Selenium and Sulfur to Produce Allium Functional Crops: History
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Contributor:
Susana González-Morales
,
Fabián Pérez-Labrada
,
Ema Laura García-Enciso
,
Paola Leija-Martínez
,
Julia Medrano-Macías
,
Irma Esther Dávila-Rangel
,
Antonio Juárez-Maldonado
,
Erika Nohemí Rivas-Martínez
,
Adalberto Benavides-Mendoza

Selenium is an element that must be considered in the nutrition of many crops since its use allows the obtaining of biofortified crops with a positive impact on human health. 

  • nutritional quality
  • biofortification
  • phytochemicals of Allium
  • sulfur metabolism
  • selenium metabolism

1. Introduction

It is known that cultivated terrestrial plants require at least 17 elements for their metabolism, growth, and reproduction [1]. In the case of humans, the essential elements are at least 28 [2]. This difference has the consequence that, in practice, several elements that are important in human nutrition are not considered in crop nutrition programs, especially in the case of crops cultivated in soilless systems. The ideal number of elements to be considered for the nutrition of plants destined for human consumption should be 20, that is, the 17 elements considered essential for plants, in addition to selenium, silicon, and iodine.
However, not all species of crop plants have the same ability to absorb, metabolize, and accumulate these three additional elements. For example, some species of Brassicaceae, Fabaceae, Asteraceae, and Alliaceae can absorb and accumulate selenium [3][4][5][6]; Poaceae, Fabaceae and Cucurbitaceae do the same with silicon [7]; and Laminaria algae stand out with iodine [8].
Biofortification with one or more of the three elements mentioned would have different results according to the taxonomic group or species of plants in which the process is carried out. Among the groups of plants that may potentially be good alternatives for selenium biofortification are those that by nature accumulate many sulfur compounds in their tissues, such as Brasicaceae and those of the genus Allium. Climate change is expected to have an adverse effect on selenium availability in agricultural soils [9]. Hence the importance of directing biofortification efforts towards crops like Allium that have an exceptional ability to absorb, metabolize and store selenium.
The genus Allium includes more than 550 species distributed throughout the world in temperate, tropical, and semi-arid regions. Some species are of great importance for their culinary, medicinal, and ornamental use [10]. Some of the species that stand out are: garlic (A. sativum), wild garlic (A. ursinum), elephant garlic (A. ampeloprasum L. var. ampeloprasum), white garlic (A. neapolitanum), onion (A. cepa L.), chives (A. fistulosum), garlic onion or scallion (A. schoenoprasum L.), Chinese chives (A. tuberosum L.), and leek (A. ampeloprasum L. var. porrum). All are of great importance for being edible plants and for their use in medicine as antimicrobial, lipid-lowering, hypocholesterolemic, antithrombotic, cardiovascular, hypoglycemic and antitumorigenic [11][12].
A large number of enzymes involved in the metabolism of assimilation and volatilization of S are functional in the presence of Se. The ability to accumulate S and Se in a certain species will depend on their ability to transform ionic forms into more stable organic forms that can be stored and fulfill certain metabolic functions [13]. On the other hand, the concentration of S and Se in plant tissues also depends on the balance between absorption, transport, and assimilation with the volatilization process; such activities occur for both S and Se [14]. Many plant species and accompanying microbiomes volatilize Se when this is highly available [15][16]; similarly, the rate of sulfur volatilization is inversely related to the concentration of sulfate in the growth medium [17]. Allium plants do not show such a great volatilization activity in the presence of high concentration of S and Se, allowing to obtain crops enriched in both sulfur and selenium that can be an excellent dietary source of these elements [16].

