hazard and effects of pollution by lead on vegetable crops

REVIEW PAPER

Hazard and Effects of Pollution by Lead on VegetableCrops

M. N. Feleafel • Z. M. Mirdad

Accepted: 31 May 2012

� Springer Science+Business Media B.V. 2012

Abstract Lead (Pb) contamination of the environment is an important human

health problem. Children are vulnerable to Pb toxicity; it causes damage to the

central nervous system and, in some extreme cases, can cause death. Lead is

widespread, especially in the urban environment, and is present in the atmosphere,

soil, water and food. Pb tends to accumulate in surface soil because of its low

solubility, mobility, and relative freedom from microbial degradation of this ele-

ment in the soil. Lead is present in soil as a result to weathering and other pedogenic

processes acting on the soil parent material; or from pollution arising caused by the

anthropogenic activities; such as mining, smelting and waste disposal; or through

the adoption of the unsafe and unethical agricultural practices such as using of

sewage sludge, and waste water in production of vegetable crops or cultivation of

vegetables near highways and industry regions. Lead concentrations are generally

higher in the leafy vegetables than the other vegetables. Factors affecting lead

uptake included its concentration in the soil, soil pH, soil type, organic matter

content, plant species, and unsafe agriculture practices. Generally, as Pb concen-

tration increased; dry matter yields of roots, stems and leaves as well as total yield

decreased. The mechanism of growth inhibition by lead involve: a decrease in

number of dividing cells, a reduction on chlorophyll synthesis, induced water stress

to plants, and decreased NO3- uptake, reduced nitrate and nitrite reductase activity, a

direct effect of lead on protein synthesis, a decrease on the uptake and concentration

of nutrients in plants. The strategies to minimize Pb hazard can be represented in:

M. N. Feleafel (&) � Z. M. Mirdad

Department of Arid Land Agriculture, Faculty of Meteorology, Environment and Arid Land

Agriculture, King Abdulaziz University, Jeddah 80208, Saudi Arabia

e-mail: [email protected]

Z. M. Mirdad

e-mail: [email protected]

M. N. Feleafel

Department of Vegetable Crops, Faculty of Agriculture, Alexandria University, Alexandria, Egypt

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J Agric Environ Ethics

DOI 10.1007/s10806-012-9403-1

(a) Phytoremediation, through natural plants are able to bio-accumulate Pb in their

above–ground parts, which are then harvested for removal such as, using Indian

Mustard (Brassica juncea), Ragweed (Ambrosia artemisiifolia), Hemp Dogbane

(Apocynum cannabium), or Poplar trees, which sequester lead in its biomass.

(b) Good and ethical agricultural practices such as cultivation of vegetables crops as

far from busy streets or highways and industry regions as well as nonuse of sewage

sludge and waste water in cultivated soils. (c) Increasing the absorptive capacity of

the soil by adding organic matter and humic acid. (d) Growing vegetable crops and

cultivars with a low potential to accumulate lead, especially in soils exposed to

atmospheric pollution. (e) Washing of leafy vegetables by water containing 1 %

vinegar or peeling roots, tubers, and some fruits of vegetables before consumption

may be an important factor in reducing the lead concentration.

Keywords Hazard of lead pollution � Vegetable � Lead uptake � Unsafe �Unethical agriculture practices � Remediation

Introduction

Environmental pollution, especially by chemicals is one of the most effective

factors in the destruction of the biosphere components. Among all chemical

contaminates, heavy metals are considered potential hazardous contaminants in the

biosphere to human health. Heavy metals are commonly adopted as a group name of

the metals and metalloids which are associated with pollution and toxicity, such as

cadmium (Cd), Lead (Pb), Mercury (Hg), Arsenic (As), Nickel (Ni) and chromium

(Cr), but also includes some elements which are essential for living organisms at

low concentrations, such as Co, Cu, Mn, Se, and Zn.

Lead is one of the most important heavy metals that pollute the natural

environment due to man’s impact. Lead, however, has a long residence time

compared with other pollutants. Lead exists naturally in soils at levels of

10–50 ppm (Angima and Sullivan 2008). As a result, Pb and its compounds tend

to accumulate in soils over decades and will continue to circulate in the biological

cycle for the next 300–500 years (Heinrichs and Mayer 1977); because of the low

solubility, mobility, and relative freedom from microbial degradation or bioreme-

diation by microorganisms of this element in the soil (Davies 1995; Suruchi and

Khanna 2011). The amount of lead in the environment has reached a level able to

evoke the first symptoms of toxicity in humans (Mengle and Kirkby 1980). Lead is

widespread, especially in the urban environment, and present in the atmosphere,

soil, water, and food (Wozny and Jerczynska 1991). Vegetables are an important

part of human’s diet. In addition to a potential source of important nutrients,

vegetables constitute important functional food components by contributing protein,

vitamins, iron, and calcium which have marked health effects (Arai 2002).

The objective of the present review article is to demonstrate the pollution effects

of lead (Pb) on vegetable crops to find out the best methods or treatments to arrest

the deleterious effects of this element.

M. N. Feleafel, Z. M. Mirdad

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Lead and Public Health

Lead is a non-essential element and does not play any role in the metabolism of

plants or animals. Although, Pb is present in all tissues and organs of the mammals

(Forstner and Wittmann 1983), increasing its concentration inhibits most of the

basic physiological processes. Nicklow et al. (1983) stated that children are

vulnerable to Pb toxicity and that Pb causes damage to the central nervous system

and, in extreme cases, death. However, Forstner and Wittmann (1983) declared that

metabolism of both Pb and Ca are similar in both their deposition in and

mobilization from bone. Under normal conditions, more than 90 % of the lead

retained in the body is present in the skeleton. Furthermore, during pregnancy and

lactation, lead mobilization from the mothers bones to fetuses and breastfed infants

(Suruchi and Khanna 2011). Lead is poisonous and there are fears that body burdens

below those at which clinical symptoms of Pb toxicity appear may cause mental

impairment in young children (Davies 1995) and raise blood pressure in adults

(Suruchi and Khanna 2011). Moreover, the carcinogenic and mutagenic properties

of lead have been repeatedly demonstrated (Michalak and Wierzbicka 1998).

