Review Article

A Review on Heavy Metals (As, Pb, and Hg) Uptake by Plants through Phytoremediation

Table 2

Phytoremediation study on soil medium.

No.ResearcherResearch scale and durationUptake mechanisms and media (substrate)Contaminant or parameter and concentrationPlants name and typeResult

(1)[16]Greenhouse pot experiment (6, 10, and 16 days)Phytoextraction (soil was added to aqueous solution and was dried overnight in an oven at 120°C, cooled, and transferred to the pot)Aqueous solution containing 0.1041 g of sodium arsenate heptahydrate (Na2HAsO4· 7H2O), the mixture which contained 50 mg/kg of As (wet weight)Leersia oryzoides (rice-cut grass)—terrestrial plantThe increase in plant size is matched by a decrease in shoot arsenic concentration. The data show that 12, 13, and 13 mg/m2 of arsenic were absorbed by the shoots at 6, 10, and 16 weeks, respectively. Since the SRQ and PECs all exhibit the same downward trend after 6 wk, it is suggested that periodic mowing of Leersia oryzoides grown for phytoextraction purposes on contaminated land could maintain the high arsenic uptake at 6 week.

(2)[33]Laboratory (pot experiment) (90 days)Fly ash and soil mixturesPb as lead nitrate, Zn as zinc sulfate, Ni as nickel sulfate, Mn as manganese chloride, and Cu as copper sulfate (1000 ppm concentration each (Spiked))Scirpus littoralis—semiaquaticThe metal content ratios BO/soil (B/S) were higher than shoot/soil ratios (T/S) for all the metals, the highest being for Ni. Metal ratios BO/water (B/W) were also higher than shoot/water (T/W) ratios, but the B/W ratio was maximum for Zn. All the metals except Ni showed negative correlation with nitrogen but they were all nonsignificant. However, P uptake showed positive correlations with all the metals, and all were significant at 1% confidence limit.

(3)[49]Field study (90 days)Soil (agricultural land area)(Cu, Cd, Cr, Zn, Fe, Ni, Mn, and Pb)Wheat (Triticum aestivum L.)—terrestrial Indian mustard (Brassica campestris L.)—terrestrialAnalyses of effluents and soil samples have shown high metal content than the permissible limit except Pb. Analyses of plant samples have indicated the maximum accumulation of Fe followed by Mn and Zn in root > shoot > leaves > seeds. Maximum increase in photosynthetic pigment was observed between 30 and 60 days while protein content was found maximum between 60 and 90 days of growth period in both plants.

(4)[5]Laboratory (65 days)Phytoextraction (soil)Pb by using standard Pb solutions (75 mg Pb/1 kg soil)Creeping zinnia (Alternanthera phyloxeroides)—aquatic Moss rose (Sanvitalia procumbens)—terrestrial Alligator weed (Portulaca grandiflora)—aquaticAlternanthera phyloxeroides shows the highest lead content in its tissues. This might be caused by it forming long stolons, a massive fibrous root system, and large surface area which benefits the accumulation of lead. Efficiency process 30–80%.

(5)[34]Literature reviewSoilCd, Cr, Cu, Ni, Pb, and ZnBrassica juncea (Indian mustard), Brassica rapa (field mustard), and Brassica napus (rape)—terrestrialBrassica rapa exhibited the highest affinity for accumulating Cd and Pb from the soil, either with/without additional use of mobilizing soil amendments. Two Brassica species (Brassica napus and Raphanus sativus) were moderately tolerant when grown on a multi-metalcontaminated soil. The distribution of heavy metals in the organs of crops decreased in the following order: leaves > stems > roots > fruit shell > seeds.

(6)[50]Laboratory—pot experiment (12 days)Agropeat and half strength Hoagland solutionArsenic (As) as of sodium (meta-) arsenite (50 uM, 150 uM and 300 uM)Brassica juncea var. Varuna and Pusa Bold—terrestrialIncrease/decrease of antioxidant enzymes activities showed not much changes at the given concentrations. The data presented indicates the differential responses in both the varieties and also that the increased tolerance in P. Bold may be due to the defensive role of antioxidant enzymes, induction of MAPK, and upregulation of PCS transcript which is responsible for the production of metal-binding peptides.

