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Review

Stability of the Inherent Target Metallome in Seed Crops and a Mushroom Grown on Soils of Extreme Mineral Spans

by
Gerhard Gramss
1,* and
Klaus-Dieter Voigt
2
1
Institute of Earth Sciences, Friedrich-Schiller-University, Burgweg 11, D-07749 Jena, Germany
2
Food GmbH Jena, Orlaweg 2, D-07743 Jena, Germany
*
Author to whom correspondence should be addressed.
Agronomy 2016, 6(1), 14; https://doi.org/10.3390/agronomy6010014
Submission received: 18 August 2015 / Revised: 1 February 2016 / Accepted: 2 February 2016 / Published: 18 February 2016
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Abstract

:
Extremes in soil mineral supply alter the metallome of seeds much less than that of their herbage. The underlying mechanisms of mineral homeostasis and the “puzzle of seed filling” are not yet understood. Field crops of wheat, rye, pea, and the mushroom Kuehneromyces mutabilis were established on a set of metalliferous uranium mine soils and alluvial sands. Mineral concentrations in mature plants were determined from roots to seeds (and to fungal basidiospores) by ICP-MS following microwave digestion. The results referred to the concentrations of soil minerals to illustrate regulatory breaks in their flow across the plant sections. Root mineral concentrations fell to a mean of 7.8% in the lower stem of wheat in proportions deviating from those in seeds. Following down- and up-regulations in the flow, the rachis/seed interface configured with cuts in the range of 1.6%–12% (AsPbUZn) and up-regulations in the range of 106%–728% (CuMgMnP) the final grain metallome. Those of pea seeds and basidiospores were controlled accordingly. Soil concentration spans of 9–109× in CuFeMnNiZn shrank thereby to 1.3–2× in seeds to reveal the plateau of the cultivar’s desired target metallome. This was brought about by adaptations of the seed:soil transfer factors which increased proportionally in lower-concentrated soils. The plants thereby distinguished chemically similar elements (As/P; Cd/Zn) and incorporated even non-essential ones actively. It is presumed that high- and low-concentrated soils may impair the mineral concentrations of phloems as the donors of seed minerals. In an analytical and strategic top performance, essential and non-essential phloem constituents are identified and individually transferred to the propagules in precisely delimited quantities.

1. Introduction

Extreme variations in the natural or anthropogenically influenced trace mineral stock of arable land are a challenge to non-endemic high-productivity seed crops rather than to locally-adapted landraces [1,2]. Insufficient Zn resources down to 2–3 mg kg−1 soil denote up to 50% of the cropland in India, China, and some countries in the Middle East [3]. Of the 14,900 Indian soil samples, 49% were deficient in Zn, 33 in B, 12 in Fe, 11 in Mo, 5 in Mn, and 3 in Cu [4]. Local crops experienced yield losses due to deficiencies in Zn (49%); B (31%); Mo (15%); Cu (14%); Mn (10%); and Fe (3%) [5]. Low soil concentrations of the plant- and nutritionally essential elements of CuFeMnNiZn (Block presentation of the single elements) and traces of IMoSe, in addition to their poor plant availability due to unfavorable sorption and redox conditions [6,7], as well as insufficiency in their uptake by some crop genotypes [8,9] serving as staple food and feed are all factors causing mineral malnutrition and health problems in humans and livestock [10,11,12]. They also impair health and productivity of the crop itself [5,13,14]. Applications of micronutrient fertilizers are obligatory [9,12].
Land consumed by mining, industrial heavy-metal (HM) and radionuclide emissions, and applications of sewage sludge, husbandry sludges, and AsCdU-contaminated phosphate fertilizers as world-wide practices result in potential croplands with single or multiple metal toxicants [15,16,17] in concentrations outside permissible limits [7,18,19]. The late 20th century was faced with a world-wide annual release of 22,000 MgCd; 954,000 MgCu; 796,000 MgPb; and 1,372,000 MgZn [20]. Land contaminated by mining and metallurgy with AsCdCrCuNiPbZn may be gradually recovered with the downwash of metal-clay complexes from plough layer to subsoil strata (clay migration) [21] within several decades rather than by inefficient phytoextraction with plants [22,23,24]. Less contaminated cropland may be reserved for industrial, forage, or food crops whose hygienic deficits are non-critical [25,26] or negligible as in the case of grain crops with their strict indigenous HM control. Unlike the herbage, grains respond least to oversupply of soil minerals and nitrogen, and they stabilize their metallome inherently in a narrow range [27,28,29]. This was also reported for the FeZn content of soybean [30], rice [28], and pea [31], although the respective concentrations in vegetative tissues rose drastically. Similarly, variable regimes of fertilization had little impact on the seed content of fatty acids and cellulose in peanut [32], of amino acids and sugars in pea [33], and of starch and proteins in maize [34]. It is neither known how plants coordinate the uptake and shoot translocation of the required metal stock [35,36] nor is the “puzzle of seed filling” understood [37,38]. A “preset program of interacting genes and pathways” [34] then leads to the production of vigorous and stress-protected propagules almost irrespective of the extremes in the mineral stock of natural or contaminated soils [18,27].
The wealth of details describing the (putative) intervention of moleculargenetics in uptake and translocation of minerals from soil to seed e.g., [39,40,41] do not fall within the scope of this paper. Instead, the mineral distribution within the mature plant, its uptake control, and the ability to distinguish (micro)nutrients from chemically similar non-essential toxicants will be discussed.