Lead Sources in the Environment

Lead is present in soil as a result of weathering and other pedogenic processes acting

on the soil parent material, or by pollution arising from anthropogenic activities,

such as mining, smelting, and waste disposal, or from the ethics of unsafe

agricultural practices by using sewage sludge, waste water, and other agrochemicals

in vegetable production. Jones et al. (1973) reported that aerial Pb is mostly

generated by combustion of leaded gasoline in vehicles. Fleming and Parle (1977)

suggested that, in urban soil, Pb could also be derived from coal, plastics and rubber

factories, insecticides, and car batteries. Nicklow et al. (1983) indicated that Pb is

used in the production of gasoline additives, acid batteries and, until recently, in

lead-based paints. They added that these products and many others represent sources

of Pb in the air that we breathe, water that we drink, and soil in which we grow our

crops. The lead evolves as a result of many years of weathering or, in some cases,

sand-blasting of painted buildings. Soil is a sink for anthropogenic Pb and there are

several well-recognized major sources; namely mining and smelting activities,

sewage sludge usage in agriculture and contamination from vehicle exhausts

(Davies 1995; Yusuf and Oluwole 2009). Lead has been emitted into the

environment for thousands of years. However; over the last 70 years, the amount

of lead finding its way into the environment has drastically increased as a result of

human activity (Michalak and Wierzbicka 1998). While, Angima and Sullivan

(2008) illustrated that lead-arsenate sprays were commonly used for pest control in

fruit and nut orchards from about 1910 to the 1950s. They added that lead

concentrations were highest in paints prior to 1960 and leaded gasoline was used

until 1996.

Hazard and Effects of Pollution by Lead on Vegetable Crops

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Lead Content in Egyptian Soils

A large number of investigations were carried out to determine Pb- contents in

Egyptian soils. The total amounts of Pb in 71 soil samples from 14 saline alkaline

profiles in the Nile Delta ranged from 25 to 100 ppm (El-Rashidi et al. 1979). Abd

El-Shakour (1982) stated that Pb concentration in the cultivated soil of Lower

Egypt, away from pollution sources, averaged 9–21 ppm; While, the Pb content in

soils of Shoubra El-Kheima area was more than 100 ppm This figure reached more

than 700 ppm near a group of complex foundries. In Bahteem area, Abd El-Halaem

(1984) found that Pb concentration was 15 mg kg-1soil; while, in Mostorod the

concentration was 20.06–64.30 mg kg-1soil. Baghdady and Sippola (1984) found

that total Pb in Egyptian alluvial soils ranged between 7 and 23 ppm El-Sikhry

(1985) reported that total Pb of selected soils from Ismailiah and Sinai Governorates

ranged from 20 to 260 ppm The highest values of Pb were recorded in Quantra and

Sant Catherine soil samples.

In Bahr El-Baqar soil, Hassan (1994) found that extractable Pb from soil samples

varied from 3.1 to 7.2 ppm in cultivated soil and the highest amount was extracted

from soil irrigated with drainage water for 40 years; while, the lowest one was

obtained from soil irrigated for only 10 years. In uncultivated soil the extractable Pb

was 2–10 ppm.

Ramadan (1995) reported that, in polluted alluvial soils, the Pb content ranged

between 34.4 and 101.1 ppm with an average of 92.8 ppm. In the same contex,

Rashad et al. (1995) showed that the total content of Pb in the normal alluvial soils

of Nile Delta ranged from 32 to 48 ppm.

On the other hand, in an industrial area, north of great Cairo, the highest

enrichment factor ratio was for Pb in the soil clay fraction (El-Sayed and Hegazy

1993) or in the soil silt fraction (Rabie and Abdel-Sabour 1999).

Factors Affecting Lead Uptake by Vegetable Crops

Uptake of Pb in vegetable crops is regulated by lead concentration in the soil, soil

pH and cation exchange capacity (CEC) of the soils as well as by plant species, the

ethics of unsafe agriculture practices.

Lead Concentration in the Soil

Concerning the correlation between the concentrations of Pb in the soil and

vegetables, Nicklow et al. (1983), in their studies on various vegetable crops found

that Pb concentrations in leaves and roots tissues were positively proportional to the

concentrations of Pb in the soil. Similarly, Davies (1995), Whatmuff (2002),

McBride (2003) reported a positive relationship between the concentrations of Pb in

the soil and those in the plants.

Watanabe and Nakamora (1972) stated that Pb uptakes by eggplants from soil

treated with Pb ASO3 up to 750 mg kg-1 soil, ranged between 0.21 and 0.35 ppm in

the fruits and were dependent on the rate of Pb applied, but the uptake of the other


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plant parts were higher and more dependent on the application rates. Thornton and

Jones (1984) mentioned that increasing soil Pb content increased Pb contents in

radish and lettuce plants. Warren (1987) reported that Pb contents of the plants,

grown on mineral soils, were highly correlated with Pb concentrations in the soils,

although the relationships among plant organs were different. Likewise, Poskuta

et al. (1987) found that the influence of Pb concentration in roots medium on its

accumulation in pea seedlings was independent; whereas, the correlation between

Pb accumulation in shoots and Pb concentration in the root medium appeared almost

linear. Hassan (1994) mentioned that Pb contents in broad bean and spinach plants

were positively correlated with Pb concentrations in the rhizosphere and growth

stage.