(7)[51]Field study (trials to extract heavy metals from two contaminated soils, one calcareous (5 years) and one acidic (2 years))Phytoextraction (soil)Cd and ZnWillow (Salix viminalis)—terrestrialSalix had performed better on the acidic soil because of larger biomass production and higher metal concentrations in shoots. Addition of elemental sulphur to the soil did not yield any additional benefit in the long term, but application of an Fe chelate improved the biomass production. Cd and Zn concentrations were significantly higher in leaves than stems. On both soils, concentration in shoots decreased with time.

(8)[52]Laboratory (26 days)Sludge-amended soilsCd and ZnRaphanus sativus L.This study has shown that clear evidence of as ludge-driven plateau response in metal uptake by plants will only be obtained when studies have found a good hyperbolic relationship between soil solution metal concentration with increasing sludge application rate and can link this to a plateau response in plant uptake of metals.

Laboratory—lysimeter pot (March 1995–September 1995)SoilZn as ZnSO4 (50, 1,500, 2,000 μg/g (ppm) Zn. and 2,000 μg/g (ppm), and 0 μg/g (ppm) (control) received nutrient only)Hybrid poplar (Populus sp.)—terrestrialAt levels of zinc above 1,000 μg/g (ppm) in nutrient added, leachate levels were always below 100 μg/g (ppm) in samples as the zinc addition; these levels increased the following day and then decreased sharply the second day after the zinc addition, to concentrations less than 100 μg/g (ppm). The zinc concentration steadily decreased as the plants apparently reabsorbed the zinc as the nutrient was cycled through the pots on subsequent days. The root tissues showed much higher concentrations of accumulated and sequestered metal than did the above ground parts.
(9)[3]Laboratory (April 1996, 2 months)SoilZn (160 μg/g Zn, 600 μg/g Zn, and 0 μg/g Zn (control))Eastern gamagrass (Tripsacum dactyloides)—terrestrialLeachate analyses for zinc indicate that initially plants subjected to both levels of zinc were removing up to 70% of the zinc from the leachate. The plants receiving 160 μg/g Zn had grown considerably and were almost the same size as the controls (no zinc), but some of the mature leaf blades were rolled; the mean zinc removal rate for these plants was 50% of the zinc in the leachate. The plants receiving 600 μg/g Zn were smaller than the controls, their color was a darker green, most of the mature leaf blades were rolled, and the mean zinc removal rate was about 30% of the zinc in the leachate.
SoilPb and As (up to 1000 μg/g Pb and up to 200 μg/g As)Hybrid willow (Salix sp.) and hybrid poplar (Populus sp.)—terrestrialThe willows were able to remove approximately 9.5% of the available lead and about 1% of the total arsenic from the contaminated soil. The less mature poplars removed about 1% of the available lead and 0.1% of the total arsenic from the same soil. In the sand experiment, the willows took up about 40% of the administered lead and 30 to 40% of the administered arsenic.

(10)[53]Field (1976–2001)(Soil)Nonessential (Cd, Ni, Pb) and essential heavy metals (Cu, Fe, Mn, Zn). The tetrasodium salt of EDTA was applied at rates of 0, 0.5, 1, 2 g EDTA salt/kg surface (25 cm depth) soilSunflower (Helianthus annuus L.) and Hybrid poplar (Populus deltoides Marsh. x P. nigra L.)—terrestrialFor sunflower, the 1.0 g/kg rate of chelate addition resulted in maximal removal of the three nonessential heavy metals (Cd, Ni, Pb). Uptake of the essential heavy metals by sunflower was little affected by the EDTA. The leaves of sunflower grown with 1.0 g EDTA Na4·2H2O/kg soil accumulated more Cd, Ni, and Pb than leaves of sunflower grown without the EDTA salt. Removal of the non-essential heavy metals by sunflower was greater at the higher plant density compared to the lower one.

(11)[54]Laboratory18 different phytoremedation treatments. I. parcel: mine waste without fly ash. Control and untreated plot. 3 test plants. II. mine waste + fly ash without liming. Control and untreated plot. 3 test plants. III. mine waste + fly ash + liming. Control and untreated plot. 3 test plants.As, Cd, Mo, Pb, Zn (soil) and As, Cd, Pb, Ni, Zn (water)Grasses (mixture of selected species), sorghum (Sorghum bicolor L.) and Sudan grass (Sorghum sudanense)—terrestrialThe chemical risks of the Gyöngyösoroszi spoils were assessed. The major contaminants of the waste mine were identified: Pb, Zn, Cd, As. The concept of the integrated phytoremediation was successfully applied to vegetate Gyöngyösoroszi spoil. The biomass production was different, depending on the technology variant. The highest biomass production was achieved, when multilevel revitalization was also applied. The integrated phytoremediation treatments not only produced high biomass, but also decreased the heavy metal content in the plants.

