Introduction
Human activities, including mining, the utilization of wastewater in
agriculture and other industrial/agricultural activities, induces the
accumulation of heavy metals in plants, leading to a host of ultrastructural
anomalies in plants (Jia et al. 2017;
Rizwan et al. 2017; Scimeca et al.
2017). Among these heavy metals, cadmium (Cd) is one of the most aggressive and
persistent; it is relatively mobile in soil and can be toxic to both plants and
animals (Poschenrieder and Barceló 1999; Khan et al. 2016). According to the Chinese
national survey of soil pollution, more than 7% of surveyed samples had
excessive levels of cadmium (Ministry of Environmental Protection 2014).
Therefore, Cd pollution is very serious. However, we seem to be powerless to
reduce Cd inputs due to the pervasiveness of this metal, which even occurs in
phosphorous fertilizers used in agriculture. To ensure food security while
coping with the growing population, the exploration of ways to improve crop
resistance to Cd stress is urgently needed.
Cadmium toxicity alters the uptake of
water and mineral nutrients in plants and diminishes biomass, photosynthesis,
grain yield, and quality in crops (Anh and Popova 2013; Moradi and Ehsanzadeh 2015). Cd toxicity also affects biochemical
processes in plants, causing oxidative stress by inducing reactive oxygen
species (ROS) accumulation, which causes great damage to the antioxidant enzyme
system (Mesnoua
et al. 2016; Javed et al. 2017). Cd was also found to reduce leaf transpiration by affecting
root water uptake (Rucińska-Sobkowiak 2016). In
recent decades, researchers have performed fruitful work centered on reducing
Cd uptake, translocation, and toxicity by applying soil amendments, biochar,
manure, compost, silicon and other plant growth regulators, e.g., jasmonic acid (Xu et
al. 2014; Gondor et al. 2016; Xu et al. 2016; Abozeid et al. 2017).
Jasmonic acid, a plant growth regulator,
has been found to play a vital role in the process of plant development and
stress responses (Fragoso et al.
2014; Abouelsaad and Renault 2018). In the last
decade, jasmonic acid (JA) has been mostly studied as
an immune response factor in response to biotic stresses (herbivore attack and
pathogen infection) (Farmer and Ryan 1992; Seo et al. 2001). More recently, studies
have highlighted the important role of JA in improving plant resistance to
abiotic stresses, including Cd stress (Li et al. 2003; Abouelsaad and Renault 2018; Ali et al. 2018). In general, treatment with exogenous methyl jasmonate (MeJA)
significantly enhanced Cd stress tolerance in plant seedlings by decreasing the
concentration of malondialdehyde (MDA) and H2O2 by
increasing the transcription levels and activities of superoxide dismutase,
peroxidase, catalase and ascorbate peroxidase. On the other
hand, exogenous MeJA increased the contents of
glutathione, Chl b and carotenoids to enhance the
growth of Cd-stressed seedlings (Chen et
al. 2014; Yan et al. 2015; Ali et al. 2018). Although the action of JA
as a possible antioxidant in improving Cd stress is well understood, the
underlying mechanisms involved in this process remain unclear.
Polyamines
(PAs), another class of biomolecules that mainly consists of putrescine (put),
spermidine (spd) and spermine (spm),
have been found to be essential for normal plant growth, development and stress
responses (Sanchez-Elordi et al. 2019). Under saline conditions, wheat seedlings treated
with melatonin exhibited more free polyamines, especially spd,
to mitigate salt stress and maintain plant growth (Ke et al. 2018). A primary study on JA
indicated that exogenous MeJA induced polyamine
accumulation to protect against powdery mildew in barley (Mitchell et al. 2002) and to delay peach fruit
ripening (Ziosi
et al. 2009). Taking all this into consideration, MeJA-induced
polyamine accumulation functions in biotic stress responses and developmental
regulation. However, whether MeJA induces polyamine
accumulation and whether MeJA-induced polyamine
accumulation plays a role in the plant abiotic stress response is unclear.
Unraveling the underlying effects of MeJA-induced
polyamine accumulation on the plant response to Cd stress could broaden our
vision for improving crop Cd tolerance.
