Sharma et al. 2023 — Phytoremediation mechanisms and metal-binding proteins for heavy metal soil remediation

Sharma and colleagues review the four phytoremediation strategies used to remove heavy metals from contaminated soils — phytoextraction, phytostabilization, phytovolatilization, and rhizofiltration — and the plant molecular machinery (metal-binding proteins, transporters, and chelators) that underlies metal tolerance and accumulation. The review tabulates hyperaccumulator plant species reported in the primary literature for Zn, Cu, Ni, Cd, Pb, As, Hg, and Cr (Table 1), the plant proteins and genes involved in metal handling across model and crop species (Table 2), and plant–microbe consortia tested for assisted phytoremediation (Table 3). Biotechnological enhancement via genetic modification, biochar amendment, chelating agents, and plant growth-promoting rhizobacteria is discussed as a route to improve phytoextraction efficiency in candidate cereal and dicot species. The paper is open-access (CC BY) in Frontiers in Plant Science.

Key numbers

The paper is a narrative review and reports no original experimental measurements. The quantitative content consists of three summary tables aggregating values from primary literature, supplied with source attribution but not pooled or synthesized further by the authors.

• Table 1 — Hyperaccumulator BCF and TF values (page 3). Selected entries: Brassica juncea on Ni-spiked soil BCF 6.71; Tagetes erecta on Cd/Zn soil BCF 9.35 (Cd) and 10.5 (Zn) with TF 1.77 (Cd) and 0.24 (Zn); Helianthus annuus on Cu soil BCF 0.99, TF 0.71; Pterocypsela laciniata on Cd soil BCF 4.55, TF 3.73; Lantana camara on Cd soil BCF 4.78, TF 4.90; Typha angustifolia on Ni/Pb water BCF 1.42 (Ni)/1.03 (Pb), TF 1.29 (Ni)/4.90 (Pb); Eichhornia crassipes on the same matrix BCF 1.83 (Ni)/0.88 (Pb), TF 7.63 (Ni)/1.73 (Pb); Hydrocotyle umbellata on 50 mg/L Cr BCF 37.8, TF 0.191. Initial soil concentrations listed in the metal column are the spike levels reported by the cited primary studies (e.g., Cd 5–100 mg/kg for Malva rotundifolia; As 468/442/304 mg/kg for Pteridium aquilinum and three co-occurring species).
• Table 2 — Plant proteins and genes in phytoremediation (page 6). Lists NRAMP genes (AtNramp1/3/4/6 in Arabidopsis, OsNramp1/2/5 in rice, HvNramp5 in barley) associated with Cd handling; phytochelatin synthase (PCS1) in Sesbania rostrata, Nicotiana tabacum, Arabidopsis, and Ipomoea pescaprae for Cd, Zn, As; metallothionein-and-PCS combinations (MT2 and PCS1) in Azolla pinnata and A. filiculoides for Ni, Zn, Cu, Cd; mercury-specific transgenes (MerC-SYP121 fusion in Arabidopsis; PtABCC1 in Arabidopsis and Populus tomentosa); Pb-tolerance proteins (NtCBP4 and AtCNGC1; SmNhaD Na⁺/H⁺ antiporter in Salvinia minima); Cr-tolerance constructs in Nicotiana langsdorffii (glucocorticoid receptor + rolC).
• Table 3 — Plant–microbe consortia for phytoremediation (page 8). Reports remediation percentages from primary literature. Selected entries: Zea mays with Serratia marcescens Bac156 and Pseudomonas sp. Bac138 for Hg — 47.16% and 62.42% removal via endophytic volatilization; Medicago sativa with Bacillus subtilis for Cd — 139% phytoextraction enhancement vs control; Solanum nigrum with Glomus versiforme (mycorrhizal) for Cd — 90.0% phytoextraction; Vetiveria zizanioides with Bacillus cereus for Cr(VI)/Ni/Zn/Cu/Cd — 130–211% Cr(VI), 31–40% Ni, 30–61% Zn, 65–178% Cu, 84–107% Cd phytostabilization; Pelargonium hortorum with Aspergillus flavus and Microbacterium paraoxydans — two- to fivefold more Pb uptake than control.

