

̶ 67–180 55–124 34–49

62 125 84.5 42

[47] [48,49] [37] [41]

̶ 13–98 26.5–79

54 50.5 52.5

[44] [37] [41]

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Gleysols (soils formed from various Great Britain materials with hydromorphic Poland properties within the top horizon) Russia

Reference

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Country

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Soil type/unit

[45] [46]

Poland Russia Germany

58–150 23–71 ̶

77 47 100

[37,38] [40,41] [42]

Kastanozems and brown soils (soils formed under steppe vegetation)

Romania Russia

27–113 32.5–54

57 43

[39] [41,50]

Solonchaks (formed from recent alluvial deposits, with salt accumulation) and solonetz (high exchangeable Na content)

Bulgaria Russia

39–63 44–155

̶ 100

[47] [41,51]

Chernozems (Soils developed under prairie vegetation)

Bulgaria Poland Russia

63–97 33–82 39–82

̶ 61.5 57

[47] [37] [41,52]

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Rendzinas (shallow soils over limestones)

Table 2. (Continued) Country

Zn

Mean Zn

Histosols (organic soils, having H horizon of more than 40 cm) and other organic soils

Bulgaria Denmark Poland Russia

̶ 48–130 13–250 7.5–74

80 72.5 60 34

[47] [45,53] [38] [40,41]

Forest soils

Bulgaria Russia

35–106 42.5–118

̶ 71.5

[47] [41]

Various soils

Bulgaria Denmark Great Britain Italy Poland Romania Russia

39–99 ̶ 20–284 16–157 3–762 35–115 47–139

65 31 80 68 46.6 61 78

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Reference

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Soil type/unit

[54] [45] [44,49] [55] [56] [57] [41]

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Table 3. Sensitivity of crops to soil Zn deficiency (based mainly on data by [71–73]. High

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Common bean (Phaseolus vulgaris L.) Pha spp. Citrus Fruit trees (deciduous) Grapes (Vitis vinifera L.) Hops (Humulus lupulus L.) Maize (Zea mays L.) Onions (Allium cepa L.) Nuts (pecan) (Carya illinoinensis L.) Rice (Oryza sativa L.) Sorghum (Sorghum bicolor L.) Sweet corn (Zea mays convar. saccharata var. Rugosa)

Medium

Low

Barley (Hordeum vulgare L) Lettuce (Lactuca sativa L.) Potato (Solanum tuberosum L) Spinach (Spinacia oleracea L.) Soybean (Glycine max L. Merr.) Sugar beet (Beta vulgaris L. subsp vulgaris) Table beet (Beta vulgaris L.) Tomato (Solanum lycopersicum L.)

Alfalfa (Medicago sativa L.) Asparagus (Asparagus officinalis L.) Carrot (Daucus carota subsp. sativus) Oat (Avena sativa L.) Pea (Pisum sativum L.) Rye (Secale cereale L.) Wheat (Triticum aestivum L.)

Table 4. Sufficiency levels/critical content of Zn (mg/kg) in selected crops, vegetables and fruits.

Crop a

Lower critical contents b, other sufficiency levels /Reference:

Sufficiency levels [92,94]

A

Cauliflower Broccoli Cabbage Carrot

a

25–60 20–45 15–60 20–50 20–50 ̶ ̶

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Vegetables

SC R

N

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15 b / [95] ̶ ̶ b 20, 16, 14 / [95, 98]

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Fruits Blueberry Grape Raspberry Strawberry Apple Apricot, Plums Cherries

20 b / [95] 15–22 b/ [95] 32 b / [91]

21–70 20–70 15–70 20–40 ̶ 15–80 25–100 21–80 10–80 ̶ ̶

25 b / [98] 18 b / [98]

A

Alfalfa Corn Spring wheat Potato Rice Edible bean Pea Soybean Sugar beet Chickpea Mustard

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Arable crops

20–250 20–80 20–200 25–250

30–60 [97] 20–50 [97] ̶ 20–40 [97] 20–50 [97] 15–40 [97]

̶ ̶ ̶ ̶

For special conditions on the sampling period and on the specific harvested above-ground

plant part on which sufficiency ranges were based on please see individual references.

b

Lower critical contents concentration? (under which Zn is inadequate for proper growth due to deficiency). 40

Table 5. Whole grain content in Zn (mg/kg) for eight quinoa varieties at two experimental locations. Results adopted from reference [99].

Denmark Chile England England The Netherlands Denmark Brazil Chile

Location 2

(Clay soil)

(Sandy soil)

56 67 62 53 63 61 63 60 61 9

38 44 37 34 41 39 42 38 39 4

L1-L2

18** 23** 25** 19** 22** 22** 21** 22** 22**

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E-DK-4-PQCIP-DANIDA-UNA BAER-II-U-CONCEPTION RU-2- PQCIP- DANIDA-UNA RU-5- PQCIP- DANIDA-UNA NL6- PQCIP- DANIDA-UNA G-205-95- PQCIP- DANIDA-UNA 02-EMPRARA No 407 Average (Location) LSD (5% within locations)

Location 1

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Country Origin

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Varieties

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** Significant differences between the locations at 1% probability level according to

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Student’s pair-wise t-test.

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Table 6. Metals (mg/kg) in annual grazing biomass and perennial pasture crops (n=24). Results adopted from reference [100]. Annual grazing biomass Min.

Max.

SD a

Mean

Min.

Max.

SD

166.8 259.9 76.8 7.4

28 94 37 4.5

462 652 148 11

146.7 120.9 30.1 1.6

38.1 135.9 155.1 6.2

24 59 31 5

76 246 308 8

14.2 50.1 75.9 1.2

SD, standard deviation

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a

Mean

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Zinc Iron Manganese Cooper

Perennial pasture crops

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Metal

42