sustainability
Article
Selenium Distribution and Translocation in Rice
(Oryza sativa L.) under Different Naturally
Seleniferous Soils
Jia Shen, Chaoqiang Jiang *, Yifeng Yan and Chaolong Zu *
Tobacco Research Institute, Anhui Academy of Agricultural Sciences, Hefei 230031, China;
[email protected] (J.S.);
[email protected] (Y.Y.)
* Correspondence:
[email protected] (C.J.);
[email protected] (C.Z.);
Tel.: +86-551-6514-8998 (C.J.); +86-551-6514-8978 (C.Z.)
Received: 4 December 2018; Accepted: 15 January 2019; Published: 19 January 2019
Abstract: Selenium (Se) accumulation in plant foods may be providing dietary Se to minimize the
health problems related to Se deficiency. In this study, rice plants were cultivated in different naturally
seleniferous soils (0.5–1.5 mg Se kg−1 ). Se concentration in rice plant tissues was analysed, and the
distribution and translocation of Se in rice were also studied. The effect of exogenous Se on yield and
Se concentration in rice grain was also investigated by spraying Na2 SeO3 (15 mg L−1 , 15 g ha−1 ).
Results show that Se concentration in root, straw and grain of rice was increased with increased
concentrations of Se in seleniferous soils. The root accumulated higher Se than straw and grain under the
same naturally seleniferous soil. Spraying Se significantly increased Se concentration in grain, hull, brown
rice and polished rice compared with spraying water. Se concentration in the grain fractions was in the
following order: Bran > brown rice > whole grain > polished rice > hull. About 13.7% Se in wholegrain
was discarded by milling process if about 6.9% of it was polished as bran. Se-enriched rice could be
produced in naturally seleniferous soils with Se concentration from 0.5 to 1.0 mg kg−1 , and this polished
rice would provide enough Se (60–80 µg day−1 ) to satisfy the human requirement. Therefore, naturally
seleniferous soils may be an effective way to produce Se-enriched rice without spraying Se fertilizer,
which will be more economically feasible and environmentally friendly for without exogenous Se added
to the soils or plants. However, the polished rice and brown rice, produced by spraying Na2 SeO3 (15 g
ha−1 ) or grown in soil with total Se upto 1.5 mg kg−1 was not suitable for daily human consumption,
unless diluted with Se-deficient rice to meet the standard (≤0.3 mg Se kg−1 ). This study imparted a
better understanding of the utilization of seleniferous soils and Se-enriched rice for human health and
food safety.
Keywords: rice Oryza sativa L.; selenium; distribution; accumulation; polished rice
1. Introduction
Selenium (Se) is considered as an essential micronutrient for animals and humans [1–3], and has
an important role in improving the immune system and reducing the risk of cancer [2–4]. However, Se
deficiency is an important cause of some human diseases, including Keshan disease and Kaschin-Beck
disease [5]. The recommended level of Se recommended by the World Health Organization (WHO) for
adults is 40 µg day−1 [3,6,7]. However, in many regions in China, the daily Se intake of people is lower
than the suggested level [3], and its levels in some Se-deficient areas are less than 10 µg day−1 [8].
People could acquire Se from their diet to reduce the occurrence of diseases related to Se deficiency,
as previously reported [3,9]. Rice (Oryza sativa L.) is a staple food in many countries, particularly in
China [3,10]. Nevertheless, Se concentration in rice is too low to meet the people’s daily demand in
Sustainability 2019, 11, 520; doi:10.3390/su11020520
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many countries, including many areas in China [10,11]. Se concentration in rice varies according to
Se status of the paddy soil. The rice grown in soil with Se concentration within the range of 0.5 to
47.7 mg kg−1 could produce Se in wholegrain ranged from 0.084 to 9.67 mg kg−1 [3]. Some field
experiments have indicated that Se concentration in rice grain can be significantly increased by spraying
Se fertilizers [8,12,13]. However, this method is associated with high costs, and exogenous Se spraying
may cause soil and water pollution [10,14,15]. Therefore, the production of high-Se food under natural
Se-rich soil may be an effective Se biofortification scheme.
The accumulation of Se in the edible parts of the plant depends on Se concentration in soil and the
Se distribution in plant organs [3,9]. Evidence indicated that rice grain accumulated more Se in high-Se
soils than that in the low-Se condition [3]. However, when plants were grown in high Se concentration,
the growth was significantly inhibited, even led to death [1,2]. The Se concentration between deficiency
and toxicity is narrow [2], which has a major implication for human health. The upper limitation of Se
intake is 400 µg d−1 for adults recommended by the WHO [16]. The upper standard Se concentration
in cereal for food is 0.3 mg kg−1 in China [3]. For the purpose of this study, a limit of 0.3 mg kg−1 is
also applied to rice grain, including the whole grain, brown rice and polished rice. Therefore, to ensure
the safety of Se in food, understanding Se absorption by the roots, accumulation and distribution
within the rice, is important to predict the Se concentration in grain under seleniferous soils.
