Biofortification and phytoremediation of selenium in China
- 1Key Laboratory of Agri-Food Safety of Anhui Province, School of Resources and Environment–School of Plant Protection, Anhui Agriculture University, Hefei, China
- 2Advanced Lab for Selenium and Human Health-Jiangsu, Bio-Engineering Research Centre of Selenium, Suzhou Institute for Advanced Study, University of Science and Technology of China, Suzhou, China
- 3School of Earth and Space Sciences, University of Science and Technology of China, Hefei, China
- 4United States Department of Agriculture—Agricultural Research Service, Parlier, CA, USA
- 5Department of Biological Sciences, Southern Illinois University Edwardsville, Edwardsville, IL, USA
- 6Environmental Sciences Program, Southern Illinois University Edwardsville, Edwardsville, IL, USA
Selenium (Se) is an essential trace element for humans and animals but at high concentrations, Se becomes toxic to organisms due to Se replacing sulfur in proteins. Selenium biofortification is an agricultural process that increases the accumulation of Se in crops, through plant breeding, genetic engineering, or use of Se fertilizers. Selenium phytoremediation is a green biotechnology to clean up Se-contaminated environments, primarily through phytoextraction and phytovolatilization. By integrating Se phytoremediation and biofortification technologies, Se-enriched plant materials harvested from Se phytoremediation can be used as Se-enriched green manures or other supplementary sources of Se for producing Se-biofortified agricultural products. Earlier studies primarily aimed at enhancing efficacy of phytoremediation and biofortification of Se based on natural variation in progenitor or identification of unique plant species. In this review, we discuss promising approaches to improve biofortification and phytoremediation of Se using knowledge acquired from model crops. We also explored the feasibility of applying biotechnologies such as inoculation of microbial strains for improving the efficiency of biofortification and phytoremediation of Se. The key research and practical challenges that remain in improving biofortification and phytoremediation of Se have been highlighted, and the future development and uses of Se-biofortified agricultural products in China has also been discussed.
Biofortiﬁcation is an agricultural process that increases the uptake and accumulation of specific nutrients (Rouached, 2013), e.g., selenium (Se), in agricultural food products through plant breeding, genetic engineering, and manipulation of agronomic practices. The development and uses of biofortiﬁed agricultural products have been proposed as a promising functional agricultural strategy to increase the dietary nutrient intake for humans (Banuelos and Lin, 2009; Zhao and McGrath, 2009; Zhu et al., 2009; Kieliszek and Blazejak, 2013; Borrill et al., 2014). Phytoremediation of Se is the use of plants and their associated microbes for environmental cleanup, through processes that include, phytoextraction, rhizofiltration, and phytovolatilization (LeDuc and Terry, 2005; Pilon-Smits, 2005; Robinson et al., 2009; Yasin et al., 2015b). Water and soil Se-contamination resulted from coal production and agricultural drainage has caused significant toxic impacts on aquatic wildlife, such as deformity of waterfowl in the Kesterson National Wildlife Refuge in central California. Phytoremediation is an alternative and sustainable remediation technology compared with traditional physical and chemical remediation approaches. Both Se phytoextraction and biofortiﬁcation processes are based on bioaccumulation of Se that involves plant uptake, distribution, accumulation, and transformation of Se from soil into the plant’s matrix (Zhao and McGrath, 2009; Zhu et al., 2009; Bañuelos et al., 2015). Although the goals of biofortiﬁcation and phytoremediation of Se are different, these two processes can sometimes be closely connected on enhancing the efﬁciency of Se uptake and accumulation in plants (Vamerali et al., 2014). Therefore, it is important to better understand the rhizosphere physical, chemical, and biological processes that affect soil Se bioavailability, plant uptake, distribution, and transformation of Se in the plant. Understanding and optimizing these critical processes will help to determine the success of biofortiﬁcation and phytoremediation of Se (Wang et al., 2014). In this review, we will focus on Se and use this nutrient as an example to demonstrate the processes of biofortiﬁcation and phytoremediation as a combined emerging concept for addressing the environmental and human health concerns.
The Importance of Essential Micronutrient Selenium to Human Health
Selenium is a metalloid and commonly has four valence states in natural environment, including selenide (2–), elemental Se (0), selenite (4+), and selenate (6+). Selenium is an essential nutrient for humans and animals to form selenoproteins such as glutathione peroxidase (GPx) and thioredoxin reductases (TrxR; Barcelo and Poschenrieder, 2011; Meplan, 2011; Kaur et al., 2014). Selenoproteins play critical roles in reproduction, thyroid hormone metabolism, DNA synthesis, and protection from oxidative damage and infection (Sunde, 2012; Hatfield et al., 2014). Earlier laboratory and clinical trials showed some scientific evidence suggesting that Se might lower the risk of certain types of cancer (Yang et al., 1981; Clark et al., 1996; Reid et al., 2008; Wallace et al., 2009; Hatfield et al., 2014), but recent SELECT (the Selenium and Vitamin E Cancer Prevention Trial) studies indicated that this evidence is currently limited and not conclusive (Klein et al., 2011). More research is needed to confirm the potential relationship between Se daily intake and chemoprevention, especially for specific regions with specific sectors of the population.
The range between beneﬁcial and harmful Se concentrations is relatively narrow for humans and animals. The minimal Se concentration in livestock feed is 0.05–0.10 mg/kg dry forage, while the toxic Se concentration in animal feed is 2–5 mg/kg dry forage (Wilber, 1980; Wu et al., 1996). In humans, the World Health Organization (WHO) and USDA recommended the required human dietary intake of Se to be 55–200 μg/day for adults (Thomson, 2004; WHO, 2009). Selenium deficiency and low Se daily dietary intake can cause endemic diseases or other significant environmental health problems, such as Keshan disease (a degenerative heart disease observed in Keshan, China) and Kaschin–Beck disease (an osteoarthropathy that causes deformity of affected joints; Tan and Huang, 1991; Tan et al., 2002; Renwick et al., 2008). However, long-term exposure to high levels of Se can also lead to Se toxic effects. The common Se toxic symptoms include hair and nail loss and nervous system disorders that were previously observed in Se-rich areas such as in Enshi, Hubei, China (Li et al., 2012).