2. Bottlenecks in Plant Mineral Flow

On their passage across the plant, trace mineral concentrations in general fall gradually and are highest in the root and lowest in the seed. Heavy-metal loads in whole grains of four wheat cvs. grown on comparatively mineral-poor soils thus ranged in the order of 10% (for both CdCr); 17%–25% (MnNi); and 40%–70% (CuPbZn) of those in the roots [42,43,44,45]. This indicated that food-quality cereals can be potentially obtained even from seriously metalliferous soils [46].
To prevent cell damage by the reaction of transition metal cations such as CuFeMnZn with oxygen species in the root symplast [47], the metals pass as neutral nicotianamine (NA) complexes [48,49]. They are then unloaded into the xylem as free cations or recomplexed with common ligands such as carboxylates, NA, histidine, and phytochelatins in dicots; with carboxylates and 2’-desoxymugineic acid in monocots; or as arsenite > arsenate and selenate metalloids, respectively (for reviews, e.g., [50,51,52]). At the base of cereal grains, the xylem transport is discontinuous [53]. The minerals therefore pass over, after further putative recomplexations [50], at peduncle and rachis of cereals into the phloem [54,55] to supply sink tissues of the shoot, leaves, and seeds. In the seed coat of the wheat grain, aleurone cells form a layer of the three to four cells highest in the content of FeZn [56], contact the starchy endosperm, and catalyze the mobilization of the storage polymers enzymatically upon germination [57]. Accordingly, Zn flow into wheat grains was seen to be blocked by two barriers located between the rachis and grain and between the maternal and filial tissues of the grain itself [58]. In pea, xylem fluids are loaded into the phloem of leaves, stipules, and pod walls [59]. Connected with the pod wall over the funiculus, the seed coat is furnished with phloem-derived minerals, sucrose, and amino acids. The compounds are unloaded into the liquid-filled intercellular space (apoplast) between seed coat and embryo to be taken up by the latter [60].
In order to locate bottlenecks in the plant mineral flow, several seed crops were consecutively grown on an 11-hectare gradient of geologically related soils Corg 3.5%–4% with a wide span of diminishing HM concentrations. The gradient had been formed by the inclusion of metalliferous overburden soil from uranium mining into non-contaminated cropland some decades ago [18,27]. Mineral concentrations exceeding the permissible limits for cropland reached 156 mg kg−1 DW in As, 41 mg kg−1 DW in Cd, 283 mg kg−1 DW in Cu, 2130 mg kg−1 DW in Mn, 150 mg kg−1 DW in Pb, 41 mg kg−1 DW in U, and 3005 mg kg−1 DW in Zn within the central gradient soil A. Figure 1 and Figure 2 and the associated Table 1 and Table 2 illustrate the breaks in the nutrient flow for minerals with similar modes of passage across mature plants of wheat and pea. Figure 3 and Table 3 illustrate striking similarities with the conditions in crop plants in the mineral flow across basidiomes of the wood-degrading mushroom Kuehneromyces mutabilis as a lower-plant saprobe. Mushrooms grew on leafwood sections embedded in sand, soil A, and a garden soil Corg 8.9%. Available mineral resources in Ca, K, and the essential trace minerals were up to 96%–99.9% located in the bed soils [61].
Displayed by the bell-shaped curves, concentrations in K (Figure 1 and Table 1) and CaKMg (Figure 2 and Table 2) essentially surpassed those in the roots and were drastically cut down to rest concentrations of 6.2%–55% on passage from rachis/pod wall to the seeds. In contrast, resources of the macronutrients MgP (Figure 1) and NP (Figure 2) persisted below those in the roots but rose to 184%–823% from rachis/pod to seeds. This mode of passage also applied to CaCoFeMnNiPb in K. mutabilis which enriched at rates of 150% (Fe) to 700% (Ni) at the gill/basidiospore interface.
In the heterogeneous group AsCdCuKMgPZn of the mushroom, most intermediate concentrations exceeded those in the lower stipe. Although cut down at the gill/spore interface to 24%–97% (Figure 3 and Table 3), AsCdMgPZn unlike CuK continued to exceed the concentrations in the lower stipe significantly.
The common feature of the micronutrients CuFeMnNiZn and the toxicants AsCdCrPbU in the crop plants was their poor transfer from root to shoot and their subsequent predominant decline (Figure 1 and Figure 2 and Table 1 and Table 2). Deviating from this mode, (As)CuFeMnNiZn were enriched in wheat from lower stem to rachis in preparation for their high demand in grains.
A comparison of the resulting seed and basidiospore metallomes with those of analogous crops from uranium mine gradient soils and with common hygiene guidelines for herbage comprises Table 4. The concentration spans represented by the wheat cvs. Akteur, Brilliant, and Bussard and the rye cv. Visello (“cereals”; [27]) matched with those of CaKMgP in wheat Asano, in the basidiospores (Table 1 and Table 3; [61]), and with MgP in pea. They were surpassed by CaK of pea (Table 2; [18]). The essential micronutrients CuFeMnNiZn of wheat and pea (Table 1 and Table 2) also matched with the limits drawn by Table 4 cereals and corresponded, apart from the elevated value of Zn in wheat, with the spans of ”normal plant concentrations.” Basidiospores were normal in Zn but elevated in FeNi > Mn > Cu whereby CuFeMn are co-factors of laccase and manganese peroxidase enzymes that are untypical of herbs [62]. Concentrations of AsCdPb in seeds and basidiospores (Table 1, Table 2 and Table 3) met the Table 4 ranges in cereals. While AsPb resources were negligible and concurred with the standards of food hygiene, Cd surpassed the respective limits.
In the mineral costume of the mature plant, the stock of trace elements in the lower stem of wheat had dropped to a mean of 7.8% relative to the root (Table 1). Whereas AsCdPbUZn concentrations thereby exceeded, and those of CuFeMnNi fell short of the target level in the grain (Table 1), all the minerals but PbU were enriched in the direction of the upper stem (by a mean of 176%) and the rachis (157%). They were then cut down at the rachis/grain interface to 1.6%–12% (AsPbUZn) or up-regulated to 106% (Mn) and 225% (Cu) within a common mean of 65.4%. Interventions into the mineral flow are thus by far more drastic at the interface of the root and the lower stem but do not yet reflect the proportions in the mature seed. Mineral excesses (CaFeKZn) and deficits (CuMgP) expressed in the upper 12-cm sections of the stem (Table 1) vary greatly with the soil fertilization regime [63,64]. In confining its impact on the narrow and preset target metallome of the seed, the rachis/grain interface plays a unique and astonishingly versatile part. The metallomes of pea seeds and even those of fungal basidiospores were controlled accordingly (Table 2 and Table 3).

3. The Adopted Seed Metallome in Correspondence with the Geochemical Environment

Data sets of Table 4 reflect the cultivation of three wheat and single rye and pea cvs. on three metalliferous uranium mine gradient soils. Reference crops were grown on garden soil and alluvial sand, which represented HM loads at the lower range of arable soils (Table 4; [18,27]). Concentrations of essential and non-essential minerals of the seeds varied much less than those in the soils. Respective concentration spans of 9–35× in CuFeMn(Ni) shrank to 1.3–2× in the seeds. Wide variations in Zn (109 to 2.13×) and Cd (475 to 15.9×) were more efficiently out-regulated by pea than by cereals. Potential health problems linked with the repressed uptake of As(Cd)Pb [38,65,66] and amplified by the concerted action of other HM [19] were subsequently minimized and excluded (Table 4). The grain deposition in BaCs evoking concern by the presence of their radioisotopes deviated from this general mode. The concentration spans in seeds surpassed those in different sets of soils permanently [18].
Owing to the flexibility of the rachis/pod to seed interface, seed crops compensated for the drastic variations in the soil mineral load by down-regulation of the seed:soil transfer factors (TFs) on high-concentrated soils and their up-regulation on low-concentrated soils to reach a narrow and preset plateau concentration span (Figure 4). Viable seeds were thus equipped with an optimum but not the maximum of essential minerals [18,27] in the range of “normal plant concentrations” (Table 4; [7,68]) rather than with non-essential toxicants. This ensures the metal-stress-free development of the germling until it starts interacting with the soil solution. On several test soils, the seed metallomes of most crop plants surpassed the variability ranges of ≤2× in CdZn (Table 4; Figure 4 and Figure 6).
Pea expressively reached the concentrations of the apparent target metallome on the organic- and extremely mineral-poor alluvial sand (Corg 1.97%). In the absence of the dominating humic-acid ligands which are notorious for the organic-rich soils, alluvial sand was dominated by the highly plant-available free metal cations and metal-organic-acid complexes of highest water-solubility [18,27]. Failures to reach the target seed concentration may thus correlate with low plant availabilities of minerals in the respective soils.
Approaching plateau concentration spans in seed crops with their cultivar-specific variation is evidently the result of polygenic interactions [70,71]. The concentrations in the nutritionally essential FeZn range by factors 2–2.6× in bean, 3.3–4× in rice, 2× in wheat, and around 1.5× in maize seeds [72,73]. Respective differences, e.g., in wheat, may result from long-term adaptations to the local geochemistry rather than to closer relationships with diploid and tetraploid high FeZn wheat species such as ssp. boeoticum and dicoccoides (178/159 mg kg−1 DW in Zn) [74]. Comparable long-term adaptations are strongly suggested by the seed’s Ni content of up to 4800 mg kg−1 from the Ni hyperaccumulator Alyssum lesbiacum endemic to serpentine soils [75]. Moreover, the inherent degree of Ni hyperaccumulation in different A. lesbiacum accessions varied with the Ni content of their local soils [76] indicating that the regional within-species variations as studied for the shoot Zn of plants are actually in part an evolutionary trait [77].
It is then not surprising that mineral concentrations needed by herbivores (Table 4) [10,13] have also been adapted to the order of those considered normal by plants [7,68] and adequate for seed germination in the given geochemical environment [27,78]. Seed concentrations in KMgP rather than in Ca corresponded with the need of monogastric animals (horse, swine, chicken) and ruminants (beef and dairy cattle, sheep). Pretensions in CuFeMnNiZn coincided, too. Of the non-essential toxicants AsCdPb, non-tolerable concentrations of Cd in cereals were confined to soils reaching 40 mg kg−1, whereas AsPb levels in seeds remained marginal (Table 4). According to the illustration for Cu (Figure 5), concentrations in wheat, rye, and pea seeds as well as the pretensions of herbivores matched predominantly with the lower range of Cu in herbs grown on non- and severely contaminated soils [10,18,27]. They thereby surpassed the putative minimum demand for Cu required for vigorous plant growth [13].

