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Journal of Plant Nutrition, 38:497–508, 2015
Copyright C Taylor & Francis Group, LLC
ISSN: 0190-4167 print / 1532-4087 online
DOI: 10.1080/01904167.2014.934476
STRESS INDUCED BY HEAVY METALS CD AND PB IN BEAN
(PHASEOLUS VULGARIS L.) GROWN IN NUTRIENT SOLUTION
Marcele G. Cannata,1
Alexandre C. Bertoli,1
Ruy Carvalho,1
Amanda S.
Augusto,1
Ana Rosa R. Bastos,2
Matheus P. Freitas,1
and Janice G. Carvalho2
1
Department of Chemistry, Federal University of Lavras, Lavras, Brazil
2
Department of Soil Science, Federal University of Lavras, Lavras, Brazil
2 The increasing number of cases of soil contamination by heavy metals has affected crop yields,
and represents an imminent risk to food. Some of these contaminants, such as cadmium (Cd) and
lead (Pb), are very similar to micronutrients, and thus can be absorbed by plants. This study eval-
uated the translocation of increasing amounts of cadmium and lead and the effects of these metals
in the production of beans. Bean plants were grown in nutrient solution Clark and subjected to in-
creasing levels of Cd (from 0 to 0.5 mg L−1
) and Pb (from 0 to 10 mg L−1
). Cadmium concentration
of 0.1 mg L−1
translocated 39.8% to the shoot, and dry matter production was reduced by 45% in
shoots and 80% in roots, compared to the control treatment. Lead showed impaired movement in
the plant, however the concentration of 1.0 mg L−1
was observed in 5.7% of metal translocation to
the leaves. The concentration of 10 mg L−1
Pb reduced dry matter production of roots and shoots in
83% and 76%, respectively, compared to the control treatment.
Keywords: cadmium, lead, nutritive solution, Phaseolus vulgaris L.
INTRODUCTION
Aquatic ecosystems and soils constitute the main receptor of heavy metals
of both natural origin (such as rocks) and of anthropogenic nature, like
mining activities, industries and the excessive use of fertilizers (Paim et al.,
2006). Although some metals are essential for living systems [iron (Fe),
manganese (Mn), copper (Cu), zinc (Zn), etc.], others like cadmium (Cd)
and lead (Pb) are carcinogenic, mutagenic, or deleterious to metabolic
processes (Hadjiliadis, 1997). Soils seem to be an apparent natural barrier
to protect underground water; however, the comprehension of the activity
of heavy metals in soils is difficult, given the complexity of this system, which
Received 18 April 2012; accepted 20 May 2013.
Address correspondence to Alexandre C. Bertoli, Department of Chemistry, Federal University of
Lavras, PO Box 3037, 37200-000 Lavras, MG, Brazil. E-mail: bertolialexandre@yahoo.com.br
497
498 M. G. Cannata et al.
is composed of liquid, solid, and gas phases. Several factors like contents
and types of clay, pH, capability of cations exchange, content of organic
matter, and others affect adsorption/desorption, precipitation/dissolution,
complexation, and redox reactions of metals in soil (Carvalho et al., 2008).
Nutritive solutions, underused at commercial scales, means the use of
aqueous solutions containing essential minerals for the vegetable produc-
tion without the direct use of soil. It is a technique potentially useful for
the food production at large scale due to the decreasing area available for
plantation worldwide; in Brazil, this is particularly due to the expansive area
required for sugar-cane cultivation, cattle breeding and to the deforesting,
as a consequence of population increasing and migration to cities, especially
in the 2000s (IBGE, 2006). Therefore, nutritive solution is a suitable en-
vironment for the availability of metals, favoring their transportation from
the nutritive solution to the cultures and allowing more robust studies on
translocation, absorption kinetics and redistribution of minerals in plants
(Bell et al., 1991; Qu et al., 2003).
Vegetables like bean are rich in proteins even when cooked (6% to
11%), in addition to fibers, vitamins, and minerals, and therefore they are
important source of energy for low-income populations (IBGE, 2006). The
world production in 23.2 million hectares is ca. 16.8 tons (FAO, 2007). Brazil,
together with India, China, Myanmar, and Mexico are responsible for 65%
of the world production, whose main importers are the United States of
America (USA), India, Cuba, Japan, and United Kingdom; among them,
only USA shows an enhanced trend of importation (FAO, 2007).
Overall, the goal of this work is a) to study the effect of increasing dosages
of Cd and Pb on the production of bean in nutritive solution system; b) to
evaluate the translocation of Cd and Pb in bean plants; c) to show and discuss
the tolerance limits of bean plants to Cd and Pb, with respect to the ability of
influencing production and; d) to compare the behavior of a given variety
of bean plant cultivated in nutritive solution system and soils.
MATERIALS AND METHODS
The experiments were carried out in greenhouse using nutritive solution
cultivation by 75 days, corresponding to the vegetative cycle of bean plants.
The treatments constituted of increasing concentrations of Cd (0, 0.025,
0.1, 0.25, and 0.5 mg L−1
) and Pb (0, 0.25, 1, 5, and 10 mg L−1
) added
to the Clark’s nutritive solution (1973), using cadmium nitrate tetrahydrate
[Cd(NO3)2.4H2O] and lead nitrate [Pb(NO3)2] as contaminants in nutritive
solution system. These contents were chosen by taking into account those
values that intoxicate without eliminate plants during cultivation, as reported
elsewhere (Malavolta, 1994), in order to obtain vegetal material enough for
laboratorial analysis. The bean plant (Phaseolus vulgaris L.) was developed
Cadmium and Lead on Phaseolus vulgaris L. 499
in opaque 2L plastic containers, and the solutions were constantly aerated
using plastic tubes and compressor.
Seeds were irrigated with demineralized water in order to keep them
wet during 14 days. Plants were removed to a Clark’s solution at 25% of
the maximum concentration after growing ca. 8 cm, where they were main-
tained by 7 days. The solution was replaced by another one with 50% of
the maximum concentration. After one week, the solution was replaced by
another solution with 75% of the maximum concentration. Exchange of the
nutritive solution at 75% of the maximum concentration and the addition of
metals were performed once a week, during 8 weeks. The gradual increase of
nutritive solution aimed at adapting the plants to different chemical media;
75% of the maximum concentration was enough for a good cultivation.
After finishing the vegetative cycle, plants were separated into aerial part,
root system and husks, washed with deionized water and dried at 65–70◦
C
until constant mass. The material was ground and digested using a 2:1 (v/v)
nitroperchloric solution [nitric acid (HNO3):perchloric acid (HClO4)]
(Malavolta et al., 1997). The contents of Cd and Pb of the dry matter of
the aerial portion (DMAP), of the root system (DMRS), and of fruits (DMF)
and were quantified using a Varian flame absorption spectrophotometer,
with acetylene flame and hollow cathode lamp: Cd (228.8 nm, 0.5 crack)
and Pb (217 nm, 1.0 crack).
