Environmental Science and Pollution Research (2020) 27:717–728

https://doi.org/10.1007/s11356-019-06914-0

RESEARCH ARTICLE

Understanding boosting selenium accumulation in Wheat (Triticum

aestivum L.) following foliar selenium application at different stages,
forms, and doses
Min Wang 1 & Fayaz Ali 1 & Mengke Wang 1 & Quang Toan Dinh 1 & Fei Zhou 1 & Gary S. Bañuelos 2 & Dongli Liang 1,3

Received: 9 May 2019 / Accepted: 29 October 2019 / Published online: 5 December 2019
# Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
There are a lack of systematic studies comparing the effects of foliar-applied selenium (Se) with different Se sources at different
growth stages in wheat. Herein, we biofortified wheat via the foliar application of selenite and selenate at different rates and
different stages under field conditions. Results showed that foliar-applied selenate and selenite had no significant effect either on
wheat biomass or grain yield (p < 0.05). Selenium distribution in different parts of wheat plant ranked decrease as leaf > root >
grain > glume > stem with selenite treatment, and it appeared in the decline order as leaf > grain > glume > stem > root with
selenate treatment. These results suggested that biofortification with selenate caused, relatively to selenite, a higher accumulation
of Se in grains. Foliar application of Se of either selenate or selenite at pre-filling stage was superior in improving the Se
concentration of wheat grains than application at pre-flowering stage. Meanwhile, organic Se comprised about 72–93% of total
Se in wheat grains, which was reduced by 5.8% at high Se rate (100 g ha−1), irrespective of the forms of Se or stages applied. The
organic Se proportion in wheat grains was 9% higher with the selenate treatment than with the selenite treatment.
Selenomethionine (SeMet) was the main organic species (67–86%) in wheat grains, followed by selenocysteine (SeCys2). In
summary, our results indicate that Se biofortification of wheat is most effective with 20 g ha−1 selenate foliar-applied at pre-filling
stage.

Keywords Wheat . Organic Se . Selenite . Selenate . Foliar application . Se speciation

