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Phytoremediation of soil metals
Rufus L Chaney*t, Minnie Malikz, Yin M Li*, Sally L Brown*, Eric P
Brewer*, J Scott Angle* and Alan JM Bake&

The phytoremediation of metal-contaminated soils offers a presently used [2**,3*,7**]. Categories of phytoremediation
low-cost method for soil remediation and some extracted include phytoextraction (the use of plants to remove
metals may be recycled for value. Both the phytoextraction contaminants from soils), phytovolatilization (the use of
of metals and the phytovolatilization of Se or Hg by plants plants to make volatile chemical species of soil elements),
offer great promise for commercial development. Natural rhizofiltration (the use of plant roots to remove contami-
metal hyperaccumulator phenotype is much more important nants from flowing water) and phytostabilization (the use
than high-yield ability when using plants to remove metals of plants to transform soil metals to less toxic forms, but
from contaminated soils. The hypertolerance of metals is not remove the metal from the soil). The use of plants
the key plant characteristic required for hyperaccumulation; and associated rhizosphere organisms or bioengineered
vacuolar compartmentalization appears to be the source plants to metabolize toxic organic compounds also appears
of hypertolerance of natural hyperaccumulator plants. promising (recently reviewed by Cunningham eta/. [lo*.]).
Alternatively, soil Pb and Crs+ may be inactivated in the
soil by plants and soil amendments (phytostabilization).
Phytostabilization appears to have strong promise for two
Little molecular understanding of plant activities critical to
toxic elements, chromium and lead. The reduction of
phytoremediation has been achieved, but recent progress
Cr6+, which poses an enviromental risk, to CrJ+, which
is highly insoluble and not demonstrated to pose an
in characterizing Fe, Cd and Zn uptake by Arabidopsis and
environmental risk [ll], by deep rooted plants can be
yeast mutants indicates strategies for developing transgenic
very effective. Chemical species of Pb in soil are usually
improved phytoremediation cultivars for commercial use.
somewhat bioavailable if the soil is ingested by childern,
livestock or wildlife [12], whereas a Pb phosphate mineral,
Addresses chloropyromorphite, is both extremely insoluble and non
*Environmental Chemistry Laboratory, United States Department of bioavailable [13,14**,15,16,17**] but it is formed slowly,
Agriculture, Agricultural Research Service, Building 007, Beltsville apparently because the reactants have low solubility. The
Agricultural Research Center West, Beltsville, MD 20705, USA
roots of Agrostis capi/laris growing in highly contaminated
*Department of Natural Resources and Landscape Architecture, Pb/Zn mine wastes caused the formation of pyromorphite
University of Maryland, College Park, MD 20742. USA from soil Pb and phosphate, but the mechanism remains
8Department of Animal and Plant Sciences, University of Sheffield, unknown [17**]. Although it was believed that Thlaspi
Sheffield SlO 2U0, UK
rotundifhm hyperaccumulated Pb, Zea mays accumulated
Current Opinion in Biotechnology 1997, 8:279-284 higher Pb levels in controlled tests if soil pH and
P were low [18*]. The addition of chelating agents
(e.g. N-hydroxyethyl-ethylenediamine-N, NW-triacetate
0 Current Biology Ltd ISSN 0958-l 669 [HEDTA], ethylenediaminetetraacetic acid [EDTA]) to
Abbreviations such soils increased Pb solubility and mobility within
EDTA ethylenediaminetetraacetic acid plants: shoot Pb reached l%, allowing the removal
MT metallothionein of enough Pb to encourage further evaluation of this
PC phytochelatin
approach [18*,19**]. Methods to prevent the leaching of Pb
chelates down the soil profile would be required to permit
such additions in the field in regions where net infiltration
Introduction occurs. Inactivating soil Pb using of soil amendments and
Because the costs of growing a crop are minimal compared revegetation to prevent erosion is increasingly seen as the
to those of soil removal and replacement, the use of promising soil Pb remediation technology [12,20].