2. Absorption and Metabolism of Sulfur and Selenium in Allium

In every terrestrial plant species, the assimilation of selenium is carried out through the metabolic absorption route of sulfur [18]. However, in species of the genus Allium, a greater capacity to absorb, metabolize, and assimilate S and Se have been found. A characteristic that gives Alliaceae such capacity is that they can methylate the seleno-amino acids, thus reducing the rate of incorporation of the same in proteins and, on the other hand, increasing, if necessary, the rate of volatilization of Se. That is why the concentration of S and Se and its metabolites in this group of plants is very high compared to other groups [19]. Indeed, if the natural concentration of selenium in wheat grain in the UK (0.0155–0.0438 mg·kg−1) [20] and rice in some regions of China (0.015–0.046 mg·kg−1) [21] is compared to selenium levels of onion (0.024–0.5 mg·kg−1) and garlic (0.015–0.5 mg·kg−1) [22][23] cultivated in low selenium soils, the highest levels for Allium sp. exceed ten times those of the grasses. When biofortifying the grasses with Se, they reach 1.64 mg·kg−1 [24], while the onion shows 28–140 mg·kg−1 and the garlic 68–1355 mg·kg−1 [22][25]. In biofortified Allium tricoccum, the Se level ranges from 48 to 784 mg·kg−1 [22][26]. Something similar is observed with sulfur: the ranges of adequate concentration of total sulfur in wheat and maize range from 300 to 8900 mg·kg−1 [27], while for garlic are 4600–6000 [28] and for onion are 1540–5350 [29].

3. Phytochemicals of Allium spp. Derived of Se and S

In Allium spp., the metabolism of sulfur, after cysteine synthesis, differs from other groups of plants, since the synthesis of an extensive battery of sulfur compounds occurs. These compounds are traditionally associated with the scents and flavors of Alliaceae [30], but fulfill other functions such as sulfur storage, cellular redox balance, antioxidant protection and stress defense [31][32][33]. In the sulfur route, phytochemicals are mostly represented by glucosinolates, used in defense against different types of stress [34]. In addition, specific secondary routes are used. In the case of sulfur, the formation of a wide range of defense molecules, such as H2S and GHS, is included. From these derives the synthesis of the sulfoxides precursors of the volatile molecules that give the smell and characteristic organoleptic properties to the alliaceous. H2S is used by the plant as a defense against pathogens [35]. However, it is also considered as part of a mechanism of regulation in the accumulation of cysteine [36]. The functions of glutathione (GSH) are important for the maintenance of redox status in the cell, as an antioxidant and precursor of S-alk(en)yl cysteine sulfoxides methiin, alliin, propiin, isoalliin, ethiin, and butiin. These non-protein sulfur amino acids are hydrolyzed by the enzyme alliinase to produce flavor and pungency imparting compounds in Allium [32]. Randle and Lancaster [37] reviewed the sulfur’s compounds related with the flavor in Allium. Although most of the enzymes involved in the biosynthesis of these compounds have not been identified in Allium, the AsGGT1, AsGGT2, and AsGGT3 genes of garlic have been described. These genes encode the enzyme γ-glutamyltranspeptidase (GGTs), which suggest that they may contribute in a different way to the biosynthesis of alliin in garlic [38]. Recent findings have characterized a compound analog to alliin, this is a precursor sulfoxide of allicin derived from selenium metabolism [39].
An alternative in the metabolism of sulfur amino acids leads to the synthesis of volatile compounds, such as H2S, or volatile methylated compounds such as DMDS, DMSP, and DMS. These compounds are produced by some living organisms, including anaerobic bacteria [40], seaweed [41] and plants [42], and are widely associated with marine waters, wetlands, decomposition of organic matter, and volcanic emissions [43]. The physiological function of these compounds is mainly associated with sulfur dissipation [44][45] as regulator and signal in the stress response [46][47], and is also involved in biogeochemical processes [48][49][50].
In the selenium route, analogous compounds are synthesized. However, the function and chemical nature of these compounds are not entirely described. Se-methyl selenocysteine (SeMeSeCys) is considered the most abundant Se compound in garlic, onion, and A. ampeloprasum when supplemented with Se [4][51]. It is thought that the synthesis of SeMeSeCys is part of a mechanism of tolerance to Se in plants, allowing the conversion of potentially toxic selenoamino acids to non-protein derivatives such as MeSeCys [52][53]. Likewise, compounds such as DMDSe, DMSeP, and DMSe are considered part of a strategy to increase tolerance to Se, by producing volatile forms of Se [54].

Impact of Se and S on the Nutritional and Functional Quality of Allium spp.