In plants, Se is not considered as an essential element. In general, concentrations of Se in plants grown in seleniferous soils are less than 25 mg/kg DW (Bell et al., 1992; Terry et al., 2000; Yasin et al., 2015b), except Se-hyperaccumulator species that accumulate over 1000 mg/kg Se in plant tissues (Ellis and Salt, 2003). In crop studies where soils were supplied with selenate, garlic (Allium sativum), onion (Allium cepa), leek (Allium ampeloprasum), and broccoli (Brassica oleracea) accumulated some Se as seleno-amino acid (selenomethyl cysteine, SeMeCys), while Arabidopsis thaliana and Brassica juncea accumulated Se primarily in the chemical form of selenite (Beilstein et al., 1991; Kahakachchi et al., 2004; Pilon-Smits and Quinn, 2010). Generally, SeMet is the most common dominant Se compound found in most grains, such as wheat, barley, and rye (Stadlober et al., 2001; Poblaciones et al., 2014). However, the Se hyperaccumulator Stanleya pinnata accumulated up to 90% of the total Se as MeSeCys in plant tissues (Freeman et al., 2006). For non-hyperaccumulating species, plants use S uptake and assimilation pathway to metabolize Se, since Se is chemically similar to S, and the uptake transporter and enzymes cannot distinguish between these two chemical analogs (Arvy, 1993). In addition, Se hyperaccumulator species use the same assimilation pathway from SeO4 to SeCys, but possess specialized or Se-specific transporters according to recent studies by Pilon-Smits and Quinn (2010). For example, the accumulation of selenate in S. pinnata was not inhibited by high concentrations of sulfate (Feist and Parker, 2001; Schiavon et al., 2015).
Plant-derived food products contain different amounts of Se because concentrations of Se in soil vary substantially in the natural environment. There are approximately one billion people facing with Se malnutrition in the world. For example, approximately 2/3 Chinese dietary Se intake is about 40 μg per day, which is significantly lower than the recommended Se dietary intake value of 55 μg per day according to the WHO (2009). The recommended nutritional intake (RNI) rate and upper limit (UL) of Se is 50 and 200 μg/day, respectively. For developing countries increasing the daily dietary Se intake by implementing the biofortiﬁcation strategies could substantially increase Se contents in food products. Previous studies on Se biofortification provide basic understanding on the biofortiﬁcation technology, potential health effects, and food safety regulations (White and Broadley, 2009; Zhao and McGrath, 2009; Zhu et al., 2009).
Like some other essential nutrients, Se is essential in small amounts but become toxic at high levels (Kieliszek and Blazejak, 2013; Sperotto et al., 2014). To minimize local environmental risk to wildlife, field sites with excessive Se need to be identified and remediated. In the past two decades, phytoremediation of Se has been evaluated and introduced as a successful biotechnology (Terry and Bañuelos, 2000; Barcelo and Poschenrieder, 2011). However, one of the difficulties associated with Se phytoremediation management is how to utilize/dispose of Se-contaminated plant waste materials harvested from phytoremediation sites. Different management options have been discussed by researchers regarding the disposal of plant waste materials, including landﬁll and incineration, but none of these options are considered sustainable or environmental-friendly. Generally, the plant materials harvested from phytoremediation sites can contain high concentrations of Se, which if not properly managed can be potentially toxic to waterfowl and wildlife via biomagnification. One alternative disposal option is to utilize Se-enriched plant materials for Se biofortification of agricultural products (Liu et al., 2011; Lin et al., 2014). If the Se-enriched plant material is used to amend agricultural soils, the decomposition of plant wastes will gradually release Se from the plant material, and bioavailable Se can be taken up by the crops (Bañuelos et al., 2015).
Recent developments in omics analysis and analytical technologies have led to incremental changes in research targeted on biofortification and phytoremediation of Se at molecular level (Shinmachi et al., 2010; Winkel et al., 2012; Harris et al., 2014; Schiavon et al., 2015; Visioli et al., 2015). New perspectives are emerging with the “Omics technologies” (e.g., genomics, transcriptomics, proteomics, metabolomics, nutrigenomics) and advanced analytical instruments such as micro-focused x-ray fluorescence elemental and chemical mapping and x-ray absorption near-edge structure spectroscopy, are available to further elucidate the speciation of Se in relation to specific molecular mechanisms for biofortiﬁcation and phytoremediation of Se (Bañuelos et al., 2011; Meplan, 2011; Hung et al., 2012; Winkel et al., 2012; Visioli et al., 2015). Biofortiﬁcation and phytoremediation of Se involves the changes in gene expression, protein modifications and influenced by genetic components. In particular, transcriptomics and proteomics approaches could help to further understand the phenotypic consequences of variations in Se status and unveiled Se targeted pathways for biofortiﬁcation and phytoremediation. These molecular targets and pathways could be used to unravel the effects of sulfur on biofortiﬁcation and phytoremediation of Se using non-Se hyperaccumulation plants (Barcelo and Poschenrieder, 2011). Generally, these “Omics” approaches and the recent development of analytical techniques and methods provide new perspectives to study the mechanisms for biofortiﬁcation and phytoremediation of Se and help identify and potentially develop new Se transporters to promote plant uptake and accumulation of Se.
Use of Phytoremediation Plant Materials for Biofortification
Some plants are able to accumulate moderate amounts of Se and other trace elements in their leaves or stems (Bañuelos et al., 2009, 2015; Bañuelos and Dhillon, 2010). This plant extraction process has been applied to manage soluble Se in Se-laden soils and waters. As a result, Se-enriched materials produced from a phytoremediation field site can be further used as supplementary sources of Se to produce food or feedstuff, or functional Se biofortiﬁed agricultural products. Selenium-laden plant materials can be used as green fertilizers to increase Se concentrations in agricultural soils, or used as supplemental animal feed to increase dietary intake of Se by animals. For example, Indian mustard was used for the phytoremediation of Se-contaminated water and soil in agricultural lands of the San Joaquin Valley in Central California. After harvest, the Se-laden mustard plant materials were then used as biofortiﬁed Se supplement for animals (Bañuelos, 2006; Bañuelos et al., 2009). In this regard, by integrating phytoremediation and biofortiﬁcation processes, the chemical composition of plant materials harvested from phytoremediation should be of concern. The presence of other toxic metals (e.g., Cd, Hg, and As) in the plant materials could essentially jeopardize the use of phytoremediation plant materials for Se biofortiﬁcation. When phytoremediation plant materials are used as organic sources of Se or for specific nutrients for biofortiﬁcation, the connection between phytoremediation and biofortiﬁcation can be problematic, since the remediation soil sites are oftentimes contaminated with multi-pollutants (Vamerali et al., 2014). Thus, it is critically important to screen and select the appropriate plant species and to use toxic metal-free phytoremediation ﬁeld sites for integrating Se phytoremediation and biofortiﬁcation strategies. In general, there are two very basic requirements to meet this goal: firstly, the selected plant tissues should be edible, and secondly, the edible part of the plant should accumulate higher and safe concentrations of Se, but not other toxic metals (or chemical compounds). Phytoremediation strategies commonly attempt to select plant species that accumulate more pollutants in shoots to increase the phytoremediation efﬁciency, while biofortiﬁcation focuses on increasing a specific micronutrient content in edible plant tissues. If the biofortiﬁed materials are directly consumed to increase human nutrient dietary intake, a portion of the phytoremediation plant should be edible, such as broccoli (Bañuelos, 2002; Rodrigo et al., 2014).