Additional in-text figures cited from primary sources:

• Soil-remediation cost: phytoremediation ≈ US$60,000–1,000,000 per acre vs four to six times that for physical remediation (Salt et al. 1995, cited; page 2).
• Approximately 450–500 plant species have been identified as hyperaccumulators (Chaudhary et al. 2018, cited; page 3).
• Lemna valdiviana can extract up to 82% of As from contaminated water (Souza et al. 2019, cited; page 4).
• Bixa orellana can accumulate 82.8% of Cr(VI) and 40.4% of As(III) starting from 3 and 6 ppm respectively (Kumar et al. 2022b, cited; page 4).
• Arundo donax with Stenotrophomonas maltophilia + Agrobacterium volatilized ≈75% of an initial 20 mg/L As, with ≈25% retained in sand and 0.15% in plant tissue (Guarino et al. 2020, cited; page 4).
• Biochar amendment at 5% (w/w) reduced extractable Cd, Cu, Pb, and Zn in polluted soil by 52%, 46%, 29%, and 36% respectively (Chen et al. 2018, cited; page 7). A separate citation reports 5% (w/w) bamboo, rice-straw, and biochar amendment reduced extractable Cd, Cu, Pb, and Zn in polluted soil (Lu et al. 2017, cited; page 7) — no per-metal reduction percentage is given for that citation. The paper also states that biochar functional-group contact with heavy metals is responsible for 38–42% of total Pb²⁺ adsorbed (page 7; mechanism statement, not a four-metal reduction figure).
• Rutin application to Amaranthus hypochondriacus enhanced Cd phytoextraction by 219–260% (Kang et al. 2022, cited; page 7).
• Typha angustifolia Cd and Zn uptake: 4,941.1–14,109.4 mg per plant (Cd) and 14,039.3–59,360.8 mg per plant (Zn) — Woraharn et al. 2021, cited; page 4.

Sample sizes and analytical detection limits are not stated for the review-level summary; refer to the primary citations for those parameters.

Methods (brief)

Narrative review; no systematic search protocol, inclusion/exclusion criteria, or quantitative pooling is described. The authors organize the literature around (i) the four phytoremediation mechanisms, (ii) the molecular machinery of plant metal handling (MTs, PCs, HMAs, NRAMPs, ZIP, ABCC, CAXs), (iii) crop-specific MBP studies in rice, maize, wheat, and barley, and (iv) biotechnological enhancement via genetic engineering, biochar, chelating agents, and plant growth-promoting rhizobacteria. Hyperaccumulator selection criteria are restated as TF > 1 and BCF > 1 (Mazumdar and Das 2015, cited). No primary lab work, no instrument vendor/model, no reference material, no LOD/LOQ statements — those parameters belong to the cited primary studies.

Phytoremediation strategies covered

Phytoextraction. Plants uptake metals from soil, translocate them to harvestable aboveground biomass, and the biomass is removed and disposed of by composting, compression, dehydration, or thermal decomposition. The paper’s selection criteria for phytoextraction species are metal tolerance, high biomass production, active accumulation in harvestable parts, short life cycle, broad distribution, and TF > 1. The hyperaccumulators tabulated in Table 1 span Brassicaceae (Sinapis arvensis, Brassica campestris, Brassica juncea), Tagetes erecta, Helianthus annuus, Pinus sylvestris, Quercus robur, Malva rotundifolia, Abelmoschus manihot, Pterocypsela laciniata, Lantana camara, Typha angustifolia, Eichhornia crassipes, Plectranthus sp., Capsicum annuum, Pteridium aquilinum, Brachiaria mutica, Leptochloa fusca, Canna indica, and Hydrocotyle umbellata.