4. Discrimination of Essential and Non-Essential Elements Masked by Chemical Similarities

As reviewed by Gramss and Voigt [18], plants express hyperaccumulator and metal tolerance properties in adaptation to elevated soil concentrations of essential (CuNiZn) and non-essential (AsCdCrPb) trace minerals [35,36,75,79]. They do not seem to identify those of physiological insignificance in order to block up their acquisition via transmembrane transport proteins. Proteins acting as ligands are imperfect in the steric selection of metal cations [80]. It is thus the relative affinity of the metal cation itself that regulates the formation of protein complexes in the stability range CuZn > NiCo > Fe2+Mn > CaMg [81]. It has not yet been stated whether the respective affinities stand at least in part for quantitative differences in the non-selective (root) uptake of essential and non-essential trace minerals. Specific transporters for non-essential metals such as CdPb are not known. These metals pass cell membranes via ZIP family (Zinc/iron permease), DMT1 (Divalent metal transporters), and P-type ATPase transport proteins, preventing essential elements from reaching their physiological optima [82]. Arsenite (AsO33−) passes aquaglyceroporins with glycerol, urea, and water [82], whereas arsenate (AsO43−) as phosphate (PO43−) analog uses the phosphate transporters Pht1;1 and Pht1;4, e.g., in Arabidopsis thaliana [83]. Selective uptake of Cd versus Fe2+MnZn by the ZIP family transporter IRT1 is complicated as its electron configuration and the preference for phytochelatins and histidine ligands coincide with those of Zn [38]. In addition, Cd shares its preference for thiols with further non-essential metals that can then pass as unsplit complexes via amino acid and cation/anion transporters [84]. Moreover, the ubiquitous membrane-voltage-independent non-selective cation channels (VI-NSCCs) give room to the passive and non-selective transmembrane flow of Cs+Hg+K+Na+NH4+ and the divalent cations of CaCdMgMnPbZn [85]. Root uptake of Fe2+Mn2+ by wheat as a strategy-II plant proceeds by the immediate uptake via ZRT- and IRT-like proteins (ZIPs) or as Fe(III)-phytosiderophores by yellow-stripe-like (YSL) transporters [86]. Is then the plant prepared to perceive the ingress of a particular (non-essential) element and to denote its presence with an element-specific and unique signal?
Metal cations such as Cd2+ induce NADPH oxidase activity in contacted cell membranes and a rise in the production of reactive oxygen species (ROS) [87] that damage cellular components such as lipids, proteins, carbohydrates, and DNA [88,89,90,91]. ROS incited signals expressed in formation and modulation of mitogen-activated protein kinases (MAPKs), Ca2+/calmodulins, nitric oxide, and the common plant hormones alter nuclear gene expression and the formation of cation-neutralizing chelants to control the cellular redox status [92,93,94,95].
Nevertheless, similar plant signaling responses specifically attributable to the presence of a unique (non-essential) element are poorly documented. In rice roots, Cd2+ and Cu2+ induced identical MAP kinase activities via distinct ROS-generating systems [96]. In roots of alfalfa seedlings, Cd2+ and Cu2+ provoked different cellular signaling mechanisms by the induction of distinct MAPK variants [97]. Cu exposed to Arabidopsis thaliana roots led by activation of NADPH oxidases and Fenton reactions to the production of H2O2 that triggered signaling activities by MAPK and oxylipin. In contrast, oxidative signaling was the sole response by root exposure to Cd [90]. Arabidopsis thaliana grown on an agar medium amended with 100 µM CdPb contained 0.6/0.15 µM of the toxicants. The rates of up-/down-regulated genes amounted to 65/338 and 19/76 in the Cd and Pb treatment, respectively, with half the genes responding likewise to both Pb and Cd treatment [98]. In Deschampsia cespitosa roots exposed to Ni, concentrations of cytokinins and abscisic acid did not change whereas the content of nicotianamine increased. Exposure to Cd caused increase in phytochelatins and abscisic acid but reduction in the content of cytokinins [95].
The random plant uptake of minerals which are termed non-essential at the current evolutionary state may be excused for their cell membrane passage in chemical resemblance to, or in company of, essential elements [38,82,84,85]. Several data, however, contradict the impression that plants discriminate minerals insufficiently. In Chinese cabbage (Brassica chinensis L.) treated with NH4Cl, shoot concentrations in (metallo) proteins (Norg) and in the protein-associated group of (Cd)CoCuMnNiZn rose concomitantly by factors of 3.4–3.7. Uptake of non-essentials such as AlBaCrLiPbTiUV diminished or failed to surpass the factor 1.2×. This was due to their predominant lack in affinities to proteinaceous ligands and their relative dilution in a biomass propagated by the nitrogen treatment [99]. Seeds determined to persist in the current geochemical environment were actively equipped with out-regulated, optimized, and tolerable concentrations of both essential and non-essential minerals including the toxicants AsCdPb (Figure 1, Figure 2 and Figure 4; Table 1, Table 2 and Table 4; [18,27]. Of the arsenate (As(V)) entering via phosphate transporters [83], >90% passed the xylem of the hyperaccumulator Pteris vittata as arsenite (As(III)) [79] and could not be distinguished from phosphate by the respective aquaporin transporters [100]. Nevertheless, data from Figure 6 show that seed:soil TFs in As and P given for pea differed in the absolute values heading the columns; these absolute values divided by the respective soil concentrations also differed drastically.
Both in wheat and pea, the differences in the passages of As/P from roots to the rachis/pod interfaces were less pronounced but terminated in drastic and mineral-specific down-/up-regulations upon seed filling (Figure 1 and Figure 2; Table 1 and Table 2). The respective passages of Cd/Zn also ended with individual differences in their rates of cut-down to the seeds. Soil-A-grown grains of the wheat cvs. Akteur, Brilliant, Bussard, Asano, and the rye cv. Visello then contained 78/61/96/89/120 times less Cd than Zn [27].
As discussed by Gramss and Voigt [18], the issue of why plants incorporate non-essentials actively remains subject to speculation. Experience with the respective pathways could help plants such as couch grass (Agropyron repens L.) tolerate and colonize regions of normally lethal toxic imissions around metal smelters within a few decades [101]. Clemens [102] explains the current rating of chemically similar elements as essential or non-essential with evolutionary adaptations of living organisms to those of higher abundance in the earth’s crust. This could imply that the physiological activities of “non-essential” elements situated in the nanomolar range might have been overlooked. Maintaining ruminants on feeds < 4 µg kg−1 DW of Cd may result in growth depression and higher mortality rates in their offspring. Diets of 14 µg kg−1 led to higher weight gain [103]. Respective experiments indicating the essentiality of low CdPb doses for health and development of animals go back to the nineteen seventies [104].

5. Conclusion

Soil concentrations ranging 9–109× in CuFeMnNiZn shrank to spans of 1.3–2× in seeds to mark the order of their adopted target mineral load (Table 4; Figure 4) and the stability of their inherent metallome in the presence of soil mineral extremes. This regulatory process comprised the initiation of the phloem-to-seed mineral transfer at anthesis and its sensing and termination by unknown back-coupling (feedback) mechanisms as soon as the target mineral load had been reached. The big green-plant seeds of cereals and peas and the 7-µm basidiospores of the lower-plant saprobe K. mutabilis (Table 1, Table 2 and Table 3) were concerned likewise. Approaches to the genetically fixed seed target metallome were based on proportionate up-regulations of the seed:soil mineral transfer factors on low-concentrated soils, and their down-regulation on high-concentrated soils (compare Figure 4 and Figure 6). Non-essential elements were actively incorporated in the same way. Mineral concentrations in the phloem- (and cytoplasmic-stream) draining tissues of rachis, pea pod, and mushroom gill as well as in the remaining sections of the plants, deviated considerably and irregularly from those of the propagules’ target metallome (Table 1, Table 2 and Table 3). This may also bear true for the phloem composition whose dependence on changes in the soil mineral stock, the rate of soil water supply, and the plant’s transpiration rate are not documented. Phloem extracted from wheat plants by aphids, a treatment known as aphid stylectomy, showed increases in MgZn to 190% and reductions in K to 50% in samples taken 1–2 to 17–21 day after anthesis. Concentrations of Fe did not change [105]. The total concentrations in phloem samples persisted below those in mature grains (Table 4) [105]. In the phloem of five pea cvs., concentrations of 22 amino acids were ranged 1.4–3 times [106]. Contemplating these variations, one can not presume that the percentage proportions between phloem constituents are congruent with, or immediately determine those, of the fed grain. This means grain fill could not end with the non-selective incorporation of the constituents introduced, e.g., by 10 mL of phloem. Seed filling out of the phloem may thus imply the identification of its essential and non-essential minerals (as well as organics) and their selective and individual transfer to the propagule to constitute its target composition. The extreme numerical variation in the seed:soil transfer factors (Figure 4 and Figure 6); [18,27] of plants from mineral-rich and poor soils may therefore be pretended, i.e., the “transfer factors” phloem:soil could be much smaller. The huge numerical transfer factors may then be reached when the required absolute amounts, e.g., of As and Cu (Figure 4 and Figure 6) are selectively transferred from the variably concentrated phloem of plants from rich and poor soils to the seed. In explaining this analytical and strategic top performance, gene-RNA interferences (RNAi) [40,107] alone may contribute to shape the seed metallome, but they may not represent the unknown principle which is active in the coordination of the mineral homeostasis. It is concluded that seed crops with their stable metallome can be obtained from severely mineral-poor and metalliferous soils whose permissible HM loads can even be considerably expanded in AsCdCuMnUZn [18,108]. This implies that seed crops reduce the pressure on the quality of detoxification of non-remediable metalliferous croplands. In optimizing the plant-soil partnership, actively selected and bred food and forage crops should be provided whose uptake/excluder profile, including the Zn/Cd proportion, should be certified for clay-loam and sandy soils under standard conditions. The quality of the resulting crop must be substantiated in a local case study.