plants to remediate hazardous soils is seen as having great
promise; several recent reviews on many aspects of soil Different views of the potential for use of phytoremedia-
metal phytoremediation are available [1,2”,3*,4*“,5’,6,7*o]. tion to clean up contaminated soils have developed among
Phytoremediation is the use of plants to make soil contam- researchers. Some have examined the naturally occurring
inants nontoxic, and is often also referred to as bioremedi- metal hyperaccumulators, plants that can accumulate
ation, botanical bioremediation and, Green Remediation. 10-500 times higher levels of elements than crops; Reeves
The idea of using rare plants that hyperaccumulate metals [21] suggested a widely accepted definition of Ni hyper-
to selectively remove and recycle excessive soil metals was accumulators: ‘a plant in which a nickel concentration of
introduced in 1983 [8], gained public exposure in 1990 at least 1000 pg g-1 has been recorded in the dry matter of
[9], and has increasingly been examined as a potential any above-ground tissue in at least one specimen growing
practical and more cost-effective technology than the in its natural habitat’. This definition can be adapted
soil replacement, solidification and washing strategies to other elements. Most plant species suffer significant

Whether Ni(histidine)z. Similar results were found for Zn in direct demonstration used isolated vacuoles from the ZI caendescens (AJ Pollard. mays patterns have been observed in different groups of hyper. In contrast. be optimized to develop commercially useful practices. nearly all of the histidine in exudate are alternative approaches to treating irrigation drainage is chelated with Ni. S.7**]. Whether hypertolerance in the For the effective development of phytoremediation. and Zn and Cd at high soil solution levels. root Zn. The most and fungal diseases. Here.34] have the element in root and shoot cells: hypertolerance is demonstrated that high (but not low) Ni levels in the the key property that makes hyperaccumulation pos. the xylem by a membrane transporter remains unknown. the highly etc.30]. a biomass is more important in the phytoremediation of nonhyperaccumulator species. Such tolerance is believed to result from vacuolar chewing insects and reduce the incidence of bacterial compartmentalization and chelation [24. 300-500mgZn kg-r). The plant must be able to tolerate high levels of lation give these species? Boyd et a/. There must be a rapid uptake rate for the element crop plant is grown on a contaminated soil with the at levels that occur in soil solution. shoot the Se-hyperaccumulators) [36]. so ‘hyperaccumulators’ contain >l% the Ni-hyperaccumulator Alyssum species accumulate re- shoot Zn or Mn [7”]. co-contaminating sulfate metal concentrations can exceed root levels [27. Normally. leaves of hyperaccumulators can reduce herbivory by sible. a few can reach 5% Ni. A quantitative example may provide clarity: presume that a high-biomass 3.28**. unpublished data). [27] found that Z caedescens Under favorable conditions. crop plants tomato was severely injured at 30uM Zn. Crop plants Zn and Cd appears to require the plant to accumulate tolerate higher shoot Zn and Mn levels than Ni (about much more Zn to have an adequate supply. electron of its uniq-ue soil and plant chemistry. Shoot Cd levels are usually markably higher shoot Ni levels compared to other species <l mg kg-r. This term seems Zn concentrations (100-300 mg kg-1 versus lo-12 mg kg-r appropriate for the plant species that accumulate over 1% in normal plants) to grow normally than do related of several elements (hypernickelophore. hyperzincophore. However. soil metals has been debated [2**.371. [33.38]. it is found in among the smaller group of plants that can tolerate nature with l-4% Zn whereas surrounding plants are at least 1% Ni in shoots. so ‘hyperaccumulators’ must accumulate and grown at the same Niz+ activity in solution [29”. these plants can reach 20 tons accumulated Zn and Cd from nutrient solution only dry biomass/ha. and salinity in Se-contaminated soils commonly inhibit Kramer et a/.32].280 Environmental biotechnology yield reduction when shoots reach 50-100 mg Ni kg-r dry at 320pM Zn. vu/gabs suffer a significant yield reduction when the shoots have . <<500 mg Zn kg-1 (Zn excluders). By implication. Brown et a/. some tolerate >I% Cd [23]. Both agronomic microprobe analysis [26] supports this conclusion for Zn management practices and plant genetic abilities need to in leaves of Thl’aspi caedescens. protoplasts of tobacco cells that had accumulated high levels of Cd and Zn [24]. characteristics that are important: What evolutionary advantage does metal hyperaccumu- 1. In the case of the usual Zn and Cd about as well as tomato and Silene vulgaris did. which are much higher in B and sulfate than the mixed chelate such as Ni(histidine. Further. but co-contamination at 100 mg Zn: 1 mg Cd. and Brassica juncea are examples of such annual crops). growing beside plants with more normal levels and slow cumulation of soil metals? Research has identified several volatilization [31. shown that highly Z-r-tolerant genotypes of T. known hyperaccumulators is due to an enhancement of each element must be considered separately because these mechanisms is not yet known. A plant must have the ability to translocate an element converted toavolatile species such as dimethylselenide from roots to shoots at high rates. Niz+ or a waters.3*.25**]. weight whereas Ni hyperaccumulators tolerate at least Because this species can keep tolerating and accumulating IO-20 times the normal maximum tolerable levels.) because this ability is qualitatively different than the effective compartmentalization to reduce the toxicity of hyperaccumulators as defined by Reeves [Zl]. in can phytovolatilize soil Se or accumulate Se into the forage the xylem exudate histidine chelates about 40% of the biomass for sale as an Se supplement for livestock feeds total Ni present. Additions of histidine to nutrient solution increased Ni Whether metal hyperaccumulation in shoots or high shoot tolerance and transport to shoots by A/yssum montanum. and l? caedescens only at 10 OOOpM Zn. Although many plants can volatilize Cd or Ni concentrations are 10 or more times higher dimethylselenide (or dimethyldiselenide in the case of than shoot concentrations. So growing species in normal crop rotations that hyperaccumulators are chelates with malate and citrate. nonaccumulator species [28**].29**]. studies have or 500 times the shoot Ni tolerated by crop plants. accumulators. malate) is pumped into water used for irrigation [36. Some elements can be accumulated by plant roots and 2. and tolerate 2 100 mg Cd kg-r. very high B or salinity can kill most chemical forms of Ni found in extracts of leaves of Alyssum plants. quite different pH adjusted to attain a 50% yield reduction (2. [32] or Hgu [35”]. [29”] recently found that although the this process (36. AJM Baker. but in hyperaccumulators. the Se-accumulating species similarly accumulate higher shoot Se levels and many can volatilize Se at high rates How do hyperaccumulators achieve this remarkable bioac. caenrlescens Species that accumulate over 1% Ni have been called require much higher solution Znz+ (10”-fold) and leaf ‘hypernickelophores’ by JaffrC [ZZ].

