An Overview of Selenium Uptake, Metabolism, and Toxicity in Plants

Abstract

Selenium (Se) is an essential micronutrient for humans and animals, but lead to toxicity when taken in excessive amounts. Plants are the main source of dietary Se, but essentiality of Se for plants is still controversial. However, Se at low doses protects the plants from variety of abiotic stresses such as cold, drought, desiccation, and metal stress. In animals, Se acts as an antioxidant and helps in reproduction, immune responses, thyroid hormone metabolism. Selenium is chemically similar to sulfur, hence taken up inside the plants via sulfur transporters present inside root plasma membrane, metabolized via sulfur assimilatory pathway, and volatilized into atmosphere. Selenium induced oxidative stress, distorted protein structure and function, are the main causes of Se toxicity in plants at high doses. Plants can play vital role in overcoming Se deficiency and Se toxicity in different regions of the world, hence, detailed mechanism of Se metabolism inside the plants is necessary for designing effective Se phytoremediation and biofortification strategies.

Full text

REVIEW
published: 11 January 2017
doi: 10.3389/fpls.2016.02074
Frontiers in Plant Science | www.frontiersin.org 1January 2017 | Volume 7 | Article 2074
Edited by:
Prabodh Kumar Trivedi,
National Botanical Research Institute
(CSIR), India
Reviewed by:
Sudhakar Srivastava,
Banaras Hindu University, India
Seema Mishra,
National Botanical Research Institute
(CSIR), India
*Correspondence:
Meetu Gupta
meetu_gpt@yahoo.com;
mgupta@jmi.ac.in
Specialty section:
This article was submitted to
Plant Traffic and Transport,
a section of the journal
Frontiers in Plant Science
Received: 13 October 2016
Accepted: 29 December 2016
Published: 11 January 2017
Citation:
Gupta M and Gupta S (2017) An
Overview of Selenium Uptake,
Metabolism, and Toxicity in Plants.
Front. Plant Sci. 7:2074.
doi: 10.3389/fpls.2016.02074
An Overview of Selenium Uptake,
Metabolism, and Toxicity in Plants
Meetu Gupta *and Shikha Gupta
Ecotoxicogenomics Lab, Department of Biotechnology, Jamia Millia Islamia, New Delhi, India
Selenium (Se) is an essential micronutrient for humans and animals, but lead to toxicity
when taken in excessive amounts. Plants are the main source of dietary Se, but
essentiality of Se for plants is still controversial. However, Se at low doses protects
the plants from variety of abiotic stresses such as cold, drought, desiccation, and
metal stress. In animals, Se acts as an antioxidant and helps in reproduction, immune
responses, thyroid hormone metabolism. Selenium is chemically similar to sulfur, hence
taken up inside the plants via sulfur transporters present inside root plasma membrane,
metabolized via sulfur assimilatory pathway, and volatilized into atmosphere. Selenium
induced oxidative stress, distorted protein structure and function, are the main causes of
Se toxicity in plants at high doses. Plants can play vital role in overcoming Se deficiency
and Se toxicity in different regions of the world, hence, detailed mechanism of Se
metabolism inside the plants is necessary for designing effective Se phytoremediation
and biofortification strategies.
Keywords: selenium, toxicity, sulfate transporters, phytoremediation, biofortification, oxidative stress
INTRODUCTION
The breakthrough in selenium (Se) research came into existence in 1957, when Schwartz and
Foltz showed that addition of Se in fodder prevented muscular dystrophy and liver cirrhosis in
rats (Rayman, 2000). Another turning point in Se research came through the discovery of Se in
enzyme Glutathione peroxidase (Rotruck et al., 1973; Behne and Kyriakopoulos, 2001). Since, then
the essentiality of Se for animals and human beings came into limelight, and is considered as an
essential nutrient in human diet (Hartikainen, 2005). Although, Se performs in variety of functions,
its antioxidant and anticancerous properties are of primary concern for mankind (Reid et al.,
2008; Wallace et al., 2009; Hatfield et al., 2014). Seleno-aminoacids, selenocysteine (SeCys), and
selenomethionine (SeMet) are responsible for most of the reported biomedical effects of dietary
Se (Dumont et al., 2006). Selenium acts as the catalytic centre of several selenoproteins, such as
glutathione peroxidase (GSHPx), thioredoxin reductase, and iodothyronine-deiodinases hence, it
is important in the scavenging of free radicals, protection against oxidative stress, strengthening
of immune system etc. (Méplan, 2011; Kaur et al., 2014). Deficiency of Se in human diet causes
growth retardation, impaired bone metabolism and abnormalities in thyroid function (Reeves and
Hoffman, 2009).
Certain regions of the world are Se-deficient while others are becoming Se-toxic due to natural
and anthropogenic activities (Zhu et al., 2009). Both the problems of Se i.e., deficiency and toxicity
are harmful to humans and animals (Box 1), hence, all over the world it is called as two edged
sword. WHO has recommended 50–55 µg/day Se in human diet all over the world (WHO, 2009;
Malagoli et al., 2015; Wu et al., 2015). In humans, Se deficiency occurs when dietary intake of Se is
(<40µg/day) and chronic toxicity is observed above levels of (>400 µg/day) (Winkel et al., 2012).

Gupta and Gupta An Overview of Selenium Understanding in Plants
BOX 1 | Role of Se in animals (Mehdi et al., 2013).
Tragic instance of Se-toxicity in humans was observed in Hubei Province, China after digesting Se rich plants (Fordyce et al., 2000). Livestock is threatened persistently
due to weathering of Se-rich bedrocks, and anthropogenic activities like irrigation and mining. Se toxicity lead to a condition called selenosis i.e., garlic odor
of the breath, gastrointestinal disorders, hair loss, sloughing of nails, and neurological damage. In extreme selenosis cirrhosis of the liver, pulmonary edema, or
even death can occur. Selenium deficiency causes Keshan disease i.e., weakening of heart and also atrophy, degeneration, and necrosis of cartilage tissue in the
joints.
About 30 selenoproteins have been identified in animals, which play important roles in antioxidant defense, DNA synthesis, reproduction, immune response, formation
of thyroid hormones. Apart from above roles, several studies have reported anticancerous effect of Se against liver, pancreas, prostate, esophagus, and colon cancer.
In some studies, cardiovascular risk was found to be associated with low intake of Se and Se-enriched diet found to improve overall health conditions in patients
suffering from cardiovascular diseases. Also, Se helps in embryo implantation, placenta retention, reduces infertility by increasing sperm mobility, testosterone, and
sperm synthesis. Selenoproteins like Glutathione peroxidase, Thioredoxin reductase play important role as antioxidants in maintaining intracellular redox potential.
Deiodinase is involved in thyroid hormone metabolism. Selenoprotein P transports Se between tissues and is an important extracellular antioxidant constitutes about
50% of plasma Se.
In livestock, the minimal requirement of Se is 0.05–0.10 mg/kg
dry forage while, the toxic Se concentration in animal feed is 2–
5 mg/kg dry forage (Wu et al., 2015). Keshan and Kashin Beck
are severe Se deficiency diseases reported in China and Central
Serbia due to low intake of Se in diet at a level of 7–11 µg/day
(Renwick et al., 2008; Wu et al., 2015). Toxic symptoms of Se
were known before the discovery of this element, when Marco
Polo in 13th century observed that in Province of Shanxi, in
China, animals died of eating certain Se accumulators (Bodnar
et al., 2012). However, toxicity of Se came into limelight after
the tragedy of Kesterson wild-life Refuge and Reservoir in San
Joaquin Valley in California in 1980, which gave this element a
worldwide concern (Winkel et al., 2012). The essentiality of Se to
plants is still debatable however; beneficial effect of low doses of
Se on plants has been reported by several workers (Cartes et al.,
2010; Hasanuzzaman et al., 2011; Saidi et al., 2014).
Selenium was discovered accidentally by Swedish chemist
Jons Jacob Berzelius in 1817. The word selenium is derived
from Greek word “selene” which means moon (Reilly, 2006;
Bodnar et al., 2012). Selenium is a metalloid belongs to group 16
(Oxygen Family) of the periodic table. Being member of the same
group of the periodic table, ionic radius of Se and S are closer,
hence, physico-chemical properties of both elements are similar
to each other (Bodnar et al., 2012). Due to its semiconductive
properties, Se is widely used in making electronic and electrical
goods. In nature, it occurs as pyrites of Cu, sulfides of Pb, Au,
and Cu. It is also a byproduct of metallurgical operations, and
widely used in glass industry, paints, lubricating oil, pigments,
food supplements, agricultural products etc. (Bodnar et al., 2012;
Mehdi et al., 2013).
Plants are the main source of dietary Se for human beings
and animals hence, knowledge of the Se compounds in plants is
crucial (Dumont et al., 2006). Selenium shares similar chemical
properties to sulfur, hence taken up inside the plants via sulfate
transporters and assimilated by sulfur assimilating pathway (Sors
et al., 2005; Dumont et al., 2006) as shown in (Figure 1).
SELENIUM IN ENVIRONMENT
Selenium occurs naturally in sedimentary rocks formed during
the carboniferous to quaternary period (White et al., 2004).
Worldwide, average Se concentration in soils is 0.4 mg/Kg
FIGURE 1 | Pictorial representation of the interface of Se with soil,
plant and atmosphere. Selenium present in soil is transported inside the
plant through sulfate transporters present in the plasma membrane of root
cells. It is then assimilated to organic Se via sulfur metabolic pathway inside
the plant and volatilized as DMSe (Dimethylselenide) and DMDSe
(Dimethyldiselenide) into atmosphere.
however, in seleniferous soils elevated levels of Se (>2–
5000 mg/Kg) are found (Hartikainen, 2005). The occurrence of
Se in soil depends upon type of soil, organic matter and rainfall
(Sors et al., 2005).
