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IV. External Factors Affecting Cadmium Concentration in Tobacco Leaves
N. LUGON-MOULIN ET AL.
almost all Cd was sorbed to iron- or aluminum-oxides and aluminosilicates when
the pH was above 8. When the pH decreases, Cd adsorption by clay iron,
manganese (Mn) oxides and organic matter decreases (Alloway, 1995).
Soil pH is important in controlling Cd accumulation by tobacco (Mulchi et al.,
1987a; Bell et al., 1988; Adamu et al., 1989; King and Hajjar, 1990; Khan et al.,
1992; Gondola and Kadar, 1995; Tsadilas, 2000), although its effect depends on
various factors (pH range, soil characteristics, agronomic practices, environmental factors, crop species; King and Hajjar, 1990; McLaughlin and Singh,
1999; McBride, 2002). In contrast to most studies, Schmidt et al. (1985), in a
greenhouse experiment, did not ﬁnd a signiﬁcant effect between two pH
treatments (5.5 and 7.3) on the Cd content of tobacco leaves.
Cation Exchange Capacity, Cadmium Content of Soil,
and Other Soil Properties
Various studies have attempted to predict Cd accumulation in tobacco leaves
based on some soil properties. The differences reported between these studies
may be due to various factors (e.g., different soil type used). Gondola and Kadar
(1995) found a signiﬁcant positive correlation between leaf Cd content and clay
content of soils. In a study done in southern Maryland over a ﬁve-county region,
encompassing 11 different soils at 33 farms, a signiﬁcant positive correlation
was found between leaf Cd and soil cation exchange capacity (CEC) (Adamu
et al., 1989). However, there was no signiﬁcant correlation between the Cd
concentration of tobacco leaves and the total or DTPA-extractable Cd in the soil
(Adamu et al., 1989). Similarly, the latter fraction could not predict Cd
accumulation by tobacco (cv. Samsun 53) grown in an acid Cd-contaminated
soil (20 ppm CdCl2 added) having received various amounts of lime. But there
was a strong correlation between potassium nitrate (KNO3)-extractable Cd and
total Cd uptake by tobacco (Tsadilas, 2000). Matsi et al. (2002) analyzed ﬁve
tobacco types (Burley, ﬂue-cured, Basma, Kabakulak, Samsun) in northern Italy
and Greece and found a signiﬁcant correlation between the level of Cd in
tobacco and soil characteristics (DTPA-extractable Cd, pH, clay content;
correlation coefﬁcient ¼ 0.40, p , 0:001). However, the correlation coefﬁcients
ðrÞ were rather low. The correlations improved when only considering soils with
ﬁne and moderately ﬁne texture. Moreover, when each variety was analyzed
separately, the importance of the soil variables in predicting the Cd
concentration in tobacco showed some variation (Matsi et al., 2002). This
further emphasizes the complexity of the relationship between many interacting
factors. Using stepwise regression analysis, Miner et al. (1997) could explain
the Cd content of tobacco (cv. K326) grown on sewage-sludge-treated ﬁelds as
being inﬂuenced (R2 up to 0.96) by soil factors, namely the pH, CEC, and
extractable Cd (either EDTA-, DTPA-, or Mehlich 3-extractable). King (1988)
OPTIONS FOR REDUCING CADMIUM IN TOBACCO
predicted the Cd concentration in tobacco leaves grown on limed (pH 5.7 – 7.0)
mineral soils by considering two soil variables, namely ammonium oxalateextractable Fe and Cd from limed soil (regression model, R2 ¼ 0:99). Cadmium
removal by tobacco was also accurately estimated by considering the same two
variables and pH R2 ẳ 0:99ị: Exogenous Cd was added as a salt in this study.
In a study done in Hungary, the soil Cd content did not signiﬁcantly correlate
with the Cd contents of cured tobacco leaves obtained from the same crop year
(Gondola and Kadar, 1995).