Even The remediation of other elements (e. an enzyme supports to convert high biomass agronomic plants into special more transfer to form more PCs and longer PCs. such that there is tolerance (A. Even with a low yield of to provide no benefit for phytoremediation. . We conclude that the concentration of PCs showed no difference. model. As genes and the characterization or confirmation of metabolic and U) will be. the outcome Increasing the yield of a crop could give a linear increase was a surprise in that the sensitive mutants (low PCs) had in phytoremediation capacity with increasing yield. the finding that the /zmtl vacuolar membrane the phytoremediation of an element may require soil pump protein (which restored Cd tolerance to mutant amendments such as chelating agents because soil or fission yeast) transported both Cd-PCs and PCs without plant chemistry reduces element uptake or translocation Cd. Thus.44’. the less expensive the disposal of the Although these studies have allowed the cloning of new phytoremediation crop residue or ash (e. with and without effective PC biosynthesis. 137Cs. whereas Zn phytotoxicity and coaccumulation of trace levels of Cd are normal Use of biotechnology to improve biogeochemical phenomena. Further. since that for hyperaccumulators such as r caerulescens. We believe that scientists phytoremediation should be more suspicious of ‘Cd tolerance’ in plants.41**] may been demonstrated.25**. higher of the soil contaminant 25400-fold.7**. the but can tolerate up to 25 000 mg Zn kg-1 (25 kg ton-l) transfer of mammalian MT genes to higher plants appear [39] without yield reduction. Phytoremediation of soil metals Chaney et al. the higher the concentration. Some authors have suggested that the yield of The evidence for the role of PCs is that their presence a crop would be two orders of magnitude higher than does correlate with normal levels of metal tolerance.43].3*. Because phytoremediation cultivars if this is required for some the level of Zn present in nearly all environments is 100 elements [7**]. Continuing the above level of tolerance. but is expected to be possible if result from the acutely toxic Cd supply without Zn. suggesting ability to hyperaccumulate and hypertolerate the metals that hypertolerance to Cd and Zn in these plants were to be phytoremediated is of greater importance than high not due to the hyperaccumulation of PC peptides [42.g. dry biomass contains 500 mg kg’ in plant cells would increase metal-binding capacity (500 g Zn ton-l). the formation of the sulfide-stabilized high molecular Sr. the environmental relevance of findings from of the domestication of metal hyperaccumulator plants such acute Cd exposure has not been established. Further. Zn when natural metal-tolerant plants were examined. Although Cd-PCs only use the available genetic diversity within a species can be found at low levels in plants in the environment.19*‘]. As. Although plant cell cultures expressing I: caerulescens. 281 about 500mg Zn kg-* at harvest. if the acutely toxic Cd dose is provided. But a significantly lower degree of transport of Cd to shoots increasing from ‘normal’ tolerance to ‘hypertolerance’ and than the wild type [45-l. Cd phytotoxicity in soil is a recent anthropogenic effect. Further. raises questions about how the pump works to induce to shoots [18’. An and the breeding of improved cultivars [7**. Cu. inhibition of the y-glutamyl-cysteine transferase: as long as and. which can remove both soil Zn and mammalian metallothioneins (MTs) [40] or phytochelatins Cd. the alternative view of Cd-catalyzed PC biosynthesis is that characterization of the mechanisms used by hyperaccu. A similar result was observed in hyperaccumulation increases the potential annual removal corn inbreds that differed substantially in shoot Cd. Even for elements levels of PCs were associated with higher shoot Cd [46]. when these researchers tested genotypes whereas the latter is a phytotoxic waste requiring disposal. but only 0. creative research is applied [2”. It Biotechnology approaches to develop phytoremediacion seems increasingly likely that Cd tolerance mechanisms plants have been examined. In some cases. times higher than that of Cd. the former is a rich ore. Interestingly. Cs.45’].35**]. At a 50% yield the concentrations of metal-binding proteins or peptides reduction (10 tons ha-l).5% for Z. translocate and tolerate metals. we have emphasized the importance pathways. U) from soils by hyperaccumulator crops has not weight Cd-PC complex in vacuoles [4**. the cloning and use of these genes Cd activity in the cytoplasm is high. Researchers expected that increasing is the factor controlling plant yield. has a low yield compared with the above species. but mutations that abolished PC production in Arabidopsis pot and field studies show that such perennial species and fission yeast resulted in hypersensitivity to Cd grown as a crop can attain as high as 5 tons ha-l before [41”. Traditional plant breeding can are incidental biochemical phenomena. eventually.28**]. the recycling of have been identified and studied (blocked in glucathione shoot metals in commerce may provide value for the synthesis or PC synthesis). that have little value in the biomass. PCs were essential for the normal no need to pay for safe disposal. and tolerance.g.28**]. Cd hypertolerance in ho. mays. 5 tons ha-1 at the point of incipient yield reduction. For a plant species with normal ash from metal hyperaccumulators. Cd-sensitive (hypotolerant) single gene breeding to increase the combination of yield and shoot mutants cad1 [44*] and cad2 [45’] of Arabidopsis thaliana metal concentration [27. one removes only 5 kg of Zn ha-l yearl. the removal would be 125 kgha-1. the plants would be killed by Zn. biomass. the chelation of PCs with Cd alienates the feedback mulators to accumulate. because Cd is not to combine the characteristics needed for successful 100 times more toxic than Zn: soil Zn phytotoxicity phytoremediation. biomass ash contains 20-40% Zn for T caerulescens. (PCs) [41**] are more tolerant of acute Cd toxicity. thahana).

