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Review

Selenium Biofortification of Crop Food by Beneficial Microorganisms

by
Yuanming Ye
,
Jingwang Qu
,
Yao Pu
,
Shen Rao
,
Feng Xu
and
Chu Wu
*
College of Horticulture & Gardening, Yangtze University, Jingzhou 434025, China
*
Author to whom correspondence should be addressed.
J. Fungi 2020, 6(2), 59; https://doi.org/10.3390/jof6020059
Submission received: 30 March 2020 / Revised: 25 April 2020 / Accepted: 26 April 2020 / Published: 3 May 2020
(This article belongs to the Special Issue Fungi and Fungal Metabolites for the Improvement of Human and Animal Nutrition and Health)
Review Reports Versions Notes

Abstract

Selenium (Se) is essential for human health, however, Se is deficient in soil in many places all around the world, resulting in human diseases, such as notorious Keshan disease and Keshin–Beck disease. Therefore, Se biofortification is a popular approach to improve Se uptake and maintain human health. Beneficial microorganisms, including mycorrhizal and root endophytic fungi, dark septate fungi, and plant growth-promoting rhizobacteria (PGPRs), show multiple functions, especially increased plant nutrition uptake, growth and yield, and resistance to abiotic stresses. Such functions can be used for Se biofortification and increased growth and yield under drought and salt stress. The present review summarizes the use of mycorrhizal fungi and PGPRs in Se biofortification, aiming to improving their practical use.

1. Introduction

At present, it is widely accepted that selenium (Se) possesses multiple physiological functions in various biological systems as an integral part of a range of proteins containing Se. Therefore Se is important for human health. However, Se distribution in the earth’s crust is greatly uneven, ranging from 0.005 mg·kg−1 in Finland to 8000 mg·kg−1 in Tuva-Russia [1]. Se deficiency has been reported in many places all around the world including China, North America, New Zealand, Australia, Sweden, and Finland [2,3,4,5]. Some notorious diseases are directly related to Se deficiency, such as Keshan disease and Keshin–Beck disease, two endemic diseases related to Se deficiency. Keshan disease was first prevalent at alarge scale in 1935 in Keshan county, Heilongjiang province, China. Keshan disease generally occurs in children and women of childbearing age and its symptoms are related to impairment of cardiac function, cardiac enlargement, and arrhythmia [6]. Although the main factor was not determined for the disease in etiology, it was closely related to Se because it was found that there was an obvious Se deficiency in local soil, and Se supplementation could partly control the disease. An investigation analyzed some physiological parameters, including blood Se level, glutathione peroxidase-1 (GPx-1) activity, and variance at codon 198 in GPx-1 gene, and found that the main risk factors for the disease were low GPx-1 activity, Keshan disease family history, and living in an endemic area [7], suggesting that Keshan disease is closely related to low GPx-1 activity. Kaschin–Beck disease is an osteoarthropathy, which manifests as severe dysarthrosis of joints, shortened fingers and toes, and in severe cases dwarfism. In China, the disease is prevalent in the Tibetan Plateau [8,9]. An investigation carried out by Zhang et al. [8] showed that the levels of environmental Se were very low, and Kaschin–Beck disease in the Tibetan Plateau was much severe with decreasing environmental Se under the Se-deficient condition, suggesting the relationship between Kaschin–Beck disease and Se deficiency in the Tibetan Plateau. In addition, Se is related to other human diseases and health, such as cancer [10,11,12,13], muscle disease [14], and healthy aging and longevity [15,16,17]. Therefore, it is essential to maintain Se homeostasis in human body [18,19]. It was estimated that Se intake of >900 μg·day−1 is harmful, and intake of <30 μg·day−1 is not enough [20]. Some data have shown that over 800million people all around the world might suffer from Se deficiency [21,22,23,24,25,26]. Therefore, sufficient dietary Se uptake is important for human health.
Acquired Se is converted into some proteins thatcontain at least one of the two amino acids (i.e., selenocysteine (SeCys) and selenomethionine (SeMet)) as a key component (i.e., selenoproteins). Human health and diseases are related to selenoproteins, and selenocysteine is regarded as the 21st proteinogenic amino acid. The human genome encodes about 30 selenoproteins. In the article written by Reeves and Hoffmann [27], they described functions of selenoproteins in detail. Among the selenoproteins in human, glutathione peroxidases (GPxs) seem to be more important, because they include eight proteins (GPx1–GPx8) having antioxidant properties with multidimensional roles in living cells, ranging from H2O2 homeostasis to regulation of apoptosis [28]. Therefore, enough Se uptake is essential for functional maintenance of these selenoproteins. Since Se is deficient in many places all around the world, Se fortification in food is necessary. In view of high toxicity of selenite and selenate, Se biofortification is relatively bio-safe. Organic Seleno-compounds act as potential therapeutic and chemo-preventive agents that function as antioxidants, enzyme modulators, antitumor, antimicrobials, antihypertensive agents, antivirals, and cytokine inducers [29]. Organic seleno-compounds are provided with crop food [30,31,32,33,34,35], vegetables [36,37,38,39,40,41,42], fruits [43,44,45], and even nuts [46,47,48]. Therefore, how to increase concentrations of organic seleno-compounds in these plants is of significance for improvement of dietary Se acquisition by human being.
Se biofortification may be carried out by multiple ways, such as application of Se fertilizers on leaves [49,50,51,52,53] and in soil [52,54,55]. Se-enriched organic fertilizers are also applied. For example, Bañuelos et al. [56] used Se-enriched Stanleya pinnata to cultivate Se-enriched broccoli and carrots, and found that more than 90% of organic Se was converted to inorganic selenate and selenite. Se foliar application seems to be most effective way to fortify Se uptake in most arable crops [52,57]. However, a contrary result was observed by Lyons et al. [58]. They found foliar application was less efficient than application to soil at planting (at application rates of 40 and 120 g·ha−1, respectively) in Australian trials. The agronomic application of Se fertilizers are more expensive and short-term solutions, especially in large-scale fields. Relatively, agronomic Se biofortification with beneficial microorganisms (BMOs) is a more inexpensive and long-term solution, especially in poor places and Se-rich places, such as Enshi, Hubei province, China [59] and Pineridge Natural Area, a seleniferous site west of Fort Collins, CO, USA [60].
In the present article, we focus on the roles of beneficial microorganisms in Se biofortification and our aim is to improve use of beneficial microorganisms in practice.

2. Improvement of Se Biofortification by BMOs

Symbiosis of plants with BMOs is helpful for plant growth and to increase in micronutrition uptake and resistance to abiotic and biotic stresses. Based on the characteristics of BMOs, BMOs can be used for Se biofortification. BMOs, including mycorrhizal fungi (endo- and ectomycorrhizal fungi), root endophytic fungi (REFs), and PGPRs, are popular in biofilmed biofertilizers. Arbuscular mycorrhizal fungi (AMFs) are preferential to colonize in roots of angiosperms, and ectomycorrhizal fungi are popular in gymnosperms. Most REFs possess a wide range of plant hosts.