Previous studies indicated that the manipulation of soil physio-chemical properties, such as soil pH, Eh, total organic carbon (TOC), and chelates, can affect the uptake and accumulation of Se and other nutrient elements by plants (Vamerali et al., 2014). In addition, some organic acids exuded by roots may play important roles in determining bioavailability of Se and other mineral nutrient elements in the soil. New research efforts have been made to integrate phytoremediation with biofortiﬁcation processes (Bhatia et al., 2013; Lin et al., 2014), but this is solely dependent on the element of concern, such as Fe, Zn, and Se. There are still many scientiﬁc questions that have not been well answered. For example, future research should investigate the feasibility of biofortiﬁcation of multiple micronutrients, such as increasing accumulation of both Se and Zn in crops or vegetables (Zhu et al., 2009). In this respect, zinc hyperaccumulator Noccaea caerulescens (formerly Thlaspi caerulescens) and Se hyperaccumulator (S. pinnata) may be suitable plant species for future consideration. The application of Zn- and Se-enriched plant materials as a green manures could signiﬁcantly increase the total content and bioavailability of both Zn and Se in the soil, which will enhances the accumulation of Zn and Se in the edible portion of crops (i.e., biofortification).
Developing Se-Biofortified Agricultural Products for Human Health
The Se daily dietary intake rate varies considerably between countries/regions. With Se daily intake rates of <30 μg/d, Keshan disease has been reported in parts of China, Saudi Arabia, Czech Republic, Burundi, New Guinea, Nepal, Croatia, and Egypt (Yin and Yuan, 2012). In addition, many other countries, like India, Belgium, Brazil, UK, France, Serbia, Slovenia, Turkey, Poland, Sweden, Germany, Spain, Portugal, Denmark, Slovakia, Greece, Netherlands, Italy, China, Austria, and Ireland, were identified to have Se deficient areas because the levels of Se daily intake were below the WHO recommended amount of 55 μg/d. Korea, Australia, New Zealand, Switzerland, and Finland were identiﬁed as Se-adequate to Se-low areas because the levels of Se daily intake were in a range of 55–100 μg/d, while Japan, USA, and Canada were recognized as Se-high to Se-adequate countries with the Se daily intake of 100–200 μg/d (Yin and Yuan, 2012). In contrast, Venezuela was designated as a country with a high Se intake rate of 200–350 μg/d. If the Se daily intake is more than 550 μg/d, selenosis symptoms could be recorded, such as those observed in Enshi, China (e.g., hair and finger nail loss; Yin and Yuan, 2012). In China, the Se daily intake varied considerably from toxic levels in Enshi, to low levels of <55 μg/d in Suzhou, and to the deﬁcient levels of <11 μg/d in Keshan disease areas (Yin and Yuan, 2012).
Soil Se distribution varies signiﬁcantly in the world. More than 40 countries have limited natural Se resources, while about 80% of the world’s total Se reserves are located in Chile, the United States, Canada, China, Zambia, Zaire, Peru, Philippines, Australia, and Papua New Guinea (Liu et al., 2011). Although China is ranked the fourth in Se reserves worldwide (after Canada, the United States, and Belgium), Se-deﬁciency occurs in a geographic low-Se belt stretching from Heilongjiang Province in the northeast to Yunnan Province in the southwest, affecting 71.2% of Chinese land (Zhu et al., 2009). Therefore, Se food supplements are commonly needed for many Chinese people. In deficient areas of China, plant-based Se intake has been the primary source for humans and animals. Generally, Se-biofortified wheat, rice, and vegetables are available to provide supplemental Se (Zhu et al., 2009; Liu et al., 2011).
Selenium Biofortification Strategy
Biofortiﬁcation is a biotechnological strategy, which aims to increase micronutrient contents, e.g., Se, in the edible parts of plants, animals, or mushrooms, via breeding, biotechnology, or application of Se fertilizers. These strategies are considered to be safe and effective in alleviating micronutrient malnutrition in many areas or countries (Nestel et al., 2006; Mayer et al., 2008; Zhao and McGrath, 2009). Generally, plant-based biofortiﬁcation is the most effective and commonly used approach, especially on staple crops, because it is a natural strategy for improving the lack of nutritional trace elements like Se in the world (White and Broadley, 2009). However, Se is not an essential micronutrient for higher plants, and it is metabolized via S-transport pathway into plant tissues (see above; Harris et al., 2014). In fact, the ability to absorb and accumulate Se varies significantly among plant species. Therefore, it is important to select specific plant species that can moderately accumulate Se in their edible parts for successful Se biofortiﬁcation. Plants selected for accumulating Se are useful as a “Se-delivery vehicle” to supplement Se in animal diet in many Se-deﬁcient areas. As a result, producing Se-biofortiﬁed meat products from animals fed Se-enriched animal feed could be another important approach for higher dietary Se intake. In addition, the excrements from the Se-fortiﬁed animals could also be used as an organic source of Se-rich fertilizers for staple crops.
Agronomic Biofortification Strategies to Improve Se Nutrition
Agronomic biofortiﬁcation strategies are often based on application of mineral fertilizers to improve the Se bioavailability in the soil (White and Broadley, 2009; Mao et al., 2014). Agronomic Se-biofortiﬁcation strategies to increase crop Se contents by using inorganic Se fertilizers have been successfully implemented in Finland and New Zealand (Lyons et al., 2003; Hartikainen, 2005; Premarathna et al., 2012; Schiavon et al., 2013; Wang et al., 2013b). Different forms of Se supplied for biofortiﬁcation may result in different amounts and chemical forms of Se accumulated in plants (Brummell et al., 2011; Schiavon et al., 2013; Pezzarossa et al., 2014). Due to chemical similarity to sulfate, selenate can be readily absorbed by plants, and plant leaves can accumulate substantial amounts of selenate, but much less selenite or SeMet (De Souza et al., 1998; Zayed et al., 1999; Kikkert and Berkelaar, 2013). When organic acids are mixed with Se mineral fertilizers, Se can be chelated with organic compounds, which could increase plant uptake of Se and elevate the efﬁciency of Se fertilizers (Morgan et al., 2005; Lynch, 2007). The mixture of organic acids increased the efficiency of Se mineral fertilizers and resulted in a better developed and extensive root system (White and Broadley, 2005; Lynch, 2007; Kirkby and Johnston, 2008; White and Hammond, 2008). Moreover, the rhizosphere microbes and endophytic microbes may also play an important role in increasing phytoavailability of Se (Morgan et al., 2005; Lynch, 2007; Kirkby and Johnston, 2008; Duran et al., 2014; Lindblom et al., 2014). In this regard, the inoculation of soil with specific microbes might be beneficial for enhancing Se biofortification strategy for crops (Acuna et al., 2013; Duran et al., 2013, 2014; Lindblom et al., 2013a,b; Yasin et al., 2015a).