In the
present study, we applied Cd and MeJA to maize (Zea mays L.) to evaluate the effect of MeJA on maize resistance to Cd stress. We also detected the
accumulation of PAs with MeJA application under Cd
stress. We added the spd synthetic inhibitor dicyclohexylamine (DCHA) to examine the role of PAs in MeJA-induced improved maize resistance to Cd stress.
Materials and Methods
Plant material and treatment
The widely cultivated maize variety Zhengdan
958, bred by the Henan Academy of Agronomy, was used in this study. Two
experiments were conducted. Experiment 1 was performed to test whether MeJA affected PA content under Cd stress. First, seeds were
disinfected with 3% NaClO and washed with
double-distilled water. Then, six seeds were planted per pot (20 cm × 35 cm)
with 9 kg soil, and the pots were placed in a rain-proof shed. The soil was a
light silt loam (Heilutu series) collected from the
top 0–20 cm of cropland. The soil organic carbon content, total nitrogen,
available phosphorus, available potassium, pH and bulk density were 13.5 g kg−1,
0.62 g kg−1, 18.5 mg kg−1, 138.5 mg kg−1,
7.0 and 1.26 g cm−3, respectively. When seedlings grew to the
three-leaf stage, thinning to three seedlings of the same size per pot was
conducted. Then, the CK, Cd and Cd + MeJA treatments
performed. The treatments were conducted through irrigation with water (CK),
100 µM Cd2+ (CdCl2)
and 100 µM Cd2++100
µM MeJA
to maintain a soil water content of 75 ± 5% field water capacity. Each
treatment had three replications. The MeJA and Cd
concentrations were ascertained with reference to published studies (Chen et al. 2014; Yan et al. 2015; Ali et al.
2018). After treatment for two weeks, new fully expanded
leaves (the sixth leaves) were collected to detect the PA content.
Experient 2 was performed to detect the mechanism
of JA in regulating Cd stress tolerance in maize. The
soil and procedures used in experiment 1 were used to plant the maize seedlings
and three seedlings were retained at the three-leaf stage. The experiment was
comprised of six treatments: CK, Cd, Cd + MeJA (MeJA), Cd + spd
(SPD), Cd + MeJA + spd (MeJA + SPD), and Cd + MeJA + DCHA
(Cd
+ DCHA). Cd was applied in all treatments except CK. These
treatments were performed through irrigating with water (CK), water
containing 100 µM Cd2+ (Cd), water
containing 100 µM Cd2+ +
100 µM MeJA
(MeJA), water containing 100 µM Cd2+ + 0.5 mM spd (SPD), water containing 100 µM Cd2+ + 0.5 mM spd + 100 µM
MeJA (MeJA + SPD) and water
containing 100 µM Cd2+ +
100 µM MeJA+1 mM DCHA
(Cd + DCHA). Each treatment had 12 replications. After treatment for two weeks,
the observations were recorded. All measurements (plant height, aboveground
biomass, leaf gas exchange traits, chlorophyll contents, Hydrogen peroxide,
MDA, antioxidant enzyme activities and tissue Cd concentration) except the
polyamine content analyses were performed using the seedlings from experiment
2.
Polyamine content analyses
This analysis was only performed in
experiment 1. A new fully expanded leaf was used to test the PA content
according to Ke’s method (Ke
et al. 2018). Briefly, a new fully
expanded leaf (approximately 1 g) was sampled with liquid nitrogen, ground in a
mortar to a fine powder and extracted in 5 mL of 5% (w/v) chilled perchloric
acid. After 18 h of extraction at 25°C, the homogenate was centrifuged for 15
min at 15,000 g. The supernatant phase was used to detect the free polyamine
content. For benzoylation, 500 µL supernatant phase
containing the free polyamine fraction was mixed
with 1 mL 4 N NaOH and then 10 µL benzoyl chloride was immediately
added. The benzoylated samples were separated on an Insertsil ODS-3 (5 µm,
4.6 × 250 mm, GL Science Inc., United States) under the following program: 0 ∼ 15 min, 60% methanol; 15 ∼ 35 min, 60 ∼ 90%; 35 ∼ 45 min,
90 ∼ 60%; 45 ∼ 60 min, 60% at a flow rate of 0.8 mL min−1
at 35°C. Polyamine peaks were detected with a UV detector at 254 nm. The
measurements included three biological replications.