improve the efficiency of phytoremediation. Dushenkov S. A fundamental understanding of both uptake Another goal of developing transgenic plants with in. Many of the studies noted hyperaccumulator plants and agronomic technology. It is increasingly clear that hypertolerance is fusion protein with B-glucuronidase (GUS). published within the annual period of review. which i review of phytoremediation of metals that notes the limited natural Pb indicated that Zn deficiency also induced the biosynthesis accumulation by plants in soil. muys. Kumar PBAN. and translocation processes in normal plants and metal creased metal-binding capacity was to use these metal. can make and secrete into the rhizosphere at adequate . McKenna and Chaney [54*] used chelator-buffered phytovolatilization has already begun. Rauser and Meuwly [49] used nontoxic biomass is very likely to support commercial environ- levels of Cd (3pM. of special interest promise. Chet I. Cunningham SD. ology of plants that hyperaccumulate and hypertolerate the Cd-binding ‘a-domain’ part of the protein. the hmtl vacuolar pump for Cd-PCs from fission yeast [25**] has not yet been successful. barley was induced by Fe-deficiency. transport protein for the metal chelate seems difficult. hyperaccumulators.56**. concentrations and simultaneously creating a selective Bio-Technology 1996. Dushenkov S. but.61*. The authors stress the importance of higher biomass worth examination to develop unique phytoremediation plants for use in phytoremediation. Raskin I. over time. Ow DW: Promises and prospects for phytoremediation. over 90% of root Cd was bound to to improve the cultivars for field use. but A thorough review with opinions about approaches for commercrally use- ful phytoremediation. Finding other simple biosynthetic 5:265-290. and /ztntZ [25**] have not yet progressed to soil studies which must be the expression in higher plants is expected soon. The expression of MT as the whole protein. Trends Biotechnol 1995. in the short term. Salt DE. 13:393-397. Lastly. but from their up- take of nearly only Fe phytosiderophores by a membrane 1. Blaylock M. but not Mn. Many opportunities [55**] Cd to grow lettuce at Cd levels relevant to foodchain have been identified for research and development to safety and found no evidence of Cd-PCs in lettuce leaves. extensive progress has recently been achieved in yreview of phytoremediatibn from the perspective of plant biochemists and identifying genes and proteins involved in the uptake of molecular biologists. carrier [55”.62]. Although most phytoremediation that. Raskin [5*] suggested that transgenic plants could be References and recommended reading developed to secrete metal-selective ligands into the Papers of particular interest. Improved important measure of success. Huang JW: Phytoremediation of contaminated soils. of outstanding interest chelation specifically only of Fe in soils. 30 times the level generally found in mental remediation. regulatory control of these activities.. Curr Opin Biotechnoll994. phytosiderophores obtain their specificity not by . PCs bound only a small fraction of systems are still in development. and found with present practices. Cunningham SD. New commercial firms are Because Poaceae species secrete mugineic acid family moving into this field and phytoremediation technologies phytosiderophores (chelating agents) to solubilize soil Fe. rhizosphere which could specifically solubilize elements of have been highlighted as: phytoremediation interest. or a metals. or 3. tests with the mercuric ion reductase [35”]. 4. under several fundamental to hyperaccumulation. Salt DE: Bioconcentration of heavy metals by plants. but had little effect on Cd transport to shoots. P/ant Physiol 1996.49’]. Zn. molecules with selective chelation ability that plants 2. Ensley BD. and secretion of phytosiderophores. such that the increase the annual rate of phytoextraction and to allow study results do not model-metal contaminated soils in recycling of toxic soil metals accumulated in plant the environment. It considers fruitful areas of research to understand . Progress has been hindered in the 12 years since the first report on Possible use of ‘metallophores’ to aid the model for phytoremediation [8] by limited funds for phytoextraction of soil metals research and development. application for Se PCs. Berti WR. to here have used acutely toxic levels of Cd. the expression in plants of phytoremediation plants for soil metals. 