Lead Accumulation in Soil Profiles

Regarding the lead accumulation in soil layers, Yousry and El-Sherif (1977) showed

that Pb was largely retained within the surface soil and showed very little movement

through the subsoil horizon. Similar findings were documented by many other

investigators such as Taylor and Griffin (1981), Khan and Frankland (1983),

Cieslinski and Mercikm (1993) they reported that the soil Pb was mainly found in

the plough layer. Also, Malavolta (1994) and Davies (1995) showed that Pb

appeared to accumulate naturally in surface horizons of soil.

Czuba and Hutchinson (1980) found that Pb concentrations in cultivated soils

tended to decrease with about 50 % from the surface to a depth of 48 cm. Moreover,

undrained soils contained higher Pb levels than cultivated soils at all depths.

However, Angima and Sullivan (2008) reported that in soil, lead is held tightly on

the surfaces of very fine clay and organic matter particles.

Soil pH

Many studies indicated a clear reduction in Pb uptake by vegetable crops as the soil

pH decreased (Cox and Kains 1972; Matt John and Laerhoven 1972; Merry and

Tiller 1986).

Nicklow et al. (1983) reported that Pb uptake by vegetables, grown in Pb

containing soils depended on soil pH. They added that lead is more soluble in acidic

soils than in alkaline ones; where Pb precipitates as hydroxides, and becoming less

readily available to plants. Merry et al. (1986) stated that increasing soil pH

decreased Pb concentrations in the plants, an effect that was more remarkable in

highly contaminated soils. A high pH may precipitate Pb as hydroxide, phosphate,

or carbonate and promotes the formation of Pb-organic complexes. Alteration of pH

resulted in changes of chemical forms of the Pb in the soil; the changes were more

significant when soil pH values were decreased from 7.0 to 4.5, whereas the levels

of Pb in an exchangeable form increased. Meanwhile, Pb in carbonate form

decreased, but the uptake rates of the Pb in exchangeable and carbonate forms were

similar (Xian and Shokohifard 1989). Cieslinski and Mercikm (1993) reported that

Pb uptake by strawberry plants was influenced by changes in soil pH.


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Matt John and Laerhoven (1972) showed that application of lime to the soil

depressed Pb uptake by lettuce plants. Whereas, Leschber and Davis (1985) found

that the solubility of Pb can be greatly decreased by liming.

Plant Species

Plants take up heavy metals by absorbing them from deposits on the parts of the

plants exposed to the air from polluted environment as well as from contaminated

soils (Khairiah et al. 2004; Al-Jassir et al. 2005; Kachenko and Singh 2006; Singh

and Kumar 2006; Sharma et al. 2008a, b). Singh et al. (2010) stated that Pb

concentration varied among the tested vegetables, which reflect the difference in

their uptake capabilities and their further translocation to edible portion of the

plants.

Lead uptake is generally reported to be the highest in leafy vegetables, especially

lettuce and spinach, and the lowest in root and fruit vegetables (Weigert 1991;

Jinadasa et al. 1997; Lehoczky et al. 1998; Sharma et al. 2006; De Nicola et al.

2008; Farooq et al. 2008; Lacatusu and Lacatusu 2008). However, Singh et al.

(2010) reported that percent contribution of fruit vegetables to daily human intake

for Pb was higher than that of leafy vegetables (Table 1).

Nicklow et al. (1983) studied the effect of varying soil Pb levels on Pb uptake of

leafy and root vegetables. They pointed out that leaf tissues of lettuce and turnip

accumulated the highest concentrations of Pb, while leaf tissues of beet and carrot

accumulated medium concentrations of Pb, but collard and Kale accumulated the

lowest concentrations. However, Nasralla and Ali (1985) studied the accumulation

of Pb in vegetable crops grown around six Egyptian traffic roads. They showed that

the edible portions of leafy vegetables, such as cabbage and lettuce were, the highest

accumulators of Pb (78.4 ppm); while the root vegetables, such as carrots and

radish, were the least Pb accumulators (3.8 ppm). But fruit vegetables, such as

pepper and tomato, were intermediate Pb accumulators (0.7–18.6 ppm); depending

on traffic densities and distances from the road.

Antosiewicz (1993) studied the mineral status of dicotyledonous plants in

relation to their ability to tolerance to Pb. He clarified that tomato had a high ability

to tolerance to Pb due to high tissue Ca content during administration of Pb.

Wierzbicka (1999) mentioned that constitutional tolerance of vegetable crops to Pb

depending on the species, cultivar, developmental stage, and duration of treatment

with Pb. He also, added that the species, cultivars and populations, considerably,

affected Pb uptake; although no relationship was found between the degree of

tolerance to Pb and the amount of Pb in tissues.

Table 1 Lead contents in vegetable crops, mg kg-1 (Weigert 1991)

Vegetable crops Mean value Minimum value Maximum value

Potatoes 0.09 0.005 1.9

Lettuce, cabbage 0.2 0.001 6.1

Tomatoes, cucumber 0.07 0.005 1.9


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Farooq et al. (2008) found that the leaves of spinach, cabbage, cauliflower,

radish, and coriander contained higher concentration of Pb as compared to other

parts of each vegetable. High concentration of Pb as analyzed in the present analysis

of different parts of the vegetables might be related to their concentration in the soils

irrigated with industrial waste water.