2.1. Arbuscular Mycorrhizal Fungi

Arbuscular mycorrhizal fungi are used for Se biofortification because of their ability to enhance nutrition uptake of their host plants (Table 1). Functions of mycorrhizal fungi have been the primary focus of research, especially those involved in phosphate uptake. The genomes of these fungi encode some high-affinity inorganic phosphate transporters and some of them have been isolated and identified [61,62,63,64,65]. On the other hand, in planta, some symbiosis-specific phosphate transporters can be induced by symbiosis with mycorrhizal fungi [61,66,67,68,69,70,71,72]. Thus, the interaction between plants and mycorrhizal fungi strengthens phosphate uptake and transportation to host plants [73,74,75,76,77]. Similarly, there are some sulfate transporters encoded by genomes of mycorrhizal fungi, such as sulfate transporters GBC38160.1 and GBC25943.1 and sulfate permeases PKY50973.1 in arbuscular mycorrhizal fungus Rhizophagus irregularis, sulfate transporters EDR02618.1 and EDR02177.1, and sulfate permeases EDR11271.1 and EDR00466.1 in ectomycorrhizal fungus Laccaria bicolor. Since Se and sulfur (S) belong to the same element family (VI-A), the chemical properties of Se are very similar to S. Se is absorbed as selenate or selenite, which is metabolized via the sulfur assimilation pathway in plants, leading to biosynthesis of SeCys, SeMet, and other Se isologs of various S metabolites [78,79,80,81,82]. Se can be transported by sulfur transporters to host plants, just like phosphate transported between mycorrhizal fungi and their host plants, such as the high-affinity sulfate permease [83] and the high-affinity sulfate transporters Sultr1:1 and Sultr1:2 [84,85,86]. The two sulfate transporters are proton-sulfate symporters, such that for every molecule of selenate entry into root cells, three protons are taken up. Sulfate transporters function in Se accumulation in food crops. Wheat genotype ‘Puelche’ is the most Se-tolerant and has the greatest Se accumulation among the three wheat genotypes studied (i.e., ‘Puelche’, ‘Tinto’, and ‘Kumpa’), such that its Se accumulation was related to the strongest transcript level of the sulfate transporter TaeSultr4.1 in roots [87]. In addition, other transporters also take part in Se transport, such as silicon transporters in rice [88] and tomato [89], phosphate/orthophosphate transporters in wheat [90], rice [91,92,93], tomato [89], and yeast (Saccharomyces cerevisiae) [94,95], and monocarboxylates transporters in yeast (S. cerevisiae) [96]. Thus, it is reasonable to explain the experimental results that plant availability of selenate and selenite was influenced by the competing ions phosphate and sulfate [97,98]. Competition between phosphate and Se uptake led to decrease in Se accumulation translocation coefficients, and Se concentrations in wheat roots, stems, leaves, and spikes when phosphate fertilizers were applied to selenite fertilized soil [99]. However, a different case occurred. An investigation was carried out on sulfate and selenate uptake in Astragalus species (two Se hyperaccumulators A. racemosus and A. bisulacatus and two closely related non-accumulators A. glycyphyllos and A. drummondii), and results showed that sulfur deficiency increased Se accumulation, and increased Se supply increased sulfate accumulation in both root and shoot tissues [100]. In certain Astragalus species, the high expression of sulfate transporters led to enhanced ability of Se uptake and translocation, and therefore contributed to the Se hyperaccumulation trait. At present, except for sulfate and phosphate transporters, it is not clear whether other transporters have their homologous proteins in mycorrhizal fungi. If these homologous proteins occur in mycorrhizal fungi, they could mediate Se transport to host plants. On the other hand, decreases in sulfate bioavailability and mycorrhizal symbiosis enhanced expression of sulfate transporters, resulting in increase in ability to absorb sulfate and consequent uptake of Se [101,102,103,104]. Similarly, Se deficiency also enhances expression of sulfate transporters, resulting in an increase in Se uptake, and mycorrhizal symbiosis also enhances Se uptake.
Some evidence supports the role of mycorrhizal fungi in enhancing Se uptake in plants. Wheat seedlings were inoculated with Glomusversiform or Funneliformis mosseaein hydroponic culture medium for eight weeks, the two arbuscular mycorrhizal fungi significantly increased selenate and selenite uptake by wheat root, but they did not show effect on uptake of SeMet [105]. Meanwhile, compared to non-mycorrhizal roots, mycorrhizal roots showed significantly higher Vmax for selenate and selenite uptake (179.6 vs. 55.93 nmol·g−1DW·h−1 for selenate and 1688.0 vs. 860.3 nmol·g−1DW·h−1 for selenite). Higher Se accumulation was carried out through up-regulating the expression of three genes encoding sulfate transporters, i.e., TaSultr1:1, TaSultr1:3, and TaSultr2:1, in the mycorrhizal roots, especially TaSultr1:1. In mycorrhizal roots with G. versiform and F. mosseae, the relative expressions of TaSultr1:1 gene was significantly up-regulated by 2.18-fold and 2.12-fold, respectively. Garlic (Allium sativum L.) is an important condimental species. This species ispopular all around the world because of its diallyl disulfide, a component of garlic, which can inhibit proliferation of various cancer cells (e.g., colon, lung, and skin cancer cells) and WEHI-3 leukemia cells [115,116,117]. Garlic is used for Se biofortification with mycorrhizal fungi. A survey of applying selenate fertilizer and mycorrhizal fungus Glomus irtraradices to soil was conducted, and the results showed mycorrhizal addition increased the Se uptake of garlic by10-fold to 15 μg·g−1DW, and fertilization with selenate and amendment of mycorrhizal fungi strongly increased the Se concentrations in garlic to around 1% [55]. Further analyses showed that the amendment of soil with the mycorrhizal fungus and/or selenate increased selenate concentrations in garlic, but did not affect distribution of detected Se species in garlic. In Se-contaminated soil, mycorrhizal fungi inoculation increased Se accumulation of plants. Alfalfa, maize, and soybean seedlings were cultivated in the soil contaminated with different levels of Se, and results showed that mycorrhizal fungi inoculation decreased Se accumulation in roots and shoots of all the plants at low Se levels (0 or 2 mg·kg−1), but increased Se accumulation in alfalfa shoots and maize roots and shoots at Se level of 20 mg·kg−1 [112]. Contrary results were observed on ryegrass (Lolium perenne cv. ‘Barclay’) [111]. Their results showed that Se concentrations in roots of ryegrass were not affected by mycorrhizal inoculation with the AMF G. mosseae, but mycorrhizal inoculation significantly reduced Se concentrations in shoots [111], further decreasing Se uptake in whole plants. Lettuce (Lactuca sativa L.) is one of the most consumed leaf vegetables in some places around the world because of its good properties, such as high levels of antioxidants (such as carotenoids, polyphenols, ascorbate, α-tocopherol) and dietary fiber [118,119,120], thus it is suitable for Se biofortification to enhance dietary Se consumption. When two lettuce cultivars ‘Batavia Rubia Munguia’ (BRM) and ‘Maravilla de Verano’ (MV) were treated with Se compounds (selenite, organic Se compounds SeU and SeCH3) and AMFs (a mixture of Rhizophagus intraradices and Funneliformis mosseae), their growths were continuously improved by AMFs, except for BRM under treatment of SeCH3 [106]. The positive effect of AMFs on plant biomass was different among lettuce cultivars and forms of seleno-compounds, and BRM lettuce plants showed the highest mycorrhizal efficiency index (MEI) under treatment of SeU, MV lettuce plants with the highest MEI under SeCH3, suggesting that the two lettuce cultivars possessed preference for different seleno-compounds when they were inoculated with AMFs. Meanwhile, AMFs inoculation significantly affected mineral accumulation in the leaves of BRM lettuce. In general, mycorrhizal inoculation significantly increased levels of macro and micronutrients, but significantly reduced Se levels in leaves of BRM lettuce. Significant interaction occurred about Se levels in shoots of BRM lettuce between seleno-compounds and AMFs inoculation. Similar status occurred on MV lettuce. Under treatment of selenite, AMFs inoculation reduced Se concentrations in leaves of MV lettuce. In contrast, under treatment of organic seleno-compound SeCH3, MV lettuce never accumulated detectable levels of Se in leaves, regardless of whether they were inoculated with AMFsor not. Treatment of organic seleno-compound SeU slightly increased Se concentrations in leaves of MV lettuce without AMFs inoculation [106]. Other research showed similar results [108]. All the results suggest that combination of seleno-compounds and AMFs inoculation does not increase Se levels in lettuce leaves, although it increases levels of some macro- and micronutrients and antioxidants. Therefore, some AMFs are not suitable for Se biofortification in lettuce. Of course, other AMFs should be chosen to examine their role in Se biofortification in lettuce under treatment of seleno-compounds. At present, it is not clear whether lettuce symbioses with some ectomycorrhizal fungi. Thus, more research is necessary for Se biofortification in lettuce.
Consversa et al. [107] investigated the effect of Se fern application and AMFs (Rhizophagus intraradices and Funneliformis mosseae) inoculation on Se biofortification for two years, such that Se fern application was carried out on green asparagus (Asparagus officinalis L.). Their experimental results showed that Se levels in non-mycorrhizal A. officinaliscv. ‘Grande’ plants increased in trial A1 as exogenous selenate levels increased. Under selenate treatment of 75 and 125 g·ha−1, Se concentrations in spears increased 4.7 and 6.4-fold on a dry weight basis compared to control, respectively. Similar results occurred in trail B1. In trail B1, Se concentrations in spears were significantly affected by the interaction between Se amendment and AMFs inoculation. In spears of plants without Se amendment, Se levels were similar in mycorrhizal and non-mycorrhizal plants. All the results suggest a combination of Se amendment and mycorrhizal fungi greatly improve Se biofortification in A. officinalis and the combination should be recommended in field by large scale. However, contrary results have also been observed. When the AMF Glomus mosseae was used for inoculation with alfalfa (Medicago sativa L. cv. ‘Chuangxin’), maize (Zea mays cv. ‘ND108′), and soybean (Glycine max cv. ‘Zhonghuang No. 17′), mycorrhizal inoculation significantly decreased Se concentrations in roots with the highest reduction for alfalfa (50–70%), while it was less than 40% for maize and soybean, Se concentrations in shoots decreased by 7–38% for mycorrhizal treatment, and the difference caused by inoculation influence was insignificant among the plant species [112]. When Se was added at the levels of 0 and 2 mg·kg−1, the total Se accumulation in roots and shoots of all the three plant species were lower in mycorrhizal than in non-mycorrhizal treatment, while the opposite pattern was observed in roots of maize and shoots of alfalfa and maize when Se was applied at 20 mg·kg−1 [112]. These results show negative effects on Se accumulation in these plant species when low levels of exogenous Se were added.
In addition, some ectomycorrhizal fungi can accumulate Se in their fruit bodies [121,122,123], suggesting their ability to acquire Se. Some of these ectomycorrhizal fungi are edible, thus they are used for biofortification of Se in fruit bodies. Few investigations on the role of REFs in Se biofortification have beencarried out (Table 1). In general, REFs, especially members of the genus Trichoderma, can colonize roots of some host plants, thus they can be widely used for Se biofortification. At present, there are not reports on roles of dark septate fungi in Se biofortification of food crops.
Taken together, mycorrhizal inoculation might increase Se accumulation in some crop species, leading to Se biofortification of crops. For some crop species, more investigations are needed, especially for interactions between mycorrhizal fungi and crop species. For the abovementioned negative effects of G. mosseae on Se accumulation in alfalfa, maize, and soybean, more mycorrhizal fungi and root endophytic fungi should be used to investigation.

