Citation: Srivastava D, Singh A, Baunthiyal M. Lead Toxicity and Tolerance in Plants. J Plant Sci Res. 2015;2(2): 123.

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Abstract

Lead (Pb) is the most common heavy metal contaminant in the environment. Plants absorb Pb from their environment, but it is not an essential element. Pb is quite common especially in the soil of roadside fields as a result of emission from the automotive exhaust. It is also found in fields with a long history of fertilization with fertilizers containing Pb as impurity. In fact, there are numerous sources of Pb including soil, water, air, batteries, toys, cans and fertilizers among others. Here in this review, we focus on the effects of Pb on plant growth and development and also discuss the mechanisms plants adopt to tolerate lead toxicity. Pb is among the most commonly present heavy metals in terrestrial and aquatic ecosystems. It enters these ecosystems through various natural and anthropogenic sources. Pb gets accumulated in a dose-dependent manner and causes toxicity to the plant. Due to uptake of Pb, the concentration of Mn is increased, while the total concentrations of most other minerals including K, Ca, Na, P, Mg, Zn, Fe, and Cu is reduced by Pb. The sprouting of young seedling and its development is limited by the plant exposure to Pb exposure. Plants protect themselves against Pb toxicity through various mechanisms. There are at least three basic mechanism plants use to protect against Pb toxicity and they are passive mechanisms, inducible mechanisms and via antioxidant enzymes. Overall, we can conclude that Pb is harmful, but plants employ mechanisms to resist it. Thus further research should be to select and develop cultivars that have superior tolerance to Pb.

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Keywords: Lead; Lead toxicity; Sources of lead; Tolerance; Uptake

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Introduction

A metal or metalloid that is hazardous to the environment, for example metals such as chromium (Cr), cobalt, nickel (Ni), copper(Cu), zinc (Zn), arsenic (As), selenium (Se), silver (Ag), cadmium(Cd), antimony (Sb), mercury (Hg), thallium (TI) and lead (Pb) thatare normally denser than iron are termed heavy metals [1].

Heavy metals naturally occur in the earth and are releasedduring the weathering process. The concentrations of various heavymetals released during natural weathering are called backgroundconcentrations. However, human activities including disposal ofindustrial and domestic wastes, vehicular emissions, wastes fromPb acid batteries, paints and treated woods and the use of variousorganic and mineral fertilizers are the common sources of this heavymetal contamination [1]. During the 1930s-1970s, Pb was extensivelyused in gasoline as a component of tetra-ethyl lead [3]. In the aquaticenvironments of industrialized societies, it has been estimated thatthe Pb level increased two to three times those of pre- industrial level[4]. In North America, the use of leaded gasoline was largely phasedout by 1996; however, soils in the fields in the vicinity of roads have high Pb concentration. From about 500 BC to 300 AD there wasextensive use of lead in Roman aqueducts. As the lead azide or leadstyphnate are used in firearms, there is accumulation of Pb in thefirearms training grounds and such sites pose the risk of Pb poisoningof local population, especially the firing range employees [5].

There are several routes for heavy metals to end up in plants, animal and human tissues via air inhalation, contaminated diet and during manual handling. The major source of airborne contaminationis via motor vehicle emission. It’s not clear how the heavy metals areoriginated [6]. Heavy metal leaching from consumer and industrialwastes can pollute the water sources such as ground water, lakes,streams and rivers. Acid rain can exacerbate this process by releasingheavy metals trapped in soils [7]. Through the uptake of water ladenwith heavy metals, these metals enter the plants; and they find placein the animals when they feed on these contaminated plants; and thelargest sources of heavy metals in humans is through the ingestionof plant- and- animal- based foods. Another potential source ofheavy metal contamination is the contact with skin, followed by itsabsorption through skin [8]. The heavy metals can accumulate inorganisms as they are not metabolized [9].

The objective of this paper is to review the recent literature onthe effects of Pb toxicity on plant growth and enzymatic activities.The salient results are discussed with examples from recent literature.Varietal differences in tolerance or resistance to Pb toxicity are alsocovered along with the need for future research to reduce Pb toxicityto crops.