The potential of plants in uptaking Cd and Pb from the nutritive solution
was measured by the phytoextraction coefficient or transfer factor, t, using
the following relation.
t = total metal in plant/metal in solution
The calculations were performed by considering the contents of Cd and
Pb in DMAP+DMRS+DMF, in all concentrations used; the larger this factor,
the larger the contaminant absorption (Henry, 2000).
The relative production index (RP), related to the influence of the metal
on the variation of dry matter production (DMAP+DMRS), is obtained by:
RP(%) = (dry matter produced using a given metal content/dry matter
produced with metal absent) × 100
The translocation index (TI) gives the capability of species in translocat-
ing Cd and Pb from root to the aerial portion (Paiva et al., 2002):
TI = [MDAP/(DMAP + DMRS + DMF)] × 100
TI = [MDF/(DMAP + DMRS + DMF)] × 100
500 M. G. Cannata et al.
TABLE 1 Plant behavior in the presence of Cd: production of dry matter of the root system (DMRS), of
the aerial portion (DMAP), and of the fruits (DMF), and relative production index of root, aerial
portion and fruits
Dry matter (weight, in g) Relative production index (%)
Doses Cd (mg L−1) DMRS DMAP DMF DMRS DMAP DMF
0 2.87 6.67 2.21 100.00 100.00 100.00
0.025 2.04 5.70 4.44 71.07 85.48 200.52
0.1 0.58 3.63 3.44 20.40 54.38 155.37
0.25 0.36 2.04 1.21 12.69 30.53 54.77
0.5 0.27 1.46 0.32 9.63 21.94 14.39
Significant data at 5% of probability according to the Tukey test.
The experiment was arranged in a completely randomized factorial
(2×5)×4 design (two metals, Cd and Pb, and five dosages for each metal:
Cd: 0, 0.025, 0.10, 0.25, and 0.5 mg L−1
, and Pb: 0, 0.25, 1, 5, and 10 mg
L−1
, with four replicates. The average results were submitted to Tukey’s test
(5% probability) using the SISVAR program (SisVar International, Rueil
Malmaison, France) (Ferreira, 2011).
In this work, the effects of Cd and Pb on the bean plant using nutritive
solution are compared to those evaluated by Carvalho et al. (2008, 2009) for
this plant in latosols, namely humic red-yellow latosol (RYLh) and dystrophic
red latosol (RLd), which are representative soils in the Brazilian agriculture
and significantly different to each other with regard to the contents of clay
and organic matter. Carvalho et al. (2008, 2009) have used the following
contents of metals: 0; 5; 10; and 20 mg L−1
for Cd, and 0; 125; 250; and
500 mg L−1
for Pb, which are significantly larger than those dosages applied
in nutritive solution. This difference is due to the heterogeneity of soil, which
affects more the activity and kinetics of mineral absorption when compared
to the nutritive solution.
RESULTS AND DISCUSSION
Different dosages of Cd and Pb applied in nutritive solution affected the
production of dry matter in diverse ways, as well as the relative production
index, the absorption, the translocation index and the transfer index of the
bean plant (Phaseolus vulgaris L.); statistics and discussions are presented as
follows.
Productivity (Cadmium)
The development of bean plants was monitored at different cadmium
dosages, and the relative average data are shown in Table 1. It has been found
in DMF (Table 1) a fruit production 100% larger at 0.025 mg L−1
of Cd
Cadmium and Lead on Phaseolus vulgaris L. 501
TABLE 2 Content of cadmium in the root system, aerial portion and fruits of bean plants
Content (mg kg−1) TI (%)
Doses Cd (mg L−1) Roots Aerial portion Fruits Aerial portion Fruits t (%)
0 0.00 0.00 0.00 0.00 0.00 0.00
0.025 26.72 13.13 3.18 31.78 7.38 0.88
0.1 52.65 37.63 4.38 39.80 4.65 0.45
0.25 107.85 58.75 7.12 33.82 4.10 0.16
0.5 263.40 145.83 12.78 32.99 2.89 0.11
TI: Translocation index, t: transfer factor. Significant data at 5% of probability according to the Tukey
test.
when compared to the control treatment, but the result was different when
dealing with the root and aerial portion: the production of DMRS decreased
by 29% and DMAP by 15%. An inverse relationship is also observed between
Cd dosages in the nutritive solution and the production of roots and aerial
portion, but not fruits. The production of husks and grains (DMF) increased
by ca. 55% for the plants under 0.1 mg L−1
of Cd, while DMAP reduced by
45% when compared to the control treatment, and by 31% in comparison
to the 0.025 mg L−1
dosage. The production of DMRS was 80% below that
of the control treatment, and 51% lower than that obtained at the 0.025 mg
L−1
dosage. Despite the reduction of DMRS and DMAP until 0.025 mg L−1
of Cd, similar phenomenon was not observed for DMF (husks and grains),
which is the main goal of cultivating beans either in nutritive solution or soil;
opposite to expected, a benefit for the production of grains was found.
It is supposed that a competitive effect (antagonism) between Cd and
some essential elements takes place when one relates the increasing dosages
of Cd to the relative production index (RP) in Table 1. Significant increases
occurred in the production of fruits at the 0.025 and 0.1 mg L−1
dosages; it
seems that, at balanced contents of Zn in the nutritive solution, the amounts
of Cd utilized (especially 0.025 mg L−1
) were low enough to facilitate the
absorption of Zn by roots. According to Faquin (2005), there is a competition
(antagonism) between Zn and Cd for the absorption by plants. Therefore, it
is reasonable to assume, among the possible antagonistic effects, the stimulus
of the very low concentration of Cd (e.g. 0.025 mg L−1
) to a higher absorption
of Zn, an essential element.
The greater weight of DMF for the plants cultivated in solution with
0.025 mg L−1
of Cd is also supposed to be due to the Cd × Zn competition.
The 0.25 and 0.5 mg L−1
dosages of Cd were statistically similar for the root
system, while the plant growing was inversely proportional to the remaining
dosages. By comparing Tables 1 and 2, this latter behavior was also observed
for DMAP, with a significant deleterious effect in the plant development at
the 0.5 mg L−1
dosage.