Author Contributions

In this cooperative work, Gerhard Gramss primarily conducted the agricultural part, whereas Klaus-Dieter Voigt performed the mineral analyses. The script was elaborated in mutual consultation.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Graham, R.; Senadhira, D.; Beebe, S.; Iglesias, C.; Monasterio, I. Breeding for micronutrient density in edible portions of staple food crops: Conventional approaches. Field Crops Res. 1999, 60, 57–80. [Google Scholar] [CrossRef]
  2. Hernández Rodríguez, L.; Morales, D.A.; Rodríguez Rodríguez, E.; Díaz Romero, C. Minerals and trace elements in a collection of wheat landraces from the Canary Islands. J. Food Compos. Anal. 2011, 24, 1081–1090. [Google Scholar] [CrossRef]
  3. Alloway, B.J. Soil factors associated with zinc deficiency in crops and humans. Environ. Geochem. Health 2009, 31, 537–548. [Google Scholar] [CrossRef] [PubMed]
  4. Singh, M.V. Micronutrient deficiencies in crops and soils in India. In Micronutrient Deficiencies in Global Crop Production; Alloway, B.J., Ed.; Springer: Dordrecht, The Netherlands, 2008; pp. 93–126. [Google Scholar]
  5. Sillanpää, M. Micronutrient Assessment at Country Level: An International Study; FAO Soils Bulletin No. 63; The Food and Agriculture Organization of the United Nations (FAO): Rome, Italy, 1990. [Google Scholar]
  6. Groenenberg, J.E.; Römkens, P.F.A.M.; Comans, R.N.J.; Luster, J.; Pampura, T.; Shotbolt, L.; Tippin, E.; de Vries, W. Transfer functions for solid-solution partitioning of cadmium, copper, nickel, lead and zinc in soils: Derivation of relationships for free metal ion activities and validation with independent data. Eur. J. Soil Sci. 2010, 61, 58–73. [Google Scholar] [CrossRef]
  7. Schachtschabel, P.; Blume, H.P.; Brümmer, G.; Hartge, K.H.; Schwertmann, U. Lehrbuch der Bodenkunde, 14th ed.; Enke: Stuttgart, Germany, 1998. [Google Scholar]
  8. Sperotto, R.A.; Boff, T.; Duarte, G.L.; Santos, L.S.; Grusak, M.A.; Fett, J.P. Identification of putative target genes to manipulate Fe and Zn concentrations in rice grains. J. Plant Physiol. 2010, 167, 1500–1506. [Google Scholar] [CrossRef] [PubMed]
  9. Wissuwa, M.; Ismail, A.M.; Graham, R.D. Rice grain zinc concentrations as affected by genotype, native soil-zinc availability, and zinc fertilization. Plant Soil 2008, 306, 37–48. [Google Scholar] [CrossRef]
  10. McDowell, L.R. Minerals in Animal and Human Nutrition, 2nd ed.; Elsevier Science: Amsterdam, The Netherlands, 2003. [Google Scholar]
  11. Gupta, U.C.; Gupta, S.C. Sources and Deficiency Diseases of Mineral Nutrients in Human Health and Nutrition: A Review. Pedosphere 2014, 24, 13–38. [Google Scholar] [CrossRef]
  12. Yang, X.E.; Chen, W.R.; Feng, Y. Improving human micronutrient nutrition through bio-fortification in the soil-plant system: China as a case study. Environ. Geochem. Health 2007, 29, 413–428. [Google Scholar] [CrossRef] [PubMed]
  13. Kirchmann, H.; Mattsson, L.; Eriksson, J. Trace element concentration in wheat grain: Results from the Swedish long-term soil fertility experiments and national monitoring program. Environ. Geochem. Health 2009, 31, 561–571. [Google Scholar] [CrossRef] [PubMed]
  14. Marschner, H. Mineral Nutrition of Higher Plants, 2nd ed.; Academic: London, UK, 1995. [Google Scholar]
  15. Dushenkov, S. Trends in phytoremediation of radionuclides. Plant Soil 2003, 249, 167–175. [Google Scholar] [CrossRef]
  16. European Communities. Council regulation (EC) No. 1881/2006 of December 2006 on setting maximum levels of certain contaminants in foodstuffs. Off. J. Eur. Communities L Ser. 2006, 364, 5–24. [Google Scholar]
  17. Wuana, R.A.; Okieimen, F.E. Heavy metals in contaminated soils: A review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol. 2011, 2011, 402647. [Google Scholar] [CrossRef]
  18. Gramss, G.; Voigt, K.-D. Regulation of the mineral concentrations in pea seeds from uranium mine and reference soils diverging extremely in their heavy metal load. Sci. Hort. 2015, 194, 255–266. [Google Scholar] [CrossRef]
  19. Huang, M.; Zhou, S.; Sun, B.; Zhao, Q. Heavy metals in wheat grain: Assessment of potential health risk for inhabitants in Kunshan, China. Sci. Total Environ. 2008, 405, 54–61. [Google Scholar] [CrossRef] [PubMed]
  20. Alloway, B.J.; Ayres, D.C. Chemical Principles of Environmental Pollution; Chapman and Hall: London, UK, 1993. [Google Scholar]
  21. Gramss, G.; Voigt, K.-D. The legacy of uranium mining: Farming on non-remediable soils? In Uranium: Sources, Exposure and Environmnetal Effects; Nelson, J.R., Ed.; Novapublishers: New York, NY, USA, 2015; pp. 21–52. [Google Scholar]
  22. Duquène, L.; Vandenhove, H.; Tack, F.; Meers, E.; Baeten, J.; Wannijn, J. Enhanced phytoextraction of uranium and selected heavy metals by Indian mustard and ryegrass using biodegradable soil amendments. Sci. Total Environ. 2009, 407, 1496–1505. [Google Scholar] [CrossRef] [PubMed]
  23. Evangelou, M.W.H.; Ebel, M.; Schaeffer, A. Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 2007, 68, 989–1003. [Google Scholar] [CrossRef] [PubMed]
  24. Gramss, G.; Voigt, K.-D. Forage and rangeland plants from uranium mine soils: Long-term hazard to herbivores and livestock? Environ. Geochem. Health 2014, 36, 441–452. [Google Scholar] [CrossRef] [PubMed]
  25. Klang-Westin, E.; Eriksson, J. Potential of Salix as phytoextractor for Cd on moderately contaminated soils. Plant Soil 2003, 249, 127–137. [Google Scholar] [CrossRef]
  26. Meers, E.; Lamsal, S.; Vervaeke, P.; Hopgood, M.; Lust, N.; Tack, F.M.G. Availability of heavy metals for uptake by Salix viminalis on a moderately contaminated dredged sediment disposal site. Environ. Pollut. 2005, 137, 354–364. [Google Scholar] [CrossRef] [PubMed]
  27. Gramss, G.; Voigt, K.-D. Regulation of heavy metal concentrations in cereal grains from uranium mine soils. Plant Soil 2013, 364, 105–118. [Google Scholar] [CrossRef]
  28. Stomph, T.J.; Jiang, W.; Van Der Putten, P.E.L.; Struik, P.C. Zinc allocation and re-allocation in rice. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
  29. Xue, Y.-F.; Yue, S.-C.; Zhang, Y.-Q.; Cui, Z.-L.; Chen, X.-P.; Yang, F.-C.; Cakmak, I.; McGrath, S.P.; Zhang, F.-S.; Zou, C.-Q. Grain and shoot zinc accumulation in winter wheat affected by nitrogen management. Plant Soil 2012, 361, 153–163. [Google Scholar] [CrossRef]
  30. Vasconcelos, M.W.; Clemente, T.E.; Grusak, M.A. Evaluation of constitutive iron reductase (AtFRO2) expression on mineral accumulation and distribution in soybean (Glycine max L.). Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
  31. Grusak, M.A. Iron transport to developing ovules of Pisum sativum. (I. Seed import characteristics and phloem iron-loading capacity of source regions). Plant Physiol. 1994, 104, 649–655. [Google Scholar] [PubMed]
  32. Osuji, G.O.; Brown, T.K.; South, S.M.; Duncan, J.C.; Johnson, D.; Hyllam, S. Molecular adaptation of peanut metabolic pathways to wide variations of mineral ion composition and concentration. Am. J. Plant Sci. 2012, 3, 33–50. [Google Scholar] [CrossRef]
  33. Grusak, M.; Emerick, J. Dynamics of Dry Matter and Mineral Allocation to Pod Walls versus Seeds in Common Bean; Meeting Abstract; Southern Plains Area Home/Children’s Nutrition Research Center: Houston, TX, USA, 2012. [Google Scholar]