Introduction enzymes such as glutathione peroxidase (GSH-Px) and

thioredoxin reductase (TR) (Kápolna et al. 2009). Although
Selenium (Se) is essential not only for bacteria, Archaea, and its essentiality to plants is still controversial, Se is deemed a
animals, including humans (Zhai et al. 2019; Wang et al. beneficial element for plants, and can promote plant growth
2018), but it is also an essential component of antioxidant and stress resistance (Schiavon and Pilon-Smits 2017).
Worldwide, it is estimated that approximately 0.5–1 billion
Responsible editor: Gangrong Shi people are affected by low dietary Se intake (Broadley et al.
Electronic supplementary material The online version of this article
2007; Bañuelos et al. 2015; Ros et al. 2016). Moreover, ap-
(https://doi.org/10.1007/s11356-019-06914-0) contains supplementary proximately 51% of China is affected by Se deficiency (Dinh
material, which is available to authorized users. et al. 2018). The deficiency of Se has been linked with the
occurrence of Kaschin-Beck disease, Keshan disease, and
* Dongli Liang chronic diseases, which are associated with oxidative damage,
dlliang@nwsuaf.edu.cn such as cardiovascular diseases, cancers, and lung diseases
1 (asthma and chronic lung disease) (Zhu et al. 2017).
College of Natural Resources and Environment, Northwest A&F
University, Yangling 712100, Shaanxi, China Due to the extremely narrow gap between dietary Se defi-
2 ciency and Se toxicity in humans (Wang et al. 2014), it is
USDA, Agricultural Research Service, San Joaquin Valley
Agricultural Sciences Center, Parlier, CA 93648-9757, USA inevitable to regulate or establish safe Se content in crops.
3 Compared with crop breeding and genetic engineering, Se-
Key Laboratory of Plant Nutrition and the Agri-environment in
Northwest China, Ministry of Agriculture, enriched crops produced by Se agronomic biofortification
Yangling 712100, Shaanxi, China strategies are recognized as an optimal choice for enhancing
718
Se intake in numerous Se-deficient populations (Ali et al.
2017; Zhou et al. 2018; Li et al. 2018). For example,
Finland, a typical Se-deficient country, has significantly in-
creased the Se levels in various foods and humans since the
soil application of sodium selenate (Se (VI)) was introduced in
1984 (Broadley et al. 2007). Similarly, the UK (Lyons 2010),
Africa (De Valença et al. 2017), and New Zealand (Curtin
et al. 2006) also have successfully implemented agricultural
Se biofortification strategies, albeit on a smaller, more local-
ized scale.
In general, Se fertilizer can be applied using six major tech-
niques: seed dressing, seed soaking, seed coating, hydroponics,
foliar application, and soil application (Wang et al. 2019; Wang
et al. 2013). Seed dressing and seed soaking are difficult to
popularize, because they are not practical or convenient to ex-
ecute (Sun et al. 2017). Meanwhile, in seed coating, the fertil-
izer is in direct contact with the seeds and the fertilizer may fall
off when sowing, which will reduce the efficiency of fertilizer.
Hydroponics is not suitable for cultivation of upland crops or
large area production (Wang et al. 2019). Although soil appli-
cation of Se can significantly enhance Se content in crops, it is
still challenging due to various soil properties (e.g., types, redox
potential, pH, organic matter, and microbiological activity)
(Kápolna et al. 2009). Moreover, soil application of selenite is
easily fixed by iron and aluminum oxides from the soil surface,
while selenate is easily leached and can contaminate ground-
water (Keskinen et al. 2011). Foliar Se application is more
efficient because the individual plants can directly absorb ex-
ogenous applied Se and subsequently transport it efficiently to
other parts of the plant, especially in the edible parts of the crops
(Deng et al. 2017). Numerous studies have shown that foliar
application of Se has successfully promoted the Se content in
various crops, including lentil (Rahman et al. 2015), onion bulb
(Kápolna et al. 2012), carrot root and leaf (Kápolna et al. 2009),
potato (Zhang et al. 2019), grapes (Zhu et al. 2017), and blue-
berry (Li et al. 2018). Similarly, remarkable enhancement of Se
content also has been made via foliar application in edible parts
of cereals, such as corn (Wang et al. 2013), buckwheat (Smrkolj
et al. 2006), wheat (Lara et al. 2019; Ducsay et al. 2016; Nawaz
et al. 2015; Mao et al. 2014), and rice (Lidon et al. 2018; Lemos
et al. 2014; Boldrin et al. 2013). Based upon the above exam-
ples, a better understanding is needed for foliar Se application
on the translocation and absorption of Se by plants (Deng et al.
2017).
Presently, selenite and selenate are recognized as the major
Se sources in exogenous Se fertilizer (Boldrin et al. 2013).
Due to the different physiological characteristics of crops at
different growth stages, the absorption and utilization of Se
also changes with different growth stages (Li et al. 2018; Deng
et al. 2017; Govasmark et al. 2008). Previous studies have
indicated that the soil Se application at the seedling stage of
wheat was less effective in enhancing grain Se content than
the foliar application of selenate at flowering stage, due to the
Environ Sci Pollut Res (2020) 27:717–728
interactions between selenate and soil subsequently decreased
the bioavailability of Se in soil with the application time
(Curtin et al. 2006). The Se concentration of corn for selenate
foliar application at an early stage was 33% lower than that
application at a later stage (Chilimba et al. 2012).
Additionally, the accumulation ratio of Se in the brown rice
was significantly improved, particularly with foliar Se appli-
cation at full heading stage compared with late tillering stage
(Deng et al. 2017). Consequently, the application of Se in the
later growth stage may be more conducive to improve the Se
content in crops, i.e., rice. However, the optimum late time for
the foliar application of Se to wheat has not been reported yet.
The Se bioassessibility largely depends on the Se spe-