Mountainous countries like Finland, Sweden, and Scotland
are generally deficient in soil Se content whereas Shale soils
and dried regions of the world are Se-rich regions. Countries
like UK, France, India, Belgium, Brazil, Serbia, Slovenia, Spain,
Portugal, Turkey, Poland, Germany, Denmark, Slovakia, Austria,
Ireland, Greece, Netherlands, Italy, China, Nepal, Saudi Arabia,
Czech Republic, Croatia, Egypt, Burundi, and New Guinea are
reported to have Se deficient areas (Zhu et al., 2009; Yin and
Yuan, 2012;Figure 2) while, Se rich regions are North-East
region of Punjab in India (Bajaj et al., 2011), Enshi district
in Hubei province region in China (Feng C. X. et al., 2009),
State of Para in Brazilian Amazon (Lemire et al., 2009), Japan,
Greenland (Fordyce et al., 2005), USA, Venezuela and Canada
(Yin and Yuan, 2012;Figure 2). About 80% of the world’s total
Se reserves are located in Peru, China, Chile, the United States,
Frontiers in Plant Science | www.frontiersin.org 2January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
FIGURE 2 | Outline of occurrence of Se in different regions of world as Se-deficient, Se-low and Se-rich regions.
Canada, Zambia, Philippines, Zaire, Australia, and New Guinea
(Liu et al., 2011). Although China is ranked the fourth in Se
reserves worldwide (after Canada, United States, and Belgium),
Se-deficiency occurs in a geographic low-Se belt stretching from
Heilongjiang Province in the northeast to Yun-nan Province
in the southwest, affecting 71.2% of Chinese land (Zhu et al.,
2009). Almost 40 countries in the world have limited natural
Se resources. Certain areas in countries like Switzerland, Korea,
Australia, New Zealand, and Finland are also identified as Se
adequate to Se low regions (Wu et al., 2015;Figure 2).
Selenium level in public water supplies should not increase
more than 10 µg/L (NAS, 1976, 1977; Gore et al., 2010). In
underground water, Se concentration is increasing due to overuse
of Se-containing fertilizers (Winkel et al., 2012) and has reached
upto estimated concentration of 0.12 µg/L in Belgium, 2.4–40
µg/L in France (Mehdi et al., 2013), and 341 µg/L in Punjab
(Bajaj et al., 2011). In fresh and sea water, its concentration
varies from 4000 to 12000 µg/L. WHO has recommended 10
µg/L as the lower intake limit of Se in drinking water (Mehdi
et al., 2013). Natural and anthropogenic activities add Se into
atmosphere, and play an important role in biogeochemical
cycling of Se in environment (Winkel et al., 2012). Natural
activities include, forest fire, soil erosion whereas, anthropogenic
activities are burning of fossil fuels, tires, papers etc. (Mehdi et al.,
2013). In atmosphere, Se is mostly present as volatile organic
compounds i.e., DMSe, DMDSe, methaneselenol, and volatile
inorganic compound (SeO2). SeO2is unstable and converted into
selenious acid. The Se content in air is generally low, as compared
to soil and water, and ranges between 1 and 10 ng/m3(Mehdi
et al., 2013).
Selenium content in food sources varies from plant to plant.
It depends upon Se uptake and accumulating capacity of plant,
soil Se content, which varies according to geographical locations
and presence of other elements in soil (Dumont et al., 2006;
Bodnar et al., 2012; Mehdi et al., 2013). Fruits generally contain
low amount of Se as compared to vegetables. Selenium content in
cereals ranges between 0.01 and 0.55 µg/g, and in milk and dairy
products varies between 0.001 and 0.17 µg/g FW (Dumont et al.,
2006). Brazil nuts, Brassica species, garlic effectively accumulate
Se, and are rich sources of Se in diet (Dumont et al., 2006; Bodnar
et al., 2012).
SELENIUM UPTAKE AND ACCUMULATION
IN PLANTS
Selenium exists as inorganic and organic forms in nature.
Inorganic forms are selenate (SeO2−
4), selenite (SeO2−
3), selenide
(Se2−), elemental Se, and the major organic forms are SeCys and
SeMet (Sors et al., 2005; Bodnar et al., 2012; Wu et al., 2015).
Selenium Uptake
The uptake, translocation and distribution of Se depends upon
plant species, phases of development, form and concentration
of Se, physiological conditions (salinity and soil pH) and
presence of other substances, activity of membrane transporters,
translocation mechanisms of plant (Zhao et al., 2005; Li et al.,
2008; Renkema et al., 2012). Selenate (SeO2−
4) is the most
prevalent form of bioavailable Se in agricultural soils, and more
water soluble than selenite (Sors et al., 2005; Missana et al., 2009).
In alkaline soils, Se mostly exists as selenate whereas, in acidic
Frontiers in Plant Science | www.frontiersin.org 3January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
soils it exists as selenite. Both forms of Se differ in terms of their
mobility and absorption within the plant and are metabolized
to form selenocompounds (Li et al., 2008). Translocation of an
ion or molecule to shoot tissue depends on the rate of xylem
loading and the rate of transpiration (Renkema et al., 2012).
Kikkert and Berkelaar (2013) evaluated mobility of Se species in
Canola and Wheat by studying translocation factor and was in
the following order: selenate>SeMet>selenite/SeCys. Selenium
uptake in plants is mediated by transporters present in root cell
membrane. Selenite is found to be transported by phosphate
transport mechanism (Li et al., 2008) whereas, selenate through
sulfate transporters and channels (Feist and Parker, 2001; Zhang
et al., 2003).
Nutritional status inside and outside the plant; determines
the preference of these transporters for selenate and sulfate
(White et al., 2004). Under high external sulfate concentrations
selectivity of these transporters for Se decreases, and inducible
sulfate transporters showed higher selectivity for sulfate over
selenate than constitutive active sulfate transporters (White et al.,
2004). In Arabidopsis thaliana sulfate transporters, SULTR1;2
and SULTR1 found to transport selenate inside the plant (El
Kassis et al., 2007). In other study enhanced selenate resistance
in SULTR1;2 lacking Arabidopsis plants but not SULTR1 suggests
that SULTR1;2 is the predominant transporter for uptake of
selenate into the plant root (Shibagaki et al., 2002; El Kassis
et al., 2007). In Triticum aestivum, sulfur starvation enhanced
Se uptake (Li et al., 2008). According to several workers,
selenite uptake is known to be done through passive diffusion
(Terry et al., 2000; Ellis and Salt, 2003), however, in another
study it is mediated by active transport as uptake of selenite
was significantly inhibited by metabolic inhibitor CCCP (Li
et al., 2008). Terry et al. (2000) reported non-involvement
of membrane transporters in selenite uptake. Li et al. (2008)
reported enhanced selenite uptake in phosphorous deficiency,
which indicates selenite uptake by phosphate transporters, and
supports the earlier findings of decreased selenite uptake under
increasing phosphate concentrations.
Se Accumulation in Plants
Generally, Se concentration found to be higher in younger
leaves as compared to older ones during seedling growth (Cappa
et al., 2014; Harris et al., 2014). Inside the plant cells, Se is
mostly accumulated in their vacuoles (Ximénez-Embún et al.,
2004; Mazej et al., 2008) and can be effluxed through sulfate
transporters present in the tonoplast (Gigolashvili and Kopriva,
2014). The Fabaceae constitutes greatest number of Se species
known to hyperaccumulate Se.
Plants have been classified as hyperaccumulators, secondary-
accumulators, and non-accumulators depending upon Se
accumulation inside their cells (Galeas et al., 2007; Bodnar et al.,
2012;Figure 3). Hyperaccumulators accumulate higher amounts
of Se in their cells i.e., >1000 mgSe/Kg DW and thrive well in
Se rich regions of the world. They have methylated forms of
SeCys and SeMet, which confer Se tolerance of these plants,
and can be vaporized further as dimethyldiselenide (DMDSe).
Hyperaccumulators include Stanleya,Astragalus species,
Conopsis,Neptunia,Xylorhiza etc. Secondary-accumulators
accumulate Se and show no signs of toxicity upto 100–
1000 mgSe/Kg DW, for e.g., Brassica juncea,Brassica napus,
Broccoli, Helianthus,Aster,Camelina,Medicago sativa etc.
Non-accumulators are those plants which accumulate less
than 100 mgSe/Kg of their DW, and if they grow on Se-rich
soils they can’t survive, show retarded growth, volatilize Se as
dimethylselenide (DMSe) for e.g., grasses and crops (Galeas et al.,
2007; Bodnar et al., 2012). When non-accumulators are enriched
with Se, it is sequestered quickly in vacuoles of mesophyll cells
of leaves (Ximénez-Embún et al., 2004; Mazej et al., 2008).
Selenium content in common Se-enriched crops and cereals after
fortification with different concentrations of Se have been given
in Table 1.
SELENIUM METABOLISM IN PLANTS
As Se is chemically similar to S, it competes with S and is
transported inside the plant through sulfate transporters present
in root plasma membrane (Sors et al., 2005; Li et al., 2008). After
entry into plant, it is translocated to leaves and metabolized in
plastids via sulfur assimilation pathway to SeCys or s SeMet.
Sulfur analog of Se can be further methylated and vaporized into
atmosphere in a non toxic form Pilon-Smits and Quinn (2010)
(Figure 4).
First step in Se assimilation is conversion of inorganic Se to
selenite. It requires the sequential action of two enzymes known
as ATP sulfurylase (APS) and APS reductase (APR). APS catalyzes
the hydrolysis of ATP to form adenosine phosphoselenate,
which is further, reduced to selenite by APR (Sors et al.,
2005). Selenite is then converted to selenide by enzyme sulfite
reductase. In plants, this step can also be reduced by glutathione
or glutaredoxins (Wallenberg et al., 2010). Selenide is then
converted to SeCys by coupling with O-Acetyl serine (OAS) in
the presence of an enzyme cysteine synthase. Cysteine-synthase
has greater affinity for selenide as compared to sulfide. Depending
upon plant species and environmental conditions SeCys can
then be converted to elemental Se in the presence of enzyme
SeCys lyase or can be methylated to methyl-SeCys (Me-SeCys)
by selenocysteine methyltransferase or can be converted to
selenomethionine (SeMet) by a series of enzymes.
