Environmental Pollution 265 (2020) 114890

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Influences of high-level atmospheric gaseous elemental mercury on

methylmercury accumulation in maize (Zea mays L.)*
Ting Sun a, b, Zhangwei Wang a, c, *, Xiaoshan Zhang a, c, Zhenchuan Niu d, Jian Chen a
a
State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China
b
Western University, Ontario, N6A 3K7, Canada
c
University of Chinese Academy of Sciences, Beijing, 100049, China
d
Institute of Earth Environment, Chinese Academy of Science, Xi’an, 710061, China

a r t i c l e i n f o a b s t r a c t

Article history: Maize (Zea mays L.) leaves play an important role in stomatal uptake and surface adsorption of atmo-
Received 28 February 2020 spheric mercury (Hg). However, the influence of atmospheric gaseous elemental mercury (GEM) on
Received in revised form methylmercury (MeHg) accumulation in maize plants is poorly understood. In this study, we conducted a
26 May 2020
field open-top chambers (OTCs) experiment and a soil Hg-enriched experiment to investigate the
Accepted 27 May 2020
Available online 9 June 2020
response of MeHg accumulation in maize tissues to different GEM levels in the air. Maize upper leaves
had a higher average MeHg concentration (0.21 ± 0.08 ng g
1) than bottom leaves (0.15 ± 0.05 ng g
1) in
the OTCs experiment, which was inconsistent with that in the soil Hg-enriched experiment (maize upper
Keywords:
Maize
leaves: 0.41 ± 0.07 ng g
1, maize bottom leaves: 0.60 ± 0.05 ng g
1). Additionally, significantly positive
Atmospheric gaseous elemental mercury correlations were found between MeHg concentrations in maize leaves and air Hg levels, suggesting that
Methylmercury elevated air Hg levels enhanced MeHg accumulation in maize leaves, which was possibly attributed to
Accumulation methylation of Hg on leaf surfaces. Mature maize grains from the OTCs experiment had low MeHg
concentrations (0.12e0.23 ng g
1), suggesting a low accumulation capability of MeHg by maize grains.
Approximately 93e96% of MeHg and 51e73% of total Hg in maize grains were lost from the grain-filling
stage to the grain-ripening stage at all GEM level treatments, implying that self-detoxification in maize
grains occurred. MeHg concentrations in maize roots showed a significant linear relationship (R2 ¼ 0.98,
p < 0.01) with soil Hg levels, confirming that MeHg in maize roots is primarily from soil. This study
provides a new finding that elevated air GEM levels could enhance MeHg accumulation in maize leaves,
and self-detoxification may occur in maize grains. Further studies are needed to clarify these mecha-
nisms of Hg methylation on maize leaf surfaces and self-detoxification of Hg by maize grains.
© 2020 Published by Elsevier Ltd.

1. Introduction
Mercury (Hg) is a highly toxic pollutant, which has been a global
concern for decades due to its ability to methylate, bioaccumulate,
Abbreviations: Hg, mercury; MeHg, methylmercury; GEM, gaseous elemental
mercury; OTCs, open-top chambers; RGM, reactive gaseous mercury; PBM, partic-
ulate-bound mercury; THg, total mercury; SRB, sulfate-reducing bacteria; FeRB,
iron-reducing bacteria; RS, ripening stage; GFS, grain-filling stage; IHg, inorganic
mercury; CRM, certified reference materials; u-leaf, upper leaf; b-leaf, bottom leaf;
u-stem, upper stem; b-stem, bottom stem.
*
This paper has been recommended for acceptance by Jo €rg Rinklebe.
* Corresponding author. State Key Laboratory of Urban and Regional Ecology,
Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences,
Beijing, 100085, China.
E-mail address: wangzhw@rcees.ac.cn (Z. Wang).
and biomagnify in the food webs (Clarkson and Magos, 2006). Hg
exists in the natural environment, while human activities such as
artisanal gold mining activities, coal combustion, incineration of
medical waste, sewage sludge, and base metal melting increase Hg
emission to the atmosphere at regional and global scales (Beckers
and Rinklebe, 2017; Driscoll et al., 2013; Streets et al., 2009).
Recent global modeling showed that human activities release
approximately 1900e2900 Mg of Hg per year, and this anthropo-
genic source accounts for a third of total global Hg emissions to the
atmosphere (Streets et al., 2009). The massive Hg emissions from
human activities to the environment pose a health threat to
humans and wildlife because Hg can convert to the more bio-
accumulative and neurotoxic methylmercury (MeHg) in anaerobic
soils/sediments by anaerobic microorganisms, such as sulfate-
reducing bacteria (SRB) (Gilmour et al., 1992), iron-reducing