13~468-474. Kumar PBAN. the use of the improved 35Sz promoter may have cloning of genes required for phytoremediation has begun increased the ability of MT to keep Cd in roots [53]. Fundamental characterization of mechanisms.. and high rates of promoters (SO-531 increased Cd tolerance of tobacco and uptake and translocation are observed in hyperaccumulator other plants. and discuss the biochemistry of metal tools.60**. [63] and Cu membrane transporters have also been found in yeast. binding factors to keep Cd in plant roots. and physi- [35**]). high affinity Zn [47. and promising approaches to develop metal phytoremediation technologies. thus reducing and the use of tissue-specific promoters offer great Cd movement to the food chain or into tobacco [SO-531.57’]. will be increasingly applied commercially in the near term. and accumulate the intact chelate into root cells [56”]. or in plant breeding cell Cd. Cu deficiency [58’] in contrast with other reports. Regulatory control of phytosiderophore secretion in uptake and tolerance. which society can afford in contrast soil solution) to study PC physiology in 2. 110:715-719.48. plants. promise that the use of molecular biology tools can give Vacuolar compartmentation of Cd only in roots may reduce scientists the ability to develop effective and economic Cd translocation to shoots. and the modification Conclusion of codons will be required before its effectiveness can Extensive progress has been made in characterizing the be tested (similar to the mercury reductase gene changes soil chemistry needed for phytoremediation. Although this approach holds . Raskin I: Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants.282 Environmental biotechnology they account for only a small fraction of the tissue Cd Fe by yeast and plants [59”. and Recently.

and the determination of the inheritance of these different proper- Cadmium in Urban Soils. 1983:50-76. J Biol Chem 1995. Raab TK. Chaney RL: Plant uptake of inorganic waste constituents. Phytoremediation of soils contaminated with organic Botanica Acta 1994. Kerschner BA. . 19:772-777. Zakharova 0. and phytochemistry. 24. 70:21-25. 270:4721-4728. Smith JAC: Free histidine as a metal chelator in plants that soils by ATEM and EXAFS. 31. In Selenium 20. 26. 29:1118-l 126. ecology. Chaney RL. froc Nat/ Acad Sci USA 1996. Presl (Brassicaceae). membrane pump for Cd-PCs. Green CE: and cadmium-binding peptides in tobacco leaves: implication . 81:294-300. plants. relative to Zn. J Environ Oual 1990. Ruscitti T. Adv Agron 1996. 31:860-665. Beauvisage) per on transgenic Arabidopsis expressing Hg reductase. Extensive offers the ability to reduce chromate below the tilled soil layer. Cotter-Howells JD. Capom S: Remediation of contaminated land . New fhytol 6. Ensley BD. Anderson TA. 379:635-638. 27. and gives 2 brief report of finding pyromorphite volatilization among crop species. Sci Technol 1994. Phytoremediation of soil metals Chaney et al. Min Environ Mag of a transport function for cadmium binding peptides. Identification of pyromorphite in mine-waste contaminated . Pb/Zn-tolerant plant on the soil. Reeves RD. in transaenic ArabidoDsis thaliana olants exoressina a 19. variation in lead uptake and translocation. and includes strategies to make Zn and . Causality remains This paper examines the use of inexpensive phosphate rock as the phos. Poschenreider C. 8. 278:1727-l 730. Berti WR. Logan TJ. 11. Vogeli-Lange R. The addition of 35. Edited by Parr JF. Chaney RL. Phytoremediation caerulescens in high Zn and Cd nutrient solutions and field plots.. Chaney RL. in particles of rhizosphere soils that were not observed before growing a 21:34 l-344. however. Jaffr6 T.. Schwab AP. Marsh PD. binding peptides by HMTl. Baker AIM. .. contaminated soils [abstractl. Kapulnik Y. Brooks RR: Terrestrial higher plants which 16. Even species with an unusual ability to accumulate soil Pb defends Strepfanthus polygaloides (Brassicaceae) against require low soil phosphate and low soil pH to facilitate soil Pb phytoavail. Thlaspi caerulescens J. Frankfurt: DECHEMA. This paper shows the difficulty of the phytoextraction of soil Pb using plants 34. but only accumulate a few hundredmg Pb per kg. The bactenal gene had to be modified The authors reports on the effect of several chelating agents on the up. Am J Bat 1994. environmental cleanup [commentary]. accumulate nickel. 33. Environ Sci Tech 1997. Summers chelating agents. Hsu FC: the zinc hyperaccumulator Thlaspi caerufescens J6C Presl. which is not genetic variation was found in Zn tolerance. K&mimerU. could make soil Pb soluble and keep it from being . -. and Cd in shoots by EGTA additions. in Indian mustard by soil-applied chelating agents. Cotter-Howells JD. McCue KF. unsettled because only 40% of the xylem exudate Ni was chelated with phate amendment to inactivate soil Pb. Tech 1997. 