The concentration of total Se in soil ranges from less than 0.1 mg kg−1 to more than 100 mg
kg−1 [17]. In general, 0.1 to 0.6 mg kg−1 total Se in soil is considered deficient [18]. The average Se
content in the soil of Shitai district, Chizhou city, Anhui province, China, is 0.67 mg kg−1 , which is
categorized as medium-high Se content in China [19]. Se concentration in rice varies depending on the
Se concentration in which rice is grown [3,14]. Currently, only few pieces of research have focused
on Se accumulation and distribution in rice plant and the grain fractions [3], especially in natural
seleniferous soils. Therefore, understanding the amount of Se stored in the different components of the
grain and detecting the absolute loss of Se during the dehusking process of rice are of great importance.
To understand the accumulation and distribution of Se in rice, a local rice variety “Wandao
205” was selected and planted in three different levels of naturally seleniferous soil of Shitai district,
Chizhou city, Anhui province, China. And the effect of exogenous Se on yield and Se concentration in
rice grain was also investigated by exogenous Se spraying. This study aimed to confirm the suitable Se
concentration range of the soil for achieving Se-enriched rice and to elucidate the correlations between
Se concentration in rice and the seleniferous soils.
2. Material and Methods
2.1. Experimental Site and Growth Conditions
Two pot experiments were carried out in this study, including experiment of seleniferous soil
(Exp. 1) and the experiment of exogenous Se application (Exp. 2). The experiments were conducted
under greenhouse conditions in major rice-growing areas of Anhui province, China [20]. Rice (O.
sativa) cultivar “Wandao 205” was used in this study.
Experiment. 1: Three paddy soils with different Se concentrations (0.50, 0.97, and 1.47 mg Se kg−1 )
were selected to investigate the effect of naturally seleniferous soil on yield and Se content of rice in this
study. Before the present study, selenium content in paddy soils was investigated by collecting 22 surface
soil (0–20 cm) samples in Shitai county, Anhui province in 2011. The total Se content in soil was between
0.31 and 1.99 mg kg−1 , with an average of 0.60 mg kg−1 in all soil samples. Soil Se concentration was
measured following the methods of Sun et al. [3]. Two pots were used for one treatment. A randomized
block design with three replicates was used in the experiment. Therefore, 6 pots were included in
each treatment.
Experiment. 2: Exogenous application of Se was conducted by spraying on rice plants grown in paddy
soil with low Se concentration (0.31 mg Se kg−1 ). The Se applied was Na2 SeO3 with the concentrations
of 0 and 15 mg L−1 (at a rate of 15 g Na2 SeO3 ha−1 , i.e., 3 mL for one hill). The Na2 SeO3 was sprayed at
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the heading stage of rice (50 d before maturity). For 0 mg Na2 SeO3 L−1 treatment, the rice plants were
sprayed with distilled water. Two pots were used for each treatment, and three replicates were used.
Rice seedlings (three-leaf stage) were transplanted to experimental pot (35 cm of diameter, 28 cm
of height) containing 15 kg of different naturally seleniferous soils on 1 August 2012. Two rice seedlings
per hill were transplanted with space of 20 cm × 15 cm. Four hills were contained in one experimental
pot. Two pots were used for one treatment. Three replicates were used. Therefore, 6 pots (total 24 hills)
were contained for each treatment. The basal fertilizer (60 kg N ha−1 , 30 kg P2 O5 ha−1 , 45 kg K2 O
ha−1 ) was applied before transplanting, and the first top-dressing (15 kg N ha−1 and 15 kg K2 O ha−1 )
and second top-dressing (15 kg N ha−1 and 15 kg K2 O ha−1 ) was applied at 20 d and 40 d after
transplanting, respectively. The temperature was 25–33 ◦ C for daytime and 15–23 ◦ C for night-time,
with a relative humidity of 60%–85% in the greenhouse during the experiment. The physicochemical
properties of the experimental soils were provided in Table 1.
Table 1. Main physicochemical properties of the experimental soils.
Experiments
Treatments
pH
2.5:1
Organic Matter
(g kg−1 )
Available N
(mg kg−1 )
Available P
(mg kg−1 )
Available K
(mg kg−1 )
Exp. 1
Low-Se
Middle-Se
High-Se
4.8
4.9
4.7
19.4
22.6
33.3
117.1
120.4
153.9
44.3
81.2
51.1
249.0
285.5
301.7
Exp. 2
Spraying water
Spraying Se
4.9
22.2
130.9
50.4
251.2
Note: Spraying Se: Na2 SeO3 was applied with the concentrations of 15 mg L−1 at the heading stage of rice.