Misincorporation of SeCys or SeMet in proteins leads to
disruption of structure and function of protein, and cause Se
toxicity in plants (Pilon-Smits and Quinn, 2010). SeMet can be
used to form selenoproteins or methylated to form methyl-SeMet
(Me-SeMet). Me-SeCys or Me-SeMet can be further volatilized
into atmosphere as non-toxic dimethylselenide (DMSe) in
non-hyperaccumulators or dimethyldiselenide (DMDSe) in
hyperaccumulators (Pilon-Smits and Quinn, 2010;Figure 4)
SELENIUM SPECIATION IN PLANTS
Brassica juncea is a secondary Se accumulator which shows
varied pattern of Se accumulation depending upon the type
of Se specie absorbed. Uptake kinetics proved that selenate is
more efficient than any other Se species. In SeMet enriched
Brassica plants, Se-MeSeCys (Selenomethylselenocysteine) is
Frontiers in Plant Science | www.frontiersin.org 4January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
FIGURE 3 | Classification of plants depending upon Se accumulation as hyperaccumulators, Secondary accumulators and non-accumulators.
TABLE 1 | Common Se-enriched crops, cereals after fortification with different concentrations of Se.
SNo.Crops, vegetables, Se-enriched plant part Se used for biofortification Se accumulated References
fruits studied (mg/kg or mg/L) (mg/kg)
1 Rice Grain 2.850 mg/kg 1.3–3.3 Sharma et al., 2014
2 Chick Pea Sprouts 50 mg/L 1.134 Zhang et al., 2012
3 Sorghum Seeds 75 mg/L 2.1 Djanaguiraman et al., 2010
4 Soyabean Bean 130 mg/kg 75 Chan et al., 2010
5 Barley Grain 0.20 mg/kg 0.047 Yan et al., 2011
6 Kale Sprouts 60 mg/L 155 Thosaikham et al., 2014
7 Broccoli Sprouts 60 mg/L 467 Thosaikham et al., 2014
8 Pear Fruit 1 mg/L 0.199 Pezzarossa et al., 2012
9 Lettuce Shoots below 2.8 mg/L 43 Hawrylak-Nowaka, 2013
the predominant Se accumulating specie followed by Se-
Homocysteine and Se-Cystathionine. In selenate enriched
Brassica plants, ion-pairing LC-ICP-MS was used to detect Se-
speciation in which shoot extracts mostly consisted selenate,
Se-MeSeCys and SeMet whereas, root extracts consisted
selenate, selenite and SeMet. In selenite enriched plants,
shoot extracts consisted of SeMetSeOxide hydrates as the
predominant organic metabolite followed by selenite and SeMet
whereas, root extracts showed the presence of SeMet and
Se-MeSeCys. GC-MS technique confirmed the presence of
volatilized DMSe and DMDSe in Brassica seedlings (Dumont
et al., 2006).
In Oryza sativa accumulation of Se is mostly found to
be in organic form i.e., SeMet followed by Se-MeSeCys and
SeCys (Carey et al., 2012). Studies showed that in rice grain,
Se is mostly concentrated in bran and is almost twice the
levels of Se found in polished grain. The content of Se in rice
decreased in the following trend: straw>bran>wholegrain >
polished rice >husk (Sun H.-W. et al., 2010). In garlic,
the most predominant form of Se is Se-MeSeCys, which
accounts for most of the anticarcinogenic properties of garlic,
followed by SeMet and SeCys. In onions also, Se-MeSeCys
is the major form of Se speciation (Zhu et al., 2009). In
Broccoli, Se-MeSeCys, selenate, selenite are the major forms
of Se (Wu et al., 2015), whereas in mushrooms SeMet is
the most accumulated form of Se (Dumont et al., 2006).
In Astragalus bisulcatus plants, Se-MeSeCys is the main Se
compound, whereas in seeds γ–glu–Se-MeSeCys (γ–glutamyl
selnomethylselenocysteine) is the most predominant form. In
Brazil nuts, SeMet is the most occurring Se compound (Dumont
et al., 2006; Zhu et al., 2009). In grains such as wheat,
rye, and barley SeMet is the most dominant Se compound
(Stadlober et al., 2001; Poblaciones et al., 2014). Selenium
hyperaccumulator Stanleya pinnata accumulated up to 90%
of the total Se as Me-SeCys in plant tissues (Freeman et al.,
2006).
Frontiers in Plant Science | www.frontiersin.org 5January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
FIGURE 4 | Schematic representation of Se metabolism inside plant cells. Selenate is transported inside the plant through sulfate transporters present in
plasma membrane of roots. It is then transported to leaf through xylem. Selenate is then assimilated to DMSe and DMDSe by a series of sulfur metabolic enzymes.
APS, ATP sulfurylase; APR, APS reductase; CS, Cysteine synthase; SL, Selenocysteine lyase; SMT, Selenocysteine methyl transferase; A, Accumulation; T, tolerance.
BENEFICIAL EFFECTS OF SELENIUM IN
PLANTS
Although essentiality of Se to plants is in dilemma however,
many workers have reported beneficial effect of Se in
different plants (Cartes et al., 2010; Hasanuzzaman and
Fujita, 2011; Pandey and Gupta, 2015). Brief outline of
various role of Se in plants is described in pictorial form
in Figure 5. All of the below mentioned roles of Se are
interrelated to each other and contribute to overall growth
and development of plant under stress and non-stressed
conditions.
Studies have shown that Se at low doses protect the plants
from variety of abiotic stresses such as cold (Chu et al., 2010),
drought (Hasanuzzaman and Fujita, 2011), desiccation (Pukacka
et al., 2011), and metal stress (Kumar et al., 2012; Pandey and
Gupta, 2015). Under stress conditions, reactive oxygen species
are produced in plants which disrupt cell membranes, proteins
etc. Cartes et al. (2010) reported reduction in Al toxicity in rye
grass by Se mediated dismutation of superoxide radical to H2O2.
Kumar et al. (2012) reported reduction in ROS accumulation
in Cd-stressed marine algae after application of 50 µM Se
and Cd stressed Brassica seedlings after application of 2 µM
Se (Filek et al., 2008). Similarly, decreased ROS accumulation
was also reported in heat stressed Sorghum (Djanaguiraman
et al., 2010), and As-stressed mungbean (Malik et al., 2012).
However, at high doses, Se acts as pro-oxidant and causes
oxidative stress in plants, for e.g., in Pb stressed roots of Vicia
faba 1.5 µM Se decreased ROS but 6 µM increased ROS
accumulation and decreased cell viability (Mroczek-Zdyrska and
Wójcik, 2012). Filek et al. (2010) reported positive effect of 2
µM Se in maintaining the structure and fluidity of chloroplast
Frontiers in Plant Science | www.frontiersin.org 6January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
FIGURE 5 | Brief outline of beneficial effects of Se in plants.
membrane in Cd-stressed rape seedlings. Similar effect of low
dose of Se on plastid membranes was also reported in Cd-stressed
wheat seedlings (Filek et al., 2009), which could be attributed
to reactivation of membrane enzymes or transportation of
metabolites in chloroplast upon Se application. Se-mediated
reduction in electrolytic leakage and improved cell integrity was
also observed by many workers under various stress conditions
(Zembala et al., 2010; Pukacka et al., 2011; Malik et al., 2012).
Djanaguiraman et al. (2010) reported positive effect of low dose
of Se on photosynthesis in Sorghum, which could be due to
decreased ROS levels and increased antioxidant activity upon
Se application. Similarly, Wang et al. (2012) found increased
photosynthesis in rice seedlings at low doses but reported
disrupted photosynthetic apparatus and photosynthesis at high
dose of Se. Studies have reported beneficial role of Se in
protecting the plants from heavy metal toxicity, which could
be attributed to Se mediated detoxification of heavy metals
due to less uptake, translocation or formation of non toxic
Se-metal complexes (Belzile et al., 2006; Filek et al., 2008;
Pedrero et al., 2008; Sun G.-X. et al., 2010; Zembala et al., 2010;
Feng et al., 2011). Contrary to inhibited heavy metal uptake,
active role of Se has been reported in Fe uptake (Feng R. W.
et al., 2009; Feng and Wei, 2012), and could be considered as
one of the Se mediated mechanism to reduce metal toxicity
in plants, as Fe is an important constituent of chloroplast
and photosynthetic electron transport chain (He et al., 2004).
Apart from above mentioned roles, Se has been reported to
delay senescence (Xue et al., 2001), increased yield in Cucerbita
pepo (Germ et al., 2005), increased nutritive value of potato
(Turakainen et al., 2006), increased respiratory potential in Pisum
sativum (Smrkolj et al., 2006), chicory (Germ et al., 2007a) and
Eruca sativa (Germ and Osvald, 2005), protecting the plants
from pathogens, insects and herbivores (Freeman et al., 2006;
Quinn et al., 2010).
SELENIUM TOXICITY IN PLANTS
Selenosis or Se toxicity occurs in plants when optimum
concentration of Se exceeds. Selenium causes toxicity by two
mechanisms, one of which is malformed selenoproteins and
another by inducing oxidative stress. Both the mechanisms are
known to be harmful for plants in one or other way.
Toxicity due to Malformed Selenoproteins
Malformed selenoproteins are formed due to the
misincorporation of SeCys/SeMet in place of Cys/Met in
protein chain. As compared to SeMet, substitution of SeCys
is more reactive and detrimental to protein functioning. In
a protein chain, cysteine residues play an important role in
protein structure and function, and helps in formation of
disulfide bridges, enzyme catalysis, and metal binding site.
Hence, replacement of cysteine with SeCys is detrimental to
protein structure and function as SeCys is larger, reactive and
more easily deprotonated than cysteine (Hondal et al., 2012), as
seen in case of methionine sulfoxide reductase function that got
impaired after substitution with SeCys (Châtelain et al., 2013).
SeCys substitution distorts tertiary structure of protein due to
larger diselenide bridge formation and altered redox potential
Frontiers in Plant Science | www.frontiersin.org 7January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
affect enzyme kinetics (Hondal et al., 2012). Fe-S cluster proteins
of chloroplast and mitochondrial electron transport chain (Balk
and Pilon, 2011) are prone to SeCys substitution for example
as in case of chloroplast NifS-like protein (Pilon-Smits et al.,
2002). Fe-Se cluster are larger in size and does not fit properly
in apoproteins. Nitrogenase activity of Klebsiella pneumonia
decreased five-fold after replacement of Fe-S cluster with Fe-Se
(Hallenbeck et al., 2009). However, in another study substitution
reaction proved to be beneficial for glutathione dependent
peroxidase in Citrus sinensis (Hazebrouck et al., 2000). Several
studies have shown that diversion of selenocysteine from protein
synthesis is associated with enhanced Se tolerance in plants for
e.g., overexpression of SeCys-methyltransferase in Arabidopsis
and Brassica juncea (LeDuc et al., 2004), Cystathionine gamma-
synthase, NifS-like protein with selenocysteine lyase activity in
Brassica juncea (Van Huysen et al., 2003; Van Hoewyk et al.,
2005).
