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Review

Selenium Biofortification of Allium Species

by
Nadezhda Golubkina
1,*,
Victor Nemtinov
2,
Zarema Amagova
3,
Liubov Skrypnik
4,
Sergey Nadezhkin
1,5,
Otilia Cristina Murariu
6,
Alessio Vincenzo Tallarita
7 and
Gianluca Caruso
7
1
Federal Scientific Vegetable Center, Moscow 143072, Russia
2
Research Institute of Agriculture of the Crimea, Simferopol 295043, Russia
3
Chechen Scientific Institute of Agriculture, Grozny 366021, Russia
4
Scientific and Educational Cluster MEDBIO, Immanuel Kant Baltic Federal University, Kaliningrad 236040, Russia
5
Soil-Ecological Center, Russian State University, Moscow 119981, Russia
6
Department of Food Technology, “Ion Ionescu de la Brad” Iasi University of Life Sciences, M. Sadoveanu Alley, 700440 Iasi, Romania
7
Department of Agricultural Sciences, University of Naples Federico II, 80055 Naples, Italy
*
Author to whom correspondence should be addressed.
Crops 2024, 4(4), 602-622; https://doi.org/10.3390/crops4040042
Submission received: 20 September 2024 / Revised: 30 October 2024 / Accepted: 6 November 2024 / Published: 11 November 2024
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Abstract

Allium species have great potential in the production of functional food via selenium biofortification. This review is devoted to the specificity of Allium plant biofortification with Se, including the genetic peculiarities, effect of the chemical form of the microelement, methods of supply, sulfur and AMF effects, and hormonal regulation. The biosynthesis of methylated Se amino acids and the beneficial effect of Se treatment on secondary metabolite accumulation and plant yield are discussed. Special attention is paid to the production of functional foods based on Allium plants enriched in different ways: bread with leek leaf powder, Allium microgreens and seedlings, and ‘Black garlic’ biofortified with Se. Further focus is provided to the high variability of Allium crop yield and quality under Se supply governed by genetic factors and environmental stresses, and to the need for plant growth technology optimization to obtain the predicted nutritional characteristics of the derived functional product with high anti-carcinogenic activity.

Graphical Abstract

1. Introduction

Selenium is an essential microelement for mammals, contributing to the maintenance of the immunity, antioxidant defense, fertility, and brain activity in human organisms. Selenium takes action via the active sites of different enzymes, such as glutathione peroxidases, thioredoxin reductases, and tri-iodothyronine deiodinases, participating in antioxidant defense, iodine metabolism, and maintenance of immunity. Identification of 25 genes responsible for selenoprotein biosynthesis in the human body provides the basis of the significance of human Se status optimization. Indeed, the protective role of numerous selenoproteins against viral diseases [1,2], including COVID-19 [3,4], cardiovascular diseases, and cancer [5,6,7], makes selenium one of the most promising elements to improve human health via optimization of the human antioxidant status [8].
Taking into account the low Se status of the population in many countries, and the possible increase in Se deficiency in the future [9], Se supplements and Se fortified food products are deemed essential for residents of many areas worldwide. In this respect, plenty of reviews devoted to human Se status optimization have been published in recent years [1,6,7,8,10,11,12,13,14,15,16,17]. To valorize the wide benefits of Se utilization for human health optimization, different approaches have been proposed: the development of Se-containing supplements, both for humans and for livestock [14,18]; Se nanoparticle production [1]; chemical synthesis of organic Se derivatives [19]; wheat Se biofortification [16]; ubiquitous utilization of Se fertilizers [20]; and a wide spectrum of Se-biofortified cereals [17], fruit, and vegetables [15]. From a practical point of view, agronomic biofortification of crops is considered the most economically efficient strategy, providing the opportunity to produce highly valuable functional foods with high Se content and improved biological activity [15]. Indeed, the first global optimization of the human Se status has been achieved in Se-deficient Finland, via ubiquitous utilization of Se fertilizers [20]. Such a policy provided the population with a powerful defense, such that this country moved from the first ranked in Europe in terms of the occurrence of cardiovascular disease mortality to the last one, currently. Nowadays, the urgent need to improve the human Se status arises also as a consequence of rejection of Se-rich grain imports from endemic regions in the world, causing the occurrence of Se deficiency among the population [21]. At present, Se deficiency is widespread worldwide: between 500 million and 1 billion people do not reach the Se adequate consumption level of 70 µg day−1 for men and 60 µg day−1 for women [17,22].
The present review aimed to emphasize the outstanding prospects of Allium species utilization targeting Se biofortification and human health safeguarding.