2.2. Grain Yield and Yield Components
At harvest, rice plants were separated into roots, straws and grains. The straws and roots were cleaned
and dried at 60 ◦ C to a constant weight. The grains were air dried at room temperature, and weighed.
The number of panicles, spikelets per panicle, filling rate, and 1000 seed weight, were also scored [21].
2.3. Total Se Analysis
The grain parts were dehusked by a roller sheller (SY2001-NSART100, SANGYONG, Korea),
and were divided into hull and brown rice. A portion of the brown rice was milled into polished rice
and rice bran using a rice polisher (Kett Electric Laboratory, Tokyo, Japan) [22]. The grain and its four
fractions (i.e., hull, brown rice, bran, and polished rice) were dried at 60 ◦ C to a constant weight [22].
All plant samples, including the root and straw, were milled into powder with a DFY-1000C mixer mill
(Shanghai Bilon Instrument, Shanghai, China).
Se concentration of the samples was determined by the method of Gao et al. [23] and Zhou et al. [24]
The dried powders of all samples (0.5 g) were digested by 10 mL HNO3 :HClO4 (9:1) in a polypropylene
sample tube at room temperature overnight. Then, the digestion solution was heated at 60 ◦ C and 100 ◦ C
for 2 h and 1 h, respectively. The addition of 10 mL of HNO3 :HClO4 (9:1) in the tube was maintained
at 170 ◦ C to generate white fume and till the white fume was completely out. The tubes were allowed
to cool, and then added 5 mL of HCl (1:1) and maintained at least for 3 h until it became colorless.
After cooling, the digests were filtered and added with deionized water to 50 mL. The digest solutions
were determined for Se concentration using an inductively coupled plasma mass spectrometry (ICP-MS) [X
Series ICP-MS (Thermo Electron Corporation, Waltham, MA, USA)] [25,26]. During the digestion procedure
and measurement, a reagent blank and standard reference material [GBW10010(GSB-1) (polished rice) [27],
purchased from Institute of Geophysical and Geochemical Exploration, Chinese Academy of Geological
Sciences, Langfang, Hebei, China] were used to validate the accuracy and precision. The average recovery
of Se was between 95% and 98% [26]. All materials were determined in three replicates. All the above
reagents used in the experiment were super pure grade.
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2.4. Statistical Analysis
Data were analyzed using ANOVA and Duncan’s multiple range test at P < 5% with SPSS
13.0 software (SPSS Inc., Chicago, IL, USA). Figures were drawn using Microsoft Excel 2013.
3. Results
3.1. Grain Yield and Its Components
Se concentration in soil significantly affected the grain yield of rice (Figure 1A). Grain yield
in high-Se treatment was significantly lower than that in middle-Se treatment. However, foliar
application of Se did not significantly affect the grain yield compared with spraying water (Figure 1B).
As shown in Figure 2, the panicle number of panicles decreased as the Se concentration in soil increased.
However, no significant difference among the treatments was detected. By contrast, compared with
that of the low-Se treatment, the spikelets per panicle, filling rate and 1000-seed weight were all slightly
increased in the middle-Se treatment, but decreased in the high-Se treatment (Table 2).
ab
120
150
A
a
b
90
60
30
0
Low-Se
B
a
a
Spraying water
Spraying Se
120
Ggrain yield (g/pot)
Ggrain yield (g/pot)
150
Middle- Se
90
60
30
0
High-Se
Figure 1. Grain yield of rice under different naturally seleniferous soils (A) and foliar of Se application (B).
Columns withed different lowercase letters indicate a significant difference (P < 5%).
12
150
a
a
a
9
6
3
0
100
Low-Se
ab
Middle- Se
High-Se
a
b
60
40
20
0
120
Low-Se
Middle- Se
High-Se
ab
a
b
90
60
30
0
Low-Se
Middle- Se
High-Se
b
a
ab
Low-Se
Middle- Se
High-Se
30
1, 000 seed weight (g)
Filling rate (%)
80
Spikelets per panicle (count)
Pancile number per hill (count)
15
24
18
12
6
0
Figure 2. Analysis of seed production parameters in different soil Se concentrations of treated plants.
Columns with different lowercase letters indicate a significant difference (P < 5%).
−
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3.2. Se Concentration and Coefficient of Accumulation in Rice Plants
The increasing levels of Se in soil significantly increased (P < 5%) the concentration of Se in the
root, straw, and grain (Table 2). However, Se concentration in root was significantly higher than that in
straw and grain under the same treatment. In general, Se concentration in the rice plant fractions was
in the following order: Root > straw > grain. For example, under high-Se treatment, Se concentration
in root reached up to 2.72 mg kg−1 , which was 4.9 and 8.2 times of that in straw and grain, respectively.
Both the coefficient of Se accumulation in straw and grain were highest in low-Se treatment, which
were significantly higher than that of middle-Se and high-Se treatments (Table 2).