Sources of lead contamination of soil and water

Lead is harmful to human health as it is a toxic metal. Theconcentration of Pb, current medical condition, route of exposure (viaair, water or food), and age of the person are the factors to considerfor the degree of exposure and harmful effect. According to estimates,in children up to 20% of the total lead exposure can be attributed to awaterborne route. The main cause of Pb intake is via the drinking ofthe Pb contaminated water. The young children, fetuses and infantsare vulnerable to poisoning caused through Pb contaminated water.

Lead processing and smelting plants work with both the primaryand secondary Pb sources. Primary Pb is mined, separated from ore,and refined into various products; whereas, secondary Pb is recoveredfrom used objects - such as used Pb-acid batteries - for reuse in otherproducts. Smelting is a key process in production of Pb products,and involves the heating Pb ore or the recovered Pb with chemicalreducing agents. Both secondary and primary smelting processes canbe responsible for releasing large amounts of Pb into the surroundingenvironment.

There are different sources of Pb contamination of water resourcesas well as soil:

From home fittings made up of brass with Pb part of it, thedelivery of water through water pipes made up of Pb or Cu pipes withPb soldering, are the sources of Pb. In addition, the chances of Pbcontamination of water are greater in recently built house (< 5yearsold) with the above-stated fittings, and when such pipes are used tocarry naturally soft water and the water sits for several hours in thesepipes.

The sources of Pb indeed are from numerous daily used commonproducts in diverse locations, some of them quite unexpected.Some of the sources of Pb can be one never thought of; for example,selected toys, candies, and traditional medicines used in daily routine.Dust and chips from old paints are the most common sources ofPb contamination of soil and water resources, leading at times topoisoning via food chain.

The salient results on Pb contamination through various sourcesare summarized in the following section:

i. Soil: Since 1973, a gradual phasing out of Pb in gasoline inthe USA/India was started by the federal government, and the saleof leaded-gasoline was completely banned by 1996. However, Pbfrom car exhausts mixed with soil by roadside is still a source of Pb.The homes in the vicinity of busy streets likely have higher levels ofPb in the soil. Today, Pb still comes from metal smelting, batterymanufacturing, and from industrial units that use Pb. The Pb emittedfrom these sources gets into the air and part of it settles down onthe soil surface near homes, especially if the home is near one ofthese sources. Flaking Pb-based paint on the outside of buildings can also mix with the soil close to buildings. The soil contaminatedby Pb-based paint can be problem during home remodeling if thework is not carried out with proper precautions. However, once thesoil is contaminated with Pb, wind can do the rest by stirring thecontaminated dust and blowing it into homes and yards [10].

ii. Drinking Water: Pb seldom occurs naturally in water sourcessuch as rivers and lakes. Pb enters drinking water primarily as aresult of the corrosion or wearing of materials containing Pb in waterdistribution system in the households or via the plumbing workcarried out in the buildings. These materials include Pb-based solderused to join copper pipes, brass and chrome plated brass faucets,and in some cases, pipes made of Pb used to connect houses andbuildings to water mains. In 1986, the congress in USA banned theuse of Pb solder containing greater than 0.2% Pb, and restricted thePb content of faucets, pipes and other plumbing materials to 8.0%.Older construction may still have plumbings that have the potentialto contribute Pb to drinking water [10].

iii. Paint: Pb has been used in paints to improve the ability ofthe paint to hide the surface it covers, add color and to make it moredurable. The federal government in the USA for example, banned Pbpaint for use in homes in 1978. Home, furniture and toys, which weremade and painted before 1978 might contain Pb-based paints. Whenthe chips of Pb-based paint turns into dust, or gets into the soil, thenit becomes a point of concern.

iv. Dust: The most common way people are exposed to Pb isvia Pb dust. There are many ways to generate Pb dust in homes like,Pb dust which mostly originates from flaking of the paint or whenthe paint is scraped, sanded, chipped and or disturbed during homeremodeling. When young children put some items containing Pbdust on it into their mouths, they get exposed to Pb. Moreover, dustmay be invisible to a naked eye.