502 M. G. Cannata et al.
Injuries to bean plants (Phaseolus vulgaris L.) caused by Cd in soils
differed from those discussed in this work, mainly with respect to the
antagonism Cd × essential elements. Carvalho et al. (2009) have studied
the development of bean plants under the Cd dosages of 0, 5, 10 and 20 mg
L−1
, in humic red-yellow (RYLh) and dystrophic red (RLd) latosols; the
dry matter of the aerial portion was negatively affected from the 5 mg L−1
dosage of Cd. In that work, the production of DMAP decreased by ca. 66%
when comparing the control treatment and the maximum dosage applied,
in both latosols. Moreover, the authors found a decreased production of
fruits (husks and grains) with increasing the applied dosages, reaching a
reduction of 93% in production at the 20 mg L−1
dosage when compared
to the treatment control, in both soil types.
Opposite to nutritive solution condition, all dosages of Cd applied by
Carvalho et al. (2009) were toxic to the bean plant. A preliminary comparison
of nutritive solution and soil shows that the homogeneity of the nutritive
solution enhances the toxicity of Cd at lower dosages than those applied
in soils. There was a significant difference in the amounts of Cd and Pb
utilized in this work and by Carvalho et al. (2009), since nutritive solution
offers larger mobility to metals. According to the value established by the
Brazilian Ministry of Health (2005), the potable standard of Pb is 0.01 mg
L−1
, the same content adopted by the United States; the corresponding
value for Cd is 0.005 mg L−1
. These limits explain the difference of ten
times between the Cd and Pb dosages utilized in this work. In the soil, the
National Council of Environment (CONAMA, 2006), Brazil, imposes the
maximum concentration of Cd and Pb in sewage sludge of 39 and 300 mg
kg−1
, respectively, with annual maximum limits of 1.9 and 15 kg ha−1
for Cd
and Pb, respectively.
Content and Translocation (Cadmium)
The absorption of Cd by bean plants depends on the applied dosages,
as illustrated in Table 2. According to Table 2, the absorption was directly
proportional to the available amount of metal in all three moieties of the
plant. However, there was a clear difference among the amounts absorbed
at the 0, 0.025, 0.1, 0.25, and 0.5 mg L−1
dosages, the respective absorptions
were 0, 16.4, 52.6, 107.8, and 263.4 mg kg−1
for DMRS, 0, 9.1, 37.6, 58.8, and
145.8 mg kg−1
for DMAP, and 0, 3.2, 4.4, 7.1, and 12.8 mg kg−1
for DMF.
Therefore, it can be concluded that Cd translocates very poorly throughout
the plant, given the significant difference of contaminant found in the three
plant compartments (higher in the roots).
The translocation index (TI) indicates the amount of metal translocated
from the roots to aerial portion and fruits; in the aerial portion, Cd was
translocated mostly at the 0.1 mg L−1
dosage (39.8%), followed by the 0.25,
0.5, and 0.025 mg L−1
dosages, with 33.8, 33.0, and 31.8% of translocation,
Cadmium and Lead on Phaseolus vulgaris L. 503
respectively (Table 2). The largest TI for the fruits was computed at the
0.025 mg L−1
dosage (7.4%), followed by the 0.1 (4.6%), 0.25 (4.1%), and
0.5 mg L−1
(2.9%) dosages. The largest translocation to fruits was found for
the lowest dosage applied (0.025 mg L−1
), decreasing with increasing the
availability of the metal. The transfer factor t (Table 2) exhibited a direct
relationship to TI for the fruits.
The toxicity of Cd to plants and other living systems relates to the abil-
ity of this metal in combining with chemical groups in enzymes involved
in metabolism. According to Baird (2002), the reaction Cd2+
+ 2R–SH →
R–S–Cd–S–R + 2H+
is responsible for diminishing the activity of enzymes or
even for their inactivation; this author suggests ethylenediamenetetraacetic
acid (EDTA) solution at pH 6.5 to remedy Cd intoxication in animals, ac-
cording to the following reaction: CdS2R2 + [H2EDTA] → [Cd(EDTA)] +
2R–SH.
The facility of Cd2+
to combine with electron donors in free amino
acids and proteins has been confirmed by Silva et al. (2007a, 2007b), who
synthesized diethylenetriaminepentacetic acid (DTPA) chelates with Cu, Zn,
Cd, and Pb, suggesting not only the intoxication pathway of plants by Cd, but
also the high performance of EDTA to remedy the organism intoxication
cited by Baird (2002). The remobilization of Cd in the plant is related to
phytochelatines (PC’s) (Guo and Marschner, 1995); the complex Cd-PC can
represent a mobile form to transport Cd from root to aerial portions. PC’s are
complex structures, forming peptides rich in cysteine, electron donor amino
acids. The –SH group of PC’s are able of forming coordination compounds
with heavy metals, such as Cd, decreasing their toxicity. Cadmium itself
induces the synthesis of chelatins, which will reduce its toxicity (Malavolta,
2006).
The chemical mechanisms proposed by Baird (2002), Silva et al. (2007a,
2007b), Guo and Marschner (1995), and Malavolta (2006) confirm not only
the deleterious effects of Cd, but especially those data of Tables 1 and 2,
which are related to the behavior of bean, especially with regard to the
production of fruits, in the presence of Cd.
Productivity (Lead)
Different dosages of lead applied to the nutritive solution of bean plant
led to the growing and production profiles of Table 3. According to the
results of Table 3 for DMRS and DMAP, the control treatment exhibited the
best development. The most important fruit production was achieved at the
0.25 mg L−1
of Pb, which is ca. 73% larger than the control treatment. For
DMF, the 1 and 5 mg L−1
dosages of Pb influenced positively the productivity
of bean plants, increasing by 60% and 42%, respectively, in comparison to
the control treatment.
504 M. G. Cannata et al.
TABLE 3 Plant behavior in the presence of Pb: production of dry matter of the root system (DMRS), of
the aerial portion (DMAP), and of the fruits (DMF) and relative production index of root, aerial
portion and fruits
Dry matter (weight, in g) Relative production index (%)
Doses Pb (mg L−1) DMRS DMAP DMF DMRS DMAP DMF
0 2.87 6.67 2.22 100.00 100.00 100.00
0.25 1.07 3.90 3.84 37.25 58.46 173.34
1.0 1.03 3.99 3.56 35.86 59.87 160.53
5.0 0.76 2.79 3.16 26.58 41.81 142.76
10.0 0.48 1.55 1.34 16.71 23.25 60.58
Significant data at 5% of probability according to the Tukey test.
The absorbed Pb accumulates in the cellular wall, particularly of roots,
and this seems to contribute for the diminishment of its toxic effect to the
plant, as well as its transportation to fruits (Faquin, 2005). This fact explains
the “beneficial effect” of some dosages of Pb to some plants; according to
Kabata-Pendias and Pendias (2001), the exclusion mechanism of Pb is in
fact the root deposition. This phenomenon occurs because of the linkage of
the metal to insoluble organic polymers like phosphates as electron donors,
forming amorphous precipitates.
