Methods to Remediate Arsenic-Contaminated Soils: Comparison
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Arsenic is a metalloid widely distributed in the environment and of global concern for human health. In a promising breakthrough for sustainable arsenic soil remediation, a fern, Pteris vittata L., was discovered to take up arsenic from the soil and accumulate it in its fronds at up to ~100 times soil concentrations. Successively harvesting the fronds removes, or phytoextracts, arsenic from the soil with potential environmental and economic benefits including low site disturbance and low cost. 

  • arsenic
  • soil
  • rhizosphere

1. Introduction

Arsenic is a metalloid widely distributed in the environment and of global concern for human health. Arsenic can cause acute and chronic poisoning through exposure routes including inhalation and ingestion of water, food, and soil material. Arsenic causes numerous adverse health effects to humans [1]. Globally, the major concern comes from the contamination of drinking water from natural geological sources [2,3][2][3]. However, health risks from arsenic-contaminated soil should not be underestimated. In the USA, arsenic tops the Substance Priority List (SPL) created by the Agency for Toxic Substances and Disease Registry/US EPA, which ranks pollutants at Superfund sites based on toxicity and potential for exposure [4].
Conventional arsenic remediation methods are too expensive to clean up large, moderately contaminated areas, where the risk of negative environmental and health impacts is still unacceptably high [5]. In a promising breakthrough for large-scale, sustainable arsenic soil remediation, Pteris vittata L., a fern distributed globally in tropical and subtropical climates [6], was discovered to take up arsenic from the soil and accumulate it in its fronds at up to ~100 times soil concentrations [7]. Successively harvesting the fronds removes, or phytoextracts, arsenic from the soil with limited disturbance. Although there are costs associated with phytoextraction, for example, treating arsenic-enriched fronds, phytoextraction could be less expensive than other methods [8].
Many challenges still lie ahead for arsenic phytoextraction with P. vittata [9]. These challenges largely stem from the complex nature of the soil, especially spatial and temporal variation in soil characteristics. Remediation time estimates derived from rates measured under field conditions are long, about 40 years to remove 180 kg As/ha (100 mg As/kg) from soil (0 to 15 cm depth) [10,11,12,13][10][11][12][13]. The application of soil amendments has been investigated in efforts to increase arsenic uptake rates and shorten remediation times, but results are inconsistent. Frond arsenic concentrations and biomass were higher in P. vittata supplied with sparingly soluble compared to soluble phosphorus [14[14][15],15], though in other cases phosphorus application did not affect arsenic uptake in P. vittata regardless of solubility [16,17[16][17][18][19],18,19], and soluble phosphorus increased arsenic concentrations in porewater but not in P. vittata fronds [20]. Furthermore, some studies have shown that the presence of other soil contaminants will negatively affect arsenic uptake by P. vittata [20,21][20][21]. Finally, it is not well understood how arsenic depletion from soil correlates to arsenic accumulation in P. vittata fronds, for example, if all arsenic depleted from soil is accumulated in the fern or lost to other processes [11[11][13][22],13,22], especially under field conditions where fern roots have access to a larger volume of soil than in pot experiments [23,24][23][24].

2. Chemical Stabilization

Chemical stabilization, which involves applying a sorptive amendment to the soil to lower the soluble fraction of contaminants and decrease plant uptake [52][25], could be a less destructive alternative to conventional remediation approaches [53][26]. Chemical stabilization of arsenic typically involves applying precursors of iron (Fe) oxides (ferrous (FeSO4) or ferric sulfates (Fe2(SO4)3)) and zerovalent iron (Fe(0)), or directly applying poorly crystalline (ferrihydrite (Fe(OH)3) or crystalline iron oxides goethite α-FeOOH). Other materials, including aluminum-based industrial by-product compounds, have also been shown to be effective [54][27]. Amending soil with iron compounds decreases arsenic mobility and therefore soil and porewater toxicity in ex situ studies. Amendment with iron sulfates, together with lime to avoid soil acidification, decreased the concentration of water-soluble arsenic [55][28] and of arsenic in leachates [56[29][30],57], as well as arsenic uptake by crops [52,58][25][31]. The addition of zerovalent iron decreased the concentration of arsenic in soil porewater, leachates, and plant tissues, as well as of extractable and bioaccessible arsenic [56,57,59,60,61,62,63][29][30][32][33][34][35][36]. Goethite and ferrihydrite amendments decreased arsenic concentrations in porewater [64[37][38][39],65,66], in leachates [56[29][30][38],57,65], and arsenic uptake by plants and phytoavailability [67][40]. However, there are limitations to using these methods in more complex field conditions [53,62,68,69][26][35][41][42]. For example, amendments with iron sulfates plus lime or zerovalent iron led to increased concentrations of metals such as cadmium, copper, zinc, and lead in leachates or in plant tissues compared to untreated soils [56,57,61][29][30][34]. Additionally, when used in situ, arsenic stabilization methods were much less efficient than when used in batch or pot experiments [58,59][31][32]. Finally, even if amendments effectively decrease arsenic mobility under current geochemical conditions, changing conditions, especially changing redox potential due to microbial activity [70][43] could lead to arsenic release. On-going site monitoring is required to ensure effective remediation over timescales of years, akin to monitored natural attenuation [71][44].