2. Vegetables as Targets of Se Biofortification

Among the different approaches to human Se status optimization, biofortification of agricultural crops with this microelement is considered the most promising and cost-effective [10]. It is closely connected with the ability of plants to transfer soil inorganic Se compounds to organic derivatives with high bioavailability, particularly selenomethionine (SeMet) and selenocysteine (SeCys) (Scheme 1) [11].
Being a chemical analog of sulfur, Se freely substitutes the latter in various natural compounds, firstly amino acids, proteins, and peptides and, to a lesser extent, polysaccharides, polyphenols, and glucosinolates [23]. The main chemical forms of Se in the environment are selenates (Se+6), selenites (Se+4), organic derivatives (Se−2), and Se nanoparticles (Seo). Most agricultural crops are extremely sensitive to high Se concentrations as Se-containing amino acids incorporated into proteins decrease enzyme activity, resulting in plant growth inhibition. On the other hand, low and moderate Se doses provide growth stimulation, with a narrow optimal concentration range controlled by genetic factors.
Contrary to Se-biofortified cereal and legume crops which accumulate SeMet and SeCys (the main Se sources for humans), biofortification of vegetables promotes the synthesis of methylated forms of Se-containing amino acids and peptides, with their background of high natural antioxidant content [24] (Figure 1).
The methylation process provides protection for plants against Se toxicity, arresting the incorporation of methylated amino acids in proteins.
Compared to cereals, Allium and Brassica representatives occupy a special place within the agricultural crops as an initial material for Se biofortification thanks to their high sulfur content, suitable for Se substitution [25,26,27]. Firstly, these plants belong to the secondary Se accumulator group, capable of assimilating up to 100–1000 mg Se kg−1 d.w. without signs of Se toxicity [23] and more tolerant to different chemical forms of Se, which provides the opportunity to increase their Se accumulation level, contrary to most other agricultural crops. On the other hand, only these groups of plants are able to predominantly synthesize methylated Se-containing compounds, Se-methyl-selenocysteine (MeSeCys) and γ-glutamyl Se-methyl-selenocysteine (γ-Glu-MeSeCys) [24], which is of great practical importance due to the higher anti-carcinogenic activity of these compounds compared to their sulfur analogs and non-methylated Se amino acids [28] (Figure 1 and Figure 2). Brassicaceae representatives are also able to synthesize Se-containing glucosinolates (a combination of glucose and amino acids), while Allium crops show much higher diversity of low molecular weight S/Se derivatives with outstanding health-promoting effects (S/Se amino acids, allicine, ajoene, thiosulfinates, etc.).
Notably, chemical forms of Se used for biofortification may cause variations both in the efficiency of Se assimilation and in the Se component profile of Allium species. Indeed, according to Kapolna et al. [35], A. cepa produces more organic Se forms as a result of biofortification with selenite (Se+4) than with selenate (Se+6).
All representatives of the Allium species are rich in biologically active compounds, such as quercetin and other flavonoids, sulfur-containing compounds, and saponins. Practically, all of them demonstrate anti-carcinogenic activity and participate in anti-inflammatory, anti-diabetic, anti-microbial, neuroprotective, and immuno-modulating activity [36], properties also typical for Se compounds. Furthermore, it was established that Se shows synergism with natural antioxidants [37,38], which provides significant improvement in Se-biofortified vegetable nutritional value. In this respect, the unusually high anti-carcinogenic activity of Se-biofortified garlic is supposed to be connected with the accumulation of methylated Se amino acids, allicin and other sulfur derivatives, polyphenols, and flavonoids, and their interaction with Se [12,37,39,40].
Among more than 550 species of the Allium genus, the most abundant are garlic (A. sativum), onion (A. cepa), wild garlic (A. ursinum), the Welsh onion (A. fistulosum), chives (A. schoenoprasum), Siberian chives (A. nutans), leek (A. porrum), shallot (A. ascalonicum), etc. All of them are commonly used in nutrition and are known for their wide spectrum of biological activity, which allows their ascription as medicinal herbs [41,42].

3. Peculiarities of Allium Species Biofortification with Se

Despite the intensive investigations regarding Se biofortification of Allium crops, there are still important issues hampering the industrial production of appropriate functional foods. Firstly, the typical dynamics of Se accumulation in plants under increasing doses of Se have been constructed with an analysis of previous garlic data [43] and are presented in Figure 3.
The curve indicates two important zones: (1) relatively low Se accumulation at moderate Se doses; and (2) intensive Se increases in plants at high supplied Se concentrations. While the first zone corresponds to the growth stimulating properties of Se, the latter refers to the growth inhibition and the reduction of sulfur accumulation. The character of such interactions is common to all plants, though the optimal Se concentration range varies depending on the plant species, method of Se supply (soil, foliar, or hydroponics), chemical form of Se (organic, selenate (Se+6), selenite (Se+4), or Se nanoparticles), participation of soil microorganisms, and peculiarities of hormonal regulation (Figure 4).
Indeed, previous investigations revealed the existence of variability in the tolerance of different Allium species to Se treatment. In this respect, A. sativum accumulates Se easier than A. cepa at different Se doses [44], while among perennial onions, the highest accumulation of Se was recorded in A. schoenoprasum and A. senescence subsp. montanum (3000 µg kg−1 d.w.), with much lower values in A. cepa (2000 µg kg−1 d.w.), A. fistulosum (1400 µg kg−1 d.w.), and A. ampeloprasum (1200 µg kg−1 d.w.) under soil sodium selenate supply twice a week for 4–5 weeks at a dose of 20 mg L−1 [45].
Se levels in leek and shallot after foliar selenate treatment reached 5000 and 8000 mg kg−1 d.w. [46,47], though no comparative evaluation of the efficiency of Se biofortification has been achieved so far.
The chemical form of this element also plays an important role in the efficiency of Se biofortification. In this respect, selenite was shown to be more toxic to plants than selenate, the latter being more easily absorbed than selenite [35]. Chives (A. schoenoprasum) accumulate more Se under a selenate supply compared to selenite and nano-Se (Figure 5) [48]. Furthermore, it is worth highlighting that the amount of Se water-soluble forms in plants treated with nano-Se were 1.5 times lower than in cases of organic Se application [48].
Among three perennial onion species (A. schoenoprasum, A. nutans, and A. obliquum) treated with similar Se doses, the highest Se biofortification levels were recorded in A. schoenoprasum and the lowest in A. obliquum (Figure 5), while the biofortification levels decreased according to the following sequence: selenate > nano-Se > selenite [48]. Selenocystine caused higher levels of Se accumulation in shallot bulbs compared to selenate [46].
The problems of Allium species biofortification with Se under soil application relate to their shallow root apparatus, high Se immobilization by soil components, particularly the adsorption by soil organic matter, the formation of non-soluble compounds with iron and manganese oxides in acidic soils, and several biochemical reactions from the participation of soil microorganisms with the formation of the volatile Se derivatives, di- and tri-selenides [24,49]. According to Kaur et al. [13], Se assimilation by plants under soil Se supply does not exceed 15% of the dose applied, while 85% of this microelement is immobilized by soil components.