The 0.25 and 1 mg L−1
dosages of Pb were statistically equivalent for
DMRS and DMAP (Table 3). The 10 mg L−1
showed the most substantial,
negative influence to the plant development, causing a production decay of
40% for DMF, 76% for DMAP, and 83% for DMRS (Table 3).
Similarly to Cd, Carvalho et al. (2009) analyzed the Pb effect on the
behavior of bean plant in two different latosols (in terms of contents of
clay and organic matter). The development of the bean plant (Phaseolus
vulgaris L.) were evaluated under the 0, 125, 250, and 500 mg L−1
dosages
of Pb, using the latosols RYLh and RLd; the production of DMAP decreased
with increasing the amount of Pb in RLd, while the 125 mg L−1
affected
only modestly the production of DMAP in RYLh – the production decreased
significantly at the 500 mg L−1
dosage (ca. 44%).
Carvalho et al. (2009) also investigated the production of grains, and Pb
caused a 18.5% and 30% reduction at the 125 and 250 mg L−1
dosages, re-
spectively, in RLd, while production was kept nearly unaltered in comparison
to the treatment control in RYLh at these dosages. There was an improved
production of grains between 250 and 500 mg L−1
for both soil types.
Content and Translocation (Lead)
The amount of lead absorbed by the plant was dependent on the
metal dosages, as shown in Table 4. Again, the absorption of metal was
proportional to the dosages applied, as measured in DMAP and DMRS
Cadmium and Lead on Phaseolus vulgaris L. 505
TABLE 4 Content of lead in the root system, aerial portion and fruits of bean plants
Content (mg kg−1) TI (%)
Doses Pb (mg L−1) Roots Aerial portion Fruits Aerial portion Fruits t (%)
0 0.00 0.00 0.00 0.00 0.00 0.00
0.25 480.73 11.73 6.20 2.62 1.38 0.99
1.0 1006.78 61.60 8.30 5.72 0.77 0.58
5.0 1763.48 82.68 47.05 3.49 1.99 0.20
10.0 2433.63 100.05 67.10 3.85 2.58 0.05
TI: Translocation index, t: transfer factor. Significant data at 5% of probability according to the Tukey
test.
(Table 4). For DMF, the absorptions at the 0.25 and 1 mg L−1
dosages were
statistically equivalent (Table 4).
Similarly to observed for Cd, the absorption of lead differed substantially
among the plant moieties studied, varying from 430 to 2433 mg kg−1
in the
root system, from ca. 12 to 100 mg kg−1
in the aerial portion, and from
6.2 to 67 mg kg−1
in the fruits (husks and grains), at the 0.25 and 10 mg
L−1
dosages of metal, respectively. This data indicate that lead translocates
very poorly throughout the plants, such as Cd, since there was an expressive
difference in the amount of Pb found in the three plant compartments.
Table 4 clears up the difficulty of Pb in mobilizing in the plants, due to
low translocation index. The most efficient dosage when the aerial portion is
analyzed is 1 mg L−1
, giving 5.7% of translocation; the corresponding value
for fruits is only 0.8%. The transfer of metals from solution to plants was
practically total at the 0.25 mg L−1
dosage, in which the factor t was 0.99,
and the difference between the extreme dosages reached 95% (Table 4).
Malavolta (1994) describes that the toxic effects of Pb, such as the dam-
ages to photosynthesis, mitosis and water absorption, and physical symptoms,
like dark green leafs, wilted old leafs and slight development of roots and
aerial portion, can be observed in plants, but they are not totally specific.
In the present work, various similar symptoms were observed in the plants
under the 5 and 10 mg L−1
dosages of Pb. Moreover, there is an interference
of Pb in the synthesis of chlorophyll together with a reduced transport of
Fe, which is necessary to the formation of heme groups. Therefore, leafs
experience a deficiency symptom (chlorosis), causing damages in stressed
plants (Fodor et al., 1998).
Carvalho et al. (2009) have also quantified the content of Pb uptaken
from bean plants cultivated in two latosols. The content of Pb in DMAP, at
the 250 mg L−1
dosage, was 21% and 26% in RLd and RYLh, respectively,
while the corresponding values at the 500 mg L−1
were 19% and 18%.
These results confirm the low translocation of Pb, even at higher dosages
in soils than in nutritive solution. Carvalho et al. (2008, 2009) confirmed
the low translocation of Cd and notably Pb, showing that, depending on the
dosage applied in the soil, these plants can be used for nutrition without
506 M. G. Cannata et al.
the risk to health, due to the insignificant content of metal in husks and
grains. These authors have also attributed the low translocation of Pb to
the steric hindrance of chelates formed between Pb and amino acids or
related substances of roots; this hypothesis corroborates the work by Silva
et al. (2007a, 2007b) on the synthesis and characterization of chelates based
on Pb, Cd, Zn, and Cu with diethylenetriaminepentacetic acid (DTPA), who
determined the high steric hindrance of the DTPA-Pb structure. This seems
to justify the difficulty of the metal in ascending in plant, since it remains
partially complexed to free amino acids, proteins or plant secretions, rich in
electron donors, such as DTPA.
The similar chemical behavior of Pb and Cd in plants (analogous to the
similarity between Cu and Zn) was also verified by Paim et al. (2006) in soil
contaminated by mining residues of Zn; after extraction of Zn from the min-
eral, the side products rich in Pb, Cd, and Zn cause serious environmental
problems to the soil.
The difference in translocation between Cd and Pb becomes evident
when comparing Tables 2 and 4; TI was significantly lower in the Pb-
containing medium than in the Cd-containing solution, especially for leafs.
An explanation for this finding lies on the periodic properties of these
metals, particularly the atomic radius (1.71 and 1.81 pm for Cd and Pb,
respectively) and density (8.6 and 11.3 g cm−3
for Cd and Pb, respectively);
these factors reflect the mobility and therefore the activity of Pb. In addition
to these properties, Antoniadis et al. (2007) and Oliveira et al. (2009) also
attribute the low mobility of Pb to the electronegativity.
CONCLUSIONS
Increasing dosages of Cd and Pb reduce the development of bean plants,
expressed in terms of dry matter of the aerial portion and root system. 0.025
and 0.1 mg L−1
dosages of Cd, and 0.25, 1, and 5 mg L−1
of Pb contribute
for the increasing production of fruits (husks and grains) in bean plants.
This behavior has also been observed in latosols. Cadmium and mainly Pb
translocate very poorly in plants, and therefore they are concentrated in the
roots. Increments in the absorption of Zn by bean plants at low dosages of
Cd and Pb seem to explain the increasing in the production of fruits. Low
translocation of metals and the increasing production of fruits by bean plants
cultivated both in nutritive solution and soils contaminated with Cd and Pb
do not allow pointing out toward the consume of grains, since there still
remains controversy regarding the tolerability of organisms to these metals.