Table 2. Se concentration and coefficient of accumulation in different organs of rice plants under
different treatments.
Se Concentration (mg kg−1 )
Treatment
Low-Se
Middle-Se
High-Se
Coefficient of Accumulation
Root
Straw
Grain
Straw
Grain
1.16 c
1.68 b
2.72 a
0.30 c
0.38 b
0.56 a
0.16 c
0.21 b
0.33 a
0.59 a
0.38 b
0.37 b
0.32 a
0.21 b
0.22 b
Coefficient of accumulation was presented as ratio of plants Se/soil Se concentration. Within rows, values for the
different Se level followed by different lowercase letters indicate a significant difference (P < 5%).
3.3. Relationship between Se Concentration in Soil and the Rice Plants
As shown in Figure 3, Se concentrations in the root, straw, and grain were significantly positively
correlated with Se concentration in naturally seleniferous soil, and the R2 values was 0.9691, 0.9287 and
0.9544, respectively. The amount of absorbed Se in the root, straw, and grain was closely associated
with Se concentration in the seleniferous soil.
Se concentration (mg kg−1 DW)
3.0
Root 0.8
Shoot 0.4
0.6
0.3
0.4
0.2
2.4
Grain
1.8
1.2
y = 1.5179x + 0.4413
R² = 0.9691
0.6
0.0
0.0
0.5
1.0
1.5
2.0
y = 0.2509x + 0.1779
R² = 0.9287
0.2
0.0
0.0
0.5
1.0
1.5
Se concentration of soil (mg
y = 0.165x + 0.0781
R² = 0.9544
0.1
2.0
0.0
0.0
0.5
1.0
1.5
2.0
kg−1)
Figure 3. Relationship between Se concentration in naturally seleniferous soil and Se concentration in
different parts of rice. Data were the means of three replicates.
3.4. Se concentration in Different Fractions of Rice Grain
As shown in Figure 4, Se concentration in the grain, hull, brown rice, bran, and polished rice was
significantly increased with increasing Se in seleniferous soil (P < 5%). Se concentration of polished
rice (0.32 mg kg−1 ) in the high-Se treatment was 2.1 and 1.6-fold higher than those in low-Se and
−
middle-Se soils, respectively. Likewise, Se concentration of brown rice (0.35 mg kg−1 ) in high-Se
−
treatment was 1.1 and 0.5-fold higher than those in low-Se and middle-Se treatments, respectively.
Under the same treatment, Se concentration in the grain fractions was in the following order: Bran
−
−
−
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Se concentration (mg kg−1 DW)
> brown rice > whole grain > polished rice > hull. As shown in Figure 5, spraying Se significantly
increased Se concentration in the grain, hull, brown rice and polished rice compared with spraying
water treatment. The Se concentration in brown rice and polished rice was 0.55 and 0.51 mg kg−1
under spraying Se treatment, respectively, which was significantly higher than that in spraying water
treatment (0.11 mg kg−1 in brown rice and 0.10 mg kg−1 in polished rice). Similar to seleniferous soil
treatments, for both spraying water and spraying Se treatment, Se concentration in the grain fractions
was in the following order: Brown rice > whole grain > polished rice > hull.
0.8
Low-Se
0.7
Middle-Se
a
High-Se
0.6
b
0.5
0.4
0.3
0.2
a
a
c
a
b
c
a
b
c
b b
c
b
0.1
0.0
Grain
Hull
Brown rice
Bran
Polished rice
Se concentration (mg kg −1 DW)
Figure 4. Selenium concentration in different grain fractions of rice under different naturally
seleniferous soil. Data were the means of three replicates. Columns with different lowercase letters
indicate a significant difference (P < 5%).
0.8
Spraying water
0.7
Spraying Se
0.6
a
a
a
a
0.5
0.4
0.3
0.2
0.1
0.0
b
Grain
b
Hull
b
Brown rice
b
Polished rice
Figure 5. Selenium concentration in different grain fractions of rice under foliar application of Se.
Columns with different lowercase letters indicate a significant difference (P < 5%).
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80
Low-Se
70
Middle-Se
60
a a a
Percentage distribution of Se (%)
Percentage distribution of weight (%)
As shown in Figure 6, the weight percentages for hull, bran, and polished rice were 18.4%, 6.9%,
and 74.6% of the whole grain, respectively. Both the weight percentages for bran and polished rice were
not significantly affected by Se concentration in the naturally seleniferous soils. However, the weight
percentage for hull was higher in high-Se than that in low-Se treatment. The percentage distributions of
Se in the three rice grain fractions were shown in Figure 6. Se accumulation in grain was preferentially
distributed to polished rice (more than 70%), followed by hull or bran. The weight percentage for
hull was 1.7-fold higher than that for bran, while the Se percentage in the hull and bran was nearly
the same.