(12)[55]Field (1995–1997)SoilNi, Cu, Cd, ZnWillow (Salix spp.)—terrestrialOne group of willow had relatively low Ni and Cu in the bark and high Cd and Zn in the wood, with a good survival rate and biomass production. The second group of willow had relatively high Ni and Cu in the bark and low Cd and Zn in the wood and performed poorly in terms of survival and biomass production.

(13)[8]Laboratory (15 May and 25 September 2002)Phytoextraction (soil)Cu, Pb, ZnFescue (Festuca arundinacea Schreb.), Indian mustard (Brassica juncea (L.) Czern.), and willow (Salix viminalis L.)—terrestrialThe use of the freeacid form of EDTA and exposure time of one to two weeks before harvesting increased the concentration of metals translocated to plant tissues.
It is found no significant difference in heavy metal concentrations in higher and lower soil horizons between EDTA treated and untreated soils. Exposing plants to EDTA for a longer period (2 weeks) could improve metal translocation in plant tissue as well as the overall phytoextraction performance.

(14)[24]Field experiment (3 years)Phytoextraction (soil content with Hg)Hg (mean Hg content of the soil was 29.17 μg/g for the 0–10 cm horizon and 20.32 μg/g for 10–40 cm horizon with less than 2% of the total Hg being bioavailable)Three agriculture crop plants: Triticum aestivum (wheat)—terrestrial
Hordeum vulgare (barley)—terrestrial
Lupinus luteus (yellow lupin)—terrestrial
The decrease of mean Hg concentration from 29.17 μg g–1 at 0–10 cm horizon to 20.32 μg g–1 at 10–40 cm horizon demonstrated the anthropogenic origin of the mercury in the soil. Preliminary results show that all crops extracted mercury, with Hg plant concentration reaching up to 0.479 μg g–1 in wheat. The mercury concentration in the plants accounted for less than 3% of mercury concentration in the soil. The Hg concentrations in the plants were similar or even higher than that of the bioavailable Hg in the soils. Mercury extraction yields reached up to 719 mg/ha for barley.

(15)[56]Pot experiment (20 weeks)Soil from waste deposits of the lead smelterPbAgrostis capillaris—terrestrialInoculation with indigenous or nonindigenous AMF in this experiment did not decrease Pb uptake by the host in comparison with nonmycorrhizal plants grown in contaminated soil. It can be concluded that 13 months of subculturing in an inert substrate did not affect development of G. intraradices PH5 isolated from the waste deposits of a Pb smelter in contaminated soil of its origin. The interaction of the fungus with the host plant was changed: the ability of the lineage cultured without HM to support plant growth in Pb-contaminated soil was decreased, while translocation of Pb from plant roots to shoots increased.

(16)[38]Field and greenhouse experimentsPhytoextraction (As- and Pb-contaminated soil)Arsenic (As) and lead (Pb)Chinese Brake Ferns (Pteris vittata)—terrestrial
Indian Mustard (Brassica juncea)—terrestrial
It appears that EDTA is necessary for Pb extraction due to the low soil Pb bioavailability. Soil amendments like EDTA are necessary because they mobilize soil Pb, making it available to plant roots. It may not be advisable to apply EDTA in the environment, because EDTA mobilizes metals, which may leach into surrounding property of groundwater. The presence of other metals that compete for EDTA may increase the amount of EDTA required for Pb remediation.

(17)[27]Laboratory experiment, using chamber (6 weeks)Phytostabilization (mercury-contaminated soil used in this experiments was obtained from a chemical factory located in the southeast part of Poland, which has been in operation for over 50 years)HgSpecies Festuca rubra (red fescue)—terrestrial Poa pratensis (meadow grass)—terrestrial Armoracia lapathifolia (horseradish)—terrestrial
Helianthus tuberosus (Jerusalem sunflower)—terrestrial
S. viminalis (willow)—terrestrial
The highest concentrations of mercury were found at the roots, but translocation to the aerial part also occurred. Most of the plant species tested displayed good growth on mercury contaminated soil and sustained a rich microbial population in the rhizosphere. An inverse correlation between the number of sulfur amino acid decomposing bacteria, and root mercury content was observed. These results indicate the potential for using some species of plants to treat mercury-contaminated soil through stabilization rather than extraction.