Se Toxicity due to Oxidative Stress
At high doses, Se acts as pro-oxidant and generates reactive
oxygen species which cause oxidative stress in plants. Generally,
under Se stress decreased level of glutathione is observed
(Hugouvieux et al., 2009), except in Se-tolerant plants where
elevated levels are observed (Grant et al., 2011). In another study
by Grant et al. (2011) on cad2-1 mutant plants having defective
glutathione synthetic pathway showed many folds decreased
root length as compared to wild type plants grown on 20 µM
selenate. In apr2-1 mutant of Arabidopsis, glutathione depletion
and ROS accumulation found to be interlinked to each other
under Se stress (Grant et al., 2011). Increased lipid peroxidation
was observed in wheat seedlings under Se stress (Łabanowska
et al., 2012). Several studies have reported increased activity
of antioxidant enzymes indicating ROS accumulation under Se
stress (Gomes-Junior et al., 2007; Chen et al., 2008; Akbulut and
Cakır, 2010; Schiavon et al., 2012). Tamaoki et al. (2008) found
higher accumulation of ROS in vtc1 mutant having defective
ascorbic acid biosynthetic pathway as compared to wild type
plants under Se stress. In another study, Se generated ROS
initiated defense mechanism against Se stress (De Pinto et al.,
2012). Previous studies reported that ROS accumulation under Se
stress increased lipid peroxidation, cell mortality in Arabidopsis
and Vicia faba (Lehotai et al., 2012; Mroczek-Zdyrska and
Wójcik, 2012). Apart from plant cells, Wallenberg et al. (2010)
reported generation of mitochondrial superoxide in human cells
under Se stress. Altogether, above studies indicate role of reactive
oxygen species in imparting Se toxicity in plants.
SELENIUM PHYTOREMEDIATION
Phytoremediation is a plant based technology, in which toxic
metals are removed from the soil by the roots of the plant.
Further, metals translocated to the upper parts of the plant
from where they can be easily removed by harvesting, or
volatilized into atmosphere in less toxic forms (Newman and
Reynolds, 2004). This method of cleaning up of soil is cheaper,
and it does not reduce the fertility of the soil like other
engineering methods (Robinson et al., 2000; Pilon-Smits and
Freeman, 2006). Due to natural and anthropogenic activities Se
pollution is increasing in certain regions of the world (Hamilton,
2004; Hira et al., 2004). Studies have shown increasing use of
plants to counteract Se pollution in the environment. Plants
volatilize the accumulated Se as DMSe and DMDSe, which
are almost 600 times less toxic than elemental Se (Dumont
et al., 2006). Apart from terrestrial plants (Kahakachchi et al.,
2004), macrophytes such as muskgrass, Phragmites australis
(Shardendu et al., 2003), and Potamogeton crispus (Wu and
Guo, 2002) had been used to clean Se present in agricultural
drainage water (Lin et al., 2002). Brassica species have been
known to accumulate and volatilize Se (Bañuelos et al., 2005,
2007). Stanleya pinnata and Astragalus bisulcatus are well-
known Se-accumulators; however, slow growth rate and low
biomass production often limit their phytoremediation potential
(Germ et al., 2007b). In hyperaccumulators, Se is detoxified by
methylation of SeCys and SeMet to Me-SeCys and Me-SeMet
which are non-toxic and accumulated safely. Methylation occurs
in presence of enzyme selenocysteine methyltransferase (Pilon-
Smits and LeDuc, 2009).
Phytoremediation efficiency of plants has been enhanced
using genetic engineering (Eapen and D’Souza, 2005; Meagher
and Heaton, 2005;Figure 6). Overexpression of ATP sulfurylase
(APS1) of Arabidopsis thaliana in Brassica juncea increased
selenate reduction along with two- to three- fold increase in Se
accumulation in shoots and roots (Pilon-Smits and LeDuc, 2009).
Overexpression of mouse selenocysteine lyase in Arabidopsis
thaliana and B. juncea resulted in higher Se accumulation
and tolerance as compared to wild type plants (Garifullina
et al., 2003). Overexpression of cystathionine-γ-synthase of
Arabidopsis enhanced two- to three- folds Se volatilization in
B. juncea (Van Huysen et al., 2003). Double transgenic plants
obtained by expressing both APS and SMT gene showed 9 times
higher Se accumulation than wild type plants. All transgenic
plants showed promising traits of enhanced Se accumulation,
volatilization, and tolerance which are needed for effective and
efficient phytoremediation of Se.
SELENIUM BIOFORTIFICATION
Although phytoremediation is an efficient method of cleaning
up of soil from Se, but the problem still exists regarding the
disposal of the contaminated plant material which could be toxic
to human and animal survival if left as such. Biofortification is
an alternative method to dispose-off these waste plant material
(Liu et al., 2011; Lin et al., 2014). In this strategy, Se enriched
plant material will be decomposed in agricultural soil which can
be used further for the enrichment of food products with Se
(Bañuelos et al., 2015). Hence, biofortification is a practice of
enriching the agricultural food products with certain nutrients,
for example Se, to increase the dietary intake through plant
breeding, genetic engineering and manipulation of agronomic
practices (Zhu et al., 2009; Kieliszek and Blazejak, 2012; Borrill
et al., 2014). Biofortification is an economical safe agricultural
technique, which aims to cope up with deficiency of a particular
nutrient in diet, and increase the content of a micronutrient for
e.g., Se in edible portion of plant (Nestel et al., 2006; Mayer
Frontiers in Plant Science | www.frontiersin.org 8January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
FIGURE 6 | Transgenic approach to improve Se-phytoremediation and biofortification. Overexpression of ST, APS, APR, Cys–γ–synthase, SMT genes have
shown enhanced Se accumulation and tolerance in different plants hence this technique can be used for Se phytoremediation and biofortification in Se-toxic and
Se-deficient regions, respectively. ST, sulfur transporter; APS, ATP sulfurylase; APR, APS reductase; Cys–γ–synthase, Cystathionine–γ–synthase; SMT,
Selenocysteine methyl transferase.
BOX 2 | Transgenic approach.
Selenium metabolism inside the plants can be manipulated using transgenic approach for effective Se-phytoremediation or biofortification. Prime focus should
be to:
• Increase plant tolerance of high soil Se concentration.
• Increase Se uptake and transport to shoot.
• Increase Se accumulation in shoot tissues.
• Increase Se volatilization.
et al., 2008; Zhao and McGrath, 2009). Selenium biofortification
substantially increases Se contents of agricultural food products,
and can help in alleviation of Se malnutrition to which more
than 1 billion people all over the world is suffering (WHO,
2009). Researchers round the world are trying to develop
Se-enriched food products to minimize Se related deficiency
disorders. Selenium fertilization also affects the synthesis of
amino acids, protein and phenolics compounds. Selenium-
biofortified tomato fruit has been reported to have high contents
of flavonoids and leaf phenolic contents (Schiavon et al., 2013).
Selenium biofortification affects the synthesis of glucosinolates
(GLS), S-secondary compounds, which on hydrolysis produce
isothiocyanates having anticancerous properties (Dinkova-
Kostova, 2013). Brassica species are rich source of GLS (Robbins
et al., 2005; Barickman et al., 2013), however, high levels GLS may
be toxic to humans and animals (Tripathi and Mishra, 2007). As
different plants have different Se accumulation capacity (Galeas
et al., 2007), hence, to produce Se-biofortified food products it is
very important to select those plant species that can moderately
accumulate Se in their edible parts for e.g., Se levels in different
plants are of following order: brassica >bean >cereal (Liu
et al., 2011). The rice cultivars Jinlong No.1 and Longquin No.4,
accumulate more Se than ordinary normal rice, and are naturally
Se enriched. These cultivars are being cultivated on large scale in
Frontiers in Plant Science | www.frontiersin.org 9January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
Se deficient regions of China (Yang et al., 2007; Yin and Yuan,
2012; Wang J. W. et al., 2013).
Foliar application of Se is better and efficient means of Se-
biofortification than application of Se fertilizers in soil, due to
avoidance of root to shoot translocation of Se (Winkel et al.,
2015). Use of Se fertilizers in soil have low rates of Se enrichment
in edible part of plant, moreover, long term use can be toxic
to nearby ecosystem, hence use of Se fertilizers should be done
carefully to avoid toxic aspects (Winkel et al., 2015). In Finland
and New Zealand, use of inorganic Se fertilizers is a common
practice to increase Se content in agricultural products (Schiavon
et al., 2013; Wang Y. D. et al., 2013). Implementation efficiency
of Se fertilizers for Se-biofortification strategy can be increased
by the use of organic acids (Morgan et al., 2005; Lynch, 2007),
organic forms of Se (Schiavon et al., 2013; Pezzarossa et al.,
2014), or microbes (Duran et al., 2013, 2014) which enhance the
chances of Se availability to plants. Genetic engineering is another
useful strategy to obtain Se-biofortified food products, which
generally focuses on manipulation of Se-related enzymes for Se
uptake, assimilation and volatilization (Figure 6,Box 2). Brassica
juncea plants over-expressed with Astragalus bisulcatus SMT gene
(selenocysteine methyltransferase) and Arabidopsis thaliana ATP
sulfurylase gene showed significantly improved Se accumulation
and tolerance than wild type plants (LeDuc et al., 2004, 2006).
Wheat is the most efficient accumulator of Se within the
common cereal crops (wheat>rice>maize>barley>oats) and in
cereals SeMet is the dominant organic form of Se (Stadlober
et al., 2001; Poblaciones et al., 2014). Wheat is also one of the
most important sources of dietary Se for human population
in UK (Lyons, 2010). Thus, wheat is an obvious target crop
for agronomic biofortification to increase the dietary Se intake,
and thus the Se status of UK population. Studies conducted
by Cubadda et al. (2010) showed that wheat collected from
seleniferous belt of Nawanshahr-Hoshiarpur region in Punjab
(India), have high concentrations of Se ranging from 29 to 185
µg/g. The regular consumption of such wheat can produce Se
toxicity, but can be used as Se supplement in diet in low Se areas.
