The 20 ?mol/L ABA; shoot Cd contents

The effects of abscisic acid (ABA) addition on cadmium
accumulation of two ecotypes ofSolanum photeinocarpum
Jin Wang &Lijin Lin &Li Luo &Ming’an Liao ;
Xiulan Lv ;Zhihui Wang ;Dong Liang ;Hui Xia ;
Xun Wang ;Yu n s o n g L a i ;Yi Tang
Received: 12 September 2015 / Accepted: 16 February 2016 / Published online: 22 February 2016
#
Springer International Publishing Switzerland 2016
Abstract The study of the effects of exogenous abscisic
acid (ABA) addition on cadmium (Cd) accumulation of
two ecotypes (mining and farmland) of Solanum
photeinocarpum was operated through a pot experiment.
The results showed that the biomass and chlorophyll
content of the two ecotypes of S. photeinocarpumin-
creased with increasing ABA concentration. Applying
exogenous ABA increased Cd content in the two eco-
types of S. photeinocarpum . The maximum Cd contents
in shoots of the two ecotypes of S. photeinocarpumwere
obtained at 20 ?mol/L ABA; shoot Cd contents respec-
tively for the mining and farmland ecotypes were 33.92
and 24.71 % higher than those for the control. Applying
exogenous ABA also increased Cd extraction by the two
ecotypes of S. photeinocarpum , and the highest Cd
extraction was obtained at 20 ?mol/L ABA with
569.42 ?g/plant in shoots of the mining ecotype
and 520.51 ?g/plant in shoots of the farmland
ecotype respectively. Therefore, exogenous ABA
can be used for enhancing the Cd extraction ability of S. photeinocarpum
,and20?mol/L ABA was the opti-
mal dose.
Keywords ABA.
Solanum photeinocarpum .
Ecotype .
Cadmium .
Phytoremediation .
Hyperaccumulator
Introduction
Plant hormones, which are induced by environmental
signals, can affect plant growth and development by
regulating physiological reactions (Li et al. 2003).
Abscisic acid (ABA) is an important hormone in plants
and is also an important signaling molecule (Ikegami
et al. 2009;Zhangetal. 2006). This hormone can
promote stomata closure and induce resistance protein
synthesis through signal transduction of the defense cell
membrane to enhance plant stress resistance and can
also regulate the expression of genes and proteins
(Adie et al. 2007). When the plant experiences stressful
conditions, such as drought, low temperature, high salt
concentration, or high concentration of heavy metals,
large amounts of ABA are synthesized in the plant body
to increase the plant stress resistance (Ikegami et al.
2009 ; Zhang et al. 2006). Under cadmium (Cd) stress,
ABA enhances the tolerance of wheat seedlings (Han
et al. 2012)and Hordeum vulgare seedlings (Li and
Zhang 2012), and decreases Cd content in shoots of
Brassica campestris ssp.chinensis seedlings (Qian
et al. 2008) and rice seedlings (Rubio et al. 1994;Hsu
and Kao 2003). ABA could enhance the tolerance of
common plants to Cd stress and decrease Cd absorption
Environ Monit Assess (2016) 188: 182
DOI 10.1007/s10661-016-5194-6
Jin Wang, Lijin Lin and Li Luo contributed equally to this work.
J. Wang
:L. Luo :M. Liao :Z. Wang
College of Horticulture, Sichuan Agricultural University,
Chengdu, Sichuan 611130, China
L. Lin
:X. Lv ( *) :D. Liang :H. Xia :X. Wang :Y. L a i :
Y. T a n g
Institute of Pomology and Olericulture, Sichuan Agricultural
University, Chengdu, Sichuan 611130, China
e-mail: [email protected]

in plants. If ABA was applied to hyperaccumulator or
accumulator species, it might enhance their resistance to
Cd stress and could increase Cd absorption by these
plants, but few studies have addressed this question.Solanum photeinocarpum is a potential Cd-
hyperaccumulator and is an ideal candidate for
phytoremediation of Cd-contaminated soil (Zhang
et al. 2011). However, compared with other
hyperaccumulator or accumulator species, such as
Solanum nigrum (Wei et al.2005) and Siegesbeckia
orientalis (Zhang et al. 2013), the remediation ability
of S. photeinocarpum is low and requires improvement.