Unsafe Agricultural Practices Ethics

Modern farming is a race against time—to produce enough food for six billion

people. The world’s population is a ticking clock; the day is approaching when we

will no longer be able to support this many people, may be this leads to adoption of

unsafe agricultural practices for unethical production of some of our food. Ethics is

about choices, and agricultural practices (farming practices) ethics, is about choices

for people engaged in agriculture either directly as farmers, or indirectly as

government regulators, extension agents, and researchers. Many of the agricultural

practices may be unethical, from these practices use of questionable chemicals, in

vegetables production, that may be toxic to humans, and/or carcinogenic (cause

cancer) or teratogenic (cause birth defects). This is largely due to insufficient

scientific research into the safety of these chemicals, and the lack of viable

alternatives to define the farmers by seriousness of use these chemicals. Also, from

unethical agricultural practices; planting vegetable crops near highways or industry

regions, using sewage sludge, sewage water and industrial waste water in production

vegetable crops that may be contribute to increase the Pb soil content or other heavy

metals and then rapid access to the food chain.

Ethics of Using Unsafe Sewage Water

During last decade, there is a growing concern about usable water resources

decreasing. Currently, the world is moving towards a water crisis. Water shortage is

an important concern in arid areas such as Africa, Southern Asia and Middle East

and even in some parts of the world where it may lead to a war crisis (Jaafarzadeh

1996). On the other hand, continued population growth, increased per capital water

consumption and increased water requirements for industry and irrigation result in

considerable decrease of usable water resources (Behbahaninia and Mirbagheri

(2008). Disposal of sewage water and industrial wastes is a great problem. Often it

is drained to the agricultural lands where it is used for growing crops including

vegetables. In this situation, wastewater use for agricultural irrigation can be

beneficial and cost-effective in low-income arid and semi-arid countries, that can

have a high payoff in human welfare, with increased possibilities for food

production and increased employment opportunities for poor population groups

living in the peripheries of towns and cities (Drechsel et al. 2010). Although the

practice is aimed at producing socio-economic benefits, it is not safe and may not be

sustainable in the long-term (Mapanda et al. 2005). These sewage effluents are

considered not only a rich source of organic matter and other nutrients but also they

elevate the level of heavy metals like Fe, Mn, Cu, Zn, Pb, Cr, Ni, Cd, and Co in

receiving soils (Singh et al. 2004). However, Behbahaninia and Mirbagheri (2008)


123

concluded that the use of wastewater application in agricultural lands enriched soils

with Pb, and other heavy metals to concentrations that may pose potential

environmental and health risks in the long-term. Similarly, successive applications

of wastewater may affect the uptake of Pb by modifying the physico-chemical

properties of the soil such as pH, organic matter, bioavailability of Pb and other

heavy metals in the soil (Yusuf and Osibanjo 2006; Muchuweti et al. 2006; Singh

et al. 2010). Sharma et al. (2007) showed that wastewater irrigation increased

contamination of edible parts of vegetables with Pb, resulting in potential health

risks in the long term. Similar findings have been documented from a study

conducted in Harare, Zimbabwe where farmers used wastewater for irrigating leafy

vegetables (Mapanda et al. 2005).

Ethics of Using Unsafe Sewage Sludge as Fertilizer

As a result to the national standards for the addition of sewage sludge to

agricultural land were less stringent in many countries, sewage sludge is

commonly touted as free fertilizer and some farmers accept it in hopes of

improving their living conditions, since it has the potential to boost production for

certain crops as result to its content of macro and micronutrients (Berti and Jacobs

1996). Sludge may be free fertilizer for the farmer, but it is also free landfill in the

agricultural land. Also, it can present a high metal concentration (Pb, Cd, Cu, Ni

and Zn) that can cause serious problems in vegetable plants and its consumers. For

this, ethically, Farmers need to recognize that there are other things in municipal

sewage sludge that they are getting for free, like heavy metals, pathogens and

pharmaceuticals. Bioaccumulation transforms normal concentrations of Pb into

toxic concentrations in different biotic species and man (Tavares and Carvalho

1992). Thus, it is necessary to be alert and aware of the use of organic fertilizers

produced from sewage sludge.

Successive applications of sewage sludge in agricultural soil may result in

accumulation of Pb and other heavy metals in the environment and in the food chain

as follows: from sewage to soil to plant to animal to man, orderly (Kabata-Pendias

and Pendias 1992; Mensah et al. 2008) and may effect on the uptake of Pb by

modifying properties of the soil and bioavailability of Pb and other heavy metals

(Yusuf and Osibanjo 2006; Muchuweti et al. 2006; Singh et al. 2010).

Ethics of Unsafe Planting Vegetable Crops Near Highways

Also, from unsafe agricultural practices ethics, allow for farmers, by planting leafy

vegetables near highways or industry regions, in the peripheries of towns and cities,

are exposed to atmospheric pollution with Pb which may deposited on soil and

absorbed by the vegetables or deposited on the leaves and fruits then absorbed

during growing vegetable crops in the field or during their transportation and

marketing (Yousry and EL-Sherif 1977; El-Sokkary 1978; Al-Jassir et al. 2005;

Radwan and Salama 2006; Yusuf and Oluwole 2009).


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Distribution of Pb in Plant Organs

The content of Pb in various plant organs tends to decrease in the following order:

roots [ leaves [ stem [ inflorescence [ seeds. However this order can vary with

plant species (Antosiewicz 1992). Munday (1975) demonstrated that foliar

application of Pb resulted in higher concentrations of this element in roots of

Phaseolus vulgaris, than in the untreated plants, indicating its absorption by leaves

and then translocation within the plants to roots. Nicklow et al. (1983) found that

vegetable crops differed greatly in this connection. Beets had the highest Pb

concentration in the root peel (90 ppm) and the lowest Pb concentrations in the root

(23 ppm). Turnip had the highest Pb level in the leaf, but the lowest in the root peel.