4. Arbuscular Mycorrhizal Fungi Utilization

The second aspect of Se biofortification of Allium species is the shallow plant root apparatus causing the need to increase the doses of mineral fertilizers. In this respect, previous reports indicate the high prospects of arbuscular mycorrhizal fungi (AMF) utilization [50]. AMF was proved to expand the volume of the root system and increase the bioavailability of nutrients, especially P and N, but also Se [51,52,53]. The latter characteristic allows AMF to increase the yield and partially reduce the mineral fertilizer supply [54,55,56,57]. Regarding the mentioned topic, among Allium species, garlic ranks the first in terms of importance, as witnessed by the multiplicity of publications devoted to its growth in presence of various AMF such as Glomus fasciculatum [58], G. intraradices [33], and G. mosseae [58]. The growth of A. cepa under AMF inoculation has been described only for Rhizophagus intraradices application [50]. AMF were shown to stimulate the accumulation of both organic and inorganic Se forms and significantly increase yield (Figure 6).
Additionally, AMF inhibit the accumulation of toxic metals in plants, regulating the balance between essential element uptake and contaminant exclusion [59]. As an example, Figure 7 illustrates the effect of different Se forms and AMF inoculations on aluminum accumulation in shallot bulbs [46]; notably, the highest decrease in Al content was recorded under joint Se–AMF application.
Despite such promising results, it is also worth highlighting that the field outcome related to AMF inoculation is not always positive, both in terms of yield and quality [60].

5. Biochar Application

Some problems regarding Allium Se biofortification relate to the low biofortification efficiency of Se in tendentially sandy soils, where most of the Se supplied is easily eluted with rain and watering. In this respect, a partially positive effect of decreasing Se losses may be obtained under the application of Biochar, a carbon-rich component derived from agricultural waste through pyrolysis in anaerobic conditions [61]. The beneficial effect of Biochar relates to its significant porosity, high levels of carbon content, adsorption activity and pH, capability to improve soil fertility, and high water retention, and the increased Se bioavailability in these conditions [27,62,63]. Aneseyee and Wolde [63] reported that the presence of Biochar significantly improved Se assimilation by lettuce in calcareous soils under selenate supply. A beneficial Biochar effect on the yield and biochemical characteristics of A. cepa was demonstrated [63,64], though no attempts have been made to use Biochar in crop systems with Se-enriched Allium species. As Biochar properties greatly depend on the production technology and characteristics of the agricultural wastes used, deeper investigations are needed to reveal the most pronounced opportunities of its utilization in crop Se biofortification.

6. Selenium–Sulphur Interaction

Soil sulfur bioavailability is another important factor affecting the efficiency of Se accumulation in Allium species. Indeed, the chemical similarity of S and Se significantly affects the efficiency of these elements’ assimilation by Allium plants. At the same time, depending on the concentration of S in the soil, the levels of Se accumulation may either increase or decrease [25]. In this respect, in previous research, the onion yield and Se biofortification level increased under sulfur supply in organic soils [65,66] and, contrarily, Se assimilation decreased at high concentrations of sulfates [67]. At high concentrations of Se, selenate competes with S and, contrarily, sulfur assimilation increases at moderate and low Se doses; the latter phenomenon is typical only for Allium but not for Brassica species [68]. Notably, it is well-known that selenates are assimilated by the sulfate pathway, while selenites are assimilated by the phosphate one. Therefore, Allium species biofortification with Se under low soil S levels should be achieved using selenates, while selenite (Se+4) is preferred in cases of high soil sulfate levels and adequate levels of phosphates. The mentioned approach decreases the competition between these two elements, providing efficient absorption of both sulfate and selenates/selenites, and increasing crop yield [25]. A similar synergism–antagonism phenomenon between S and Se was recorded in hydroponically grown A. cepa under different S and Se concentrations [69], which indicates the importance of S–Se interaction.