High-Se
50
40
30
20
b b a
a a a
10
0
Hull
Bran
80
Low-Se
70
Middle-Se
60
a a
a
High-Se
50
40
30
20
a b ab
a a a
Hull
Bran
10
Polished rice
0
Polished rice
Figure 6. Percentage distribution of weight and Se in different fractions of rice grain. Columns with
different lowercase letters indicate a significant difference (P < 5%).
4. Discussion
Selenium is an important element for human and animal nutrition. However, Se is not considered
essential for plants [1,28]. Based on reports, when plants were grown in high Se concentration,
the growth would exhibit symptoms of injury, even led to death [1,2,29,30]. In the present study,
we studied the effect of Se on the plant growth and Se concentration of rice under difference naturally
seleniferous soils. In this study, the spikelets per panicle and filling rate of rice under high-Se were
significantly lower than that in middle-Se treatment, and the grain yield (GY) was significantly higher
in middle-Se treatment than that in high-Se treatment (Figure 1). The grain yield was mainly affected
by four components, including panicles per plant, spikelets per panicle, filling rate and total seed
weight [21,31]. Although the difference was not significant, GY of high-Se was 12% lower than that of
low-Se treatment. Accordingly, the spikelets per panicle was of high-Se was 7% and 12% lower than
that of low-Se and middle-Se treatment, respectively. Therefore, high-Se in soil affected the GY of rice
mainly by reducing the spikelets per panicle of rice. Our results are different with those found by
Hu et al. [32], which showed no significant biomass difference in root, straw and grain of rice under
−1 soil concentration by applying exogenous Se. The effect of spraying Se on
0.2, 0.7 and 1.2 mg
− Se kg
rice grain yield was also investigated in the present study. The grain yield did not significantly affect
by spraying Se, and the spikelets per panicle, filling rate and 1000-seed weight were not significantly
affected by spraying Na2 SeO3 with the concentration of− 0 and 15 mg L−1 . The difference results
may be due to the differences in selenium concentrations and the morphologies of Se in the soil [31].
Therefore, more studies should be conducted, in order to investigate the effect of exogenous Se added
in soils and naturally seleniferous soils on plant growth and development.
In the present study, there were large differences in the concentrations of organic matter,
and available nitrogen, phosphorus and potassium among different kinds of experimental soils.
It was reported that soil fertility, particularly organic matter, is the basis for high rice yield in paddy
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soil [33]. Moreover, the application of nitrogen and phosphorus fertilizer pays an important role in a
high yield of rice [34,35]. High-Se obtained the lowest rice yield, spikelets per panicle and filling rate
in all treatments, although the organic matter, available nitrogen and available potassium in high-Se
soil were higher than that in low-Se and middle-Se soil. Therefore, our results suggested that selenium
content in soil significantly affected rice yield, and the negative effects of high selenium on yield did
not alleviate by higher soil organic matter, nitrogen and potassium in high-Se soil. Taken together,
it suggests that the main physical and chemical properties in soils generally improved for plant growth
(Table 1), however, it implies that 1.5 mg Se kg−1 in the naturally seleniferous soil is probably too
high to maintain rice GY, and it also implies that Se level plays leading role compared with the other
parameters. However, it is unclear whether the inhibition of Se on plant growth can be alleviated by
significantly increasing nitrogen and organic matter in soils, which may require further research.
Rice accumulated different Se content in different plant tissues. Some studies have been conducted to
compare the uptake among the tissues of plants [15,36]. However, the mechanism of Se absorption and
accumulation in rice plants under different Se levels in the soil are still unclear [15]. As shown in Table 2,
Se concentration in rice plant tissues was in the following order: Root > straw > grain. Se concentration
in the root, straw, and grain was increased significantly (P < 5%) with increasing concentrations of Se
in the natural seleniferous soil. Similar results obtained in rice plants were reported by Sun et al. [3].
A previous study has also illustrated that Se concentration in rice plant tissues was positively associated
with the available Se concentration of Se-deficient paddy soils [37]. Moreover, Se concentrations in different
grain fractions were quite different. The rice grain is composed of four fractions, including hull, bran,
and polished rice (endosperm) [3,22]. Under the same treatment, Se concentration in the grain fractions
was following order: Bran > brown rice > whole grain > polished rice > hull (Figure 4). And a similar
result was detected in both the spraying Se and the spraying water treatment (Figure 5). Our result was
slightly different from that obtained by Sun et al. [3]. Nevertheless, Sun et al. [3] also agreed with the order:
Bran > whole grain > polished rice. Other research has also indicated that Se concentration in bran was
higher than that in polished rice (endosperm) [2,3,11].
In this study, Se-enriched rice grain (0.16–0.33 mg Se kg−1 ) can be produced in naturally seleniferous
soils (0.5–1.5 mg Se kg−1 ). Se-enriched food is an efficient resource for human dietary Se intake [11,38].
