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Phytoremediation
Phytoremediation N Dickinson, Lincoln University, Christchurch, New Zealand Ó 2017 Elsevier Ltd. All rights reserved. This article is a revision of the previous edition article by M. Pletsch, volume 2, pp. 781–786, Ó 2003, Elsevier Ltd.
Phytoremediation attempts to use plants and microbes associated with plant root systems to harness natural processes to protect the environment and to clean up polluted and degraded land, water, and the atmosphere. Phytoremediation is promoted as an emerging, low-cost, environmentally sound technology for plant-based solutions to pollution. The scientific use of the terminology is more recent than the effective use of the technology; two examples of the established practical application of phytoremediation are wastewater treatment using constructed wetlands and vegetation barriers to restrict leakage of hazardous compounds from waste dumps and landfills. This has particular appeal in its potential to exploit biological processes and uptake mechanisms in plants to remove, degrade, or volatilize pollutants. Plants can be used in place of expensive engineering solutions for contaminated land, avoiding disposal of the soil (dig and dump), installation of protective artificial barriers (clays or HDPE membranes), and coverage with clean soil imported from land excavation elsewhere. A limited number of field studies have demonstrated the effectiveness of phytoremediation to remove pollutants from soil (phytoextraction), but applications of this technology frequently have been exaggerated in the context of heavy metals. In contrast, plant-based solutions have proven to be very effective in nutrient-stripping of former agricultural soils for ecological restoration, stabilizing soil pollutants (phytostabilization), and in enhancing the degradation (phytodegradation, rhizodegradation) and volatilization of a wide range of organic chemicals including oils, pesticides, and explosives. Realistic and practical applications for phytoremediation of degraded and contaminated land are currently referred to as phytotechnologies. The International Phytotechnology Society and its official journal The International Journal of Phytoremediation provide the best representation of the current status of the science and practice of phytoremediation. Phytoremediation of inorganic and organic pollutants is fundamentally different and often presents separate challenges for scientific inquiry and practical actions. This is largely because inorganic chemical compounds as pollutants can change their chemical structure or be transferred from one medium to another, but the component toxic chemical elements, such as heavy metals, cannot be degraded and made to disappear. In contrast, the carbon ring–based structure of organic pollutants associated with toxicity can be degraded effectively through breakdown into less complex and nontoxic chemical forms of carbon, hydrogen, and oxygen. Any residual heavy metal that was a component of the organic compound is usually present in too small an amount to create further problems as an inorganic pollutant.
landscapes, for example, through pioneering applied ecology research led by A.D. Bradshaw in northwest United Kingdom in the 1970s. New insights into many aspects of soil and plant science were provided through studies of degraded land often devoid of organic matter, nutrient deficient, and contaminated by heavy metals from mining wastes and industrial pollution. The extreme physical and chemical status of exposed substrates and pollution-impacted soils were not compatible with the essential processes required to maintain nutrient cycles and to support a sustainable vegetation cover. Furthermore, there was increasing awareness of human health risks from the legacy of wastes, spillages, residues, and fallout from mining, industry, agriculture, and urban pollution. In some cases soil amendments of lime and organic matter helped the initial establishment of plants, but longer-term maintenance of a vegetation cover often proved to be problematic. There are natural differences in the uptake of chemical elements by plants, ranging from preferential uptake to exclusion, and differing both between species of plants and chemical elements. This has a particular application for heavy metals, normally found in low concentrations but frequently highly elevated in polluted environments. Attempts to understand and describe mobility of heavy metals in soils, and their bioavailability to plants and animals, have led to significant scientific advances. Studies on plants in heavy metal–polluted environments provided evidence of adaptation to pollution and possibly the first examples of plant evolution outside the fossil record. This stimulated considerable interest in metal tolerance as a heritable trait in plants and the explanatory physiological and biochemical mechanisms associated with the responses of plants to pollution. More efficient ways to restore vegetation on metalcontaminated soils were becoming better understood, and metal-tolerant plants allowed the greening of areas previously devoid of vegetation. There was some concern, however, that toxic heavy metals might be transferred along food chains and to the wider environment, especially when land was restored to agriculture for crops or livestock. Restoration of contaminated and degraded land to more naturalistic vegetation cover became a more common goal, especially in urban areas and on previously mined and former industrial land. The science and practice of ecological restoration developed more broadly in the 1980s, renewing and restoring degraded, damaged, or destroyed ecosystems and habitats in the environment by active human intervention and action. The Society of Ecological Restoration (SER.org) represents the leading edge of progress in this field, partly through its journal Restoration Ecology.