https://doi.org/10.1016/j.envpol.2020.114890
0269-7491/© 2020 Published by Elsevier Ltd.
2 T. Sun et al. / Environmental Pollution 265 (2020) 114890
bacteria (FeRB) (Kerin et al., 2006), methanogenic archaea
(Hamelin et al., 2011), and syntrophic and acetogenic bacteria
(Gilmour et al., 2013). MeHg can rapidly cross the blood-brain and
placental barriers due to its lipid solubility (Clarkson and Magos,
2006), posing a severe threat to human and wildlife health
(Beckers and Rinklebe, 2017).
One primary exposure pathway of MeHg to humans and wildlife
is the dietary consumption of MeHg-contaminated seafood (Harris
et al., 2003). Stein et al. (1996) reported that fish could accumulate
106 times higher of MeHg than ambient water (Stein et al., 1996).
Besides, MeHg can accumulate in the ground vegetation, especially
in the edible parts of crops and vegetables, and is finally accumu-
lated in human bodies via the food chain (Qiu et al., 2008; Zhang
et al., 2010a). For instance, recent investigations showed that rice
(Oryza sativa L.) grown in Hg contaminated soil or atmosphere sites
can accumulate high levels of MeHg (>100 mg kg
1) (Qiu et al.,
2008; Wang et al., 2018; Zhang et al., 2010a), making rice con-
sumption as MeHg exposure pathway to humans (Zhang et al.,
2010a; Zhang et al., 2010b).
Maize (Zea mays L.) is a staple crop around the world due to its
high nutritional and economic value. The production of maize is the
highest among that of major crops (e.g., maize, rice, wheat, and
soybeans), with the average global production (1998e2002): 607
million Mg of maize, 591 million Mg of rice, 586 million Mg of
wheat, and 168 million Mg of soybeans (Lobell et al., 2011; Troyer,
2006). Maize can absorb and accumulate Hg in its edible parts (Fu
et al., 2014; Liu et al., 2004; Niu et al., 2011; Zhao et al., 2017), posing
a potential Hg pathway to humans and livestock by the massive
consumption of maize and its products. Many studies indicated that
maize grains have a low capability in accumulating MeHg (Cui et al.,
2014; Qiu et al., 2008; Sun et al., 2019) because plant roots (except
rice roots (Meng et al., 2011)) can act as a barrier for MeHg trans-
portation to aboveground portions (Debeljak et al., 2013). However,
atmospheric Hg (gaseous elemental mercury (GEM) (>95%), reac-
tive gaseous mercury (RGM: HgBr2, HgCl2, Hg(NO3)2, etc.), and
particulate-bound mercury (PBM)) could be another source of
MeHg for plants except soil Hg (Ericksen et al., 2003; Wang et al.,
2018; Wang et al., 2019). Previous studies, such as natural stable
Hg isotope measurements (Obrist et al., 2017; Sun et al., 2019),
controlled field and lab experiments (Ericksen et al., 2003; Mao
et al., 2013; Niu et al., 2013; Niu et al., 2011; Stamenkovic and
Gustin, 2009), and field investigations (Risch et al., 2012;
Tabatchnick et al., 2012) suggested that plant leaves play an
important role in stomatal absorption and surface adsorption of
atmospheric Hg (Obrist et al., 2017; Wang et al., 2016), and maize is
a significant biospheric sink of atmospheric Hg (Niu et al., 2011; Sun
et al., 2019). Furthermore, some literature showed that in-planta/
on-foliar surface Hg methylation is possible in forest foliage un-
der high atmospheric Hg concentrations (Ericksen et al., 2003;
Tabatchnick et al., 2012). Therefore, it is necessary to clarify the
effects of increased GEM concentrations on MeHg accumulation by
maize with the massive Hg emissions by human activities. This
study aims to evaluate the influences of high-level atmospheric
GEM on MeHg accumulation in maize. We hypothesize that an
elevated GEM concentration could increase MeHg concentration in
maize. To test this hypothesis, we conducted a field open-top
chambers (OTCs) experiment and a soil Hg-enriched experiment.
2. Materials and methods
2.1. Site description
Our experimental site for maize is located in the North China
Plain, a major maize-producing area in China. The field experiment
for maize was performed in a village (38.70 N, 115.23 E) in Wangdu
County, Hebei. The experimental site is far from industrialized and
densely populated areas and has a warm and continental monsoon
climate. Its average annual rainfall and temperature are 555.0 mm
and 12.3  C, respectively. The village has the lowest and highest
monthly mean air temperatures of
4.1  C in January and þ26.5  C
in July, respectively. The site has background Hg levels in air and soil
of 2 ± 1 ng m
3 and 25 ± 6 ng g
1, respectively (Niu et al., 2011).
2.2. OTCs fumigation experiment
A field OTCs fumigation experiment was performed to study the
effect of the elevated GEM levels in the air on MeHg accumulation
in maize tissues. The experiment apparatus was composed of 12
clear open-top chambers, 12 GEM generated systems, and 12 gas
transmission systems (Fig. S1), following the design by Heagle et al.
