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Contaminants in Crop Plants
WEEDS AND COMPETITION
Contents Contaminants in Crop Plants Gene Flow and Herbicide Resistance Herbicide Application Technology Herbicide Resistance and Molecular Aspects Integrated Weed Management Thermal Weed Control Weed Biology Weed Competition Weed Control in Orchards and Vineyards Weed Seed Biology
Contaminants in Crop Plants R Maul, Leibniz Institute of Vegetable and Ornamental Crops Großbeeren/Erfurt e.V., Großbeeren, Germany C Schwake-Anduschus, MRI Max Rubner-Institut, Detmold, Germany M Wiesner, Leibniz Institute of Vegetable and Ornamental Crops Großbeeren/Erfurt e.V., Großbeeren, Germany Ó 2017 Elsevier Ltd. All rights reserved.
Abbreviations BCF Bioaccumulation factor HBCD Hexabromocyclododecane PAH Polycyclic aromatic hydrocarbon PBDE Polybrominated diphenyl ether PCB Polychlorinated biphenyl
Introduction Contamination of crop plants can be defined in a manner similar to that of food contamination, as the unintended presence of toxic substances, pathogens, or pharmaceuticals in crop plants. A contaminant is distinguished from a residue, which may also be a harmful compound present on crops. A residue is a substance that is added deliberately to the crop, and whose incomplete removal turns this agent into a residue. The presence of genetically modified material in nongenetically modified crops or seeds can also be defined as a contaminant. However, genetic contamination is beyond the scope of this article. The most important contaminants in crop plants are divided according to their origin into natural and anthropogenic. While mycotoxins, microorganisms, and toxic elements have always been present in the environment, and therefore also in human
442
PFAA Perfluorinated alkyl acid PFOA Perfluorooctanoate PFOS Perfluorooctane sulfonate POP Persistent organic pollutant
diets, biologically active or persistent organic pollutants or pharmaceuticals are predominantly man-made. By direct use of the crops in foodstuffs or as a consequence of carry-over effects from contaminated feed to animal foodstuffs, these contaminants enter the human food chain (Figure 1). Modern horticulture and agriculture can affect the occurrence of nonanthropogenic contaminants in diets, for example, by mobilization of mineral elements and organic compounds in the soil. In times of global water shortage and the necessity to enhance crop production by means of irrigation, sewage and industrial wastewater can become important water resources for crop production. Contaminated irrigation water bears the risk of spreading undesirable substances to agricultural fields, thereby allowing their accumulation by crop plants. Consequently, the contamination of vegetables with fecal microorganisms or pharmaceutical substances will be an important issue in the future.
Encyclopedia of Applied Plant Sciences, 2nd edition, Volume 3
http://dx.doi.org/10.1016/B978-0-12-394807-6.00247-1
Weeds and Competition j Contaminants in Crop Plants
Fungal infestation Pathogenic bacteria (sewage)
443
Pharmaceuticals / bioactive compound from personal care products
Fruits/ vegetables for human consumption (Persistent / halogenated) organic pollutants
(Heavy) metals
Feeding of livestock animals
Diary products/ meat for human consumption
Anthropogenic and natural sources of contaminants leading to contaminaƟon of food and fodder
Figure 1 Flowchart depicting the external influences that may lead to contamination of a crop plant with various substances and the potential routes of exposure to the contaminants for the human consumer.
In the following sections, five main sources of contamination relevant for crop plants will be introduced and discussed on the basis of examples.
Mycotoxins The risk of mycotoxin contamination of food and feed is as old as the history of mankind itself. Mold and mycotoxin contamination can occur at any stage in the food production chain: during cultivation, between harvesting and drying, and during storage. The Food and Agriculture Organization of the United Nations (FAO) estimates that 25% of the world’s agricultural commodities are contaminated with mycotoxins to some extent. Fungi of the genera Aspergillus, Penicillium, Fusarium, Alternaria, and Claviceps are the predominant mycotoxin producers with aflatoxins, ochratoxins, fumonisins, patulin, deoxynivalenol, and their derivatives, as well as zearalenone and its derivatives being the economically and toxicologically most important mycotoxins. However, numerous other potentially toxic fungal secondary metabolites have been detected, leading to a long list of the so-called emerging mycotoxins (e.g., fusaproliferin, beauvericin, enniatins, and moniliformin formed by Fusarium spp. or various ergot alkaloids formed by Claviceps purpurea). Several hundreds of fungal metabolites have been detected in food, feed, and its raw materials. While Aspergillus and Fusarium spp. are the predominant causes for the infestation of grains and nuts, Alternaria and Rhizopus spp. are more important for vegetables and fruits. Although certain Rhizopus spp. are mainly responsible for postharvest decay, or storage rot, of, for example, strawberry, tomato, and Brassicaceae, they do not produce any significant amounts of toxins, while alternaria toxins (alternariol, alternariol
monomethyl ether, altenuene, altertoxin I-III, tentoxin, tenuazonic acid) have been found in fruits, vegetables, oilseeds, and cereals visibly infected by Alternaria spp. Contamination of food and feed by aflatoxins produced by Aspergillus spp. poses enormous economic and health concerns because these substances are highly carcinogenic. The presence of these toxins in food correlates positively with the high incidence of liver cancer in various developing countries. The severity of a fungal infection, as well as the extent of toxin production, is dependent on various parameters. The climatic conditions are crucial for fungal growth, with humid and warm climates favoring their growth. However, particular toxigenic strains (e.g., Fusarium spp.) also can adapt to colder and drier environments. Furthermore, agronomic practices have an impact on the extent of fungal infestation and mycotoxin occurrence. Many, although not all, studies have reported a higher probability of fungal growth on crop plants under organic farming conditions. For coffee beans, a larger number of filamentous fungi could be observed under organic farming conditions. In Italian maize and Polish oats, fungal infection, and the number of mycotoxin-positive samples, differed significantly between farming systems, with a greater incidence in organic farming. By contrast, a more frequent crop rotation with noncereals was found to reduce mycotoxin concentrations and Fusarium infestations. When mineral fertilizers and herbicides were used, infestation of grains by Fusarium graminearum was reduced. The frequent occurrence, and the severe health concerns associated with some mycotoxins, has led to legislative consequences for consumer protection in almost all countries. Aflatoxin concentrations are regulated in more than 50 countries worldwide, with an upper limit between 2 and 30 mg kg1
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toxin in grains and nuts. For deoxynivalenol, which is a frequently occurring mycotoxin, the EU, China, Russia, Japan, and Canada have established legal limits of between 200 and 2000 mg kg1, while the USA has provided an advisory limit for selected commodities (e.g., 1000 mg kg1 on finished wheat products). The FAO together with the World Health Organization adopted a code of practice to prevent and reduce fungal infestation in cereals and occurrence of mycotoxins in the crop. The recommendations include measures related to good agricultural manufacturing practices for zearalenone, trichothecenes, ochratoxin A, fumonisines, and aflatoxins. Since the infested plants recognize the mycotoxins as xenobiotics, these toxins are subjected to metabolic changes in the plant. Thus, in infested plant tissue, mycotoxins such as deoxynivalenol and zearalenone are also detected as, for example, their glycosides. These so-called modified mycotoxins have been poorly investigated so far, but will need to be considered in future toxicological evaluations.