ciation rather than the total content of Se in edible parts
(Premarathna et al. 2012). Studies of Se speciation in
wheat treated with selenite (or selenite versus selenate)
have been rarely reported, since wheat is a non-Se accu-
mulator. Galinha et al. (2015) found that Se in wheat is
mostly present in the organic form of selenomethionine
(56–100%), with smaller fractions as selenocysteine (4–
12%) and selenomethyl-selenocysteine (1–4%), as well as
selenate (5–19%) and other inorganic forms (4–26%).
Previous studies have demonstrated that organic Se in
crop grains generally accounted for more than 80% of
total Se (Seppänen et al. 2010). Selenomethionine
(SeMet) occupied more than 40% in rice grain when sel-
enite was applied to the soil (Gong et al. 2018), which
was over 76% in Lentinula edodes (Zhou et al. 2018).
Numerous studies have demonstrated that in soil applica-
tion of Se, selenite absorbed by roots was quickly trans-
formed into organic Se (such as selenomethionine,
selenocysteine, etc.) and mainly accumulated in root tis-
sue, while selenate was more readily transported to the
shoots in the form of Se(VI) (Wang et al. 2014; Li et al.
2018; Natasha et al. 2018). Thus, it is still unclear how
the proportion in foliar Se application at different growth
stages changes, and which Se species is more efficient in
converting inorganic Se into organic Se under field
conditions.
Among potential Se-enriched crops, wheat (Triticum
aestivum L.) is highly demanded since it is the main staple
food for more than one third of the world’s population
(Kalhoro et al. 2016), and its derivative products, such as
bread, cake, cereal, and pasta, are also indispensable compo-
nents in peoples’ diets (Curtin et al. 2006). Given the wide-
spread consumption of wheat, the production of Se-enriched
wheat may be an effective approach for Se supplementation in
many Se-deficient populations. The objectives of this study
were to test the effect of different forms of foliar Se fertilizers
applied at both different rates and growth stages of wheat on
the following: (1) biomass and grain yield, (2) distribution of
Se and tissue Se accumulation, and (3) Se speciation in wheat
grain.
Environ Sci Pollut Res (2020) 27:717–728
Materials and methods
Field experimental site and wheat cultivar
The field trails were carried out during 2016 in the experimen-
tal field located at Northwest A&F University in Yang Ling,
Shaanxi Province, China (34° 20′ N, 108° 24′ E at 521 m
altitude). The annual precipitation is 630 mm. Soil samples
were air-dried, homogenized, ground, and passed through 2
and 0.149 mm sieves for physicochemical analysis. The phys-
icochemical properties of the tested soil from 0 to 20 cm were
determined according to the procedures described by Li et al.
(2015), and are shown in Table 1.
Soil pH was determined at a soil-to-water ratio of 1:1 using
a pH meter. Carbonate content was measured by gas volumet-
ric method. Organic matter content was determined by hot
K2CrO4 oxidation and FeSO4 titration. The cation exchange
capacity (CEC) was extracted by NH4OAC solution and de-
termined using flame spectrophotometer. Amorphous iron and
amorphous aluminum were extracted by oxalic acid-
ammonium oxalate solution and determined using an induc-
tively coupled plasma mass spectrometry (ICP-MS). Soil clay
was determined by a laser particle size instrument. Total Se
was digested by HNO3:HClO4 (3:2) at 170°C until clear and
analyzed for total Se by an atomic fluorescence spectropho-
tometer (AFS-930, Beijing Titan Instruments Co., Ltd.) with
hydride generation, according to the Chinese National
Standard Method GB/T 5009.93-2003.
The seeds of winter wheat (Triticum aestivum L.) variety
“Xinong 538” were purchased from Yang Ling Seed Group
(Yang Ling, Shaanxi, China), and analytical-grade Na2SeO4
and Na2SeO3 were purchased from Tianjin Chemical Reagent
Factory (China) and used as selenate and selenite sources,
respectively. The standard substances of selenomethionine
(SeMet), selenocysteine (SeCys2), and methylselenocysteine
(MeSeCys) were all purchased from Sigma, USA, and used
for speciation identification.
Experimental design
The experiment was performed using a randomized complete
block design. The plot area was 3.8 m × 1.4 m and row spac-
ing of wheat was 30 cm. Eight treatments consisted of differ-
ent growth stages (pre-flowering and pre-filling stage), and
different Se species (selenite and selenate), and different foliar
Table 1 Physicochemical properties of the experimental soil
Soil pH Carbonate Organic Cation exchange
type content matter capacity (cmol
(g kg−1) (g kg−1) kg−1)
Lou soil 7.99 55 14.34 23.34
719
rates of Se (20 g ha−1 and 100 g ha−1) were set up in the
experiment. In addition, a treatment sprayed of only distilled
water was provided as the control group (CK). The specific
factors of foliar experiments are shown in Table 2. Each treat-
ment was replicated three times. The sowing date was October
6, 2016, wheat was harvested at June 5, 2017. Other measures
of agronomic management followed local practices.
The fertilizer was applied as follows: nitrogen 100 kg ha−1
(urea) and phosphorus 80 kg ha−1 (triple superphosphate)
were applied as basal fertilizers to all plots before sowing.
The sodium selenite and sodium selenate solutions were
sprayed once at pre-flowering stage (F1; April 4), or at pre-
flowering stage (F2; May 4). The concentration of each spray
solution was 10 mg Se L−1 and 50 mg Se L−1, respectively.
The final volume of the Se solution applied was 1 L per plot
(5.32 m2). The plants were sprayed with a small atomizer.
Meanwhile, foliar application experiments were carried out
on sunny days at 17:00–18:00 am for both growth stages.
Sample preparation
The biomass and grain yield of wheat were calculated for all
plots after one row was removed from each side of the plot.
Within the plot, ten plants were randomly selected and divided
into five parts: root, stem, leaf, glume, and grain. Each part
was carefully washed with tap water to remove attached soil