(1973) (Heagle et al., 1973). Details of the OTCs fumigation exper-
iment design were described in the Supporting Information. The
GEM concentrations in chambers were monitored on-line by a
portable Zeeman Mercury Analyzer RA-915þ (Lumex Inc., Russia) in
the morning, noon, and afternoon every day. The GEM levels in
chambers were adjusted by rotameters to maintain the variation of
GEM levels less than 10%. We established four levels of GEM con-
centrations, 10 ± 1 ng m
3, 20 ± 2 ng m
3, and 50 ± 2 ng m
3 in the
air mixture for the OTCs, as well as a reference condition
(2 ± 1 ng m
3). The design for the reference treatment was as same
as other GEM level treatments, and the difference is that field
ambient gas was pumped into the open-top chambers with no GEM
added in airflow. There were three repetitions for each GEM con-
centration treatment. The chambers were spaced out in 3-m in-
tervals to avoid mutual shading.
2.3. Soil mercury enriched experiment
A soil Hg-enriched experiment was simultaneously conducted
to distinguish the influence of soil Hg on MeHg accumulation in
maize. All Hg-enriched soils were aged for six months after adding
a mercuric chloride (HgCl2) solution. New added Hg in soil was
readily re-emitted to the atmosphere in the first 6 h, followed by a
relatively steady re-emission that only 6% of added Hg would be re-
emitted to the atmosphere annually (Ericksen et al., 2005). The
fractions of new added Hg in soil included residual Hg, active Hg,
alkaline soluble Hg, and acid-soluble Hg. Fractions of active Hg,
alkaline soluble Hg, and acid-soluble Hg were gradually trans-
formed into residual Hg that was the dominant fraction after 6
months. All Hg-enriched soils, therefore, were aged six months
before the cultivation of maize. The Hg-enriched soils were sub-
sequently covered by the reference soil (~2 cm) to reduce the re-
emission of soil Hg. The final soil Hg concentrations were set at
five levels 158 ± 45 ng g
1, 325 ± 59 ng g
1, 496 ± 63 ng g
1 and
763 ± 133 ng g
1, as well as a reference concentration of
25 ± 6 ng g
1 after six months aging. Summer maize (Xianyu 335)
was cultivated in these field experiments. The OTCs experiment
and soil Hg-enriched experiment were from July to October 2010.
2.4. Sample collection and analysis
In the OTCs experiment and soil Hg-enriched experiment, maize
plants were collected in their entirety at the ripening stage (RS).
Maize grains were also collected at the grain-filling stage (GFS) in
the OTCs experiment (about 30 days after pollination or 20 days
before the RS). All plant samples were washed with tap water in situ
followed by further cleaning with deionized water, and then they
were rinsed with ultrapure water in a clean laboratory. Each plant
was segmented into six fractions: grains, upper foliage, bottom
foliage, upper stems with the sheath removed, bottom stems with
 T. Sun et al. / Environmental Pollution 265 (2020) 114890
the sheath removed, and roots. Soil (0e20 cm) samples were
collected both before and after the OTCs and soil Hg-enriched ex-
periments. All soil and plant samples were freeze-dried, ground,
and homogenized. Each fraction was packed into a polyethylene
bag to avoid cross-contamination and stored in a freezer at
4  C.
For the MeHg analyses, plant samples (~0.2 g (d.w.)) were
digested using the KOH-methanol/solvent extraction technique
(Liang et al., 1996), and soil samples (~0.3 g (d.w.)) were prepared
using HNO3 leaching/solvent extraction technique (Liang et al.,
2004). There are two reasons for choosing these two MeHg
extraction techniques: (1) recoveries of MeHg are closed to 100% for
all samples (Liang et al., 1996; Liang et al., 2004), and (2) artifact
MeHg formation could be neglected during MeHg extraction for
low Hg-contaminated samples (<2 u˛ g g
1 Hg(II)) (Hintelmann,
1999; Liang et al., 2004). MeHg in all of the samples was extrac-
ted by methylene chloride followed by back-extraction using
deionized water, aqueous ethylation, and purification, and was
finally trapped onto a Tenax trap. The concentrations of pre-
concentrated MeHg were then determined by gas chromatography-
cold vapor atomic fluorescence spectrometry (GC-CVAFS) using the
USEPA 1630 method.
Ratios of MeHg concentrations in maize grains, stems, and roots
to that in maize leaves (R(i/upper leaves), i ¼ grains, bottom leaves, and
upper and bottom stems) were used to identify possible trans-
location of MeHg from leaves to other tissues in our OTCs experi-
ment. Higher R-value means more MeHg are translocated to this
tissue from maize leaves.
2.5. Statistical analysis and quality control
One-way analyses of variance (One-way ANOVA) were used to
establish the difference for MeHg concentrations in plants among
experimental treatments. Statistical analysis was performed on
Microsoft Office Excel 2010, and statistical significance was