Genetic Engineering for Se Biofortification
Biofortiﬁcation involving genetically modified organisms is based on genetic variations or transgenic technology to increase plants’ abilities to acquire the target micronutrients and accumulate them in edible parts of plants (White and Broadley, 2009). Additionally, genetic engineering techniques can increase the level of “promoter” substances, such as ascorbate (Vitamin C), β-carotene, and cysteine-rich polypeptides, which can accelerate the absorption of micronutrients in plants, and result in higher concentrations of mineral nutrients in plants. There is also genetic variation in the concentrations of mineral elements accumulated in the grains of most cereal species, whereby researchers indicated that concentrations of Fe and Zn in cereal grain may vary 1.5- to 4-folds among genotypes depending on the genetic diversity of the material tested (Cakmak, 2008; Tiwari et al., 2008). For example, the Se levels in different plants show a descending order: brassica > bean > cereal (Liu et al., 2011). Regarding transgenic approaches, the selenocysteine methyltransferase gene of Astragalus bisulcatus (two-grooved poison vetch) was introduced into Arabidopsis thaliana (Thale cress) to overexpress Se-methylselenocysteine and γ-glutamylmethylselenocysteine in shoots (Ellis et al., 2004; Sors et al., 2005a,b; Pilon-Smits and LeDuc, 2009), and resulted in an increased accumulation of Se. Others also reported that it is possible to mutagenize the Se-related genes in Arabidopsis thaliana to improve the efﬁciency of breeding Se-enriched crops at molecular level (Pilon-Smits and LeDuc, 2009). Genetic engineering as a supplementary technique to breeding, in combination with functional genomics gene technology could significantly contribute to future Se biofortification research (Poletti and Sautter, 2005).
Selenium-Biofortified Agricultural Products in China
Considering that there are so many Se-deﬁcient regions in the world, it is promising to take advantage of Se-enriched plants/crops originating from Se-rich regions, e.g., in Enshi, China, as a natural and green resource of Se. One utilization option is to harvest the Se-enriched plants grown in Enshi to soils in other Se-deﬁcient areas as a source of organic Se fertilizer supporting forage crops and the application of this plant-based organic Se fertilizer can improve the Se status in the local soil, and likely result in crops enriched with Se. Carefully blending these Se-enriched plant materials as a forage blend for animals raised in Se-deﬁciency areas may result in Se-enriched meat products. Thirdly, the Se-enriched staple crops grown in Enshi can be regarded as naturally Se-biofortiﬁed products, and these Se-enriched products can be consumed by populations in Se-deﬁciency areas (Mei, 1985; Yuan et al., 2013). In this regard, local businesses in Enshi have developed various Se-enriched products, such as tea, rice, maize, herb, and drinks, which contribute to the on-going Se-biofortiﬁcation program in China (Yang et al., 2007).
Selecting Se Accumulating Crop Plants
Selecting or breeding crop varieties with high Se-accumulation characteristics are essential for sustaining a successful Se-biofortification program (Broadley et al., 2006). For example, the black rice-Jinlong No. 1 (cultivated by Jilin Academy of Agricultural Sciences in China) was able to accumulate Se up to 6.5 μg/g DW (Yang et al., 2007; Yin and Yuan, 2012; Wang et al., 2013a). Jiangsu Academy of Agricultural Sciences cultivated another Se-enriched rice cultivar—Longqing No. 4 from Suzi No. 4 in Yunnan province (Yang et al., 2007; Yin and Yuan, 2012; Wang et al., 2013a), while Shanxi Academy of Agricultural Sciences developed a new black wheat cultivar that can accumulate 112.8% more Se than an ordinary wheat variety (Yang et al., 2007; Yin and Yuan, 2012; Wang et al., 2013a). Using these selected Se-accumulated species/cultivars can significantly increase the significance of a Se-biofortification program (Yang et al., 2007; Wang et al., 2013a).
Foliar and Soil Application of Se Fertilizer
Foliar application of Se fertilizer is a popular practical way for producing Se-enriched foods in China (Pezzarossa et al., 2012; Boldrin et al., 2013; Wang et al., 2013a). Under optimal application conditions, Se concentrations in rice were significantly increased by 19.4% without reducing grain yields and protein/ash content (Fang et al., 2008). Chen et al. (2002) reported that, by foliar application of Se-fertilizer at a rate of 20 g Se/ha as sodium selenite and sodium selenate, the Se concentration in rice was significantly increased to 0.471 and 0.640 μg/g, respectively. Presently, Se-enriched rice is available in the market and its increased consumption can contribute to improving Se dietary intake as major staple foods in China. Tea is another popular Se-biofortiﬁed product in China. Hu et al. (2003) reported that, in addition to increased Se concentrations, the number of sprouts, yield, amino acid content, vitamin C content, as well as the sweetness and aroma of tea leaves were also significantly increased with the Se fertilizer application.
The application of soil Se fertilizers has increased the total Se and also bioavailable Se for plant uptake (Zhao et al., 2005; Broadley et al., 2010; Lavu et al., 2012, 2013; Premarathna et al., 2012; Hawrylak-Nowak, 2013; Smolen et al., 2014). Compared with natural biofortiﬁcation and foliar Se fertilizer application approaches, the soil Se fertilizers can be effective under uniform soil conditions. Earlier studies showed that soil Se fertilizers have successfully been used to enrich Se contents in a variety of agricultural products in Se-deficient regions, such as in Finland and China. However, Se fertilizers need to be reapplied annually, and farmers need to be carefully instructed on rates and the method of application. Generally, fruits and vegetables in China contain less than 3 μg/kg Se (wet weight), and rice contains less than 50 μg/kg without any application of Se (Yin and Li, 2011). The use of soil Se fertilizers can however increase the Se concentration in grains, fruits, and vegetables by several 100 times (Liu et al., 2011; Yin and Li, 2011). In recent years, the Se fertilizer application approach has been commonly used in agricultural production in some regions of China. Indeed, the novel concept of “functional agriculture” and biofortified agricultural products have been adopted by Chinese scientists and farmers, and received more acceptance and popularity (Banuelos and Lin, 2009; Zhao and Huang, 2010).