Plant height and aboveground
biomass
In experiment 2, after two weeks of treatment, plant height was detected
using a centimeter ruler. Dry biomass was measured after two weeks of treatment
using a previous method (Liu et al.
2014a). Briefly, the shoot was sampled and dried to a
constant weight at 80°C. Measurements were taken for fifteen biological
replications.
Leaf gas exchange traits and
chlorophyll contents
The gas exchange parameters of new fully expanded leaves were measured at
10:00 – 11:00 a.m. using a portable photosynthesis system with an IRGA analyzer
(Li-6400; LI-COR Inc., Lincoln, N.E., U.S.A.) after two weeks of the treatments
in experiment 2. The leaf photosynthetic pigments were used to detect the
chlorophyll contents with the method of Knudson et al. (1977). Measurements were taken for eight biological
replications.
Hydrogen peroxide, MDA and
antioxidant enzyme activities
The hydrogen peroxide contents, and antioxidant enzyme activities were measured according to Liu et al. (2015). The superoxide dismutase
activity was assayed by its ability to inhibit the photochemical reduction of
nitro blue tetrazolium (NBT). The peroxidase activity was determined using the
guaiacol oxidation method. The catalase activity was estimated by measuring the
initial rate of the disappearance of H2O2 at 240 nm.
Hydrogen peroxide contents were measured as follows: Leaf samples (0.5 g fresh
weight, FW) were homogenized in an ice bath with 0.1% (w/v) trichloroacetic
acid. The homogenate was centrifuged at 12,000 g for 15 min, and 1 mL of
supernatant was added to 1 mL of 10 mM potassium phosphate buffer (pH
7.0) and 0.8 mL of 1 M KI. The
absorbance was measured at 390 nm. The H2O2 content was
calculated using a standard curve. MDA was detected using thiobarbituric
acid (TBA) according to Li et al.
(2017). For this measurement, a new fully expanded leaf was used. Measurements
were taken for five biological replications.
Determination of tissue Cd
concentration
Leaves were dried at 80°C, ground artificially and used to detect the Cd concentration.
Root samples were taken from the soil and then washed with double-distilled
water to eliminate soil and cadmium from the root surfaces. The root was dried
at 80°C, ground artificially and used to detect the Cd concentration. The Cd concentration
was detected using an ICP-MS according to the instrument's specifications.
Briefly, approximately 500 mg of dry, ground plant material was used for acid
digestion. The digestion matrix contained 5 mL HNO3 and 2 mL H2O2.
Digestion was performed with a Multiwave 3000 (64 MG5
rotor, Anton Paar). After
digestion, the microdigests were acidified with
hydrofluoric acid to a final concentration of
0.01% to prevent the polymerization or precipitation of the ions. The Cd
concentrations in the digests were measured with inductively coupled plasma mass spectrometry (ICP-MS; IACP-MS-Qc, ThermoFisher
Scientific, M.A., U.S.A.). Each measurement was performed for three biological
replications.
Statistical analysis
Statistical analyses were performed with SPSS version 18.0. One-way ANOVA
was used to ascertain the effects of MeJA under the
different treatments. Differences between the means were compared by the least
significant difference (LSD) test at P
< 0.05. The figures were produced using SigmaPlot
version 12.01 (Systat Software, Inc.).
Results
Experiment
1
Effect of exogenous MeJA on Pas: After two weeks of treatment with Cd + MeJA and Cd, the maize leaves had significantly increased
free put content (P < 0.05, Fig.
1). The exogenous Cd + MeJA group had the highest
free put content, with increases of 34.5% and 22.8% compared with the CK and Cd groups, respectively. The free spd
of the Cd + MeJA group was 12.9% and 9.1% higher than
that of the CK and Cd groups, respectively. The free spm
of the Cd + MeJA group was 25.5% and 16.6% higher
than that of the CK and Cd groups, respectively. These results showed that
exogenous MeJA could significantly increase
endogenous PAs under Cd stress, which might be beneficial in improving maize Cd
tolerance.