particles, and then rinsed at least three times with deionized
water. Samples were randomly collected and each treatment
was divided into two parts. One part was oven-dried at 60°C
for 72 h to a constant weight, and then crushed into powder for
the determination of total Se content, described later. The oth-
er part was lyophilized at − 65°C for speciation identification
and quantification, as described later.
Analytical methods
Determination of total Se content in wheat
About 0.5 g oven-dried sample was digested in an acid mix-
ture of 4:1 (v/v) HNO3–HClO4 in a 100 mL glass tube. Acid
digestion was performed at 165°C in an automatic
temperature-controlled furnace until the digestion solution be-
came clear. Then the digestion solution was reduced to Se(IV)
in 6 mol L−1 HCl solution medium by placing the solution in a
hot water bath at 100°C for 30 min. After cooling, the Se
Amorphous Amorphous Clay (%) Amibient
iron aluminum total Se
(g kg−1) (g kg−1) (mg kg−1)
1.2 0.4 39.5 0.059
720
Table 2 Factors of the foliar experiment
Factor Foliar application stage Se source
Se rate (g ha )
Treatment Pre-flowering Selenite 20
Pre-filling Selenate 100
content was determined by hydride generation atomic fluores-
cence spectrometry (HG-AFS).
The standard sample GSW10011 (GSB-2, wheat seeds,
China) was obtained from the Center of National Standard
Reference Materials and used for quality control. The mea-
sured value for GSW10011 (certified value; 0.053 ± 0.007 mg
kg−1) was 0.048 ± 0.003 mg kg−1. The method detection limits
for Se were limited on the basis of the standard deviation (SD)
of the signals measured (15 times) for the blank solution,
which was 0.1 μg L−1; the relative standard deviation was <
10%; and the Se recovery rate was 96%.
Determination of Se speciation in wheat grain
The method of the determination of Se speciation was modi-
fied from Bañuelos et al. (2012). The powder of lyophilized
samples (1 g) was accurately weighed into
polytetrafluoroethylene bottles. Subsequently, 0.05 g protease
XIV, 0.05 g cellulose, and 25 mL ultrapure water were added
into the bottle, conducted Ultrasonic Enzymatic Hydrolysis at
37°C for 30 min, and then shook at 210 rpm for 12 h at 37 °C.
Afterward, 10 mL dichloromethane was added into the bot-
tles, shook for five times, and then placed overnight in a re-
frigerator at 4 °C until the upper part of the sample was puri-
fied. Then the bottle was gently tapped to make the black
supernatant precipitation sink. The supernatant was then re-
moved and pipetted into new polypropylene tubes, and total
Se was determined in 5 mL supernatant. Nextly, the remaining
samples were condensed overnight in a vacuum cryopreser-
vation centrifuge and successively redissolved with 2 mL ul-
trapure water and 11.2 μL methanol. The C-18 column was
used with methanol and ultrapure water. The samples were
placed onto in the concentrator, and then redissolved with
0.5 mL ultrapure water. Finally, 1.5-mL samples were taken
and pipetted into miniature centrifuge tubes.
The sample was centrifuged for 30 min by a high-speed
centrifuge at 1000 rpm to draw the supernatant into the special
sample bottle, and then the speciation of Se was determined
by HPLC-ICP-MS (Agilent 7500 cx, Santa Clara, CA) sys-
tem. The retention time of 78, 80, and 82 Se isotopes was
monitored simultaneously by HPLC-ICP-MS, and the reten-
tion time of the sample was directly compared with the fol-
lowing standard Se to determine the speciation of Se in the
sample: selenomethionine (SeMet), selenocysteine (SeCys2),
methylselenocysteine (MeSeCys".), SeO42−, and SeO32−.
Environ Sci Pollut Res (2020) 27:717–728
To examine the effect of protease XIV enzymatic hydroly-
−1
sis on the extraction of wheat grain Se speciation, the total Se
concentration was determined in the supernatant after centri-
fugation. The extraction rate was the ratio of total Se in super-
natant to total Se in samples. The results showed that all the
extraction efficiency rates of different foliar Se application
were above 88%, which indicated the enzymatic hydrolysis
of protease XIV could efficiently extract the Se species of
wheat grain. SELM-1 (Se-enriched yeast, SeMet 3431 ±
157 mg kg−1), which was purchased from the Canadian
National Research Council, was used as the standard sub-
stance for the calibration of SeMet. The measured value for
SeMet was 3398 ± 37 mg kg−1.
Statistics
Microsoft Excel 2013 and Origin 2016 were used for process-
ing data and diagram plotting. Data in the chart were the
average of three replications and were expressed as the mean
value ± standard deviation (SD). SPSS 20.0 statistical analysis
software was used for significance analysis, and the LSD
method for difference significance test (at significant level α
= 0. 05).
Results
Wheat biomass and grain yield
Table 3 illustrates wheat biomass and grain yield with foliar-
applied selenite or selenate for different rates at pre-flowering
or pre-filling stages. As was depicted in Table 3, slight but not
positive significant difference were observed on the biomass
and grain yield of wheat for all treatments compared with
control. As a consequence, neither the rates of exogenous Se
nor the forms of Se applied had no significant effect on wheat
biomass and grain yield (p > 0.05). Futhermore, both the
highest wheat grain yield (5.73 t ha−1) and biomass (13.33 t
ha−1) were obtained at pre-flowering stage for 20 and 100 g
ha−1 foliar-applied selenite treatments, respectively.
Selenium concentration distribution in different parts
of wheat
Compared with control, Se concentration in various parts of
wheat was significantly improved (p < 0.05) with various Se
species and each growth stages of foliar Se application
(Table 4). Irrespective of exogenous Se species, the Se con-
centration of various wheat parts was significantly higher in
100 g ha−1 treatment than in 20 g ha−1 treatment (p < 0.05). At
pre-filling stage, the Se concentration in wheat grains of foliar-
applied 100 g ha−1 selenite and selenate reached 6.64 and
Environ Sci Pollut Res (2020) 27:717–728 721