93:9-l 6. Brown SL. in selenium enriched soils. Nicholson A: In situ formation of lead because it has been shown that the levels of ligands and nutrients in xylem phosphates in soils as a method to immobilize lead. Edited by Frankenberger WT Jr. Banuelos GS. 13. Angle JS. 31 :in press. distribution. J Environ Qua/ 1992. 92:1086-l 093. Chaney RL. 269:302-303. Shaw JJ. 1994. Angle JS. Terry N.. Li YM. Charnock JM. 22. Angle JS. pumping the Cd-PCs into a storage location by Cd-tolerant cells. the alternative to phytoremediation. Schmid M: Accumulation du nickel par une RubiacCe A commentary published in the same issue as the Rugh et al. Moffat A: Plants proving their worth in toxic metal cleanup. 93:3164-3166. Pb transfer to shoots was hydrolase gene in the same way so that these plants can reduce the risk of increased most by EDTA additions. Cotter-Howells J: Lead phosphate formation in soils. 1994:343-367. Appf Geochem 1996. This paper describes the use of Zn and Cd hyperaccumulator plants in the 25. Zayed AM: Rates of selenium the inactivation of soil Pb. 134:75-84. ties. Reeves RD. In The Vegetation of Ultramafic (Serpentine) Soils. Meek DW: Selenium uptake by different species 11:335-342. Ruby MV. Raskin I: Enhanced accumulation of Pb 93:3182-3187. Blaylock MJ. solutions and contaminated soils using phosphate rocks. Boyd RS. 26:646-654. 1994:1-l 30. Martens SN: Nickel hyperaccumulation studied to date. Biorecovery 1989. Ma ClY. 28. methyl-Hg so much that emission of Hgo vapor is environmentally accept- showing that the chelation specificity of the agent added strongly affects able. 9. Ortiz DF. histidine. de Nouvelle Calltdonia: psychotria douarrei (G. Thompson DM. fur J Soil Sci 1994. Potential use of metal hyperaccumulators. 451393-402. 3:9-l 1. Zn requirement. Environ exudate change 1 h after severing the stem. . Champness PE. Sci Sot Am J 1995. 5. achieves the removal ot Hg trom solI. Edited by Baker AIM. Boyd RS. pathogens. Rugh CL. Pattrick RAD: 29. biological methods. which metals have increased uptake and transfer to shoots.. Baker AIM. NJ: Noyes Data Corporation. Dushenkov S. Li YM. Charnock JM. 107:243-250. and Cd uptake provided by identified soil amendments to reduce chromate. pollutants. 135**1 pa. The first demonstration of a specific ligand that may be involved in the high 14. Environ hyperaccumulate metal elements-a review of their Pollut 1996. Wagner GJ: Subcellular localization of cadmium 7. Such genetic diversity may support the breeding of improved 12. Stack NM. Park Ridge. Crit Rev Acad Sci Paris 1974. . Andover: Intercept Ltd. Hajar ASM: Heavy metal accumulation development of phytoremediation cultivars using novel biotechnology meth- and tolerance in British populations of the metallophyte ods.. This team is working to obtain 2 methyl-Hg take and translocation to shoots of five metals. Ryan JA: Risk Based Standards for Arsenic. . Baker AJM. montanum is acutely toxic to an insect . James BR: The challenge of remediating chromium. . Reeves RD: The hyperaccumulation of nickel by serpentine higher plants. Cotter-Howells JD. Chen KY. New York: Marcel Dekker.6C. . Physioll990. Environ Sci This paper describes the first transgenic phytoremediation plant that . Raskin I: Plant genetic engineering may help with 1992:253-277. Cunningham SD: Lead phytoextradion: species montanum var. 127:61-68. Environ Sci Tech 1996. ance and uptake of Ni by 2 nonhyperaccumulator species. Anonymous: NEA dumps on science art Science 1990. 36. Gussman C. It discusses the Diiniker. Baker AJM: Genotypical differences in zinc and cadmium 30:248-251. by formation of heavy metal phosphates. AO. . contaminated soils. the inertness and insolubility of chromic oxides in soil will The authors report on the comparison of 20 diverse genotypes of 7: limit the formation of chromate and limit environmental risk. membrane protein. Cunningham SD: In-place inactivation of Pb in Pb in the Environment. Cope GH: Compartment&ion of zinc in roots and leaves of 10. Carlson C. Martens SN: Nickel hyperaccumulated by Thlaspi 18. New Phytol 1996. 