considered at p < 0.05. OriginLab 8.0 (Microcal Software Inc., MA)
was used to process all data and produce the graphs. Data were
presented as mean and standard deviation (mean ± SD).
To ensure the quality of analyses, method blanks, matrix spikes,
triplicates of each sample, and several certified reference materials
were conducted. All procedural blanks were below the method
detection limit (0.008 ng g
1 for MeHg in soil and plant samples).
The relative standard deviation (RSD) was <10% for triplicate
samples. Recoveries of MeHg for matrix spikes and certified refer-
ence material (CRM, IAEA-405) were about 86e113%. The mean
MeHg concentration of CRM was at 5.35 ± 0.46 ng g
1 (n ¼ 9),
Fig. 1. The MeHg concentrations in maize leaves (A) in the OTCs experiment, and (B) in the soil Hg-enriched experiment. u-leaf and b-leaf represent upper leaf and bottom leaf
(hereafter the same), respectively.
3
which was comparable well with the certified MeHg concentration
of 5.49 ± 0.53 ng g
1.
3. Results and discussion
3.1. MeHg accumulation in maize leaves
The MeHg concentrations of maize leaves in the OTCs experi-
ment and the soil Hg-enriched experiment are shown in Fig. 1. The
influences of elevated GEM concentrations on soil MeHg levels
(mean: 0.07 ± 0.01 ng g
1) could be neglected, while soil MeHg
concentrations in the soil Hg-enriched experiment (range:
0.08 ± 0.01 ng g
1
0.91 ± 0.10 ng g
1) were positively correlated to
soil total mercury (THg) levels (Figs. S2 and S3). In the OTCs
experiment, the average MeHg concentrations in maize upper and
bottom leaves were 0.21 ± 0.08 ng g
1 and 0.15 ± 0.05 ng g
1,
respectively, which was inconsistent with those in the soil Hg-
enriched experiment (maize upper leaves: 0.41 ± 0.07 ng g
1,
maize bottom leaves: 0.60 ± 0.05 ng g
1) (Fig. 1). Although MeHg
concentrations in maize leaves were extremely low, One-way
ANOVA showed that MeHg concentration differences between
upper leaves and bottom leaves were still statistically significant
(p < 0.05). THg concentrations in maize tissues were much lower
than 2 u˛ g g
1 (Niu et al., 2011), and the artifacts of MeHg during
MeHg extraction could be neglected (Hintelmann, 1999; Liang et al.,
2004).
In the soil Hg-enriched experiment, the average MeHg con-
centrations in maize leaves were ~2e4 times higher than those
from the OTCs experiment (Fig. 1). One plausible explanation is that
although Hg-enriched soils were aged six months before the
cultivation of maize, a small amount of Hg could still be re-emitted
to the air from the soils (Gao et al., 2020; O’Connor et al., 2019;
Rinklebe et al., 2010; Rinklebe et al., 2009), and then be assimilated
by maize leaves. Hg release could be affected by many factors, such
as soil and atmospheric Hg concentrations (Bahlmann et al., 2006),
meteorological factors (e.g., solar radiation, air temperature, wind
speed, atmospheric pressure) (Gustin et al., 2002), soil temperature
and moisture (Bahlmann et al., 2006; Gustin and Stamenkovic,
2005; O’Connor et al., 2019). Hg release in the soil Hg-enriched
experiment might be readily affected by factors (e.g., wind speed
and air and soil temperature) in the open space than that in the
OTCs experiment. However, Ericksen et al. (2005) reported that
only 6% of new added Hg in soil could be re-emitted to the atmo-
sphere annually after the first 6 h of Hg addition (Ericksen et al.,
2005). Therefore, the effects of this small amount of Hg re-
4 T. Sun et al. / Environmental Pollution 265 (2020) 114890
emission were still very small compared to the high levels of soil
Hg. Another possible reason is that although roots are barriers for
Hg transport from the soil to the aboveground plant tissues, a small
amount of Hg in the roots might still be transported to the
aboveground plant tissues (Cui et al., 2014). MeHg concentrations
in soils and maize roots in the soil Hg-enriched experiment were
~1.14e13.22 times and ~2.64e11.81 times higher than that in the
OTCs experiment, respectively (Figs. S2 and S3; Section 3.3).
Therefore, MeHg concentrations in maize leaves in the soil Hg-
enriched experiment were higher than those from the OTCs
experiment. The same explanations could be applied to maize
grains that higher maize grain MeHg concentrations were found in
the soil Hg-enriched experiment than that in the OTCs experiment
(Fig. S4).
The results of the OTCs experiment showed that MeHg levels in
maize leaves, especially the upper leaves, had significantly positive
correlations with the air GEM concentrations (R2 ¼ 0.96e0.98,
p < 0.05) (Fig. 1A). Combining the above results that the average
MeHg levels in upper maize leaves were higher than that in maize
bottom leaves in the OTCs experiment and lower than that in maize
bottom leaves in the soil Hg-enriched experiment, our study sug-
gested that elevated air GEM levels increased MeHg accumulation