3. Phytoextraction Using Pteris vittata and Other Arsenic-Hyperaccumulating Plants

3.1. Phytoextraction with Hyperaccumulators

Phytoextraction is a soil remediation method where plants extract contaminants from the soil and concentrate them in their aboveground biomass, which is then harvested to remove the contaminants while leaving the soil in place. Phytoextraction of metal(loid)s has been investigated using naturally occurring metal(loid) hyperaccumulators and non-hyperaccumulators including genetically modified plants [72][45]. Here, we focus on phytoextraction with non-genetically modified hyperaccumulators to explore the relationships between natural hyperaccumulator ecology and soil geochemistry. Brooks et al. [73][46] established the term hyperaccumulator in a study focusing on nickel to describe plants able to accumulate nickel at concentrations >1000 mg/kg (ppm) in dry leaf tissue. Since then, the term hyperaccumulator has been extended to other metals and metalloids with element-specific thresholds. Other criteria include extreme metal tolerance [74][47], a shoot-to-root metal(loid) concentration ratio (or translocation factor) typically >1 [75][48], and a ratio of metal(loid) concentrations in plant biomass to those in soils (or bioconcentration factor) typically >1. Hyperaccumulators tolerate high concentrations of metal in soils, but hyperaccumulation is a genetically distinct trait from tolerance [76][49]. Natural hyperaccumulation depends on both constitutive up-regulation of transporters to move metal(loid)s across membranes [77][50], and mechanisms that confer tolerance of the high concentrations of metal(loid)s thus taken up [78][51]. Several theories have been proposed to explain hyperaccumulation, including the defense theory, where high metal(loid) concentrations kill or deter pests [79,80][52][53]; allelopathy, where litterfall locally increases soil metal(loid) concentrations above those tolerable to other species [81][54]; and the phosphorus starvation theory, where metal(loid) uptake is a byproduct of nutrient acquisition [82][55].

3.2. Arsenic-Hyperaccumulators

As early as 1975, many plants accumulating >1000 mg/kg arsenic in their leaves and with a translocation ratio >1 were found growing in soils enriched in arsenic, mainly around mining sites. Among them Jasione montana L., Calluna vulgaris (L.) Hull, Agrostis tenuis Sibth. and Agrostis stolonifera L. were found in the UK [83][56], Agrostis castellana in Portugal [84][57] and Paspalum racemosum and Bidens cynapiifolia in Peru [85][58]. However, since those plants grew on soils extremely enriched in arsenic, the bioconcentration factor was <1, despite high concentrations in plant tissues, and those plants are consequently not hyperaccumulators, according to the bioconcentration criterion presented earlier. The first plant to be labeled an arsenic hyperaccumulator was the fern Pteris vittata L. P. vittata, an invasive species in Florida, USA [86][59], was identified in 1998 as an arsenic hyperaccumulator during a survey of plants growing on a Florida site contaminated with chromated copper arsenate (CCA) [87,88][60][61]. There, P. vittata accumulated between 1442 and 7526 mg/kg arsenic in its fronds with no observed toxicity effects [7]. In addition, in a pot experiment with a soil spiked with 1500 mg/kg arsenic, P. vittata was able to accumulate as high as 22,630 mg/kg arsenic [7]. The ratio of arsenic concentrations in fronds to roots in P. vittata was >20 and the bioconcentration factor ranged between 5 and >100 [7]. Simultaneously, arsenic hyperaccumulation in P. vittata was discovered separately in populations growing in an arsenic sulfide mine in Hunan Province, China [89][62]. Since then, other arsenic-hyperaccumulating plants have been identified, most of them belonging to the fern family, and more specifically to the Pteris genus [9]. However, not all Pteris species hyperaccumulate arsenic [90,91][63][64]. Known arsenic-hyperaccumulating ferns include many varieties of Pteris cretica [90,91[63][64][65][66][67][68][69],92,93,94,95,96], Pityrogramma calomelanos [97[70][71],98], Pteris longifolia [94][67], Pteris umbrosa [90[63][67][72],94,99], many varieties of Pteris multifida [91[64][65],92], Pteris biaurita L., Pteris quadriaurita Retz and Pteris ryukyuensis Tagawa [95][68], Pteris aspericaulis, Pteris fauriei, and Pteris oshimensis [91][64]. Zhao et al. [94][67] suggested that arsenic hyperaccumulation is a constitutive property in P. vittata (i.e., it is expressed in all members of the species regardless of the presence of arsenic in the soil), similarly to what was proposed for hyperaccumulation of metals generally [100][73], and for zinc and cadmium in Arabidopsis halleri and Thlaspi caerulescens specifically [101][74]. The constitutive property of arsenic hyperaccumulation was later revealed in populations of P. multifida, P. oshimensis and P. cretica var. nervosa and confirmed in P. vittata [91][64]. P. vittata is the most studied of the above ferns and is considered a model arsenic-hyperaccumulating plant [102,103][75][76].