Conclusions and Future Directions
Selenium is needed for the formation of selenoproteins, including the important GPx and TrxR. The gap between the beneficial and harmful levels of Se is, however, quite narrow. The Keshan disease has been related to Se deﬁciency, including a very low dietary Se intake of 11 μg per day in Keshan, Heilongjiang Province, China, while the loss of human hair and fingernails was observed with a daily Se intake reported as high as >2000 μg/d in Enshi, central China (Qin et al., 2013). The observations of both endemic diseases of Se-deﬁciency and selenosis from excessive Se in China are indicative of greatly uneven distribution of Se in the country. Although the Se concentrations in foods and the daily Se intake decreased significantly from 1963 to 2010 in Enshi, the present daily Se intake is still above the recommended maximum safe intake 550 μg/d (Mao et al., 2014). Moreover, the total soil Se concentration ranges from 20 to 60 mg/kg DW in Enshi, which is almost 150–500 times greater than the average Se content (0.125 mg/kg DW) in Se-deﬁcient areas and approximately 50–150 times greater than the soil Se concentration (0.40 mg/kg DW) in Se-rich areas in China. In contrast, there are about 76% countries located in Se-deﬁciency regions where the Se daily intake level is less than 55 μg/d for adults. In about 70% of China, Se-deﬁciency occurs in a geographic low-Se belt stretching from northeastern Heilongjiang Province to southwestern Yunnan Province. Therefore, developing the natural Se-biofortiﬁcation program in Enshi is a positive strategy. Then, Se-enriched plants or crops can be utilized as a source organic Se fertilizer to increase the Se contents in staple crops, or used as Se-enriched forage to support livestock in Se-deﬁcient areas. In addition, Se-enriched crops, such as rice, maize, wheat, can also be consumed by populations as a natural and safe Se-supplement in Se deﬁciency areas. Furthermore, the newly-identified Se-hyperaccumulator plant (Cardamine hupingshanesis; Yuan et al., 2013) can be planted in Enshi to yield high-Se plant materials to obtain an additional source of organic Se fertilizer for Se-biofortification practices.
ZW, LY and ML prepared the draft manuscript. GB and ZL revised the manuscript. All authors have read and provided input or assistance to the submission of the final manuscript.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank all members of Advanced Laboratory for Selenium and Human Health, University of Science and Technology of China for their assistance during the preparation of this manuscript. This work was supported by the National Natural Science Foundation of China (Grant 31400091 and 50949038), the Natural Science Foundation of Anhui province (Grant 1408085MC68), the Natural Science Foundation of Jiangsu Province (Grant BK2012195 and BK2012202), Jiangsu Provincial Postdoctoral Science Foundation (Grant 1302080C), and China Postdoctoral Science Foundation (Grant 20100470108 and 2013M540518).
Acuna, J. J., Jorquera, M. A., Barra, P. J., Crowley, D. E., and Mora, M. D. (2013). Selenobacteria selected from the rhizosphere as a potential tool for Se biofortification of wheat crops. Biol. Fertil. Soils 49, 175–185. doi: 10.1007/s00374-012-0705-2
Bañuelos, G. S., Arroyo, I., Pickering, I. J., Yang, S. I., and Freeman, J. L. (2015). Selenium biofortification of broccoli and carrots grown in soil amended with Se-enriched hyperaccumulator Stanleya pinnata. Food Chem. 166, 603–608. doi: 10.1016/j.foodchem.2014.06.071
Bañuelos, G. S., and Dhillon, K. (2010). Developing a sustainable phytomanagement strategy for excessive selenium in western United States and India. Int. J. Phytoremediation 13, 208–222. doi: 10.1080/15226514.2011.568544
Bañuelos, G. S., Fakra, S. C., Walse, S. S., Marcus, M. A., Yang, S. I., Pickering, I. J., et al. (2011). Selenium accumulation, distribution, and speciation in spineless prickly pear cactus: a drought- and salt-tolerant, selenium-enriched nutraceutical fruit crop for biofortified foods. Plant Physiol. 155, 315–327. doi: 10.1104/pp.110.162867
Bañuelos, G. S., Robinson, J., and Da Roche, J. (2009). Developing selenium-enriched animal feed and biofuel from canola planted for managing Se-laden drainage waters in the Westside of Central California. Int. J. Phytoremediation 12, 243–254. doi: 10.1080/15226510903563850
Barcelo, J., and Poschenrieder, C. (2011). Hyperaccumulation of trace elements: from uptake and tolerance mechanisms to litter decomposition: selenium as an example. Plant Soil 341, 31–35. doi: 10.1007/s11104-010-0469-0
Bell, P. F., Parker, D. R., and Page, A. L. (1992). Contrasting selenate sulfate interactions in Se accumulating and nonaccumulating plant species. Soil Sci. Soc. Am. 56, 1818–1824. doi: 10.2136/sssaj1992.03615995005600060028x
Bhatia, P., Aureli, F., D’Amato, M., Prakash, R., Cameotra, S. S., Nagaraja, T. P., et al. (2013). Selenium bioaccessibility and speciation in biofortified Pleurotus mushrooms grown on selenium-rich agricultural residues. Food Chem. 140, 225–230. doi: 10.1016/j.foodchem.2013.02.054
Boldrin, P. F., Faquin, V., Ramos, S. J., Boldrin, K. V. F., Avila, F. W., and Guilherme, L. R. G. (2013). Soil and foliar application of selenium in rice biofortification. J. Food Compost Anal. 31, 238–244. doi: 10.1016/j.jfca.2013.06.002
Borrill, P., Connorton, J. M., and Balk, J. (2014). Biofortification of wheat grain with iron and zinc: integrating novel genomic resources and knowledge from model crops. Front. Plant Sci. 5:53. doi: 10.3389/fpls.2014.00053