in maize leaves, especially in the upper leaves. There were no sig-
nificant differences of MeHg concentrations (p > 0.05) in maize
leaves under different soil Hg/MeHg concentrations in the soil Hg-
enriched experiment (Fig. 1B and Fig. S5), implying that soil MeHg
is not the dominant Hg source for maize leaves.
Previous field investigations (Fay and Gustin, 2007; Niu et al.,
2013), the OTCs experiment (Niu et al., 2011), stable isotope
tracer experiment (Mao et al., 2013), and natural stable isotope
signatures (Obrist et al., 2017), showed that atmospheric GEM is the
primary source of Hg to the aboveground biomass of vegetation.
Stomata and nonstomatal pathways are two significant routes of
foliar accumulation of Hg from the atmosphere (Stamenkovic and
Gustin, 2009). Atmospheric Hg can be incorporated into the plant
foliage by stomata absorption of gaseous Hg species and by the
surface adsorption of gaseous and particulate Hg species. GEM can
be oxidized by oxides in the atmosphere (e.g., O3, Cl2, Br2, and H2O2)
and on the moisture films at the foliar surfaces to bivalent Hg (Rea
et al., 2001), possibly followed by Hg methylation on the foliar
surfaces or in the inner leaves (Fortmann et al., 1978; Tabatchnick
et al., 2012). The absence of a positive linear relationship between
MeHg concentrations in the maize foliage and the soil suggested
that roots uptake of Hg from the soil is not a significant source of
MeHg accumulation in leaves. The majority of MeHg in maize
Fig. 2. MeHg concentrations in maize stem in the OTCs experiment (A) and the soil Hg-enriched experiment (B). au-stem and b-stem represent upper stem and bottom stem
(hereafter the same), respectively. aThe same letters on the top of columns in each group indicate MeHg values are not significantly different at the 0.05 levels. The same below.
leaves, therefore, was possibly derived from in vivo transformations
of atmospheric Hg (Ding et al., 2011; Ericksen et al., 2003; Fortmann
et al., 1978; Tabatchnick et al., 2012). However, the stable isotope
tracer experiment showed that in-planta methylation is unlikely
(Strickman and Mitchell, 2017). Thus, the MeHg concentration in-
crease in the maize leaves under elevated atmospheric GEM levels
can be partly attributed to Hg methylation on the leaf surfaces.
MeHg in the environment is generally produced by anaerobic
microorganisms, such as SRB (Gilmour et al., 1992), FeRB (Kerin
et al., 2006), methanogenic archaea (Hamelin et al., 2011), and
syntrophic and acetogenic bacteria (Gilmour et al., 2013) in
anaerobic soils/sediments. Abiotic methylation of Hg, however, was
another important MeHg source in aquatic systems, with the dis-
solved organic matter, such as methylcobalamin, methyltin com-
pounds, and acetate as the methyl donors in the dark conditions
(Celo et al., 2006; Siciliano et al., 2005; Yin et al., 2012). Moreover,
solar radiation can also promote MeHg production (Siciliano et al.,
2005; Yin et al., 2012), although much evidence showed solar ra-
diation could increase MeHg degradation in aquatic environments
(Lehnherr and Louis, 2009; Li et al., 2010). No evidence showed
abiotic methylation of Hg or photoproduction of MeHg in vegeta-
tion. Leaf epidermis wax, however, contains many methyl donors
n et al., 2017;
(e.g., acetic acid, alcohol, acetate, and coniferol) (Arago
Domínguez et al., 2011; Falter, 1999; Ferna ndez et al., 2016), that
might provide the possibility for abiotic Hg methylation on the
moisture films at leaf surfaces. Further studies are needed to clarify
the factors controlling Hg methylation on leaf surfaces and to
quantify the relative contributions of atmospheric Hg and soil Hg to
maize tissue MeHg contents.
3.2. MeHg accumulation in maize stems
MeHg concentrations in maize stems are shown in Fig. 2. The
average MeHg concentrations in maize upper and bottom stems in
the OTCs experiment were 0.09 ± 0.02 ng g
1 and
0.03 ± 0.01 ng g
1, respectively, which were similar to that in the
soil Hg-enriched experiment (upper stems: 0.08 ± 0.04 ng g
1,
bottom stems: 0.04 ± 0.02 ng g
1). The average MeHg concentra-
tions in maize stems were the lowest among other tissues in both
the OTCs experiment and the soil Hg-enriched experiment (Fig. S4),
suggesting that maize stems have a lower capability in accumu-
lating MeHg.
Many previous studies showed that trunks could assimilate Hg
from the atmosphere as well as from the soil, and the former may
dominate (Fay and Gustin, 2007; Millhollen et al., 2006). The
 T. Sun et al. / Environmental Pollution 265 (2020) 114890
average Hg concentrations in trunks accounted for no more than
10% of the Hg in the entire plant (Ericksen et al., 2003; Millhollen
et al., 2006). Niu et al. (2011) found a similar trend for crops (Niu
et al., 2011). In our study, there were no significant correlations
between MeHg concentrations of maize stems and air/soil Hg levels