  34. Wu, Y.; Messing, J. Proteome balancing of the maize seed for higher nutritional value. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
  35. Krämer, U.; Talke, I.N.; Hanikenne, M. Transition metal transport. FEBS Lett. 2007, 581, 2263–2272. [Google Scholar] [CrossRef] [PubMed]
  36. Xing, J.P.; Jiang, R.F.; Ueno, D.; Ma, J.F.; Schat, H.; McGrath, S.P.; Zhao, F.J. Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytol. 2008, 178, 315–325. [Google Scholar] [CrossRef] [PubMed]
  37. Grillet, L.; Mari, S.; Schmidt, W. Iron in seeds-loading pathways and subcellular localization. Front. Plant Sci. 2014, 4. [Google Scholar] [CrossRef] [PubMed]
  38. Khan, M.A.; Castro-Guerrero, N.; Mendoza-Cozatl, D.G. Moving toward a precise nutrition: Preferential loading of seeds with essential nutrients over non-essential toxic elements. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
  39. Bashir, K.; Ishimaru, Y.; Nishizawa, N.K. Molecular mechanisms of zinc uptake and translocation in rice. Plant Soil 2012, 361, 189–201. [Google Scholar] [CrossRef]
  40. Paul, S.; Datta, S.K.; Datta, K. miRNA regulation of nutrient homeostasis in plants. Front. Plant Sci. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
  41. Waters, B.M.; Sankaran, R.P. Moving micronutrients from the soil to the seeds: Genes and physiological processes from a biofortification perspective. Plant Sci. 2011, 180, 562–574. [Google Scholar] [CrossRef] [PubMed]
  42. Barman, S.C.; Sahu, R.K.; Bhargava, S.K.; Chaterjee, C. Distribution of heavy metals in wheat, mustard, and weed grown in field irrigated with industrial effluents. Bull. Environ. Contam. Toxicol. 2000, 64, 489–496. [Google Scholar] [CrossRef] [PubMed]
  43. Bose, S.; Bhattacharyya, A.K. Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 2008, 70, 1264–1272. [Google Scholar] [CrossRef] [PubMed]
  44. Liu, W.-X.; Liu, J.-W.; Wu, M.-Z.; Li, Y.; Zhao, Y.; Li, S.-R. Accumulation and translocation of toxic heavy metals in winter wheat (Triticum aestivum L.) growing in agricultural soil of Zhengzhou, China. Bull. Environ. Contam. Toxicol. 2009, 82, 343–347. [Google Scholar] [CrossRef] [PubMed]
  45. Mishra, M.; Sahu, R.K.; Sahu, S.K.; Padhy, R.N. Growth, yield and elements content of wheat (Triticum aestivum) grown in composted municipal solid wastes amended soil. Environ. Dev. Sustain. 2009, 11, 115–126. [Google Scholar] [CrossRef]
  46. Il’in, V.B. Heavy metals in the soil-crop system. Eurasian Soil Sci. 2007, 40, 993–999. [Google Scholar] [CrossRef]
  47. Briat, J.F.; Fobisloisy, I.; Grignon, N.; Lobreaux, S.; Pascal, N.; Savino, N.; Thoiron, S.; Vonwiren, N.; Vanwuytswinkel, O. Cellular and molecular aspects of iron metabolism in plants. Biol. Cell 1995, 84, 69–81. [Google Scholar] [CrossRef]
  48. Deinlein, U.; Weber, M.; Schmidt, H.; Rensch, S.; Trampczynska, A.; Hansen, T.H.; Husted, S.; Schjoerring, J.K.; Talke, I.N.; Krämer, U.; et al. Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 2012, 24, 708–723. [Google Scholar] [CrossRef] [PubMed]
  49. Stephan, U.W.; Schmidke, I.; Stephan, V.W.; Scholz, G. The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. BioMetals 1996, 9, 84–90. [Google Scholar] [CrossRef]
  50. Álvarez-Fernández, A.; Díaz-Benito, P.; Abadía, A.; López-Millán, A.-F.; Abadía, J. Metal species involved in long distance metal transport in plants. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
  51. Callahan, D.L.; Baker, A.J.M.; Kolev, S.D.; Wedd, A.G. Metal ion ligands in hyperaccumulating plants. J. Biol. Inorg. Chem. 2006, 11, 2–12. [Google Scholar] [CrossRef] [PubMed]
  52. Gramss, G.; Bergmann, H. Impact of soil applications of sand, compost and nitrogen on uptake of trace elements by Chinese cabbage. J. Nat. Sci. Sustain. Technol. 2013, 7, 1–28. [Google Scholar]
  53. Stomph, J.T.; Jiang, W.; Struik, P.C. Zinc biofortification of cereals: Rice differs from wheat and barley. Trends Plant Sci. 2009, 14, 123–124. [Google Scholar] [CrossRef] [PubMed]
  54. Herren, T.; Feller, U. Transfer of zinc from xylem to phloem in the peduncle of wheat. J. Plant Nutr. 1994, 17, 1587–1598. [Google Scholar] [CrossRef]
  55. Pearson, J.N.; Rengel, Z.; Jenner, C.F.; Graham, R.D. Transport of zinc and manganese to developing wheat grains. Physiol. Plant. 1995, 95, 449–455. [Google Scholar] [CrossRef]
  56. Borrill, P.; Connorton, J.M.; Balk, J.; Miller, A.J.; Sanders, D.; Uauy, C. Biofortification of wheat grain with iron and zinc: Integrating novel genomic resources and knowledge from model crops. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
  57. Burton, R.A.; Fincher, G.B. Evolution and development of cell walls in cereal grains. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
  58. Wang, Y.X.; Specht, A.; Horst, W.J. Stable isotope labelling and zinc distribution in grains studied by laser ablation ICP-MS in an ear culture system reveals zinc transport barriers during grain filling in wheat. New Phytol. 2011, 189, 428–437. [Google Scholar] [CrossRef] [PubMed]
  59. Grusak, M.A.; Pearson, J.N.; Marentes, E. The physiology of micronutrient homeostasis in field crops. Field Crops Res. 1999, 60, 41–56. [Google Scholar] [CrossRef]
  60. Van Dongen, J.T.; Ammerlaan, A.M.H.; Wouterlood, M.; Van Aelst, A.C.; Borstlap, A.C. Structure of the developing pea seed coat and the post-phloen transport pathway of nutrients. Ann. Bot. 2003, 91, 729–737. [Google Scholar] [CrossRef] [PubMed]
  61. Gramss, G.; Voigt, K.-D. Clues for regulatory processes in fungal uptake and transfer of minerals to the basidiospore. Biol. Trace Elem. Res. 2013, 154, 140–149. [Google Scholar] [CrossRef] [PubMed]
  62. Gramss, G. Potential contributions of oxidoreductases from alfalfa plants to soil enzymology and biotechnology: A review. J. Nat. Sci. Sustain Technol. 2012, 6, 169–223. [Google Scholar]
  63. Aciksoz, S.B.; Yazici, A.; Ozturk, L.; Cakmak, I. Biofortification of wheat with iron through soil and foliar application of nitrogen and iron fertilizers. Plant Soil 2011, 349, 215–225. [Google Scholar] [CrossRef]
  64. Kutman, U.B.; Yildiz, B.; Cakmak, I. Effect of nitrogen on uptake, remobilization and partitioning of zinc and iron throughout the development of durum wheat. Plant Soil 2011, 342, 149–164. [Google Scholar] [CrossRef]
  65. Ali, H.; Khan, E.; Sajad, M.A. Phytoremediation of heavy metals–Concepts and applications. Chemosphere 2013, 91, 869–881. [Google Scholar] [CrossRef] [PubMed]
  66. World Health Organization. Drinking Water Guidelines for Drinking Water Quality, 4th ed.; WHO: Geneva, Switzerland, 2011. [Google Scholar]
  67. Bowen, H.J.M. Environmental Chemistry of the Elements; Academic: London, UK, 1979. [Google Scholar]
  68. Auermann, E.; Dässler, H.-G.; Jacobi, J.; Cumbrowski, J.; Meckel, U. Untersuchungen zum Schwermetallgehalt von Getreide und Kartoffeln. Die Nahrung 1980, 24, 925–937. [Google Scholar] [CrossRef] [PubMed]
  69. Commission of the European Communities Directive EC 466/2001. Setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Comm. L Ser. 2001, 77, 1–13. [Google Scholar]
  70. Ghandilyan, A.; Vreugdenhil, D.; Aarts, M.G.M. Progress in the genetic understanding of plant iron and zinc nutrition. Physiol. Plant. 2006, 126, 407–417. [Google Scholar] [CrossRef]