Phytostabilization. Plants reduce metal mobility in the rhizosphere via root exudates that precipitate or adsorb metals, decreased leaching, organic-matter binding, and improved aerobic conditions in the root zone. Examples discussed: organic acid-producing metal-tolerant beneficial rhizobacteria with biogas residues for Cd in maize; intercropping Thalia dealbata (alligator flag) with rice for mild-Cd field remediation; Scariola orientalis on Zn/Fe-polluted soil; Tetraena qataranse in arid-zone soils for Cd/Cr/Cu/Ni.

Phytovolatilization. Plants absorb metals and release them as volatile, less hazardous species via transpiration. Discussed primarily for Hg and Se; Hg-volatilizing examples include muskgrass (Chara canescens), Indian mustard (Brassica juncea), and Arabidopsis thaliana. Arundo donax with Stenotrophomonas maltophilia and Agrobacterium volatilized ≈75% of 20 mg/L As. The authors note that plants do not methylate inorganic As in detectable amounts; volatile trimethylated/dimethylated As species are largely root-sourced (Jia et al. 2012, cited). Se exists in nature in five oxidation states; selenate (+6) is taken up via sulfate transporters and converted to volatile DMSe, DMDSe, DMSeS, and methaneselenol.

Rhizofiltration (hydraulic control). Plant roots absorb and sequester metal pollutants from water. Zea mays showed 12% decrease in Hg, 32% in Pb, and 30% in Cr (Benavides et al. 2018, cited). Typha angustifolia with high BCF and low TF is cited as an excellent rhizofiltration candidate. Pistia (water lettuce), Eichhornia (water hyacinth), and Azolla (water fern) are discussed as common aquatic phytoremediators with different specificity profiles.

Metal-binding proteins and transporters

The review’s most detailed content is the molecular machinery of plant metal handling.

• Metallothioneins (MTs). Cysteine-rich low-molecular-weight chelators. The plant MT superfamily includes four subfamilies (p1/p2/p3/pec). The paper enumerates MT1, MT2, MT3, MT4a (Ec-2), MT4b (Ec-1), and Ec-1 in Cicer arietinum, Arabidopsis thaliana, Musa acuminate, A. thaliana, and T. aestivum. The plant MT family was discovered roughly 30 years ago and is less well characterized than its animal counterpart.
• Phytochelatins (PCs). Glutathione-derived enzymatically synthesized peptides with structural formula (γ-Glu-Cys)n-Aa where n = 2–11. Primary response to Cd and As exposure; PC–metal complexes are sequestered in vacuoles via ABCC1/ABCC2 transporters. PC4, PC6, PC7 species accumulated more Cd than the lower-polymerization PC2, PC3 in L. minor.
• Heavy-metal ATPases (HMAs). P-type ATPases that transport metals across membranes. The paper specifically discusses OsHMA3 (vacuolar Cd sequestration in rice) and OsHMA2 (located in root pericycle cells; mediates Cd translocation from root to shoot).
• NRAMP transporters. Natural resistance-associated macrophage proteins. The paper lists OsNramp5 (rice; key Cd absorption transporter, root tip-localized) and AtNramp1/3/4/6, OsNramp1/2, HvNramp5 (barley) — all linked to Cd handling.
• ZIP family transporters. Zn-regulated and Fe-regulated transporter proteins; the paper notes their role in Cd uptake alongside MTPs and NRAMPs.
• Vacuolar transporters. ATP-binding cassette transporters (ABCCs) and H⁺/cation exchangers (CAXs) are described as the route for free Cd and PC–Cd into the vacuole.