Upper and lower leaves can accumulate approximately four and eight
times, respectively, the Cd concentration found in the soil (Frank et al., 1980).
Interestingly, ratios for chromium (Cr), Hg, molybdenum (Mo), nickel (Ni),
and Pb were all much lower than for Cd (Frank et al., 1980). Frank et al.
(1987) found that the ratio of Cd in lower (sand) leaves to available Cd in soil
was 29 and 77 for crop years 1981 and 1983, respectively. The ratio of
available soil Cd to total soil Cd varied according to year (0.30, 0.52, and 0.14
in 1980, 1981, and 1983, respectively) and was much higher than that for Cr,
Ni, or Pb.
3. Inﬂuence of Other Metals
The divalent cations calcium (Ca), cobalt (Co), copper (Cu), Ni, and Pb can
compete with, and hence retard, the sorption of Cd by soils (McLaughlin et al.,
1996). Moreover, the interactions of Cd with other metals and nutrients can
occur during both the uptake process and the subsequent transport within the
plant, and these interactions can vary with plant tissue, genotypes, metal,
nutrients, and their concentrations (Pendias and Pendias, 1992; Landberg
and Greger, 1994; Carvalho et al., 2002; Kabata-Kim et al., 2002; Zhang
et al., 2002).
Important complex interactions occur during plant uptake between the
chemically related Zn and Cd (Welch and Norvell, 1999). Several studies have
been designed to better understand the interactions between some metals and Cd
in tobacco. Wen (1983) supplied Cu, Zn, and Cd at various concentrations to
tobacco (cv. “Taiwan tobacco #5”) grown in quartz pots (pH 6.0– 6.5). The
reported results suggest antagonistic effects between Zn and Cd, but because
most treatments used metal concentrations impacting plant growth, and because
only two plants were used per treatment, deﬁnitive conclusions could not
be drawn. However, data obtained in a study using wheat suggest that these two
ions may compete with each other during the uptake process at the root plasma
membrane (Hart et al., 2002). It was suggested that Zn may inhibit the movement
of Cd from one organ to another via the phloem (Welch et al., 1999).
Interestingly, Cd concentration in wheat grain could be decreased by up to 50%
N. LUGON-MOULIN ET AL.
by adding 2.5– 5.0 kg Zn/ha to ﬁelds with low levels of available Zn (Oliver et al.,
1994). However, the effectiveness of this treatment decreased over time. Results
by Green et al. (2003) also suggest that Zn addition can reduce Cd translocation
from roots to the shoot of “Grandin” hard red spring wheat. Interactions between
Cd and Fe have also been studied in tobacco. After a 7-day Cd treatment, Yang
and Kuboi (1991) found that cultured tobacco (cv. Xanthi NC and cv. Saman
SR-1) cells accumulated more Fe and Ca. The Cd concentration of pot-grown
tobacco (cv. Dajinyuan) mid-leaves increased with increasing Cd concentration
in the growth medium, and this increase was greater when Fe (1000 ppm) was
applied with the Cd treatments (Li et al., 1990). In contrast, increasing Cd
exposure caused plants to take up less Fe (Duan et al., 1994). Antagonistic effects
between Cd and Fe on the physiological traits of tobacco (cv. Dajinyuan) were
reported by Li et al. (1992).
B. AGRONOMIC PRACTICES
Agronomic practices can impact the uptake of Cd by crops, including
tobacco. To better understand the fate of Cd in soils and its uptake by plants,
empirical stochastic models considering both metal inputs (e.g., through
fertilizers) and outputs (e.g., plant uptake, leaching) have been developed
(Keller et al., 2001a, 2002).
1. Sludge Amendments
The use of municipal and industrial sludges as soil amendments has both
economic and ecological advantages. However, as they can contain Cd, they can
also elevate the level of this metal in soils and the plants growing in the soils
(Wagner, 1993; Smith, 1994; Keller et al., 2001b). The leaf laminae of tobacco
(cv. Virginia 115) experimentally grown on a sludge-amended ﬁeld contained 20
times the Cd concentration of control plants (67.4 and 3.2 ppm, respectively;
Gutenmann et al., 1982). In a greenhouse study, Bache et al. (1985) grew cv.