2.2. Se Biofortification by PGPRs

Plant growth-promoting rhizobacteria (PGPRs) are popular in improving nutrition uptake, plant growth, and resistance to abiotic stresses [124,125,126,127]. Some of them possess the ability to solubilize phosphate in soil. Such ability could be used for Se biofortification (Table 2), because in some soil agrotypes, such as volcanic Andisols in southern Chile, Se bioavailability is very low. On the one hand, Se can form stable complexes with clays and/or can be strongly absorbed onto oxy-hydroxides of aluminum, iron, or manganese, and remain low in terms of bioavailability to plants [128,129,130]. On the other hand, oxyanions of Se, i.e., selenite and selenate, are bioavailable to plants. When selenate and selenite are supplied to soil, they are rapidly reduced to insoluble forms (e.g., Se–metal ion complex), leading to their low bioavailability (less than 10% only). The Se fertilizers that are not acquired by plant roots readily after application are not bioavailable to plants in the next season or the next year [131]. Thus, Se re-solubility in soil is very important. Although there are no report concernsregarding Se-solubilizing PGPRs at present, some seleno-bacteria have been studied [30,35,109,132,133]. Trivedi et al. [35] isolated and identified some endophytic seleno-bacteria from the various tissues of Ricinus communis plants and molecular identification analyses showed that they were Paraburkholderia megapolitana, Alcaligenes faecalis, and Stenotrophomonas maltophilia. Among the three bacteria, P. megapolitana was most effective in improving the growth of Glycine max plants under drought and enhancing Se biofortification which was 7.4-fold higher compared to control. The synergistic effect on Se biofortification and increased drought tolerance is important for plants grown in arid and semi-arid places with Se deficiency. A great number of people all around the world are dependent on wheat as their main component of diet, thus it is important to fortify Se in wheat grains [30]. Many studies have been carried out on Se biofortification in wheat. Durán et al. [109] evaluated the effects of Se acquisition by wheat plants through the co-inoculation of native seleno-bacteria strains Stenotrophomonas sp. B19, Enterobacter sp. B16, Bacillus sp. R12, and Pseudomnas sp. R8, both individually and in mixture, as a seleno-nanosphere source with AMF Glomus claroideum. They found that Se concentrations in plant tissues in inoculated plants were significantly higher than those of un-inoculated controls.Meantime, regardless of presence of AMF G. claroideum, Se concentrations in grains of wheat plants inoculated with Enterobacter sp. B16 were higher than those of plants inoculated with the rest of the microbial strains. In addition, PGPRs showed their synergistic role in improving Se concentrations with AMFs. When plants were inoculated with the seleno-bacteria strains and G. claroideum, Se concentrations in grains were 23.5% higher than those in non-mycorrhizal plants. The synergisms might be related to the relationship between seleno-bacteria strains and AMFs, because the seleno-bacteria could acquire more nutrition from the hyphae of their neighboring AMFs or ectomycorrhizal fungi [134,135,136,137]. Moreover, Durán et al. [132] isolated two Se-tolerant endophytic bacteria Acinetobacters sp. E6.2 and Bacillus sp. E5. They studied production of seleno-compounds (SeMet and seleno-methyl-selenocysteins (MeSeCys)) by the two bacteria, but they did not study the effects of the two bacteria on Se biofortification. Co-application of Se fertilizers and seleno-bacteria sometimes leads to changes in bacterial population. When Se-tolerant bacteria and Se amendment were supplied to wheat in Andisols, Se amendment stimulated population growth of two bacterial groups (Paenibacillaceae and Brucellaceae), but inhibited other bacterial groups (Clostridia, Burkholderiales, Chitinophagaceae, and Oxalobacteraceae) [133]. Meanwhile, Se concentrations in roots and leaves of wheat plants inoculated with Se-tolerant bacterial strains Pseudomonas sp. R8 and Stenotrophomonas sp. B19 were significantly higher than those of the un-inoculated controls. Higher Se biofortification is related to the Se tolerance of the two bacteria, because higher Se concentrations in roots and leaves were also observed when wheat plants inoculated with Stenotrophomonas sp. B19 were grown at concentrations of 5 and 10 mM of selenite, compared to those grown at 2 mM [133]. The results suggested that Se in seleno-bacteria could be transferred into their host plants. Effects of other Se-tolerant bacteria on Se biofortification were also investigated. When wheat plants were inoculated with two Se-tolerant bacterial strains Bacillus cereus YAP6 and Bacillus licheniformis YAP7, Se concentrations in the stems of the Se-treated wheat plants were increased up to 375%, and Se concentrations in kernels increased up to 154% of those in un-inoculated Se-treated wheat plants [34]. Meanwhile, the Bacillus strains can produce auxin, leading to increased number of leaves and greater biomass and shoot length [34]. When wheat plants were inoculated with Bacillus pichinotyi in the presence of selenate, they posed significantly higher biomass, shoot length, and spike length compared to un-inoculated plants [33]. Meanwhile wheat plants inoculated with B. pichinotyi had significantly higher Se concentrations in wheat kernels (167%) and stems (252%), compared to un-inoculated plants. Overall, greater biomass means higher Se biofortification, which is important for crops cultivated by large scale in field. Rhizobia not only fixes nitrogen, but also helps Se accumulation. Data from Alford et al. [138] showed rhizobia significantly increased shoot biomass and Se accumulation in shoots of the Se-hyperaccumulator Astragalus bisulcatus and the nonhyperaccumulator A. drummondii. The dual roles of rhizobia are of significance for organic Se production.
Interestingly, volatile organic compounds (VOCs) released by PGPRs improve Se biofortification of plants. VOCs from Bacillus amyloliquefaciens BF06 significantly increased photosynthesis and growth of Arabidopsis plants and these VOCs led to an obvious increase in expressions of some genes encoding sulfate transporters and Se concentrations in plants [141]. VOCs released by B. amyloliquefaciens could not increase Se biofortification of Arabidopsis Sultr1:2 mutants. All the results suggested sulfate transporters with high expression mediate Se uptake, as shown above. Meanwhile, the results indicate an unknown mechanism that PGPRs improves Se biofortification. The question is inevitable, how do the VOCs improve expression of sulfate transporters?
Taken together, Se amendment could improve population growth of some Se-tolerant bacteria; if these bacteria show synergistic effect on Se biofortification, they could be mixed in some biofilmed biofertilizers specific to certain crops and vegetables, thus, their combinative amendment along with Se fertilizers become a Se biofortification tool in sustainable agriculture [52,145].

3. Concluding Remarksand Perspectives

Since Se is essential for human health, Se biofortification must be carried out in Se-deficient places by various ways on food crops, vegetables, fruits, and nuts. Foliar and soil fertilization are effective for enhancing Se accumulation in crops. However, the two ways are expensive for large-scaled food crops, especially in poor places. Moreover, the effect of the two ways is short-term and they easily cause area source pollution. BMOs improve Se uptake and accumulation in food crops. Therefore, combination of BMOs and soil fertilization is a good approach to Se biofortification of crop food. At present, for Se biofortification by BMOs, there remain some questions to resolve. The first relates to the synergisms among these beneficial microorganisms. Biofilmed biofertilizers often include many BMOs. As they can compete for nutrition from their common host plants, some of them are possibly antagonistic. Therefore, before they are mixed in biofilmed biofertilizers, the synergism should be examined in detail. The second relates to Se biofortification and phytoremediation. Phytoremediation of Se is popular in Se-rich places. The plants harvested in phytoremediation could be used as the organic source of Se. However, attention must be paid to the fact that there are possibly other heavy metals in the harvested plants. In addition, transgenic plant technology has been used for phytoremediation and Se biofortification. Since some people are very sensitive to genetically modification of crop plants, application of transgenic plants for Se biofortification should be careful. The third relates to theuse of Se hyperaccumulators. Some Se hyperaccumulators, such as Stanleya pinnata and Astragalus bisulcatus and Cardamine enshiensis, should be paid more attentions, especially C. enshiensis, because it is edible and can be directly used in food. The forth relates to the use of Se nanoparticles. Relatively, Se nanoparticles are less toxic and more eco-friendly for both humans and the environment. More researches are necessary for use of Se nanoparticles, especially for the production of Se nanoparticles using plants and fungi. The fifth relates to increased plant resistance to abiotic stresses. Exogenous Se compounds and seleno-bacteria synergistically improve plant resistance to abiotic stresses, thus the synergism should be well used for plant resistance to abiotic stresses, especially drought and salt stress. Finally, the sixth relates to functions of root endophytic fungi and dark septate fungi. The two types of fungi possess ecological functions similar to mycorrhizal fungi, and they often colonize many plant species. However, very little attention has been paid to them.

Author Contributions

C.W. and F.X. planned the whole article and outline, and provided some references. C.W. and J.Q. revised the second manuscript. Y.Y. wrote the rough manuscript; Y.P. and S.R. reviewed the rough manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Natural Science Foundation of China (grant numbers 31870378); Fujian University Key Laboratory for Plant-Microbe Interaction (grant numberPMI2018KF2).