The plants that integrate the genus Allium have been used since ancient times because of the multiple beneficial effects on human health such as antiasthmatic, hypolipemic, antithrombotic, anticarcinogenic, antimicrobial, and hypoglycemic actions [32]. The most studied phytochemicals of Allium are sulfur compounds.
Garlic is the species that has been shown by in vitro and in vivo studies to be the species with the greatest number of beneficial effects on human health, due to its higher concentration of sulfur compounds [55].
The biological activity of the sulfur compounds is linked to the level of unsaturation and asymmetry in the molecules, the cepaenes, a class of structurally related α-sulfinyl disulfides [56], having two double bonds (e.g., bis[2-methyl-1-(1-methylethenyl)-1-propenyl] disulfide) are more active than those having a single, double bond (e.g., methyl (E)-1-(1-propenylthio)propyl disulfide), and than thiosulfinates with lower level of unsaturation (e.g., methyl allyl-thiosulfinate). In addition, thiosulfinates with aromatic and poly-substituted substituents (e.g., S-phenyl 2,2-dimethyl-propane-thiosulfinate) are more reactive than those lacking these chemical characteristics (e.g., Dimethyl thiosulfinate) [57]. These compounds are usually extracted using organic solvents (methanol, ethanol, etc.) while sulfoxides and some phenolic compounds such as quercetin or other antioxidants are isolated by aqueous extraction. Therefore, the beneficial effects of extracts of Allium species depend on the polarity of the extractant in conjunction with the chemical nature of the extracted compounds.
In humans, the organosulfur compounds of Allium are associated with the modulation of the activity of enzymes such as glutathione S-transferase (GST), quinone reductase (NQO1), and UGT-glucuronosyltransferase (UGDT), which are important in the detoxification of carcinogenic compounds [32][58][59]. Allium’s anticancer and antiproliferative activity, as well as antimicrobial capacity against a broad spectrum of infectious agents, is attributed to the effect of allicin, which is highly permeable through membranes [60], and undergoes a thiol-disulfide exchange reaction with free thiol groups present in the proteins. It is believed that these properties are the basis of its antimicrobial effect [61], having effects against different bacteria, fungi, and yeasts [62].
Similarly, the unsaturated trisulfide compounds (as diallyl trisulfide) have potent anticancer activity, which has been tested in colon adenocarcinoma, prostate, and lung cancer [63][64][65][66]. The mechanisms of action described are the induction of apoptosis [67], inhibition of malignant cell growth in vitro [68] and inhibition of adenomas [69]. Sulfur compounds containing more sulfur atoms mitigate the damage caused by diabetes [70].
Aqueous extracts of garlic and A. ampeloprasum have been shown to be effective in reducing N-nitrosorpholine (liver carcinogen). A. ampeloprasum is also effective against several types of malignant cells inducing apoptosis and necrosis [71].
A. ampeloprasum has several antioxidant, anticancer, antimicrobial, hepatoprotective, antidiabetic, anti-inflammatory and other anti-osteoporotic properties [72], showing immunomodulatory activity, since the pectic polysaccharides of this species stimulate [73], platelet anti-aggregation [74] and spasmolytic activity [75].
The functional components of A. schoenoprasum are valued for their healing, food, and antimicrobial properties; this is perhaps related to their antioxidant activity [76]. In A. ampeloprasum, antioxidant activity is an effect demonstrated by several authors [77][78][79][80]. These studies are carried out through alcoholic extractions of this species, demonstrating their effectiveness both as hypolipidemic and antioxidant, however, as mentioned, the compounds involved in these mechanisms are unknown.
The high content of allicin in leaf extracts of A. schoenoprasum may explain the anti-inflammatory effect, in addition to compounds also present in this species such as β-sitosterol and campesterol [81].
Extracts from leaves of A. humile and A. hirtifolium are rich in sulfur compounds. A. humile has cardio-protective effect related to metabolites such as ajoene, allicin, and alliin [82][83], decreasing the risk factors of cardiovascular accidents [84].
Garlic can accumulate up to five times more selenium (110–150 mg·kg−1 vs. 28 mg·kg−1) and constitutes a more potent anticarcinogen natural agent than onion [25]. Regarding selenium in animal organisms, the MeSeCys ingested with food or administered in supplements is absorbed and distributed more effectively than inorganic Se, and is metabolized to methyl selenol, the chemical species to which anticarcinogenic and antioxidant properties are attributed [85].
In all cases, the potent anti-cancer effect is a result of the presence of Se [86], finding that the selenium-analogs of the sulfur compounds of Allium, such as diallyl selenide vs. diallyl sulfide and benzyl selenocyanate vs. benzyl thiocyanate, are often more effective as anticarcinogenic agents [87].