(Heavy) Metals Elements of particular concern in relation to harmful effects on human health are mercury (Hg), lead (Pb), cadmium (Cd), arsenic (As), and selenium (Se). All of these elements are important to consider in terms of plant-associated food chain contamination. Soils enriched in these elements usually occur as a result of the agricultural, industrial, or urban activities of man. In particular, the proximity of mining and industry to agricultural areas poses serious threats to food safety. The tendency of plants to take up and translocate these contaminants to edible and harvested parts depends largely on soil and climatic factors, and plant genotype. Cd inputs to soil in fertilizer, sewage sludge, soil amendments, and atmospheric deposition often exceed outputs in crops and drainage waters. Consequently, in many agricultural soils, Cd concentrations are slowly increasing. Cd intake through food is a chronic intoxication process by small doses. As for many toxic elements, uptake and accumulation are low. However, Cd excretion is even slower leading to a half-life period in humans of about 17–38 years. Mines, smelters, power plants, and other industries are sources of metal emissions. If these areas are used for crop production at the same time, high amounts of Cd that may exceed safe concentrations in foods (legal limits of 0.1 mg kg1 have been set in some countries) are detectable in tubers. Tubers are most susceptible to Cd accumulation. Potatoes grown on artificially contaminated soil (between 3 and 100 mg kg1) resulted in Cd concentrations of up to 1.0 mg kg1 in the tubers. Cd contamination can occur in rice when paddy fields are irrigated with water sources containing high Cd concentrations. Concentrations of up to 1 mg kg1 have been reported in brown rice. In rice plants, manganese and iron transporters are involved in the uptake and translocation of Cd, and rice cultivars differ significantly in terms of Cd uptake and tolerance, which may be explained by differences in the expression these transporters between cultivars. Moreover, iron deficiency enhances the uptake of Cd. Beside tubers and rice, cocoa plants and beans can be contaminated with Cd. Cd concentrations of >1 mg kg1 were detected in South American cocoa beans. The Cd concentrations in beans does not appear to be related
to high concentrations of available Cd in the soil. High Cd concentrations in beans appears to be correlated with Zn deficiency of the plants. Various other crops, for example, leafy vegetables also contribute to dietary Cd intakes, but to a lower extent. In all cases, the pH and composition of the soil as well as varietal differences are important factors that controls uptake, with low pH favoring Cd accumulation. As has the potential to enter crop plants and affects plant growth. There are two general types of As compounds in water, food, air, and soil: organic and inorganic. The inorganic forms of As are the forms that have been more closely associated with long-term effects on human health. Inorganic As is significantly more toxic than the organic As compounds, such as arsenosugars and arsenobetaine; however, metabolic interconversion occurs. Particularly, in rice-based infant food the levels of inorganic As found in the range of 0.1 mg kg1 are critical as children may consume high amounts of such foodstuff. For other plants, As contamination does not pose a major risk. At As levels that would affect the health of human adults (i.e., >2 mg kg1), the phytotoxicity of As leads to plant death before it enters the food chain. In potato peel, elevated As concentrations can be detected when grown in areas of high soil As levels, but the potato flesh is less affected. For ‘below ground produce,’ for example, potatoes, the levels of As in the soil often determine the As concentrations found in produce, whereas for ‘above ground produce,’ for example, apples, this is not always the case. Small amounts of Hg and the organic methyl-Hg are taken up by plants from the soil, with a greater proportion of methyl-Hg being translocated into above ground plant parts. However, the extent of uptake is low, and therefore Hg from plant sources poses little concern with respect to food chain contamination. Elevated concentrations of Se in soils occur naturally and mostly originate from sedimentary rocks. Although Se is probably not essential for the plant, it is taken up and distributed within the plant due to its chemical similarity to sulfur. Plant Se concentrations are generally low and often poorly correlated with total soil Se levels, due to the complex chemistry of Se in soils. The probability of insufficient Se in the human diet exceeds that of Se toxicity, with Se deficiency in humans usually being associated with vegetarian diets in areas with Se-deficient soils. Gadolinium (Gd) is a rare earth element frequently used as contrast agent in magnetic resonance imaging in medical centers. For medical purposes, preparations are used that contain a complex of Gd with different stabilizing ligands. These complexes are persistent and are not entirely removed in sewage plants. Gd-based magnetic resonance imaging contrast media are taken up by plants and transported from the roots to the leaves where the highest Gd concentrations are observed. These chelated Gd forms are considered safe, but nephrotoxic effects have been described for free ionic Gd. To date, the fate of chelated Gd in plants (and other environmental compartments) is not fully elucidated, and it remains uncertain whether there is a health risk due to Gd in plantbased food. In most cases the contamination of plants with heavy metals is low, and generally does not pose a threat to human health. However, local hotspots exist in areas of mining and
Weeds and Competition j Contaminants in Crop Plants ore processing. Moreover, the increasing use of rare earth elements, such as Gd, could lead to food safety issues in the future.