However, under high-Se treatment, Se concentration in polished rice and brown rice was 0.32 and 0.35 mg
kg−1 (Figure 4), respectively, which was higher than the maximum standard of Se concentration (0.3 mg
kg−1 ) in cereal [3]. The tolerable upper Se intake level recommended by the WHO for adults is 400 µg
day−1 [16]. The polished rice and brown rice, which were grown in paddy soil with total Se up to 1.5 mg
kg−1 , were not suitable for daily consumption of humans, unless diluted with Se-deficient rice to meet the
standard (≤0.3 mg Se kg−1 ) [3]. Lots of studies showed that Se-enriched rice was achieved by spraying Se
fertilizer [38]. The experiment of exogenous Se application also found that Se concentration in brown rice
and polished rice reached 0.55 and 0.51 mg kg−1 by spraying Se (Figure 5). However, Se concentration
in polished rice and brown rice considerably exceeded 0.3 mg kg−1 . In order to achieve Se-enriched rice
within the standard of Se concentration (0.3 mg kg−1 ) by spraying Se, more studies should be carried to
investigate optimal spray concentration of Se. Nonetheless, our results suggested that Se-enriched rice
could be produced in natural conditions in the study area, which will be more feasible and environmentally
friendly as exogenous Se pollution is avoided.
Understanding the percentage distributions of Se in the different fractions of the grain is important
for the efficient use of rice. The weight percentages for the hull, bran, and polished rice were 18.4%, 6.9%,
and 74.6% of the total whole grain, respectively, while the Se percentages were 14.3%, 13.7%, and 71.9%,
respectively (Figure 6). Rice bran is very popular for nutrition because it’s rich in lipid, protein, vitamin,
and dietary fiber [3,39,40]. We found that Se concentration in bran was 2.0-fold and 1.8-fold of polished
rice and brown rice under the same treatment, respectively (Figure 4). The present study suggested that
13.7% Se in the wholegrain will be discarded by the milling process if 6.9% of it was polished as bran,
which will reduce the Se value of the rice grain. Therefore, the bran is very important for Se intake, due to
its characteristic enrichment of Se, and can be used for Se-enriched food resources.
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5. Conclusions
In summary, the rice grown on the naturally seleniferous soil with suitable Se concentration
(1.0 mg kg−1 ) showed a high grain yield; however, 1.5 mg Se kg−1 in natural soil is inappropriate
for getting optimum rice production in this study. Under the same naturally seleniferous soils, root
accumulated higher Se than straw and grain. Se concentration in the grain fractions was in the
following order: Bran > brown rice > whole grain > polished rice > hull. Se-enriched rice could be
produced in naturally seleniferous soils with Se concentration from 0.5 to 1.0 mg kg−1 , and this polished
rice would provide enough Se (60–80 µg d−1 ) to satisfy the human requirement. However, both the
brown rice and polished rice, produced by spraying Na2 SeO3 (15 g ha−1 ) or grown in paddy soil
with total Se up to 1.5 mg kg−1 , was not suitable for daily human consumption, unless diluted with
Se-deficient rice to meet the standard (≤0.3 mg Se kg−1 ).
Author Contributions: J.S., Y.Y. and C.J. performed the experiments; C.J. and C.Z. designed the research; J.S. and
C.J. collected and analyzed data, and wrote the paper; C.J. and C.Z. revised the manuscript.
Funding: This work was jointly supported by 2012 and 2014 Dean Younth Innovation Fund of Anhui Academy of
Agricultural Sciences (12B0919, 14B0945).
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
Terry, N.; Zayed, A.M.; de Souza, M.P.; Tarun, A.S. Selenium in higher plants. Annu. Rev. Plant Physiol. 2000,
51, 401–432. [CrossRef]
Zhu, Y.G.; Pilon-Smits, E.A.H.; Zhao, F.J.; Williams, P.N.; Meharg, A.A. Selenium in higher plants:
Understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci. 2009, 14, 436–442.
[CrossRef] [PubMed]
Sun, G.X.; Liu, X.; Williams, P.N.; Zhu, Y.G. Distribution and translocation of selenium from soil to grain and
its speciation in paddy rice (Oryza sativa L.). Environ. Sci. Technol. 2010, 44, 6706–6711. [CrossRef] [PubMed]
Li, H.F.; McGrath, S.P.; Zhao, F.J. Selenium uptake, translocation and speciation in wheat supplied with
selenate or selenite. New Phytol. 2008, 178, 92–102. [CrossRef] [PubMed]
Li, S.; Xiao, T.; Zheng, B. Medical geology of arsenic, selenium and thallium in China. Sci. Total Environ. 2013,
421–422, 31–40. [CrossRef] [PubMed]
Combs, G.F., Jr. Selenium in global food systems. Br. J. Nutr. 2001, 85, 517–547. [CrossRef] [PubMed]
Abdulah, R.; Miyazaki, K.; Nakazawa, M.; Koyama, H. Low contribution of rice and vegetables to the daily
intake of selenium in Japan. Int. J. Food Sci. Nutr. 2005, 56, 463–471. [CrossRef]
Chen, L.; Yang, F.; Xu, J.; Hu, Y.; Hu, Q.; Zhang, Y.; Pan, G. Determination of selenium concentration of rice
in china and effect of fertilization of selenite and selenate on selenium content of rice. J. Agric. Food Chem.