Table 3 Wheat biomass and

grain yield with foliar-applied Se Source Growth stage Se rates (g ha−1) Grain yield (t ha−1) Biomass (t ha−1)
selenite or selenate of different
rates (20 g ha−1 and 100 g ha−1) at CK 5.49 ± 0.46 a† 12.49 ± 1.20 a
pre-flowering (F1) or pre-filling Se(IV) F1 20 5.54 ± 0.54 a 12.87 ± 0.95 a
stages (F2) 100 5.73 ± 0.51 a 13.31 ± 0.67 a
F2 20 5.61 ± 0.55 a 13.17 ± 0.72 a
100 5.64 ± 0.69 a 12.69 ± 1.50 a
Se(VI) F1 20 5.70 ± 0.45 a 13.33 ± 0.46 a
100 5.65 ± 0.32 a 13.27 ± 0.56 a
F2 20 5.61 ± 0.79 a 12.97 ± 1.33 a
100 5.50 ± 0.47 a 12.63 ± 1.05 a
ANOVA (F value)
Se contents (C) NS‡ NS
Se species (S) NS NS
Growth stage (G) NS NS
S×G NS NS
S×C NS NS
G×C NS NS
S×G×C NS NS
†
Lowercase letters after the same column indicates the significant differences among foliar selenite or selenate
applied at both different rates (20 g ha−1 and 100 g ha−1 ), and at pre-flowering (F1) or pre-filling stages (F2) (p <
0.05)
‡
“NS” means non-significant differences (p < 0.05)