v. Air: There may be Pb in outdoor and indoor air. Pb in outdoorair comes mainly from industrial sources (e.g., smelters, wasteincinerators, utilities, and Pb-acid battery manufacturing). Windblownsoil and road dust also might contain naturally occurring Pbas well as Pb from industrial sources, deteriorated paint, and thecombustion of leaded gasoline and aviation fuels. Sources of Pb inindoor air include outdoor air, suspended dust, and during the courseof selected recreation or hobbies (e.g., making stained glass objectsusing Pb solder, shooting using Pb bullets at indoor firing ranges).Motor vehicle emissions are a major source of airborne contaminantsincluding arsenic, cadmium, cobalt, nickel, lead, antimony, vanadium,zinc, platinum, palladium and rhodium [6].

vi. Folk medicines, Ayurvedic medicines and cosmetics: Someof the folk medicines have Pb as contaminant. They often are importedfrom the Southeast Asia, Middle East, India, the Dominican Republic,or Mexico. Regarding this issue there are two examples - Azarconand Greta folk medicines. Azarcon is also known as Rueda, MariaLuisa, Coral and Alarcon and it is an orange powder where as Gretais present in yellow powder form. These medicines are used to treatthe illness arising out of upset stomach. There is one more medicinecalled Pay-loo-ah which contains Pb, and is in red powder form. Thismedicine is used for the treatment of fever or rashes. There are some other folk medicines, which generally contain Pb including Golf, Bala(or BalaGoli), Ghasard, and Kandu. Some cosmetics such as Surmaand Kohl (Alkohl) have also been reported to contain Pb .

In India or other eastern Asian countries, the traditional form ofmedicine practiced is Ayurveda. Ayurvedic medications may containminerals, herbs, animal products or metals. These medicines maybe non-standardized or standardized formulated. These Ayurvedicmedicines are typically exported to the United States through both byfollowers and practitioners of Ayurvedic medicine.

vii. Used Lead Acid Batteries: The residents of Uznova(Municipality of Berat) agreed to report on the exposure of Pb andagreed to get blood samples tested after a number of workshops andstakeholder meetings. This was followed by soil, air, and water testing.The assessment report of the findings was given to governmentagencies, and then the report was shared with the community, andwith the help of media it was distributed to the general public. Tobring the awareness in the society the World Health Day (2011) wasused by EDEN Center [2].

Symptoms and mechanism of lead toxicity to plants

Pb is among the most commonly present heavy metals interrestrial and aquatic ecosystems. It enters these ecosystems throughvarious natural and anthropogenic sources [11-13].

The Pb present in the soil solution soil is absorbed by theplant roots. A large proportion of Pb2+ is retained in plant roots inprecipitated form [14]. The accumulation of Pb in plants differs withplant species. The sprouting of seedlings and development is limitedby the plant exposure to Pb exposure [15-17]. The growth of aerialpart of plants and roots are inhibited by the low concentration ofPb [18,19]. If the Pb content is higher in the growing medium, theinhibition is strongly seen on root growth [12]. The stubby, short, bentand swollen roots with an increase number of secondary roots perunit root length are seen due to Pb toxicity [18]. The accumulation ofPb results in reduced growth and lower uptake of various minerals byplants. The concentration and total amount of the most of the minerals(Na, K, Ca, P, Mg, Fe, Cu and Zn) are reduced, although an increasein Mn concentration is seen as Mn uptake is less reduced relative tothe growth of the whole plant. A stronger decrease in the proline andchlorophylls a and b is seen due to the deficiency of mineral nutrients.It has also been observed that Pb reduces soluble proteins in wheatplants at a range of concentrations; and Pb accumulation increaseswith the increase in the exogenous Pb level. Moreover, Pb leads to abroad range of biochemical and physiological dysfunctions includingseed germination, nitrate assimilation, water status and the growth ofplants due to Pb [13,20,21]. However, there are some limitations in thetransportation of Pb from root to shoot [22]. Pb also adversely affectscarbon dioxide assimilation, photosynthetic rate, carotenoid contentsand chlorophyll, and these processes strongly reduced so much so thatthe exposure of plants greatly reduces the photosynthetic rate [23].Following Pb exposure of plants, there was a decrease in Ca, Fe andZn levels in the root tips [24]. The inhibition of mineral ion uptakeappears to be a general consequence of Pb exposure. Conversely, anincreased provision of certain inorganic salts can indeed antagonizePb effects to some extent [25]. The generation of free radicals such as superoxide anion radical (O₂–), hydrogen peroxide (H₂O₂), singletoxygen, and hydroxyl radical (HO•), which cause oxidative stress toplants and reactive oxygen species (ROS) are the important featuresof Pb toxicity to plants [26]. Following 48-72 h of Pb exposure, theloss of cristae, mitochondrial swelling, vacuolization of endoplasmicreticulum, injured plasma membrane and dictyosomes and deepcolored nuclei have been reported [27]. Lead interacts with theproteins present in cytoplasm and higher concentration of Pb maydecrease the protein pool [28-31]. Due to the modification in geneexpression, increased ribonuclease activity [17], acute oxidativestress of reactive oxygen species (ROS) [31-33], protein utilizationby plants for the purposes of Pb detoxification and diminution offree amino acid content [32] that is correlated with a disturbance innitrogen metabolism [28] the quantitative decrease in total proteinis seen with Pb addition. However, certain amino acids, like prolineincrease under Pb stress [34]. Such proteins play a major role in Pbtolerance by the plant. In contrast, low concentrations of Pb increasetotal protein content [29].