Virginia 115 on a Peat-Lite mix soil. When 1% Cd-polluted sludge (87.2 ppm
Cd) was added to the soil, the leaf laminae contained 5.3 ppm Cd, while controls
had 1.9 ppm. In a subsequent publication, Bache et al. (1986) reported 3.6 ppm
Cd in the laminae of cv. Virginia 115 grown in soil, and 62.9 ppm Cd when
grown on a municipal sludge-amended soil (sludge Cd concentration: 84 ppm;
application rate: 224 tons/ha).
Increasing the application rate of a Cd-containing sludge usually leads to an
increase in tobacco leaf Cd concentration (Mulchi et al., 1987a,b; Bell et al.,
1988; King and Hajjar, 1990). In ﬁeld experiments, Mulchi et al. (1987a) found
OPTIONS FOR REDUCING CADMIUM IN TOBACCO
that Cd content of Maryland tobacco (cv. MD609) leaves increased with
increasing sludge application rates for three of the ﬁve sludge sources examined.
The plant response was not linear; rather, it was quadratic, with respect to sludge
application rates (Mulchi et al., 1987a,b). Application of two limed sludges did
not result in signiﬁcant changes in leaf Cd concentrations. In a pot study, the
effect of increasing sludge application rate (0, 18, 27, and 81 mg/ha) was shown
to be more pronounced at low pH, and diminished as pH increased (King and
Residual soil Cd (and other metals) can be derived from soil amendments
used on other crops or in previous growing seasons. Hence, past sludge
applications may still impact the Cd concentration of plants grown several years
later, as suggested by results obtained by Bell et al. (1988). They studied the
long-term effect of a sludge applied in 1972 on the Cd content of Maryland
tobacco (cv. MD 609) grown in 1983 and 1984, and they reported an increase
in leaf Cd concentration with increasing sludge application rate. Frink and
Hullar (1985) (cited by Bell et al., 1988) studied tobacco grown in 1976 on a
loam soil amended in 1974 with sludges from several sources. They also
found an increase in leaf Cd concentration with increasing sludge
In a ﬁeld study, Baldwin and Shelton (1999) applied three composts
(containing from 1.0 to 2.9 ppm Cd) at three application rates (25, 50, and
100 tons/ha) to a Dyke soil in North Carolina, USA. The amount of Cd added to
the soil varied from 0.03 to 0.29 kg Cd/ha according to the compost and the rate
of application. They studied the uptake of metals by Burley tobacco (cv. TN90)
grown in 1994 and 1995. Only the rate of application of the co-composted
municipal solid waste/wastewater biosolids compost had a linear relationship
with the Cd content of cured tobacco leaves; however, it should be noted that in
1994, 21% of the mature cured leaf samples had Cd values below the detection
limit (0.8 ppm) using inductively coupled plasma-emission spectrometry
(ICP-ES) and in 1995, samples had, in general, values below detection limits.
Using soil variables (total- or extractable-Cd, pH), Mulchi et al. (1992) tried to
predict the Cd concentration in tobacco leaves grown on two sludge-amended
soils. The prediction efﬁcacy differed for these soils (R2 ¼ 0:75 – 0:84 and
0.91– 0.97, respectively), which may have been due to the different sludges used
(some being limed), different soil types and soil –sludge interactions at the two
sites (Mulchi et al., 1992).
These studies show that sludge application can impact the uptake of Cd by
tobacco. Several factors must be considered, such as the metal content of
the sludge, the origin of the sludge, its application rate, the way in which the
sludge and its components will interact with the soil (e.g., effect of pH), and both
short- and long-term effects. In general, tobacco should not be grown in soils that
have been amended with metal (Cd)-contaminated sludges in the past.