According to our field survey, the morphology and Cd
accumulation of different ecotypes of
S. photeinocarpum were quite different. Compared with
the farmland ecotype, the mining ecotype of
S. photeinocarpum was shorter and had lower biomass,
but had higher plant Cd content. Because of the effects
of different climatic conditions, the same
hyperaccumulator or accumulator might have differing
ability to remediate Cd-contaminated soil in different
regions. Therefore, to enhance the remediation potential
of S. photeinocarpum for Cd-contaminated soil, differ-
ent concentrations of ABA were used to treat the two
ecotypes (mining and farmland) of S. photeinocarpum.
The aims of the study were to determine the optimal
ABA concentration for enhancing the phytoremediation
ability of S. photeinocarpum and provide a reference for
improving phytoremediation ability of other
hyperaccumulator or accumulator species.
Materials and methods
Materials
Seeds of the two ecotypes (mining and farmland) of
S. photeinocarpum were collected from the
Tangjiashan lead-zinc mine and farmland of the Ya ‘an
campus farm of the Sichuan Agricultural University,
respectively, in August 2013. The seeds were air dried
and stored at 4 °C. The Tangjiashan lead-zinc mine
(29°24 ?N, 102°38 ?E) is located in Hanyuan County,
Sichuan Province, China, which represents the mining
ecotype with the dry-hot valley climate (Lin et al.
2014a). The farm of the Sichuan Agricultural
University (29°59 ?N, 102°59 ?E) is located in Yucheng
County, Sichuan Province, China, which represents the farmland ecotype with the humid subtropical monsoon
climate (Lin et al.
2014a).
Soil samples for the experiment were collected from
the Ya ‘an campus farm of the Sichuan Agricultural
University in February 2014. Soils were inceptisols
(purple soil in the Genetic Soil Classification of
China), and the soil basic properties are described in
the reference of Lin et al. ( 2014a). The total Cd content
was 0.101 mg/kg, and the available Cd content was
0.021 mg/kg (Lin et al. 2014b).
Experimental design
The experiment was conducted in the greenhouse of the
Ya ‘an campus farm from February to June 2014. The
soil samples were air dried and passed through a 5-mm
sieve. Four kilograms of the air-dried soil was weighed
into each polyethylene pot (18 cm high and 21 cm in
diameter). Cd was added to soils as CdCl
2·2.5H 2Oat
10 mg/kg (Lin et al. 2014c) in February 2014. The soil
moisture was maintained at 80 % of field capacity for
2 months. The seeds of the two ecotypes of
S. photeinocarpum were sown in farmland of the
Ya ‘an campus farm in March 2014. Two uniform seed-
lings of S. photeinocarpum (four euphyllas expanded)
were transplanted into each pot in April 2014, and the
soil moisture content was maintained at 80 % of field
capacity from the time the plants were transplanted into
the pots until the time the plants were harvested. When
the plants had grown for 1 month in Cd-contaminated
soil (May 2014), six concentrations (0, 1, 5, 10, 20, and
40 ?mol/L) of ABA (Khadri et al. 2007;Liaoetal.
2008 ) were sprayed on the leaves of plants for each
pot of the two ecotypes of S. photeinocarpum.
Treatments were replicated four times. The amount of
each treatment was 100 mL of ABA solution (25 mL for
each pot). After ABA treatment for 1 month
(June 2014), the upper mature leaves of
S. photeinocarpum were collected to determine the pho-
tosynthetic pigment (chlorophyll a,chlorophyll b,total
chlorophyll, and carotenoid) contents (Hao et al. 2004).