Rice, being the staple food crop for more than half of world’s
population, is an important source of Se especially for inhabitants
of China who depend on it for their nutritional requirements
(Chen et al., 2002; Hu et al., 2002). China stands high as Se rich
country (ranked fourth) however, Se deficiency is also observed in
certain regions, for instance Heilongjiang and Yunnan Province
where Se-fortified wheat, rice, and vegetables are the primary
source of Se in diet (Zhu et al., 2009; Liu et al., 2011). Significant
increase in Se content of rice grains have been reported by foliar
applications of Se-enriched fertilizers (Pezzarossa et al., 2012;
Boldrin et al., 2013). High content of Se ranging between 15
and 270 µg/kg DW was observed in legumes in Spain (Matos-
Reyes et al., 2010). Peas are the best candidate among legumes
to carry out Se biofortification under Mediterranean conditions
(Poblaciones et al., 2012).
FUTURE PROSPECTS
In this review, we have addressed the basic mechanism of
uptake, metabolism, and toxicity of Se in plants including
phytoremediation and biofortification aspects. But still there are
many faces of Se which needs to be uncovered. The beneficial
effect of Se at low doses also mentioned, however, the exact
mechanism behind the effect is still untouched. We also need
to explore in detail how S and Se biochemistry are interlinked,
and influence each other during Se uptake. Focus on enzyme
kinetics of various steps of S assimilatory pathway at different
concentrations of Se, also need to be explored. In addition, how
different plants have different Se tolerance and detoxification
mechanisms, and exploitation of these mechanisms to improve
phytoremediation and biofortification of Se, also needs to be
uncovered by integrating both the approaches. Furthermore,
product of phytoremediation can become raw material for
biofortification purposes, hence, it is very important to screen
Se-hyperaccumulator plants and those plant species that can
accumulate Se in edible parts within the safer limits for human
consumption.
AUTHOR CONTRIBUTIONS
MG planned, drafted and checked the manuscript. SG designed,
wrote and executed the manuscript.
ACKNOWLEDGMENTS
SG thanks Council of Scientific and Industrial Research (CSIR),
New Delhi, India for fellowship.
REFERENCES
Akbulut, M., and Cakır, S. (2010). The effects of Se phytotoxicity on the antioxidant
systems of leaf tissues in barley (Hordeum vulgare L.) seedlings. Plant Physiol.
Biochem. 48, 160–166. doi: 10.1016/j.plaphy.2009.11.001
Bajaj, M., Eiche, E., Neumann, T., Winter, J., and Gallert, C. (2011). Hazardous
concentrations of selenium in soil and groundwater in North-West India. J.
Hazard. Mater. 189, 640–646. doi: 10.1016/j.jhazmat.2011.01.086
Balk, J., and Pilon, M. (2011). Ancient and essential: the assembly of iron-sulfur
clusters in plants. Trends Plant Sci. 16, 18–26. doi: 10.1016/j.tplants.2010.12.006
Bañuelos, G., LeDuc, D. L., Pilon-Smits, E. A., and Terry, N. (2007). Transgenic
Indian mustard overexpressing selenocysteine lyase or selenocysteine
methyltransferase exhibit enhanced potential for selenium phytoremediation
under field conditions. Environ. Sci. Technol. 41, 599–605.
Bañuelos, G., Terry, N., LeDuc, D. L., Pilon-Smits, E. A., and Mackey, B.
(2005). Field trial of transgenic Indian mustard plants shows enhanced
phytoremediation of selenium-contaminated sediment. Environ. Sci. Technol.
39, 1771–1777.
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
Barickman, T. C., Kopsell, D. A., and Sams, C. E. (2013). Selenium influences
glucosinolate and isothiocyanates and increases sulfur uptake in Arabidopsis
thaliana and rapid-cycling Brassica oleracea.J. Agric. Food Chem. 61, 202–209.
doi: 10.1021/jf3037227
Behne, D., and Kyriakopoulos, A. (2001). Mammalian selenium-containing
proteins. Annu. Rev. Nutr. 21, 453–473. doi: 10.1146/annurev.nutr.21.1.453
Frontiers in Plant Science | www.frontiersin.org 10 January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
Belzile, N., Wu, G. J., Chen, Y. M., and Appanna, V. D. (2006). Detoxification of
selenite and mercury by reduction and mutual protection in the assimilation
of both elements by Pseudomonas fluorescens.Sci. Total Environ. 367, 704–714.
doi: 10.1016/j.scitotenv.2006.03.008
Bodnar, M., Konieczka, P., and Namiesnik, J. (2012). The properties, functions, and
use of selenium compounds in living organisms. J. Environ. Sci. Health Part C
30, 225–252. doi: 10.1080/10590501.2012.705164
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 Comp. 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
Cappa, J. J., Cappa, P. J., El Mehdawi, A. F., McAleer, J. M., Simmons,
M. P., and Pilon-Smits, E. A. (2014). Characterization of selenium
and sulfur accumulation across the genus Stanleya (Brassicaceae): a
field survey and common-garden experiment. Am. J. Bot. 101, 830–839.
doi: 10.3732/ajb.1400041
Carey, A. M., Scheckel, K. G., Lombi, E., Newville, M., Choi, Y., Norton, G. J.,
et al. (2012). Grain accumulation of selenium species in rice (Oryza sativa L.).
Environ. Sci. Technol. 46, 5557–5564. doi: 10.1021/es203871j
Cartes, P., Jara, A. A., Pinilla, L., Rosas, A., and Mora, M. L. (2010).
Selenium improves the antioxidant ability against aluminium-induced
oxidative stress in ryegrass roots. Ann. Appl. Biol. 156, 297–307.
doi: 10.1111/j.1744-7348.2010.00387.x
Chan, Q., Afton, S. E., and Caruso, J. A. (2010). Selenium speciation profiles
in selenite-enriched soybean (Glycine Max) by HPLC-ICPMS and ESI-ITMS.
Metallomics 2, 147–153. doi: 10.1039/B916194E
Châtelain, E., Satour, P., Laugier, E., Ly Vu, B., Payet, N., Rey, P., et al.
(2013). Evidence for participation of the methionine sulfoxide reductase repair
system in plant seed longevity. Proc. Natl. Acad. Sci. U.S.A. 110, 3633–3638.
doi: 10.1073/pnas.1220589110
Chen, L., Yang, F., Xu, J., Hu, Y., Hu, Q., Zhang, Y., et al. (2002). Determination
of selenium concentration of rice in China and effect of fertilisation of selenite
and selenate on selenium content of rice. J. Agric. Food Chem. 50, 5128–5130.
doi: 10.1021/jf0201374
Chen, T. F., Zheng, W. J., Wong, Y. S., and Yang, F. (2008). Selenium-
induced changes in activities of antioxidant enzymes and content of
photosynthetic pigments in Spirulina platensis.J. Integr. Plant Biol. 50, 40–48.
doi: 10.1111/j.1744-7909.2007.00600.x
Chu, J., Yao, X., and Zhang, Z. (2010). Responses of wheat seedlings to exogenous
selenium supply under cold stress. Biol. Trace Elem. Res. 136, 355–363.
doi: 10.1007/s12011-009-8542-3
Cubadda, F., Aureli, F., Ciardullo, S., D’Amato, M., Raggi, A., Acharya, R.,
et al. (2010). Changes in selenium speciation associated with increasing tissue
concentrations of selenium in wheat grain. J. Agri. Food Chem. 58, 2295–2301.
doi: 10.1021/jf903004a
De Pinto, M. C., Locato, V., and De Gara, L. (2012). Redox regulation
in plant programmed cell death. Plant Cell Environ. 35, 234–244.
doi: 10.1111/j.1365-3040.2011.02387.x
Dinkova-Kostova, A. T. (2013). Chemoprotection against cancer by isothio-
cyanates: a focus on the animal models and the protective mechanisms. Top.
Curr. Chem. 329, 179–201. doi: 10.1007/128_2012_337
Djanaguiraman, M., Prasad, P. V., and Seppanen, M. (2010). Selenium protects
sorghum leaves from oxidative damage under high temperature stress by
enhancing antioxidant defense system. Plant Physiol. Biochem. 48, 999–1007.
doi: 10.1016/j.plaphy.2010.09.009
Dumont, E., Vanhaecke, F., and Cornelis, R. (2006). Selenium speciation from food
source to metabolites: a critical review. Anal. Bioanal. Chem. 385, 1304–1323.
doi: 10.1007/s00216-006-0529-8
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 pro-motion, biofortification and Gaeumannomyces
graminis biocontrol in wheat production. Biol. Fertil. Soils 50, 983–990.
doi: 10.1007/s00374-014-0920-0
Eapen, S., and D’Souza, S. F. (2005). Prospects of genetic engineering of
plants for phytoremediation of toxic metals. Biotechnol. Adv. 23, 97–114.
doi: 10.1016/j.biotechadv.2004.10.001
El Kassis, E., Cathala, E., Rouached, H., Fourcroy, P., Berthomieu, P., Terry, N.,
et al. (2007). Characterization of a selenate-resistant Arabidopsis mutant. Root
growth as a potential target for selenate toxicity. Plant Physiol. 143, 1231–1241.
doi: 10.1104/pp.106.091462
Ellis, D. R., and Salt, D. E. (2003). Plants, selenium, and human health. Curr. Opin.
Plant Biol. 6, 273–279. doi: 10.1016/S1369-5266(03)00030-X
Feist, L. J., and Parker, D. R. (2001). Ecotypic variation in selenium
accumulation among populations of Stanleya pinnata.New Phytol. 149, 61–69.
doi: 10.1046/j.1469-8137.2001.00004.x
Feng, C. X., Liu, J. J., Liu, S., Hu, R. Z., and Chi, G. X. (2009). Petrogenesis
and sedimentary environment of the cherts from Yutangba, Western
Hubei province: evidence from silicon, oxygen, carbon and sulfur isotopic
compositions. Acta Petrol. Sin. 25, 1253–1259.