N. LUGON-MOULIN ET AL.
As the solubility of Cd is increased in acidic soils, liming is commonly used to
raise soil pH and thereby lower Cd uptake by plants (McLaughlin et al., 1996;
Dousset et al., 1999). However, liming does not always lead to a reduction of the
Cd concentration in crops (Mench et al., 1994b; Mench, 1998; Maier et al.,
Liming strategies have been tested to reduce the Cd concentrations of tobacco
leaves. It was suggested that lime be applied to highly acidic tobacco soils. In a
ﬁeld experiment, Khan et al. (1992) found that Cd concentration in Maryland
tobacco leaves signiﬁcantly decreased after dolomitic lime application to two
sandy loam soils. In a pot experiment, calcium carbonate (CaCO3) addition
resulted in a signiﬁcant decrease in the Cd concentration of tobacco (cv. PBD6)
leaves when the soil pH increased from 6.0 to 7.3 (Phu-Lich et al., 1990). When
further increasing the pH to 7.7, only the Cd concentrations of the lower leaves
decreased signiﬁcantly. In a ﬁeld experiment, a signiﬁcant decrease of Cd was
found in all leaves of Burley tobacco (cv. BB16) when the pH increased from 5.5 to
6.4 with different concentrations of Ca– Mg amendments (Tancogne et al., 1989;
Phu-Lich et al., 1990). A further increase in pH resulted in only a slight decrease in
leaf Cd concentration. When using CaCO3 to change the pH from the 5.8– 5.9
range to the 6.6 –6.7 range, leaf Cd concentration was signiﬁcantly reduced
(calcium nitrate [Ca(NO3)2] or ammonia sulfate [(NH4)2SO4] as the nitrogen (N)
source, Phu-Lich et al., 1990; see also Tancogne et al., 1988).
Liming, however, did not always lead to a reduced Cd content of tobacco
leaves grown in Cd-polluted soil. Mench et al. (1994b) applied lime to a metalpolluted sewage-sludge application ﬁeld trial and found that this treatment
signiﬁcantly increased the content of Cd in tobacco leaves, compared with the
unlimed treatment (170 and 120 ppm, respectively). Liming did not change the Cd
content of tobacco grown in an agricultural area near a non-ferrous metal smelter
in France. Thus, the efﬁciency of liming on tobacco Cd concentration appeared to
depend on the type and rate of liming material added and the type of soil. Other
environmental and genetic factors may also affect the response to liming. By
reviewing the effect of lime application to sludge-amended ﬁelds, Dousset et al.
(1999) noticed that the form of the Cd salt at the time of soil application can be
important. Liming may increase the proportion of exchangeable Cd when it is in
the form of CdSO4 (salt), but when the Cd originates from sludge or previous
harvest residue, the proportion of exchangeable Cd may remain unchanged.
Moreover, the effect of liming on other tobacco characteristics, such as yield
and chemical composition, has not been extensively studied. Lime application
increased tobacco (cv. BU21) yield without considerably affecting leaf quality
(chemical and organoleptic characteristics; Lee et al., 1989). However, liming
may lead to an undesirable reduction in Mn concentration in tobacco leaves
(Mulchi et al., 1987a, 1991, 1992; Khan et al., 1992; Moustakas et al., 1999).
OPTIONS FOR REDUCING CADMIUM IN TOBACCO
(a) Cadmium in fertilizers. Phosphate fertilizers (P-fertilizers) can contain
high to very high levels of Cd, as phosphate rocks used in their manufacturing
may contain from 0.2 to about 340 ppm Cd (reviewed in McLaughlin et al., 1996;
McLaughlin and Singh, 1999). Cadmium may accumulate to high levels in
certain soils as a result of Cd-contaminated P-fertilizers application. Therefore,
Cd in P-fertilizers is of great concern, and individual European Union Member
States have recently begun to assess the risks arising from fertilizer-derived soil
accumulation of Cd (Cupit et al., 2002; de Meeuˆs et al., 2002).