66:55-l 14. Zayed AM: Selenium volatilization in plants. ability. Benson S. Davis A. modified bacterial m&A gene. Further. Ow DW: Transport of metal- remediation of contaminated soils. Meagher RB: Mercuric ion reduction and resistance precipitated by phosphate in roots. the addition of histidine to the nutrient solution increased the toler- Environ Sci Tech 1995. Baker AJM. 1 7. Huang JW.. 59:125-l 33. Cunningham SD. Soil organics in soils by plants or rhizosphere microbes supported by plants. Agron Research has shown that if chromate is reduced to chromic by chemical or Abstr 1996. I:81 -126. this may have resulted from the long exudate collection period 15. to obtain expression in plants. It is the first unequivocal demonstration of Kla JM. Wilde HD. 30. herbivore. Lead and cultivars.. This paper reports on the use of phosphate soil amendment to promote 32. Baker AJM: Zinc and cadmium A timely and thorough review of many aspects of the biodegradation of uptake of Thfaspi caerulescens grown in nutrient solution. Science 1995. Oikos 1994. a fission yeast ABC-type vacuolar Cd remediation cultivars of 7: caerulescens. hyperaccumulation in Thlaspi caerufescens tabstractl. Proctor J. 250:1515. Homer FA. Vtiquez MD. Plant 1995.. Salt DE. 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J Environ &a/1994. Parker DR. Chen Y: Cd uptake and translocation by the mutants was much lower than that by . Maiti IB. Ben-Asher J. Wagner GJ: Tissue interactions in selenium-accumulating and nonaccumulating partitioning of cadmium in transgenic tobacco seedlings and plant species. Koevoets PLM. MO/ Gen Genet 1994. Duau Z.. New Phytoll992. . Meuwly P: Retention of cadmium in roots of maize . 47. after functional expression in yeast Proc Nat/ Acad Sci USA 1996.. Mackey B. . Nielsen MT. Price NM. in graminaceous plants. complex in lettuce leaves. Andersen CR. Miki BL: Field performance and heaw metal concentrations in transaenic flue-cured tobacco 62. In this case. 20:27-34. Rauser WE: Phytochelatins and related peptides: structure. 60.and cadmium-contaminated soil. Details of the biosyn- . 63. Klausner RD: Iron- . Bell PF. 61433-440. Ma JF. regulated metal transporter from plants identified by short term. Plant Pbysiol1995. Verkleij JAC. 51. Did not include 100 times as 935624-5628. These issues were debated for over 10 years before this clean Howden et a/. Ernst WHO: Evidence trient solutions because of the presence of chelated metals. Kuske C. Page AL: Contrasting selenate-sulfate 52. Parker DR. Norvell WA: Equilibrium computer . Askwith CC. Rauser WE.. . seedlings: role of complexation by phytochelatins and related regulon in yeast EMBO J 1996. J Environ Oval 1993. in contrast with others’ observations that Zn defi- ciency might also induce biosynthesis and secretion of these ligands. In Chemical An updated review on metal-binding peptides by a leader in the field. tosiderophores by barley. several days.ance and keep it from being translocated. 93:2455-2456. Chen Z.1:261-26X Beuselinck F’. Plant Physiol to both i&eaie Cd tole. and discusses how to increased cadmium tolerance in Sikne vu/garis (hloench) use chelator buffering to make the different metals in a test system indepen- Garcke. Van Beusichem ML: Phytochelatin . Howden R. Proc Nat/ Acad Sci USA 1994. De Silva D. This indicates. rather than grasses being able to obtain Fe from microbial of glutathione alleviate the PC deficiency. Rauser used levels of Cd that ware AP. It was also reported that 57. 10:835-644. PC is essential to that phenotype. De Knecht JA. 58. Transgenic Res 1992. gene. Hunt AG. limitation. 22:766-792. genesis of a protein required for PC biosynthesis. 55. Wana Z. In ihe . Biol Tmce E/em Res 1995 46:13-29 23:1151-1157. release in relation to micronutrient metal deficiencies in barley. and used Fe chelate. Chaney RL. Zambrzuski S: Boron and selenium 53. 50. 122:681-688. Den Hartog PR. 1995:163-200. 15:3377-3384. Proc Nat/ Acad Sci USA 1996. Robinson NJ. Harmens H. Cardon G. Plant ohvtosideroohores. Guerinot ML: A novel iron- of the peptides is affected by the intensity and longevity of exposure. Goldsbrough PB.112:1273-1200. concentrations and binding state of Cd in roots of maize Plant Soil 1995. models: applications to plant nutrition research. Plant Physiol 1995. Cobbett CS: A This paper clarifies literature that is full of artifacts due to the exchange of . cad7 mutants of Arabidopsis theliane are thesis have been worked out. regulated DNA binding by the AFT1 protein controls the iron 49. Crowley DE. Broderius M. Plant Physiol 1995. potential of Thlaspi caerulescens and bladder companion for 54. Three families of PCs are present in maize. This paper reviews the problems of controlling metal phytoavailability in nu- 42. as microbial siderophores must be exchanged to phyiosiderophores before The characterization of another mutant in PC synthesis. Kaplan J: Molecular biology of iron strain? Plant Physiol 1992. Mol Microbial 1996. biosynthesis and function. Hadar Y. Yana M. 56:1818-l 824. 