  71. Grusak, M.A.; DellaPenna, D. Improving the nutrient composition of plants to enhance human nutrition and health. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 133–161. [Google Scholar] [CrossRef] [PubMed]
  72. House, W.A.; Welch, R.M.; Beebe, S.; Cheng, Z. Potential for increasing the amounts of bioavailable zinc in dry beans (Phaseolus vulgaris L) through plant breeding. J. Sci. Food Agric. 2002, 82, 1452–1457. [Google Scholar] [CrossRef]
  73. Welch, R.M.; Graham, R.D. Breeding for micronutrients in staple food crops from a human nutrition perspective. J. Exp. Bot. 2004, 55, 353–364. [Google Scholar] [CrossRef] [PubMed]
  74. Cakmak, I.; Ozkan, H.; Braun, H.J.; Welch, R.M.; Romheld, V. Zinc and iron concentrations in seeds of wild, primitive, and modern wheat. Food Nutr. Bull. 2000, 21, 401–403. [Google Scholar] [CrossRef]
  75. Adamidis, G.C.; Aloupi, M.; Kazakou, E.; Dimitrakopoulos, P.G. Intra-specific variation in Ni tolerance, accumulation and translocation patterns in the Ni-hyperaccumulator Alyssum lesbiacum. Chemosphere 2014, 95, 496–502. [Google Scholar] [CrossRef] [PubMed]
  76. Kazakou, E.; Adamidis, G.C.; Baker, A.J.M.; Reeves, R.D.; Godino, M.; Dimitrakopoulos, P.G. Species adaptation in serpentine soils in Lesbos Island (Greece): Metal hyperaccumulation and tolerance. Plant Soil 2010, 332, 369–385. [Google Scholar] [CrossRef]
  77. Broadley, M.R.; White, P.J.; Hammond, J.P.; Zelko, I.; Lux, A. Zinc in plants. New Phytol. 2007, 173, 677–702. [Google Scholar] [CrossRef] [PubMed]
  78. White, P.J.; Veneklaas, E.J. Nature and nurture: The importance of seed phosphorus content. Plant Soil 2012, 357, 1–8. [Google Scholar] [CrossRef]
  79. Wang, X.; Ma, L.Q.; Rathinasabapathi, B.; Cai, Y.; Liu, Y.G.; Zeng, G.M. Mechanisms of efficient arsenite uptake by arsenic hyperaccumulator Pteris vittata. Environ. Sci. Technol. 2011, 45, 9719–9725. [Google Scholar] [CrossRef] [PubMed]
  80. Waldron, K.J.; Rutherford, J.C.; Ford, D.; Robinson, N.J. Metalloproteins and metal sensing. Nature 2009, 460, 823–830. [Google Scholar] [CrossRef] [PubMed]
  81. Irving, H.; Williams, R.J.P. Order of stability of metal complexes. Nature 1948, 162, 746–747. [Google Scholar] [CrossRef]
  82. Martinez-Finley, E.J.; Chakraborty, S.; Fretham, S.J.B.; Aschner, M. Cellular transport and homeostasis of essential and nonessential metals. Metallomics 2012, 4, 593–605. [Google Scholar] [CrossRef] [PubMed]
  83. Shin, H.; Shin, H.S.; Dewbre, G.R.; Harrison, M.J. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low-and high-phosphate environments. Plant J. 2004, 39, 629–642. [Google Scholar] [CrossRef] [PubMed]
  84. Zalups, R.K.; Ahmad, S. Molecular handling of cadmium in transporting epithelia. Toxicol. Appl. Pharmacol. 2003, 186, 163–188. [Google Scholar] [CrossRef]
  85. Demidchik, V.; Maathuis, F.J.M. Physiological roles of nonselective cation channels in plants: From salt stress to signalling and development. New Phytol. 2007, 175, 387–404. [Google Scholar] [CrossRef] [PubMed]
  86. Sperotto, R.A.; Ricachenevsky, F.K.; Waldow, V.D.; Fett, J.P. Iron biofortification in rice: It’s a long way to the top. Plant Sci. 2012, 190, 24–39. [Google Scholar] [CrossRef] [PubMed]
  87. Cakmak, I. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 2000, 146, 185–205. [Google Scholar] [CrossRef]
  88. Gill, S.S.; Narendra Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef] [PubMed]
  89. Hossain, M.A.; Piyatida, P.; Teixeira da Silva, J.A.; Fujita, M. Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012, 2012, 872875. [Google Scholar] [CrossRef]
  90. Opdenakker, K.; Remans, T.; Keunen, E.; Vangronsveld, J.; Cuypers, A. Exposure of Arabidopsis thaliana to Cd or Cu excess leads to oxidative stress mediated alterations in MAP kinase transcript levels. Environ. Exp. Bot. 2012, 83, 53–61. [Google Scholar] [CrossRef]
  91. Viehweger, K. How plants cope with heavy metals. Available online: http://www.as-botanicalstudies.com/content/55/1/35 (accessed on 29 May 2015).
  92. Chmielowska-Bąk, J.; Gzyl, J.; Rucińska-Sobkowiak, R.; Arasimowicz-Jelonek, M.; Deckert, J. The new insights into cadmium sensing. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef]
  93. DalCorso, G.; Manara, A.; Furini, A. An overview of heavy metal challenge in plants: From roots to shoots. Metallomics 2013, 5, 1117–1132. [Google Scholar] [CrossRef] [PubMed]
  94. Gallego, S.M.; Pena, L.B.; Barcia, R.A.; Azpilicueta, C.E.; Iannone, M.F.; Rosales, E.P.; Zawoznik, M.S.; Groppa, M.D.; Benavides, M.P. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ. Exp. Bot. 2012, 83, 33–46. [Google Scholar] [CrossRef]
  95. Hayward, A.R.; Coates, K.E.; Galer, A.L.; Hutchinson, T.C.; Emery, R.J.N. Chelator profiling in Deschampsia cespitosa (L.) Beauv. reveals a Ni reaction, which is distinct from the ABA and cytokinin associated response to Cd. Plant Physiol. Biochem. 2013, 64, 84–91. [Google Scholar] [CrossRef] [PubMed]
  96. Yeh, C.M.; Chien, P.S.; Huang, H.J. Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J. Exp. Bot. 2007, 58, 659–671. [Google Scholar] [CrossRef] [PubMed]
  97. Jonak, C.; Nakagami, H.; Hirt, H. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol. 2004, 136, 3276–3283. [Google Scholar] [CrossRef] [PubMed]
  98. Kovalchuk, I.; Titov, V.; Hohn, B.; Kovalchuk, O. Transcriptome profiling reveals similarities and differences in plant responses to cadmium and lead. Mutat. Res. 2005, 570, 149–161. [Google Scholar] [CrossRef] [PubMed]
  99. Gramss, G.; Schubert, R.; Bergmann, H. Carbon and nitrogen compounds applied to uranium mine dump soil determine (heavy) metal uptake by Chinese cabbage. Environ. Res. J. 2011, 5, 793–818. [Google Scholar]
  100. Mitani-Ueno, N.; Yamaji, N.; Zhao, F.J.; Ma, J.F. The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J. Exp. Bot. 2011, 62, 4391–4398. [Google Scholar] [CrossRef] [PubMed]
  101. Brej, T. Heavy metal tolerance in Agropyron repens (L.) P. Bauv. populations from the Legnica copper smelter area, Lower Silesia. Acta Soc. Bot. Pol. 1998, 67, 325–333. [Google Scholar] [CrossRef]
  102. Clemens, S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 2006, 88, 1707–1719. [Google Scholar] [CrossRef] [PubMed]
  103. Khan, Z.I.; Ashraf, M.; Ahmad, K.; Akram, N.A. A study on the transfer of cadmium from soil to pasture under semi-arid conditions in Sargodha, Pakistan. Biol. Trace Elem. Res. 2011, 142, 143–147. [Google Scholar] [CrossRef] [PubMed]
  104. World Health Organization. Trace elements in human nutrition and health. Available online: http://www.who.int/nutrition/publications/micronutrients/9241561734/en/ (accessed on 14 April 2015).
  105. Palmer, L.J.; Palmer, L.T.; Rutzke, M.A.; Graham, R.D.; Stangoulis, J.C.R. Nutrient variability in phloem: Examining changes in K, Mg, Zn and Fe concentration during grain loading in common wheat (Triticum aestivum). Physiol. Plant. 2014, 152, 729–737. [Google Scholar] [CrossRef] [PubMed]
  106. Sandström, J.; Pettersson, J. Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J. Insect Physiol. 1994, 40, 947–955. [Google Scholar] [CrossRef]
  107. Kamthan, A.; Chaudhuri, A.; Kamthan, M.; Datta, A. Small RNAs in plants: Recent development and application for crop improvement. Front. Plant Sci. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