(18)[57]Field (July and October)Phytoextraction and phytostabilisation (soil)Zn, Cu, Cr and CdTwo poplar clones (Populus deltoides x maximowiczii-clone Eridano and P. x euramericana-clone I-214)—terrestrialLeaf, stem, root and woody cutting biomasses of treated plants were significantly greater than those in the controls in both clones, except for stem biomass at the beginning of October. Among the four heavy metals (Zn, Cu, Cr, and Cd), only Zn, Cu, and Cr concentrations in plants differed consistently between clones or soil treatments, while Cd levels were always below the detection limits.

(19)[58]Field study and laboratory experiment (2002-2003 (field study), 3 months for laboratory experiment)SoilFe, Zn, Pb, Cu, Ni, Cr, MnBrachythecium populeumThe results obtained from this study on B. populeum lead to the inference that physiological/bio-chemical analysis of epiphytic bryophytes can serve as cost-effective indicators/monitors for the environmental quality of any area, and on the basis of this information appropriate steps can be taken to improve the air quality of an area.

(20)[59]Pot experiment and field trial (2004-2005 for pot experiment, and 2005 field trial)Phytoextraction and phytostabilization (soil)As, Co, Cu, Pb, and ZnThree poplar species (Populus alba, Populus nigra, Populus tremula) and Salix alba—terrestrialTrace element concentrations were much higher in roots than in above-ground tissues, with particularly high concentrations in fine roots. The highest accumulations were measured in P. nigra and S. alba. In wood, the highest concentrations of Cu and Zn were in S. alba. Salix alba foliage contained highest concentrations of As, Cu, Pb, and Zn; leaf Zn concentration exceeded those of wood by almost 6 times. The overall removal of trace elements was only significantly higher in P. alba than in S. alba; P. alba.

(21)[60]Pot experiment and field trial (2 years (2004-2005) for pot experiment and field trial on May–September 2005)Phytoextraction and phytostabilization (soil (Pyrite ore contains mainly pyrite (FeS2), lesser amounts of chalcopyrite (CuFeS2), sphalerite (ZnS), magnetite (Fe3O4), and various trace elements))As, Co, Cu, Pb and ZnP. alba L. (white poplar)—terrestrial
P. nigra L. (black poplar)—terrestrial
P. tremula L. (European aspen)—terrestrial
Salix alba L. (white willow)—terrestrial
The result shown that establishment of Populus and Salix species at the site is achievable through ripping of the surface, minimal tillage, some mixing of the wastes with imported soil, irrigation and fertilisers. Potentially, the elevated concentrations of Pb, As and other elements could be leached from the remediated wastes towards groundwater or other receptors, and these fluxes could also be influenced by soil amendments, changes in the rhizosphere or both. Immobilisation of trace elements in both coarse and fine roots may reduce leaching, particularly of Cu and Zn but also As and Pb.

(22)[61]GreenhousePhytoextraction and phytostabilization (soil)Six sediment-derived soils with increasing field Cd levels (0.9–41.4 mg/kg)Two willow clones (Salix fragilis “Belgisch Rood” and Salix viminalis “Aage”)—terrestrialNo growth inhibition was observed for both clones for any of the treatments. Dry weight root biomass and total shoot length were significantly lower for S. viminalis compared to S. fragilis for all treatments. Willow foliar Cd concentrations were strongly correlated with soil and soil water Cd concentrations. Both clones exhibited high accumulation levels of Cd and Zn in above ground plant parts. Cu, Cr, Pb, Fe, Mn, and Ni were found mainly in the roots. Bioconcentration factors of Cd and Zn in the leaves were the highest for the treatments with the lowest soil Cd and Zn concentration.

(23)[62]Laboratory and fieldRhizobox experiment was used to investigate the short-term effect of willow roots on metal availability in oxic and anoxic sediment. Longer-term effects were assessed in a field trial (soil)Cd, Zn, Cu, and PbWillow (Salix spp.)—terrestrialThe rhizobox trial showed that Cd, Zn, and Cu extractability in the rhizosphere increased while the opposite was observed for Pb. The field trial showed that Cu and Pb, but not Cd, were more available in the root zone after water and ammonium acetate (pH 7) extraction compared with the bulk sediment. Sediment in the root zone was better structured and aggregated and thus more permeable for downward water flows, causing leaching of a fraction of the metals and significantly lower total contents of Cd, Cu, and Pb.