3.3. Arsenic Hyperaccumulation in P. vittata

The mechanisms of arsenic tolerance, translocation and transformation in P. vittata have been extensively reviewed [9,25,26][9][77][78] and will be discussed here briefly in regard to implications for arsenic cycling in the whole soil-water-plant system. P. vittata absorbs arsenic from soil through its roots, which are primarily found in the 0–10 cm soil depth interval [104][79]. P. vittata primarily takes up arsenate and only limited arsenite, with the rate of arsenate uptake being 10 times that of arsenite uptake [105][80]. Like many plants, P. vittata takes up arsenate, a chemical analogue of phosphate, through the phosphate intake pathway, specifically through phosphate transporters in the root plasmalemma [82,105][55][80]. Arsenite uptake is also efficient and occurs through an active transport process [106][81]. P. vittata translocates and sequesters most accumulated arsenic in its pinnae [107][82], though arsenic translocation decreases under metal stress [108][83] and the rhizome can be a secondary storage organ when soil arsenic is highly available [104][79]. In pinnae, arsenic is compartmentalized in the vacuoles of pinnae epidermal cells [107][82], located on pinnae surfaces as crystalline deposits [109][84], and in trichomes on pinnae surfaces [110][85]. Between 47 and 94% of the arsenic in P. vittata fronds is present as arsenite and the rest as arsenate [7,107,111,112][7][82][86][87]. Indeed, during arsenic translocation in the fern, arsenate is reduced to arsenite [7], although there is disagreement about whether reduction occurs in roots [113][88], stipes [114][89] and/or pinnae [115][90]. Arsenite reoxidation was found in older fronds 18 weeks of age [112][87] and in senesced fronds [103][76].

3.4. Mechanisms for Arsenic Release from Soil

Arsenic uptake, and therefore hyperaccumulation, is likely linked to nutrient uptake in P. vittata. According to the phosphorus starvation theory, arsenic could be released from soil and taken up into the fern as a byproduct of rhizosphere-based nutrient scavenging processes [82,116][55][91]. In response to nutrient deficits [117][92], P. vittata likely releases root exudates [14,118,119,120][14][93][94][95] that mobilize phosphorus, iron, and arsenic from soil through ligand-enhanced dissolution of iron minerals [118,121,122][93][96][97]. P. vittata exudates include oxalic (C2H2O4), malic (C4H6O5), and phytic (C6H18O24P6) acids [14,119,123][14][94][98]. Oxalic and malic acids are common root exudates across plant communities [124][99], and oxalic acid is a well-known effective metal complexer [125,126][100][101]. Phytic acid, also a metal complexer [127][102] is less well-known as a root exudate but is released by fern roots [119,123][94][98]. Iron-oxalate and -phytate complexes lead to dissolution of iron oxides [128][103]. Both oxalic and phytic acid supplied hydroponically to P. vittata lead to release of arsenic from iron oxides and to higher P. vittata frond arsenic concentrations [123,128][98][103], but phytic acid could be more important to arsenic uptake in the fern [128][103]. P. vittata produced 4 to 7 times more phytic acid than oxalic acid [119][94], phytic acid released 1.2 to 50 times more arsenic from FeAsO4 than oxalic acid [119[94][98],123], and P. vittata frond arsenic concentrations were 3–10 times higher when phytate compared to oxalate was supplied [128][103]. The ability to sustain phytic acid production in the presence of arsenic could be a characteristic of arsenic tolerance in P. vittata, as phytic acid release from non-hyperaccumulating ferns decreased in the presence of arsenic [119,123][94][98]. The importance of root exudates to P. vittata arsenic uptake suggests the rhizosphere is a key zone for arsenic phytoextraction. Indeed, 66–95% of arsenic accumulated in P. vittata was shown to be extracted from rhizosphere soils, depending on soil texture, based on calculations of the mass of arsenic taken up in the fern through transpiration of bulk soil porewater [129][104]. The importance of rhizosphere processes suggests that is primarily rhizosphere, not bulk, soils that are effectively phytoextracted. Even if arsenic uptake in the fern is closely associated with root exudate activity, the link between exudate compounds and nutrient budgets, especially phosphorus and iron, in P. vittata needs further elucidation. P. vittata frond phosphorus concentrations increased when ferns were supplied with higher (500–1000 μM) [123,130][98][105] but not lower (50 μM) [128,130][103][105] concentrations of phytic acid. It remains unclear how phytic acid release relates to P. vittata phosphorus budgets. P. vittata could use externally supplied phytic acid as a phosphorus source [123][98]. Phytase present in P. vittata root exudates [14,123][14][98] could help the fern recover released phytic acid [131][106]. Iron and arsenic cycling in P. vittata are likely related, given that arsenic in oxic soils is usually associated with iron minerals. Frond iron concentrations increased when ferns were supplied with phytic or oxalic acid in some cases [123][98] but not in others [128,130][103][105]. In addition to acting through ligand-exchange mechanisms, root exudates could affect rhizosphere pH and therefore arsenic availability. P. vittata rhizosphere pH, a key factor in arsenic release from iron oxides, is not well understood. Compared to bulk soil, P. vittata rhizosphere pH has been found to be lower [132][107], similar [118][93], or higher [120,133][95][108]. Counterintuitively, decreasing pH below neutral would increase iron oxyhydroxide solubility [134][109] but also increase the amount of arsenic sorbed [34][110]. pH also affects root exudate behavior. Oxalate has a higher affinity for iron at lower pH [135][111], so decreasing pH could increase ligand-enhanced dissolution of iron oxides, increasing arsenic release. Alternately, oxalic and acetic acid release was shown to increase soil pH adjacent to artificial roots, possibly due to mineral dissolution or dissimilatory metal reduction [125][100], which would also increase arsenic release.