Mechanisms of Lead Tolerance

There are various ways by which plants respond to the noxious effects of Pb. For example, via uptake of selective metal, metal binding to the root surface, and induction of antioxidants like proline, nonprotein thiol (NP-SH), glutathione, cysteine, ascorbic acid, and antioxidant enzymes, such as guaiacol peroxidase (GPX), superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR) [33].

i. Passive Mechanisms: Pb interacts with cellular components and even a small amount of Pb increases the cell wall thickness. Plant cell walls contain pectin; and the complexation of Pb with the carboxyl groups of pectin is regarded as the most important interaction by which plant cells can resist Pb toxicity [25]. It was observed in F. hygrometrica protonemata that binding of Pb to JIM5-P acted as a physical barrier, and restricted the access Pb to the plasma membrane. However, in later studies it was reported that the Pb bound to JIM5-P within the cell can be taken up or remobilized by endocytosis, together with pectin epitope [35].

ii. Inducible Mechanisms: Recently, it has been reported by several authors that when the transporter proteins are present among plant cells, they play an important role in metal detoxification as they allow the metal ion excretion into extracellular spaces [36-38]. The human divalent metal transporter 1 (DMT1) expressed in yeast has been shown to transport Pb via a pH-dependent process [39] in plants. Simultaneously, several ATP-binding cassette (ABC) carriers such as AtATM3 or AtADPR12 at ATP-binding sites in Arabidopsis were reported to be involved in resistance to Pb [40,41]. Although, suspected to act against Pb, this detoxification mechanism has not yet been clearly established. Transcriptome analysis has shown that the gene expression of these carriers is stimulated by Pb [11].

iii. Antioxidant Enzymes: To avoid oxidative damage andfor achieving the increased production of ROS, all plants have anantioxidant enzymes system. This system scavenges the ROS, whichare present in different cell compartments [32]. The synthesis of theseactive enzymes may be induced or inhibited by Pb-induced toxicity. However, Pb-induced induction or inhibition of antioxidant enzymesdepends on metal, plant species, specific form of the metal, and theduration/intensity of the treatment [19,32]. Generally, the plantenzymatic activities are inhibited by Pb, and this is followed by changein the values of the inactivation constant (Ki) range between 10–5 and2 × 10–4 M, which means 50% inhibition in enzymatic activities in thisconcentration range [21]. The affinity of Pb for enzyme -SH groupssuggests enzyme inhibition [13,32]. These results have been testedon more than 100 enzymes, and seems correct for nitrate reductaseand including ribulose-1, 5-bisphosphate carboxylase oxygenase(RuBisCO). The altered tertiary structure of protein on catalytic sitesor elsewhere shows inactivation. When Pb binds with the protein-COOH group, the same effect is produced [32] and Pb interacts withmetalloid enzymes. Indeed, Pb can disrupt some essential parts ofthese enzymes like plant absorption of minerals including Mn, Zn andFe. Pb and other divalent cations also can substitute for these metals,and thereby inactivate enzymes, as occurs with ALAD [32,42,43]. Theeffect Pb has on ROS constitutes another mechanism by which Pbexposure affects protein behavior [32].