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IV. External Factors Affecting Cadmium Concentration in Tobacco Leaves

IV. External Factors Affecting Cadmium Concentration in Tobacco Leaves

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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.



2.



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)



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129



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%



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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



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131



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

Hajjar, 1990).

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

application rate.

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.



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2.



Liming



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.,

2002a,b).

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).



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133



3. Fertilizers

(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



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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

Greek tobaccos.

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



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135



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).



5.



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

(Mench, 1998).



C. ADDITIONAL FACTORS

1.



Climatic Conditions



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,



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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).



2.



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.



3.



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



137



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

above sections.



D. SUMMARY

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

agricultural fields.

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



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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.



1.



Root Exudates



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

cellular Cd.

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



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IV. External Factors Affecting Cadmium Concentration in Tobacco Leaves

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