Origins of Phytoremediation
Inorganic Pollutants: Metal Tolerance and Hyperaccumulation
Modern scientific interest in phytoremediation probably has its origins in the ecological restoration of postindustrial degraded
Inorganic pollutants include macronutrients (nitrate and phosphate), trace elements (metals and metalloids, often referred to
Encyclopedia of Applied Plant Sciences, 2nd edition, Volume 3
http://dx.doi.org/10.1016/B978-0-12-394807-6.00016-2
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as heavy metals), and radioactive isotopes (238U, 137Cs, and 90 Sr). Some plants that naturally evolved on metal-enriched soils, referred to as metallophytes, accumulate exceptionally high concentrations of specific but different chemical elements in their living foliage and stems. This was probably first identified in the mid-nineteenth century by J. Sachs on calamine soils near Aachen, Germany, in species of Thlaspi, Viola, Armeria, and Silene. Their location has been used by mining prospectors in the search for outcrops of metalliferous ores. Scientific interest in the plants notably increased from the 1990s through research variously led by A.J.M. Baker, R.R. Brooks, R.D. Reeves, F. Malaise and J. Proctor, and T. Jaffré on the unique vegetation of ultramafic (serpentine) soils. Occupying less than 1% of the Earth’s surface, ultramafic soils are widely scattered throughout both temperate and tropical regions. The term hyperaccumulator was coined by R.D. Reeves to describe a minority of the plants found growing on these soils that accumulated nickel (Ni) in foliage and stems at concentrations >1000 mg g1 (more than 1%) of dry weight. This is 100–1000 times higher than the amount in nonmetallophyte plants, and 10–100 times higher than normally found in plants on ultramafic soils. A concentration of >1000 mg g1 similarly defines the hyperaccumulator trait for of copper (Cu), cobalt (Co), arsenic (As), and lead (Pb), but different critical concentrations apply to elements where normal concentrations in plants are typically much higher or lower. Thus, hyperaccumulation of manganese (Mn) and zinc (Zn) is defined at plant concentrations >10 000 mg g1 and cadmium (Cd) at >100 mg g1 (Figure 1). Hyperaccumulators have the ability to transfer chemical elements from the soil to above-ground plant tissues when growing within healthy self-sustaining populations in their natural habitat. The most commonly cited hyperaccumulator is a New Caledonian endemic woody plant, Sebertia acuminata (Sapotaceae), that has 11 700 mg Ni g1 (11.7% of dry weight)
recorded in its leaves and 257 400 mg Ni g1 (25.7% of dry weight) in its sap, although the total number of species exhibiting hyperaccumulation traits is now well in excess of 500. It seems likely that these plants could provide the source of planting material for phytoextraction of the same metals from anthropogenically contaminated soils. Subsequent harvesting of the plants would remove metals from the contaminated soil and allow subsequent recovery of the metal from ash following plant combustion (phytomining). Potentially this would also provide an economic return through the market value of the metal (Figure 2).
Inorganic Pollutants: Phytoremediation Significant advances in biomolecular science have allowed identification and transformation of high uptake traits in plants, linking genetic and physiological traits with transport and storage of metals in plants. However, transferring what often may be a multicomponent stress-tolerance physiological trait into a high-yield cropping system has met with less success. Most hyperaccumulators are tropical plants that are unable to grow in cooler climates, and temperate hyperaccumulator plants are almost all herbaceous plants of diminutive stature and low productivity, such as Noccaea caerulescens (Syn. Thlaspi caerulescens) and Arabidopsis halleri (Brassicaceae) which have been used as model plants to study the remarkable phenomenon of hyperaccumulation. In addition to the practical and agronomic challenges, there are significant regulatory restrictions and public-perception issues associated with the release of genetically modified organisms into the environment. Many misleading claims of hyperaccumulation have been published from inadequate sampling in the field or by
Figure 1 Prof. Robert Brooks with Ornella Gambi next to Alyssum bertolonii (Brassicaceae) at Monte Prinzera, Italy, where she discovered this to be the first Ni-hyperaccumulator plant in 1948. More than 500 hyperaccumulator species have been discovered since then.
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productivity advantage would counterbalance a 10-fold lower metal concentration in plant tissues, providing the same final offtake of metals from the soil as a slow-growing hyperaccumulator. Clones of willows and poplars have been suggested as likely candidates. In field trials these plants have been shown to uptake relatively large amounts of Zn and Cd into aboveground woody parts that can be harvested in winter and also used as a bioenergy crop. While this offers some potential in soils in urban and industrial areas where these metals are frequently elevated, a significant proportion of metal uptake into these deciduous plants may be raised to the soil surface from deeper layers following leaf fall, potentially enhancing exposure and risk from the pollutants. Furthermore, unless plants have the characteristics of both hyperaccumulation and high growth rates, the time required to achieve significantly reduced concentrations of heavy metals through plant uptake and harvest invariably would take several decades. Other plants that have been claimed to offer the possibility of phytoextraction of metals include a number of grasses, including vetiver grass (Vetiveria zizanioides) and Miscanthus spp. One apparently unique application for phytoremediation is the proven volatilization of Se in significant amounts by plants and microorganisms that methylate Se to a less toxic volatile form. Selenium is taken up from the soil and emitted to the atmosphere in diluted nonharmful form as a gas. Similar results have been achieved for Hg in transgenic plants (Figure 3).