The plants were then gently removed from the soil. The
roots and shoots of S. photeinocarpumwere harvested
and washed with tap water. The roots were immersed in
10 mM HCl for 10 min to remove Cd adhering to the
root surface. Then, roots, stems, and leaves were further
washed with deionized water and dried at 80 °C to
constant weight for dry weight and Cd content determi-
nation. The dried plant samples were finely ground and
182 Page 2 of 8 Environ Monit Assess (2016) 188: 182

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sieved through a 0.149-mm-mesh nylon sieve for chem-
ical analysis. Samples (0.5 g) were digested in HNO
3/
HClO
4(4:1, v/v ), and then the volume was adjust-
ed to 50 mL with deionized water. The Cd con-
centrations in the roots, stems, and leaves were
determined using an iCAP 6300 ICP spectrometer
(Thermo Scientific, Waltham, MA, USA; Tessier
et al. 1979).ThemeasuredvaluesofCdwere
checked by using certified standard reference ma-
terial (GBW-07602, bush branches, and leaves)
obtained from the China National Center for
Standard Reference Materials.
Statistical analyses
Statistical analyses were performed using SPSS
13.0 statistical software (IBM, Chicago, IL,
USA). Data were analyzed by one-way analysis
of variance with the least significant difference at
a 5 % confidence level. The following calculations
were used: the root/shoot ratio = root biomass /
shoot biomass (Luka ?ová Kuliková and Lux 2010),
translocation factor (TF = Cd content in shoot / Cd con-
tent in root (Rastmanesh et al. 2010), and Cd
extraction = the Cd content in plant × biomass of plant
(Zhang et al. 2010). Results and discussion
Biomass of
S. photeinocarpum
When the plant is under salt stress, drought conditions,
water logging, or low-temperature stress, the ABA con-
centration in the plant body increases, and the ability to
withstand stress is enhanced (Chandler and Robertson
1994 ). There is a positive correlation between the exog-
enous ABA concentration and the endogenous ABA
concentration, and the exogenous ABA can supply the
endogenous ABA concentration or directly induce
downstream signaling (Jia and Lu 2003). For example,
when ABA was sprayed on the leaves of Cyamopsis
tetragonoloba , the concentration of ABA in plant leaves
increased, but the concentrations of indole acetic acid,
gibberellin, and kinetin in plant leaves decreased (Zhou
et al. 2010). Other studies showed that ABA can in-
crease the height, leaf area, tiller number, and biomass of
rice seedlings, and also increase the proline and soluble
sugar contents in the shoots and grain biomass of rice
(Flowers and Yeo 1995; Chen and Zhang 2000). In this
experiment, applying ABA increased the root, stem,
leaf, and shoot biomass of the two ecotypes of
S. photeinocarpum (Table1), which was similar to
results from previous studies (Flowers and Yeo 1995;
Ta b l e 1 Biomass of Solanum photeinocarpum
ABA concentrations
( ? mol/L) Root biomass
(g/plant)Stem biomass
(g/plant) Leaf biomass
(g/plant) Shoot biomass
(g/plant) Root-shoot ratio
Mining ecotype 0 1.95 ± 0.06e 6.05 ± 0.06d 3.80 ± 0.21e 9.85 ± 0.27d 0.198
1 2.20 ± 0.03d 6.13 ± 0.15d 3.96 ± 0.26de 10.09 ± 0.41d 0.218
5 2.48 ± 0.04c 6.85 ± 0.16c 4.23 ± 0.10cd 11.08 ± 0.06c 0.224
10 3.00 ± 0.07b 7.15 ± 0.18b 4.48 ± 0.06c 11.63 ± 0.12b 0.258
20 3.03 ± 0.15b 7.23 ± 0.22b 4.83 ± 0.21b 12.06 ± 0.43b 0.251
40 3.55 ± 0.07a 7.93 ± 0.05a 5.30 ± 0.21a 13.23 ± 0.16a 0.268
Farmland ecotype
0 3.33 ± 0.11c 6.70 ± 0.14d 5.15 ± 0.08d 11.85 ± 0.06e 0.281