Bacterial Contamination Living (pathogenic) bacteria, or their endo- and exotoxins, are detectable in and on crop plants. Usually these pathogens are present due to the use of polluted irrigation water. In addition, the direct contact of vegetables with animal excrements or liquid manure transfers fecal microorganisms to the plant. Some of the microorganisms enter plant tissues while a substantial quantity remains on the leaf surface where they may persist for up to several weeks. Further, bacteria may migrate within plant tissues. The extent of this migration is still a matter of debate. Incursions of bacteria into roots and movement to other plant parts seem possible. However, substantial contamination of produce is not likely to occur when manure is applied before planting. Common bacterial pathogens on fresh fruits and vegetables are Salmonella spp., Shigella spp., Listeria monocytogenes, and Escherichia coli and common nonbacterial pathogens include gastrointestinal viruses and the parasite Entamoeba histolytica. Coliforms are common but not necessarily pathogenic contaminants and may be present in large numbers. Their presence does not usually indicate fecal contamination but may originate from handling and processing. Escherichia coli is a relatively rare contaminant of blanched vegetables, and its presence may indicate fecal contamination. Most of the reported outbreaks of gastrointestinal disease linked to fresh produce have been associated with bacterial contamination, particularly with members of the Enterobacteriaceae family (e.g., members of the genera Klebsiella, Enterobacter, Serratia, or Citrobacter). While fruits are generally too acidic for growth of most food-borne pathogens, including Salmonella spp. and Shigella spp., some microorganisms can survive at low pH, such as L. monocytogenes on both chopped and whole tomatoes. Although contamination with E. coli strains is rare, it can have particularly severe consequences because some E. coli (i.e., enterohemorrhagic E. coli (EHEC)) produce the so-called Shiga-like-toxins or verotoxins that are strong cytotoxins that may lead to diarrhea and, in severe cases, to life-threatening diseases like hemolytic uremic syndrome in humans. An increasing number of outbreaks of food poisoning are associated with the consumption of leafy vegetables in which contamination may be due to contact with feces from domestic or wild animals at some stage during cultivation or handling. The strain EHEC O104:H4 was responsible for a large outbreak of food poisoning in 2011 leading to several fatal cases in Europe. Since many bacteria, as well as their respective toxins, are not heat resistant, plants that are consumed raw bear the most threat to the consumer. In the case of verotoxins, however, it was found that conventional pasteurizations did not lead to inactivation of the toxic peptide. However, the detection of some determinants on vegetables grown only in freshly manured soil validates the advice of mandating offset times between manuring and harvesting vegetables for human consumption along with careful postharvest treatment.
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Pharmaceuticals The worldwide annual use of pharmaceuticals in human and veterinary medicine is steadily increasing, and every year many new substances are released for medical purposes. The combination of an increase in the dosage of pharmaceutical substances, a frequent application rate, and normal excretion rates of over 70% may result in the contamination of wastewater, biosolids, manure, surface water, and sediments with active pharmaceutical substances. When these agents are used as fertilizers or irrigation water, the exposure of crops to pharmaceutical substances is increased. Although the activity of these pharmaceuticals might be reduced by various environmental processes, it has been reported that some pharmaceutical substances can be stable over long periods of time in the soil system (e.g., ciprofloxacin or carbamazepine). Moreover, studies have observed that soil bacteria can also produce various kinds of antibiotic substances, resulting in the contamination of soil and plants with naturally produced antibiotics. Some naturally occurring antibiotics found in plants have been banned from application in agriculture (e.g., chloramphenicol). The uptake of different pharmaceutical substances by the roots of crops has been studied in various experimental systems, including hydroponic cultures, soil-pot experiments, or field trials. The amounts taken up seem to be dependent on the system, the plant studied, the concentration, and the chemical characteristics of the substance and environmental factors such as soil composition. It has been observed that the uptake and translocation of substances such as tetracycline occurs by apoplastic transport, and an accumulation has been observed in intercellular spaces. Once accumulated in plant tissue, even low concentrations of pharmaceutical compounds can interfere with plant secondary metabolism. At greater concentrations, they may also cause oxidative stress or have other negative effects on plant growth and photosynthesis. Some evidence suggests that these effects are a consequence of altered plant– microorganism symbioses. However, several pharmaceuticals have been detected in crop plants at concentrations up to mg per g dry weight. In many cases, the concentrations of these substances in the stem and leaves are reported to be much lower than those detected in the roots. The latter gives bioaccumulation factors (BCF) greater than one. For stem and leaves the BCFs are usually below one, although exceptions have been reported. For example, the uptake of carbamazepine into cucumber plants resulted in higher concentrations of carbamazepine in older leaves than in roots, suggesting that the substance might be translocated with the mass flow of water and accumulated in the leaves. Even though bioaccumulation factors for phloem-fed tissues, such as in cereal grains, seem to be small, veterinary pharmaceuticals have been detected in cereals grown in areas of intense livestock farming. Several studies indicate that some plants, such as maize, are able to detoxify pharmaceuticals via the glutathione pathway, whereas others, such as pinto beans, are not able to detoxify them. In addition, detoxification metabolites of pharmaceuticals catalyzed by cytochrome P-450 enzymes have been detected in plants. Hydroxylation of the pharmaceutical substance followed by conjugation to glucose or glucopyranose has been described as the main metabolic process. The metabolites detected so far seem to have differing chemical and physical
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Weeds and Competition j Contaminants in Crop Plants
characteristics. However, glycosylation can be easily reversed by soil microorganisms or during gastrointestinal passage. In addition to pharmaceuticals, personal care products such as shampoo and shower gel or laundry detergents contain a multitude of substances that have the potential to persist in the environment and may end up in crop plants. Several of these substances possess bioactivity, being, for example, endocrine disruptors or antimicrobial agents. Triclocarban and triclosan are two examples of antibacterial preservatives in personal care products that have been shown to be taken up by plants. Their potential for causing antibacterial resistance in the environment is still a matter of discussion.