6.82 mg kg−1 dry weight (DW), which was 55.3 and 55.8
times higher than control, respectively.
In terms of the stages of Se application, except for 100 g
ha−1 selenate treatment, the root Se concentration was higher
at pre-flowering stage than that at pre-filling stage for all treat-
ments. Se concentration in root was significantly increased by
52% at pre-flowering stage compared with pre-filling stage for
20 g ha−1 selenite treatment (p < 0.05). On the contrast, Se
concentration of stem significantly increased by 43% at pre-
filling stage than that at pre-flowering stage for 100 g ha−1
selenite treatment (p < 0.05). In addition, except for 100 g ha−1
selenate treatment, the leaf Se concentration was higher at pre-
filling stage than at pre-flowering stage for all treatments (av-
erage of 15%). Similarily, irrespective of Se rates and forms
applied, the glume and grain Se concentration were higher at
pre-filling stage than at pre-flowering stage for all treatments.
The average grain Se concentrations were 3.81 and
4.21 mg kg−1 for selenite and selenate foliar-applied at pre-
filling stage, which were 55% and 4% higher than correspond-
ing treatment at pre-flowering stage, respectively. At the same
time, irrespective of applciation rates of selenite, the Se con-
centration in wheat grain gradually increased for pre-filling
stage treatment compared with pre-flowering stage treatment,
indicating that properly delaying foliar application time was
beneficial for enhancing the Se concentration in wheat grain.
In regard to forms of exogenous Se applied, the root Se
concentration of selenite treatment was higher than selenate
treatment at pre-flowering stage irrespective of Se application
rates, whereas the opposite trend was found for the root Se
concentration at the pre-filling stage, and root Se concentra-
tion was significantly increased by 27% in selenate treatment
than that in selenite at 20 g ha−1 treatment (p < 0.05). As for
stem, the Se concentration of selenate treatment with 20 g ha−1
and 100 g ha−1 at pre-flowering stage was significantly in-
creased by 33% and 56% than the corresponding selenite
treatment, respectively (p < 0.05). In addition, except for the
selenate treatment of 100 g ha−1 at pre-filling stage, the leaf Se
concentration of selenate treatment was higher than that in
selenite treatment. Interestingly, grain Se concentration was
consistent with stem and glume, while the grain Se concentra-
tion was significanantly higher in selenate treatment than in
selenite treatment (50% in average). Overall, a stronger pro-
moting effect on grain Se concentration had been found in
selenate treatment than in selenite treatment.
Selenium concentration distribution was observed in various
parts of wheat (Table 4). Overall, the distribution of Se concen-
tration in CK treatment was as follows in different parts of
wheat: leaf > glume > root > stem > grain. Selenium distribu-
tion in wheat plant was observed in the descending order of leaf
> root > grain > glume > stem with foliar-applied selenite, while
it ranked as leaf > grain > glume > stem > root with foliar-
applied selenate. Irrespective of the forms of Se applied, Se
concentrations of various parts of wheat increased with an in-
creasing application rates of Se, especially in wheat leaf.
Nevertheless, no significant effect on Se distribution was ob-
served with either Se forms applied at the same application rate.
722 Environ Sci Pollut Res (2020) 27:717–728

Table 4 Selenium concentration in different parts of wheat with foliar selenite or selenate applied at different rates (20 g ha−1 and 100 g ha−1) at pre-
flowering (F1) or pre-filling stages (F2)

Treatment Se Concentration (μg g−1)

Root Stalk Leaf Glume Grain

CK 0.20 ± 0.04 BC† 0.16 ± 0.04 BC 0.36 ± 0.06 A 0.20 ± 0.03 B 0.12 ± 0.00 C
-1
20 g ha Se(IV) F1 1.11 ± 0.12 Ba 0.51 ± 0.11 Bb 3.07 ± 0.76 Aa 1.07 ± 0.15 Bb 0.61 ± 0.11 Bc
F2 0.73 ± 0.08 CDb 0.46 ± 0.08 Db 3.83 ± 0.16 Aa 1.48 ± 0.37 Bab 0.97 ± 0.15 Cb
Se(VI) F1 1.01 ± 0.22 Ba 0.76 ± 0.17 Ba 2.43 ± 0.58 Ab 1.36 ± 0.17 Bab 1.34 ± 0.22 Ba
F2 1.00 ± 0.11 Ca 0.60 ± 0.09 Dab 2.82 ± 0.17 Ab 1.68 ± 0.24 Ba 1.59 ± 0.24 Ba
100 g ha -1 Se(IV) F1 4.78 ± 1.31 Ba 1.33 ± 0.25 Cb 13.47 ± 2.67 Aa 2.85 ± 0.32 Bb 2.81 ± 0.30 Bb
F2 3.86 ± 0.58 Ca 2.35 ± 0.51 Ca 15.05 ± 2.46 Aa 7.97 ± 1.67 Ba 6.64 ± 0.23 Ba
Se(VI) F1 3.54 ± 0.10 Ca 3.00 ± 0.76 Ca 9.71 ± 1.33 Ab 4.42 ± 0.43 Cb 6.76 ± 1.48 Ba
F2 4.01 ± 0.12 Ca 3.06 ± 0.60 Ca 9.29 ± 1.88 Ab 7.27 ± 1.17 Aba 6.82 ± 0.93 Ba
ANOVA (F value)
Se contents (C) ** ** ** ** **
Se species (S) NS‡ NS NS ** **
Growth stage (G) NS ** ** NS **
S×G NS NS NS NS **
S×C NS NS NS ** *
G×C NS * ** NS *
S×G×C NS NS NS NS **
†
Lowercase letters after the same column indicates a significant difference between different leaf areas in the same position (p < 0.05); uppercase after the
same row data indicates a significant difference in different parts of wheat treated with selenium on the same leaf surface (p < 0.05)
‡
“NS” means non-significant difference (p < 0.05); * and ** show significant difference at P ≤ 0.05 and 0.01, respectively