However, in cucumber seedlings, Burzynski (1984) reported that Pb accumulation

was mainly in roots (93–96 %) and partially in hypocotyle (4–7 %). Likewise,

Krzeslowska and Wozny (1996) stated that, generally, Pb is not a mobile element,

and that more than 90 % of its contents in the plant accumulated in roots and only

10 % can reach to the stems and cells containing chloroplasts. Moreover, Tung and

Temple (1996) reported that soil-borne Pb accumulated primarily in the roots of

tomato and bean; although, at high concentrations, Pb also accumulated at the ends

of transpirational streams and the terminal of xylem streams. Michalak and

Wierzbicka (1998) found that onion plants developed from seedlings contained

more Pb in their roots and shoots than the onion plants developed from bulbs.

Where, adventitious roots of onion bulb plants were about twice thicker than the

roots of seedlings. Therefore, the uptake surface of adventitious roots was much

lower than that of seedling roots.

Less severe influence of Pb on the stem was most likely due to its weak mobility

and, hence, lower lead contents of the above-ground organs. For instance, Poskuta

et al. (1987) found a nearly linear rise in the Pb content of pea stems as the Pb

concentration in the medium increased. Simultaneously, the Pb contents of roots

reached their maximum at the lowest concentration of Pb in the medium and

exceeded several times those of stems. They concluded that root is considered to be

the main lead storage portion. The same conclusion was reported by El-Shebiny

(1989) who found that, after Pb application, ratio of Pb in shoots to roots of tomato

plants was depressed due to its more accumulation in roots. Likewise, Cieslinski and

Mercikm (1993) reported that Pb content was the highest in roots of strawberry and

there was a significant positive correlation between Pb concentration in the soil and

the roots and leaves. On the other extreme, Pb concentration of the fruits was very

low.

Michalak and Wierzbicka (1998) found that the lead in onion plant tissues,

developed from bulb, was distributed in the following way. The roots always

contained the largest amount of Pb. However, it was not uniformly distributed along

the root. Root tips contained the highest concentration, and intermediate amounts

were found in the farther parts of the root; while, the lowest concentration of Pb was

in the root base. They added that shoots, usually, contained much less Pb than roots.

Also, distribution of this element was uneven. The largest amount of Pb was found

in the basal part of the leaves, while their apexes contained 1.2–2.4 times less.

Recently, Farooq et al. (2008) found that the leaves of spinach, cabbage,


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cauliflower, and coriander contained higher concentrations of Pb as compared to

other parts of each vegetable (Table 2).

Lead Effects on Vegetable Crops

Two pathways are available for Pb uptake by plants; roots and foliage. Once inside

the system, Pb seems to be retained by cell membrane, mitochondria, and

chloroplats (Sabnis et al. 1969). Nevertheless, Nasralla and Ali (1985) suggested

that Pb accumulation in vegetable plants was performed through both foliage and

root systems, but Pb absorption via foliage was more pronounced at locations close

to the emission source of Pb vapor and fine particles. Elevated Pb level in soils may

adversely effect soil productivity and even a very low concentration can inhibit

some vital plant processes, such as inhibition of enzyme activities, photosynthesis,

disturbed mineral nutrition, change in hormonal status, and alteration in membrane

permeability, mitosis, and water absorption showing toxic symptoms of dark leaves,

wilting of older leaves, stunted foliage and brown short roots (Patra et al. 2004;

Sharma and Dubey 2005).

Visual Symptoms of Lead on Vegetable Crops

Khan and Frankland (1983) found that root and shoot growth of radish plants were

reduced when the Pb application exceeded 1,000 lg g-1 soil. Moreover, at high Pb

level (5,000 lg g-1 soil) the seedlings ceased growth, and had very thin stems and

small leaves, but without any chlorosis; although they survived for nearly 3 weeks.

El-Shebiny (1989) reported that spraying the tomato plants with various rates of Pb

led to burning of leaves margin, bending of branches and drop of a high proportion

of the flowers. Wozny and Jerczynska (1991) studied, at early stages of growth, the

effect of Pb on morphology of organs of Phaseolus vulgaris. They discovered that

presence of Pb at a concentration of 10-5 M reduced length of the main and lateral

roots, as well as thickness of the main root. They added that the circumference of

Table 2 Lead Concentration (mg kg-1) in plant organs of different vegetables (Farooq et al. 2008)

Vegetables Leaves Stems Roots

Spinach 2.251 ± 0.09b 1.193 ± 0.04e 1.121 ± 0.02d

Coriander 2.652 ± 0.04a 1.642 ± 0.02c 1.531 ± 0.05c

Lettuce 2.411 ± 0.08b 1.883 ± 0.02b 1.854 ± 0.06b

Radish 2.035 ± 0.10c 2.161 ± 0.03a 2.254 ± 0.09a

Cabbage 1.921 ± 0.04c 1.624 ± 0.02c 1.152 ± 0.04d

Cauliflower 1.331 ± 0.04d 1.313 ± 0.01d 1.222 ± 0.03d

Values are mean ±SD of three samples of leaves, stems and roots of each vegetable, analyzed indi-

vidually in triplicate. Mean values in the same column followed by the same superscript letters are not

significantly different (p [ 0.05)


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the root in the transition region was large after 24 h from culture and, after the next

2 days, the whole root systems turned brown.

Effect of Lead on Biomass Accumulation

Many reports showed that Pb induced inhibition of biomass accumulation in

vegetable crops. Merakchiliska et al. (1976) reported that PbCl2, at a concentration

of 10-5 M, had an adverse effect on growth and development of bean seedlings.