Persistent Organic Pollutants Many persistent, man-made, organic substances are distributed globally through air and water reaching every spot on Earth. While the ‘traditional’ contaminants (e.g., dioxins or polychlorinated biphenyl (PCBs)) are increasingly controlled and reduced in the environment, new substances are taking their place. Among these emerging persistent organic pollutants (POPs), brominated flame retardants or perfluorinated detergents (e.g., perfluorinated alkyl acids (PFAA)), are of major concern due to their abundance and increasing use, for example, in plastics and textile applications. Additionally, there are persistent pollutants that are not produced intentionally. These POPs may also enter the food web via plant-based food. Polycyclic aromatic hydrocarbons (PAHs) formed during incomplete combustion or pyrolysis of organic materials are of concern for human health due to their widespread occurrence, persistence in terrestrial ecosystems, and carcinogenic properties. The main uptake pathway for PAH entry to the plant is from the air to the leaf surface, where the substances persist and cannot be removed easily by washing or cooking. Movement of these substances from soil to root to leaf has been shown in soils highly contaminated by PAHs, but no PAHs were found in fruits and in storage organs. Soil and agronomic factors also influence the uptake of the PAH phenanthrene by roots, which is increased by the application of ammonium fertilizer, but reduced by the application of nitrate fertilizer. Uptake of phenanthrene by wheat roots is primarily driven by diffusion or mass flow, and to a lesser extent by a transporter-mediated mechanism. PCBs are also translocated from roots to shoots, and their presence in xylem sap was confirmed in Cucurbita species, with greater amounts of lower chlorinated congeners being found in xylem sap than higher chlorinated congeners. Polybrominated diphenyl ethers (PBDEs) are flame retardants which are increasingly used in electronic goods, polyurethane foam, plastics, and textiles. Mean values for the sum of eight important PBDE congeners measured in rice and wheat from Pakistan were 0.70 mg kg1 and 4.50 mg kg1 dry weight, respectively. Wheat roots can take up PBDEs, and the amount taken up is related to soil total organic carbon. However, atmospheric deposition accounts for most of PBDEs found in wheat grain, except when plants are grown in soils with an extremely high PBDE contamination. Another important flame retardant, hexabromocyclododecane (HBCD), can also be accumulated by plants and has been reported to be present in reed (Phragmites sp.) growing
in proximity to chemical production sites. The distribution of HBCDs in plant is diastereomer specific, as observed in cabbage or radish. Perfluorinated detergents, such as perfluorooctane sulfonate (PFOS), perfluorooctanoate (PFOA) and related compounds, possess different toxicological properties and persistence in the environment. PFOS is persistent, accumulated by biota, and toxic to mammalian species according to an OECD statement, and its use is restricted in many countries. However, many replacement products are also suspected to cause environmental problems and health issues. PFOA is detectable in higher amounts than PFOS in vegetables such as carrots, potatoes, and cucumbers. PFOA with alkyl chains with less than 11 carbon atoms can be taken up by roots of plants growing in hydroponic systems and are translocated to leaves in large amounts.
Conclusion Contamination of crop plants is both a current and future issue, as the occurrence of nonanthropogenic and anthropogenic contaminants is practically inevitable in staple crops, fruits, and vegetables. For anthropogenic substances, there exists a dynamic landscape of new agents, toxicological evaluation, and regulatory consequences, which leads to the replacement of banned substances with others that might create similar problems. Because contaminants, unlike residues, are not used intentionally, their consequences for crop production and quality cannot always be foreseen. However, by applying careful and responsible agricultural practices the likelihood of severe contamination can be reduced significantly. This principle should be maintained, despite the necessity for greater food production to feed a growing global population.
See also: Biotechnology: Pharmaceuticals, Plant Drugs. Crop Diseases and Pests: Fungal and Oomycete Diseases. Plant Nutrition: Mineral Uptake; Nutritional Quality of Plants for Food and Fodder.
Further Reading Abadias, M., Usall, J., Anguera, M., Solsona, C., Viñas, I., 2008. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int. J. Food Microbiol. 123, 121–129. Carvalho, P.N., Basto, M.C., Almeida, C.M., Brix, H., 2014. A review of plant–pharmaceutical interactions: from uptake and effects in crop plants to phytoremediation in constructed wetlands. Environ. Sci. Pollut. Res. 21, 11729–11763. Clemens, S., Aarts, M.G.M., Thomine, S., Verbruggen, N., 2013. Plant science: the key to preventing slow cadmium poisoning. Trends in Plant Sci. 18, 92–99. Collins, C., Fryer, M., Grosso, A., 2006. Plant uptake of non-ionic organic chemicals. Environ. Sci. Technol. 40, 45–52. Marti, R., Scott, A., Tien, Y.-C., et al., 2013. Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl. Environ. Microbiol. 79, 5701–5709. McLaughlin, M.J., Parker, D.R., Clarke, J.M., 1999. Metals and micronutrients – food safety issues. Field Crops Res. 60, 143–163. Streit, E., Schwab, C., Sulyok, M., Naehrer, K., Krska, R., Schatzmayr, G., 2013. Multi-mycotoxin screening reveals the occurrence of 139 different secondary metabolites in feed and feed ingredients. Toxins 5, 504–523.