7. Hormonal Regulation

Hormonal regulation is another factor affecting Se biofortification of plants. Among the phytohormones capable of affecting plant Se status, it is worth mentioning epibrassinolides, heteroauxin, gibberellin, methyl jasmonic acid, ethylene, and salicylic acid (Table 1) [70]. According to numerous publications, the interaction between Se and phytohormones is achieved via changes in gene expression of these compounds under Se supply [71].
Despite the limited information about the phytohormone effect on Se biofortification, the published data indicate that phytohormones may both ensure Se accumulation in plants and change the Se distribution between leaves and bulbs of Allium species (Figure 8).

8. Methods of Se Supply

In general, among different technologies of biofortification such as soil Se application with fertilizers, foliar supply, and hydroponic conditions, the latter two are considered the most suitable to produce functional food: the foliar supply results in a higher Se accumulation level compared to soil treatment and less intensive Se absorption by soil components [76]; and hydroponics allows the maintenance of the constant conditions of biofortification and the prevention of Se environmental pollution. Foliar application of Se is shown to be eight times more efficient than soil supply [35]. Hydroponic technology was used by the Sabinsa corporation to produce Se-enriched garlic (Selenoforce) with a Se content of 1000 mg kg−1 d.w. of garlic powder. Variations of Se concentrations in the nutrient solution may provide a wide range of Se concentrations in the resulting product. For instance, at 2 mg Se L−1 in the nutrient solution, Kopsel et al. [68] obtained garlic cloves with Se content up to 71 mg Se kg−1 d.w. Among Allium species, garlic, A. cepa, and leek are considered the most suitable for hydroponic growing [77].
As previously reported [78], foliar Se supply improves Se absorption and prevent Se immobilization by soils. To increase the efficiency of foliar biofortification, surfactants are used for leaf wettability optimization [79], and multiple processing of plants with diluted Se solution has been indicated as an efficient technology [31]. The maximum permissible concentration of Se for A. cepa should not exceed 100 µg L−1. In these conditions, the level of Se accumulation may reach 4 mg kg−1 d.w. [35].
Despite numerous studies regarding the Se biofortification of Allium species and the anti-carcinogenic effect of the resulting products, the industrial production of Allium plants with high levels of Se has not been achieved so far [80], except for the Sabinsa corporation (USA), which produces Se-enriched garlic. Examples of different technology utilization for the biofortification of Allium representatives are presented in Table 2, Table 3 and Table 4.

9. Effect of Se Biofortification on Product Quality

The improvement of the Allium species nutritional quality due to Se biofortification is deemed one of the most attractive outcomes of Se application. Indeed, though Se is not essential for plants, at low concentrations it may show a growth stimulating effect and increase the biosynthesis of secondary metabolites participating in antioxidant defense [93] (Figure 9).
The changes in plant biochemical composition are species and varietal dependent, suggesting the crucial role of genetic factors. In this respect, biofortification of perennial onion seedlings with sodium selenate provided the highest antioxidant activity levels in A. nutans and A. fistulosum, and the lowest in A. altaicum, while among A. cepa cultivars, ‘Black prince’ and ‘Red lace’ were both the richest sources of antioxidants (due to the presence of anthocyanins) and the most promising Se suppliers (Figure 10).
Numerous investigations indicate that Se can improve antioxidant activity and decrease cell redox potential, as well as alleviate the accumulation of toxic elements such as Hg, As, and Al [94,99,100].
It is well known that Se increases photosynthesis and the production of photosynthetic pigments, thus improving plant growth [101]. Figure 11 provides an example of the effect of a foliar selenate supply on the total antioxidant activity and polyphenol, chlorophyll, and carotene accumulation in A. ursinum leaves.
Along with sulfur derivatives, quercetin plays an important role in Allium antioxidant defense, showing significant anti-diabetic, anti-bacterial, anti-inflammatory, and antioxidant properties, decreasing the risk of cardiovascular diseases, cancer, and Alzheimer disease [102]. In plants, quercetin participates in photosynthesis, antioxidant defense, seed germination, osmoregulation, and auxin transport [103]. Onion and shallot are considered the most powerful sources of quercetin for humans [104]. Biofortification with Se provides the opportunity to significantly increase quercetin content, supposedly via the activation of the phenylalanine ammoniac lyase, essential for the synthesis of polyphenols [105]. Indeed, a two-fold increase in quercetin, 1.5 times increase in anthocyanins, and 1.3 times increase in polyphenol content in A. cepa bulbs were recorded under foliar application of Se [85]. Similar results proving a beneficial effect of Se on the antioxidant status of Allium plants were obtained by other authors [86,106]. Moreover, it is worth mentioning that the efficiency of the Se beneficial effect on plant antioxidant status may vary greatly depending on multiple factors [107]. In this respect, in conditions in India, Keshari et al. [83] reported a 71–86% increase in proline and water-soluble protein content in garlic leaves subjected to different concentrations of selenate. An increase of 80–105% in phenolic content was recorded in the Se concentration range of 2–6 mg L−1, while higher Se concentrations resulted in a flavonoid content decline. Reilly et al. [108] indicated only a tendency for polyphenol and flavonoid increases in A. cepa under Se supply. Adhikari et al. [109] did not record any effect on flavonoid accumulation under Se supply at a dose of 20–50 mg m−2. Furthermore, while Gazhemi et al. [110] reported a decrease in flavonoid and allicin accumulation in garlic under Se treatment, Shokri et al. [111] demonstrated a significant increase in allicin accumulation in drought conditions under Se supply [111]. Contrarily, Gandea et al. [45] found a negative correlation between Se doses and total polyphenol content, and the existence of complex relationships between Se and individual phenolics. At the concentration of 1 mg Se L−1, the amount of gallic and ferulic acids decreased, while the quercitrin and quercetin levels increased. In A. schoenoprasum, there was a positive correlation, with the gallic acid content increasing with the increase in Se concentration. Furthermore, each perennial species demonstrated a unique flavonoid composition predominantly determined by genetic factors.
The presented data reveal a serious problem of Allium species biofortification with Se, and the urgent need to identify optimal conditions for obtaining products with high contents of biologically active compounds including polyphenols, flavonoids, vitamin C, and others [92,112], and decreased amounts of toxic elements such as As and Al [101]. In this respect, the utilization of silicon derivatives (silicates and nano-Si) as anti-stressor factors may reduce the unfavorable variability of Se biofortification and increase product quality [113,114,115,116]. Unfortunately, to date, no literature data are available about the Si effect on Allium species under Se supply.