In addition to the Cd concentration in P-fertilizers, other factors need to be
considered, such as the total input of fertilizer to the soil and the source of the
phosphorus (P) anion (Lee and Doolittle, 2002). Bielinska et al. (1999) studied
the effect of fertilizer application on the Cd concentration of soil under tobacco
cultivation in Poland. The topsoil (0 –5 cm) of a ﬁeld fertilized with 240 kg NPK
fertilizer/ha had about the same Cd content as the topsoil of a ﬁeld fertilized with
700 kg Flovit/ha (0.264 and 0.237 ppm, respectively). However, the 5– 15 cm
layer and the 15 – 20 cm layer of the ﬁeld fertilized with the NPK fertilizer had
higher Cd concentration (0.282 and 0.204 ppm, respectively) than the
corresponding layers of the ﬁeld that was fertilized with Flovit (0.077 and
0.069 ppm, respectively). Reducing the use of high Cd fertilizers may limit
further Cd contamination of agricultural soils, and total P application rates may
be reduced by applying fertilizer in a concentrated area (banding) instead of an
even application across a ﬁeld (broadcast).
In contrast, non-P-fertilizers generally contain low levels of Cd. However,
their use can still lead to an increase in Cd concentrations in crops, possibly
through soil acidiﬁcation, enhanced mass ﬂow, or desorption of Cd from the soil
solid phase into the soil solution (Gray et al., 2002; Maier et al., 2002b).
(b) Effects of fertilizers on cadmium uptake by tobacco. A few studies suggest
that the use of P-fertilizers may impact Cd accumulation by tobacco, although the
Cd concentrations of the fertilizers used were not given or unknown (Murty et al.,
1986; Semu and Singh, 1996). In India, Murty et al. (1986) grew tobacco on two
different soils (Vertisol and Alﬁsol), with or without superphosphate application
(the amounts of N, K, P and irrigation waters were different for the two soils).
Tobacco grown in Vertisol without P addition had a lower Cd concentration in the
leaf laminae (range: 0.100 – 0.347 ppm; mean: 0.218 ppm) than the tobacco that
had received superphosphate (range: 0.392– 0.501 ppm; mean: 0.455 ppm).
However, when farmyard manure was added to the treatments, the opposite was
observed (without P addition the mean Cd concentration was 0.432 ppm; with P
addition it was 0.354 ppm). Cadmium accumulation in tobacco grown in Alﬁsol
did not vary with P treatment. Although no regular trend was observed for the effect
of P application on the Cd content of tobacco leaves, these results support other
published data that suggest that superphosphate addition may play a role in Cd
N. LUGON-MOULIN ET AL.
uptake by tobacco depending on soil characteristics. For example, in Tanzania,
Semu and Singh (1996) compared the Cd concentrations in tobacco leaves grown
in soils having received either low or high levels of P-fertilizers. The ﬁelds that
received high levels of P-fertilizers had more total Cd and DTPA-extractable Cd
than the ﬁelds that received low levels of P-fertilizers. The lower leaves of the
tobacco grown in ﬁelds with low levels of P-fertilizers contained less Cd (but not
signiﬁcant) than the lower leaves of the tobacco grown in ﬁelds with high Pfertilizers (means: 0.084 and 0.159 ppm, respectively; ranges: 0.055 – 0.112 and
0.072 – 0.388 ppm, respectively). In a recent experiment, Miele et al. (2002) found
that increasing rates (up to 160 kg/ha) of superphosphate fertilizer application had
only a slight effect on the Cd concentration of tobacco leaves in Greece (cv. KS82)
and Italy (cv. NC55). Metal accumulation in the plant was dependent on site and
year. They concluded that a wise choice of P-fertilizers and their application at the
suggested rates may not represent a major input source of metals in Italian and
Besides P-fertilizers, nitrogen fertilizers (N-fertilizers) may also, to some
extent, affect Cd accumulation by tobacco, as suggested by results obtained by
Phu-Lich et al. (1990). Under hydroponic conditions, they found signiﬁcant
differences in the Cd concentration of tobacco leaves when the N form in
fertilizers was in the form of nitrate (NO3) versus NO3:NH4 (2:1). By using
NO3:NH4, a two- to fourfold increase in Cd concentration in leaves occurred,
depending on solution Cd concentration (0.05, 0.10, and 1.50 mg/l) and stalk
position. Nitrate slightly raised the pH of the solution, while ammonium (NH4)
slightly lowered it. This may explain the differences in Cd uptake between the
two treatments. In a pot experiment (limon-sandy soil; pH 5.8– 5.9) using
(NH4)2SO4 as the N source, a threefold increase in leaf Cd concentration was
found (irrespective of the stalk position), compared with using Ca(NO3)2 as the N
source. However, when CaCO3 was added, no further signiﬁcant differences were
found between the two types of N-fertilizers.