Contents Contaminants in Crop Plants Gene Flow and Herbicide Resistance Herbicide Application Technology Herbicide Resistance and Molecular Aspects Integrated Weed Management Thermal Weed Control Weed Biology Weed Competition Weed Control in Orchards and Vineyards Weed Seed Biology
Contaminants in Crop Plants R Maul, Leibniz Institute of Vegetable and Ornamental Crops Großbeeren/Erfurt e.V., Großbeeren, Germany C Schwake-Anduschus, MRI Max Rubner-Institut, Detmold, Germany M Wiesner, Leibniz Institute of Vegetable and Ornamental Crops Großbeeren/Erfurt e.V., Großbeeren, Germany Ó 2017 Elsevier Ltd. All rights reserved.
Abbreviations BCF Bioaccumulation factor HBCD Hexabromocyclododecane PAH Polycyclic aromatic hydrocarbon PBDE Polybrominated diphenyl ether PCB Polychlorinated biphenyl
Introduction Contamination of crop plants can be defined in a manner similar to that of food contamination, as the unintended presence of toxic substances, pathogens, or pharmaceuticals in crop plants. A contaminant is distinguished from a residue, which may also be a harmful compound present on crops. A residue is a substance that is added deliberately to the crop, and whose incomplete removal turns this agent into a residue. The presence of genetically modified material in nongenetically modified crops or seeds can also be defined as a contaminant. However, genetic contamination is beyond the scope of this article. The most important contaminants in crop plants are divided according to their origin into natural and anthropogenic. While mycotoxins, microorganisms, and toxic elements have always been present in the environment, and therefore also in human
442
PFAA Perfluorinated alkyl acid PFOA Perfluorooctanoate PFOS Perfluorooctane sulfonate POP Persistent organic pollutant
diets, biologically active or persistent organic pollutants or pharmaceuticals are predominantly man-made. By direct use of the crops in foodstuffs or as a consequence of carry-over effects from contaminated feed to animal foodstuffs, these contaminants enter the human food chain (Figure 1). Modern horticulture and agriculture can affect the occurrence of nonanthropogenic contaminants in diets, for example, by mobilization of mineral elements and organic compounds in the soil. In times of global water shortage and the necessity to enhance crop production by means of irrigation, sewage and industrial wastewater can become important water resources for crop production. Contaminated irrigation water bears the risk of spreading undesirable substances to agricultural fields, thereby allowing their accumulation by crop plants. Consequently, the contamination of vegetables with fecal microorganisms or pharmaceutical substances will be an important issue in the future.
Encyclopedia of Applied Plant Sciences, 2nd edition, Volume 3
http://dx.doi.org/10.1016/B978-0-12-394807-6.00247-1
Weeds and Competition j Contaminants in Crop Plants
Fungal infestation Pathogenic bacteria (sewage)
443
Pharmaceuticals / bioactive compound from personal care products
Fruits/ vegetables for human consumption (Persistent / halogenated) organic pollutants
(Heavy) metals
Feeding of livestock animals
Diary products/ meat for human consumption
Anthropogenic and natural sources of contaminants leading to contaminaƟon of food and fodder
Figure 1 Flowchart depicting the external influences that may lead to contamination of a crop plant with various substances and the potential routes of exposure to the contaminants for the human consumer.
In the following sections, five main sources of contamination relevant for crop plants will be introduced and discussed on the basis of examples.
Mycotoxins The risk of mycotoxin contamination of food and feed is as old as the history of mankind itself. Mold and mycotoxin contamination can occur at any stage in the food production chain: during cultivation, between harvesting and drying, and during storage. The Food and Agriculture Organization of the United Nations (FAO) estimates that 25% of the world’s agricultural commodities are contaminated with mycotoxins to some extent. Fungi of the genera Aspergillus, Penicillium, Fusarium, Alternaria, and Claviceps are the predominant mycotoxin producers with aflatoxins, ochratoxins, fumonisins, patulin, deoxynivalenol, and their derivatives, as well as zearalenone and its derivatives being the economically and toxicologically most important mycotoxins. However, numerous other potentially toxic fungal secondary metabolites have been detected, leading to a long list of the so-called emerging mycotoxins (e.g., fusaproliferin, beauvericin, enniatins, and moniliformin formed by Fusarium spp. or various ergot alkaloids formed by Claviceps purpurea). Several hundreds of fungal metabolites have been detected in food, feed, and its raw materials. While Aspergillus and Fusarium spp. are the predominant causes for the infestation of grains and nuts, Alternaria and Rhizopus spp. are more important for vegetables and fruits. Although certain Rhizopus spp. are mainly responsible for postharvest decay, or storage rot, of, for example, strawberry, tomato, and Brassicaceae, they do not produce any significant amounts of toxins, while alternaria toxins (alternariol, alternariol
monomethyl ether, altenuene, altertoxin I-III, tentoxin, tenuazonic acid) have been found in fruits, vegetables, oilseeds, and cereals visibly infected by Alternaria spp. Contamination of food and feed by aflatoxins produced by Aspergillus spp. poses enormous economic and health concerns because these substances are highly carcinogenic. The presence of these toxins in food correlates positively with the high incidence of liver cancer in various developing countries. The severity of a fungal infection, as well as the extent of toxin production, is dependent on various parameters. The climatic conditions are crucial for fungal growth, with humid and warm climates favoring their growth. However, particular toxigenic strains (e.g., Fusarium spp.) also can adapt to colder and drier environments. Furthermore, agronomic practices have an impact on the extent of fungal infestation and mycotoxin occurrence. Many, although not all, studies have reported a higher probability of fungal growth on crop plants under organic farming conditions. For coffee beans, a larger number of filamentous fungi could be observed under organic farming conditions. In Italian maize and Polish oats, fungal infection, and the number of mycotoxin-positive samples, differed significantly between farming systems, with a greater incidence in organic farming. By contrast, a more frequent crop rotation with noncereals was found to reduce mycotoxin concentrations and Fusarium infestations. When mineral fertilizers and herbicides were used, infestation of grains by Fusarium graminearum was reduced. The frequent occurrence, and the severe health concerns associated with some mycotoxins, has led to legislative consequences for consumer protection in almost all countries. Aflatoxin concentrations are regulated in more than 50 countries worldwide, with an upper limit between 2 and 30 mg kg1
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Weeds and Competition j Contaminants in Crop Plants
toxin in grains and nuts. For deoxynivalenol, which is a frequently occurring mycotoxin, the EU, China, Russia, Japan, and Canada have established legal limits of between 200 and 2000 mg kg1, while the USA has provided an advisory limit for selected commodities (e.g., 1000 mg kg1 on finished wheat products). The FAO together with the World Health Organization adopted a code of practice to prevent and reduce fungal infestation in cereals and occurrence of mycotoxins in the crop. The recommendations include measures related to good agricultural manufacturing practices for zearalenone, trichothecenes, ochratoxin A, fumonisines, and aflatoxins. Since the infested plants recognize the mycotoxins as xenobiotics, these toxins are subjected to metabolic changes in the plant. Thus, in infested plant tissue, mycotoxins such as deoxynivalenol and zearalenone are also detected as, for example, their glycosides. These so-called modified mycotoxins have been poorly investigated so far, but will need to be considered in future toxicological evaluations.
