Urban farming as a possible source of trace metals in human diets

HOW TO CITE: Olowoyo JO, Lion GN. Urban farming as a possible source of trace metals in human diets. S Afr J Sci. 2016;112(1/2), Art. #2014-0444, 6 pages. http://dx.doi.org/10.17159/ sajs.2016/20140444 Rapid industrialisation and urbanisation have greatly increased the concentrations of trace metals as pollutants in the urban environment. These pollutants (trace metals) are more likely to have an adverse effect on peri-urban agriculture which is now becoming a permanent feature of the landscape of many urban cities in the world. This review reports on the concentrations of trace metals in crops, including leafy vegetables harvested from different urban areas, thus highlighting the presence of trace metals in leafy vegetables. Various pathways of uptake of trace metals by leafy vegetables, such as the foliar and roots, and possible health risks associated with urban faming are discussed and various morphological and physiological impacts of trace metals in leafy vegetables are described. Defensive mechanisms and positive aspects of trace metals in plants are also highlighted.


Introduction
Urban farming can be defined as the act of cultivating food crops, mostly vegetables, wherever land is available around or in the immediate vicinity of a major city. 1,2Farming activities around urban areas have become a prominent feature of some urban city landscapes, especially in developing countries. 3There are several reasons for farming activities around peri-urban areas and these include easy access to markets and transportation of goods.In some countries, poor urban households use urban farming to increase their household income by selling the yield or surplus to reduce part of daily expenses. 4The other probable reason for the increase in urban farming is the shortage of land.This involves farming areas previously used for either household or industrial waste, 5 supported by the notion that the soil will be very fertile.Urban farming also supports the campaign for organic farming.Consumers, in most cases, evaluate quality of leafy vegetables on their dark green colour and on size of the leaves as opposed to where farming activities have taken place. 6However, in urban city centres where farming activities are carried out around industrial areas, safety around the consumption of these vegetables cannot be guaranteed because various disposal practices often cause the accumulation of potentially toxic trace elements in the soil. 7,8thropogenic activities such as mining, emissions from vehicles, wrong agricultural practices and improper waste disposal are major sources of trace metal pollution in the urban environment. 5,97][8][9][10][11][12][13][14] In acceptable limits, trace metals play an important role in the health and physiological activities of plants, animals and humans. 15They are required in minute quantities as natural components of the environment.For example, zinc is an essential element required in minute quantities in living organisms, but when supplied in high quantities, it can be toxic to plants, producing purplish-red coloured leaves which is a symptom associated with phosphorus deficiency.Zinc may also cause chlorosis in younger leaves which may extend to older leaves. 16In humans, excess zinc may lead to metal poisoning and growth retardation.Excess nickel and lead may result in increased production of reactive oxygen species and membrane permeability disruption in plants.In all, concentrations of heavy metals above the required limits in plants are known to cause various deleterious effects on several plants systems such as the photosynthetic ability of the plants, mineral uptake and interactions with the water regime from the soil.In humans, excess lead may affect the functions of the liver and kidneys. 10,17,18e present review will establish, amongst others, the various pathways by which trace metals may be taken up by plants, the effects of trace metals on the morphology and physiology of the plants, the positive aspects of trace metals in plants and also the possible health risk for humans and livestock if trace metals are ingested in high concentrations.

Evidence of trace metals in plants
High deposition and accumulation of trace metals in the edible part of root and leafy crops has been reported in the literature. 19,20Vegetables are capable of accumulating trace metals from polluted soil and also from surface deposition onto their shoots in polluted atmospheric environments. 14Trace metals in the air have been reported to significantly influence total metal concentration of vegetable plants, especially when washing is not thoroughly done. 18mospheric fallout is one of the chief contributors to heavy metal uptake by plants through the stomata.The stomata openings are located on the surface of the plant leaves and perform multiple functions that include water regulation in the plant.Particulate matter from atmospheric fallout may be found deposited on the leaf surface and find a way into the leaves through the stomata.Smaller particles from atmospheric fallout may be incorporated into the leaves, whereas large agglomerates are trapped on the surface wax. 21,22The extent of uptake and the pathways involved may depend on the plant species and on the metal involved. 23The opening and closing of stomata may provide entrance for trace metals, blocking the stomata in some cases and may ultimately lead to the death of the plant. 23Entrance of metals via the foliage parts of plants was noted to be one of the major pathways by which metals enter leaves in a polluted area. 24 In a separate study on lead uptake by lettuce leaves, it was discovered that particulate matter deposited on plant leaves may be retained by cuticular waxes and trichomes, while some of the metals contained in particulate matter can penetrate inside plant tissues. 26Micro-Xray fluorescence, scanning electron microscopy coupled with energy dispersive X-ray microanalysis, and time-of-flight secondary ion mass spectrometry were used to investigate the localisation and the speciation of lead in the leaves of different plants around a copper smelter company and it was found out that lead-enriched particulate matter was present on the surface of plant leaves. 24The study further reported on biogeochemical transformations on the leaf surfaces with the formation of lead secondary species (PbCO 3 and organic lead).