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Chasteen, T.G.; Bentley, R. Biomethylation of selenium and tellurium: Microorganisms and plants. Chem. Rev. 2003, 103, 1–25. [Google Scholar] [CrossRef] [PubMed]
  2. Gissel-Nielsen, G.; Gupta, U.C.; Lamand, M.; Westermarck, T. Selenium in soil and plants and its importance in livestock and human nutrition. Adv. Agron. 1984, 37, 397–460. [Google Scholar]
  3. Gupta, U.C.; Gupta, S.C. Selenium in soils and crops, its deficiencies in livestock and humans: Implications for management. Commun. Soil Sci. Plant Anal. 2000, 31, 1791–1807. [Google Scholar] [CrossRef]
  4. Ylaranta, T. Sorption of selenite and selenate added in the soil. Ann. Agr. Fenn. 1983, 22, 9–39. [Google Scholar]
  5. Blazina, T.; Sun, Y.; Voegelin, A.; Lenz, M.; Berg, M.; Winkel, L.H.E. Terrestrial selenium distribution in China is potentially linked to monsoonal climate. Nat. Commun. 2014, 5, 4717. [Google Scholar] [CrossRef]
  6. Xu, G.; Wang, S.; Gu, B.; Yang, Y.; Song, H.; Xue, W.; Liang, W.; Zhang, P. Further investigation on the role of selenium deficiency in the aetiology and pathogenesis of Keshan disease. Biomed. Environ. Sci. 1997, 10, 316–326. [Google Scholar]
  7. Lei, C.; Niu, X.; Ma, X.; Wei, J. Is selenium deficiency really the cause of Keshan disease? Environ. Geochem. Health 2011, 33, 183–188. [Google Scholar] [CrossRef]
  8. Zhang, B.; Yang, L.; Wang, W.; Li, Y.; Li, H. Environmental selenium in the Kaschin-Beck disease area, Tibetan Plateau, China. Environ. Geochem. Health 2011, 33, 495–501. [Google Scholar] [CrossRef]
  9. Sun, L.Y.; Yuan, L.J.; Fu, Y.; Deng, J.Y.; Wang, L.H. Prevalence of Kaschin-Beck disease among Tibetan children in Aba Tibetan and Qiang Autonomous Prefecture: A 3-year epidemiological survey. J. Pediatrics 2012, 8, 140–144. [Google Scholar] [CrossRef]
  10. Encio, I.; Sanmartin, C.; Palop, J.A.; Font, M.; Moreno, E.; Plano, D.; Lamberto, I. Bisacylimidoselenocarbamates cause G2/M arrest associated with the modulation of CDK1 and Chk2 in human breast cancer MCF-7 Cells. Curr. Med. Chem. 2013, 20, 1609–1619. [Google Scholar]
  11. Hatfield, D.L.; Tsuji, P.A.; Carlson, B.A.; Gladyshev, V.N. Selenium and selenocysteine: Roles in cancer, health, and development. Trends Biochem. Sci. 2014, 39, 112–120. [Google Scholar] [CrossRef] [PubMed]
  12. Yoo, M.H.; Carlson, B.A.; Tsuji, P.A.; Tobe, R.; Naranjo-Suarez, S.; Lee, B.J.; Davis, C.D.; Gladyshev, V.N.; Hatfield, D.L. Selenoproteins harboring a split personality in both preventing and promoting cancer. In Selenium: Its Molecular Biology and Role in Human Health; Hatfield, D.L., Berry, M.J., Gladyshev, V.N., Eds.; Springer: New York, NY, USA, 2011; pp. 325–333. [Google Scholar]
  13. Patra, A.R.; Hajra, S.; Baral, R.; Bhattacharya, S. Use of selenium as micronutrients and for future anticancer drug: A review. Nucleus 2019. [Google Scholar] [CrossRef]
  14. Michalke, B. Uncovering the importance of selenium in muscle disease. In Selenium; Michalke, B., Ed.; Molecular and Integrative, Toxicology; Springer: Cham, Switzerland, 2018; pp. 345–362. [Google Scholar]
  15. Mocchegiani, E.; Malavolta, M. Role of zinc and selenium in oxidative stress and immunosenescence: Implications for healthy aging and longevity. In Handbook of Immunosenescence; Fulop, T., Franceschi, C., Hirokawa, K., Pawelec, G., Eds.; Springer: Cham, Switzerland, 2019; pp. 2539–2573. [Google Scholar]
  16. Zhang, Y. Trace elements and healthcare: A bioinformatics perspective. Adv. Exp. Med. Biol. 2017, 1005, 63. [Google Scholar] [PubMed]
  17. Varlamova, E.G.; Maltseva, V.N. Micronutrient selenium: Uniqueness and vital functions. Biophysics 2019, 64, 510–521. [Google Scholar] [CrossRef]
  18. Rayman, M.P. The importance of selenium to human health. Lancet 2000, 356, 233. [Google Scholar] [CrossRef]
  19. Combs, G.F. Selenium in global food systems. Br. J. Nutr. 2001, 85, 517–547. [Google Scholar] [CrossRef]
  20. Fairweather-Tait, S.J.; Bao, Y.; Broadley, M.R.; Collings, R.; Ford, D.; Hesketh, J.E.; Hurst, R. Selenium in human health and disease. Antioxid. Redox Signal. 2011, 14, 1337–1383. [Google Scholar] [CrossRef]
  21. Fordyce, F.M. Selenium deficiency and toxicity in the environment. In Essentials of Medical Geology; Springer: Dordrecht, The Netherlands, 2013; pp. 375–416. [Google Scholar]
  22. Khalid, S.; Asghar, H.N.; Akhtar, M.J.; Aslam, A.; Zahir, Z.A. Biofortification of iron in chickpea by plant growth promoting rhizobacteria. Pak. J. Bot. 2015, 47, 1191–1194. [Google Scholar]
  23. Kumar, A.; Patel, J.S.; Bahadur, I.; Meena, V.S. The Molecular Mechanisms of KSMs for Enhancement of Crop Production Under Organic Farming; Springer: New Delhi, India, 2016. [Google Scholar]
  24. Jat, L.K.; Singh, Y.V.; Meena, S.K.; Meena, S.K.; Parihar, M.; Jatav, H.S.; Meena, R.K.; Meena, V.S. Does integrated nutrient management enhance agricultural productivity? J. Pur. Appl. Microbiol. 2015, 9, 1211–1221. [Google Scholar]
  25. Malagoli, M.; Schiavon, M.; Dall’Acqua, S.; Pilon-Smits, E.A.H. Effects of selenium biofortification on crop nutritional quality. Front. Plant Sci. 2015, 6, 280. [Google Scholar] [CrossRef]
  26. Ahmad, M.; Nadeem, S.M.; Naveed, M.; Zahir, Z.A. Potassium-solubilizing bacteria and their application in agriculture. In Potassium Solubilizing Microorganisms for Sustainable Agriculture; Meena, V.S., Maurya, B.R., Verma, J.P., Meena, R.S., Eds.; Springer: New Delhi, India, 2016; pp. 293–313. [Google Scholar]
  27. Reeves, M.A.; Hoffmann, P.R. The human selenoproteome: Recent insights into functions and regulation. Cell. Mol. Life Sci. 2009, 66, 2457. [Google Scholar] [CrossRef] [PubMed]
  28. Brigelius-Flohé, R.; Maiorino, M. Glutathione peroxidases. Biochim. Biophys. Acta 2013, 1830, 3289–3303. [Google Scholar] [CrossRef]
  29. Soriano-Garcia, M. Organoselenium compounds as potential therapeutic and chemopreventive agents: A review. Curr. Med. Chem. 2004, 11, 1657–1669. [Google Scholar] [CrossRef] [PubMed]
  30. Abadin, Z.U.; Yasin, M.; Faisal, M. Bacterial-mediated selenium biofortification of Triticum aestivum: Strategy for improvement in selenium phytoremediation and biofortification. In Agriculturally Important Microbes for Sustainable Agriculture; Meena, V., Mishra, P., Bisht, J., Pattanayak, A., Eds.; Springer: Singapore, 2017; pp. 299–315. [Google Scholar]
  31. Chomchan, R.; Siripongvutikorn, S.; Puttarak, P.; Rattanapon, R. Influence of selenium bio-fortification on nutritional compositions, bioactive compounds content and anti-oxidative properties of young ricegrass (Oryza sativa L.). Funct. Foods Heal. Dis. 2017, 7, 195–209. [Google Scholar] [CrossRef]
  32. D’Amato, R.; Fontanella, M.C.; Falcinelli, B.; Beone, G.M.; Bravi, E.; Marconi, O.; Benincasa, P.; Businelli, D. Selenium Biofortification in Rice (Oryza sativa L.) Sprouting: Effects on Se yield and nutritional traits with focus on phenolic acid profile. J. Agric. Food Chem. 2018, 66, 4082–4090. [Google Scholar] [CrossRef]
  33. Yasin, M.; El-Mehdawi, A.F.; Anwar, A.; Pilon-Smits, E.A.H.; Faisal, M. Microbial-enhanced selenium and iron biofortification of wheat (Triticum aestivum L.)—Applications in phytoremediation and biofortification. Int. J. Phytoremediation 2015, 17, 341–347. [Google Scholar] [CrossRef] [PubMed]