  108. Gramss, G.; Voigt, K.-D. Seed crops: Alternative for non-remediable uranium mine soils. In Uranium—Past and Future Challenges, Proceedings of the 7th International Conference on Uranium Mining and Hydrogeology, Freiberg, Germany, 21–25 September 2014; Merkel, B.J., Arab, A., Eds.; Springer International Publishing: Cham, Switzerland, 2015; pp. 777–784. [Google Scholar]
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Figure 1. Variation in concentrations of minerals from the root (R; 100%) via the lower part (L; 12 cm) of the mature wheat stem to upper stem (U), rachis (R), and grain (G). Values are arithmetic means for sets of minerals with similar modes of passage (refer to Table 1).
Figure 1. Variation in concentrations of minerals from the root (R; 100%) via the lower part (L; 12 cm) of the mature wheat stem to upper stem (U), rachis (R), and grain (G). Values are arithmetic means for sets of minerals with similar modes of passage (refer to Table 1).
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Figure 2. Variation in concentrations of minerals from roots (R) of straw-type pea plants (100%) via upper vine (V) and pod (P) to the whole seed (S). Values are arithmetic means for sets of macronutrients, essential traces, and toxicants with similar modes of passage (refer to Table 2). Adapted from primary data of Gramss and Voigt [18].
Figure 2. Variation in concentrations of minerals from roots (R) of straw-type pea plants (100%) via upper vine (V) and pod (P) to the whole seed (S). Values are arithmetic means for sets of macronutrients, essential traces, and toxicants with similar modes of passage (refer to Table 2). Adapted from primary data of Gramss and Voigt [18].
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Figure 3. Variation in concentrations of minerals from the lower stipe (L) of Kuehneromyces mutabilis basidiomes (100%) via upper stipe (U), cap plectenchyma (C), and gills (G) to basidiospores (S). Values are arithmetic means for sets of minerals with similar modes of passage (refer to Table 3). Adapted from Gramss and Voigt [61].
Figure 3. Variation in concentrations of minerals from the lower stipe (L) of Kuehneromyces mutabilis basidiomes (100%) via upper stipe (U), cap plectenchyma (C), and gills (G) to basidiospores (S). Values are arithmetic means for sets of minerals with similar modes of passage (refer to Table 3). Adapted from Gramss and Voigt [61].
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Figure 4. Concentration spans (factors in parentheses) in the CuZn stock (mg kg−1 DW) of the soils diminish drastically in the seeds of wheat, rye, and pea due to proportionate up-regulations of the seed:soil transfer factors (values heading the columns × 10−3) on lower concentrated soils. Soils, left to right: Uranium gradient soils (3×) Corg 3.5%–4%; soil Corg 8.9%; alluvial sand Corg 1.97%. Concentrations in CuZn represented by the bars are given in mg kg−1 DW. Adapted from primary data of Gramss and Voigt [18,27].
Figure 4. Concentration spans (factors in parentheses) in the CuZn stock (mg kg−1 DW) of the soils diminish drastically in the seeds of wheat, rye, and pea due to proportionate up-regulations of the seed:soil transfer factors (values heading the columns × 10−3) on lower concentrated soils. Soils, left to right: Uranium gradient soils (3×) Corg 3.5%–4%; soil Corg 8.9%; alluvial sand Corg 1.97%. Concentrations in CuZn represented by the bars are given in mg kg−1 DW. Adapted from primary data of Gramss and Voigt [18,27].
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Figure 5. Normal shoot Cu concentrations of crops and rangeland plants adapted to the geochemical environment of non-contaminated soils (A) rise in the presence of elevated soil Cu (B). In contrast, seeds of wheat, rye, and pea observe their adopted mineral target stock by compensating for widest soil mineral fluctuations with proportionate seed:soil TF adaptations (C–E). Their mineral content surpasses the putative minimum crop demand (F) but concurs exactly with pretensions to the forage for herbivores (G, H). ( ), concentration spans. Refer to Table 4 for the ecological position of further nutritionally relevant elements. Adapted from primary data of Gramss and Voigt [18,27].
Figure 5. Normal shoot Cu concentrations of crops and rangeland plants adapted to the geochemical environment of non-contaminated soils (A) rise in the presence of elevated soil Cu (B). In contrast, seeds of wheat, rye, and pea observe their adopted mineral target stock by compensating for widest soil mineral fluctuations with proportionate seed:soil TF adaptations (C–E). Their mineral content surpasses the putative minimum crop demand (F) but concurs exactly with pretensions to the forage for herbivores (G, H). ( ), concentration spans. Refer to Table 4 for the ecological position of further nutritionally relevant elements. Adapted from primary data of Gramss and Voigt [18,27].
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Figure 6. Incorporation of the chemically similar elements As/P and Cd/Zn in pea seeds. Up-regulations of the seed:soil TFs (values heading the columns × 10−3) on low-concentrated soils (mg kg−1 DW) indicate the active acquisition of both essential and non-essential elements. Differences in TFs and in the quotients of TF: soil concentrations indicate the safe discrimination of chemically similar elements. Concentrations in AsCdPZn represented by the bars are given in mg kg−1 DW. Adapted from primary data of Gramss and Voigt [18].
Figure 6. Incorporation of the chemically similar elements As/P and Cd/Zn in pea seeds. Up-regulations of the seed:soil TFs (values heading the columns × 10−3) on low-concentrated soils (mg kg−1 DW) indicate the active acquisition of both essential and non-essential elements. Differences in TFs and in the quotients of TF: soil concentrations indicate the safe discrimination of chemically similar elements. Concentrations in AsCdPZn represented by the bars are given in mg kg−1 DW. Adapted from primary data of Gramss and Voigt [18].
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Table
Table 1. Up- and down-regulated mineral concentrations (mg kg−1 DW) across the mature plants of wheat cv. Asano grown on the high-contaminated uranium gradient soil A. ( ), quotients calculated from mineral concentrations of the actual to the preceding column expressed in percent.
Table 1. Up- and down-regulated mineral concentrations (mg kg−1 DW) across the mature plants of wheat cv. Asano grown on the high-contaminated uranium gradient soil A. ( ), quotients calculated from mineral concentrations of the actual to the preceding column expressed in percent.
ElementRootLower stemUpper stemRachisWhole grain
K591011,820 a (200)12,690 (107)10,103 (80)4052 a (40)
Mg1060352 a (33)965 a (274)631 a (65)1162 a (184)
P784102 a (13)314 a (308)359 (114)2612 a (728)
Ca3,380989 a (29)4,095 a (414)1,190 a (29)346 a (29)
Zn1,203536 a (45)1,059 a (198)1,117 (105)138 a (12)
Cd29.42.29 a (7.8)4.26 a (186)2.34 a (55)1.55 a (66)
Cu65.61.43 a (2.2)3.05 a (213)2.86 (94)6.43 a (225)
Fe2,41016.6 a (0.7)15 (91)35.7 a (238)24.6 a (69)
Mn2174.95 a (2.3)10.8 a (218)18.8 a (174)19.9 (106)
Ni11.80.28 a (2.4)0.615 a (220)2.51 a (408)2.09 a (83)
As20.20.215 a (1.1)0.745 a (347)0.920 a (123)0.100 a (11)