1 3.53 ± 0.08bc 6.95 ± 0.13cd 5.35 ± 0.14d 12.30 ± 0.01de 0.287
5 3.60 ± 0.09b 7.25 ± 0.07bc 5.43 ± 0.05 cd 12.68 ± 0.02cd 0.284
10 3.74 ± 0.16ab 7.45 ± 0.13ab 5.68 ± 0.02bc 13.13 ± 0.15bc 0.285
20 3.88 ± 0.16a 7.62 ± 0.20a 5.93 ± 0.13ab 13.55 ± 0.07ab 0.286
40 3.95 ± 0.17a 7.73 ± 0.31a 6.13 ± 0.31ca 13.86 ± 0.00a 0.285
Values are means (±SE) of four replicate pots. Different lowercase letters within a columnindicate significant differences based on one-way
analysis of variance in SPSS 13.0 followed by the least significant difference test ( p; 0.05). The root-shoot ratio = root biomass / shoot
biomass
Environ Monit Assess (2016) 188: 182 Page 3 of 8182

Chen and Zhang2000). In this study, concomitant with
the increase in ABA concentrations, the root, stem, leaf,
and shoot biomass of the two ecotypes of
S. photeinocarpum increased. The root biomass of the
mining ecotype increased significantly ( p; 0.05) by
12.82, 27.18, 53.85, 55.38, and 82.05 % at 1, 5, 10,
20, and 40 ?mol/L ABA, respectively, compared with
that of the control. The shoot biomass of the mining
ecotype increased by 2.44 % at 1 ?mol/L ABA and
significantly ( p; 0.05) increased by 12.49, 18.07,
22.44, and 34.31 % at 5, 10, 20, and 40 ?mol/L ABA,
respectively, compared with that of the control. For the
farmland ecotype, the root biomass increased by 6.01 %
at 1 ?mol/L ABA and significantly ( p; 0.05) increased
by 8.11, 12.31, 16.52, and 18.62 % at 5, 10, 20, and
40 ?mol/L ABA, respectively, compared with that for
the control. The shoot biomass of the farmland ecotype
increased by 3.80 % at 1 ?mol/L ABA and significantly
( p ; 0.05) increased by 7.00, 10.80, 14.35, and 16.96 %
at 5, 10, 20, and 40 ?mol/L ABA, respectively, com-
pared with that of the control. The rate of biomass
increase by ABA was higher for the mining ecotype
than that for the farmland ecotype, indicating that the
ABA was more effective at increasing biomass of the
mining ecotype than that of the farmland ecotype. The
root-shoot ratio of the mining ecotype showed an in-
creasing trend with the increase in ABA concentration, but there was no obvious trend in the variation of the
ratio for the farmland ecotype (Table
1), indicating that
the mining ecotype of S. photeinocarpumwas more
sensitive than the farmland ecotype to ABA treatment.
Photosynthetic pigment content of S. photeinocarpum
ABA is the most important signal molecule for plants to
adapt to stress conditions (Adie et al. 2007). The chlo-
roplast is the main location of ABA synthesis in the leaf,
and synthesized ABA is transported freely through the
phloem and xylem together (Mohamed et al. 2012).
Under conditions of heavy metal contamination, the
chlorophyll and carotenoid contents in plants decrease,
and the photosynthetic ability decreases with the in-
crease in heavy metal concentration in soil (Barickman
et al. 2014). When spraying exogenous ABA on plant
leaves, the chlorophyll and carotenoid contents in the
plant can effectively increase, enhancing the stress re-
sistance of the plant (Huang et al. 2009). In this study,
with the increase in ABA concentration, the chlorophyll
a ,chlorophyll b, and total chlorophyll contents of the
two ecotypes of S. photeinocarpum increased (Table2),
which was similar to results from previous studies (Han
et al. 2012; Li and Zhang 2012). The total chlorophyll
content of the mining ecotype increased by 6.62 and
10.27 % at 1 and 5 ?mol/L ABA, respectively, and
Ta b l e 2 Photosynthetic pigment content of Solanum photeinocarpum