Figure 2 Botanist Dr Antony van der Ent next to a hyperaccumulator tree Pycnandra acuminata (Sapotaceae) at the Rivière Bleue reserve in New Caledonia. The tree is estimated to contain 6 kg nickel. Photo: AJM Baker.
overdosing plants in unnatural conditions. Toxicologically challenged plants or plant tissues grown in hydroponics, pot experiments, or other artificial conditions do not represent species with constitutional and heritable traits of hyperaccumulation. Many claims of hyperaccumulation of lead, copper, cobalt, chromium, and thallium are almost certainly unfounded. The requirement for a productive plant that can be cultivated as a crop and that also hyperaccumulates metals presents a plethora of problems. Particular attention has been given to N. caerulescens (Pb, Zn, Cd, Ni), Alyssum spp. (Ni, Co), and a fern Pteris vittata (As) which have produced mixed results in small-scale short-term field trials. However, there have been a small number of convincing larger-scale and longer-term field trials that have demonstrated phytoextraction is both agronomically feasible and economically viable. In the United States, selenium (Se) has been harvested and transferred as a fodder crop to selenium-deficient areas. Berkheya coddii (Asteraceae) has been grown on Ni mine wastes in South Africa and extracted as an ore. Removal of significant amounts of metal from soil requires a combination of high harvestable plant tissue concentrations of the metal and high rates of plant growth. An alternative strategy for phytoextraction is to use plants known as accumulators that uptake higher concentrations of metals than most plants but that are also highly productive and can be grown in cropping systems. These plants accumulate metals, rather than hyperaccumulate metals. Logically, a 10-fold
Organic Pollutants Organic pollutants that have been targeted for phytoremediation include petroleum hydrocarbons (e.g., oils, polyaromatic hydrocarbons (PAHs)) and industrial solvents (particularly trichloroethylene (TCE)), pesticides (e.g. atrazine), and explosives (2,4,6-trinitrotoluene (TNT)). Phytodegradation of organic pollutants involves either degradation of the chemicals (phytodegradation) to simpler nontoxic compounds, or sequestration and volatilization. Degradation of contaminants can occur either within plant tissues or may also involve microbial activity in the soil or root zone (rhizosphere). Phytodegradation is effective for organic chemicals that are mobile in plants, such as atrazine and other herbicides. Other pollutants such as TCE and methyl tertiary butyl ether (MTBE) are also volatilized more readily to the atmosphere through processes of plant uptake or in the presence of plant root systems. Petroleum hydrocarbons, PAHs, and polychlorinated biphenyls (PCBs) are degraded by soil microbial activity in the soil, itself enhanced by plant root systems. Rhizosphere processes stimulate microbial activity, for example, through increasing soil aeration and releasing secondary plant compounds as root exudates. Bacteria that include species of Arthrobacter, Pseudomonas, and Bacillus can degrade recalcitrant pollutants such as the PAHs, but they may also solubilize compounds bound within the soil matrix, facilitating uptake by plants. Enzymes, such as dehalogenases, nitroreductases, and laccases, released into the soil from plant sources have been shown to degrade a range of organics including TCE, PCBs, TNT, and various aromatic compounds. A wide range of plants have been used including poplars, willows, maize, rice, and alfalfa. Laboratory studies have demonstrated the potential to use transgenic
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Figure 3 Phytoremediation expert Prof. Alan Baker standing in a field trial (set up by Dr Mei Lei) of an As-hyperaccumulator fern, Pteris vittata, on contaminated agricultural land downwind of a large Pb smelter, Jiguan in Henan Province, China. Photo: A.J.M. Baker.
plants and microbes to remediate organic contaminants, for example, by overexpressing genes that encode enzymes involved in degradation pathways, but this is largely untested in the field. Enhancing phytoremediation efficiency with endophytes (microorganisms that live within plant tissues) has shown, for example, that degradation of benzene, toluene, and TCE is enhanced in poplar by endophytic species of Pseudomonas and Bacillus in ex situ small-scale trials.
Integrated Phytoremediation Strategies The chemical forms of inorganic pollutants such as metals in soil invariably consist of the largest fraction being tightly bound to particles such as clay and organic matter. A much smaller proportion of the total amount of metal in soil is readily soluble in water in the pore spaces between soil particles, but this fraction is more mobile, more readily bioavailable for uptake by plants and animals, but also more easily leached from soil. It is this mobile fraction of metals that presents most toxicological risk. However, metals continually but slowly transfer between the two fractions of the total pool of metals in the soil, for example, when organic matter is added to soil (locking up mobile metals) when organic matter decomposes (releasing metals to the mobile fraction). The flux between these two fractions is also strongly influenced by several other physical, chemical, and biological factors including soil pH, conductivity, aeration, water logging, root exudates, earthworm activity, and mycorrhizae. Adding amendments to soil modifies these factors and alter the mobility and bioavailability of metals, although these actions rarely satisfied regulatory criteria that are usually based on the total concentrations of heavy metals in soil. In experimental studies, a range of chemicals including chelates and organic acids have been used to enhance metal uptake into plants, improving the success of phytoextraction but often also increasing leaching of metals through the soil and subsequent contamination of the wider environment.