Further study is needed to assess the effects of different types of fertilizers on
Cd accumulation in real ﬁeld conditions, in soils with different characteristics,
using different agronomic practices, and various tobacco cultivars.
4. Irrigation Water
Irrigating ﬁelds is necessary for optimal growth of crops and, in some
locations, for tobacco cultivation. Salts in irrigation waters and groundwater
affect soil salinity and can impact the Cd concentration in plants because, for
example, chloride may reduce Cd sorption by soil and form phytoavailable
chloro-Cd complexes (McLaughlin et al., 1994; Welch and Norvell, 1999). Wu
et al. (2002) reported a 15-fold difference between the minimum and the
OPTIONS FOR REDUCING CADMIUM IN TOBACCO
maximum Cd concentration in grains of durum wheat grown in the same ﬁeld,
while soil Cd content varied only about 2.5-fold in various areas of the ﬁeld.
Interestingly, there was signiﬁcant correlation between grain Cd content and soil
salinity, particularly with the natural logarithm (ln) of soil chloride ion (Cl2).
High levels of Ca2ỵ in irrigation waters may compete with, and lead to,
desorption of Cd from soil surfaces (McLaughlin et al., 1996).
While unpolluted irrigation waters may impact plant uptake of Cd through
salinization, Cd-polluted irrigation waters can sometimes represent another
important source of Cd contamination to the soil, thereby impacting plant uptake
of Cd. In China, about 11,000 ha of land may have been polluted with Cd by
irrigation water. A survey done in Dayu county in the Jiangxi province of China
showed that Cd pollution was due to irrigation water contaminated by waste
waters of tungsten-ore dressing plants (Cai et al., 1995). Average Cd concentrations were 0.047 mg/l in the irrigation water from the tributaries of the Zhang
river and 0.89 ppm in the irrigated soil (background Cd level: 0.09 ppm). The
average Cd concentration of tobacco grown in the exposed area was about nine
times higher (17.4 ppm) than that in the control area (1.86 ppm, Cai et al., 1995).
Other Agronomic Practices
Other agronomic practices may impact Cd uptake by plants, including
tobacco. In a pot experiment, Mench (1998) found that the Cd concentration in
the tobacco shoot systematically and signiﬁcantly increased after a 1-year fallow,
regardless of the soil type (four soils tested) or soil Cd content (from 0.14 to
10.7 ppm). However, it is unknown whether fallowing affects Cd accumulation
by tobacco in ﬁeld conditions.