Toxicity of trace metals in plants
The effect of trace metals on the epidermis was demonstrated on the young leaves of soyabean. 26,27The young leaves did not show visual symptoms when exposed to cadmium ions and the authors observed that cadmium ions did not have any effect on the closing and opening of the stomata.However, findings have revealed that interactions of cadmium ions with K + , Ca 2+ and abscisic acid showed strong interference with the guard cells. 28,29The application of cadmium on the leaf surfaces influenced the number of stomata, decreasing the number of stomata and stomatal openings on the leaf surface of the young leaves of soybeans. 27veral authors have also reported on the adverse effect of lead in plants.
Lead toxicity is said to have a negative effect on biomass production in plants as it affects chlorophyll biosynthesis and photosynthesis. 30,31ncreased concentrations of lead may also inhibit or delay enzyme activity changes in membrane permeability and water disturbance in plants, which may affect the growth of the plant negatively. 32dmium may penetrate the root via cortical tissue and reach the xylem through either the apoplastic or symplastic pathways possibly resulting in cadmium toxicity in plants. 33,34Soil pH is known to influence cadmium uptake and transportation.Uptake of cadmium by corn was lower in acid soils with high organic matter content.Cadmium has also been found co-accumulated with zinc in the aerial parts of Arabidopsis halleri. 35Toxicity of nickel affected the seedlings of Pisum sativum by changing the potassium uptake and water content, 36 showing that higher concentrations of nickel may lead to a reduction in plant growth, leading to oxidative stress.
When leafy vegetables are properly washed, the concentrations of chromium and lead may be reduced.However, the exogenous contamination of leaves may not be reduced in some instances owing to the nature of the vegetables, as was in the case with Gynandropsis gynandra L. that showed a marked tendency to accumulate lead and chromium. 5A similar observation was noted in a study by Gabrielli and Sanità di Toppi 37 where the dominant pathway for most trace elements to vegetable roots was from the soil, while trace elements in vegetable leaves appeared to originate mostly from the atmosphere.The result further indicated that high accumulation of trace metals such as lead, cadmium and chromium were the result of atmospheric deposition.
In all, it was evident that trace metals could reach the edible parts of vegetables, especially the leafy parts, through atmospheric deposition and could also be translocated to various parts of the plants via the root system.