Experiment 2
Maize growth status: After two weeks of treatment, the
exogenous substances had obviously affected maize growth (Fig. 2). Cd stress
significantly decreased the maize plant height and dry biomass (P < 0.05) and the application of MeJA or spd mitigated the
inhibition of maize growth under Cd stress (Fig. 2AB). However, the combined
application of DCHA and MeJA did not improve maize
seedling growth under Cd stress.
Leaf gas exchange traits and
chlorophyll contents
The trends in the net photosynthetic rate were
similar to those of the biomass, and the CK group had the highest
photosynthetic rate (Fig. 3A). The application of Cd decreased the
photosynthetic rate compared with that in CK (P < 0.05). MeJA+ SPD, SPD and MeJA
application improved the photosynthetic rate, while the combined application of
DCHA and MeJA under Cd stress did not improve the
photosynthetic rate compared with that under only Cd
application. In addition, exogenous MeJA and spd alleviated the Cd stress-induced inhibition of stomatal
conductance, but the application of DCHA eliminated this alleviating effect
(Fig. 3B).
Fig. 1: Effects of exogenous MeJA on polyamine metabolism under Cd stress (100 µM Cd2+). Cellular polyamines
include putrescine (Put), spermidine
(Spd) and spermine (Spm). Data represent the mean ± SE of three biological
replications; different lowercase letters above the bars indicate significant
differences at P < 0.05 according
to the least significant difference method
Fig. 2: Effects of MeJA
on the growth of maize seedlings under Cd stress (100 µM Cd2+). (A) Plant height of maize seedlings. (B)
Biomass of maize seedlings under Cd stress. Data represent the mean ± SE of
fifteen biological replications, and different lowercase letters above the bars
indicate significant differences (P
< 0.05)
Fig. 3: Effects of MeJA
on the photosynthetic rate (A) and stomatal conductance (B)
of maize seedlings under Cd stress (100 µM
Cd2+). Data represent the mean ± SE of eight biological
replications, and different lowercase letters above the bars indicate
significant differences (P < 0.05)
Fig. 4: Effect of MeJA
on the chlorophyll contents of maize seedlings under Cd stress (100 µM Cd2+). Data represent the
mean ± SE of eight biological replications, and different lowercase letters
above the bars indicate significant differences (P < 0.05)
Fig. 5: Effects of MeJA
on the hydrogen peroxide and MDA content of maize seedlings grown under Cd
stress (100 µM Cd2+). Data
represent the mean ± SE of five biological replications, and different
lowercase letters above the bars indicate significant differences (P < 0.05)
Compared with that in the CK group,
Cd stress significantly decreased the chlorophyll content (P < 0.05, Fig. 4). When MeJA and spd were added under Cd stress, they significantly
increased leaf chl a content
(P < 0.05) compared with Cd
application alone. When the combination of MeJA and spd was added, the effect was not obvious (Fig. 4A). The
results for chl a, b and total chlorophyll are
similar (Fig. 4B–C). Taking chl a and
chl b together, exogenous MeJA
and spd eliminated the decline in the total
chlorophyll content induced by Cd stress.
Hydrogen peroxide, MDA and antioxidant enzyme activities
The results for the H2O2
concentrations in leaves were very interesting. Compared to that in the CK
group, treatment with Cd significantly increased the H2O2
concentration (Fig. 5A). The application of MeJA,
Cd + DCHA and SPD did not decrease the H2O2 concentration
compared with that under Cd stress. There were no significant differences among
the treatments of Cd, MeJA, Cd + DCHA and SPD in
terms of H2O2 concentration (18.34–22.44 μmol/g FW).
Compared with the other treatments under Cd stress, the MeJA+
SPD group (15.19 μmol/g FW) had a significantly decreased H2O2
concentration (P < 0.05) and was
not significantly different from the CK group (17.07 μmol/g FW).