Khan and Frankland (1983) stated that, in metal-contaminated soils, stunted growth

of radish was a reflection of Pb toxicity and this influence was more pronounced on

roots than on shoots. Similar findings were reported by Wagatsuma et al. (1985)

who mentioned that growth of adzuki beans (Vigna angularis) was inhibited in soils

polluted with Pb or with added Pb. Similarly, Hassan (1994) reported that Pb

adversely affected the whole plant growth, as well as growth of individual plant

parts, of broad bean and spinach; especially at the high levels of Pb in nutrient

solution. Recently, Hamid et al. (2010) found that increasing lead acetate levels up

to 100 ppm lead to several disruptions of Phaseolus vulgaris plants.

Application of Pb at the lowest dose (75 ppm), significantly, increased the dry

matter yields of tomato and eggplant; whereas the reverse was true with the highest

dose of Pb (600 ppm), as reported by Khan and Khan (1983). Xian and Shokohifard

(1989) found that as soil pH decreased, Pb content in roots, stems, and leaves of

bean plants increased, while dry matter yields of roots and stems as well as total DM

yield were decreased. Likewise, El-Shebiny (1989) mentioned that soil or foliar

addition of Pb lowered the fresh and dry weights of roots and shoots of tomato

plants grown in the alluvial clay soil. Salim et al. (1992) and El-Koumey (1999)

stated that soil addition of Pb to carrot and cowpea plants, irrespective of the used

level, decreased dry matter yield. On the same direction, Sorial and Abd El-Fattah

(2001) found that plant height, root length, dry matter content, net assimilation rate

(NAR) and relative growth rate (RGR) of pea plants decreased with increasing the

amount of Pb applied in the nutrient solution.

Regarding the effect of lead on leaf area, Merakchiliska et al. (1976) found that

PbCl2 at 10-3 M, strongly, depressed leaf area and fresh weight of bean seedlings.

Wozny and Jerczynska (1991) showed that the surface area of the blades of primary

and trifoliate leaves of bean plants were smaller in the lead-treated plants than the

untreated ones. Also, Sorial and Abd El-Fattah (2001) reported that increasing Pb

concentration in the nutrient solution decreased leaf area ratio (LAR) of pea plants.

Concerning the effects of Pb on yield and its components, Matt John and

Laerhoven (1972) and Patel et al. (1977) mentioned that the application of Pb

reduced significantly the lettuce and bean yields, orderly. In addition, Xian (1989)

reported that the high concentrations of the Pb decreased significantly the yield of

kidney beans. Also, the fresh weight of the tomato fruits was adversely affected as a

result of increasing Pb concentrations (EL-Shebiny 1989). Moreover, Sorial and

Abd El-Fattah (2001) illustrated that increasing the concentration of Pb, decreased

appreciably number of pods plant-1, number of seeds pod-1, seed yield plant-1, as

well as total protein content of pea plants.


123

Effect of Lead on Cell Division

The mechanism of growth inhibition by lead is not well known in details. However,

the available evidence suggest that one of the ways of growth inhibition involve a

decrease in number of dividing cells under the influence of lead. Wozny and

Jerczynska (1991) estimated the mitotic index (MI), as percentage of dividing

nuclei, for root apical meristems of bean plants grown on the Pb containing medium.

The percentages of cells at particular stages of mitosis were also calculated. They

found that values of MI, number of prophases and telophases decreased under the

influence of lead; whereas, the metaphases increased.

Wierzbicka (1989) found that a partial inhibition of cytokinesis during c-mitosis

(abnormal mitosis); leading to formation of polyploid nuclei, enveloping a fragment

of the cell plate, and full inhibition of cytokinesis, led to binucleate cells, when

onion plants were treated with Pb. In another work, Wierzbicka (1994) clarified that

root growth and mitotic activity of onion were gradually inhibited by Pb Cl2 during

the initial hours of incubation (7.5–12 h) and were accompanied by an increase in

the incidence of abnormal mitosis to about 40 %. Liu et al. (1994) found that lead

nitrate reduced root growth of onion plants and caused mitotic irregularities,

including c-mitoses, anaphase bridges and chromosome stickiness. They added that

the c-mitoses effect was the greatest in the meristem with [10-4 M lead nitrate,

when almost all of the anomalous dividing cells were of this type.

Hassan (1994) studied the chromosome behavior in root tips and pollen mother

cells of Vicia faba as affected by increasing concentrations of Pb. He found that the

aberration percentages, such as fragments, gaps, stickiness, and irregular anaphase,

in each of the mitotic and meiotic systems increased with increasing Pb levels.

Effect of Lead on Lipids

Stefanov et al. (1992) reported that Pb ions affected glycolipid metabolism,

particularly in the roots of bean, but did not significantly affect phospholipids or

sterols. The effects of lead acetate on lipid composition of leaves, thylkoid

membranes and cell debris of spinach were studied by Stefanov et al. (1995). They

reported that Pb treatment decreased monoglactosyl, diacylgycerols and phospho-

lipids content, while increased the other glycolipids, but there were insignificant

differences in the total lipids of thylakoid membranes. Moreover, they added that

the concentration of Pb in leaves and cell debris was higher than that in thylakoid

membranes. This was probably due to a protection of thylakoid membranes,

essential for photosynthesis, which is of great importance for plant.

Effect of Pb on Chlorophyll Biosynthesis

Some published reports indicated that Pb caused a reduction on chlorophyll

synthesis. Burzynski (1984) found that Pb uptake by young cucumber seedlings

reduced the chlorophyll content in the cotyledons. Also, Sengar and Pandey (1996)

stated that supply of lead acetate to green pea leaf segments, either in the absence or

in the presence of inorganic nitrogen, lowered total chlorophyll content. They added


123

that supply of reduced glutathione could completely overcome the inhibition of

chlorophyll biosynthesis by Pb. It is suggested that Pb interferes with chlorophyll

biosynthesis through glutothione availability. On the other hand, treatment of mung

bean seedlings with Pb inhibited delta-aminolevulinic acid, dehydratase activity,and

decreased total chlorophyll content; suggesting the possible regulatory role of the

enzyme on chlorophyll synthesis (Prasad and Prasad 1987).