FUNDING
CAPES and CNPq are gratefully acknowledged for the studentship and
fellowship (to M.G.C. and M.P.F.).
Cadmium and Lead on Phaseolus vulgaris L. 507
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Stress induzido por metais pesados Cd e Pb em feijoeiro

  • 1. Journal of Plant Nutrition, 38:497–508, 2015 Copyright C Taylor & Francis Group, LLC ISSN: 0190-4167 print / 1532-4087 online DOI: 10.1080/01904167.2014.934476 STRESS INDUCED BY HEAVY METALS CD AND PB IN BEAN (PHASEOLUS VULGARIS L.) GROWN IN NUTRIENT SOLUTION Marcele G. Cannata,1 Alexandre C. Bertoli,1 Ruy Carvalho,1 Amanda S. Augusto,1 Ana Rosa R. Bastos,2 Matheus P. Freitas,1 and Janice G. Carvalho2 1 Department of Chemistry, Federal University of Lavras, Lavras, Brazil 2 Department of Soil Science, Federal University of Lavras, Lavras, Brazil 2 The increasing number of cases of soil contamination by heavy metals has affected crop yields, and represents an imminent risk to food. Some of these contaminants, such as cadmium (Cd) and lead (Pb), are very similar to micronutrients, and thus can be absorbed by plants. This study eval- uated the translocation of increasing amounts of cadmium and lead and the effects of these metals in the production of beans. Bean plants were grown in nutrient solution Clark and subjected to in- creasing levels of Cd (from 0 to 0.5 mg L−1 ) and Pb (from 0 to 10 mg L−1 ). Cadmium concentration of 0.1 mg L−1 translocated 39.8% to the shoot, and dry matter production was reduced by 45% in shoots and 80% in roots, compared to the control treatment. Lead showed impaired movement in the plant, however the concentration of 1.0 mg L−1 was observed in 5.7% of metal translocation to the leaves. The concentration of 10 mg L−1 Pb reduced dry matter production of roots and shoots in 83% and 76%, respectively, compared to the control treatment. Keywords: cadmium, lead, nutritive solution, Phaseolus vulgaris L. INTRODUCTION Aquatic ecosystems and soils constitute the main receptor of heavy metals of both natural origin (such as rocks) and of anthropogenic nature, like mining activities, industries and the excessive use of fertilizers (Paim et al., 2006). Although some metals are essential for living systems [iron (Fe), manganese (Mn), copper (Cu), zinc (Zn), etc.], others like cadmium (Cd) and lead (Pb) are carcinogenic, mutagenic, or deleterious to metabolic processes (Hadjiliadis, 1997). Soils seem to be an apparent natural barrier to protect underground water; however, the comprehension of the activity of heavy metals in soils is difficult, given the complexity of this system, which Received 18 April 2012; accepted 20 May 2013. Address correspondence to Alexandre C. Bertoli, Department of Chemistry, Federal University of Lavras, PO Box 3037, 37200-000 Lavras, MG, Brazil. E-mail: bertolialexandre@yahoo.com.br 497
  • 2. 498 M. G. Cannata et al. is composed of liquid, solid, and gas phases. Several factors like contents and types of clay, pH, capability of cations exchange, content of organic matter, and others affect adsorption/desorption, precipitation/dissolution, complexation, and redox reactions of metals in soil (Carvalho et al., 2008). Nutritive solutions, underused at commercial scales, means the use of aqueous solutions containing essential minerals for the vegetable produc- tion without the direct use of soil. It is a technique potentially useful for the food production at large scale due to the decreasing area available for plantation worldwide; in Brazil, this is particularly due to the expansive area required for sugar-cane cultivation, cattle breeding and to the deforesting, as a consequence of population increasing and migration to cities, especially in the 2000s (IBGE, 2006). Therefore, nutritive solution is a suitable en- vironment for the availability of metals, favoring their transportation from the nutritive solution to the cultures and allowing more robust studies on translocation, absorption kinetics and redistribution of minerals in plants (Bell et al., 1991; Qu et al., 2003). Vegetables like bean are rich in proteins even when cooked (6% to 11%), in addition to fibers, vitamins, and minerals, and therefore they are important source of energy for low-income populations (IBGE, 2006). The world production in 23.2 million hectares is ca. 16.8 tons (FAO, 2007). Brazil, together with India, China, Myanmar, and Mexico are responsible for 65% of the world production, whose main importers are the United States of America (USA), India, Cuba, Japan, and United Kingdom; among them, only USA shows an enhanced trend of importation (FAO, 2007). Overall, the goal of this work is a) to study the effect of increasing dosages of Cd and Pb on the production of bean in nutritive solution system; b) to evaluate the translocation of Cd and Pb in bean plants; c) to show and discuss the tolerance limits of bean plants to Cd and Pb, with respect to the ability of influencing production and; d) to compare the behavior of a given variety of bean plant cultivated in nutritive solution system and soils. MATERIALS AND METHODS The experiments were carried out in greenhouse using nutritive solution cultivation by 75 days, corresponding to the vegetative cycle of bean plants. The treatments constituted of increasing concentrations of Cd (0, 0.025, 0.1, 0.25, and 0.5 mg L−1 ) and Pb (0, 0.25, 1, 5, and 10 mg L−1 ) added to the Clark’s nutritive solution (1973), using cadmium nitrate tetrahydrate [Cd(NO3)2.4H2O] and lead nitrate [Pb(NO3)2] as contaminants in nutritive solution system. These contents were chosen by taking into account those values that intoxicate without eliminate plants during cultivation, as reported elsewhere (Malavolta, 1994), in order to obtain vegetal material enough for laboratorial analysis. The bean plant (Phaseolus vulgaris L.) was developed