References

  1. Mitchell, V.L. Health Risks Associated with Chronic Exposures to Arsenic in the Environment. Rev. Mineral. Geochem. 2014, 79, 435–449.
  2. Oremland, R.S.; Stolz, J.F. The ecology of arsenic. Science 2003, 300, 939–944.
  3. Ratnaike, R.N. Acute and chronic arsenic toxicity. Postgrad. Med. J. 2003, 79, 391–396.
  4. Agency for Toxic Substances and Disease Registry. Substance Priority List. U.S. Department of Health and Human Services. Available online: https://www.atsdr.cdc.gov/spl/#2019spl (accessed on 17 November 2022).
  5. Tack, F.M.G.; Meers, E. Assisted Phytoextraction: Helping Plants to Help Us. Elements 2010, 6, 383–388.
  6. Vélez-Gavilán, J. Pteris vittata (Chinese ladder brake fern). In Invasive Species Compendium; CABI: Wallingford, UK, 2020.
  7. Ma, L.Q.; Komar, K.M.; Tu, C.; Zhang, W.H.; Cai, Y.; Kennelley, E.D. A fern that hyperaccumulates arsenic—A hardy, versatile, fast-growing plant helps to remove arsenic from contaminated soils. Nature 2001, 409, 579.
  8. Wan, X.M.; Lei, M.; Chen, T.B. Cost-benefit calculation of phytoremediation technology for heavy-metal-contaminated soil. Sci. Total Environ. 2016, 563, 796–802.
  9. Xie, Q.E.; Yan, X.L.; Liao, X.Y.; Li, X. The Arsenic Hyperaccumulator Fern Pteris vittata L. Environ. Sci. Technol. 2009, 43, 8488–8495.
  10. Cantamessa, S.; Massa, N.; Gamalero, E.; Berta, G. Phytoremediation of a Highly Arsenic Polluted Site, Using Pteris vittata L. and Arbuscular Mycorrhizal Fungi. Plants 2020, 9, 211.
  11. Kertulis-Tartar, G.M.; Ma, L.Q.; Tu, C.; Chirenje, T. Phytoremediation of an arsenic-contaminated site using Pteris vittata L.: A two-year study. Int. J. Phytoremediation 2006, 8, 311–322.
  12. Matzen, S.; Fakra, S.; Nico, P.; Pallud, C. Pteris vittata arsenic accumulation only partially explains soil arsenic depletion during field-scale phytoextraction. Soil Syst. 2020, 4, 71.
  13. Niazi, N.K.; Singh, B.; Van Zwieten, L.; Kachenko, A.G. Phytoremediation of an arsenic-contaminated site using Pteris vittata L. and Pityrogramma calomelanos var austroamericana: A long-term study. Environ. Sci. Pollut. Res. 2012, 19, 3506–3515.
  14. Lessl, J.T.; Ma, L.Q. Sparingly-Soluble Phosphate Rock Induced Significant Plant Growth and Arsenic Uptake by Pteris vittata from Three Contaminated Soils. Environ. Sci. Technol. 2013, 47, 5311–5318.
  15. da Silva, E.B.; Lessl, J.T.; Wilkie, A.C.; Liu, X.; Liu, Y.; Ma, L.Q. Arsenic removal by As-hyperaccumulator Pteris vittata from two contaminated soils: A 5-year study. Chemosphere 2018, 206, 736–741.
  16. Chen, T.-b.; Wei, C.; Huang, Z.; Huang, Q.; Lu, Q.; Fan, Z. Effect of phosphorus on arsenic accumulation in As-hyperaccumulator Pteris vittata L. and its implication. Chin. Sci. Bull. 2002, 47, 902–905.
  17. Cao, X.; Ma, L.Q.; Shiralipour, A. Effects of compost and phosphate amendments on arsenic mobility in soils and arsenic uptake by the hyperaccumulator, Pteris vittata L. Environ. Pollut. 2003, 126, 157–167.
  18. Tu, S.; Ma, L.Q. Interactive effects of pH, arsenic and phosphorus on uptake of As and P and growth of the arsenic hyperaccumulator Pteris vittata L. under hydroponic conditions. Environ. Exp. Bot. 2003, 50, 243–251.
  19. Fayiga, A.O.; Ma, L.Q. Using phosphate rock to immobilize metals in soil and increase arsenic uptake by hyperaccumulator Pteris vittata. Sci. Total Environ. 2006, 359, 17–25.
  20. Caille, N.; Swanwick, S.; Zhao, F.J.; McGrath, S.P. Arsenic hyperaccumulation by Pteris vittata from arsenic contaminated soils and the effect of liming and phosphate fertilisation. Environ. Pollut. 2004, 132, 113–120.
  21. Shelmerdine, P.A.; Black, C.R.; McGrath, S.P.; Young, S.D. Modelling phytoremediation by the hyperaccumulating fern, Pteris vittata, of soils historically contaminated with arsenic. Environ. Pollut. 2009, 157, 1589–1596.
  22. Lei, M.; Wan, X.; Guo, G.; Yang, J.; Chen, T. Phytoextraction of arsenic-contaminated soil with Pteris vittata in Henan Province, China: Comprehensive evaluation of remediation efficiency correcting for atmospheric depositions. Environ. Sci. Pollut. Res. Int. 2018, 25, 124–131.