Broadley, M. R., Alcock, J., Alford, J., Cartwright, P., Foot, I., Fairweather-Tait, S. J., et al. (2010). Selenium biofortification of high-yielding winter wheat (Triticum aestivum L.) by liquid or granular Se fertilisation. Plant Soil 332, 5–18. doi: 10.1007/s11104-009-0234-4
Broadley, M. R., White, P. J., Bryson, R. J., Meacham, M. C., Bowen, H. C., Johnson, S. E., et al. (2006). Biofortification of UK food crops with selenium. Proc. Nutr. Soc. 65, 169–181. doi: 10.1079/PNS2006490
Brummell, D. A., Watson, L. M., Pathirana, R., Joyce, N. I., West, P. J., Hunter, D. A., et al. (2011). Biofortification of tomato (Solanum lycopersicum) fruit with the anticancer compound methylselenocysteine using a selenocysteine methyltransferase from a selenium hyperaccumulator. J. Agric. Food Chem. 59, 10987–10994. doi: 10.1021/jf202583f
Chen, L., Yang, F., Xu, J., Hu, Y., Hu, Q., Zhang, Y., et al. (2002). Determination of Se concentration of rice in China and effect of fertilization of selenite and selenate on Se content of rice. J. Agric. Food Chem. 50, 5128–5130. doi: 10.1021/jf0201374
Clark, L. C., Combs, G. F., Turnbull, B. W., Slate, E. H., Chalker, D. K., Chow, J., et al. (1996). Effects of Se supplementation for cancer prevention in patients with carcinoma of the skin a randomized controlled trial—a randomized controlled trial. J. Am. Med. Assoc. 276, 1957–1963. doi: 10.1001/jama.1996.03540240035027
De Souza, M. P., Pilon-Smits, E. A. H., Lytle, C. M., Hwang, S., Tai, J., Honma, T. S. U., et al. (1998). Rate-limiting steps in selenium assimilation and volatilization by Indian Mustard. Plant Physiol. 117, 1487–1494. doi: 10.1104/pp.117.4.1487
Duran, P., Acuna, J. J., and Jorquera, M. A. (2013). 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. 57, 275–280. doi: 10.1016/j.jcs.2012.11.012
Duran, P., Acuna, J. J., and Jorquera, M. A. (2014). Endophytic bacteria from selenium-supplemented wheat plants could be useful for plant-growth promotion, biofortification and Gaeumannomyces graminis biocontrol in wheat production. Biol. Fertil. Soils 50, 983–990. doi: 10.1007/s00374-014-0920-0
Ellis, D. R., Sors, T. G., Brunk, D. G., Albrecht, C., Orser, C., Lahner, B., et al. (2004). Production of Se-methylselenocysteine in transgenic plants expressing selenocysteine methyltransferase. BMC Plant Biol. 4:1. doi: 10.1186/1471-2229-4-1
Fang, Y., Wang, L., Xin, Z., Zhao, L., An, X., and Hu, Q. (2008). Effect of foliar application of zinc, selenium, and iron fertilizers on nutrients concentration and yield of rice grain in China. J. Agric. Food Chem. 56, 2079–2084. doi: 10.1021/jf800150z
Freeman, J. L., Quinn, C. F., Marcus, M. A., Fakra, S., and Pilon-Smits, E. A. H. (2006). Se tolerant diamondback moth disarms hyperaccumulator plant defense. Curr. Biol. 16, 2181–2192. doi: 10.1016/j.cub.2006.09.015
Harris, J., Schneberg, K. A., and Pilon-Smits, E. A. H. (2014). Sulfur-selenium-molybdenum interactions distinguish selenium hyperaccumulator Stanleya pinnata from non-hyperaccumulator Brassica juncea (Brassicaceae). Planta 239, 479–491. doi: 10.1007/s00425-013-1996-8
Hatfield, D. L., Tsuji, P. A., Carlson, B. A., and Gladyshev, V. N. (2014). Selenium and selenocysteine: roles in cancer, health, and development. Trends Biochem. Sci. 39, 112–120. doi: 10.1016/j.tibs.2013.12.007
Hawrylak-Nowak, B. (2013). Comparative effects of selenite and selenate on growth and selenium accumulation in lettuce plants under hydroponic conditions. Plant Growth Regul. 70, 149–157. doi: 10.1007/s10725-013-9788-5
Hu, Q., Xu, J., and Pang, G. J. (2003). Effect of Se on increasing the antioxidant activity of tea leaves harvested during the early spring tea producing season. J. Agric. Food Chem. 51, 3379–3381. doi: 10.1021/jf0341417
Hung, C. Y., Holliday, B. M., Kaur, H., Yadav, R., Kittur, F. S., and Xie, J. H. (2012). Identification and characterization of selenate- and selenite-responsive genes in a Se-hyperaccumulator Astragalus racemosus. Mol. Biol. Rep. 39, 7635–7646. doi: 10.1007/s11033-012-1598-8
Kahakachchi, C., Boakye, H. T., Uden, P. C., and Tyson, J. F. (2004). Chromatographic speciation of anionic and neutral selenium compounds in Se-accumulating Brassica juncea (Indian mustard) and in selenized yeast. J. Chromatogr. A 1054, 303–312. doi: 10.1016/j.chroma.2004.07.083
Kirkby, E. A., and Johnston, A. E. (2008). “Soil and fertilizer phosphorus in relation to crop nutrition,” in The Ecophysiology of Plant-Phosphorus Interactions, eds J. P. Hammond and P. J. White (Dordrecht: Springer), 177–223. doi: 10.1007/978-1-4020-8435-5_9
Klein, E. A., Thompson, I. M. Jr., Tangen, C. M., Crowley, J. J., Lucia, M. S., and Goodman, P. J. (2011). Vitamin E and the risk of prostate cancer: the selenium and vitamin E cancer prevention trial (SELECT). JAMA 306, 1549–1556. doi: 10.1001/jama.2011.1437
Lavu, R. V. S., De Schepper, V., Steppe, K., Majeti, P. N. V., Tack, F., and Du Laing, G. (2013). Use of selenium fertilizers for production of Se-enriched kenaf (Hibiscus cannabinus): effect on Se concentration and plant productivity. J. Plant Nutr. Soil Sci. 176, 634–639. doi: 10.1002/jpln.201200339
Lavu, R. V. S., Du Laing, G., Van de Wiele, T., Pratti, V. L., Willekens, K., Vandecasteele, B., et al. (2012). Fertilizing soil with selenium fertilizers: impact on concentration, speciation, and bioaccessibility of selenium in leek (Allium ampeloprasum). J. Agric. Food Chem. 60, 10930–10935. doi: 10.1021/jf302931z
Lin, Z. Q., Haddad, S., Hong, J., Morrissy, J., Bañuelos, G. S., and Zhang, L. Y. (2014). “Use of selenium-contaminated plants from phytoremediation for production of selenium-enriched edible mushrooms,” in Selenium in the Environment and Human Health, eds G. S. Bañuelos, Z.-Q. Lin, and X. B. Yin (Boca Raton, FL: CRC Press), 124–126.