Lead reduced chlorophyll a and b contents of bean and pea seedlings as

mentioned by Paivake (1983); Hamid et al. (2010) and Prasad et al. (1989),

respectively. Likewise, Sorial and Abd El-Fattah (2001) showed that all concen-

trations of Pb had deleterious effects on chlorophyll a, b and carotenoids contents of

pea leaves. Pb inhibits chlorophyll synthesis by causing impaired uptake of essential

elements such as Mg and Fe by plants Burzynski (1987b). On the other hand,

Tomsevic et al. (1991) found that Pb increased chlorophyll b content in seedlings of

bean and this was attributed to a reduced leaf size (Merakchiiska and Iordanov

1983). On the other hand, Zaman and Zereen (1998) found that Pb accumulate in

chloroplasts disorganized their ultrastructure and decreased the biosynthesis of

chloroplasts.

Effect of Lead on Water Intake

Large amounts of lead are accumulated in cell wall components and induce water

stress to plants (Burzynski and Grabowski 1984; Kumar et al. 1993; Singh et al.

1997/1998).

Burzynski (1987a, b) found that placement of 2 week old bean and cucumber

plants in PbCl2 solution caused significant decrease in transpiration and uptake of

water. He added that cucumber plants were the most sensitive to Pb and

accumulated the greatest amounts of Pb mainly in the roots. El-Shebiny (1989)

reported that the water content of tomato shoots was decreased when the plants were

treated with Pb up to 800 ppm. On the same side, Guttenberger et al. (1989)

reported that tri-ethyl lead accelerated plasmolysis and increased water permeability

of onion epidermal cells. They added also that exposure of cells to 10-3 M tri-ethyl

lead for 12 h was lethal.

Effect of Lead on Assimilation of Nitrate

Nitrate is the predominant form of inorganic nitrogen available to vegetable crops

and gets assimilated into nitrite by nitrate reductase, the rate-limiting enzyme in the

overall assimilation of nitrate.

Burzynski and Grabowski (1984) found that PbCl2 at 10-3 M decreased NO3-

uptake by 50 % and reduced nitrate and nitrite reductase activity (NRA) in

cotyledons and roots of cucumber seedlings. They added that low Pb concentrations,

which inhibited nitrate reductase activity, did not affect enzyme induction, but

depressed tissue hydration.

Mamta and Gadre (1997) reported that substrate of NRA, in green Phaseolusvulgaris leaf segments, was inhibited by 0.01–0.10 mM Pb acetate. However, the

endogenous NO3- pool, measured indirectly as nitrite secreted into the medium, was


123

decreased at 0.1 mM Pb only and not at lower concentrations. They added that an

inhibitory effect of Pb on enzyme activity was observed during the supply of various

organic and inorganic nitrogenous compounds and not in their absence. It was

concluded that Pb has an inhibitory role on NAR, apparently through an effect on

intracellular mobilization of nitrate.

The response of nitrate reductase activity (NRA) to exogenous lead supply is

different in different plant species, cultivars and organs (Singh et al. 1997/1998).

They, also, found that supply of 0.1–0.2 mM lead acetate to intact mungbean

seedlings caused decrease on root NRA, while leaf NRA increased significantly

with increasing Pb concentration which was more pronounced in light than in the

dark. On the other hand, they reported that the inhibition on root NRA could be

alleviated by addition of inorganic salts such as K2HPO4 and KNO3 in the

incubation. It is interesting to note that Pb caused inhibition on NRA is reversible.

Inhibition on NRA by Pb was reported in the other plants (Brackup and Capone

1985; Sinha et al. 1988; Kumar et al. 1993; Singh et al. 2003; Xiong et al. 2006).

The causes of inhibition may be due to reduced supply of NADPH, disorgani-

zation of chloroplasts, less NO3- supply to the site of synthesis caused by water

stress, and direct effect of lead on protein synthesis because it has a storage affinity

for functional sulfhydryl group of the enzyme (Burzynski and Grabowski 1984;

Singh et al. 1997/1998).

Effect of Lead on Nutrients Absorption and Accumulation

Lead was found to affect the uptake and concentration of nutrients in plants. In most

cases Pb blocks the entry of cations (K?, Ca, Mg, Mn, Zn, Cu, Fe 3?) and anions

(NO3- ) in the root system (Sharma and Dubey 2005). Matt John and Laerhoven

(1972) found that application of lead chloride lowered the amount of sulfur and

Phosphorus in lettuce plants. Moreover, soil application of Pb, significantly,

increased Fe and Mn concentrations in tomato plants, but decreased Mn, Zn, Fe, Cu

and Na contents in eggplant and Zn in tomato plants (Khan and Khan 1983). They

added that K, Ca and Mg concentrations in both crops were significantly increased

with the initial level of applied Pb (75 ppm) and decreased with the high doses. In

cucumber seedlings, Pb inhibited the absorption and accumulation of K, Ca and Fe,

and the high doses caused an efflux of K? from roots (Burzynski 1987a) However,

the highly negative effects of Pb polluted soil on uptake and concentration of N, P

and K were also reported by Hlusek and Richter (1992) on potato plants, and by

Paivake (1983), and Sorial and Abd El-Fattah (2001) on pea plants.