2002, 50, 5128–5130. [CrossRef]
Navarro-Alarcon, M.; Cabrera-Vique, C. Selenium in food and the human body: A review. Sci. Total Environ.
2008, 400, 115–141. [CrossRef]
Liu, k.; Gu, Z. Selenium accumulation in different brown rice cultivars and its distribution in fractions.
J. Agric. Food Chem. 2009, 57, 695–700. [CrossRef]
Williams, P.N.; Lombi, E.; Sun, G.X.; Scheckel, K.; Zhu, Y.G.; Feng, X.B.; Zhu, J.M.; Carey, A.M.; Adomako, E.;
Lawgali, Y.; et al. Selenium characterization in the global rice supply chain. Environ. Sci. Technol. 2009, 43,
6024–6030. [CrossRef] [PubMed]
Hu, Q.; Chen, L.; Xu, J.; Zhang, Y.; Pan, G. Determination of selenium concentration in rice and the effect of
foliar application of Se-enriched fertiliser or sodium selenite on the selenium content of rice. J. Sci. Food Agric.
2002, 82, 869–872. [CrossRef]
Fang, Y.; Wang, L.; Xin, Z.; Zhao, L.; An, X.; Hu, Q. Effect of foliar application of zinc, selenium, and iron
fertilizers on nutrients concentration and yield of rice grain in China. J. Agric. Food Chem. 2008, 56, 2079–2084.
[CrossRef] [PubMed]
Zhang, L.H.; Shi, W.M.; Wang, X.C. Difference in selenium accumulation in shoots of two rice cultivars.
Pedosphere 2006, 16, 646–653. [CrossRef]
Sustainability 2019, 11, 520
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
10 of 11
Zhang, L.H.; Shi, W.M.; Wang, X.C. Difference in selenite absorption between high- and low-selenium rice
cultivars and its mechanism. Plant Soil 2006, 282, 183–193. [CrossRef]
Huang, Y.; Wang, Q.; Gao, J.; Lin, Z.; Bañuelos, G.S.; Yuan, L.; Yin, X. Daily dietary selenium intake in a high
selenium area of Enshi, China. Nutrients 2013, 5, 700–710. [CrossRef] [PubMed]
Xing, K.; Zhou, S.; Wu, X.; Zhu, Y.; Kong, J.; Shao, T.; Tao, X. Concentrations and characteristics of selenium in
soil samples from Dashan Region, a selenium-enriched area in China. Soil Sci. Plant Nutr. 2015, 61, 889–897.
[CrossRef]
Lyons, G.; Stangoulis, J.; Graham, R. High-selenium wheat: Biofortification for better health. Nutr. Res. Rev.
2003, 16, 45–60. [CrossRef]
Jiang, C.Q.; Shen, J.; Xu, J.N.; Shao, F.W.; Li, T.; Zu, C.L. Effects of Se-enriched soils on the plant growth,
selenium uptake and transport in flue-cured tobacco. Acta Bot. Boreal.-Occident. Sin. 2014, 34, 2303–2308.
Jiang, C.Q.; Zu, C.L.; Shen, J.; Shao, F.W.; Li, T. Effects of selenium on the growth and photosynthetic
characteristics of flue-cured tobacco (Nicotiana tabacum L.). Acta Soc. Bot. Pol. 2015, 84, 71–77. [CrossRef]
Kim, E.H.; Kim, Y.S.; Park, S.H.; Koo, Y.J.; Choi, Y.D.; Chung, Y.Y.; Lee, I.J.; Kim, J.K. Methyl jasmonate
reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol. 2009, 149,
1751–1760. [CrossRef] [PubMed]
Lu, L.; Tian, S.; Liao, H.; Zhang, J.; Yang, X.; Labavitch, J.M.; Chen, W. Analysis of metal element distributions
in rice (Oryza sativa L.) seeds and relocation during germination based on X-ray fluorescence imaging of Zn,
Fe, K, Ca, and Mn. PLoS ONE 2013, 8, e57360. [CrossRef] [PubMed]
Gao, J.; Liu, Y.; Huang, Y.; Lin, Z.Q.; Bañuelos, G.S.; Lam, M.H.W.; Yin, X. Daily selenium intake in a moderate
selenium deficiency area of Suzhou, China. Food Chem. 2011, 126, 1088–1093. [CrossRef]
Zhou, X.B.; Shi, W.M.; Zhang, L.H. Iron plaque outside roots affects selenite uptake by rice seedlings (Oryza
sativa L.) grown in solution culture. Plant Soil 2007, 290, 17–28. [CrossRef]
Fang, Y.; Zhang, Y.F.; Catron, B.; Chan, Q.L.; Hu, Q.H.; Caruso, J.A. Identification of selenium compounds
using HPLC-ICPMS and nano-ESI-MS in selenium-enriched rice via foliar application. J. Anal. At. Spectrom.