(24)[63]Pot experimentPhytoextraction (soil)As (as Na2HAsO4), Cd (as CdCl2), Pb (as Pb(CH3COO)2), and Zn (as Zn(CH3COO)2) (100 mg As/kg, 40 mg Cd/kg, 2000 mg Pb/kg, and 2000 mg Zn/kg)Salix spp.—terrestrialAlthough As and Cd uptake slightly increased in Suchdol-Zn soil compared to Suchdol-Pb soil, the element removal from soil was significantly higher in Suchdol-Pb soil due to a significant reduction of aboveground biomass yield in Suchdol-Zn soil. The yield reduction decreased the uptake of plant-available elements by biomass; thus higher plant-available portions of As and Cd were found in Suchdol-Zn soil.

(25)[64]Field survey: from 12 As-contaminated sites (September to November 2003)Field study: contaminated soilAsSamples of 24 fern species belonging to 16 genera and 11 families as well as their associated soils were collected—terrestrialPteris multifida and P. oshimensis can (hyper-) accumulate As in their fronds with high concentrations. Total As concentrations in soils associated with P. multifida and P. oshimensis varied from 1262 to 47,235 mg/kg, but the DTPA-extractable As concentrations were relatively low, with a maximum of 65 mg/kg. Although As concentrations in the fronds of P. oshimensis were comparatively lower than those of P. multifida, its high above ground biomass makes it more suitable for phytoremediating As-contaminated soils.

(26)[65]Field survey (contaminated site since 1976; the sample was taken in 2006)SoilCu, Pb, Cd, and ZnPaulowni fortunei (seem) HemsIn the rhizosphere and bulk soils of P. fortunei, all physico-chemical properties increased with the revegetation time. The total contents of Cu, Pb, Cd, and Zn also consistently increased with the re-vegetation time; moreover, rhizosphere soils accumulated more heavy metals than bulk soils with the revegetation time. In the rhizosphere soils of P. fortunel, the immobility and bioavailability of heavy metals were enhanced. In the rhizosphere microenvironment, pH, OM, and EC were important factors affecting the distribution of heavy metal fractions. Among different heavy metal fractions, the exchangeable and organically bound fractions were easily available for P. fortunei, but carbonate, Fe–Mn oxide, and residual fractions were not easily available for P. fortunei.

(27)[4]Greenhouse pot experiment (August-September 2002)Soil was sampled in two sites: contaminated soil was taken near road with heavy traffic and clean soil was taken from park protected from the road by buildingsAg, As, B, Ba, Be, Bi, Ca, Cd, Co, Cr, Cu, Fe, K, Li, Mg, Mn, Mo, Na, Ni, P, Pb, Rb, S, Sb, Se, Sr, Th, Ti, Tl, U, V and ZnWheat Triticum vulgare, sort Umanka—terrestrialConcentrations of Ag, Cd, Cu, Pb, Sb, and Zn in the initial contaminated soil were 3–6 times higher than those in the initial clean soil. In particular, contents of Cu, Mo, Ni, Pb, Sb and Zn in roots of the wheat grown in the contaminated soil were higher than those in the roots of the plants grown in the clean soil. Moreover, all the elements except Pb transferred more easily from roots to leaves.

(28)[66]Field experiment (155 days (May–November))Soil (agricultural soil)Cd, Cr, Pb, As, and HgRice (Oryza sativa L.)—terrestrialThe results showed the rice grain contained significantly lower amounts of five metals than straw and root in all sampling sites. Rice root accumulated Cd, As, and Hg from the paddy soil. The rice plant transported As very weakly, whereas Hg was transported most easily into the straw and grain among studied heavy metals.

No. (7), (10), (12), (18), (22), (23) adapted from no. (20). Phytoremediation Bibliography, Annotated Bibliography on Phytoremediation prepared by Mark Coleman, Biological Scientist, USDA Forest Service Southern Research Station and Ronald S. Zalesny Jr., Research Plant Geneticist, USDA Forest Service North Central Research Station May 1, 2006.