  23. Neugschwandtner, R.W.; Tlustoš, P.; Komárek, M.; Száková, J. Phytoextraction of Pb and Cd from a contaminated agricultural soil using different EDTA application regimes: Laboratory versus field scale measures of efficiency. Geoderma 2008, 144, 446–454.
  24. Gerhardt, K.E.; Gerwing, P.D.; Greenberg, B.M. Opinion: Taking phytoremediation from proven technology to accepted practice. Plant Sci. 2017, 256, 170–185.
  25. Warren, G.P.; Alloway, B.J. Reduction of arsenic uptake by lettuce with ferrous sulfate applied to contaminated soil. J. Environ. Qual. 2003, 32, 767–772.
  26. Komarek, M.; Vanek, A.; Ettler, V. Chemical stabilization of metals and arsenic in contaminated soils using oxides—A review. Environ. Pollut. 2013, 172, 9–22.
  27. Álvarez-Ayuso, E.; Murciego, A. Stabilization methods for the treatment of weathered arsenopyrite mine wastes: Arsenic immobilization under selective leaching conditions. J. Clean. Prod. 2021, 283, 125265.
  28. Moore, T.J.; Rightmire, C.M.; Vempati, R.K. Ferrous Iron Treatment of Soils Contaminated with Arsenic-Containing Wood-Preserving Solution. J. Soil Contam. 2000, 9, 375–405.
  29. Hartley, W.; Edwards, R.; Lepp, N.W. Arsenic and heavy metal mobility in iron oxide-amended contaminated soils as evaluated by short- and long-term leaching tests. Environ. Pollut. 2004, 131, 495–504.
  30. Hartley, W.; Lepp, N.W. Effect of in situ soil amendments on arsenic uptake in successive harvests of ryegrass (Lolium perenne cv Elka) grown in amended As-polluted soils. Environ. Pollut. 2008, 156, 1030–1040.
  31. Warren, G.P.; Alloway, B.J.; Lepp, N.W.; Singh, B.; Bochereau, F.J.M.; Penny, C. Field trials to assess the uptake of arsenic by vegetables from contaminated soils and soil remediation with iron oxides. Sci. Total Environ. 2003, 311, 19–33.
  32. Bleeker, P.M.; Assuncao, A.G.L.; Tiega, P.M.; de Koe, T.; Verkleij, J. Revegetation of the acidic, As contaminated Jales mine spoil tips using a combination of spoil amendments and tolerant grasses. Sci. Total Environ. 2002, 300, 1–13.
  33. Baragano, D.; Forjan, R.; Welte, L.; Gallego, J.L.R. Nanoremediation of As and metals polluted soils by means of graphene oxide nanoparticles. Sci. Rep. 2020, 10, 1896.
  34. Kumpiene, J.; Ore, S.; Renella, G.; Mench, M.; Lagerkvist, A.; Maurice, C. Assessment of zerovalent iron for stabilization of chromium, copper, and arsenic in soil. Environ. Pollut. 2006, 144, 62–69.
  35. Mench, M.; Vangronsveld, J.; Beckx, C.; Ruttens, A. Progress in assisted natural remediation of an arsenic contaminated agricultural soil. Environ. Pollut. 2006, 144, 51–61.
  36. Ascher, J.; Ceccherini, M.T.; Landi, L.; Mench, M.; Pietramellara, G.; Nannipieri, P.; Renella, G. Composition, biomass and activity of microflora, and leaf yields and foliar elemental concentrations of lettuce, after in situ stabilization of an arsenic-contaminated soil. Appl. Soil Ecol. 2009, 41, 351–359.
  37. Sanchez, A.G.; Alvarez-Ayuso, E.; Rodriguez-Martin, F. Sorption of As(V) by some oxyhydroxides and clay minerals. Application to its immobilization in two polluted mining soils. Clay Miner. 2002, 37, 187–194.
  38. Nielsen, S.S.; Petersen, L.R.; Kjeldsen, P.; Jakobsen, R. Amendment of arsenic and chromium polluted soil from wood preservation by iron residues from water treatment. Chemosphere 2011, 84, 383–389.
  39. Gonzalez, V.; Garcia, I.; Del Moral, F.; Simon, M. Effectiveness of amendments on the spread and phytotoxicity of contaminants in metal-arsenic polluted soil. J. Hazard. Mater. 2012, 205, 72–80.
  40. Hartley, W.; Lepp, N.W. Remediation of arsenic contaminated soils by iron-oxide application, evaluated in terms of plant productivity, arsenic and phytotoxic metal uptake. Sci. Total Environ. 2008, 390, 35–44.
  41. Puschenreiter, M.; Horak, O.; Friesl, W.; Hartl, W. Low-cost agricultural measures to reduce heavy metal transfer into the food chain—A review. Plant Soil Environ. 2005, 51, 1–11.
  42. Kumpiene, J.; Lagerkvist, A.; Maurice, C. Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments—A review. Waste Manag. 2008, 28, 215–225.
  43. Oncu, G.; Reiser, M.; Kranert, M. Aerobic in situ stabilization of Landfill Konstanz Dorfweiher: Leachate quality after 1 year of operation. Waste Manag. 2012, 32, 2374–2384.