(Heavy) Metals Elements of particular concern in relation to harmful effects on human health are mercury (Hg), lead (Pb), cadmium (Cd), arsenic (As), and selenium (Se). All of these elements are important to consider in terms of plant-associated food chain contamination. Soils enriched in these elements usually occur as a result of the agricultural, industrial, or urban activities of man. In particular, the proximity of mining and industry to agricultural areas poses serious threats to food safety. The tendency of plants to take up and translocate these contaminants to edible and harvested parts depends largely on soil and climatic factors, and plant genotype. Cd inputs to soil in fertilizer, sewage sludge, soil amendments, and atmospheric deposition often exceed outputs in crops and drainage waters. Consequently, in many agricultural soils, Cd concentrations are slowly increasing. Cd intake through food is a chronic intoxication process by small doses. As for many toxic elements, uptake and accumulation are low. However, Cd excretion is even slower leading to a half-life period in humans of about 17–38 years. Mines, smelters, power plants, and other industries are sources of metal emissions. If these areas are used for crop production at the same time, high amounts of Cd that may exceed safe concentrations in foods (legal limits of 0.1 mg kg1 have been set in some countries) are detectable in tubers. Tubers are most susceptible to Cd accumulation. Potatoes grown on artificially contaminated soil (between 3 and 100 mg kg1) resulted in Cd concentrations of up to 1.0 mg kg1 in the tubers. Cd contamination can occur in rice when paddy fields are irrigated with water sources containing high Cd concentrations. Concentrations of up to 1 mg kg1 have been reported in brown rice. In rice plants, manganese and iron transporters are involved in the uptake and translocation of Cd, and rice cultivars differ significantly in terms of Cd uptake and tolerance, which may be explained by differences in the expression these transporters between cultivars. Moreover, iron deficiency enhances the uptake of Cd. Beside tubers and rice, cocoa plants and beans can be contaminated with Cd. Cd concentrations of >1 mg kg1 were detected in South American cocoa beans. The Cd concentrations in beans does not appear to be related
to high concentrations of available Cd in the soil. High Cd concentrations in beans appears to be correlated with Zn deficiency of the plants. Various other crops, for example, leafy vegetables also contribute to dietary Cd intakes, but to a lower extent. In all cases, the pH and composition of the soil as well as varietal differences are important factors that controls uptake, with low pH favoring Cd accumulation. As has the potential to enter crop plants and affects plant growth. There are two general types of As compounds in water, food, air, and soil: organic and inorganic. The inorganic forms of As are the forms that have been more closely associated with long-term effects on human health. Inorganic As is significantly more toxic than the organic As compounds, such as arsenosugars and arsenobetaine; however, metabolic interconversion occurs. Particularly, in rice-based infant food the levels of inorganic As found in the range of 0.1 mg kg1 are critical as children may consume high amounts of such foodstuff. For other plants, As contamination does not pose a major risk. At As levels that would affect the health of human adults (i.e., >2 mg kg1), the phytotoxicity of As leads to plant death before it enters the food chain. In potato peel, elevated As concentrations can be detected when grown in areas of high soil As levels, but the potato flesh is less affected. For ‘below ground produce,’ for example, potatoes, the levels of As in the soil often determine the As concentrations found in produce, whereas for ‘above ground produce,’ for example, apples, this is not always the case. Small amounts of Hg and the organic methyl-Hg are taken up by plants from the soil, with a greater proportion of methyl-Hg being translocated into above ground plant parts. However, the extent of uptake is low, and therefore Hg from plant sources poses little concern with respect to food chain contamination. Elevated concentrations of Se in soils occur naturally and mostly originate from sedimentary rocks. Although Se is probably not essential for the plant, it is taken up and distributed within the plant due to its chemical similarity to sulfur. Plant Se concentrations are generally low and often poorly correlated with total soil Se levels, due to the complex chemistry of Se in soils. The probability of insufficient Se in the human diet exceeds that of Se toxicity, with Se deficiency in humans usually being associated with vegetarian diets in areas with Se-deficient soils. Gadolinium (Gd) is a rare earth element frequently used as contrast agent in magnetic resonance imaging in medical centers. For medical purposes, preparations are used that contain a complex of Gd with different stabilizing ligands. These complexes are persistent and are not entirely removed in sewage plants. Gd-based magnetic resonance imaging contrast media are taken up by plants and transported from the roots to the leaves where the highest Gd concentrations are observed. These chelated Gd forms are considered safe, but nephrotoxic effects have been described for free ionic Gd. To date, the fate of chelated Gd in plants (and other environmental compartments) is not fully elucidated, and it remains uncertain whether there is a health risk due to Gd in plantbased food. In most cases the contamination of plants with heavy metals is low, and generally does not pose a threat to human health. However, local hotspots exist in areas of mining and
Weeds and Competition j Contaminants in Crop Plants ore processing. Moreover, the increasing use of rare earth elements, such as Gd, could lead to food safety issues in the future.