  34. Yasin, M.; El-Mehdawi, A.F.; Pilon-Smits, E.A.H.; Faisal, M. Selenium-fortified wheat: Potential of microbes for biofortification of selenium and other essential nutrients. Int. J. Phytoremediation 2015, 17, 777–786. [Google Scholar] [CrossRef] [PubMed]
  35. Trivedi, G.; Patel, P.; Saraf, M. Synergistic effect of endophytic selenobacteria on biofortification and growth of Glycine max under drought stress. South Afr. J. Bot. 2019, 2019, 1–9. [Google Scholar] [CrossRef]
  36. Businelli, D.; D’Amato, R.; Onofri, A.; Tedeschini, E.; Tei, F. Se-enrichment of cucumber (Cucumis sativus L.), lettuce (Lactuca sativa L.) and tomato (Solanum lycopersicum L. Karst) through fortification in pre-transplanting. Sci. Hortic. 2015, 197, 697–704. [Google Scholar] [CrossRef]
  37. Dhillon, K.S.; Dhillon, S.K. Accumulation and distribution of selenium in some vegetable crops grown in selenate-Se treated clay loam soil. Front. Agric. China 2009, 3, 366–373. [Google Scholar] [CrossRef]
  38. Dil, T.; Alex, A.; Indika, M.; Clarice, C.; Pushparajah, T.; Shiv, K. Selecting lentil accessions for global selenium biofortification. Plants 2017, 6, 34. [Google Scholar]
  39. Bachiega, P.; Salgado, J.M.; de Carvalho, A.L.T.G.; Schwarz, K.; Tezotto, T.; Morzelle, M.C. Antioxidant and antiproliferative activities in different maturation stages of broccoli (Brassica oleracea Italica) biofortified with selenium. Food Chem. 2016, 190, 771–776. [Google Scholar] [CrossRef]
  40. Peng, Q.; Guo, L.; Ali, F.; Li, J.; Qin, S.; Feng, P.; Liang, D. Influence of Pak choi plant cultivation on Se distribution, speciation and bioavailability in soil. Plant Soil 2016, 403, 331–342. [Google Scholar] [CrossRef]
  41. Slekovec, M.; Goessier, W. Accumulation of selenium in natural plants and selenium supplemented vegetable and selenium speciation by HPLC-ICPMS. Chem. Speciat. Bioavailab. 2015, 17, 63–73. [Google Scholar] [CrossRef]
  42. Susana, G.M.; Fabián, P.L.; Ema, G.E.; Paola, L.M.; Julia, M.M.; Irma, D.R.; Antonio, J.M.; Erika, R.M.; Adalberto, B.M. Selenium and sulfur to produce Allium functional crops. Molecules 2017, 22, 558. [Google Scholar]
  43. Jing, D.-W.; Du, Z.-Y.; Ma, H.-L.; Ma, B.-Y.; Liu, F.-C.; Song, Y.-G.; Xu, Y.-F.; Li, L. Selenium enrichment, fruit quality and yield of winter jujube as affected by addition of sodium selenite. Sci. Hortic. 2017, 225, 1–5. [Google Scholar] [CrossRef]
  44. Nie, J.; Kuang, L.; Li, Z.; Pang, R.; Yang, L.; Chen, Q.; Li, A.; Zhao, X.; Xu, W. Selenium content of main deciduous fruits from China and its dietary exposure assessment. Sci. Agric. Sinica 2015, 48, 3015–3026. [Google Scholar]
  45. Sun, X.; Yi, H.; Chen, Y.; Luo, Y.; Ping, T. Effects of different concentrations of Se6+ on selenium absorption, transportation, and distribution of citrus seedlings (C. junos cv. Ziyang xiangcheng). J. Plant Nutr. 2018, 41, 168–177. [Google Scholar]
  46. Cominetti, C.; de Bortoli, M.C.; Garrido, A.B., Jr.; Cozzolino, S.M.F. Brazilian nut consumption improves selenium status and glutathione peroxidase activity and reduces atherogenic risk in obese women. Nutr. Res. 2012, 32, 403–407. [Google Scholar] [CrossRef]
  47. Ip, C.; Lisk, D.J. Bioactivity of selenium from Brazil nut for cancer prevention and selenoenzyme maintenance. Nutr. Cancer 1994, 21, 203–212. [Google Scholar] [CrossRef]
  48. Lima, L.W.; Stonehouse, G.C.; Walters, C.; El Mehdawi, A.F.; Fakra, S.C.; Pilon-Smits, E.A. Selenium accumulation, speciation and localization in Brazil nuts (Bertholletia excelsa H.B.K.). Plants 2019, 8, 289. [Google Scholar] [CrossRef] [PubMed]
  49. Kápolna, E.; Gergely, V.; Dernovics, M.; Illés, A.; Fodor, P. Fate of selenium species in sesame seeds during simulated bakery process. J. Food Eng. 2007, 79, 494–501. [Google Scholar] [CrossRef]
  50. Graham, L. Biofortification of cereals with foliar selenium and iodine could reduce hypothyroidism. Front. Plant Sci. 2018, 9, 730. [Google Scholar]
  51. Kapolna, E.; Hillestrom, P.R.; Laursen, K.H.; Husted, S.; Larsen, E.H. Effect of foliar application of selenium on its uptake and speciation in carrot. Food Chem. 2009, 115, 1357–1363. [Google Scholar] [CrossRef]
  52. Ros, G.H.; van Rotterdam, A.M.D.; Bussink, D.W.; Bindraban, P.S. Selenium fertilization strategies for bio-fortification of food: An agro-ecosystem approach. Plant Soil 2016, 404, 99–112. [Google Scholar] [CrossRef]
  53. Xiong, L.; Li, B.; Yang, Y. Effects of foliar selenite on the nutrient components of turnip (Brassica rapa var. rapa Linn.). Front. Chem. 2018, 6, 42. [Google Scholar]
  54. Broadley, M.R.; Alcock, J.; Alford, J.; Cartwright, P.; Foot, I.; Fairweather-Tait, S.J.; Hart, D.J.; Hurst, R.; Knott, P.; Mcgrath, S.P. Selenium biofortification of high-yielding winter wheat (Triticum aestivum L.) by liquid or granular Se fertilisation. Plant Soil 2010, 332, 5–18. [Google Scholar] [CrossRef]
  55. Larsen, E.H.; Łobiński, R.; Burger-Meÿer, K.; Hansen, M.; Ruzik, L.; Mazurowska, L.; Rasmussen, P.H.; Sloth, J.J.; Scholten, O.; Kik, C. Uptake and speciation of selenium in garlic cultivated in soil amended with symbiotic fungi (mycorrhiza) and selenate. Anal. Bioanal. Chem. 2006, 385, 1098–1108. [Google Scholar] [CrossRef]
  56. Bañuelos, G.S.; Arroyo, I.; Pickering, I.J.; Yang, S.I.; Freeman, J.L. Selenium biofortification of broccoli and carrots grown in soil amended with Se-enriched hyperaccumulator Stanleya pinnata. Food Chem. 2015, 166, 603–608. [Google Scholar] [CrossRef]
  57. Aspila, P. History of selenium supplemented fertilization in Finland. In Proceedings of the Twenty Years of Selenium Fertilization, Helsinki, Finland, 8–9 September 2005; pp. 8–13. [Google Scholar]
  58. Lyons, G.H.; Lewis, J.; Lorimer, M.F.; Holloway, R.E.; Graham, R.D. High-selenium wheat: Agronomic biofortification strategies to improve human nutrition. J. Food Agric. Environ. 2004, 22, 171–178. [Google Scholar]
  59. Deng, X.; Zhao, Z.; Zhou, J.; Chen, J.; Lv, C.; Liu, X. Compositional analysis of typical selenium ore from Enshi and its effect on selenium enrichment in wetland and dryland crops. Plant Soil 2018, 433, 55–64. [Google Scholar] [CrossRef]
  60. Sura-de Jong, M.; Reynolds, R.J.B.; Richterova, K.; Musilova, L.; Staicu, L.C.; Chocholata, I.; Cappa, J.J.; Taghavi, S.; van der Lelie, D.; Frantik, T.; et al. Selenium hyperaccumulators harbor a diverse endophytic bacterial community characterized by high selenium resistance and plant growth promoting properties. Front. Plant Sci. 2015, 6, 113. [Google Scholar] [CrossRef] [PubMed]
  61. Carrino-Kyker, S.R.; Kluber, L.A.; Coyle, K.P.; Burke, D.J. Detection of phosphate transporter genes from arbuscular mycorrhizal fungi in mature tree roots under experimental soil pH manipulation. Symbiosis 2017, 72, 123–133. [Google Scholar] [CrossRef]
  62. Hawkesford, M.J.; Buchner, P.; Hopkins, L.; Howarth, J.R. Phosphate transporters in arbuscular myccorhizal symbiosis. In Arbuscular mycorrhzias: Physiology and Functions; Koltai, H., Kapulnik, Y., Eds.; Springer: Dordrencht, The Netherlands, 2010; pp. 117–135. [Google Scholar]
  63. Tatry, M.-V.; El Kassis, E.; Lambilliotte, R.; Corratgé, C.; van Aarle, I.; Amenc, L.K.; Alary, R.; Zimmermann, S.; Sentenac, H.; Plassard, C. Two differentially regulated phosphate transporters from the symbiotic fungus Hebeloma cylindrosporum and phosphorus acquisition by ectomycorrhizal Pinus pinaste. Plant J. 2009, 57, 1092–1102. [Google Scholar] [CrossRef] [PubMed]