The use of different crops on the same ﬁeld (crop rotation) may change soil
parameters in the rhizosphere (due to different root exudates or different root
systems) that may subsequently affect the Cd uptake of the next crop. Tillage or
plant spacing may also affect soil parameters and hence, Cd uptake by plants
and tobacco, although the effects of these factors have not been well studied
C. ADDITIONAL FACTORS
The use of experimental plot covers illustrates the impact that environmental
conditions can have on Cd uptake by plants. Indeed, plot covers can signiﬁcantly
increase air- and root-zone temperatures and relative humidity, and they can
decrease irradiance. Their use can lead to increased Cd uptake by plants,
N. LUGON-MOULIN ET AL.
compared with uncovered plants (Baghour et al., 2001; Moreno et al., 2002).
Factors such as high precipitation tend to increase Cd uptake in wheat (Andersson
and Pettersson, 1981).
Atmospheric Deposition on Leaves
As Cd can be found in the air, it may be deposited via atmospheric dust on the
surface of the tobacco leaves as well as on the soil. In a pot trial, Hovmand et al.
(1983) reported that atmospheric deposition on leaves accounted for 20 –60% of
the total Cd in plants grown in a Danish agricultural farmland located more than
5 km from industrial sources. By applying 109Cd on the leaves of various
Triticum spp., Cakmak et al. (2000) recently found important differences in foliar
uptake and subsequent translocation of Cd to the shoot and roots according to
genotypes. These results may be accounted for by different leaf characteristics,
including different uptake abilities by the plasma membranes (e.g., by
transporters, see Section V.A.2). However, the respective contribution of direct
leaf interception and root uptake to the total Cd present in tobacco leaves is
unknown, although the latter is thought to be more important.
Variation with Crop Year
As several agro-climatic variables are known to inﬂuence the concentration of
Cd in plants, and as soils evolve with time, it is expected that differences in the Cd
concentration of crops will occur in different crop years, at least under certain
circumstances. Cured tobacco leaves (mixed stalk position) from Ontario,
Canada sampled in 1973, 1974, and 1975 contained average Cd concentration of
3.20, 2.25, and 2.73 ppm, respectively, and ranges from 2.20 to 4.04, 1.25 to 4.30,
and 1.40 to 7.02 ppm, respectively. Soil collected from chief tobacco-producing
counties in Ontario between 1970 and 1975 had Cd concentrations ranging from
0.15 to 0.78 ppm, with a mean of 0.36 ppm (Frank et al., 1977). Using
regression analyses, Frank et al. (1991) did not ﬁnd a signiﬁcant decline in Cd
concentrations in cured leaves from Ontario over a 12-year period (1976 – 1988).
Similarly, Oto and Duru (1991) did not observe clear differences in the Cd
concentrations of Turkish tobacco from the same regions, obtained during
consecutive years. Gondola and Kadar (1995) found signiﬁcant differences
between crop years (1990 and 1991) for leaf Pb concentrations, but not for Cd,
which measured 1.07 ppm in 1990 and 1.15 ppm in 1991.
While studying the long term effects of sludge application, Bell et al.
(1988) did not ﬁnd signiﬁcant differences in leaf Cd concentration as a
function of crop year for Maryland tobacco (cv. MD 609) grown in 1983 and
OPTIONS FOR REDUCING CADMIUM IN TOBACCO
1984 (10.61 and 10.91 ppm, respectively). The plant concentrations for all
other metals investigated (Zn, Cu, Mn, Fe, Pb, Ni) changed signiﬁcantly.
These 2 years had different levels of rainfall in June, July, and August. Bell
et al. (1992) investigated metal contents of mid-stalk air-cured leaves of
Maryland tobacco. The mean concentration of Cd in the 1980 crop year
(1.85 ppm) differed signiﬁcantly from that in the other years studied (1981,
2.19 ppm; 1982, 2.56 ppm; 1983, 2.53 ppm).