Lindblom, S. D., Fakra, S. C., Landon, J., Schulz, P., Tracy, B., and Pilon-Smits, E. A. H. (2014). Inoculation of selenium hyperaccumulator Stanleya pinnata and related non-accumulator Stanleya elata with hyperaccumulator rhizosphere fungi—investigation of effects on Se accumulation and speciation. Physiol. Plant. 150, 107–118. doi: 10.1111/ppl.12094
Lindblom, S. D., Fakra, S. C., Landon, J., Schulz, P., Tracy, B., and Pilon-Smits, E. A. H. (2013a). Inoculation of Astragalus racemosus and Astragalus convallarius with selenium-hyperaccumulator rhizosphere fungi affects growth and selenium accumulation. Planta 237, 717–729. doi: 10.1007/s00425-012-1789-5
Lindblom, S. D., Valdez-Barillas, J. R., Fakra, S. C., Marcus, M. A., Wangeline, A. L., and Pilon-Smits, E. A. H. (2013b). Influence of microbial associations on selenium localization and speciation in roots of Astragalus and Stanleya hyperaccumulators. Environ. Exp. Bot. 88, 33–42. doi: 10.1016/j.envexpbot.2011.12.011
Liu, Y., Li, F., Yin, X. B., and Lin, Z. Q. (2011). “Plant-based biofortiﬁcation: from phytoremediation to Se-enriched agriculture products,” in Green Chemistry for Environmental Sustainability, eds S. K. Sharma and A. Mudhoo (Boca Raton, FL: CRC Press), 341–356.
Mao, H., Wang, J., Wang, Z., Zan, Y., Lyons, G., and Zou, C. (2014). Using agronomic biofortification to boost zinc, selenium, and iodine concentrations of food crops grown on the loess plateau in China. J. Soil Sci. Plant Nutr. 14, 459–470. doi: 10.4067/S0718-95162014005000036
Pezzarossa, B., Remorini, D., Gentile, M. L., and Massai, R. (2012). Effects of foliar and fruit addition of sodium selenate on selenium accumulation and fruit quality. J. Sci. Food Agric. 92, 781–786. doi: 10.1002/jsfa.4644
Pezzarossa, B., Rosellini, I., Borghesi, E., Tonutti, P., and Malorgio, F. (2014). Effects of Se-enrichment on yield, fruit composition and ripening of tomato (Solanum lycopersicum) plants grown in hydroponics. Sci. Hortic. 165, 106–110. doi: 10.1016/j.scienta.2013.10.029
Pilon-Smits, E. A. H., and Quinn, C. F. (2010). “Selenium metabolism in plants,” in Cell Biology of Metals and Nutrients. Plant Cell Monographs 17, eds R. Hell and P. R. Mendel (Heidelberg: Springer-Verlag), 225–251.
Poblaciones, M. J., Rodrigo, S., Santamaría, O., Chen, Y., and McGrath, S. P. (2014). Agronomic selenium biofortification in Triticum durum under Mediterranean conditions: from grain to cooked pasta. Food Chem. 146, 378–384. doi: 10.1016/j.foodchem.2013.09.070
Premarathna, L., McLaughlin, M. J., Kirby, J. K., Hettiarachchi, G. M., Stacey, S., and Chittleborough, D. J. (2012). Selenate-enriched urea granules are a highly effective fertilizer for selenium biofortification of paddy rice grain. J. Agric. Food Chem. 60, 6037–6044. doi: 10.1021/jf3005788
Qin, H. B., Zhu, J. M., Liang, L., and Wang, M. S. (2013). The bioavailability of selenium and risk assessment for human selenium poisoning in high-Se areas, China. Environ. Int. 52, 66–74. doi: 10.1016/j.envint.2012.12.003
Reid, M. E., Dufﬁeld-Lillico, A. J., Slate, E., Natarajan, N., Turnbull, B., Jacobs, E., et al. (2008). The nutritional prevention of cancer: 400 mcg per day Se treatment. Nutr. Cancer 60, 155–163. doi: 10.1080/01635580701684856
Renwick, A. G., Dragsted, L. O., and Fletcher, R. J. (2008). Minimising the population risk of micronutrient deficiency and over-consumption: a new approach using selenium as an example. Eur. J. Nutr. 47, 17–25. doi: 10.1007/s00394-007-0691-6
Rodrigo, S., Santamaria, O., and Chen, Y. (2014). Selenium speciation in malt, wort, and beer made from selenium-biofortified two-rowed barley grain. J. Agric. Food Chem. 62, 5948–5953. doi: 10.1021/jf500793t
Schiavon, M., dall’Acqua, S., Mietto, A., Pilon-Smits, E. A. H., Sambo, P., Masi, A., et al. (2013). Impact of selenium fertilization on chemical composition and antioxidant constituents of tomato (Solanum lycopersicon L.). J. Agric. Food Chem. 61, 10542–10554. doi: 10.1021/jf4031822
Schiavon, M., Pilon, M., Malagoli, M., and Pilon-Smits, E. A. H. (2015). Exploring the importance of sulfate transporters and ATP sulphurylases for selenium hyperaccumulation—a comparison of Stanleya pinnata and Brassica juncea (Brassicaceae). Front. Plant. Sci. 6:2. doi: 10.3389/fpls.2015.00002
Shinmachi, F., Buchner, P., Stroud, J. L., Parmar, S., Zhao, F. J., McGrath, S. P., et al. (2010). Influence of sulfur deficiency on the expression of specific sulfate transporters and the distribution of sulfur, selenium, and molybdenum in wheat. Plant Physiol. 153, 327–336. doi: 10.1104/pp.110.153759
Smolen, S., Kowalska, I., and Sady, W. (2014). Assessment of biofortification with iodine and selenium of lettuce cultivated in the NFT hydroponic system. Sci. Hortic. 166, 9–16. doi: 10.1016/j.scienta.2013.11.011
Sors, T. G., Ellis, D. R., Na, G. N., Lahner, B., Lee, S., Leustek, T., et al. (2005a). Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J. 42, 785–797. doi: 10.1111/j.1365-313X.2005.02413.x
Stadlober, M., Sager, M., and Irgolic, K. j. (2001). Effects of selenate supplemented fertilisation on the selenium level of cereals–identification and quantification of selenium compounds by HPLC-ICP-MS. Food Chem. 73, 357–366. doi: 10.1016/S0308-8146(01)00115-7
Sunde, R. A. (2012). “Selenium,” in Modern Nutrition in Health and Disease, 11th Edn, eds A. C. Ross, B. Caballero, R. J. Cousins, K. L. Tucker, and T. R. Ziegler (Philadelphia, PA: Lippincott Williams & Wilkins), 225–237.