2009, 24, 1657–1664. [CrossRef]
Feng, Y.M.; Xing, Y.X.; Liu, H.Q.; Zhang, Y. Determination of trace selenium in biological samples by
inductively coupled plasma-mass spectrometry with microwave digestion. Rock Miner. Anal. 2014, 33, 34–39.
Liu, H.; Zhang, J.; Christie, P.; Zhang, F. Influence of iron plaque on uptake and accumulation of Cd by rice
(Oryza sativa L.) seedlings grown in soil. Sci. Total Environ. 2008, 394, 361–368. [CrossRef]
Kápolna, E.; Hillestrøm, P.R.; Laursen, K.H.; Husted, S.; Larsen, E.H. Effect of foliar application of selenium
on its uptake and speciation in carrot. Food Chem. 2009, 115, 1357–1363. [CrossRef]
Hasanuzzaman, M.; Hossain, M.A.; Fujita, M. Selenium in higher plants: Physiological role, antioxidant
metabolism and abiotic stress tolerance. J. Plant Sci. 2010, 5, 354–375.
Ślusarczyk, J.; Kuraś, M.; Malinowska, E.; Skalicka-Woóniakd, K.; Głowniakd, K. Ultrastructural changes
in themycelium of Hericium erinaceum (Bull.; Fr.) Pers. under selenium-induced oxidative stress. J. Sci.
Food Agric. 2014, 94, 2718–2725. [CrossRef]
Jeng, T.L.; Tseng, T.H.; Wang, C.S.; Chen, C.L.; Sung, J.M. Yield and grain uniformity in contrasting rice
genotypes suitable for different growth environments. Field Crop Res. 2006, 99, 59–66. [CrossRef]
Hu, Y.; Huang, Y.; Huang, Y.; Liu, Y.; Liang, J. Effect of selenium on the uptake and translocation of
manganese, iron, phosphorus and selenium in rice (Oryza sativa L.). Environ. Sci. 2013, 34, 4119–4125.
Peng, W.F.; Lv, W.S.; Huang, S.; Zeng, Y.J.; Pan, X.H.; Shi, Q.H. Effects of soil Fertility on rice yield and
nitrogen use efficiency in a red paddy soil. Sci. Agric. Sin. 2018, 51, 3614–3624.
Wang, W.N.; Wei, J.L.; He, Y.Q.; Li, X.K.; Li, H. Effects of N, P, K fertilizer application on grain yield, quality,
nutrient uptake and utilization of rice. Chin. J. Rice Sci. 2011, 25, 645–653.
Si, L.; Xie, Y.; Ma, Q.; Wu, L. The Short-term effects of rice straw biochar, nitrogen and phosphorus fertilizer
on rice yield and soil properties in a cold waterlogged paddy field. Sustainability 2018, 10, 537. [CrossRef]
Zayed, A.; Lytle, C.M.; Terry, N. Accumulation and volatilization of different chemical species of selenium
by plants. Planta 1998, 206, 284–292. [CrossRef]
Cao, Z.H.; Wang, X.C.; Yao, D.H.; Zhang, X.L.; Wong, M.H. Selenium geochemistry of paddy soils in Yangtze
River Delta. Environ. Int. 2001, 26, 335–339. [CrossRef]
Sustainability 2019, 11, 520
38.
39.
40.
11 of 11
Carey, A.; Scheckel, K.G.; Lombi, E.; Newville, M.; Choi, Y.; Norton, G.J.; Price, A.H.; Meharg, A.A.
Grain accumulation of selenium species in rice (Oryza sativa L.). Environ. Sci. Technol. 2012, 46, 5557–5564.
[CrossRef] [PubMed]
Kim, J.S.; Godber, J.S.; Prinaywiwatkul, W. Restructured beef roasts containing rice bran oil and fiber
influences cholesterol oxidation and nutritional profile. J. Muscle Foods 2000, 11, 111–127. [CrossRef]
Kim, M.K.; Yu, K.W.; Kang, D.H.; Koh, J.H.; Hong, B.S.; Suh, H.J. Anti-stress and anti-fatigue effects of
fermented rice bran. Biosci. Biotechnol. Biochem. 2001, 65, 2294–2296. [CrossRef]
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