Adding lime, biochars, zeolites, and various organic amendments to lock up metals in soil has been used much more successfully, but of course this does not remove or reduce the total pool of metals. Furthermore these amendments may provide only a temporary solution; repeated applications are likely to be required as the mobile fraction of the soil pool becomes replenished. More accurate modeling of the rates of flux of transient metals may help to provide more sustainable solutions, in which phytoextraction plays an effective role in removing mobile fractions of metals, working in combination with other amendments and effectively ‘polishing’ the soil by removing the highest risk fraction. More modern approaches to risk assessment of polluted land are based on the pathway of the pollutant from source to receptor. Breaking the pathway or linkage is likely to remove or reduce the risk of contamination or harm to the receptor or the wider environment. In the context of human exposure to heavy metals in soil, inhalation of dust and indirect consumption of metals are the only significant pathways of risk. In the case of dust, a permanent vegetation cover (phytostabilization) may provide the simplest form of phytoremediation. In the case of human consumption, planting crops that exclude metals (phytoexclusion) and avoiding the consumption of unwashed and unpeeled root vegetables may provide effective protection from exposure.
Uses and Limitations of Phytoremediation There are many examples of the low-technology use of plants to protect and clean up the environment, including the use of vegetation barriers associated with roadways, waterways, agricultural systems, and landfills. At the simplest level, vegetation provides effective barriers against noise, dust, and run-off of wastes. In the urban environment, plants improve microclimates, provide better quality air, and improve human health
Plants and the Environment j Phytoremediation and well-being. Viewed as a technology to address larger challenges, the use of constructed wetlands provides the most proven, most widely, and longest used application of phytoremediation, both for inorganics (metals, nitrates and phosphates, cyanide) and organics (petroleum hydrocarbons and herbicides). In terms of the wider application of science to remediate pollution, substantial advances in research have been made over the last 50 years although the subject remains in its infancy. Efforts to translate the findings of laboratory and greenhouse research to the field have been challenging, with many inconclusive phytoremediation trials. Furthermore, a long time span is often required to prove the effectiveness of phytoremediation. Advancement of knowledge will undoubtedly witness an increasing number of phytoremediation field trials and practical demonstrations of the effectiveness of more integrated phytotechnologies. Phytoremediation has synergies with other environmental agenda including ecological restoration, climate change, sustainable soils, and ecosystem services. There have been many predictions that phytoremediation is an emergent technology that can be viewed as a low-cost, sustainable, environmentally friendly, clean, and green solution for pollution. Currently, phytotechnologies probably represent substantially less than 1% of the total money spent on environmental cleanup worldwide. The majority of polluted sites contain mixtures of both inorganics and organics, but phytoremediation research has largely progressed with a separate focus on each. Successful practical use of phytotechnologies for organic pollution has been considerably higher than for inorganics, but a larger legacy of inorganic pollution may reverse this emphasis as knowledge improves methods that can be realistically used to manage and
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manipulate pollutants. A better understanding of rhizosphere processes in soil and uptake, translocation, and degradation of pollutants is required to be able to enhance the efficiency of phytoremediation.
See also: Plant Nutrition: Ion Transport; Mineral Uptake. Plants and the Environment: Land Reclamation and Remediation, Principles and Practice; Plants as Pollution Monitors; Waste Water Treatment.
Further Reading Baker, A.J.M., Proctor, J., Reeves, R.D. (Eds.), 1992. The Vegetation of Ultramafic (Serpentine) Soils. Intercept, Andover. Batty, L.C., Dolan, C., 2016. The potential use of phytoremediation for sites with mixed organic and inorganic contamination. Crit. Rev. Environ. Sci. Technol. 43, 217–259. Dickinson, N.M., Baker, A.J.M., Doronila, A., Laidlaw, S., Reeves, R.D., 2009. Phytoremediation of inorganics: realism and synergies. Int. J. Phytorem. 11, 97–114. van der Ent, A., Baker, A.J.M., Reeves, R.D., Pollard, A.J., Schat, H., 2013. Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362, 319–334. Gerhardt, K.E., Huan, X.-D., Glick, B.R., Greenberg, B.M., 2009. Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci. 176, 20–30. Kang, J.W., 2014. Removing environmental organic pollutants with bioremediation and phytoremediation. Biotechnol. Lett. 36, 1129–1139. Passatore, L., Rossetti, S., Juwarkar, A.A., Massacci, A., 2014. Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J. Hazard. Mater. 278, 189–202. Pilon-Smits, E., 2005. Phytoremediation. Annu. Rev. Plant Biol. 56, 15–39. Tongway, D.J., Ludwig, J.A., 2011. Restoring Disturbed Landscapes: Putting Principles into Practice. Society for Ecological Restoration International. Island Press, Wellington.