  • 3. Cadmium and Lead on Phaseolus vulgaris L. 499 in opaque 2L plastic containers, and the solutions were constantly aerated using plastic tubes and compressor. Seeds were irrigated with demineralized water in order to keep them wet during 14 days. Plants were removed to a Clark’s solution at 25% of the maximum concentration after growing ca. 8 cm, where they were main- tained by 7 days. The solution was replaced by another one with 50% of the maximum concentration. After one week, the solution was replaced by another solution with 75% of the maximum concentration. Exchange of the nutritive solution at 75% of the maximum concentration and the addition of metals were performed once a week, during 8 weeks. The gradual increase of nutritive solution aimed at adapting the plants to different chemical media; 75% of the maximum concentration was enough for a good cultivation. After finishing the vegetative cycle, plants were separated into aerial part, root system and husks, washed with deionized water and dried at 65–70◦ C until constant mass. The material was ground and digested using a 2:1 (v/v) nitroperchloric solution [nitric acid (HNO3):perchloric acid (HClO4)] (Malavolta et al., 1997). The contents of Cd and Pb of the dry matter of the aerial portion (DMAP), of the root system (DMRS), and of fruits (DMF) and were quantified using a Varian flame absorption spectrophotometer, with acetylene flame and hollow cathode lamp: Cd (228.8 nm, 0.5 crack) and Pb (217 nm, 1.0 crack). The potential of plants in uptaking Cd and Pb from the nutritive solution was measured by the phytoextraction coefficient or transfer factor, t, using the following relation. t = total metal in plant/metal in solution The calculations were performed by considering the contents of Cd and Pb in DMAP+DMRS+DMF, in all concentrations used; the larger this factor, the larger the contaminant absorption (Henry, 2000). The relative production index (RP), related to the influence of the metal on the variation of dry matter production (DMAP+DMRS), is obtained by: RP(%) = (dry matter produced using a given metal content/dry matter produced with metal absent) × 100 The translocation index (TI) gives the capability of species in translocat- ing Cd and Pb from root to the aerial portion (Paiva et al., 2002): TI = [MDAP/(DMAP + DMRS + DMF)] × 100 TI = [MDF/(DMAP + DMRS + DMF)] × 100
  • 4. 500 M. G. Cannata et al. TABLE 1 Plant behavior in the presence of Cd: production of dry matter of the root system (DMRS), of the aerial portion (DMAP), and of the fruits (DMF), and relative production index of root, aerial portion and fruits Dry matter (weight, in g) Relative production index (%) Doses Cd (mg L−1) DMRS DMAP DMF DMRS DMAP DMF 0 2.87 6.67 2.21 100.00 100.00 100.00 0.025 2.04 5.70 4.44 71.07 85.48 200.52 0.1 0.58 3.63 3.44 20.40 54.38 155.37 0.25 0.36 2.04 1.21 12.69 30.53 54.77 0.5 0.27 1.46 0.32 9.63 21.94 14.39 Significant data at 5% of probability according to the Tukey test. The experiment was arranged in a completely randomized factorial (2×5)×4 design (two metals, Cd and Pb, and five dosages for each metal: Cd: 0, 0.025, 0.10, 0.25, and 0.5 mg L−1 , and Pb: 0, 0.25, 1, 5, and 10 mg L−1 , with four replicates. The average results were submitted to Tukey’s test (5% probability) using the SISVAR program (SisVar International, Rueil Malmaison, France) (Ferreira, 2011). In this work, the effects of Cd and Pb on the bean plant using nutritive solution are compared to those evaluated by Carvalho et al. (2008, 2009) for this plant in latosols, namely humic red-yellow latosol (RYLh) and dystrophic red latosol (RLd), which are representative soils in the Brazilian agriculture and significantly different to each other with regard to the contents of clay and organic matter. Carvalho et al. (2008, 2009) have used the following contents of metals: 0; 5; 10; and 20 mg L−1 for Cd, and 0; 125; 250; and 500 mg L−1 for Pb, which are significantly larger than those dosages applied in nutritive solution. This difference is due to the heterogeneity of soil, which affects more the activity and kinetics of mineral absorption when compared to the nutritive solution. RESULTS AND DISCUSSION Different dosages of Cd and Pb applied in nutritive solution affected the production of dry matter in diverse ways, as well as the relative production index, the absorption, the translocation index and the transfer index of the bean plant (Phaseolus vulgaris L.); statistics and discussions are presented as follows. Productivity (Cadmium) The development of bean plants was monitored at different cadmium dosages, and the relative average data are shown in Table 1. It has been found in DMF (Table 1) a fruit production 100% larger at 0.025 mg L−1 of Cd
  • 5. Cadmium and Lead on Phaseolus vulgaris L. 501 TABLE 2 Content of cadmium in the root system, aerial portion and fruits of bean plants Content (mg kg−1) TI (%) Doses Cd (mg L−1) Roots Aerial portion Fruits Aerial portion Fruits t (%) 0 0.00 0.00 0.00 0.00 0.00 0.00 0.025 26.72 13.13 3.18 31.78 7.38 0.88 0.1 52.65 37.63 4.38 39.80 4.65 0.45 0.25 107.85 58.75 7.12 33.82 4.10 0.16 0.5 263.40 145.83 12.78 32.99 2.89 0.11 TI: Translocation index, t: transfer factor. Significant data at 5% of probability according to the Tukey test. when compared to the control treatment, but the result was different when dealing with the root and aerial portion: the production of DMRS decreased by 29% and DMAP by 15%. An inverse relationship is also observed between Cd dosages in the nutritive solution and the production of roots and aerial portion, but not fruits. The production of husks and grains (DMF) increased by ca. 55% for the plants under 0.1 mg L−1 of Cd, while DMAP reduced by 45% when compared to the control treatment, and by 31% in comparison to the 0.025 mg L−1 dosage. The production of DMRS was 80% below that of the control treatment, and 51% lower than that obtained at the 0.025 mg L−1 dosage. Despite the reduction of DMRS and DMAP until 0.025 mg L−1 of Cd, similar phenomenon was not observed for DMF (husks and grains), which is the main goal of cultivating beans either in nutritive solution or soil; opposite to expected, a benefit for the production of grains was found. It is supposed that a competitive effect (antagonism) between Cd and some essential elements takes place when one relates the increasing dosages of Cd to the relative production index (RP) in Table 1. Significant increases occurred in the production of fruits at the 0.025 and 0.1 mg L−1 dosages; it seems that, at balanced contents of Zn in the nutritive solution, the amounts of Cd utilized (especially 0.025 mg L−1 ) were low enough to facilitate the absorption of Zn by roots. According to Faquin (2005), there is a competition (antagonism) between Zn and Cd for the absorption by plants. Therefore, it is reasonable to assume, among the possible antagonistic effects, the stimulus of the very low concentration of Cd (e.g. 0.025 mg L−1 ) to a higher absorption of Zn, an essential element. The greater weight of DMF for the plants cultivated in solution with 0.025 mg L−1 of Cd is also supposed to be due to the Cd × Zn competition. The 0.25 and 0.5 mg L−1 dosages of Cd were statistically similar for the root system, while the plant growing was inversely proportional to the remaining dosages. By comparing Tables 1 and 2, this latter behavior was also observed for DMAP, with a significant deleterious effect in the plant development at the 0.5 mg L−1 dosage.