Selenium translocation factor in different parts
of wheat
The translocation factor (TF) is the measurement of the plant’s
potential to take up a specific element/compound from source,
and transfer it to sink (Lemos et al. 2014; Dinh et al. 2019).
This factor was used to analyze the effects of different exog-
enous Se treatments on Se translocation in wheat (Fig.1).
TFgrain/leaf = Cgrain/Cleaf (C represents the Se concentration of
the corresponding parts of wheat).
Figure 1 showed that the TFgrain/leaf was less than 1, indi-
cating that the majority of the Se remained in leaves after Se
was applied, which was consistent with the results of the dis-
tribution of Se in wheat (Table 4). However, applied selenate
100 g ha−1 at pre-flowering stage and pre-filling stage resulted
in TFgrain/leaf 1.1 times and 1.24 times increase compared to
control, respectively, demonstrating that foliar Se application
could enhance the translocation of Se from leaf to grain.
It was worth noting that the TFgrain/leaf of the selenate applied at
pre-flowering stage treatment increased by 182% and 227% for
application rate of 20 g ha−1 and 100 g ha−1 compared with the
corresponding selenite treatment, respectively. Similar results were
found at pre-filling stage. TFgrain/leaf treated with selenate were
124% and 67% higher than those treated with selenite treatment
at 20 g ha−1 and 100 g ha−1, respectively. It indicated that foliar
application of selenate is more efficient for Se translocating from
leaves to grains. In addition, no significant difference in TFgrain/leaf
was observed between those two application stages.
Selenium speciation in wheat grains
Chromatogram of Se speciation in wheat
Figure 2 showed the spectrogram of Se speciation detected in
the standard sample and wheat grains from two different Se
treatments. The chromatograms of the standard sample, sele-
nate, and selenite treatments of wheat grain were represented
by (a), (b), and (c), respectively. Compared with the retention
time (tR) of each peak in the standard solution, the left to right
order in the standard sample spectrum was SeCys2, SeMeCys,
Se4+, SeMet, and Se6+, and the corresponding retention times
were 2.08–2.67 min, 2.68–3.33 min, 3.34–4.18 min, 4.18–
5.83 min, and 9.16–11.67 min, respectively. The peak area
in the spectrogram quantitatively analyzed the speciation of
Se, and the proportion of Se species detected.
The percentage of Se species in wheat grains
The various Se speciation proportion within total Se were
identified in wheat grain treated with different foliar
Environ Sci Pollut Res (2020) 27:717–728
applications of Se (Fig. 3). The main Se speciation in wheat
grain was selenomethionine (SeMet) for all foliar applications
treatments and accounted for about 67–86% of total Se,
followed by selenocysteine (SeCys 2 ) (2–8%), while
methylselenocysteine (MeSeCys) was not detected in all
wheat grains for all treatments.
The percentage of organic Se to total Se in wheat grain was
84% and 75% for foliar application of selenite and selenate,
respectively. This difference indicated that the percentage of
organic Se in wheat grain was higher with foliar-applied sel-
enite than selenate. Nevertheless, the percentage of organic Se
in wheat grain increased by 5.34% with 20 g ha−1 selenate
treatment at pre-filling stage compared to pre-flowering stage.
Irrespective of the forms and the growth stages of foliar Se
application, the proportion of organic Se in wheat grain was
decreased by 5.8% at a high application rate of Se (100 g ha−1)
than that of the low rate (20 g ha−1). Moreover, Se6+ was the
main inorganic Se species in wheat grains. When selenate was
applied, Se6+ accounted for 2–9%, and only a very small
amount of Se4+ was detected (1–3%).
Discussion
Effects of different foliar Se application on wheat
biomass and grain yield
The foliar application of selenite or selenate at pre-filling stage
and pre-flowering stage did not significantly increase the
wheat biomass (~ 3%) and grain yield (~ 2%) (Table 3), which
were consistent with previous findings in various field crops,
such as corn grain (Wang et al. 2013), Brassica seed
(Seppänen et al. 2010), durum wheat (Vita et al. 2017), and
garlic bulb (Põldma et al. 2011).
Fig. 1 Translocation factor of
selenium from leaf to grain with
foliar selenite or selenate applied
at different rates (20 g ha−1 and
100 g ha−1) of pre-flowering (F1)
or pre-filling stages (F2) of wheat.
†
Lowercase letters indicate the
significant differences among fo-
liar selenite or selenate applied at
20 g ha−1, and at pre-flowering
(F1) or pre-filling stages (F2) (p <
0.05). ‡Uppercase letters indicate
the significant differences among
foliar selenite or selenate applied
at 100 g ha−1, and at pre-
flowering (F1) or pre-filling
stages (F2) (p < 0.05)
723
However, other studies reported that the improvement of
yield and biomass of crops after foliar Se application.
Ekanayake et al. (2015) found that foliar application of sele-
nite and selenate increased the lentil grain yield by 10% and
4% compared to control, respectively. Boldrin et al. (2013)
observed that both the foliar application of selenate or selenite
increased the grain yield of rice. Deng et al. (2017) reported
that spraying selenite or selenate at both late tillering stage and
full heading stage increased the biomass and yield of rice. In
addition, the seed yield of mustard was significantly increased
by spraying Se under hydroponic conditions, which was likely
due to the increased respiration activity of leaves and flowers
(Lyons et al. 2009).
No significant increases in grain yield was found in this
study (Table 3), which was inconsistent with the findings of
the previous studies. Lara et al. (2019) observed a 31% in-
crease in wheat grain yield after foliar-applied 120 g ha−1
selenate, and Ducsay et al. (2016) reported an increase on
wheat grain yield after selenate foliar applications at 10 g Se
ha−1. Thus, different selenium effects on wheat growth might
due to different experimental conditions (Deng et al. 2017).
Absorption, translocation, and distribution of Se
in wheat under different foliar Se application
Compared with roots of crops, leaves can quickly absorb
nutrients and transport them to other parts of the plant with
foliar application of Se. Numerous previous studies have shown
that exogenous Se can be transported to other parts of wheat
plants after absorption by leaves. Lara et al. (2019) demonstrated
that the treatment with foliar-applied 120 g ha−1 of selenate pro-
vided the concentrations of Se in the grains (2.86 mg kg−1), about
10 times compared to the control. Nawaz et al. (2015) reported
levels of 1.7 mg kg−1 of Se in wheat leaves, after two foliar
724
Fig. 2 Chromatogram of selenium in wheat grain with foliar selenite or selenate applied at different rates (20 g ha−1 and 100 g ha−1) of pre-flowering (F1)
or pre-filling stages (F2)
applications of 40 mg L−1 of Se (selenate). Furthermore, others
have reported that spraying Se significantly increased maize grain
Se concentration (Wang et al. 2013), Brassica seeds Se concen-
tration (Seppänen et al. 2010), and potato tuber Se concentration
(Poggi et al. 2000). In line with those findings, this study showed
that the Se concentration of wheat grain significantly increased
after foliar application of Se, and Se concentrations increased
with the raising rate of Se application (Table 4). Interestingly,
Boldrin et al. (2013) demonstrated that the majority of Se was
transported to the non-edible parts of crops by soil Se application,
while the amount of Se was higher in rice grain after foliar sele-
nate application.
The Se application stage significantly influenced the
grain Se concentration. Chu et al. (2013) also found the
grain Se concentration was lower for foliar Se application
onto wheat at regreening stage, and jointing stage than
that at flowering stage. Similar results showed that the
average Se concentration in the grain of wheat was signif-
icantly higher when Se was foliar-applied at booting stage
than at jointing stage (Põldma et al. 2011). Our study
found that the average grain Se concentrations of foliar
application at pre-filling stage were 55% and 4% higher
than those obtained by foliar application at pre-flowering
stage for selenite and selenate, respectively (Table 4).
These results were mainly attributed to the translocation
of Se to the stem and root of the wheat at pre-flowering
Environ Sci Pollut Res (2020) 27:717–728
stage. However, the formation of wheat grain occurs dur-
ing pre-filling stage, and consequently more Se was
transported to the edible parts of the wheat (grain). This
response further illustrated that properly delaying the time
of foliar Se application increases the concentration of Se
in the edible parts of crops. Furthermore, this observation