10. Changes in Mineral Composition

Selenium is known to positively affect mineral composition in plants, including Allium species. Vucović et al. [89] demonstrated that soil supply with 10 g of sodium selenate per ha promoted the accumulation of S, K, P, and other biogenic elements both in A. schoenoprasum and A. odorum at the first year of vegetation, contrary to the second year where the highest increase in essential element content was detected at a dose of 20 g ha−1 for A. schenoprasum and 30 g ha−1 for A. odorum. A beneficial effect of joint Se–AMF application was recorded in the mineral composition of A. sativum and A. cepa [92], in both of which, under Se supply in the presence of AMF, the contents of P, K, and Mg increased, though the intensity of beneficial changes was more pronounced in A. cepa bulbs than A. sativum cloves [92]. Se-enriched onion showed increased levels of B, Cu, Fe, Mn, Si, and Zn, while in garlic only Mo and Zn were augmented. Moreover, in addition to the mineral composition changes, Se biofortification of Allium plants reportedly had increased yield [76]. According to the literature data, the intensity of mineral composition changes in Allium species depends on the Se dose, the chemical form of the element, and genetic peculiarities [84,88,90,99]. Examples of the protective effect of Se against different forms of environmental stresses in Allium representatives are presented in Table 5 and Figure 12.

11. Functional Food Products

The production of Allium-based functional food enriched with Se is intriguing, despite the wide spectrum of peculiarities related to selenium supply and the availability of a range of biofortification technologies. Indeed, Se-fortified Allium species may be used ‘fresh’ (garlic, onion, wild garlic, perennial onion), as spices (garlic enriched with Se powder), as a component of appropriate biologically active food supplements, and for the production of special functional food products with high levels of methylated Se-containing amino acids. The latter are especially interesting due to the non-sufficient utilization of many Allium representatives in the food industry and, in this respect, the leaves of garlic, leek, and perennial onions are especially important. Indeed, leek leaves compose about 33–66% of the total leek biomass and are usually considered as undesirable waste, notwithstanding their high content of biologically active compounds and high dry matter content [47]. The wide utilization of plant additives in the production of bread enriched with essential macro- and micro-elements and natural antioxidants [121,122] entails high prospects for the utilization of Allium species biofortified with Se in bread production. Investigation of leek leaves demonstrated a high beneficial effect at a dose of 4%, high Se preservation during bread baking (Se losses did not exceed 3%), and an increased content of antioxidants in the resulting bread. Taking into account that leek shows cardio-protective, anti-microbial, hypo-cholesteric, hypo-glycemic, and anti-carcinogenic effects [123], the production of such bread will facilitate consumer ingestion of significant methylated forms of Se-containing amino acids (about 22% of the adequate consumption level) and polyphenols, including quercetin, as well as a solution for leek waste utilization [47]. Moreover, it is worth highlighting that the utilization of leek leaves with high levels of Se decreased bread porosity by 8.3%, consistent with the similar reduction (−10%) in bread produced from selenium-enriched wheat [124].
The production of ‘Black garlic’ from cloves enriched with Se is very innovative [50]. There is a whole series of garlic-based products at the world market: fresh and dried cloves, garlic oil [125] and ethanol extracts (the so-called ‘Aged Garlic’) [126], and also ‘Black garlic’, produced in Korea and several other countries [127]. ‘Black garlic’ formed in conditions of long bulb storage at high temperature and humidity shows anomalously high antioxidant activity, exclusive anti-carcinogenic properties, and is widely used in traditional medicine in China, Korea, and Japan [127,128]. The production of black garlic from garlic biofortified with Se resulted in a significant increase in Se and monosaccharide content in the derived ’Black garlic’ [129,130], but did not significantly affect the total antioxidant activity compared to the product obtained from a common garlic. Prospects of ‘Black garlic’ utilization are still under investigation.
The production of microgreens is more scarcely studied as a functional food based on Se-biofortified Allium species [131]. At present, Allium microgreen production is achieved on leek, A. cepa, A. fistulosum, and A. schoenoprasum [132], though to date, Se biofortification has been carried out only in A. fistulosum seedlings [133]. In general, biofortification of microgreens with Se in hydroponic conditions is known to significantly increase the antioxidant status, yield, and microelement accumulation [134,135], which is consistent with the results obtained by Newman [133] in A. fistilosum microgreens, and in Se-enriched seedlings of Allium cepa and perennial onion (Figure 10) [97].