  44. Reisinger, H.J.; Burris, D.R.; Hering, J.G. Remediating Subsurface Arsenic Contamination with Monitored Natural Attenuation. Environ. Sci. Technol. 2005, 39, 458–464.
  45. Venegas-Rioseco, J.; Ginocchio, R.; Ortiz-Calderon, C. Increase in Phytoextraction Potential by Genome Editing and Transformation: A Review. Plants 2021, 11, 86.
  46. Brooks, R.R.; Lee, J.; Reeves, R.D.; Jaffre, T. Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J. Geochem. Explor. 1977, 7, 49–57.
  47. van der Ent, A.; Baker, A.J.M.; Reeves, R.D.; Pollard, A.J.; Schat, H. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil 2013, 362, 319–334.
  48. Baker, A.J.M. Accumulators and excluders-strategies in the response of plants to heavy metals. J. Plant Nutr. 1981, 3, 643–654.
  49. Maestri, E.; Marmiroli, M.; Visioli, G.; Marmiroli, N. Metal tolerance and hyperaccumulation: Costs and trade-offs between traits and environment. Environ. Exp. Bot. 2010, 68, 1–13.
  50. Chaney, R.L.; Angle, J.S.; Broadhurst, C.L.; Peters, C.A.; Tappero, R.V.; Sparks, D.L. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J. Environ. Qual. 2007, 36, 1429–1443.
  51. McGrath, S.P.; Zhao, F.J.; Lombi, E. Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 2001, 232, 207–214.
  52. Pollard, A.J.; Baker, A.J.M. Deterrence of herbivory by zinc hyperaccumulation in Thlaspi caerulescens (Brassicaceae). New Phytol. 1997, 135, 655–658.
  53. Jiang, R.F.; Ma, D.Y.; Zhao, F.J.; McGrath, S.P. Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytol. 2005, 167, 805–814.
  54. Morris, C.; Grossl, P.R.; Call, C.A. Elemental allelopathy: Processes, progress, and pitfalls. Plant Ecol. 2008, 202, 1–11.
  55. Meharg, A.A.; Hartley-Whitaker, J. Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol. 2002, 154, 29–43.
  56. Porter, E.K.; Peterson, P.J. Arsenic accumulation by plants on mine waste (United Kingdom). Sci. Total Environ. 1975, 4, 365–371.
  57. de Koe, T. Agrostis castellana and Agrostis delicatula on heavy metal and arsenic enriched sites in NE Portugal. Sci. Total Environ. 1994, 145, 103–109.
  58. Bech, J.; Poschenrieder, C.; Llugany, M.; Barceló, J.; Tume, P.; Tobias, F.J.; Barranzuela, J.L.; Vásquez, E.R. As and heavy metal contamination of soil and vegetation around a copper mine in Northern Peru. Sci. Total Environ. 1997, 203, 83–91.
  59. Center for Aquatic and Invasive Plants. Pteris vittata Chinese Ladder Brake Fern. University of Florida/IFAS. Available online: https://plants.ifas.ufl.edu/plant-directory/pteris-vittata/ (accessed on 21 December 2021).
  60. Komar, K.M.; Ma, L.Q.; Rockwood, D.; Syed, A. Identification of arsenic tolerant and hyperaccumulating plants from arsenic contaminated soils in Florida. Agron. Abstr. 1998, 343, 20–67.
  61. Komar, K.M. Phytoremediation of Arsenic Contaminated Soils: Plant Identification and Uptake Enhancement. Ph.D. Thesis, University of Florida, Gainsville, FL, USA, 1999.
  62. Chen, T.B.; Wei, C.Y.; Huang, Z.; Huang, Q.; Lu, Q.; Fan, Z. Arsenic hyperaccumulator Pteris vittata L. and its arsenic accumulation. Chin. Sci. Bull. 2002, 47, 902–905.
  63. Meharg, A.A. Variation in arsenic accumulation—Hyperaccumulation in ferns and their allies. New Phytol. 2003, 157, 25–31.
  64. Wang, H.B.; Wong, M.H.; Lan, C.Y.; Baker, A.J.; Qin, Y.R.; Shu, W.S.; Chen, G.Z.; Ye, Z.H. Uptake and accumulation of arsenic by 11 Pteris taxa from southern China. Environ. Pollut. 2007, 145, 225–233.
  65. Wei, C.Y.; Wang, C.; Sun, X.; Wang, W.Y. Arsenic accumulation by ferns: A field survey in southern China. Environ. Geochem. Health 2007, 29, 169–177.
  66. Wei, C.Y.; Chen, T.B.; Huang, Z.; Zhang, X. Cretan brake (Pteris cretica L.): An arsenic accumulatting plant. Acta Ecol. Sin. 2002, 22, 777–778, (In Chinese with English Abstract).
  67. Zhao, F.J.; Dunham, S.J.; McGrath, S.P. Arsenic hyperaccumulation by different fern species. New Phytol. 2002, 156, 27–31.
  68. Srivastava, M.; Ma, L.Q.; Santos, J.A. Three new arsenic hyperaccumulating ferns. Sci. Total Environ. 2006, 364, 24–31.
  69. Feng, R.; Wei, C.; Tu, S.; Tang, S.; Wu, F. Simultaneous hyperaccumulation of arsenic and antimony in Cretan brake fern: Evidence of plant uptake and subcellular distributions. Microchem. J. 2011, 97, 38–43.