Phytoremediation attempts to use plants and microbes associated with plant root systems to harness natural processes to protect the environment and to clean up polluted and degraded land, water, and the atmosphere. Phytoremediation is promoted as an emerging, low-cost, environmentally sound technology for plant-based solutions to pollution. The scientific use of the terminology is more recent than the effective use of the technology; two examples of the established practical application of phytoremediation are wastewater treatment using constructed wetlands and vegetation barriers to restrict leakage of hazardous compounds from waste dumps and landfills. This has particular appeal in its potential to exploit biological processes and uptake mechanisms in plants to remove, degrade, or volatilize pollutants. Plants can be used in place of expensive engineering solutions for contaminated land, avoiding disposal of the soil (dig and dump), installation of protective artificial barriers (clays or HDPE membranes), and coverage with clean soil imported from land excavation elsewhere. A limited number of field studies have demonstrated the effectiveness of phytoremediation to remove pollutants from soil (phytoextraction), but applications of this technology frequently have been exaggerated in the context of heavy metals. In contrast, plant-based solutions have proven to be very effective in nutrient-stripping of former agricultural soils for ecological restoration, stabilizing soil pollutants (phytostabilization), and in enhancing the degradation (phytodegradation, rhizodegradation) and volatilization of a wide range of organic chemicals including oils, pesticides, and explosives. Realistic and practical applications for phytoremediation of degraded and contaminated land are currently referred to as phytotechnologies. The International Phytotechnology Society and its official journal The International Journal of Phytoremediation provide the best representation of the current status of the science and practice of phytoremediation. Phytoremediation of inorganic and organic pollutants is fundamentally different and often presents separate challenges for scientific inquiry and practical actions. This is largely because inorganic chemical compounds as pollutants can change their chemical structure or be transferred from one medium to another, but the component toxic chemical elements, such as heavy metals, cannot be degraded and made to disappear. In contrast, the carbon ring–based structure of organic pollutants associated with toxicity can be degraded effectively through breakdown into less complex and nontoxic chemical forms of carbon, hydrogen, and oxygen. Any residual heavy metal that was a component of the organic compound is usually present in too small an amount to create further problems as an inorganic pollutant.
landscapes, for example, through pioneering applied ecology research led by A.D. Bradshaw in northwest United Kingdom in the 1970s. New insights into many aspects of soil and plant science were provided through studies of degraded land often devoid of organic matter, nutrient deficient, and contaminated by heavy metals from mining wastes and industrial pollution. The extreme physical and chemical status of exposed substrates and pollution-impacted soils were not compatible with the essential processes required to maintain nutrient cycles and to support a sustainable vegetation cover. Furthermore, there was increasing awareness of human health risks from the legacy of wastes, spillages, residues, and fallout from mining, industry, agriculture, and urban pollution. In some cases soil amendments of lime and organic matter helped the initial establishment of plants, but longer-term maintenance of a vegetation cover often proved to be problematic. There are natural differences in the uptake of chemical elements by plants, ranging from preferential uptake to exclusion, and differing both between species of plants and chemical elements. This has a particular application for heavy metals, normally found in low concentrations but frequently highly elevated in polluted environments. Attempts to understand and describe mobility of heavy metals in soils, and their bioavailability to plants and animals, have led to significant scientific advances. Studies on plants in heavy metal–polluted environments provided evidence of adaptation to pollution and possibly the first examples of plant evolution outside the fossil record. This stimulated considerable interest in metal tolerance as a heritable trait in plants and the explanatory physiological and biochemical mechanisms associated with the responses of plants to pollution. More efficient ways to restore vegetation on metalcontaminated soils were becoming better understood, and metal-tolerant plants allowed the greening of areas previously devoid of vegetation. There was some concern, however, that toxic heavy metals might be transferred along food chains and to the wider environment, especially when land was restored to agriculture for crops or livestock. Restoration of contaminated and degraded land to more naturalistic vegetation cover became a more common goal, especially in urban areas and on previously mined and former industrial land. The science and practice of ecological restoration developed more broadly in the 1980s, renewing and restoring degraded, damaged, or destroyed ecosystems and habitats in the environment by active human intervention and action. The Society of Ecological Restoration (SER.org) represents the leading edge of progress in this field, partly through its journal Restoration Ecology.