12. Conclusions

The presented results, based on the scientific experiences acquired worldwide about the Se biofortification of Allium species, indicate two important aspects: (1) the high variability of Allium crop yield and quality responses under Se supply is greatly affected by genetic peculiarities and environmental stresses; (2) the need for optimizing plant growth technology to obtain the target nutritional characteristics of the derived functional product with high anti-carcinogenic activity. In this respect, further investigations should identify the most efficient strategies to produce Se-enriched Allium crops, such as the utilization of Biochar, formulations to enhance plant stress tolerance such as Si compounds, development of cost-effective AMF-based technology, and detailed indications regarding the suitability of different Se forms, especially regarding the scarcely investigated nano- and organic Se compounds. Taking into account the outstanding biological properties shown by Allium crops upon high Se level applications, the mentioned investigations may have an important economic impact. Indeed, based on the essentiality of Se for human beings and the high risks of viral, cardiovascular, and oncological diseases, the mentioned products may fully fit Hippocrates’ words: “Let food be medicine and medicine be food,” and may create an important niche in the modern food industry.

Author Contributions

N.G., V.N., L.S., O.C.M., A.V.T. and G.C. conceived the review topics and were involved in the bibliographic search, as well as writing the draft and final version of the manuscript upon its critical revision. Z.A., S.N. and V.N. contributed to the bibliographic search and critical revision of the manuscript’s final version. Z.A. was involved in the bibliographic search and manuscript formatting. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Scheme 1. Chemical structure of selenomethionine and selenocysteine.
Scheme 1. Chemical structure of selenomethionine and selenocysteine.
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Figure 1. The main chemical forms of Se in cereal, legume, Brassica, and Allium crops.
Figure 1. The main chemical forms of Se in cereal, legume, Brassica, and Allium crops.
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Figure 2. The main chemical forms of Se in Se-biofortified Allium species. A.ascalonicum [29]; A. porrum [30]; A.schoenoprasum [31]; A. fistulosum [32,33]; A.sativum [34], A.cepa, A. sativum odorless [35].
Figure 2. The main chemical forms of Se in Se-biofortified Allium species. A.ascalonicum [29]; A. porrum [30]; A.schoenoprasum [31]; A. fistulosum [32,33]; A.sativum [34], A.cepa, A. sativum odorless [35].
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Figure 3. General patterns of Se accumulation at different Se doses.
Figure 3. General patterns of Se accumulation at different Se doses.
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Figure 4. Factors affecting Se accumulation.
Figure 4. Factors affecting Se accumulation.
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Figure 5. Species differences in Se accumulation under foliar supply of different Se forms [48].
Figure 5. Species differences in Se accumulation under foliar supply of different Se forms [48].
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Figure 6. AMF effect on shallot bulb yield (a) and the accumulation of organic and inorganic Se forms (b) [46].
Figure 6. AMF effect on shallot bulb yield (a) and the accumulation of organic and inorganic Se forms (b) [46].
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Figure 7. Effect of AMF and Se on Al accumulation in shallot bulbs [46].
Figure 7. Effect of AMF and Se on Al accumulation in shallot bulbs [46].
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Figure 8. Effect of phytohormones on Se accumulation in leaves and bulbs of garlic foliar treated with sodium selenate under heteroauxin (125 mg L−1), epibrassinolides (0.025 mg L−1), and gibberellin (125 mg L−1) supply [72,73].
Figure 8. Effect of phytohormones on Se accumulation in leaves and bulbs of garlic foliar treated with sodium selenate under heteroauxin (125 mg L−1), epibrassinolides (0.025 mg L−1), and gibberellin (125 mg L−1) supply [72,73].
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Figure 9. Effect of Se biofortification on yield and biochemical characteristics of Allium plants.
Figure 9. Effect of Se biofortification on yield and biochemical characteristics of Allium plants.
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Figure 10. Varietal and species differences in the effect of Se on seedling total antioxidant activity of perennial onion (1—A. altaicum; 2—A. obliquum; 3—A. nutans; 4—A. fistulosum) and Allium cepa cultivars (5—cv. Primo; 6—cv. Black prince; 7—cv. Red lace) (10 mg of selenate per 1 L of water) [98].