4. Use of Selenium and Sulfur in Allium Agricultural Production

As mentioned earlier, selenium consumption is of utmost importance for human health. It has been proven that the consumption of this element by humans is mainly given by food since they contribute up to 80% of Se intake [88]. In turn, the natural selenium content in food depends on the geological variations of the surface of the Earth. In most atmospheric conditions, exposure to this element is negligible, as air Se concentrations are <10 ng·m−3. In most cases, the content of Se in water is <10 µg·L−1, a value considered extremely low, while in seawater the average concentration is 0.09 µg·L−1. In the same way, the amount of Se in most soils is very low, ranging from 0.01 to 2 mg·kg−1, while the overall mean is 0.4 mg·kg−1 [89]. In some regions of Europe, Africa, China, and Thailand, for example, most soils have low concentrations of Se, which results in low concentrations in food crops [90][91][92].
Sulfur, on the other hand, is essential for plant and human metabolism, for example, forming part of amino acids, proteins, and coenzymes [93]. However, in the last 30 years, the availability of this element has declined due to the use of fertilizers with low S content, such as MAP or DAP [94], the progression of intensive agriculture that decreases the major source of sulfur in soil: soil organic matter, as well as the reduction of S in pesticides [95]. There is a need for additional sulfur applications in crops, particularly in highly sulfur-demanding crops such as Allium sp. Sulfur fertilization can be carried out through different routes: elemental sulfur, sprinkled in leaves or soil applied, and calcium sulfate incorporated in soil are inexpensive sources of S, which provides a long-term residual effect, especially in clay soils [96].
The main proposal of this resrarch is to use Allium species as specialist plants for biofortification with Se and S. The metabolism of these plants is adapted to this purpose considering the natural ability to accumulate both elements in the form of different phytochemicals, which promotes the functional value of Allium. In Allium crops grown in soils low in organic matter (< 1%) it is advisable to provide elemental sulfur applied to the soil (30–60 kg·ha−1) in addition to the sulfate that fertilizers contain. On the other hand, it is suggested to spray foliar sulfur (2 to 5 kg·ha−1 of potassium sulfate or 10 to 20 kg·ha−1 of micronized elemental sulfur) on two or three occasions during the growing season, thus avoiding leaching and volatilization of S on the soil as well as bringing the element directly to the site where it will be assimilated and accumulated in organic forms [97]. In the case of selenium, it has also been found that leaf aspersion is the most effective way of biofortifying crops, thus being possible to sprinkle nutrient solutions with sulfate and with selenate or selenite (5–15 g·ha−1).
In order to increase the final concentration of biotransformed Se in Allium crops, it is recommended to apply selenite or SeMet in concentrations up to 10 mg·L−1 of selenium in the nutrient solution or 10 to 50 mg·L−1 per leaf (sprinkling a volume of 50 mL·m−2). When applied by the irrigation system, it is preferably done once or twice during the growing season and at most once every 15 days [98]. Foliar application is done once when plants have 7–8 leaves [99]. In some species, foliar application of selenite has been found to be the most effective way to obtain biotransformed selenium in plant tissues [100] and would therefore be recommended for Allium. The application of Se as a pre-treatment in seeds (using 10–50 g of selenium applied to the seeds needed for one hectare) is another effective way to increase the concentration of Se in seedlings and adult plants. Although information on the use of selenium applied to Allium seeds or bulbs is not available, it has been a simple and effective way to apply it [101] and has favorable effects such as increasing the rate of germination under unfavorable conditions [102]. The feasibility of using selenium-enriched substrates has been demonstrated in the seedling stage, which avoids the disadvantages of the dosage in the nutrient solution [103].
Both Se and S are important determinants of the nutraceutical value of Allium [104]. However, in many cases, selenium competes with sulfur for root absorption sites because the sulfur form that is absorbed by the roots, SO42−, is taken by the same selenate-absorbing transporters (SeO42−), which is the most common form of selenium in aerobic soils (low in organic matter, and pH in alkaline side). In contrast, selenite will be the predominant form of selenium in aerobic soils with pH in acidic to neutral side. Selenite does not compete with sulfate, since its absorption is partially mediated by phosphate and silicon transporters [105][106][107] and phosphate-selenite antagonism is found to be much smaller than sulfate-selenate antagonism [108].