Bacterial Contamination Living (pathogenic) bacteria, or their endo- and exotoxins, are detectable in and on crop plants. Usually these pathogens are present due to the use of polluted irrigation water. In addition, the direct contact of vegetables with animal excrements or liquid manure transfers fecal microorganisms to the plant. Some of the microorganisms enter plant tissues while a substantial quantity remains on the leaf surface where they may persist for up to several weeks. Further, bacteria may migrate within plant tissues. The extent of this migration is still a matter of debate. Incursions of bacteria into roots and movement to other plant parts seem possible. However, substantial contamination of produce is not likely to occur when manure is applied before planting. Common bacterial pathogens on fresh fruits and vegetables are Salmonella spp., Shigella spp., Listeria monocytogenes, and Escherichia coli and common nonbacterial pathogens include gastrointestinal viruses and the parasite Entamoeba histolytica. Coliforms are common but not necessarily pathogenic contaminants and may be present in large numbers. Their presence does not usually indicate fecal contamination but may originate from handling and processing. Escherichia coli is a relatively rare contaminant of blanched vegetables, and its presence may indicate fecal contamination. Most of the reported outbreaks of gastrointestinal disease linked to fresh produce have been associated with bacterial contamination, particularly with members of the Enterobacteriaceae family (e.g., members of the genera Klebsiella, Enterobacter, Serratia, or Citrobacter). While fruits are generally too acidic for growth of most food-borne pathogens, including Salmonella spp. and Shigella spp., some microorganisms can survive at low pH, such as L. monocytogenes on both chopped and whole tomatoes. Although contamination with E. coli strains is rare, it can have particularly severe consequences because some E. coli (i.e., enterohemorrhagic E. coli (EHEC)) produce the so-called Shiga-like-toxins or verotoxins that are strong cytotoxins that may lead to diarrhea and, in severe cases, to life-threatening diseases like hemolytic uremic syndrome in humans. An increasing number of outbreaks of food poisoning are associated with the consumption of leafy vegetables in which contamination may be due to contact with feces from domestic or wild animals at some stage during cultivation or handling. The strain EHEC O104:H4 was responsible for a large outbreak of food poisoning in 2011 leading to several fatal cases in Europe. Since many bacteria, as well as their respective toxins, are not heat resistant, plants that are consumed raw bear the most threat to the consumer. In the case of verotoxins, however, it was found that conventional pasteurizations did not lead to inactivation of the toxic peptide. However, the detection of some determinants on vegetables grown only in freshly manured soil validates the advice of mandating offset times between manuring and harvesting vegetables for human consumption along with careful postharvest treatment.
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Pharmaceuticals The worldwide annual use of pharmaceuticals in human and veterinary medicine is steadily increasing, and every year many new substances are released for medical purposes. The combination of an increase in the dosage of pharmaceutical substances, a frequent application rate, and normal excretion rates of over 70% may result in the contamination of wastewater, biosolids, manure, surface water, and sediments with active pharmaceutical substances. When these agents are used as fertilizers or irrigation water, the exposure of crops to pharmaceutical substances is increased. Although the activity of these pharmaceuticals might be reduced by various environmental processes, it has been reported that some pharmaceutical substances can be stable over long periods of time in the soil system (e.g., ciprofloxacin or carbamazepine). Moreover, studies have observed that soil bacteria can also produce various kinds of antibiotic substances, resulting in the contamination of soil and plants with naturally produced antibiotics. Some naturally occurring antibiotics found in plants have been banned from application in agriculture (e.g., chloramphenicol). The uptake of different pharmaceutical substances by the roots of crops has been studied in various experimental systems, including hydroponic cultures, soil-pot experiments, or field trials. The amounts taken up seem to be dependent on the system, the plant studied, the concentration, and the chemical characteristics of the substance and environmental factors such as soil composition. It has been observed that the uptake and translocation of substances such as tetracycline occurs by apoplastic transport, and an accumulation has been observed in intercellular spaces. Once accumulated in plant tissue, even low concentrations of pharmaceutical compounds can interfere with plant secondary metabolism. At greater concentrations, they may also cause oxidative stress or have other negative effects on plant growth and photosynthesis. Some evidence suggests that these effects are a consequence of altered plant– microorganism symbioses. However, several pharmaceuticals have been detected in crop plants at concentrations up to mg per g dry weight. In many cases, the concentrations of these substances in the stem and leaves are reported to be much lower than those detected in the roots. The latter gives bioaccumulation factors (BCF) greater than one. For stem and leaves the BCFs are usually below one, although exceptions have been reported. For example, the uptake of carbamazepine into cucumber plants resulted in higher concentrations of carbamazepine in older leaves than in roots, suggesting that the substance might be translocated with the mass flow of water and accumulated in the leaves. Even though bioaccumulation factors for phloem-fed tissues, such as in cereal grains, seem to be small, veterinary pharmaceuticals have been detected in cereals grown in areas of intense livestock farming. Several studies indicate that some plants, such as maize, are able to detoxify pharmaceuticals via the glutathione pathway, whereas others, such as pinto beans, are not able to detoxify them. In addition, detoxification metabolites of pharmaceuticals catalyzed by cytochrome P-450 enzymes have been detected in plants. Hydroxylation of the pharmaceutical substance followed by conjugation to glucose or glucopyranose has been described as the main metabolic process. The metabolites detected so far seem to have differing chemical and physical
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characteristics. However, glycosylation can be easily reversed by soil microorganisms or during gastrointestinal passage. In addition to pharmaceuticals, personal care products such as shampoo and shower gel or laundry detergents contain a multitude of substances that have the potential to persist in the environment and may end up in crop plants. Several of these substances possess bioactivity, being, for example, endocrine disruptors or antimicrobial agents. Triclocarban and triclosan are two examples of antibacterial preservatives in personal care products that have been shown to be taken up by plants. Their potential for causing antibacterial resistance in the environment is still a matter of discussion.