(p > 0.05), while similar MeHg concentrations were found in both
OTCs and soil Hg-enriched experiments, suggesting that MeHg
concentrations in maize stems were affected by both the air and soil
Hg levels. Additionally, maize stems had the lowest MeHg levels in
the entire maize plant, implying that maize stems had the lowest
ability in accumulating MeHg compared to other tissues, which was
consisted with previous studies (Ericksen et al., 2003; Fay and
Gustin, 2007; Niu et al., 2011).
3.3. MeHg accumulation in maize roots
The MeHg concentrations in maize roots are shown in Fig. 3. In
the OTCs experiment, the average MeHg concentrations in maize
roots were 0.11 ± 0.02 ng g
1. The MeHg concentrations in maize
roots did not show significant correlations with air GEM concen-
trations (p > 0.05) (Fig. 3A), indicating that air GEM is not the
principal MeHg source for maize roots. MeHg concentrations in
maize roots in the soil Hg-enriched experiment, however, showed a
significant positive linear relationship with soil Hg concentrations
(R2 ¼ 0.99, p < 0.05) (Fig. 3B), indicating that soil Hg is an important
MeHg source for maize roots. These results further confirmed that
the MeHg in maize roots was primarily from the soil rather than
from the air (Cui et al., 2014; Debeljak et al., 2013).
3.4. MeHg accumulation in maize grains
3.4.1. MeHg accumulation in maize grains under elevated
atmospheric GEM levels
The MeHg concentrations in maize grains in the OTCs experi-
ment are shown in Fig. 4A. The average MeHg concentrations in
maize grains in RS were 0.17 ± 0.01 ng g
1. MeHg concentrations in
maize grains from GFS were also analyzed to clarify the mecha-
nisms of MeHg translocation and accumulation in maize grains
under different air Hg levels. The average MeHg concentrations in
GFS were 3.38 ± 1.12 ng g
1, which was approximately 19.88 times
Fig. 3. MeHg concentrations in maize roots in (A) the OTCs experiment and (B) in the soil Hg-enriched experiment.
5
higher than that in RS, indicating that self-detoxification may exist
in maize grains in RS. MeHg levels in RS did not show significant
correlations with air GEM concentrations (p > 0.05), while the
MeHg concentrations in maize grains in GFS were positively related
to the GEM levels (R2 ¼ 0.99, p < 0.05) (Fig. 4A), indicating that air
GEM levels may increase MeHg accumulation in maize grains in
GFS, and had a small effect on MeHg accumulation in maize grains
during the RS.
3.4.2. The accumulation capability for MeHg of maize grains
The percentages of MeHg to THg concentrations (%MeHg) were
calculated to estimate the accumulation capability for MeHg and
inorganic Hg (IHg) by maize tissues. In the OTCs experiment, the
average %MeHg in maize grains was 75.16 ± 24.40% and
9.01 ± 2.99% for GFS and RS, respectively (Fig. 4B). In contrast, %
MeHg in other maize tissues was generally less than 5% in RS
(Table S1). The %MeHg in maize grains in the GFS was positively
related to the GEM levels (R2 ¼ 1.00, p < 0.01), while there were
negative correlations between %MeHg in maize grains in the RS and
GEM levels (R2 ¼ 0.99, p < 0.01) (Fig. 4B). These results implied
MeHg was easier to be transported and accumulated in maize
grains in GFS compared to IHg, and high levels of air Hg may in-
crease MeHg accumulation in maize grains in GFS, while self-
detoxification may occur during the maize grain ripening stage.
Besides, MeHg was easier to be transported and accumulated in
maize grains than in other tissues, especially in GFS. The results
from the soil Hg-enriched experiment confirmed that MeHg is
much easier to be accumulated in grains than in other tissues
(Meng et al., 2010), with the average %MeHg in maize grains in RS
was 40.60 ± 16.79% that was much higher (around 3 to 100 times)
than those in other maize tissues (3.87 ± 2.07%) (Table S2).
Previous studies showed that rice grains have a high ability to
accumulate MeHg, which is first absorbed from the soil by root,
then translocated to stems and leaves, and finally accumulated in
grains (Meng et al., 2010; Meng et al., 2011; Qiu et al., 2008; Zhang
et al., 2010b). In our OTCs experiment, MeHg in maize grains may
be transported from maize leaves after the Hg methylation on the
leaf surfaces during GFS, because maize roots are acting as a barrier
in translocating Hg from the soil to aboveground tissues (Cui et al.,
2014; Debeljak et al., 2013). Self-detoxification may occur during
6 T. Sun et al. / Environmental Pollution 265 (2020) 114890
Fig. 4. The correlations between MeHg concentrations in maize grains and GEM levels (A) and between the ratios of MeHg concentrations to THg concentrations in maize grains
and GEM levels (B).
the RS with the elimination of some MeHg from maize grains.
Further studies are needed to fill the knowledge gap of how MeHg