ABA concentrations
( ? mol/L) Chlorophyll
a
(mg/g) Chlorophyll
b
(mg/g) Total chlorophyll
(mg/g) Chlorophyll
a/b Carotenoid
(mg/g)
Mining ecotype 0 1.532 ± 0.021c 0.387 ± 0.059b 1.919 ± 0.080b 3.959 0.554 ± 0.052d
1 1.641 ± 0.068bc 0.405 ± 0.049ab 2.046 ± 0.117ab 4.052 0.616 ± 0.030cd
5 1.677 ± 0.023ab 0.439 ± 0.013ab 2.116 ± 0.035ab 3.820 0.624 ± 0.021bc
10 1.721 ± 0.073ab 0.463 ± 0.035ab 2.184 ± 0.108a 3.717 0.635 ± 0.011abc
20 1.763 ± 0.019a 0.477 ± 0.014ab 2.240 ± 0.033a 3.696 0.642 ± 0.023ab
40 1.765 ± 0.027a 0.501 ± 0.045a 2.266 ± 0.072a 3.523 0.670 ± 0.014a
Farmland ecotype 0 1.315 ± 0.085c 0.315 ± 0.040c 1.630 ± 0.125d 4.175 0.472 ± 0.037c
1 1.517 ± 0.033b 0.363 ± 0.038bc 1.880 ± 0.071 cd 4.179 0.482 ± 0.025bc
5 1.550 ± 0.013b 0.384 ± 0.011bc 1.934 ± 0.024bc 4.036 0.543 ± 0.018b
10 1.725 ± 0.091a 0.441 ± 0.037ab 2.166 ± 0.128ab 3.912 0.588 ± 0.038a
20 1.796 ± 0.058a 0.486 ± 0.027a 2.282 ± 0.085ab 3.695 0.607 ± 0.015a
40 1.805 ± 0.050a 0.495 ± 0.066a 2.300 ± 0.116a 3.646 0.613 ± 0.014a
Values are means (±SE) of four replicate pots. Different lowercase letters within a columnindicate significant differences based on one-way
analysis of variance in SPSS 13.0 followed by the least significant difference test ( p20 ?mol/L (Table 3). All of the ABA
treatments increased Cd contents in the roots, stems,
leaves, and shoots of the two ecotypes, and the
maxima of the Cd contents in the roots, stems, leaves,
and shoots of the two ecotypes were all at 20 ?mol/L
ABA. Rubio et al. ( 1994) showed that ABA (19 ?mol/
L) significantly reduced the nickel (by 60 %) and cad-
mium (by 50 %) contents in rice shoots compared with
the control, but there was no significant change in the
roots; other studies showed similar results in rice (Hsu
and Kao 2003). Under Cd stress, when ABA was ap-
plied to the plant, the soluble protein and proline con-
tents of the plant increased, and the activities of super-
oxide dismutase, catalase, and ascorbate peroxidase in-
creased (Zhang et al. 2007). For common plants (such as
rice), ABA enhances resistance to Cd stress, so the plant
can decrease Cd absorption; for hyperaccumulators or
accumulators, ABA also enhances their resistance to Cd
stress and further increases Cd absorption. The Cd con-
tent in the shoots of the mining ecotype significantly
( p ; 0.05) increased by 12.17, 14.21, 20.76, 33.92, and
17.70 % at 1, 5, 10, 20, and 40 ?mol/L ABA, respec-
tively, compared with that of the control. The Cd content
in the shoots of the farmland ecotype significantly
( p 20 ?mol/L, but there was no obvious trend for the
farmland ecotype (Table 3).
Cd extraction by S. photeinocarpum
With the increase in ABA concentration, the Cd extrac-
tion by the roots of the two ecotypes of
S. photeinocarpum increased (Table4). However, the
Cd extractions by the stems, leaves, and shoots of the
two ecotypes increased when ABA was ?20 ?mol/L and
decreased when ABA was ;20 ?mol/L. The maxima
Environ Monit Assess (2016) 188: 182 Page 5 of 8182

and percentage increase in Cd extractions by the stems,
leaves and shoots of the mining ecotype were 318.12,
251.30, and 569.42?g/plant, and 60.60, 68.36, and
63.94 % ( p; 0.05), respectively, compared with that of
the control. The maxima and percentage increase in Cd extractions by the stems, leaves, and shoots of the farm-
land ecotype were 223.95, 296.56, and 520.51
?g/plant,
and 34.02, 49.85, and 42.60 % ( p

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