Feng, R. W., and Wei, C. Y. (2012). Antioxidative mechanisms on selenium
accumulation in Pteris vittata L., a potential selenium phytoremediation plant.
Plant Soil Environ. 58, 105–110.
Feng, R. W., Wei, C. Y., Tu, S. X., Tang, S. R., and Wu, F. C. (2011). Detoxification
of antimony by selenium and their interaction in paddy rice under hydroponic
conditions. Microchem. J. 97, 57–61. doi: 10.1016/j.microc.2010.06.003
Feng, R. W., Wei, C. Y., Tu, S. X., and Wu, F. C. (2009). Effects of Se on
the essential elements uptake in Pteris vittata L. Plant Soil 325, 123–132.
doi: 10.1007/s11104-009-9961-9
Filek, M., Gzyl-Malcher, B., Zembala, M., Bednarska, E., Laggner, P.,
and Kriechbaum, M. (2010). Effect of selenium on characteristics of
rape chloroplasts modified by cadmium. J. Plant Physiol. 167, 28–33.
doi: 10.1016/j.jplph.2009.07.003
Filek, M., Keskinen, R., Hartikainen, H., Szarejko, I., Janiak, A., Miszalski, Z., et al.
(2008). The protective role of selenium in rape seedlings subjected to cadmium
stress. J. Plant Physiol. 165, 833–844. doi: 10.1016/j.jplph.2007.06.006
Filek, M., Zembala, M., Hartikainen, H., Miszalski, Z., Kornas, A., Wietecka-
Posłuszny, R., et al. (2009). Changes in wheat plastid membrane
properties induced by cadmium and selenium in presence/absence of 2,
4-dichlorophenoxyacetic acid. Plant Cell Tissue Organ. Cult. 96, 19–28.
doi: 10.1007/s11240-008-9455-0
Fordyce, F. M., Guangdib, Z., Greena, K., and Xinping, K. (2000).
Soil, grain and water chemistry in relation to human selenium-
responsive diseases in Enshi district, China. Appl. Geochem. 15, 117–132.
doi: 10.1016/S0883-2927(99)00035-9
Fordyce, F., Selinus, O., Alloway, B., Centeno, J., Finkelman, R., Fuge, R., et al.
(2005). “Essentials of medical geology,” in Selenium Deficiency and Toxicity in
the Environment, ed F. Fordyce (Edinburgh: Elsevier), 373–415.
Freeman, J. L., Quinn, C. F., Marcus, M. A., Fakra, S., and Pilon-Smits, E. A.
(2006). Selenium-tolerant diamondback moth disarms hyperaccumulator plant
defense. Current Biol. 16, 2181–2192. doi: 10.1016/j.cub.2006.09.015
Galeas, M. L., Zhang, L. H., Freeman, J. L., Wegner, M., and Pilon-Smits, E. A. H.
(2007). Seasonal fluctuations of selenium and sulfur accumulation in selenium-
hyperaccumulators and related non-accumulators. New Phytol. 173, 517–525.
doi: 10.1111/j.1469-8137.2006.01943.x
Garifullina, G. F., Owen, J. D., Lindblom, S. D., Tufan, H., Pilon, M., and Pilon-
Smits, E. A. H. (2003). Expression of a mouse selenocysteine lyase in Brassica
juncea chloroplasts affects selenium tolerance and accumulation. Plant Physiol.
118, 538–544. doi: 10.1034/j.1399-3054.2003.00136.x
Germ, M., Kreft, I., and Osvald, J. (2005). Influence of UV-B exclusion and
selenium treatment on photochemical efficiency of photosystem II, yield and
respiratory potential in pumpkins (Cucurbita pepo L.). Plant Physiol. Biochem.
43, 445–448. doi: 10.1016/j.plaphy.2005.03.004
Germ, M., and Osvald, J. (2005). Selenium treatment affected respiratory potential
in Eruca sativa.Acta Agric. Slov. 85, 329–335.
Germ, M., Stibilj, V., and Kreft, I. (2007b). Metabolic importance of selenium for
plants. Eur. J. Plant Sci. Biotechnol. 1, 91–97.
Germ, M., Stibilj, V., Osvald, J., and Kreft, I. (2007a). Effect of selenium foliar
application on chicory (Cichorium intybus L.). J. Agric. Food Chem. 55, 795–798.
doi: 10.1021/jf0629888
Frontiers in Plant Science | www.frontiersin.org 11 January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
Gigolashvili, T., and Kopriva, S. (2014). Transporters in plant sulphur metabolism.
Front. Plant Sci. 5:422. doi: 10.3389/fpls.2014.00442
Gomes-Junior, R. A., Gratão, P. L., Gaziola, S. A., Mazzafera, P., Lea, P. J.,
and Azevedo, R. A. (2007). Selenium-induced oxidative stress in coffee cell
suspension cultures. Funct. Plant Biol. 34, 449–456. doi: 10.1071/FP07010
Gore, F., Fawell, J., and Bartram, J. (2010). Too much or too little? A review of
conundrum of selenium. J. Water Health 8, 405–416. doi: 10.2166/wh.2009.060
Grant, K., Carey, N. M., Mendoza, M., Schulze, J., Pilon, M., Pilon-Smits, E. A.
H., et al. (2011). Adenosine 5-phosphosulfate reductase (APR2) mutation in
Arabidopsis implicates glutathione deficiency in selenate toxicity. Biochem. J.
438, 325–335. doi: 10.1042/BJ20110025
Hallenbeck, P. C., George, G. N., Prince, R. C., and Thorneley, R. N. (2009).
Characterization of a modified nitrogenase Fe protein from Klebsiella
pneumoniae in which the 4Fe4S cluster has been replaced by a 4Fe4Se cluster. J.
Biol. Inorg. Chem. 14, 673–682. doi: 10.1007/s00775-009-0480-1
Hamilton, S. J. (2004). Review of selenium toxicity in the aquatic food chain. Sci.
Total Environ. 326, 1–36. doi: 10.1016/j.scitotenv.2004.01.019
Harris, J., Schneberg, K. A., and Pilon-Smits, E. A. (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
Hartikainen, H. (2005). Biogeochemistry of selenium and its impact on food
chain quality and human health. J. Trace Elem. Med. Biol. 18, 309–318.
doi: 10.1016/j.jtemb.2005.02.009
Hasanuzzaman, M., and Fujita, M. (2011). Selenium pretreatment upregulates
the antioxidant defense and methylglyoxal detoxification system and confers
enhanced tolerance to drought stress in rapeseed seedlings. Biol. Trace Elem.
Res. 143, 1758–1776. doi: 10.1007/s12011-011-8998-9
Hasanuzzaman, M., Hossain, M. A., and Fujita, M. (2011). Selenium-induced up-
regulation of the antioxidant defense and methylglyoxal detoxification system
reduces salinity induced damage in rapeseed seedlings. Biol. Trace Elem. Res.
43, 1704–1721. doi: 10.1007/s12011-011-8958-4
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-Nowaka, B. (2013). Comparative effects of selenite and selenate on
growth and selenium accumulation in lettuce plants under hydroponic
condition. Plant Growth Regul. 70, 149–157. doi: 10.1007/s10725-013-9788-5
Hazebrouck, S., Camoin, L., Faltin, Z., Strosberg, A. D., and Eshdat, Y. (2000).
Substituting selenocysteine for catalytic cysteine 41 enhances enzymatic activity
of plant phospholipid hydroperoxide glutathione peroxidase expressed in
Escherichia coli.J. Biol. Chem. 275, 28715–28721. doi: 10.1074/jbc.M0049
85200
He, P. P., Lv, X. Z., and Wang, G. Y. (2004). Effects of Se and Zn supplementation
on the antagonism against Pb and Cd in vegetables. Environ. Int. 30, 167–172.
doi: 10.1016/S0160-4120(03)00167-3
Hira, C. K., Partal, K., and Dhillon, K. (2004). Dietary selenium intake by men and
women in high and low selenium areas of Punjab. Public Health Nutr. 7, 39–43.
doi: 10.1079/PHN2003513
Hondal, R. J., Marino, S. M., and Gladyshev, V. N. (2012). Selenocysteine in
thiol/disulfide-like exchange reactions. Antioxid. Redox Signal. 18, 1675–1689.
doi: 10.1089/ars.2012.5013
Hu, Q., Chen, L., Xu, J., Zhang, Y., and Pan, G. (2002). Determination of selenium
concentration in rice and the effect of foliar application of Se-enriched fertilizer
or sodium selenite on the selenium content of rice. J. Sci. Food Agric. 82,
869–872. doi: 10.1002/jsfa.1115
Hugouvieux, V., Dutilleul, C., Jourdain, A., Reynaud, F., Lopez, V., and
Bourguignon, J. (2009). Arabidopsis putative selenium-binding protein1
expression is tightly linked to cellular sulfur demand and can reduce sensitivity
to stresses requiring glutathione for tolerance. Plant Physiol. 151, 768–781.
doi: 10.1104/pp.109.144808
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/S0021-9673(04)01287-7
Kaur, N., Sharma, S., and Kaur, S. (2014). Selenium in agriculture: a
nutrient or contaminant for crops? Arch. Agron. Soil Sci. 60, 1593–1624.
doi: 10.1080/03650340.2014.918258
Kieliszek, M., and Blazejak, S. (2012). Selenium: significance and outlook for
supplementation. Nutrition 29, 713–718. doi: 10.1016/j.nut.2012.11.012
Kikkert, J., and Berkelaar, E. (2013). Plant uptake and translocation of inorganic
and organic forms of selenium. Arch. Environ.Contam. Toxicol. 65, 458–465.
doi: 10.1007/s00244-013-9926-0
Kumar, M., Bijo, A. J., Baghel, R. S., Reddy, C. R. K., and Jha, B. (2012). Selenium
and spermine alleviates cadmium induced toxicity in the red seaweed Gracilaria
dura by regulating antioxidant system and DNA methylation. Plant Physiol.