Use of Se and S in Allium Production Systems

Regarding the agronomic management, the capacity of these plants to assimilate sulfur and selenium can be promoted using an adequate level of organic matter in soil [94][109], and a proper balance of S:P:Se; that is, using selenate when sulfate is not in high concentration or using selenite if a large amount of sulfate is found, but providing an adequate amount of phosphates. Thus, the competition for the sites of absorption and subsequent metabolism would not be significant, and both sulfate and selenate or selenite will be rapidly metabolized and incorporated into various compounds with nutraceutical value for humans and increasing the plant ability to tolerate environmental stress [110], through the capacity of sulfur and selenium compounds to promote antioxidant activity and a reduced cellular-redox environment, as well as to coordinate heavy metal and metalloid ions, diminishing oxidative stress and damage to DNA [111][112].
Several studies highlight the benefits of Se in the production of Allium. The application of Se relates directly to the antioxidant capacity and functional value of Allium [113][114][115]. In addition to increasing nutritional quality, increased antioxidant capacity would result in a potential increase in the plant’s ability to tolerate stress. The application of Se in plants increases biomass accumulation [116] or yield [99]. However, high concentrations (10 and 100 mg·L−1 of selenate or selenite in the nutrient solution) inhibit growth in garlic [117]. Growth inhibition in hydroponics was reported in onion with selenate at 2 mg·L−1 [117][118], with 5–100 mg·L−1 of selenate or selenite in the nutrient solution [113], or with 50 mg of selenate per kg of soil [119].
Positive effects of Se have been reported, such as Hg antagonism [120], and even the ability to decrease Hg toxicity when the plants are simultaneously exposed to both elements [121]. Selenium also presents antagonism with other nutrients such as Ca and K [115], and particularly with S [18][115][122][123]. In garlic it has been shown that the application of S can inhibit the uptake of Se [123], whereas the Se at high concentration (50–100 mg·L−1 by leaf spraying) decreases the absorption of S [115]. However, there is not always an antagonism between these elements. In different cultivars of onion it was observed that the application of Na2SeO4 in nutrient solution (up to 2 mg·L−1) generated an increase in S concentration [124] indicating the possibility of applying both elements, but with the adequate concentration of each one of them. When comparing selenite and selenate application in Allium, consistently higher selenite toxicity has been observed [117], and increased selenium accumulation when applied as selenate [125][126]. More selenium was accumulated in A. schoenoprasum when selenate was applied, in comparison to selenite and SeMet, whereas in A. fistulosum greater accumulation of the element was observed when using SeMet compared to selenite. However, considering the objective of applying S and Se together, the best way to use selenium in Allium plants would be selenite > SeMet > selenate, specifically using a low concentration of Se (≤2 mg·L−1 or ≤5 mg·kg−1 of soil). Selenium at low level results in positive effects on antioxidant capacity and growth, without negatively affecting the assimilation of sulfur.
Sulfur exerts well-documented benefits in Allium, mainly on biomass and bulb size [127][128] as well as other related characteristics as leaf number, plant height, and yield [129][130][131]. Another example is the positive relationship between sulfur availability and pungency [122][127][128][129][132][133][134][135][136], whereas low levels of S decrease pungency [137][138]. However, the effect of S on pungency may be variety dependent, as observed in onion [29].
Regarding the interaction of S with other elements, it is well known its antagonistic effect with Se as previously discussed. However, the effect is not exclusive to Se. In onion, S antagonism has been demonstrated with B, Fe, Mn and Zn [138], whereas in garlic with Cl and Na [139]. However, a synergistic effect on other elements has also been reported. In garlic the foliar application of S increased the content of N, P and K [139], whereas in A. fistulosum application in nutrient solution increased the N content [129].

This entry is adapted from the peer-reviewed paper 10.3390/molecules22040558

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