  • 6. 502 M. G. Cannata et al. Injuries to bean plants (Phaseolus vulgaris L.) caused by Cd in soils differed from those discussed in this work, mainly with respect to the antagonism Cd × essential elements. Carvalho et al. (2009) have studied the development of bean plants under the Cd dosages of 0, 5, 10 and 20 mg L−1 , in humic red-yellow (RYLh) and dystrophic red (RLd) latosols; the dry matter of the aerial portion was negatively affected from the 5 mg L−1 dosage of Cd. In that work, the production of DMAP decreased by ca. 66% when comparing the control treatment and the maximum dosage applied, in both latosols. Moreover, the authors found a decreased production of fruits (husks and grains) with increasing the applied dosages, reaching a reduction of 93% in production at the 20 mg L−1 dosage when compared to the treatment control, in both soil types. Opposite to nutritive solution condition, all dosages of Cd applied by Carvalho et al. (2009) were toxic to the bean plant. A preliminary comparison of nutritive solution and soil shows that the homogeneity of the nutritive solution enhances the toxicity of Cd at lower dosages than those applied in soils. There was a significant difference in the amounts of Cd and Pb utilized in this work and by Carvalho et al. (2009), since nutritive solution offers larger mobility to metals. According to the value established by the Brazilian Ministry of Health (2005), the potable standard of Pb is 0.01 mg L−1 , the same content adopted by the United States; the corresponding value for Cd is 0.005 mg L−1 . These limits explain the difference of ten times between the Cd and Pb dosages utilized in this work. In the soil, the National Council of Environment (CONAMA, 2006), Brazil, imposes the maximum concentration of Cd and Pb in sewage sludge of 39 and 300 mg kg−1 , respectively, with annual maximum limits of 1.9 and 15 kg ha−1 for Cd and Pb, respectively. Content and Translocation (Cadmium) The absorption of Cd by bean plants depends on the applied dosages, as illustrated in Table 2. According to Table 2, the absorption was directly proportional to the available amount of metal in all three moieties of the plant. However, there was a clear difference among the amounts absorbed at the 0, 0.025, 0.1, 0.25, and 0.5 mg L−1 dosages, the respective absorptions were 0, 16.4, 52.6, 107.8, and 263.4 mg kg−1 for DMRS, 0, 9.1, 37.6, 58.8, and 145.8 mg kg−1 for DMAP, and 0, 3.2, 4.4, 7.1, and 12.8 mg kg−1 for DMF. Therefore, it can be concluded that Cd translocates very poorly throughout the plant, given the significant difference of contaminant found in the three plant compartments (higher in the roots). The translocation index (TI) indicates the amount of metal translocated from the roots to aerial portion and fruits; in the aerial portion, Cd was translocated mostly at the 0.1 mg L−1 dosage (39.8%), followed by the 0.25, 0.5, and 0.025 mg L−1 dosages, with 33.8, 33.0, and 31.8% of translocation,
  • 7. Cadmium and Lead on Phaseolus vulgaris L. 503 respectively (Table 2). The largest TI for the fruits was computed at the 0.025 mg L−1 dosage (7.4%), followed by the 0.1 (4.6%), 0.25 (4.1%), and 0.5 mg L−1 (2.9%) dosages. The largest translocation to fruits was found for the lowest dosage applied (0.025 mg L−1 ), decreasing with increasing the availability of the metal. The transfer factor t (Table 2) exhibited a direct relationship to TI for the fruits. The toxicity of Cd to plants and other living systems relates to the abil- ity of this metal in combining with chemical groups in enzymes involved in metabolism. According to Baird (2002), the reaction Cd2+ + 2R–SH → R–S–Cd–S–R + 2H+ is responsible for diminishing the activity of enzymes or even for their inactivation; this author suggests ethylenediamenetetraacetic acid (EDTA) solution at pH 6.5 to remedy Cd intoxication in animals, ac- cording to the following reaction: CdS2R2 + [H2EDTA] → [Cd(EDTA)] + 2R–SH. The facility of Cd2+ to combine with electron donors in free amino acids and proteins has been confirmed by Silva et al. (2007a, 2007b), who synthesized diethylenetriaminepentacetic acid (DTPA) chelates with Cu, Zn, Cd, and Pb, suggesting not only the intoxication pathway of plants by Cd, but also the high performance of EDTA to remedy the organism intoxication cited by Baird (2002). The remobilization of Cd in the plant is related to phytochelatines (PC’s) (Guo and Marschner, 1995); the complex Cd-PC can represent a mobile form to transport Cd from root to aerial portions. PC’s are complex structures, forming peptides rich in cysteine, electron donor amino acids. The –SH group of PC’s are able of forming coordination compounds with heavy metals, such as Cd, decreasing their toxicity. Cadmium itself induces the synthesis of chelatins, which will reduce its toxicity (Malavolta, 2006). The chemical mechanisms proposed by Baird (2002), Silva et al. (2007a, 2007b), Guo and Marschner (1995), and Malavolta (2006) confirm not only the deleterious effects of Cd, but especially those data of Tables 1 and 2, which are related to the behavior of bean, especially with regard to the production of fruits, in the presence of Cd. Productivity (Lead) Different dosages of lead applied to the nutritive solution of bean plant led to the growing and production profiles of Table 3. According to the results of Table 3 for DMRS and DMAP, the control treatment exhibited the best development. The most important fruit production was achieved at the 0.25 mg L−1 of Pb, which is ca. 73% larger than the control treatment. For DMF, the 1 and 5 mg L−1 dosages of Pb influenced positively the productivity of bean plants, increasing by 60% and 42%, respectively, in comparison to the control treatment.