Pb20.30.374 a (1.8)0.176 (47)0.289 (164)0.044 a (15)
U8.490.571 a (6.7)0.360 (63)0.185 (51)0.003 a (1.6)
a Values within a horizontal line differ significantly at p ≤ 0.05 (n = 2–4) from preceding ones.
Table
Table 2. Up- and down-regulated mineral concentrations (mg kg−1 DW) across the mature plant of pea cv. Rocket grown on the high-contaminated uranium gradient soil A. ( ), quotients calculated from mineral concentrations of the actual to the preceding column expressed in percent.
Table 2. Up- and down-regulated mineral concentrations (mg kg−1 DW) across the mature plant of pea cv. Rocket grown on the high-contaminated uranium gradient soil A. ( ), quotients calculated from mineral concentrations of the actual to the preceding column expressed in percent.
ElementRootWhole upper vinePod wallWhole seed
Ca12,30018,800 (153)15,115 (80)932 (6.2)
K8,39011,190 (133)18,350 (164)10,090 (55)
Mg2,4006600 (275)6290 (95)1120 (18)
P986580 (59)414 (71)3,406 (823)
Cu63.912.2 (19)23.4 (192)8.14 (35)
Fe1,145109 (10)72 (66)49.8 (69)
Mn160123 (77)44 (36)11.8 (27)
Ni3.831.82 (48)2.33 (128)0.95 (40)
Zn684311 (35)160 (51)70.2 (44)
As7.450.833 (11)0.106 (13)0.049 (46)
Cd36.76.18 (17)2.81 (45)0.302 (11)
Pb7.240.548 (8)0.273 (50)0.040 (15)
All values within horizontal lines differ significantly at p ≤ 0.05 (n = 2–4) from preceding ones. Adapted from primary data of Gramss and Voigt [18].
Table
Table 3. Up- and down-regulated mineral concentrations (mg kg−1 DW) across sporulating basidiomes of the mushroom K. mutabilis grown on trunk sections of European beech embedded into non-contaminated soil Corg 8.9%. ( ), quotients calculated from mineral concentrations of the actual to the preceding column expressed in percent.
Table 3. Up- and down-regulated mineral concentrations (mg kg−1 DW) across sporulating basidiomes of the mushroom K. mutabilis grown on trunk sections of European beech embedded into non-contaminated soil Corg 8.9%. ( ), quotients calculated from mineral concentrations of the actual to the preceding column expressed in percent.
ElementLower stipeUpper stipeCap plectenchymaGillsBasidiospores
Ca176114 a (65)382 a (335)137 a (36)277 a (202)
Fe8780.5 (93)91 (113)133 a (146)199 a (150)
Mn47.542 (88)46 (110)28.5 a (62)73.5 a (260)
Ni1.401.45 (104)2.30 a (159)1.85 a (80)13 a (703)
Pb0.2100.105 a (50)0.180 a (171)0.090 a (50)0.555 a (620)
As0.0690.061 (88)0.088 a (144)0.112 a (127)0.109 (97)
Cd0.6301.08 a (171)0.300 a (28)1.23 a (410)0.850 a (69)
Cu3633.5 (93)52 a (155)71.5 a (138)24 a (34)
K26,12528,800 (110)26,940 (94)34,180 a (127)8,157 a (24)
Mg1,130890 a (79)1,340 a (151)1,580 (118)1,140 a (72)
P2,9803,920 a (132)3,280 a (84)9,610 a (293)5,150 a (54)
Zn3145.5 a (147)33 a (73)78.5 a (238)75 a (96)
Na987774 a (78)636 a (82)539 a (85)92 a (17)
a Values within a horizontal line differ significantly at p ≤ 0.05 (n = 2–4) from preceding ones. Adapted from primary data of Gramss and Voigt [61].
Table
Table 4. Wide concentration spans ( ) in sets of HM-contaminated and non-contaminated arable soils diminish drastically in seeds. The resulting seed mineral loads correspond with the dietary pretensions of (livestock) herbivores and human and indicate uptake repression to AsCdPb toxicants. All values are given in mg kg−1 DW. Adapted from primary data of Gramss and Voigt [18,27].
Table 4. Wide concentration spans ( ) in sets of HM-contaminated and non-contaminated arable soils diminish drastically in seeds. The resulting seed mineral loads correspond with the dietary pretensions of (livestock) herbivores and human and indicate uptake repression to AsCdPb toxicants. All values are given in mg kg−1 DW. Adapted from primary data of Gramss and Voigt [18,27].
ElementConcentration spans ( ) in soil and seed, number of test soils (refer to Figure 4)Balanced dietary pretensions to herb forageUsual heavy-metal ranges
Wheat (3 cvs., 3 soils)Rye (4 soils)Pea (5 soils)Monogastric livestockRuminantsArable soilsHerbage
CaSoil7235–2296 (3.15)7235–2296 (3.15)7546–1646 (4.6) --
Seed538–281 (1.9)411–330 (1.25)1256–847 (1.48)2400–9000 a2000–15,000 a --
KSoil5130–4086 (1.26)5130–4086 (1.26)2264–1296 (1.75) --
Seed6535–4289 (1.52)8006–4806 (1.67)10,335–9139 (1.13)1500–10,000 a5000–10,400 a --
MgSoil3237–2252 (1.44)3237–2252 (1.44)5595–945 (5.9) --
Seed1707–1241 (1.38)1267–996 (1,27)1236–945 (1.31)400–1300 a1000–2100 a --
PSoil873–713 (1.22)873–713 (1.22)2792–307 (9.1) --
Seed5290–4206 (1.26)4052–3086 (1.31)3902–1974 (1.98)1700–7000 a1600–5900 a --
CuSoil283–15 (18.9)283–9 (31.4)261–7.5 (34.8) 2–40 (30) c
Seed10.7–14.2 (1.33)8.21–5.09 (1.61)8.14–5 (1.63)3–10 (250–800) a7–11 (25–100) a 2–20 (LC 10) d
FeSoil23,390–10,170 (2.30)23,390–5445 (4.30)41,630–4370 (9.53) --
Seed39.6–64.3 (1.62)28–37 (1.32)49.8–72.3 (1.45)40–100 (500–3000) a15–50 (500–1000) a --
MnSoil2130–515 (4.14)2130–380 (5.61)1780–126 (14.1) 40–1000 (550)
Seed26.4–33.5 (1.27)22–16.3 (1.35)8.55–20.5 (2.40)2–60 (400–2000) a14–40 (1000) a 14–30
NiSoil40.8–11.8 (3.46)40.8–4.58 (8.91)54.3–3.9 (13.9) 3–50 (30)
Seed1.41–0.180 (7.83)0.811–0.069 (11.8)0.626–1.21 (1.93)0.05–0.2 (50–300) a0.3–0.5 (50) a 0.1–3 (LC 1)
ZnSoil3005–48 (62.6)3005–36 (83.5)2890–26.4 (109) 10–80 (90)
Seed190–35.8 (5.31)207–24.8 (8.35)33–70.2 (2.13)35–100 (500–1000) a20–55 (300–500) a 10–100 (LC 50)
AsSoil156–6.34 (24.6)156–3.53 (44.2)152–2.3 (66) 1–20 (6)
Seed0.433–<0.080 (>5.41)<0.080 all0.044–0.062 (1.41)2 (50) b2 (50) b 0.01–1 (L 0.5; LC 0.7)
CdSoil41.3–0.231 (179)41.3–0.209 (198)40.4–0.085 (475) 0.1–0.6 (0.35)
Seed3.13–0.033 (94.8)1.72–0.018 (95.6)0.333–0.021 (15.9)1 (0.5) b1 (0.5) b 0.05–0.4 (L/LC 0.1)
PbSoil150–20.5 (7.32)150–16.5 (9.1)148–9 (16.4) 2–80 (35)
Seed0.057–0.140 (2.46)0.093–0.033 (2.82)0.040–0.019 (2.11)30 (30) b30 (30) b 0.1–6 (L 0.2; LC 0.4)
a Recommended mineral concentration spans and (maximum tolerable levels in forage) according to McDowell [10]; b Legislative limits for toxicants in forage after [16] and (maximum tolerable levels) according to McDowell [10]; c Concentration ranges of non-contaminated soils after Schachtschabel et al. [7]; ( ), after Bowen [67]; d Normal plant heavy-metal concentrations after Auermann et al. [68] and Schachtschabel et al. [7]; L, legislative limits for food grains [69]; LC, tolerance limits of Chinese standards for food-quality wheat grains according to Huang et al. [19]. In cvs. of wheat/rye, correlations between HM concentrations in soils and grains were recorded for BaCsSr/BaZn (r ≤ 0.05) and CaCdNiZn/CdCuSr (r ≤ 0.33). Concentrations of AsCoCrFeMnPbThU did not correlate [27].

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Gramss, G.; Voigt, K.-D. Stability of the Inherent Target Metallome in Seed Crops and a Mushroom Grown on Soils of Extreme Mineral Spans. Agronomy 2016, 6, 14. https://doi.org/10.3390/agronomy6010014

AMA Style

Gramss G, Voigt K-D. Stability of the Inherent Target Metallome in Seed Crops and a Mushroom Grown on Soils of Extreme Mineral Spans. Agronomy. 2016; 6(1):14. https://doi.org/10.3390/agronomy6010014

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Gramss, Gerhard, and Klaus-Dieter Voigt. 2016. "Stability of the Inherent Target Metallome in Seed Crops and a Mushroom Grown on Soils of Extreme Mineral Spans" Agronomy 6, no. 1: 14. https://doi.org/10.3390/agronomy6010014

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