translocates to maize grains from leaves under high air Hg levels.
3.4.3. Self-detoxification in maize grains
Our OTCs experiment results indicated that there is a self-
detoxification process in maize grains. Both MeHg and THg con-
centrations in the maize grains reduced significantly from GFS to
the grain RS (Fig. 5). Maize grains from the GFS had a higher MeHg
(2.7e4.3 ng g
1) and THg (3.8e5.9 ng g
1) level than those from the
RS (MeHg: 0.12e0.23 ng g
1; THg: 1.4e3.1 ng g
1). The concen-
trations of MeHg and THg in maize grains reduced by 93e96% and
51e73% during the grain ripening stage. This reduction pattern of
MeHg and THg levels is unlikely to be induced by the dilution of
plant growth because the size of maize grains did not change
significantly at the sample collecting time (GFS: 30 days after
pollination; RS: 50 days after pollination) (Chen et al., 2014; Huang
et al., 2019; Mechin et al., 2007), and additionally, dilution should
cause a similar reduction of both THg and MeHg concentrations.
Furthermore, previous studies showed that THg concentrations in
wheat and rice grains did not change significantly between GFS and
RS, suggesting that bio-dilution of Hg was not the predominant
reason of the reduction of THg and MeHg levels in maize grains
(Meng et al., 2012; Niu et al., 2011). Thus, a plausible explanation for
this sharp reduction of THg and MeHg is self-detoxification in
maize grains (Xu et al., 2016).
Previous studies showed that the Hg ions produced by the in-
planta demethylation of MeHg could be reduced to Hg0 by the
photolytic process under UV light or endophytic process by mi-
croorganisms (Battke et al., 2005; Lindberg et al., 2005; Xu et al.,
2016). The produced Hg0 is subsequently lost from the plant
through transpiration (Lindberg et al., 2005). Some evidence also
showed significant losses of MeHg and IHg from rice tissues be-
tween GFS and RS (~45%) and confirmed that in planta self-
detoxification (demethylation or elimination) is possible (Li et al.,
2016; Meng et al., 2014a; Strickman and Mitchell, 2017; Xu et al.,
2016). In our study, we did not analyze the MeHg and THg con-
centrations in maize axes and bracts. However, Fu et al. (2014) and
Zhao et al. (2017) reported that Hg content in maize axes and bracts
are higher than that in maize grains, and grain’s Hg concentrations
significantly relate with those of both axes and bracts (Fu et al.,
2014; Zhao et al., 2017). Therefore, the lost MeHg and THg in
maize grains might be attributed to the transport of Hg from maize
grains to maize axes and bracts during the maize grain ripening
stage. Further researches are needed to give more direct evidence
for self-detoxification of Hg in maize grains.
3.5. Translocation of methylmercury in maize tissues
MeHg from both air and soil sources can transport in crop plants
with stems and leaves as the first location and grains as the final
destination (Meng et al., 2011; Meng et al., 2014b). In this study, the
R(i/upper leaves) (i ¼ grains, bottom leaves, and upper and bottom
stems) of MeHg from the OTCs experiment are shown in Table 1.
Average R(i/upper leaves) values for MeHg in grains, bottom leaves,
upper stems, and bottom stems were 0.93 ± 0.41, 0.73 ± 0.09,
0.52 ± 0.29, 0.15 ± 0.15, respectively, which followed the trend:
grains > bottom leaf > upper stem > bottom stem, implying that the
translocation of MeHg from maize leaves to grains was the most,
and little MeHg was transported from maize leaves to bottom
stems. Here, average R(i/upper leaves) values for MeHg in maize roots
were not calculated, because soil MeHg was the predominant
source of MeHg in maize roots (Cui et al., 2014; Debeljak et al.,
2013). Overall, although MeHg concentrations in maize plants
were very low, the increase of MeHg accumulation in maize tissues
under high-level air Hg poses a potential and environmental threat,
especially in Hg mining areas.
4. Conclusions
Using open-top chambers mesocosms facilitated by the soil Hg-
enriched experiment, our results verify the hypothesis that an
elevated GEM concentration can lead to a higher MeHg level in
maize foliage. Maize stems had the lowest ability in accumulating
MeHg, and the MeHg concentrations may be affected by both air
and soil Hg. High levels of air GEM could increase MeHg accumu-
lation in maize grains in the grain-filling stage but had no in-
fluences in grains in the grain-ripening stage. MeHg was easier to
transport and accumulate in grains in grain filling stage than IHg
and was easily accumulated in maize grains than in other tissues.
The significant loss of MeHg in maize grains from the grain-filling
stage to the grain-ripening stage suggested that self-
detoxification may occur in maize grains. Further studies are
needed to investigate the MeHg transport process among tissues of
 T. Sun et al. / Environmental Pollution 265 (2020) 114890 7