Figure 10. Varietal and species differences in the effect of Se on seedling total antioxidant activity of perennial onion (1—A. altaicum; 2—A. obliquum; 3—A. nutans; 4—A. fistulosum) and Allium cepa cultivars (5—cv. Primo; 6—cv. Black prince; 7—cv. Red lace) (10 mg of selenate per 1 L of water) [98].
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Figure 11. Increase in A. ursinum antioxidant status under foliar selenate application (50 mg L−1) [90].
Figure 11. Increase in A. ursinum antioxidant status under foliar selenate application (50 mg L−1) [90].
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Figure 12. Changes in mineral composition of A. sativum under soil selenate supply (75 mg per m2). The value related to Se is reduced by 10 times [101]. (*) The value is decreased 10 times.
Figure 12. Changes in mineral composition of A. sativum under soil selenate supply (75 mg per m2). The value related to Se is reduced by 10 times [101]. (*) The value is decreased 10 times.
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Table 1. Effect of phytohormones on plant Se status.
Table 1. Effect of phytohormones on plant Se status.
PhytohormoneBiochemical EffectRef.
EpibrassinolidesIncrease in Se accumulation by garlic leaves by 25%[72,73]
HeteroauxinHigh Se levels in young garlic leaves and reproductive organs, Se content increase in leaves and bulbs by 15–16% via heteroauxin supply (125 mg L−1)[73,74]
GibberellinSe accumulation increase in garlic cloves by 26% under single plant spray using gibberellin solution (125 mg L−1)[73]
Methyl jasmonic acid, ethylene, salicylic acidHyperaccumulators with extremely high Se content possess higher levels of these hormones compared to non-accumulators[75]
Table 2. Examples of Allium species biofortification with foliar Se supply.
Table 2. Examples of Allium species biofortification with foliar Se supply.
SpeciesSe FormEffect of Foliar Se SupplyRef.
A. sativumSe (VI) Maximum efficiency of N utilization and yield at 150 kg ha−1 N and 10 mg selenate L−1[81]
Gypsum (0–20–40 ppm S) + Se (VI) (1–15–30 ppm Se) Increased AOC, TP, sugar, and allicin under joint application of high S and low Se, which provides better results with foliar Se supply than soil Se treatment at the optimal concentration of 10 mg Se L−1[82]
Se (VI) 0.5–10 mg selenate L−1Pro-oxidant effect of 8–10 mg L−1 selenate solution increases proline and SOD and decreases total protein, sugar, phenolics, and flavonoids[83]
10–100 mg L−1 Se (VI)10–50 mg Se L−1 increased yield and AOA[84]
A. cepaSe (VI) 50 mg L−1Varietal differences in sugar, TP, and AOA levels[85]
0–200 g Se (VI) ha−1The highest yield at 100 g ha−1 had no effect on pungency and mineral composition, with foliar supply more beneficial than soil supplementation[76]
10–100 µg Se mL−1The highest yield, AOC, and TP were at 50 µg Se mL−1[86]
15–60 g Se ha−1Out of 2 cultivars, only one showed significant increases in yield and dry weight[87]
A. cepa, A. sativumAMF + Se (VI)
0.26 mM solution		The increases in yield, monosaccharides, Fl, and mineral content under AMF and Se supply were highly specific, differing between garlic and onion grown in similar environmental conditions[88]
A. cepa L. Aggregatum groupAMF + Se (VI)/Se(Cys)2
0.26 mM solution 		AMF increased Se accumulation; Se(Cys) increased yield more efficiently without AMF supply, and the opposite phenomenon was recorded for Se (VI)[46]
A. schoenoprasum,
A. odorum		10–30 g Se (VI) ha−1Increase in TP and Fl in A. schoenoprasum in both seasons,
and in A. odorum only in drought conditions; with 10 g ha−1 was the highest mineral content without drought, and under drought, it was 20 g ha−1 for A. schoenoprasum and 30 g ha−1 for A. odorum.		[89]
A. nutans, A. obliquum, A. schoenoprasumSe (VI) Leaf Se levels were affected by genetic factors and the chemical form of Se, with the highest values in A. schoenoprasum and Se (VI)[47]
A. ursinumSe (VI)
50 mg L−1		Increases in chlorophyll, carotene, TP, and AOC; Cr, Fe, V increased and Si decreased[90]
A. porrum75 mg Se (VI) m−2Increases in TP and monosaccharides in pseudo-stems and TP in leaves[47]
AOC: antioxidant capacity; TP: total phenolics; Fl: flavonoids; AMF: arbuscular mycorrhizal fungi; Se(Cys)2: selenocystine.
Table 3. Examples of Allium species biofortification with soil Se supply.
Table 3. Examples of Allium species biofortification with soil Se supply.
SpeciesSe FormEffect of Soil Se SupplyRef.
A. sativum0–15 kg ha−1 Se (VI) and Se (IV) Decreased accumulation of Mg, Mn, Cu, Fe, P, and S, but increased Zn content, with no effect on garlic growth; Se content was up to 49.5 mg kg−1 d.w. Se supplementation led to significant modifications of the accumulation and distribution of Zn, Mg, Mn, Fe, Cu, P, and S between leaves, bulbs, and roots[91]
A. cepaSe (VI)/Se (IV)Bulbing was delayed under Se supply. Se (VI) induced higher AOA than Se (IV); Se distribution was as follows: bulbs ≥ leaves > roots[92]