Trace metals uptake mechanism by plants
8][39] Among crop types, leafy vegetables such as lettuce and cabbage have the greatest ability to take up trace elements from the soil. 40The mobility of trace metals in soil is favoured mostly under acidic conditions.Treating soil with lime in order to reduce soil acidity reduces the bioavailability of trace metals. 41,42herefore, low pH levels are effective in the remediation of polluted soil, while the soil organic matter ensures the availability of trace metals to the plant. 42On the other hand, at high levels of soil pH, the formation of soluble organometallic complexes may increase metal solubility although this is not true for calcareous soil. 43 increase in the amount of soil organic matter helps plants minimise trace metal absorption. 44The introduction of organic matter amendments in conjunction with lime had been used to assist in immobilising trace metals. 45However, the effects of organic matter on the bioavailability of trace metals in soil depend on the nature of the organic matter, microbial degradability, salt content, soil type and the particular heavy metal. 46In most cases, metallic elements are actively retained by lands that are rich in organic matter.The retention of trace metals in the soil affects the mobility of these elements and interferes with the uptake process.The bioavailability of trace metals is much lower in the presence of manure when compared to humified compost, suggesting that different types of organic matter may affect mobility of trace metals differently. 47This may be as a result of the ability of the matter used to redistribute trace metals from soluble and exchangeable forms to fractions associated with organic matter or carbonates and the residual fraction. 48 the root area where the plant interacts with the soil, metal ions cannot move freely across the cellular membranes.The membrane structure of the plant root is lipophilic, which requires that the transport be facilitated by proteins with transport functions. 49,50In the rhizosphere, metal transport is carried out by two processes known as bulk flow and diffusion. 51,52This process of uptake by plants is soon followed by a process controlled by root pressure and leaf evaporation, called transpiration.Through transpiration, the plant is able to absorb the trace metals through the roots via the xylem to the shoot of the plant.The process is dependent on water demand by the leaves in the aerial part of the plant. 49take of trace metals by higher or vascular plants is often through the root system, but can also occur through the leaves.It may therefore be difficult to distinguish whether the metals found in the plant tissues were originally from the air or soil. 53Plants that are tolerant to high levels of trace metals (also called hyperaccumulators) have the capacity to remove contaminants from the soil.One example of such a plant is Thlaspi caerulescens that has been used for phytoremediation of soils, especially in areas previously polluted by mining activities. 41The mechanism for hyperaccumulation remains unclear though it is generally believed to invlove three major phases involving rapid uptake of metals by the roots, high rate of translocation from roots to shoots and high storage capacity by vascular compartmentalisation. 41 Metal uptake by plants is affected by metal solubility and availability in the soil.In a situation where the level of trace metals in soil is very high, the release of root exudates and acidification are common mechanisms that are used by plants to modify the root area to acquire nutrients from the soil. 41,49In the case of nutrient movement across the biological membrane, plants have developed a specific mechanism meditated by proteins, for uptake, translocation and storage of the nutrients. 42,49embrane transporters are equipped with a structure that binds ions before transportation.This structure is receptive only to certain ions and as such is specific in their mode of action 49,54 The transmembrane structure then facilitates the transfer of bound ions from extracellular space through the hydrophobic environment of the membrane into the cell.Despite the presence of this structure, only a fraction of the total amount of ions associated with the roots are finally absorbed into plant cells. 54The other form of metal uptake in plants, apart from binding to the cell wall, is sequestration in cellular structures such as the vacuole, though this may make the heavy metals unavailable for translocation to the shoot. 55e evaporation of water from the leaves may also affect plant uptake and accumulation of trace metals.The evaporation process serves as a pump for more nutrients and other substances to be absorbed into plant roots.This process, called evapotranspiration, moves water and contaminants into the plants. 42The accumulation of metal contaminants is mostly assisted by microorganisms, fungi and bacteria that live in the root area.These microorganisms in the rhizosphere and closely associated plants may contribute to the mobility of metal ions.At the same time, plant roots release nutrients that sustain a rich microbial community in the root area, thus establishing an important symbiotic relationship between soil microorganisms and plants. 42,49In order to facilitate the transport process, several families of proteins are involved namely (1) influx transporter families such as zinc, a regulated transporter, iron, a regulated transporter protein, yellow-stripe and natural resistance associated macrophage protein and (2) efflux protein families such as cation exchanger, ATB-binding cassette and cation diffusion facilitator. 42,56Because these proteins are substrate specific, the comparison between influx and efflux transporters revealed that efflux proteins export metals from the cytoplasm while influx proteins take up proteins from the soil or medium. 56pending on their ability to adapt and reproduce in soils heavily contaminated with trace metals, higher plant species can be divided into two main groups.The two groups are the pseudometallophytes (plants that grow on both contaminated and non-contaminated soil) and absolute metallophytes (plants that grow only on metal contaminated and naturally metal-rich soils). 57The use of Raphanus sativus (a pseudometallophyte) for example, demonstrated the potential for root uptake in lead contaminated soil. 58Baker 58 showed that radish is a hyperaccumulator plant that can concentrate trace metals in different plant parts.It was also demonstrated that radishes are effective for remediation of polluted soil through their potential to extract metals from soil up to a certain level of concentration. 58The ability of plants to accumulate metals, thereby remediating metals, is directly proportional to the presence or availability of microorganisms in that plant's rhizosphere. 59In the study it was explained that microbial communities such as fungi, bacteria and other microbes are capable of altering the soil environment and as a result will translocate, absorb or sequester contaminants such as trace metals. 59,60er the years, more than 400 plant species with the ability to take up high levels of heavy metals in soil and water have been identified.Thlapsi spp., Brassica spp., Sedum affredii and Arabidopsis spp., among others, were studied. 61,62The use of vegetable plants has also been demonstrated by some researchers. 63For example, Amaranthus dubius, also known as morogo or wild spinach in South Africa, was found to have the ability to take up and translocate metals such as chromium, mercury, arsenic, lead, copper and nickel to the aerial parts of the plant. 64Some medicinal plants such as Datura stramonium and Amaranthus spinosus are capable of accumulating some trace metals in their tissues. 60 is believed that trace metals can help plants protect themselves from diseases and biological stress. 65,66If a metal becomes more toxic to a pathogen than to the plant, the metal can hamper the virulence of the pathogen and can increase the resistance of the plant to the biotic stress 65 by suffocating the pathogen in the plant.The excess trace http://www.sajs.co.za Volume 112 | Number 1/2 January/February 2016 metals found in the plant after the pathogen has been suffocated will then be redirected to normal growth.
The production of high levels of reactive oxygen species can adversely affect the plant.Therefore, plants have developed a defensive mechanism that involves glutathione in the detoxification of reactive oxygen species through the ascorbate-glutathione cycle. 67During exposure to high levels of trace metals, accumulated metal ions are detoxified by phytochelatins that are produced from glutathione in the plant.xposure to trace elements such as mercury, cadmium, lead and nickel in the soil, encourages the plants to formulate steps to counteract the effects of these toxins.Defensive mechanisms largely prevent the metals from getting inside the cells, but for metals that find a way into plants cells, they are neutralised and sequestered. 68