  64. Fiorilli, V.; Lanfranco, L.; Bonfante, P. The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability. Planta 2013, 237, 1267–1277. [Google Scholar] [CrossRef] [PubMed]
  65. Xie, X.; Lin, H.; Peng, X.; Xu, C.; Sun, Z.; Jian, K.; Huang, A.; Wu, X.; Tang, N. Arbuscular mycorrhizal symbiosis requires a phosphate transporter in the Gigaspora margarita fungal symbiont. Mol. Plant 2016, 9, 1583–1608. [Google Scholar] [CrossRef] [PubMed]
  66. Glassop, D.; Smith, S.E.; Smith, F.W. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 2005, 222, 688–698. [Google Scholar] [CrossRef]
  67. Loth-Pereda, V.; Orsini, E.; Courty, P.E.; Lota, F.; Martin, F. Structure and expression profile of the phosphate Pht1 transporter gene family in Mycorrhizal Populus trichocarpa. Plant Physiol. 2011, 156, 2141–2154. [Google Scholar] [CrossRef]
  68. Pumplin, N.; Zhang, X.; Noar, R.D.; Harrison, M.J. Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. PNAS 2012, 109, E665–E672. [Google Scholar] [CrossRef]
  69. Nagy, R.; Karandashov, V.; Chagué, V.; Kalinkevich, K.; Tamasloukht, M.; Xu, G.; Jakobsen, I.; Levy, A.A.; Amrhein, N.; Bucher, M. The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J. 2005, 42, 236–250. [Google Scholar] [CrossRef]
  70. Paszkowski, U.; Kroken, S.; Roux, C.; Briggs, S.P. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 2002, 99, 13324–13329. [Google Scholar] [CrossRef] [PubMed]
  71. Tian, H.; Drijber, R.A.; Li, X.; Miller, D.N.; Wienhold, B.J. Arbuscular mycorrhizal fungi differ in their ability to regulate the expression of phosphate transporters in maize (Zea mays L.). Mycorrhiza 2013, 23, 507–514. [Google Scholar] [CrossRef] [PubMed]
  72. Zhang, T.; Wen, X.; Ding, G. Ectomycorrhizal symbiosis enhances tolerance to low phosphorous through expression of phosphate transporter genes in masson pine (Pinus massoniana). Acta Physiol. Plant 2017, 39, 101. [Google Scholar] [CrossRef]
  73. Smith, S.E.; Read, D.J. Arbuscular mycorrhizaes. In Mycorrhizal Symbiosis, 3rd ed.; Smith, S.E., Read, D.J., Eds.; Academic Press: London, UK, 2008; pp. 13–187. [Google Scholar]
  74. Smith, S.E.; Jakobsen, I.; Grønlund, M.; Smith, F.A. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 2011, 156, 1050–1057. [Google Scholar] [CrossRef] [PubMed]
  75. Higo, M.; Takahashi, Y.; Gunji, K.; Isobe, K. How are arbuscular mycorrhizal associations related to maize growth performance during short-term cover crop rotation? Sci. Food Agric. 2018, 98, 1388–1396. [Google Scholar] [CrossRef]
  76. Higo, M.; Tatewaki, Y.; Gunji, K.; Kaseda, A.; Isobe, K. Cover cropping can be a stronger determinant than host crop identity for arbuscular mycorrhizal fungal communities colonizing maize and soybean. Peer J. 2019, 7, e6403. [Google Scholar] [CrossRef]
  77. Higo, M.; Tatewaki, Y.; Iida, K.; Yokota, K.; Isobe, K. Amplicon sequencing analysis of arbuscular mycorrhizal fungal communities colonizing maize roots in different cover cropping and tillage systems. Sci. Rep. 2020, 10, 6093. [Google Scholar] [CrossRef]
  78. Eah, P.-S. Se in plants. In Progress in Botany; Lüttge, U., Beyschlag, W., Eds.; Springer: Cham, Switzerland, 2015; Volume 76, pp. 93–107. [Google Scholar]
  79. Ellis, D.R.; Salt, D.E. Plants, selenium and human health. Curr. Opin. Plant Biol. 2003, 6, 273–279. [Google Scholar] [CrossRef]
  80. Sors, T.G.; Ellis, D.R.; Na, G.N.; Lahner, B.; Salt, D.E. Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J. 2005, 42, 785–797. [Google Scholar] [CrossRef]
  81. Wessjohann, L.A.; Schneider, A.; Abbas, M.; Brandt, W. Selenium in chemistry and biochemistry in comparison to sulfur. Biol. Chem. 2007, 388, 997–1006. [Google Scholar] [CrossRef]
  82. Chauhan, R.; Awasthi, S.; Srivastava, S.; Dwivedi, S.; Pilon-Smits, E.A.H.; Dhankher, O.P.; Tripathi, R.D. Understanding selenium metabolism in plants and its role as a beneficial element. Crit. Rev. Environ. Sci. Technol. 2019, 49, 1937–1958. [Google Scholar] [CrossRef]
  83. Lauchli, A. Selenium in plants: Uptake, functions, and environmental toxicity. Bot. Acta 1993, 106, 455–468. [Google Scholar] [CrossRef]
  84. Lass, B.; Ullrich-Eberius, C.I. Evidence for proton/sulfate cotransport and its kinetics inLemna gibba G1. Planta 1984, 161, 53–60. [Google Scholar] [CrossRef] [PubMed]
  85. Hawkesford, M.; Davidian, J.C.; Grignon, C. Sulphate/proton cotransport in plasma-membrane vesicles isolated from roots of Brassica napus L.: Increased transport in membranes isolated from sulphur-starved plants. Planta 1993, 190, 297–304. [Google Scholar] [CrossRef]
  86. Shibagaki, N.; Rose, A.; McDermott, J.P.; Fujiwara, T.; Hayashi, H.; Yoneyama, T.; Davies, J.P. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1:2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J. 2002, 29, 475–486. [Google Scholar] [CrossRef] [PubMed]
  87. Inostroza-Blancheteau, C.; Reyes-Díaz, M.; Alberdi, M.; Godoy, K.; Rojas-Lillo, Y.; Cartes, P.; de la Luz Mora, M. Influence of selenite on selenium uptake, differential antioxidant performance and gene expression of sulfate transporters in wheat genotypes. Plant Soil 2013, 369, 47–59. [Google Scholar] [CrossRef]
  88. Zhao, X.Q.; Mitani, N.; Yamaji, N.; Shen, R.F.; Ma, J.F. Involvement of silicon influx transporter OsNIP2;1 in selenite uptake in rice. Plant Physiol. 2010, 153, 1871–1877. [Google Scholar] [CrossRef]
  89. Wang, M.; Yang, W.; Zhou, F.; Du, Z.; Xue, M.; Chen, T.; Liang, D. Effect of phosphate and silicate on selenite uptake and phloem-mediated transport in tomato (Solanum lycopersicum L.). Environ. Sci. Pollut. Res. 2019, 26, 20475–20484. [Google Scholar] [CrossRef]
  90. Li, H.F.; Mcgrath, S.P.; Zhao, F.J. Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytol. 2008, 178, 92–102. [Google Scholar] [CrossRef]
  91. Chen, G.H.; Yan, W.; Yang, S.P.; Wang, A.; Zhu, Y.L. Overexpression of rice phosphate transporter gene OsPT2 enhances tolerance to low phosphorus stress in soybean. J. Agric. Sci. Technol. 2015, 17, 469–482. [Google Scholar]
  92. Zhang, L.; Hu, B.; Li, W.; Chen, R.; Deng, K.; Li, H.; Yu, F.; Ling, H.; Li, Y.; Chu, C. OsPT2, a phosphate transporter, is involved in the active uptake of selenite in rice. New Phytol. 2014, 201, 1183–1191. [Google Scholar] [CrossRef]
  93. Zhang, M.; Wilson, L.; Xing, G.; Jiang, L.; Tang, S. Optimizing root architecture and increasing transporter gene expression are strategies to promote selenium uptake by high-se accumulating rice cultivar. Plant Soil 2020, 447, 319–332. [Google Scholar] [CrossRef]
  94. Lazard, M.; Blanquet, S.; Fisicaro, P.; Labarraque, G.; Plateau, P. Uptake of selenite by Saccharomyces cerevisiae involves the high and low affinity orthophosphate transporters. J. Biol. Chem. 2010, 285, 32029–32037. [Google Scholar] [CrossRef]
  95. Pérez-Sampietro, M.; Serra-Cardona, A.; Canadell, D.; Casas, C.; Ario, J.; Herrero, E. The yeast Aft2 transcription factor determines selenite toxicity by controlling the low affinity phosphate transport system. Sci. Rep. 2016, 6, 32836. [Google Scholar] [CrossRef] [PubMed]
  96. McDermott, J.R.; Rosen, B.P.; Liu, Z. Jen1p: A high affinity selenite transporter in yeast. Mol. Biol. Cell 2010, 21, 3934–3941. [Google Scholar] [CrossRef] [PubMed]
  97. Hopper, J.L.; Parker, D.R. Plant availability of selenite and selenate as influenced by the competing ions phosphate and sulfate. Plant Soil 1999, 210, 199–207. [Google Scholar] [CrossRef]