maize and clarify the mechanisms of Hg methylation on leaf sur-

faces and self-detoxification in maize leaves.

Declaration of competing interest

We would like to submit the research article “Influences of

High-level Atmospheric Gaseous Elemental Mercury on Meth-
ylmercury Accumulation in Maize (Zea mays L.)” to Environ-
mental Pollution for review and possible publication. The author
lists are “Ting Sun, Zhangwei Wang*, Xiaoshan Zhang, Zhenchuan
Niu, Jian Chen”, and all authors have reviewed the manuscript and
approved it to submit to Environmental Pollution journal. No conflict
of interest exists in the submission of this manuscript. Neither the
entire paper nor any part of its content has been submitted,
accepted, or published elsewhere and not under consideration for
publication elsewhere, in whole or in part.

CRediT authorship contribution statement

Ting Sun: Data curation, Software, Writing - original draft.

Zhangwei Wang: Supervision, Writing - review & editing.
Xiaoshan Zhang: Conceptualization, Methodology. Zhenchuan
Niu: Visualization, Investigation. Jian Chen: Software, Validation.

Acknowledgment

The study is supported by the National Key Research and

Development Program of China (2017YFC0210106), the Second Ti-
betan Plateau Scientific Expedition and Research Program (STEP,
Grant No. 2019QZKK0307-03-001) and the National Natural Sci-
ence Foundation of China (No. 41673113 and 41373124). The au-
thors would like to thank Pufeng Qin from Hunan Agriculture
University for his assistance in field works.

Appendix A. Supplementary data

Supplementary data to this article can be found online at

https://doi.org/10.1016/j.envpol.2020.114890.

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