As shown in Fig. 5B, Cd stress
significantly increased the MDA content compared to that in the CK group (P < 0.05). Exogenous MeJA, MeJA + SPD and SPD
decreased this increment sharply. When DCHA and MeJA
were added together, exogenous MeJA did not alleviate
the Cd-induced increase in leaf MDA accumulation compared with that under the
Cd treatment alone.
Unlike the MDA content, under Cd
stress, the peroxidase activity was increased in these treatments. However, the
Cd and Cd + DCHA combination exhibited higher peroxidase activity than the
other treatments, and CK showed the lowest peroxidase activity (Fig. 6A). For
superoxide dismutase activity, the SPD, Cd + DCHA
combination and CK treatments exhibited the highest activity, while MeJA + SPD exhibited the lowest activity (Fig. 6B). For
catalase, the CD+DCHA combination had the maximum activity level, followed by
the SPD, Cd, MeJA, MeJA + SPD
and CK treatments (Fig. 6C).
Tissue Cd concentration
Fig. 7: Effects of MeJA
on the Cd concentration of maize seedlings grown under Cd stress (100 µM Cd2+). Data represent the
mean ± SE of three biological replications, and different lowercase letters
above the bars indicate significant differences (P < 0.05)
Fig. 6: Effects of MeJA
on the antioxidant enzyme activities of maize seedlings under Cd stress (100 µM Cd2+). Data represent the
mean ± SE of five biological replications, and different lowercase letters
above the bars indicate significant differences (P < 0.05)
For leaf Cd concentration, under Cd
stress, exogenous MeJA and Spd
decreased leaf Cd accumulation, and the Cd concentration of these treatments
was lower than those of the Cd and Cd + DCHA treatments (Fig. 7A). We also found
that with the spd synthetic inhibitor DCHA, the leaves accumulated more Cd than in the only-Cd treatment. However,
for the root Cd concentration, we found that exogenous MeJA
and SPD did not change the root Cd uptake from the soil (Fig. 7B) because there
was no significant difference in the root Cd concentration among the Cd
treatments. As expected, the CK group had the lowest root Cd concentration.
Discussion
Prior studies have documented the effectiveness of JA in improving plant
resistance to abiotic stress (Seo et al. 2001; Chen et al.
2005; Han et al. 2018; Yan et al. 2019). In addition, numerous
studies have confirmed that PAs play an important role in JA-induced resistance
improvement in plants (Capitani et al. 2001; Mitchell et al.
2002; Chen et al. 2006). In the
current study, under Cd stress, MeJA induced more PA
accumulation than treatments without MeJA. In a
further study, we found that exogenous DCHA could eliminate the improvements
achieved with exogenous MeJA. These results indicate
that PAs participate in JA-induced plant resistance to Cd.
Jasmonate has been reported to participate
in many biotic and abiotic responses in plants (Chen et al. 2005; Harb et al. 2010). Here, we present evidence that Cd-induced growth
inhibition in maize seedlings was alleviated by exogenous MeJA
(Fig. 2). Numerous types of stress, such as salinity, cold, drought, and
oxidative stress, severely repress the plant leaf photosynthetic rate (Yan et al. 2016). In research on improving
resistance to environmental stress, an enhanced photosynthetic rate was
considered an important index (Liu et al.
2015). Here, exogenous MeJA alleviated the Cd-induced
inhibition of the leaf photosynthetic rate (Fig. 3), consistent with
observations of previous studies (Yan et
al. 2015; Ali et al. 2018).
In previous studies, almost all of the exogenous
substances that enhanced plant Cd resistance were considered to improve
antioxidant enzyme activities and decrease ROS contents (Singh and Shah 2014;
Gondor et al. 2016). When rice plants
were exposed to 50 µM Cd2+
alone and/or with 5 µM MeJA, MeJA increased the
antioxidant enzyme activities to clear ROS (Singh and
Shah 2014). However, in our study, we did not find any effective change in
the antioxidant enzyme activities, including those of peroxidase, superoxide
dismutase and catalase, with the application of MeJA
(Fig. 6). In our study, we added 100 µM
Cd2+ to the soil by irrigation, while in other studies, seedlings
were treated with Hoagland nutrient solution, and Cd2+ was added to
the solution, which made the stress more intense. We speculate that the
different treatment methods and different species were the main source of this
difference. In the present study, the highest H2O2
content was 22.44 μmol/g FW, which was lower than levels in
a previous report (Souza et al.