  • 8. 504 M. G. Cannata et al. TABLE 3 Plant behavior in the presence of Pb: production of dry matter of the root system (DMRS), of the aerial portion (DMAP), and of the fruits (DMF) and relative production index of root, aerial portion and fruits Dry matter (weight, in g) Relative production index (%) Doses Pb (mg L−1) DMRS DMAP DMF DMRS DMAP DMF 0 2.87 6.67 2.22 100.00 100.00 100.00 0.25 1.07 3.90 3.84 37.25 58.46 173.34 1.0 1.03 3.99 3.56 35.86 59.87 160.53 5.0 0.76 2.79 3.16 26.58 41.81 142.76 10.0 0.48 1.55 1.34 16.71 23.25 60.58 Significant data at 5% of probability according to the Tukey test. The absorbed Pb accumulates in the cellular wall, particularly of roots, and this seems to contribute for the diminishment of its toxic effect to the plant, as well as its transportation to fruits (Faquin, 2005). This fact explains the “beneficial effect” of some dosages of Pb to some plants; according to Kabata-Pendias and Pendias (2001), the exclusion mechanism of Pb is in fact the root deposition. This phenomenon occurs because of the linkage of the metal to insoluble organic polymers like phosphates as electron donors, forming amorphous precipitates. The 0.25 and 1 mg L−1 dosages of Pb were statistically equivalent for DMRS and DMAP (Table 3). The 10 mg L−1 showed the most substantial, negative influence to the plant development, causing a production decay of 40% for DMF, 76% for DMAP, and 83% for DMRS (Table 3). Similarly to Cd, Carvalho et al. (2009) analyzed the Pb effect on the behavior of bean plant in two different latosols (in terms of contents of clay and organic matter). The development of the bean plant (Phaseolus vulgaris L.) were evaluated under the 0, 125, 250, and 500 mg L−1 dosages of Pb, using the latosols RYLh and RLd; the production of DMAP decreased with increasing the amount of Pb in RLd, while the 125 mg L−1 affected only modestly the production of DMAP in RYLh – the production decreased significantly at the 500 mg L−1 dosage (ca. 44%). Carvalho et al. (2009) also investigated the production of grains, and Pb caused a 18.5% and 30% reduction at the 125 and 250 mg L−1 dosages, re- spectively, in RLd, while production was kept nearly unaltered in comparison to the treatment control in RYLh at these dosages. There was an improved production of grains between 250 and 500 mg L−1 for both soil types. Content and Translocation (Lead) The amount of lead absorbed by the plant was dependent on the metal dosages, as shown in Table 4. Again, the absorption of metal was proportional to the dosages applied, as measured in DMAP and DMRS
  • 9. Cadmium and Lead on Phaseolus vulgaris L. 505 TABLE 4 Content of lead in the root system, aerial portion and fruits of bean plants Content (mg kg−1) TI (%) Doses Pb (mg L−1) Roots Aerial portion Fruits Aerial portion Fruits t (%) 0 0.00 0.00 0.00 0.00 0.00 0.00 0.25 480.73 11.73 6.20 2.62 1.38 0.99 1.0 1006.78 61.60 8.30 5.72 0.77 0.58 5.0 1763.48 82.68 47.05 3.49 1.99 0.20 10.0 2433.63 100.05 67.10 3.85 2.58 0.05 TI: Translocation index, t: transfer factor. Significant data at 5% of probability according to the Tukey test. (Table 4). For DMF, the absorptions at the 0.25 and 1 mg L−1 dosages were statistically equivalent (Table 4). Similarly to observed for Cd, the absorption of lead differed substantially among the plant moieties studied, varying from 430 to 2433 mg kg−1 in the root system, from ca. 12 to 100 mg kg−1 in the aerial portion, and from 6.2 to 67 mg kg−1 in the fruits (husks and grains), at the 0.25 and 10 mg L−1 dosages of metal, respectively. This data indicate that lead translocates very poorly throughout the plants, such as Cd, since there was an expressive difference in the amount of Pb found in the three plant compartments. Table 4 clears up the difficulty of Pb in mobilizing in the plants, due to low translocation index. The most efficient dosage when the aerial portion is analyzed is 1 mg L−1 , giving 5.7% of translocation; the corresponding value for fruits is only 0.8%. The transfer of metals from solution to plants was practically total at the 0.25 mg L−1 dosage, in which the factor t was 0.99, and the difference between the extreme dosages reached 95% (Table 4). Malavolta (1994) describes that the toxic effects of Pb, such as the dam- ages to photosynthesis, mitosis and water absorption, and physical symptoms, like dark green leafs, wilted old leafs and slight development of roots and aerial portion, can be observed in plants, but they are not totally specific. In the present work, various similar symptoms were observed in the plants under the 5 and 10 mg L−1 dosages of Pb. Moreover, there is an interference of Pb in the synthesis of chlorophyll together with a reduced transport of Fe, which is necessary to the formation of heme groups. Therefore, leafs experience a deficiency symptom (chlorosis), causing damages in stressed plants (Fodor et al., 1998). Carvalho et al. (2009) have also quantified the content of Pb uptaken from bean plants cultivated in two latosols. The content of Pb in DMAP, at the 250 mg L−1 dosage, was 21% and 26% in RLd and RYLh, respectively, while the corresponding values at the 500 mg L−1 were 19% and 18%. These results confirm the low translocation of Pb, even at higher dosages in soils than in nutritive solution. Carvalho et al. (2008, 2009) confirmed the low translocation of Cd and notably Pb, showing that, depending on the dosage applied in the soil, these plants can be used for nutrition without
  • 10. 506 M. G. Cannata et al. the risk to health, due to the insignificant content of metal in husks and grains. These authors have also attributed the low translocation of Pb to the steric hindrance of chelates formed between Pb and amino acids or related substances of roots; this hypothesis corroborates the work by Silva et al. (2007a, 2007b) on the synthesis and characterization of chelates based on Pb, Cd, Zn, and Cu with diethylenetriaminepentacetic acid (DTPA), who determined the high steric hindrance of the DTPA-Pb structure. This seems to justify the difficulty of the metal in ascending in plant, since it remains partially complexed to free amino acids, proteins or plant secretions, rich in electron donors, such as DTPA. The similar chemical behavior of Pb and Cd in plants (analogous to the similarity between Cu and Zn) was also verified by Paim et al. (2006) in soil contaminated by mining residues of Zn; after extraction of Zn from the min- eral, the side products rich in Pb, Cd, and Zn cause serious environmental problems to the soil. The difference in translocation between Cd and Pb becomes evident when comparing Tables 2 and 4; TI was significantly lower in the Pb- containing medium than in the Cd-containing solution, especially for leafs. An explanation for this finding lies on the periodic properties of these metals, particularly the atomic radius (1.71 and 1.81 pm for Cd and Pb, respectively) and density (8.6 and 11.3 g cm−3 for Cd and Pb, respectively); these factors reflect the mobility and therefore the activity of Pb. In addition to these properties, Antoniadis et al. (2007) and Oliveira et al. (2009) also attribute the low mobility of Pb to the electronegativity. CONCLUSIONS Increasing dosages of Cd and Pb reduce the development of bean plants, expressed in terms of dry matter of the aerial portion and root system. 0.025 and 0.1 mg L−1 dosages of Cd, and 0.25, 1, and 5 mg L−1 of Pb contribute for the increasing production of fruits (husks and grains) in bean plants. This behavior has also been observed in latosols. Cadmium and mainly Pb translocate very poorly in plants, and therefore they are concentrated in the roots. Increments in the absorption of Zn by bean plants at low dosages of Cd and Pb seem to explain the increasing in the production of fruits. Low translocation of metals and the increasing production of fruits by bean plants cultivated both in nutritive solution and soils contaminated with Cd and Pb do not allow pointing out toward the consume of grains, since there still remains controversy regarding the tolerability of organisms to these metals. FUNDING CAPES and CNPq are gratefully acknowledged for the studentship and fellowship (to M.G.C. and M.P.F.).
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