1OS:i 141-l 149. 1996. Edited by Loeppert RH. Guerinot ML: Genetic evidence that induction of root expr&sing a mammalian metallothi&ein-P-glucuronidase FeW chelate reductase activity is necessary for iron uptake gene fusion. not acutely phytotoxic. 91:8433-6436. 48. 36:255-260. Brandle JE. This paper discribes the discovery of a family of genes. thereby providing The characterization of a Cd-sensitive mutant that was altered by the muta. auestionina the model wherebv increased PCs were assumed microbial siderophores by gramineous plants. Andersen CR. Dancis A. 107:1059-l 066. that for mutants selected for sensitivity to Cd or demonstration of the actual mechanism used was found. Wu L. 242:666-674. paper [44*].. Shenker M. Akohoue S. Morel FMM: Phytochelatin production by A timely review of a rapidly progressing research area closely related to the marine phytoplankton at low free metal ion concentrations: absorption of heavy metals by plants. Soil Sci Sot Am J 1992. It shows Fe against a role for phytochelatins in naturally selected chelates that minimize artifacts in nutrient solutions. Goldsbrough PB. . Zhao H. Ahner BA. Pan A. Tie F. Elmayan T. Florijn PJ. Howden R. the expression of thiol oeptides. 109:195-202. Angle JS. The role of ligand exchange in the uptake of iron from the wild tvoe.204 Environmental biotechnology 37. which is stable metallothioneins. 172:299-308. Ten Bookum WM. 295:1-l 0. Parker DR: phytosiderophore 46. Banuelos GS. acquisition in Swcharomyces cerevisiee.he authors grew lettuce with chelator buffering to give contrblled activity 40. J Plant This paper indicates that only Fe deficiency induces the secretion of phy Physiol 1993. Brunn S. WI: Soil Science Society of America. Tepfer M: Synthesis of a bifunctional removal in boron-laden soils by four sprinkler irrigated plant metallothionein/p-glucuronidase fusion protein in transgenic species. and some genes have been identified. and the length 61. The authors discribe the first gene involved in Fe uptake by dicots isolated for study. PCs bound only a small amount of the absorbed Cd but. which is regulated by a protein in response to the Fe status of cells. Jackson PJ: Plant of Zn and Cd to the plants over time. The role of mugineic acids as is not due to increased production of phytochelatins. tobacco plants as a means of reducing leaf cadmium levels 39. 97:609-617. De Knecht JA. Stearman R. RBmheld V. Marschner H. the chelating ‘amino acids secreted by 44. In Equilibrium and Reaction Models. genotypes differing in shoot/root Cd partitioning. Nomoto K: Effective regulation of iron acquisition Increased zinc tolerance in Silene vu/gads (Moench) Garcke . Labbe H. Cadmium-sensitive. A review bf phytos’iderophores. Cobbett CS: grasses to obtain soil Fe and possibly other elements. 45. Yeargan R. McKenna IM. 43. Kalff MMA: Are phytochelatins involved in differential metal tolerance or do they merely reflect metal-imposed 59. field grown plants expressing the mouse metallothionein I 38. higher tolerance of Cd. Li L. the Fes+ specificity by uptake rather than chelation. much Zn as Cd. as found in normal enviroments. Fett J. Eide D. laboratory studies and field data from Massachusetts Bay. glutathione-deficient mutant of Arabidopsis Fe between different ligands in a nutrient solution. Ru B: u. Verkleij JAC: 56. 103:1305-l 309. 99:1475-l 460. and no evidence of PCs was found. under iron deficiency. Goldberg S. dent. Hattori J. It shows that Fe added theliane. together with the siderophores. Yamaguchi-lwai Y. This paper sio& the complexity’of PCs in relation to chronic nonphytotoxic Cd exposures. Plant J 1996. Phvsiol Plant 1996. chelates with mugineic acid are transported into the root. 107:1067-l 073. Baker AIM: Phytoremediation Plant J 1994. Plant Phvsiol 1995. Madison. Physioll993. Chaney RL: Characterization of a cadmium-zinc zinc. with added Zn and Cd. 142537-542.. Yi Y. Schat H. PCs could bind all plant Cd. 41. Tommey AM. cadmium-sensitive. Eide D: The yeast ZRTl gene encodes the zinc domain of human metall&hionein\-A can bind to metals in transporter protein of a high affinity system induced by zinc transgenic tobacco plants. Yehuda Z.. Genome 1993. Intact-Fe phytochelatin deficient. Gries D. Chaney RL. Schwab contrast with other research arouos. and hisview of the literature reflects a more physio- logically and environmentally relevant evaluation of PCs. Brown SL. Biochem J 1994. addition uptake by grasses. Only the leaves were examined.