Biochem. 51, 129–138. doi: 10.1016/j.plaphy.2011.10.016
Łabanowska, M., Filek, M., Koscielniak, J., Kurdziel, M., Kulis, E., and Hartikainen,
H. (2012). The effects of short-term selenium stress on Polish and Finnish
wheat seedlings-EPR, enzymatic and fluorescence studies. J. Plant Physiol. 169,
275–284 doi: 10.1016/j.jplph.2011.10.012
LeDuc, D. L., AbdelSamie, M., Móntes-Bayon, M., Wu, C. P., Reisinger,
S. J., and Terry, N. (2006). Overexpressing both ATP sulfurylase and
selenocysteine methyltransferase enhances selenium phytoremediation traits
in Indian mustard. Environ. Pollut. 144, 70–76. doi: 10.1016/j.envpol.2006.
01.008
LeDuc, D. L., Tarun, A. S., Montes-Bayon, M., Meija, J., Malit, M. F., Wu, C. P.,
et al. (2004). Overexpression of selenocysteine methyltransferase in Arabidopsis
and Indian mustard increases selenium tolerance and accumulation. Plant
Physiol. 135, 377–383. doi: 10.1104/pp.103.026989
Lehotai, N., Kolbert, Z., Peto, A., Feigl, G., Ördög, A., Kumar, D., et al. (2012).
Selenite-induced hormonal and signaling mechanisms during root growth of
Arabidopsis thaliana L. J. Exp. Bot. 63, 5677–5687. doi: 10.1093/jxb/ers222
Lemire, M., Mergler, D., Huel, G., Passos, C. J. S., Fillion, M., Philibert, A., et al.
(2009). Biomarkers of selenium status in the amazonian context: blood, urine
and sequential hair segments. J. Expo. Sci. Environ. Epidemiol. 19, 213–222.
doi: 10.1038/jes.2008.14
Li, H. F., McGrath, S. P., and Zhao, F. J. (2008). Selenium uptake, translocation and
speciation in wheat supplied with selenate or selenite. New Phytol. 178, 92–102.
doi: 10.1111/j.1469-8137.2007.02343.x
Lin, Z. Q., de Souza, M., Pickering, I. J., and Terry, N. (2002). Evaluation of
the macroalga, muskgrass, for the phytoremediation of selenium-contaminated
agricultural drainage water by microcosms. J. Environ. Qual. 31, 2104–2110.
doi: 10.2134/jeq2002.2104
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.
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.
Lynch, J. P. (2007). Roots of the second green revolution. Aust. J. Bot. 55, 493–512.
doi: 10.1071/BT06118
Lyons, G. (2010). Selenium in cereals: improving the efficiency of agronomic
biofortification in the UK. Plant Soil. 332, 1–4. doi: 10.1007/s11104-010-0282-9
Malagoli, M., Schiavon, M., dall’Acqua, S., and Pilon-Smits, E. A. (2015). Effects
of selenium biofortification on crop nutritional quality. Front. Plant Sci. 6:280.
doi: 10.3389/fpls.2015.00280
Malik, J. A., Goel, S., Kaur, N., Sharma, S., Singh, I., and Nayyar, H.
(2012). Selenium antagonizes the toxic effects of arsenic on mungbean
(Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the
antioxidative and detoxification mechanisms. Environ. Exp. Bot. 77, 242–248.
doi: 10.1016/j.envexpbot.2011.12.001
Matos-Reyes, M. N., Cervera, M. L., Campos, R. C., and de la Guardia,
M. (2010). Total content of As, Sb, Se, Te and Bi in Spanish vegetables,
cereals and pulses and estimation of the contribution of these foods to the
Mediterranean daily intake of trace elements. Food Chem. 122, 188–194.
doi: 10.1016/j.foodchem.2010.02.052
Mayer, J. E., Pfeiffer, W. H., and Beyer, P. (2008). Biofortified crops to
alleviate micronutrient malnutrition. Curr. Opin. Plant Biol. 11, 166–170.
doi: 10.1016/j.pbi.2008.01.007
Mazej, D., Osvald, J., and Stibilj, V. (2008). Selenium species in leaves of
chicory, dandelion, lamb’s lettuce and parsley. Food Chem. 107, 75–83.
doi: 10.1016/j.foodchem.2007.07.036
Frontiers in Plant Science | www.frontiersin.org 12 January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
Meagher, R. B., and Heaton, A. C. P. (2005). Strategies for the engineered
phytoremediation of toxic element pollution: mercury and arsenic.
J. Ind. Microbiol. Biotechnol. 32, 502–513. doi: 10.1007/s10295-005-
0255-9
Mehdi, Y., Hornick, J. L., Istasse, L., and Dufrasne, I. (2013). Selenium in the
environment, metabolism and involvement in body functions. Molecules 18,
3292–3311. doi: 10.3390/molecules18033292
Méplan, C. (2011). Trace elements and ageing, a genomic perspective
using selenium as an example. J. Trace Elem. Med. Biol. 25, S11–S16.
doi: 10.1016/j.jtemb. 2010.10.002
Missana, T., Alonso, U., and García-Gutiérrez„ M. (2009). Experimental study and
modeling of selenite sorption onto illite and smectite clays. J. Colloid Interface
Sci. 334, 132–138. doi: 10.1016/j.jcis.2009.02.059
Morgan, J. A., Bending, G. D., and White, P. J. (2005). Biological costs and benefits
to plant-microbe interactions in the rhizosphere. J. Exp. Bot. 56, 1729–1739.
doi: 10.1093/jxb/eri205
Mroczek-Zdyrska, M., and Wójcik, M. (2012). The influence of selenium on root
growth and oxidative stress induced by lead in Vicia faba L. minor plants. Biol.
Trace Elem. Res. 147, 320–328. doi: 10.1007/s12011-011-9292-6
NAS (1976). Selenium. Washington, DC: National Academy of Sciences.
NAS (1977). Drinking Water and Health. Washington, DC: National Academy of
Sciences.
Nestel, P., Bouis, H. E., Meenakshi, J. V., and Pfeiffer, W. (2006). Biofortification of
staple food crops. J. Nutr. 136, 1064–1067
Newman, L. A., and Reynolds, C. M. (2004). Phytodegradation
of organic compounds. Curr. Opin. Biotechnol. 15, 225–230.
doi: 10.1016/j.copbio.2004.04.006
Pandey, C., and Gupta, M. (2015). Selenium and auxin mitigates arsenic
stress in rice (Oryza sativa L.) by combining the role of stress indicators,
modulators and genotoxicity assays. J. Hazard. Mater. 287, 384–391.
doi: 10.1016/j.jhazmat.2015.01.044
Pedrero, Z., Madrid, Y., Hartikainen, H., and Cámara, C. (2008). Protective
effect of selenium in broccoli (Brassica oleracea) plants subjected to cadmium
exposure. J. Agric. Food Chem. 56, 266–271. doi: 10.1021/jf072266w
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 Freeman, J. L. (2006). Environmental cleanup using
plants: biotechnological advances and ecological considerations. Front. Ecol.
Environ. 4, 203–210. doi: 10.1890/1540-9295(2006)004[0203:ECUPBA]2.0.
CO;2
Pilon-Smits, E. A. H., Garifullina, G. F., Abdel-Ghany, S., Kato, S., Mihara, H.,
Hale, K. L., et al. (2002). Characterization of a NifS-like chloroplast protein
from Arabidopsis. Implications for its role in sulfur and selenium metabolism.
Plant Physiol. 139, 1309–1318. doi: 10.1104/pp.102.010280
Pilon-Smits, E. A., and LeDuc, D. L. (2009). Phytoremediation of
selenium using transgenic plants. Curr. Opin. Biotechnol. 20, 1–6.
doi: 10.1016/j.copbio.2009.02.001
Pilon-Smits, E. A. H., and Quinn, C. F. (2010). “Selenium metabolism in plants,”in
Cell Biology of Metal and Nutrients, eds R. Hell, and R. Mendel (Berlin:
Springer), 225–241.
Poblaciones, M. J., Rodrigo, S. M., and Santamaría, O. (2012). Evaluation of the
potential of peas (Pisum sativum L.) to be used in selenium biofortification
programs under mediterranean conditions. Biol. Trace Elem. Res. 151, 132–137.
doi: 10.1007/s12011-012-9539-x
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
Pukacka, S., Ratajczak, E., and Kalemba, E. (2011). The protective role of selenium
in recalcitrant Acer saccharium L. seeds subjected to desiccation. J. Plant
Physiol. 168, 220–225. doi: 10.1016/j.jplph.2010.07.021
Quinn, C. F., Freeman, J. L., Reynolds, R. J., Cappa, J. J., Fakra, S. C.,
Marcus, M. A., et al. (2010). Selenium hyperaccumulation offers protection
from cell disruptor herbivores. BMC Ecol. 10:19. doi: 10.1186/1472-
6785-10-19
Rayman, M. P. (2000). The importance of selenium to human health. Lancet. 356,
233–241. doi: 10.1016/S0140-6736(00)02490-9
Reeves, M. A., and Hoffman, P. R. (2009). The human selenoproteome: recent
insights into functions and regulation. Cell. Mol. Life Sci. 66, 2457–2478.
doi: 10.1007/s00018-009-0032-4
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
Reilly, C. (2006). Selenium in Food and Health, New York, NY: Springer Science
Media.
Renkema, H., Koopmans, A., Kersbergen, L., Kikkert, J., Hale, B., and
Berkelaar, E. (2012). The effect of transpiration on selenium uptake and
mobility in durum wheat and spring canola. Plant Soil 354, 239–250.
doi: 10.1007/s11104-011-1069-3
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
Robbins, R. J., Keck, A. S., Banuelos, G., and Finley, J. W. (2005).
Cultivation conditions and selenium fertilization alter the phenolic profile,
glucosinolate, and sulforaphane content of broccoli. J. Med. Food 8, 204–214.
doi: 10.1089/jmf.2005.8.204
Robinson, B. H., Mills, T. M., Petit, D., Fung, L. E., Green, S. R., and
Clothier, B. E. (2000). Natural and induced cadmium accumulation in poplar
and willow: implications for phytoremediation. Plant Soil 227, 301–306.
doi: 10.1023/A:1026515007319
Rotruck, J. T., Pope, A. L., Ganther, H. E., Swanson, A. B., Hafeman,
D. G., and Hoekstra, W. G. (1973). Selenium: biochemical role
as a component of glutathione peroxidase. Science 179, 588–590.
doi: 10.1126/science.179.4073.588
Saidi, I., Chtourou, Y., and Djebali, W. (2014). Selenium alleviates cadmium
toxicity by preventing oxidative stress in sunflower (Helianthus annuus)
seedlings. J. Plant Physiol. 171, 85–91. doi: 10.1016/j.jplph.2013.09.024
Schiavon, M., Dall’acqua, S., Mietto, A., Pilon-Smits, E. A., Sambo, P., Masi,
A., et al. (2013). Selenium fertilization alters the chemical composition and
antioxidant constituents of tomato (Solanum lycopersicon L.). J. Agric. Food
Chem. 61, 10542–10554. doi: 10.1021/jf4031822
Schiavon, M., Moro, I., Pilon-Smits, E. A., Matozzo, V., Malagoli, M., and Dalla
Vecchia, F. (2012). Accumulation of selenium in Ulva sp. and effects on
morphology, ultrastructure and antioxidant enzymes and metabolites. Aqua.