Origins of Phytoremediation
Inorganic Pollutants: Metal Tolerance and Hyperaccumulation
Modern scientific interest in phytoremediation probably has its origins in the ecological restoration of postindustrial degraded
Inorganic pollutants include macronutrients (nitrate and phosphate), trace elements (metals and metalloids, often referred to
Encyclopedia of Applied Plant Sciences, 2nd edition, Volume 3
http://dx.doi.org/10.1016/B978-0-12-394807-6.00016-2
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as heavy metals), and radioactive isotopes (238U, 137Cs, and 90 Sr). Some plants that naturally evolved on metal-enriched soils, referred to as metallophytes, accumulate exceptionally high concentrations of specific but different chemical elements in their living foliage and stems. This was probably first identified in the mid-nineteenth century by J. Sachs on calamine soils near Aachen, Germany, in species of Thlaspi, Viola, Armeria, and Silene. Their location has been used by mining prospectors in the search for outcrops of metalliferous ores. Scientific interest in the plants notably increased from the 1990s through research variously led by A.J.M. Baker, R.R. Brooks, R.D. Reeves, F. Malaise and J. Proctor, and T. Jaffré on the unique vegetation of ultramafic (serpentine) soils. Occupying less than 1% of the Earth’s surface, ultramafic soils are widely scattered throughout both temperate and tropical regions. The term hyperaccumulator was coined by R.D. Reeves to describe a minority of the plants found growing on these soils that accumulated nickel (Ni) in foliage and stems at concentrations >1000 mg g1 (more than 1%) of dry weight. This is 100–1000 times higher than the amount in nonmetallophyte plants, and 10–100 times higher than normally found in plants on ultramafic soils. A concentration of >1000 mg g1 similarly defines the hyperaccumulator trait for of copper (Cu), cobalt (Co), arsenic (As), and lead (Pb), but different critical concentrations apply to elements where normal concentrations in plants are typically much higher or lower. Thus, hyperaccumulation of manganese (Mn) and zinc (Zn) is defined at plant concentrations >10 000 mg g1 and cadmium (Cd) at >100 mg g1 (Figure 1). Hyperaccumulators have the ability to transfer chemical elements from the soil to above-ground plant tissues when growing within healthy self-sustaining populations in their natural habitat. The most commonly cited hyperaccumulator is a New Caledonian endemic woody plant, Sebertia acuminata (Sapotaceae), that has 11 700 mg Ni g1 (11.7% of dry weight)
recorded in its leaves and 257 400 mg Ni g1 (25.7% of dry weight) in its sap, although the total number of species exhibiting hyperaccumulation traits is now well in excess of 500. It seems likely that these plants could provide the source of planting material for phytoextraction of the same metals from anthropogenically contaminated soils. Subsequent harvesting of the plants would remove metals from the contaminated soil and allow subsequent recovery of the metal from ash following plant combustion (phytomining). Potentially this would also provide an economic return through the market value of the metal (Figure 2).
Inorganic Pollutants: Phytoremediation Significant advances in biomolecular science have allowed identification and transformation of high uptake traits in plants, linking genetic and physiological traits with transport and storage of metals in plants. However, transferring what often may be a multicomponent stress-tolerance physiological trait into a high-yield cropping system has met with less success. Most hyperaccumulators are tropical plants that are unable to grow in cooler climates, and temperate hyperaccumulator plants are almost all herbaceous plants of diminutive stature and low productivity, such as Noccaea caerulescens (Syn. Thlaspi caerulescens) and Arabidopsis halleri (Brassicaceae) which have been used as model plants to study the remarkable phenomenon of hyperaccumulation. In addition to the practical and agronomic challenges, there are significant regulatory restrictions and public-perception issues associated with the release of genetically modified organisms into the environment. Many misleading claims of hyperaccumulation have been published from inadequate sampling in the field or by
Figure 1 Prof. Robert Brooks with Ornella Gambi next to Alyssum bertolonii (Brassicaceae) at Monte Prinzera, Italy, where she discovered this to be the first Ni-hyperaccumulator plant in 1948. More than 500 hyperaccumulator species have been discovered since then.
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productivity advantage would counterbalance a 10-fold lower metal concentration in plant tissues, providing the same final offtake of metals from the soil as a slow-growing hyperaccumulator. Clones of willows and poplars have been suggested as likely candidates. In field trials these plants have been shown to uptake relatively large amounts of Zn and Cd into aboveground woody parts that can be harvested in winter and also used as a bioenergy crop. While this offers some potential in soils in urban and industrial areas where these metals are frequently elevated, a significant proportion of metal uptake into these deciduous plants may be raised to the soil surface from deeper layers following leaf fall, potentially enhancing exposure and risk from the pollutants. Furthermore, unless plants have the characteristics of both hyperaccumulation and high growth rates, the time required to achieve significantly reduced concentrations of heavy metals through plant uptake and harvest invariably would take several decades. Other plants that have been claimed to offer the possibility of phytoextraction of metals include a number of grasses, including vetiver grass (Vetiveria zizanioides) and Miscanthus spp. One apparently unique application for phytoremediation is the proven volatilization of Se in significant amounts by plants and microorganisms that methylate Se to a less toxic volatile form. Selenium is taken up from the soil and emitted to the atmosphere in diluted nonharmful form as a gas. Similar results have been achieved for Hg in transgenic plants (Figure 3).