Persistent Organic Pollutants Many persistent, man-made, organic substances are distributed globally through air and water reaching every spot on Earth. While the ‘traditional’ contaminants (e.g., dioxins or polychlorinated biphenyl (PCBs)) are increasingly controlled and reduced in the environment, new substances are taking their place. Among these emerging persistent organic pollutants (POPs), brominated flame retardants or perfluorinated detergents (e.g., perfluorinated alkyl acids (PFAA)), are of major concern due to their abundance and increasing use, for example, in plastics and textile applications. Additionally, there are persistent pollutants that are not produced intentionally. These POPs may also enter the food web via plant-based food. Polycyclic aromatic hydrocarbons (PAHs) formed during incomplete combustion or pyrolysis of organic materials are of concern for human health due to their widespread occurrence, persistence in terrestrial ecosystems, and carcinogenic properties. The main uptake pathway for PAH entry to the plant is from the air to the leaf surface, where the substances persist and cannot be removed easily by washing or cooking. Movement of these substances from soil to root to leaf has been shown in soils highly contaminated by PAHs, but no PAHs were found in fruits and in storage organs. Soil and agronomic factors also influence the uptake of the PAH phenanthrene by roots, which is increased by the application of ammonium fertilizer, but reduced by the application of nitrate fertilizer. Uptake of phenanthrene by wheat roots is primarily driven by diffusion or mass flow, and to a lesser extent by a transporter-mediated mechanism. PCBs are also translocated from roots to shoots, and their presence in xylem sap was confirmed in Cucurbita species, with greater amounts of lower chlorinated congeners being found in xylem sap than higher chlorinated congeners. Polybrominated diphenyl ethers (PBDEs) are flame retardants which are increasingly used in electronic goods, polyurethane foam, plastics, and textiles. Mean values for the sum of eight important PBDE congeners measured in rice and wheat from Pakistan were 0.70 mg kg1 and 4.50 mg kg1 dry weight, respectively. Wheat roots can take up PBDEs, and the amount taken up is related to soil total organic carbon. However, atmospheric deposition accounts for most of PBDEs found in wheat grain, except when plants are grown in soils with an extremely high PBDE contamination. Another important flame retardant, hexabromocyclododecane (HBCD), can also be accumulated by plants and has been reported to be present in reed (Phragmites sp.) growing
in proximity to chemical production sites. The distribution of HBCDs in plant is diastereomer specific, as observed in cabbage or radish. Perfluorinated detergents, such as perfluorooctane sulfonate (PFOS), perfluorooctanoate (PFOA) and related compounds, possess different toxicological properties and persistence in the environment. PFOS is persistent, accumulated by biota, and toxic to mammalian species according to an OECD statement, and its use is restricted in many countries. However, many replacement products are also suspected to cause environmental problems and health issues. PFOA is detectable in higher amounts than PFOS in vegetables such as carrots, potatoes, and cucumbers. PFOA with alkyl chains with less than 11 carbon atoms can be taken up by roots of plants growing in hydroponic systems and are translocated to leaves in large amounts.
Conclusion Contamination of crop plants is both a current and future issue, as the occurrence of nonanthropogenic and anthropogenic contaminants is practically inevitable in staple crops, fruits, and vegetables. For anthropogenic substances, there exists a dynamic landscape of new agents, toxicological evaluation, and regulatory consequences, which leads to the replacement of banned substances with others that might create similar problems. Because contaminants, unlike residues, are not used intentionally, their consequences for crop production and quality cannot always be foreseen. However, by applying careful and responsible agricultural practices the likelihood of severe contamination can be reduced significantly. This principle should be maintained, despite the necessity for greater food production to feed a growing global population.
See also: Biotechnology: Pharmaceuticals, Plant Drugs. Crop Diseases and Pests: Fungal and Oomycete Diseases. Plant Nutrition: Mineral Uptake; Nutritional Quality of Plants for Food and Fodder.
Further Reading Abadias, M., Usall, J., Anguera, M., Solsona, C., Viñas, I., 2008. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int. J. Food Microbiol. 123, 121–129. Carvalho, P.N., Basto, M.C., Almeida, C.M., Brix, H., 2014. A review of plant–pharmaceutical interactions: from uptake and effects in crop plants to phytoremediation in constructed wetlands. Environ. Sci. Pollut. Res. 21, 11729–11763. Clemens, S., Aarts, M.G.M., Thomine, S., Verbruggen, N., 2013. Plant science: the key to preventing slow cadmium poisoning. Trends in Plant Sci. 18, 92–99. Collins, C., Fryer, M., Grosso, A., 2006. Plant uptake of non-ionic organic chemicals. Environ. Sci. Technol. 40, 45–52. Marti, R., Scott, A., Tien, Y.-C., et al., 2013. Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl. Environ. Microbiol. 79, 5701–5709. McLaughlin, M.J., Parker, D.R., Clarke, J.M., 1999. Metals and micronutrients – food safety issues. Field Crops Res. 60, 143–163. Streit, E., Schwab, C., Sulyok, M., Naehrer, K., Krska, R., Schatzmayr, G., 2013. Multi-mycotoxin screening reveals the occurrence of 139 different secondary metabolites in feed and feed ingredients. Toxins 5, 504–523.