A. fistulosum, A. cepa, A. ampelo-prasum, A. schoe-noprasum, A. sene-scens, subsp. montanum,
A. obliquum		3, 5, 20 mg kg−1 Se (VI)Se biofortification led to evident changes in 57 polyphenol profiles, with species-specific variations. The optimal concentration was 5 mg Se L−1[45]
A. fistulosum1, 3, 5, 15 mg Se (IV) L−1No growth inhibition; the maximum Se level was 30 mg kg−1 d.w.[34]
Se (IV)/SeMet 10–100 mg L−1The amounts of SeCys and MeSeCys depend on the chemical form and dose of Se supplied; Se accumulation levels in cases of SeMet are significantly higher than under Se (IV) supply[32]
AOA: total antioxidant activity; SeMet: selenomethionine; SeCys: selenocysteine; MeSeCys: Se-methyl-selenocysteine.
Table 4. Examples of Allium species biofortification with hydroponic Se supply.
Table 4. Examples of Allium species biofortification with hydroponic Se supply.
SpeciesSe FormEffect of Se Supply in Hydroponic SystemRef.
A. sativum0–3–5 µM L−1Lower levels of lipid peroxidation SOD activity, higher levels of GPx and catalase in garlic shoots[67]
Se (VI)/Se (IV) 50 µM L−1Garlic seedlings produced more methylated forms of Se amino acids under Se (VI) than Se (IV); Se–S antagonism was observed[93]
> 1 mg L−1 Se(VI)/Se (IV)Se (VI) and Se (IV) at high concentrations (>1 mg L−1) inhibited Hg accumulation to the same extent[94]
4–16 mg L−1 Se(VI)Se alleviated salt stress and improved TP in plants[95]
A. cepa0.5–2 mg L−1At low concentrations, Se stimulated S accumulation; Se levels decreased according to the following: leaves > roots > bulbs[68]
Nano-Se: 10–30 early stage;
20–60 middle stage;
10–20 mg L−1 late stage		Optimal conditions to obtain onion seedlings with the highest content of organic Se[96]
2 mg L−1 Se (VI)Se decreased S content in bulbs[97]
A. schoeno-prasum10–100 mg L−1 Se(IV) or SeMetSe (IV) elicited more inorganic Se in the resulting product than SeMet. The Se concentration reached 200 mg kg−1 d.w.[31]
A. porrumSe (VI)/Se (IV)A. porrum may accumulate more than 1000 mg Se kg−1 d.w. without growth inhibition; despite the higher bioavailability of Se (VI), Se (IV) led to significantly higher organic Se (MeSeCys and SeMet)[30]
A. fistulosum, A. nutants, A. obliquum, A. altaicum, 3 cvs of A. cepa10 mg Se (VI) L−1Species and varietal differences in Se accumulation levels, AOC, and TP. Se concentration decreased according to the following: A. fistulosum > A. nutans > A. obliquum > A. altaicum[98]
GPx: glutathione peroxidase; SOD: superoxide dismutase; TP: polyphenols; SeMet: seleno-methionine; MeSeCys: Se-methyl-selenocysteine.
Table 5. Examples of the protective effect of Se against different environmental stresses in A. sativum and A. cepa plants.
Table 5. Examples of the protective effect of Se against different environmental stresses in A. sativum and A. cepa plants.
ConditionsEffectReferences
Drought, vegetative experiment, foliar selenate supplyAllicin, Se, and S increased in bulbs, and water-soluble proteins and protein in leaves[111]
Foliar selenate supply, field conditionsYield increased by 1.32 times[117]
Salinity, 60 MM NaCl. Hydroponics, 16 mg L−1 selenate supplyA low dose of Se enhanced plant tolerance to salt stress and decreased oxidative injury by boosting the activities of antioxidants, decreasing garlic MDA and increasing photosynthetic pigments, yield, and enzymes of antioxidant activity[95,118]
Selenate, selenite 1 mg L−1 + mercury saltsInhibition of Hg accumulation and yield increased[94]
Selenite, perliteInhibition of Hg accumulation in A. fistulosum[119]
Selenate, semi-arid conditionsIncrease of A. cepa yield[87]
Salinity, selenate, silt loam soil with 8 dS m−1 salinity,
0.5 and 1 kg Se ha−1		A. cepa yield increase and decrease in Na+ accumulation. Maximum yield occurred with enhancements in the physiological and qualitative indices of Allium cepa[120]
MDA: malonic dialdehyde.
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Golubkina, N.; Nemtinov, V.; Amagova, Z.; Skrypnik, L.; Nadezhkin, S.; Murariu, O.C.; Tallarita, A.V.; Caruso, G. Selenium Biofortification of Allium Species. Crops 2024, 4, 602-622. https://doi.org/10.3390/crops4040042

AMA Style

Golubkina N, Nemtinov V, Amagova Z, Skrypnik L, Nadezhkin S, Murariu OC, Tallarita AV, Caruso G. Selenium Biofortification of Allium Species. Crops. 2024; 4(4):602-622. https://doi.org/10.3390/crops4040042

Chicago/Turabian Style

Golubkina, Nadezhda, Victor Nemtinov, Zarema Amagova, Liubov Skrypnik, Sergey Nadezhkin, Otilia Cristina Murariu, Alessio Vincenzo Tallarita, and Gianluca Caruso. 2024. "Selenium Biofortification of Allium Species" Crops 4, no. 4: 602-622. https://doi.org/10.3390/crops4040042

APA Style

Golubkina, N., Nemtinov, V., Amagova, Z., Skrypnik, L., Nadezhkin, S., Murariu, O. C., Tallarita, A. V., & Caruso, G. (2024). Selenium Biofortification of Allium Species. Crops, 4(4), 602-622. https://doi.org/10.3390/crops4040042

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