Figure 2 Botanist Dr Antony van der Ent next to a hyperaccumulator tree Pycnandra acuminata (Sapotaceae) at the Rivière Bleue reserve in New Caledonia. The tree is estimated to contain 6 kg nickel. Photo: AJM Baker.
overdosing plants in unnatural conditions. Toxicologically challenged plants or plant tissues grown in hydroponics, pot experiments, or other artificial conditions do not represent species with constitutional and heritable traits of hyperaccumulation. Many claims of hyperaccumulation of lead, copper, cobalt, chromium, and thallium are almost certainly unfounded. The requirement for a productive plant that can be cultivated as a crop and that also hyperaccumulates metals presents a plethora of problems. Particular attention has been given to N. caerulescens (Pb, Zn, Cd, Ni), Alyssum spp. (Ni, Co), and a fern Pteris vittata (As) which have produced mixed results in small-scale short-term field trials. However, there have been a small number of convincing larger-scale and longer-term field trials that have demonstrated phytoextraction is both agronomically feasible and economically viable. In the United States, selenium (Se) has been harvested and transferred as a fodder crop to selenium-deficient areas. Berkheya coddii (Asteraceae) has been grown on Ni mine wastes in South Africa and extracted as an ore. Removal of significant amounts of metal from soil requires a combination of high harvestable plant tissue concentrations of the metal and high rates of plant growth. An alternative strategy for phytoextraction is to use plants known as accumulators that uptake higher concentrations of metals than most plants but that are also highly productive and can be grown in cropping systems. These plants accumulate metals, rather than hyperaccumulate metals. Logically, a 10-fold
Organic Pollutants Organic pollutants that have been targeted for phytoremediation include petroleum hydrocarbons (e.g., oils, polyaromatic hydrocarbons (PAHs)) and industrial solvents (particularly trichloroethylene (TCE)), pesticides (e.g. atrazine), and explosives (2,4,6-trinitrotoluene (TNT)). Phytodegradation of organic pollutants involves either degradation of the chemicals (phytodegradation) to simpler nontoxic compounds, or sequestration and volatilization. Degradation of contaminants can occur either within plant tissues or may also involve microbial activity in the soil or root zone (rhizosphere). Phytodegradation is effective for organic chemicals that are mobile in plants, such as atrazine and other herbicides. Other pollutants such as TCE and methyl tertiary butyl ether (MTBE) are also volatilized more readily to the atmosphere through processes of plant uptake or in the presence of plant root systems. Petroleum hydrocarbons, PAHs, and polychlorinated biphenyls (PCBs) are degraded by soil microbial activity in the soil, itself enhanced by plant root systems. Rhizosphere processes stimulate microbial activity, for example, through increasing soil aeration and releasing secondary plant compounds as root exudates. Bacteria that include species of Arthrobacter, Pseudomonas, and Bacillus can degrade recalcitrant pollutants such as the PAHs, but they may also solubilize compounds bound within the soil matrix, facilitating uptake by plants. Enzymes, such as dehalogenases, nitroreductases, and laccases, released into the soil from plant sources have been shown to degrade a range of organics including TCE, PCBs, TNT, and various aromatic compounds. A wide range of plants have been used including poplars, willows, maize, rice, and alfalfa. Laboratory studies have demonstrated the potential to use transgenic
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Plants and the Environment j Phytoremediation
Figure 3 Phytoremediation expert Prof. Alan Baker standing in a field trial (set up by Dr Mei Lei) of an As-hyperaccumulator fern, Pteris vittata, on contaminated agricultural land downwind of a large Pb smelter, Jiguan in Henan Province, China. Photo: A.J.M. Baker.
plants and microbes to remediate organic contaminants, for example, by overexpressing genes that encode enzymes involved in degradation pathways, but this is largely untested in the field. Enhancing phytoremediation efficiency with endophytes (microorganisms that live within plant tissues) has shown, for example, that degradation of benzene, toluene, and TCE is enhanced in poplar by endophytic species of Pseudomonas and Bacillus in ex situ small-scale trials.
Integrated Phytoremediation Strategies The chemical forms of inorganic pollutants such as metals in soil invariably consist of the largest fraction being tightly bound to particles such as clay and organic matter. A much smaller proportion of the total amount of metal in soil is readily soluble in water in the pore spaces between soil particles, but this fraction is more mobile, more readily bioavailable for uptake by plants and animals, but also more easily leached from soil. It is this mobile fraction of metals that presents most toxicological risk. However, metals continually but slowly transfer between the two fractions of the total pool of metals in the soil, for example, when organic matter is added to soil (locking up mobile metals) when organic matter decomposes (releasing metals to the mobile fraction). The flux between these two fractions is also strongly influenced by several other physical, chemical, and biological factors including soil pH, conductivity, aeration, water logging, root exudates, earthworm activity, and mycorrhizae. Adding amendments to soil modifies these factors and alter the mobility and bioavailability of metals, although these actions rarely satisfied regulatory criteria that are usually based on the total concentrations of heavy metals in soil. In experimental studies, a range of chemicals including chelates and organic acids have been used to enhance metal uptake into plants, improving the success of phytoextraction but often also increasing leaching of metals through the soil and subsequent contamination of the wider environment.