These data support the idea that different conditions in different crop
years may, in certain situations, affect the concentration of Cd in the tobacco
plant. However, the factors responsible for these differences were not
identiﬁed and are probably related to the inﬂuences already detailed in the
The external factors that contribute to the Cd content of the plant are either
related to the Cd source (natural and artiﬁcial) or to Cd bioavailability. Even
though the experimental data are contradictory and ambiguous in many instances,
some external factors appear to impact Cd accumulation by tobacco. It
appears that Cd-contaminated P-fertilizers can be a signiﬁcant source of Cd
contamination in the tobacco ﬁeld. This is a preventable situation, and controlling this source of Cd can limit future, additional Cd contamination of
Atmospheric deposition can be a signiﬁcant source of Cd in soils, particularly
in industrialized areas. However, natural soil and other sources (e.g., manure) of
Cd will need to be addressed as well. While clay content might be adjustable by
soil amendment, pH control via lime application has emerged as a primary means
to control Cd bioavailability. Other strategies that leverage Cd bioavailability
exist (see Section V.C). A better understanding of speciﬁc agricultural practices,
as they relate to the soil properties and Cd bioavailability may guide farming
practices in the future.
V. OPTIONS TO REDUCE THE CADMIUM CONTENT
IN TOBACCO LEAVES
A. MOLECULARaAND BIOCHEMICAL APPROACHES
Recent advances in the understanding on molecular and biochemical
mechanisms of metal ion uptake, extrusion, transport, and sequestration suggest
that molecular and biochemical approaches have the potential to yield higher
N. LUGON-MOULIN ET AL.
percentage reduction of Cd in tobacco leaves than the other approaches. Research
in many of these areas is still at relatively early stages and the available information
is often limited to studies using other plants. Based on our current knowledge, it is
reasonable to expect that most of the metal transport and sequestration
mechanisms observed in other plant species are relevant for tobacco as well,
and therefore have been included in the discussions in this section.
Root exudates containing, for example, low-molecular-weight organic acids
(LMWOA), may induce changes in the physicochemical characteristics of the
surrounding soil, such as pH, moisture, electrical conductivity, redox potential,
oxygen availability, or microbial community (Hinsinger et al., 2003; Jones et al.,
2003). Hence, they may affect the solubility of various soil components (e.g., Cd)
and thus the availability of such components to plant roots. However root
exudates do not necessarily explain differences in Cd accumulation between taxa
(Zhao et al., 2001). In the rhizosphere, organo-Cd complexes may account for a
signiﬁcant portion of the soil solution Cd (Jones et al., 1994). In particular, citrate
can efﬁciently solubilize Cd (Naidu and Harter, 1998; Nigam et al., 2002) and its
exudation may enhance Cd solubility in the rhizosphere. As LMWOA may play a
role in Cd solubilization and accumulation in plants (Cieslinski et al., 1998),
genes that facilitate their release could be introduced by genetic engineering to
reduce or enhance Cd uptake (Ryan et al., 2003). The concept of phytoextraction
is further discussed in Section V.C.1.
Because root cells are mostly mature cells with large vacuoles, vacuolar
chelation may predominate over cytosol mechanisms (Rauser, 1999). Wagner
(1995) argued that, at the low levels of Cd found in agricultural soils, little or no
PCs would be induced, and vacuolar citrate would effectively complex
In response to nutrient metal ion deﬁciencies, such as Fe, graminaceous plants
secrete phytosiderophores (e.g., mugenic and avenic acids) to increase
the bioavailability of soil metals and help to carry the metals into plant tissue
(also see Section V.A.2(a), for a discussion of Cd transport under Fe-deﬁcient
conditions). For example, mugenic acids may limit the binding of Cd by hydrous
Fe-oxide (Mench et al., 1994b). Phytosiderophores can mobilize Cd from a solid
phase even in the presence of the competing metals, Fe, Ca, and Mg, but their
presence did not result in a signiﬁcant increase in Cd uptake by barley and wheat
(Shenker et al., 2001). This suggests that the release of phytosiderophores may
not increase Cd phytoextraction efﬁciency (see Section V.C.1 for a discussion of
phytoremediation). In contrast, phytosiderophores may be able to reduce Cd
uptake. When maize was exposed to Cd, in hydroponic culture, in the presence of