Quantifying human risk associated with trace metals in plants
1][72] Human health risks associated with these metals can be assessed based on the THQ method, 41 which takes into account the concentration of trace metals in food, the frequency of exposure, and the individual's age, body weight and frequency of consumption of the contaminated food.Should the THQ calculated for both adults and children exceed 1 (THQ>1) then a potential risk to the consumer will be suspected. 5,14,41Mercury was recorded as the major health risk contributor in children and chromium as the least contributor.The method for calculating the THQ is: where ADDM = (DI x MFveg) / WB. 14 ADDM is the average daily dose (mg.kg/day) of the metal and RfDM is the reference dose (mg.kg/day).RfDM is defined as the maximum tolerable daily intake of a specific metal that has no adverse effect. 73DI is the daily intake of leafy vegetables (kg/day), MFveg denotes the trace metal concentration in the vegetable tissues (mg/kg) and WB represents the body weight of investigated individuals.The DI is usually calculated at 0.182 kg/day for adults and 0.118 kg/day for children. 14,74The body weight of investigated adults is assumed to be 55.7 kg and for children 14.2 kg. 3,14If the value of HQM calculated should exceed 1 (HQM>1), then there may be potential risk to the consumer.

Conclusion
Trace metals are known for high mobility and bioavailability in consumed food products such as vegetables.Studies have shown that trace metals may find their way into the human system via the consumption of contaminated food crops harvested from polluted soil.The urban environment is constantly witnessing an increase in various developmental projects, with special reference to developing countries.If not properly managed, these projects may introduce contaminants, with special reference to trace metals, into the environment.However, farming activities are continuously been practised both on a small scale and a large scale around major cities and hence may be affected negatively by these contaminants. 71,75Reports from the literature have suggested that leafy vegetables are capable of accumulating and storing these trace metals in their edible parts.There may be a serious problem associated with urban agriculture relating to balancing demands associated with increasing populations against potential hazards arising from the use of contaminated urban sites for food production.It is necessary to investigate and document the ability and uptake mechanism of most vegetables in order to identify and document those that can grow without accumulating trace metals in order to reduce the danger trace metals might pose to consumers.It is also important to develop new farming practices around urban city centres that will reduce or elucidate the availability and uptake of trace metals by plants.

Figure 1 :Figure 2 :
Figure 1: Presence of pollutants around the stomata of leaves collected for a study conducted in Pretoria, South Africa at (a) 2000X magnification and(b) 3000X magnification.9The stomata are the bean-shaped structures and the arrow is pointing to the pollutants around them.