Adding lime, biochars, zeolites, and various organic amendments to lock up metals in soil has been used much more successfully, but of course this does not remove or reduce the total pool of metals. Furthermore these amendments may provide only a temporary solution; repeated applications are likely to be required as the mobile fraction of the soil pool becomes replenished. More accurate modeling of the rates of flux of transient metals may help to provide more sustainable solutions, in which phytoextraction plays an effective role in removing mobile fractions of metals, working in combination with other amendments and effectively ‘polishing’ the soil by removing the highest risk fraction. More modern approaches to risk assessment of polluted land are based on the pathway of the pollutant from source to receptor. Breaking the pathway or linkage is likely to remove or reduce the risk of contamination or harm to the receptor or the wider environment. In the context of human exposure to heavy metals in soil, inhalation of dust and indirect consumption of metals are the only significant pathways of risk. In the case of dust, a permanent vegetation cover (phytostabilization) may provide the simplest form of phytoremediation. In the case of human consumption, planting crops that exclude metals (phytoexclusion) and avoiding the consumption of unwashed and unpeeled root vegetables may provide effective protection from exposure.
Uses and Limitations of Phytoremediation There are many examples of the low-technology use of plants to protect and clean up the environment, including the use of vegetation barriers associated with roadways, waterways, agricultural systems, and landfills. At the simplest level, vegetation provides effective barriers against noise, dust, and run-off of wastes. In the urban environment, plants improve microclimates, provide better quality air, and improve human health
Plants and the Environment j Phytoremediation and well-being. Viewed as a technology to address larger challenges, the use of constructed wetlands provides the most proven, most widely, and longest used application of phytoremediation, both for inorganics (metals, nitrates and phosphates, cyanide) and organics (petroleum hydrocarbons and herbicides). In terms of the wider application of science to remediate pollution, substantial advances in research have been made over the last 50 years although the subject remains in its infancy. Efforts to translate the findings of laboratory and greenhouse research to the field have been challenging, with many inconclusive phytoremediation trials. Furthermore, a long time span is often required to prove the effectiveness of phytoremediation. Advancement of knowledge will undoubtedly witness an increasing number of phytoremediation field trials and practical demonstrations of the effectiveness of more integrated phytotechnologies. Phytoremediation has synergies with other environmental agenda including ecological restoration, climate change, sustainable soils, and ecosystem services. There have been many predictions that phytoremediation is an emergent technology that can be viewed as a low-cost, sustainable, environmentally friendly, clean, and green solution for pollution. Currently, phytotechnologies probably represent substantially less than 1% of the total money spent on environmental cleanup worldwide. The majority of polluted sites contain mixtures of both inorganics and organics, but phytoremediation research has largely progressed with a separate focus on each. Successful practical use of phytotechnologies for organic pollution has been considerably higher than for inorganics, but a larger legacy of inorganic pollution may reverse this emphasis as knowledge improves methods that can be realistically used to manage and
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manipulate pollutants. A better understanding of rhizosphere processes in soil and uptake, translocation, and degradation of pollutants is required to be able to enhance the efficiency of phytoremediation.
See also: Plant Nutrition: Ion Transport; Mineral Uptake. Plants and the Environment: Land Reclamation and Remediation, Principles and Practice; Plants as Pollution Monitors; Waste Water Treatment.
Further Reading Baker, A.J.M., Proctor, J., Reeves, R.D. (Eds.), 1992. The Vegetation of Ultramafic (Serpentine) Soils. Intercept, Andover. Batty, L.C., Dolan, C., 2016. The potential use of phytoremediation for sites with mixed organic and inorganic contamination. Crit. Rev. Environ. Sci. Technol. 43, 217–259. Dickinson, N.M., Baker, A.J.M., Doronila, A., Laidlaw, S., Reeves, R.D., 2009. Phytoremediation of inorganics: realism and synergies. Int. J. Phytorem. 11, 97–114. van der Ent, A., Baker, A.J.M., Reeves, R.D., Pollard, A.J., Schat, H., 2013. Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362, 319–334. Gerhardt, K.E., Huan, X.-D., Glick, B.R., Greenberg, B.M., 2009. Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci. 176, 20–30. Kang, J.W., 2014. Removing environmental organic pollutants with bioremediation and phytoremediation. Biotechnol. Lett. 36, 1129–1139. Passatore, L., Rossetti, S., Juwarkar, A.A., Massacci, A., 2014. Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J. Hazard. Mater. 278, 189–202. Pilon-Smits, E., 2005. Phytoremediation. Annu. Rev. Plant Biol. 56, 15–39. Tongway, D.J., Ludwig, J.A., 2011. Restoring Disturbed Landscapes: Putting Principles into Practice. Society for Ecological Restoration International. Island Press, Wellington.