Tiwari, V. K., Rawat, N., Neelam, K., Randhawa, G. S., Singh, K., Chhuneja, P., et al. (2008). Development of Triticum turgidum sub sp. durum—Aegilops longissima amphiploids with high iron and zinc content through unreduced gamete formation in F1 hybrids. Genome 51, 757–766. doi: 10.1139/G08-057
Vamerali, T., Bandiera, M., and Lucchini, P. (2014). Long-term phytomanagement of metal-contaminated land with field crops: integrated remediation and biofortification. Eur. J. Agron. 53, 56–66. doi: 10.1016/j.eja.2013.11.008
Visioli, G., D’Egidio, S., and Sanangelantoni, A. M. (2015). The bacterial rhizobiome of hyperaccumulators: future perspectives based on omics analysis and advanced microscopy. Front. Plant Sci. 5:752. doi: 10.3389/fpls.2014.00752
Wallace, K., Kelsey, K. T., Schned, A., Morris, J. S., Andrew, A. S., and Karagas, M. R. (2009). Se and risk of bladder cancer: a population-based case-control study. Cancer Prev. Res. 2, 70–73. doi: 10.1158/1940-6207.CAPR-08-0046
Wang, J. W., Wang, Z. H., and Mao, H. (2013a). Increasing Se concentration in maize grain with soil- or foliar-applied selenite on the Loess Plateau in China. Field Crops Res. 150, 83–90. doi: 10.1016/j.fcr.2013.06.010
Wang, Y. D., Wang, X., and Wong, Y. S. (2013b). Generation of selenium-enriched rice with enhanced grain yield, selenium content and bioavailability through fertilisation with selenite. Food Chem. 141, 2385–2393. doi: 10.1016/j.foodchem.2013.05.095
Wang, Y., Yang, X., Zhang, X., Dong, L., Zhang, J., Wei, Y., et al. (2014). Improved plant growth and Zn accumulation in grains of rice (Oryza sativa L.) by inoculation of endophytic microbes isolated from a Zn Hyperaccumulator, Sedum alfredii H. J. Agric. Food Chem. 62, 1783–1791. doi: 10.1021/jf404152u
White, P. J., and Broadley, M. R. (2009). Biofortiﬁcation of crops with seven mineral elements often lacking in human diets—iron, zinc, copper, calcium, magnesium, Se and iodine. New Phytol. 182, 49–84. doi: 10.1111/j.1469-8137.2008.02738.x
White, P. J., and Hammond, J. P. (2008). “Phosphorus nutrition of terrestrial plants,” in The Ecophysiology of Plant-Phosphorus Interactions, eds P. J. White and J. P. Hammond (Dordrecht: Springer), 51–81. doi: 10.1007/978-1-4020-8435-5_4
Winkel, L. H., Johnson, C. A., Lenz, M., Grundl, T., Leupin, O. X., Amini, M., et al. (2012). Environmental selenium research: from microscopic processes to global understanding. Environ. Sci. Technol. 46, 571–579. doi: 10.1021/es203434d
WHO. (2009). Global Health Risks: Mortality and Burden of Disease Attributable to Selected Major Risks. Available at: http://www.who.int/healthinfo/global_burden_disease/GlobalHealthRisks_report_annex.pdf (accessed March 5, 2014).
Wu, L., Mantgem, P. J. V., and Guo, X. (1996). Effects of forage plant and ﬁeld legume species on soil Se redistribution, leaching and bioextraction in soils contaminated by agricultural drain water sediment. Arch. Environ. Contam. Toxicol. 31, 329–338. doi: 10.1007/BF00212671
Yang, G. Q., Wang, S. Z., Zhou, R. H., Sun, S. Z., and Man, R. E. (1981). Research on the etiology of an endemic disease characterized by loss of nails and hair in Enshi county. J. Chin. Acad. Med. 3, 1–6.
Yang, X. E., Chen, W. R., and Feng, Y. (2007). Improving human micronutrient nutrition through biofortification in the soil-plant system: China as a case study. Environ. Geochem. Health 29, 413–428. doi: 10.1007/s10653-007-9086-0
Yasin, M., El-Mehdawi, A. F., Anwar, A., Pilon-Smits, E. A. H., and Faisal, M. (2015a). Microbial-enhanced selenium and iron biofortification of wheat (Triticum aestivum L.)—Applications in Phytoremediation and Biofortification. Int. J. Phytoremediation 17, 341–347. doi: 10.1080/15226514.2014.922920
Yasin, M., El-Mehdawi, A. F., Jahn, C. E., Anwar, A, Turner, M. F. S., Faisal, M., et al. (2015b). Seleniferous soils as a source for production of selenium-enriched foods and potential of bacteria to enhance plant selenium uptake. Plant Soil 386, 385–394. doi: 10.1007/s11104-014-2270-y
Yin, X. B., and Li, F. (2011). “The standardization in Se biofortiﬁcation,” in Se Global Perspectives of Ion Human, Animals and The Environment, eds G. S. Bañuelos, Z. Q. Lin, X. B. Yin, and N. Duan (Hefei: University of Science and Technology of China Press), 113–114.
Yuan, L., Zhu, Y., Lin, Z. Q., Bañuelos, G., and Li, W. (2013). A novel selenocystine-accumulating plant in selenium-mine drainage area in Enshi, China. PLoS ONE 8:e65615. doi: 10.1371/journal.pone.0065615
Zhu, Y. G., Pilon-Smits, E. A. H., Zhao, F. J., Williams, P. N., and Meharg, A. A. (2009). Selenium in higher plants: understanding mechanisms for biofortiﬁcation and phytoremediation. Trends Plant Sci. 14, 436–442. doi: 10.1016/j.tplants.2009.06.006
Keywords: biofortification, phytoremediation, selenium, deficiency, nutrient
Citation: Wu Z, Bañuelos GS, Lin Z-Q, Liu Y, Yuan L, Yin X and Li M (2015) Biofortification and phytoremediation of selenium in China. Front. Plant Sci. 6:136. doi: 10.3389/fpls.2015.00136
Received: 01 November 2014; Accepted: 20 February 2015;
Published: 20 March 2015.
Edited by:David W. M. Leung, University of Canterbury, New Zealand
Reviewed by:Khurram Bashir, RIKEN Yokohama Campus, Japan
John L. Freeman, Intrinsyx Technologies Corporation, USA
Copyright © 2015 Wu, Bañuelos, Lin, Liu, Yuan, Yin and Li. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Linxi Yuan and Xuebin Yin, Advanced Lab for Selenium and Human Health-Jiangsu, Bio-Engineering Research Centre of Selenium, Suzhou Institute for Advanced Study, University of Science and Technology of China, Suzhou 215123, Jiangsu, China email@example.com; firstname.lastname@example.org; Miao Li, Key Laboratory of Agri-Food Safety of Anhui Province, School of Resources and Environment–School of Plant Protection, Anhui Agriculture University, Hefei 230036, Anhui, China email@example.com