2014). These results suggest that under this treatment, the accumulation of H2O2
did not reach the threshold for causing damage, and there was no need for the
initiation of antioxidant enzyme activities to clear it. In addition, H2O2
plays an important role as a signal for regulating the stress response (Neill et al. 2002). Thus, H2O2
may have acted as a signaling molecule in the current study, indicating
that the oxidative damage was not serious. However, according to the MDA
results, primary damage had begun, and exogenous MeJA
and Spd reduced MDA production (Fig. 5B). These results showed that under Cd stress, exogenous MeJA could reduce membrane damage.
Based on the Cd concentration measurement, we
found that exogenous MeJA reduced the transport of Cd
from the root to the shoot but did not affect the root uptake of Cd (Fig. 7).
In a previous study, MeJA was found to reduce leaf Cd
in Kandelia obovata
seedlings and it was suggested that the reduced uptake of Cd in the shoots of K. obovata
might be a result of stomatal closure and decreased transpiration by exogenous MeJA (Chen et al.
2014). However, in this study, we found that exogenous MeJA
increased stomatal conductance. Therefore, we speculate that the reduced leaf
Cd accumulation was not the result of stomatal regulation. A previous study
confirmed that silicon increased organic acid production to improve Cd
resistance in sorghum seedlings (Liu et
al. 2014b). Increased organic acid production by exogenous MeJA has been reported (Zhao et al. 2001). Here, it was possible that the MeJA
treatments increased the organic acid content in the leaves of maize, thereby
repressing the uptake of Cd in leaves. In addition, phenolic compounds also
repress the uptake of Cd in shoots (Kováčik et al. 2011), which could be another
reason for the MeJA-induced lower leaf Cd
accumulation.
The role of PAs in processes
involving cell division, such as the development of roots, reproductive organs,
and embryos, fruit ripening and the control of aging processes is known to be
significant (Ke et al. 2018). It has been
reported that exogenous MeJA and spd
alone could improve Cd tolerance (Ali et
al. 2018; Tajti et al. 2018). Many studies have indicated that the involvement of
the metabolic pathways of PAs could be involved in JA-induced plant resistance
to Cd (Mitchell et al. 2002; Jia et al. 2015). MeJA
was found to upregulate biosynthetic gene expression, oxidation and the
conjugation of polyamines in tobacco (Capitani et al. 2001). Here, we found that under
Cd stress, the MeJA-treated plants showed
significantly increased PA production (Fig. 1). In addition, the exogenous
application of the spd synthetic inhibitor DCHA with MeJA eliminated the MeJA-induced
improvement in maize resistance to Cd stress (Fig. 2). These results confirmed
our primary hypothesis that PAs play an important role in MeJA-induced
improved resistance to Cd stress in maize.
In the present study, we found that
exogenous MeJA treatment partially mitigated the
Cd-induced inhibition of whole-plant growth in maize. Under Cd stress, the MeJA- and spd-treated plant
leaves contained a lower amount of Cd than the leaves of plants not treated
with MeJA and spd. Through
the addition of the spd synthesis inhibitor dicyclohexylamine under Cd stress conditions combined with MeJA, the leaf Cd concentration was higher than that under
the Cd treatment alone, and the JA-induced improvement in maize Cd resistance
was eliminated. Therefore, it could be concluded that spermidine plays an important
role in JA-induced improved Cd resistance in maize seedlings by repressing Cd
transport from roots to leaves.
Acknowledgements
The study was sponsored by the PhD
research startup fund of Yulin University (17GK19 and
17GK18), the Science and Technology Program of Yulin
Science and Technology Bureau (2018-2-50) and the National Natural Science
Foundation of China (31960223). The authors wish to express their
sincere gratitude to the anonymous reviewers and editor for their important
advice.
Author contributions
Conceived and designed the
experiments: JKY and FRK. Performed the experiments: JKY and
NNZ. Analyzed the data and wrote the paper: JKY, NNZ and FRK.
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