  98. Yang, X.; Lu, Y.; Zhong, J.; Qian, Y.; Zhao, Z.; Liu, X. The Positive effect of sulfur on selenium detoxification under selenite condition in wheat. Commun. Soil Sci. Plant Anal. 2017, 48, 1564–1573. [Google Scholar] [CrossRef]
  99. Zhang, D.; Dong, T.; Ye, J.; Hou, Z. Selenium accumulation in wheat (Triticum aestivum L.) as affected by coapplication of either selenite or selenate with phosphorus. Soil Sci. Plant Nutr. 2017, 63, 37–44. [Google Scholar] [CrossRef]
  100. Cabannes, E.; Buchner, P.; Broadley, M.R.; Hawkesford, M.J. A Comparison of sulfate and selenium accumulation in relation to the expression of sulfate transporter genes in Astragalus Species. Plant Physiol. 2011, 157, 2227–2239. [Google Scholar] [CrossRef]
  101. Hawkesford, J.M. Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. J. Exp. Bot. 2000, 51, 131–138. [Google Scholar] [CrossRef]
  102. Hawkesford, M.J.; Buchner, P.; Hopkins, L.; Howarth, J.R. The plant sulfate transporter family: Specialized functions and integration with whole plant nutrition. In Sulfur Transport and Assimilation in Plants: Regulation, Interaction and Signaling; Davidian, J.C., Grill, D., DeKok, L.J., Stulen, I., Hawkesford, M.J., Schnug, E., Rennenberg, H., Eds.; Backhuys Publishers: Leiden, The Netherlands, 2003; pp. 1–10. [Google Scholar]
  103. Shinmachi, F.; Buchner, P.; Stroud, J.L.; Parmar, S.; Zhao, F.J.; McGrath, S.P.; Hawkesford, M.J. Influence of sulfur deficiency on the expression of specific sulfate transporters and the distribution of sulfur, selenium, and molybdenum in wheat. Plant Physiol. 2010, 153, 327–336. [Google Scholar] [CrossRef] [PubMed]
  104. Giovannetti, M.; Tolosano, M.; Volpe, V.; Kopriva, S.; Bonfante, P. Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol. 2014, 204, 609–619. [Google Scholar] [CrossRef]
  105. Luo, W.; Li, J.; Ma, X.; Niu, H.; Hou, S.; Wu, F. Effect of arbuscular mycorrhizal fungi on uptake of selenate, selenite, and selenomethionine by roots of winter wheat. Plant Soil 2019, 438, 71–83. [Google Scholar] [CrossRef]
  106. Sanmartín, C.; Garmendia, I.; Romano, B.; Díaz, M.; Palop, J.A.; Goicoechea, N. Mycorrhizal inoculation affected growth, mineral composition, proteins and sugars in lettuces biofortified with organic or inorganic selenocompounds. Sci. Hortic. 2014, 180, 40–51. [Google Scholar] [CrossRef]
  107. Conversa, G.; Lazzizera, C.; Chiaravalle, A.E.; Miedico, O.; Bonasia, A.; La Rotonda, P.; Elia, A. Selenium fern application and arbuscular mycorrhizal fungi soil inoculation enhance Se content and antioxidant properties of green asparagus (Asparagus officinalis L.) spears. Sci. Hortic. 2019, 252, 176–191. [Google Scholar] [CrossRef]
  108. Goicoechea, N.; Garmendia, I.; Fabbrin, E.G.; Bettoni, M.M.; Palop, J.A.; Sanmartín, C. Selenium fertilization and mycorrhizal technology may interfere in enhancing bioactive compounds in edible tissues of lettuces. Sci. Hortic. 2015, 195, 163–172. [Google Scholar] [CrossRef]
  109. Durán, P.; Acuña, J.J.; Jorquera, M.A.; Azcón, R.; Mora, M.L. Enhanced selenium content in wheat grain by co-inoculation of selenobacteria and arbuscular mycorrhizal fungi: A preliminary study as a potential Se biofortification strategy. J. Cereal Sci. 2013, 57, 275–280. [Google Scholar] [CrossRef]
  110. Patharajan, S.; Raaman, N. Influence of arbuscular mycorrhizal fungi on growth and selenium uptake by garlic plants. Arch. Phytopathol. Plant Prot. 2012, 45, 138–151. [Google Scholar] [CrossRef]
  111. Munier-Lamy, C.; Deneux-Mustin, S.; Mustin, C.; Merlet, D.; Berthelin, J.; Leyval, C. Selenium bioavailability and uptake as affected by four different plants in a loamy clay soil with particular attention to mycorrhizae inoculated ryegrass. J. Environ. Radioact. 2007, 97, 148–158. [Google Scholar] [CrossRef]
  112. Yu, Y.; Zhang, S.; Wen, B.; Huang, H.; Luo, L. Accumulation and Speciation of Selenium in Plants as Affected by Arbuscular Mycorrhizal Fungus Glomus mosseae. Biol. Trace Elem. Res. 2011, 143, 1789–1798. [Google Scholar] [CrossRef]
  113. Golubkina, N.A.; Zamana, S.; Seredin, T.; Poluboyarinov, P.A.; Sokolov, S.; Baranova, H.; Krivenkov, L.; Pietrantonio, L.; Caruso, G. Effect of selenium biofortification and beneficial microorganism inoculation on yield, quality and antioxidant properties of shallot bulbs. Plants 2019, 8, 102. [Google Scholar] [CrossRef] [PubMed]
  114. Lindblom, S.D.; Valdez-Barillas, J.R.; Fakra, S.C.; Marcus, M.A.; Pilon-Smits, E.A.H. Influence of microbial associations on selenium localization and speciation in roots of Astragalus and Stanleya hyperaccumulators. Environ. Exp. Bot. 2013, 88, 33–42. [Google Scholar] [CrossRef]
  115. Lei, X.; Yao, S.; Zu, X.; Huang, Z.; Liu, L.; Zhong, M.; Zhu, B.; Tang, S.; Liao, D. Apoptosis induced by diallyl disulfide in human breast cancer cell line MCF-7. Acta Pharm. Sin. 2008, 29, 1233–1239. [Google Scholar] [CrossRef] [PubMed]
  116. Yang, J.S.; Kok, L.F.; Lin, Y.H.; Kuo, T.C.; Chung, J.G. Diallyl disulfide inhibits WEHI-3 leukemia cells in vivo. Anticancer Res. 2006, 26, 219–225. [Google Scholar] [PubMed]
  117. Suangtamai, T.; Tanyong, D.I. Diallyl disulfide induces apoptosis and autophagy via mTOR pathway in myeloid leukemic cell line. Tumor Biol. 2016, 37, 10993–10999. [Google Scholar] [CrossRef]
  118. Nicolle, C.; Cardinault, N.; Gueux, E.; Jaffrelo, L.; Rock, E.; Mazur, A.; Amouroux, P.; Rémésy, C. Health effect of vegetable-based diet: Lettuce consumption improves cholesterol metabolism and antioxidant status in the rat. Clin. Nutr. 2004, 23, 605–614. [Google Scholar] [CrossRef]
  119. Serafini, M.; Bugianesi, R.; Salucci, M.; Azzini, E.; Maiani, G. Effect of acute ingestion of fresh and stored lettuce (Latuca sativa) on plasma total antioxidant capacity and antioxidant levels in human subjects. Br. J. Nutr. 2003, 88, 615–623. [Google Scholar] [CrossRef]
  120. Llorach, R.; Martínez-Sánchez, A.; Tomás-Barberán, F.A.; Gil, M.I.; Ferreres, F. Characterisation of polyphenols and antioxidant properties of five lettuce varieties and escarole. Food Chem. 2008, 108, 1028–1038. [Google Scholar] [CrossRef]
  121. Slejkovec, Z.; Elteren, J.T.V.; Woroniecka, U.D.; Kroon, K.J.; Byrne, A.R. Preliminary study on the determination of selenium compounds in some selenium-accumulating mushrooms. Biol. Trace Elem. Res. 2000, 75, 139–155. [Google Scholar] [CrossRef]
  122. Stijve, T.; Noorloos, T.; Byrne, A.R.; Šlejkovec, Z.; Goessler, W.T. High selenium levels in edible Albatrellus mushroom. Deut Lebens-Rundsch 1998, 94, 275–279. [Google Scholar]
  123. Borovička, J.; Řanda, Z. Distribution of iron, cobalt, zinc and selenium in macrofungi. Mycol. Prog. 2007, 6, 249–259. [Google Scholar] [CrossRef]
  124. Etesami, H.; Maheshwari, D.K. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol. Environ. Saf. 2018, 156, 225–246. [Google Scholar] [CrossRef] [PubMed]
  125. Sayyed, R.Z.; Reddy, M.S.; Antonius, S. Plant Growth Promoting Rhizobacteria (PGPR): Prospects for Sustainable Agriculture; Springer: Singapore, 2019. [Google Scholar]
  126. Sapre, S.; Gontia-Mishra, I.; Tiwari, S. ACC Deaminase-Producing Bacteria: A Key Player in Alleviating Abiotic Stresses in Plants; Springer: Singapore, 2019. [Google Scholar]