allows us to infer that Se might be more readily
translocated into the grain during the reproductive growth
stage.
In addition, we observed that transport efficiency of Se into
grain was higher when Se species was foliar-applied at the
later stage of crop growth. In contrast to our study, Deng
et al. (2017) discovered that delaying foliar application time
may result in insufficient time to transport a large amount of
Se absorbed by crops from the husk to brown rice. Li et al.
(2018) also reported that foliar application of selenate and
selenite (200 g ha−1) at young fruit stage onto blueberry pro-
moted the accumulation of Se in fruit, while Se tended to
accumulate in roots and stems when foliar-applied at coloring
stage. The difference of crop species as well as the later stage
of foliar application may have caused this discrepancy, this
needs further clarification in future study.
In the present study, although a proportion of Se was
translocated to other parts of the wheat, the majority of the
Se absorbed by the leaves remained in the leaves (Fig. 1).
Thus, the Se concentration in leaves with foliar-applied
Environ Sci Pollut Res (2020) 27:717–728
Fig. 3 Selenium proportion of various Se species in wheat grain with foliar selenite or selenate applied at different rates (20 g ha−1 and 100 g ha−1) of pre-
flowering (F1) or pre-filling stages (F2)
selenite or selenate was higher than in any other parts
(Table 4), which was consistent with the findings reported in
carrots by Kápolna et al. (2009).
Crops have markedly different capacities for the uptake of
selenite and selenate. This study found that Se concentrations
in different parts of wheat treated with foliar selenate were
higher than those in selenite treatment at the same growth
stages. This was in agreement with the findings of Wang
et al. (1995), they had also reported that the Se concentration
in different parts of the plant was higher with foliar-applied
selenate than selenite (about 2-fold). Similarly, Borldrin et al.
(2013) observed that the proportion of Se in the grain by
foliar-applied selenate was higher than selenite in rice. These
findings suggest that selenate was more easily transported
through the phloem when applied onto leaves compared with
selenite, although selenate was transported through xylem
from the roots when Se was applied to soil (Deng et al. 2017).
Selenium absorbed by plant leaves will be transported
down through the phloem to the root after metabolic transfor-
mation (Wang et al. 2016). This study observed that Se tended
to transport to the root of wheat with foliar-applied selenite,
while which tended to transfer to the grain of wheat when
selenate was foliar-applied (Table 4). This was consistent with
the results of Wang et al. (2016), they demonstrated that 30–
35% of Se transferred to the root of strawberry after foliar
application of sodium selenite in 4 months, while less than
15% of Se was translocated from leaf to root of strawberry
for foliar-applied selenate. The discrepancy in absorption and
distribution of foliar-applied selenite and selenate in wheat
attribute to the different metabolism pathways used by selenite
and selenate in plants (Lara et al. 2019). Moreover, the fluidity
725
of Se in the phloem was higher with foliar-applied selenate in
potato, and thereby the Se concentration was significantly
increased (Poggi et al. 2000). The above findings indicated
that the translocation of Se in plants is influenced by the forms
of foliar-applied Se.
Effects of different foliar Se application on wheat
speciation
The present study showed that SeMet was the main species of
organic Se in wheat grain, irrespective of the forms of applied
exogenous Se, followed by SeCys2, however, no MeSeCys
was detected (Fig. 3). This finding is consistent with the pre-
vious study (Sors et al. 2005). Zhang et al. (2019) found that
the major Se species in potato tubers was SeMet for both
selenite and selenate treatment, which accounted for 80%
and 50% of total Se. Hart et al. (2011) observed that SeMet
accounted for 65–87% in Se-enriched flour and bread, while
SeCys, Se(IV), and Se(VI) were also detected at percentages
of 5%, 5%, and 4%, respectively. Seppänen et al. (2010) re-
ported that up to 85% of the total Se was SeMet in Brassica
seeds. Although wheat is a non-Se accumulator, a previous
study has shown that the process of assimilation of inorganic
Se into SeCys in Se accumulators is similar to that in non-Se-
accumulating crops (Schiavon and Pilon-Smits 2017). Based
upon the above results, we can conclude that wheat can be a
good choice to practice for supplements Se in Se-deficient
areas.
Plants can transfer inorganic Se into organic Se, and the
transformation differs depending on Se species. Our results
demonstrated that foliar application of selenite was more
726
efficient than selenate in converting to organic Se. The same
results were also reported by Kápolna et al. (2012); they found
that the foliar application of selenite significantly promoted
the synthesis of organic Se, compared with selenate. This phe-
nomenon may be explained by the following. In general, sel-
enate and selenite are readily transported through the plant
cuticle and metabolized via the sulfur assimilatory pathway.
The first step of Se metabolism in plants is the reduction of
Se(VI) to Se(IV) (Kápolna et al. 2009), which can be further
transformed into selenides. This step is thought to be a limit-
ing step in selenate assimilation. Some of the selenides are
metabolized by cysteine synthase to form SeCys, which can
be catalyzed by Se-methyltransferase or by trans-sulfurylase
to form MeSeCys or SeMet, respectively (Hart et al. 2011). In
this process, Se(VI) needs to be reduced to Se(IV) and then
transformed into organic forms of Se, while Se(IV) can be
directly transformed into organic forms.
In this regard, Sors et al. (2005) predicted that Se(VI) was
assumed to enter chloroplasts in the form of SeO42− in plant
leaves, and then is reduced to Se(IV) under the action of ATP
sulfatase and APS reductase. Afterwards, Se(IV) can be trans-
formed into a variety of forms of organic Se by the action of
cysteine-synthetase, selenomethionine-transferase, and other
enzymes. These organic Se forms are stored in the leaves of
plants or transported to other parts of the plant, while some
organic Se can be transported through the phloem to the root
of the plant with other nutrients in plant leaves. Therefore, the
transformation of Se from leaves to roots of Se(VI) in plant
leaves is slower than Se(IV).
Plants can take up and assimilate inorganic forms of Se into
SeCys2 and SeMet via S transporters and the S assimilation
pathway (Schiavon and Pilon-Smits 2017). When these
seleno-amino acids are nonspecifically incorporated into pro-
teins, replacing Cys and Met, this disrupts protein function
and causes toxicity (Hoewyk 2013). Though there was no
obvious toxicity at high Se foliar application (100 g ha−1) in
this experiment, our results showed that the proportion of
organic Se to total Se decreased at high foliar application rates
of 100 g ha−1 (Fig. 2), which may be due to the transformation
of some organic Se with increasing rate of Se application. In
addition, our results suggested that the excessive application
of Se was not conducive to the accumulation of organic Se in
wheat, which might be attributed to the reduced transforma-
tion ability of Se in plants.
Conclusions
Wheat (Triticum aestivum L.), an agricultural crop, is suitable
for foliar Se biofortification since it concentrates adequate
levels of Se in grains, not reducing its growth and yield.
Different forms of foliar Se application had no significant
effect on wheat plant biomass and grain yield. Selenium
Environ Sci Pollut Res (2020) 27:717–728
distribution in wheat was in the descending order of leaf >
root > grain > glume > stem when selenite was foliar-applied,
and it ranked as leaf > grain > glume > stem > root when
selenate was foliar-applied. Foliar application of either sele-
nite or selenate at pre-filling stage was more efficient at in-
creasing Se content in wheat grain than at pre-flowering stage.
SeMet was the main organic Se species in wheat grain, ac-
counting for about 67–86% of total Se. Thus, we suggest that
foliar application of selenate at 20 g ha−1 at pre-filling stage is
the most efficient way for Se biofortification in wheat. The
specific stage of the plant for foliar application of Se should be
further studied in the future to ensure the safety of Se concen-
tration in grain.
Acknowledgments The authors thank for the financial support provided
by Public Welfare Geological Survey Project of Shaanxi Geological
Survey Institute (No. 20180307) and the National Natural Science
Foundation of China (No. 41571454).
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