Toxicol. 122–123, 222–231. doi: 10.1016/j.aquatox.2012.06.014
Shardendu, Salhani, N., Boulyga, S. F., and Stengel, E. (2003). Phytoremediation
of selenium by two helophyte species in subsurface flow constructed wetland.
Chemosphere 50, 967–973. doi: 10.1016/S0045-6535(02)00607-0
Sharma, S., Goyal, R., and Sadana, U. S. (2014). Selenium accumulation
and antioxidant status of rice plants grown on seleniferous soil from
Northwestern India. Rice Sci. 21, 327–334. doi: 10.1016/S1672-6308(14)
60270-5
Shibagaki, N., Rose, A., McDermott, J. P., Fujiwara, T., Hayashi, H., Yoneyama,
T., et al. (2002). Selenate-resistant mutants of Arabidopsis thaliana identify
Sultr1;2, a sulfate transporter required for efficient transport of sulfate into
roots. Plant J. 29, 475–486. doi: 10.1046/j.0960-7412.2001.01232.x
Smrkolj, P., Germ, M., Kreft, I., and Stibilj, V. (2006). Respiratory potential and Se
compounds in pea (Pisum sativum L.) plants grown from Se-enriched seeds. J.
Exp. Bot. 57, 3595–3600. doi: 10.1093/jxb/erl109
Sors, T. G., Ellis, D. R., Na, G. N., Lahner, B., Lee, S., Leustek, T., et al.
(2005). 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
fertilization 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
Sun, G.-X., Liu, X., Williams, P. N., and Zhu, Y. G. (2010). Distribution and
translocation of selenium from soil to grain and its speciation in paddy rice
(Oryza sativa L.). Environ. Sci. Technol. 44, 6706–6711. doi: 10.1021/es101843x
Frontiers in Plant Science | www.frontiersin.org 13 January 2017 | Volume 7 | Article 2074

Gupta and Gupta An Overview of Selenium Understanding in Plants
Sun, H.-W., Ha, J., Liang, S. X., and Kang, W. J. (2010). Protective role of selenium
on garlic growth under cadmium stress. Commun. Soil Sci. Plant Anal. 41,
1195–1204. doi: 10.1080/00103621003721395
Tamaoki,M., Freeman, J. L., and Pilon-Smits, E. A. H. (2008). Cooperative ethylene
and jasmonic acid signaling regulates selenate resistance in Arabidopsis.Plant
Physiol. 146, 1219–1230. doi: 10.1104/pp.107.110742
Terry, N., Zayed, A. M., de Souza, M. P., and Tarun, A. S. (2000).
Selenium in greater plants. Annu. Rev. Plant Physiol. 51, 401–432.
doi: 10.1146/annurev.arplant.51.1.401
Thosaikham, W., Jitmanee, K., Sittipout, R., Maneetong, S., Chantiratikul, A., and
Chantiratikul, P. (2014). Evaluation of selenium species in selenium-enriched
pakchoi (Brassica chinensis Jusl var parachinensis (Bailey) Tsen & Lee) using
mixed ion-pair reversed phase HPLC–ICP-MS. Food Chem. 145, 736–742.
doi: 10.1016/j.foodchem.2013.08.116
Tripathi, M. K., and Mishra, A. S. (2007). Glucosinolate in
animal nutrition:a review. Anim. Feed Sci. Technol. 132, 1–27.
doi: 10.1016/j.anifeedsci.2006.03.003
Turakainen, M., Hartikainen, H., Ekholm, P., and Seppänen, M. M. (2006).
Distribution of selenium in different biochemical fractions and raw darkening
degree of potato (Solanum tuberosum L.) tubers supplemented with selenate. J.
Agric. Food Chem. 54, 8617–8622. doi: 10.1021/jf0613987
Van Hoewyk, D., Garifullina, G. F., Ackley, A. R., Abdel-Ghany, S. E., Marcus,
M. A., Fakra, S., et al. (2005). Overexpression of AtCpNifS enhances selenium
tolerance and accumulation in Arabidopsis.Plant Physiol. 139, 1518–1528.
doi: 10.1104/pp.105.068684
Van Huysen, T., Abdel-Ghany, S., Hale, K. L., LeDuc, D., Terry, N., and Pilon-
Smits, E. A. H. (2003). Overexpression of cystathionine-gamma-synthase
in Indian mustard enhances selenium volatilization. Planta 218, 71–78.
doi: 10.1007/s00425-003-1070-z
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
Wallenberg, M., Olm, E., Hebert, C., Björnstedt, M., and Fernandes, A. P.
(2010). Selenium compounds are substrates for glutaredoxins: a novel pathway
for selenium metabolism and a potential mechanism for selenium-mediated
cytotoxicity. Biochem. J. 429, 85–93. doi: 10.1042/BJ20100368
Wang, J. W., Wang, Z. H., and Mao, H. (2013). 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. (2012). Proteomics analysis reveals
multiple regulatory mechanisms in response to selenium in rice. J. Proteomics
75, 184–1866. doi: 10.1016/j.jprot.2011.12.030
Wang, Y. D., Wang, X., and Wong, Y. S. (2013). Generation of selenium-
enriched rice with enhanced grain yield, selenium content and bioavailability
through fertilization with selenite. Food Chem. 141, 2385–2393.
doi: 10.1016/j.foodchem.2013.05.095
White, P. J., Bowen, H. C., Parmaguru, P., Fritz, M., Spracklen, W. P., Spiby,
R. E., et al. (2004). Interactions between selenium and sulphur nutrition in
Arabidopsis thaliana.J. Exp. Bot. 55, 1927–1937. doi: 10.1093/jxb/erh192
WHO (2009). Global Health Risks: Mortality and Burden of Disease Attributable
to Selected Major Risks. Available online at: http://www.who.int/healthinfo/
global_burden_disease/GlobalHealth2009:Risks_report_annex.pdf (Accessed
March 5, 2014).
Winkel, L. H., Vriens, B., Jones, G. D., Schneider, L. S., Pilon-Smits, E.,
and Bañuelos, G. S. (2015). Selenium cycling across soil-plant-atmosphere
interfaces: a critical review. Nutrients 7, 4199–4239
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
Wu, L., and Guo, X. (2002). Selenium accumulation in submerged aquatic
macrophytes Potamogeton pectinatus L. and Ruppia maritima L. from water
with elevated chloride and sulfate salinity. Ecotoxicol. Environ. Saf. 51, 22–27.
doi: 10.1006/eesa.2001.2116
Wu, Z., Bañuelos, G. S., Lin, Z. Q., Liu, Y., Yuan, L., Yin, X., et al. (2015).
Biofortification and phytoremediation of selenium in China. Front. Plant Sci.
6:136. doi: 10.3389/fpls.2015.00136
Ximénez-Embún, P., Alonso, I., Madrid-Albarrán, Y., and Cámara, C. (2004).
Establishment of selenium uptake and species distribution in lupine,
Indian mustard, and sunflower plants. J. Agric. Food Chem. 52, 832–838.
doi: 10.1021/jf034835f
Xue, T. L., Hartikainen, H., and Piironen, V. (2001). Antioxidative and growth-
promoting effect of selenium on senescing lettuce. Plant Soil 237, 55–61.
doi: 10.1023/A:1013369804867
Yan, J., Wang, F., Qin, H., Chen, G., Eviatar, N., Fahima, T., et al. (2011).
Natural variation in grain selenium concentration of wild barley, Hordeum
spontaneum, populations from Israel. Biol. Trace Elem. Res. 142, 773–786.
doi: 10.1007/s12011-010-8770-6
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
Yin, X. B., and Yuan, L. X. (eds.). (2012). “Phytoremediation and biofortification,”
in Two Sides of One Coin, (Berlin: Springer), 1–31.
Zembala, M., Filek, M., Walas, S., Mrowiec, H., Kornas, A., Miszalski, Z.,
et al. (2010). Effect of selenium on macro and microelement distribution
and physiological parameters of rape and wheat seedlings exposed
to cadmium stress. Plant Soil 329, 457–468. doi: 10.1007/s11104-009-
0171-2
Zhang, L., Li, Q., Yang, X., and Xia, Z. (2012). Effects of sodium selenite and
germination on the sprouting of chickpeas (Cicer arietinum L.) and its content
of selenium, formononetin and biochanin a in the sprouts. Biol. Trace Elem.
Res. 146, 376–380. doi: 10.1007/s12011-011-9261-0
Zhang, Y., Pan, G., Chen, J., and Hu, Q. (2003). Uptake and transport of selenite
and selenate by soybean seedlings of two genotypes. Plant Soil 253, 437–443.
doi: 10.1023/A:1024874529957
Zhao, C., Ren, J., Xue, C., and Lin, E. (2005). Study on the relationship
between soil selenium and plant selenium uptake. Plant Soil 277, 197–206.
doi: 10.1007/s11104-005-7011-9
Zhao, F. J., and McGrath, S. P. (2009). Biofortification and phytoremediation. Curr.
Opin. Plant Biol. 12, 373–380. doi: 10.1016/j.pbi.2009.04.005
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. 19, 436–442.
doi: 10.1016/j.tplants.2009.06.006
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.
The reviewer SM and handling Editor declared their shared affiliation, and
the handling Editor states that the process nevertheless met the standards of a fair
and objective review.
Copyright © 2017 Gupta and Gupta. 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.
Frontiers in Plant Science | www.frontiersin.org 14 January 2017 | Volume 7 | Article 2074