  70. Francesconi, K.; Visoottiviseth, P.; Sridokchan, W.; Goessler, W. Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos- a potential phytoremediator of arsenic-contaminated soils. Sci. Total Environ. 2002, 284, 27–35.
  71. Visoottiviseth, P.; Francesconi, K.; Sridokchan, W. The potential of Thai indigenous plant species for the phytoremediation of arsenic. Sci. Total Environ. 2002, 118, 453–461.
  72. Koller, C.E.; Patrick, J.W.; Rose, R.J.; Offler, C.E.; MacFarlane, G.R. Pteris umbrosa R. Br. as an arsenic hyperaccumulator: Accumulation, partitioning and comparison with the established As hyperaccumulator Pteris vittata. Chemosphere 2007, 66, 1256–1263.
  73. Pollard, A.J.; Dandridge, K.L.; Jhee, E.M. Ecological genetics and the evolution of trace element hyperaccumulation in plants. In Phytoremediation of Contaminated Soil and Water; Terry, N., Banuelos, G.S., Eds.; CRC Press: Boca Raton, FL, USA, 2000; Chapter 14.
  74. Baker, A.J.M.; Whiting, S.N. In search of the Holy Grail—A further step in understanding metal hyperaccumulation? New Phytol. 2002, 155, 1–4.
  75. Singh, N.; Ma, L.Q. Assessing plants for phytoremediation of arsenic contaminated soils. In Methods in Biotechnology Volume 23: Phytoremediation: Methods and Reviews; Willey, N., Ed.; Humana Press: Totowa, NJ, USA, 2007; Volume 23, pp. 319–347, Chapter 24.
  76. Wan, X.; Zeng, W.; Zhang, D.; Wang, L.; Lei, M.; Chen, T. Changes in the concentration, distribution, and speciation of arsenic in the hyperaccumulator Pteris vittata at different growth stages. Sci. Total Environ. 2022, 841, 156708.
  77. Rathinasabapathi, B.; Ma, L.Q.; Srivastava, M. Arsenic hyperaccumulating ferns and their application to phytoremediation. Floric. Ornam. Plant Biotechnol. 2006, 3, 304–311.
  78. Danh, L.T.; Truong, P.; Mammucari, R.; Foster, N. A critical review of the arsenic uptake mechanisms and phytoremediation potential of Pteris vittata. Int. J. Phytoremediation 2014, 16, 429–453.
  79. Liao, X.-Y.; Chen, T.-B.; Lei, M.; Huang, Z.-C.; Xiao, X.-Y.; An, Z.-Z. Root distributions and elemental accumulations of Pteris vittata from As-contaminated soils. Plant Soil 2004, 261, 109–116.
  80. Wang, J.R.; Zhao, F.J.; Meharg, A.A.; Raab, A.; Feldmann, J.; McGrath, S.P. Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol. 2002, 130, 1552–1561.
  81. Wang, X.; Ma, L.Q.; Rathinasabapathi, B.; Cai, Y.; Liu, Y.G.; Zeng, G.M. Mechanisms of efficient arsenite uptake by arsenic hyperaccumulator Pteris vittata. Environ. Sci. Technol. 2011, 45, 9719–9725.
  82. Lombi, E.; Zhao, F.J.; Fuhrmann, M.; Ma, L.Q.; Mcgrath, S.P. Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol. 2002, 156, 195–203.
  83. An, Z.Z.; Huang, Z.C.; Lei, M.; Liao, X.Y.; Zheng, Y.M.; Chen, T.B. Zinc tolerance and accumulation in Pteris vittata L. and its potential for phytoremediation of Zn- and As-contaminated soil. Chemosphere 2006, 62, 796–802.
  84. Datta, R.; Das, P.; Tappero, R.; Punamiya, P.; Elzinga, E.; Sahi, S.; Feng, H.; Kiiskila, J.; Sarkar, D. Evidence for exocellular Arsenic in Fronds of Pteris vittata. Sci. Rep. 2017, 7, 2839.
  85. Li, W.; Chen, T.B.; Lei, M. Role of trichome of Pteris vittata L. in arsenic hyperaccumulation. Sci. China 2005, 48, 148–154.
  86. Zhang, W.; Cai, Y.; Tu, C.; Ma, L.Q. Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Sci. Total Environ. 2002, 300, 167–177.
  87. Tu, C.; Ma, L.Q.; Zhang, W.; Cai, Y.; Harris, W.G. Arsenic species and leachability in the fronds of the hyperaccumulator Chinese brake (Pteris vittata L.). Environ. Pollut. 2003, 124, 223–230.
  88. Vetterlein, D.; Wesenberg, D.; Nathan, P.; Bräutigam, A.; Schierhorn, A.; Mattusch, J.; Jahn, R. Pteris vittata—Revisited: Uptake of As and its speciation, impact of P, role of phytochelatins and S. Environ. Pollut. 2009, 157, 3016–3024.
  89. Webb, S.M.; Gaillard, J.-F.; Ma, L.Q.; Tu, C. XAS speciation of arsenic in a hyper-accumulating fern. Environ. Sci. Technol. 2003, 37, 754–760.
  90. Pickering, I.J.; Gumaelius, L.; Harris, H.H.; Prince, R.C.; Hirsch, G.; Banks, J.A.; Salt, D.E.; George, G.N. Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ. Sci. Technol. 2006, 40, 5010–5014.