  127. Etesami, H.; Adl, S.M. Plant growth-promoting rhizobacteria (PGPR) and their action mechanisms in availability of nutrients to plants. In Phyto-Microbiome in Stress Regulation; Kumar, M., Kumar, V., Prasad, R., Eds.; Environmental and Microbial Biotechnology; Springer: Singapore, 2020; pp. 147–203. [Google Scholar]
  128. Cartes, P.; Gianfreda, L.; Mora, M.L. Uptake of Selenium and its Antioxidant Activity in Ryegrass When Applied as Selenate and Selenite Forms. Plant Soil 2005, 276, 359–367. [Google Scholar] [CrossRef]
  129. Mora, M.D.L.L.; Pinilla, L.; Rosas, A.; Cartes, P. Selenium uptake and its influence on the antioxidative system of white clover as affected by lime and phosphorus fertilization. Plant Soil 2008, 303, 139–149. [Google Scholar] [CrossRef]
  130. Nakamaru, Y.M.; Altansuvd, J. Speciation and bioavailability of selenium and antimony in non-flooded and wetland soils: A review. Chemosphere 2014, 111, 366–371. [Google Scholar] [CrossRef]
  131. Yli-Halla, M. Influence of Se fertilization on soil Se status. In Proceedings of the Twenty Years of Se Fertilization, Helsinki, Finland, 8–9 September 2005; pp. 25–32. [Google Scholar]
  132. Durán, P.; Acuña, J.J.; Gianfreda, L.; Azcón, R.; Funes-Collado, V.; Mora, M.L. Endophytic selenobacteria as new inocula for selenium biofortification. Appl. Soil Ecol. 2015, 96, 319–326. [Google Scholar] [CrossRef]
  133. Acuña, J.J.; Jorquera, M.A.; Barra, P.J.; Crowley, D.E.; María, D.L.L.M. Selenobacteria selected from the rhizosphere as a potential tool for Se biofortification of wheat crops. Biol. Fertil. Soils 2013, 49, 175–185. [Google Scholar] [CrossRef]
  134. Artursson, V.; Finlay, R.D.; Jansson, J.K. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. 2006, 8, 1–10. [Google Scholar] [CrossRef]
  135. Barea, J.; Pozo, M.; Azcón, R.; Azcón-Aguilar, C. Microbial co-operation in the rhizosphere. J. Exp. Bot. 2005, 56, 1761–1778. [Google Scholar] [CrossRef]
  136. Marschner, P.; Baumann, K. Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant Soil 2003, 251, 279–289. [Google Scholar] [CrossRef]
  137. Hrynkiewicz, K.; Ciesielska, A.; Haug, I.; Baum, C. Ectomycorrhiza formation and willow growth promotion as affected by associated bacteria: Role of microbial metabolites and use of C sources. Biol. Fertil. Soils 2010, 46, 139–150. [Google Scholar] [CrossRef]
  138. Alford, É.; Lindblom, S.; Pittarello, M.; Freeman, J.; Fakra, S.; Marcus, M.; Broeckling, C.; Pilon-Smits, E.; Paschke, M. Roles of rhizobial symbionts in selenium hyperaccumulation in Astragalus (Fabaceae). Am. J. Bot. 2014, 101, 1895–1905. [Google Scholar] [CrossRef] [PubMed]
  139. Durán, P.; Acuña, J.J.; Jorquera, M.A.; Azcón, R.; Paredes, C.; Rengel, Z.; Mora, M.D.L.L. Endophytic bacteria from selenium-supplemented wheat plants could be useful for plant-growth promotion, biofortification andGaeumannomyces graminisbiocontrol in wheat production. Biol. Fertil. Soils 2014, 50, 983–990. [Google Scholar] [CrossRef]
  140. Rana, A.; Joshi, M.; Prasanna, R.; Shivay, Y.S.; Nain, L. Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur. J. Soil Biol. 2012, 50, 118–126. [Google Scholar] [CrossRef]
  141. Jianfei, W.; Cheng, Z.; Xin, X.; Yue, X.; Lin, Z.; Zhongyou, M. Enhanced iron and selenium uptake in plants by volatile emissions of Bacillus amyloliquefaciens (BF06). Appl. Sci. 2017, 7, 85. [Google Scholar]
  142. Lampis, S.; Ferrari, A.; Cunhaqueda, A.C.; Alvarenga, P.; Di, G.S.; Vallini, G. Selenite resistant rhizobacteria stimulate SeO(3) (2−) phytoextraction by Brassica juncea in bioaugmented water-filtering artificial beds. Environ. Sci. Pollut. Res. Int. 2009, 16, 663. [Google Scholar] [CrossRef]
  143. Souza, M.P.D.; Huang, C.P.A.; Chee, N.; Terry, N. Rhizosphere bacteria enhance the accumulation of selenium and mercury in wetland plants. Planta 1999, 209, 259–263. [Google Scholar] [CrossRef]
  144. Souza, M.P.D.; Chu, D.; Zhao, M.; Zayed, A.M.; Ruzin, S.E.; Terry, S.N. Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol. 1999, 119, 565–573. [Google Scholar] [CrossRef]
  145. Patel, P.J.; Trivedi, G.R.; Shah, R.K.; Saraf, M. Selenorhizobacteria: As biofortification tool in sustainable agriculture. Biocatal. Agric. Biotechnol. 2018, 14, 198–203. [Google Scholar] [CrossRef]
Table 1. Arbuscular mycorrhizal fungi (AMFs) and root endophytic fungi (REFs) often used for Se biofortification.
Table 1. Arbuscular mycorrhizal fungi (AMFs) and root endophytic fungi (REFs) often used for Se biofortification.
MicrobesMicrobial TypesHost PlantsReferences
Funneliformis mosseaeAMFTriticum aestivum, Lactuca sativa, Asparagus officinalis,[105,106,107,108]
Glomus claroideumAMFTriticum aestivum[109]
Glomus fasciculatumAMFAllium sativum[110]
Glomus irtraradicesAMFAllium sativum[55]
Glomus mosseaeAMFLolium perenne, Allium sativum, Medicago sativa, Glycine max, Zea mays[110,111,112]
Glomus versiformAMFTriticum aestivum[105]
Rhizophagus intraradicesAMFLactuca sativa, Asparagus officinalis, Lactuca sativa, Allium cepa[106,107,108,113]
Alternaria seleniiphilaREFStanleya pinnata[114]
Alternaria astragaliREFAstragalus bisulcatus[114]
Aspergillus leporisREFStanleya pinnata[114]
Fusarium acuminatumREFAstragalus racemosus[114]
Trichoderma harzianumREFAllium cepa[106]
Table 2. Plant growth-promoting rhizobacteria (PGPRs) often used for Se biofortification.
Table 2. Plant growth-promoting rhizobacteria (PGPRs) often used for Se biofortification.
MicrobesHost PlantsReferences
Acinetobacters sp. E6.2-[132]
Acinetobater sp.Triticum aestivum[139]
Alcaligenes faecalisRicinus communis, Glycine max[35]
Anabaena sp.Triticum aestivum[30,140]
Bacillus amyloliquefaciensArabidopsis thaliana[141]
Bacillus axarquiensTriticum aestivum[139]
Bacillus cereusTriticum aestivum[34]
Bacillus licheniformisTriticum aestivum[34]
Bacillus mycoidesBrassica juncea[142]
Bacillus pichinotyiTriticum aestivum[33]
Bacillus sp. E5-[132]
Bacillus sp. E6.1Triticum aestivum[139]
Bacillus sp. R12Triticum aestivum[109]
Bacillus subtilisAllium cepa[113]
Calothrix sp.Triticum aestivum[30,140]
Enterobacter ludwigiiTriticum aestivum[139]
Enterobacter sp. B16Triticum aestivum[109]
Klebsiella oxytocaTriticum aestivum[139]
Paraburkholderia megapolitanaRicinus communis, Glycine max[35]
Providencia sp.Triticum aestivum[30,140]
Pseudomnas sp. R8Triticum aestivum[109,133]
Rhizobium sp.Astragalus bisulcatus, A. drummondii[138]
Rhizosphere bacteriaScirpus robustus, Polypogon monspeliensis[143]
Se-tolerant bacteriaBrassica juncea[144]
Stenotrophomonas maltophiliaRicinus communis, Glycine max, Brassica juncea[35,142]
Stenotrophomonas sp. B19Triticum aestivum[109,133]

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Ye, Y.; Qu, J.; Pu, Y.; Rao, S.; Xu, F.; Wu, C. Selenium Biofortification of Crop Food by Beneficial Microorganisms. J. Fungi 2020, 6, 59. https://doi.org/10.3390/jof6020059

AMA Style

Ye Y, Qu J, Pu Y, Rao S, Xu F, Wu C. Selenium Biofortification of Crop Food by Beneficial Microorganisms. Journal of Fungi. 2020; 6(2):59. https://doi.org/10.3390/jof6020059

Chicago/Turabian Style

Ye, Yuanming, Jingwang Qu, Yao Pu, Shen Rao, Feng Xu, and Chu Wu. 2020. "Selenium Biofortification of Crop Food by Beneficial Microorganisms" Journal of Fungi 6, no. 2: 59. https://doi.org/10.3390/jof6020059

APA Style

Ye, Y., Qu, J., Pu, Y., Rao, S., Xu, F., & Wu, C. (2020). Selenium Biofortification of Crop Food by Beneficial Microorganisms. Journal of Fungi, 6(2), 59. https://doi.org/10.3390/jof6020059

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