Strategies to Minimize Lead Hazard

Remediation of Pb-contaminated Soils

The remediation of Pb-contaminated soils represents a significant challenge to many

industries and government agencies. During recent years the concept of using plants

to remediate heavy metal contaminated sites (called phytoremediation) has received


123

greater attention (Raskin et al. 1994; Vassil et al. 1998; Meagher 2000; Jarvis and

Leung 2002). Phytoremediation, natural plants are able to bioaccumulate Pb in their

above-ground parts which are then harvested for removal such as, using Indian

Mustard (Brassica juncea), Ragweed (Ambrosia artemisiifolia), Hemp Dogbane

(Apocynum cannabium), or Poplar trees which sequester lead in its biomass

(Suruchi and Khanna 2011). Phytoremediation is considered a clean, cost-effective,

and non-environmentally disruptive technology, to remove Pb from polluted soils.

However, one major disadvantage of phytoremediation is that it requires a long-

term commitment as the process is dependent on plant growth, tolerance to toxicity,

and bioaccumulation capacity.

Reducing Uptake Pb

In general, most strategies which aims to minimize lead hazard focus on reducing

uptake Pb. Good agricultural practices ethics is one of these strategies that include

(1) Cultivation of vegetables crops as far from the high traffic density of streets or

highways and industry regions (Al-Jassir et al. 2005; Radwan and Salama 2006;

Yusuf and Oluwole 2009). (2) Decrease the bioavailability (toxicity) of lead in soil

by several soil management practices such as: (a) Maintaining a near-neutral soil pH

(Merry et al. 1986), (b) Nonuse of sewage sludge and waste water in cultivated soils,

(c) Adding organic matter will enhance the formation of organic compounds that

bind lead (d) Addition humic acid and lime had better inhibition effect on the

migration of Pb in the soil-crop system (Kim et al. 1988), (e) Adding phosphorus

will reacts with lead to form insoluble compounds (Zhu et al. 2004).

Awareness Consumers of Vegetable Crops to Avoid the Hazard of Lead

Studies have shown that lead does not readily accumulate in the edible parts of fruit

vegetable crops (e.g., beans, squash, tomatoes, eggplant and strawberries). Higher

concentrations of Pb are more likely to be found on surfaces of leafy vegetables

(e.g., lettuce and spinach) from lead–laden dust and on the surface of root and tuber

crops (e.g., carrots, horseradish, potato) if soils are contaminated. To remove dust,

remove outer leaves of leafy vegetable crops, peeling root, tuber and some fruits of

vegetable crops as well as washing vegetables in water or water containing 1 %

vinegar may be an important tools in reducing the Pb concentration (Angima and

Sullivan 2008; Al-Jassir et al. 2005; Yusuf and Oluwole 2009; Sharma et al. 2009).

Conclusion

Environmental pollution, especially by heavy metals, is one of the most effective

factors in the destruction of the biosphere components. Lead and its compounds

tend to accumulate in soils because of its low solubility, mobility and relative

freedom from microbial degradation of this element in the soil. Lead is widespread,

especially in the urban environment, and is present in the atmosphere, soil, water,

and food.


123

Children are vulnerable to Pb toxicity; it causes damage to the central nervous

system and, in some extreme cases, can cause death. Lead is poisonous and there are

fears that body burdens, below those at which clinical symptoms of Pb toxicity

appear, may cause mental impairment in young children. Moreover, the carcino-

genic and mutagenic properties of lead were reported.

The major source of Pb soil-contamination appeared to be from lead-based

paints. Also, lead was widely emitted into the environment as a result of human

activity namely: mining and smelting activities, sewage sludge usage in agriculture,

and contamination from vehicle exhausts.

Lead is largely retained within the surface soil and has a very little movement

through the subsoil horizon. Lead uptake by vegetable crops is greatly reduced as

the soil pH increased. Lead is more soluble in acidic soils than in alkaline ones;

where Pb precipitates as hydroxides and becomes less readily available to plants. A

high pH may precipitate Pb as hydroxide, phosphate, or carbonate and promotes the

formation of Pb-organic complexes. Also, application of lime to the soil depressed

Pb uptake by plants.

Lead uptake is generally reported to be the highest in leafy vegetables, especially

lettuce and spinach, and the lowest in root and fruit vegetables.

Concerning the distribution of Pb accumulated in various plant organs, vegetable

crops differed greatly in this connection. Generally, Pb is not a mobile element and

more than 90 % of its contents in the plant are accumulated in roots and only 10 %

can reach to stems and cells containing chloroplasts.

Two pathways are available for Pb uptake by plants; roots and foliage. Visual

symptoms of lead on some vegetable crops are, at the high concentrations: reduced

length of the main and lateral roots, as well as the whole root system turn brown,

thin stems, small leaves, burning of leaves margin and bending of branches.

Lead induced inhibition of biomass accumulation in vegetable crops, resulting in

Pb toxicity, was more pronounced on roots than on shoots. Generally, as Pb

concentration increased; dry matter yields of roots, stems, and leaves as well as total

yield decreased. The mechanism of growth inhibition by lead is not well known in

details. However, the available evidences suggested that the ways of growth

inhibition involve: a decrease in number of dividing cells, a reduction on

chlorophyll synthesis, induced water stress to plants, decreased NO3- uptake,

reduced nitrate and nitrite reductase activity, a direct effect of lead on protein

synthesis, a decrease on the uptake and concentration of nutrients in plants.

The hazard of lead pollution can be reduced by the following approaches:

• Increasing the absorptive capacity of the soil by adding organic matter and

humic acid.

• Growing vegetable crops and cultivars with a low potential to accumulate lead,

especially in soils exposed to atmospheric pollution.

• Nonuse of sewage sludge and waste water in cultivated soils.

• Washing of leafy vegetables or peeling roots, tubers and some fruits of vegetable

crops before consumption may be an important factor in reducing the lead

concentration.


123

Acknowledgments We would like to thank the anonymous reviewers of a previous version of this paper

for their helpful comments.

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