  91. Audet, P. Examining the ecological paradox of the ‘mycorrhizal-metal-hyperaccumulators’. Arch. Agron. Soil Sci. 2013, 59, 549–558.
  92. Marschener, H. Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crops Res. 1998, 56, 203–207.
  93. Fitz, W.J.; Wenzel, W.W.; Zhang, H.; Nurmi, J.; Štipek, K.; Fischerova, Z.; Schweiger, P.; Köllensperger, G.; Ma, L.Q.; Stingeder, G. Rhizosphere characteristics of the arsenic hyperaccumulator Pteris vittata L. and monitoring of phytoremoval efficiency. Environ. Sci. Technol. 2003, 37, 5008–5014.
  94. Tu, S.; Ma, L.; Luongo, T. Root exudates and arsenic accumulation in arsenic hyperaccumulating Pteris vittata and non-hyperaccumulating Nephrolepis exaltata. Plant Soil 2004, 258, 9–19.
  95. Gonzaga, M.I.S.; Santos, J.A.; Ma, L.Q. Arsenic chemistry in the rhizosphere of Pteris vittata L. and Nephrolepis exaltata L. Environ. Pollut. 2006, 143, 254–260.
  96. Furrer, G.; Stumm, W. The coordination chemistry of weathering- I. Dissolution kinetics of δ-Al2O3 and BeO. Geochem. Et Cosmochim. Acta 1986, 50, 1847–1860.
  97. Reichard, P.U.; Kretzschmar, R.; Kraemer, S.M. Dissolution mechanisms of goethite in the presence of siderophores and organic acids. Geochim. Et Cosmochim. Acta 2007, 71, 5635–5650.
  98. Liu, X.; Fu, J.W.; Guan, D.X.; Cao, Y.; Luo, J.; Rathinasabapathi, B.; Chen, Y.; Ma, L.Q. Arsenic Induced Phytate Exudation, and Promoted FeAsO4 Dissolution and Plant Growth in As-Hyperaccumulator Pteris vittata. Environ. Sci. Technol. 2016, 50, 9070–9077.
  99. Jones, D.L. Organic acids in the rhizosphere—A critical review. Plant Soil 1998, 205, 25–44.
  100. Keiluweit, M.; Bougoure, J.J.; Nico, P.S.; Pett-Ridge, J.; Weber, P.K.; Kleber, M. Mineral protection of soil carbon counteracted by root exudates. Nat. Clim. Chang. 2015, 5, 588–595.
  101. Chen, J.; Shafi, M.; Wang, Y.; Wu, J.; Ye, Z.; Liu, C.; Zhong, B.; Guo, H.; He, L.; Liu, D. Organic acid compounds in root exudation of Moso Bamboo (Phyllostachys pubescens) and its bioactivity as affected by heavy metals. Environ. Sci. Pollut. Res. Int. 2016, 23, 20977–20984.
  102. Shang, C.; Stewart, J.W.B.; Huang, P.M. pH effect on kinetics of adsorption of organic and inorganic phosphates by short-range ordered aluminum and iron precipitates. Geoderma 1992, 53, 1–14.
  103. Liu, X.; Fu, J.W.; Da Silva, E.; Shi, X.X.; Cao, Y.; Rathinasabapathi, B.; Chen, Y.; Ma, L.Q. Microbial siderophores and root exudates enhanced goethite dissolution and Fe/As uptake by As-hyperaccumulator Pteris vittata. Environ. Pollut. 2017, 223, 230–237.
  104. Matzen, S.L.; Lobo, G.P.; Fakra, S.C.; Kakouridis, A.; Nico, P.S.; Pallud, C.E. Arsenic hyperaccumulator Pteris vittata shows reduced biomass in soils with high arsenic and low nutrient availability, leading to increased arsenic leaching from soil. Sci. Total Environ. 2022, 818, 151803.
  105. Liu, X.; Fu, J.W.; Tang, N.; da Silva, E.B.; Cao, Y.; Turner, B.L.; Chen, Y.; Ma, L.Q. Phytate induced arsenic uptake and plant growth in arsenic-hyperaccumulator Pteris vittata. Environ. Pollut. 2017, 226, 212–218.
  106. Brinch-Pedersen, H.; Sorensen, L.D.; Holm, P.B. Engineering crop plants- getting a handle on phosphate. Trends Plant Sci. 2002, 7, 118–125.
  107. Gonzaga, M.I.; Ma, L.Q.; Santos, J.A.; Matias, M.I. Rhizosphere characteristics of two arsenic hyperaccumulating Pteris ferns. Sci. Total Environ. 2009, 407, 4711–4716.
  108. Das, S.; Chou, M.L.; Jean, J.S.; Yang, H.J.; Kim, P.J. Arsenic-enrichment enhanced root exudates and altered rhizosphere microbial communities and activities in hyperaccumulator Pteris vittata. J. Hazard Mater. 2017, 325, 279–287.
  109. Hem, J.D. Chemical factors that influence the availability of iron and manganese in aqueous systems. Geol. Soc. Am. Bull. 1972, 83, 443–450.
  110. Dixit, S.; Hering, J.G. Comparison of arsenic(V) and arsenic(III) Sorption onto Iron Oxide Minerals: Implications for Arsenic Mobility. Environ. Sci. Technol. 2003, 37, 4182–4189.
  111. Kraemer, S.M. Iron oxide dissolution and solubility in the presence of siderophores. Aquat. Sci.—Res. Across Boundaries 2004, 66, 3–18.
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