Crop-specific MBP findings

• Rice. Elevated soil metal induces GSTs and glutathione, which feed PC biosynthesis; PC–As complexes are sequestered in vacuoles via ABCC1/ABCC2. OsNramp5 is the principal root-tip Cd transporter; OsHMA3 is the principal vacuolar Cd-sequestration ATPase; OsHMA2 mediates root-to-shoot Cd translocation.
• Maize. Established metal accumulator; ZmMT expression is hormonally regulated under Cu/Cd/Pb stress. Overexpression of ZmPCS1 in shoot and root prevented Cd toxicity and enhanced phytoremediation capacity. Inoculation with Nocardiopsis lucentensis (actinomycete) under As stress increased PCs, MTs, and GSH in root and enhanced As-phytoremediation in maize and barley.
• Wheat. Sparsely studied. PC synthase TaPCS1 expression increases under Cd and Pb stress. Si application increases PC and MT levels under As stress, reducing shoot translocation by sequestering As in roots.
• Barley. Tolerant to Cr/Zn/Cu/Ni/Cd/Pb. Barley P1B-ATPase transports Zn and Cd. Lipid-transfer protein has affinity for Co(II) and Pb(II) but not Cd(II)/Cu(II)/Zn(II)/Cr(III). OsMT1e expression enhances Cd tolerance and accumulation.

Biotechnological enhancement

• Genetic engineering. Transgenic Arabidopsis expressing the mercuric ion-binding protein (MerP) from Bacillus megaterium showed enhanced Hg accumulation (Hsieh et al. 2009, cited). Co-expression of wheat NHX antiporter and V-PPase proton pump in transgenic tobacco lowered Cu toxicity (Gouiaa and Khoudi 2019). Synthetic PC gene PPH6HIS in transgenic tobacco enhanced Cd accumulation (Vershinina et al. 2022). Transgenic rice overexpressing root V-PPase accumulated more Cd in roots (Cao et al. 2020).
• Biochar. pH 8–11, CEC 25–485 cmol/kg, surface area 140–336 m²/g, porosity 0.0–1.32 cm³/g. Functional groups (COOH, −CO−, −OH, ester) increase CEC and adsorption while reducing nutrient leaching. Quantitative reductions in extractable metal are cited above under Key numbers.
• Chelating agents. EDTA, EGTA, SDS, GLDA (tetrasodium glutamate diacetate), and rutin (a flavonoid) all increase metal availability or plant tolerance in specific systems. EDTA addition gave more than 13-fold Pb extraction and more than 3-fold Cd extraction in Zea mays (Suthar et al. 2014, cited). GLDA + Tagetes patula removed 12.9% of Cd from contaminated agricultural land (Li et al. 2022b, cited).
• Plant–microbe consortia. Plant growth-promoting rhizobacteria (PGPR) produce ACC-deaminase (lowering ethylene stress), siderophores, IAA, and biosurfactants; the paper presents Table 3 remediation-percentage data for ten plant–microbe pairings.

Limitations

This is a B-tier narrative review without a systematic-search protocol or quantitative meta-analysis. Tables 1 and 3 aggregate single-study BCF/TF or percent-removal values from primary literature spanning multiple matrices (soil-spike concentrations, hydroponic systems, mine soils, agricultural soils), so the values are not directly comparable across rows. Cited primary sources should be consulted for sample sizes, replication, statistical treatment, and analytical methods. The molecular-mechanism content is descriptive and does not include effect sizes for transgenic constructs (no quantitative comparison of accumulation in MT-overexpressors versus wild type, for example).

Implications

Mitigation: provides mechanistic and species-level support for agronomic coverage of phytoremediation and crop-selection levers on contaminated agricultural soils.

Courses: the MT, PC, HMA, NRAMP, and ZIP narrative is appropriate for educator-audience modules on why some crop species accumulate more Cd than others and why molecular handling of arsenate, mercury, and lead differs from cadmium handling.

App: no per-product or per-ingredient occurrence data; this review does not contribute to ingredient contamination_profile values directly.

Wiki pages updated on ingest

• agronomic

Verification notes

• Merge-enhanced from prior 2026-05-15 revision on 2026-05-18.
• Prior revision named Thlaspi caerulescens, Pteris vittata, and Arabidopsis halleri as “the classic examples cited” for phytoextraction. None of those three species appear in Sharma et al. 2023’s Table 1 or text — they are textbook hyperaccumulators but not what THIS paper cites. Replaced with the species actually tabulated by Sharma et al. (Brassicaceae, Tagetes erecta, Typha angustifolia, Eichhornia crassipes, Hydrocotyle umbellata, etc.).
• Prior revision attributed “genetically modified plants expressing bacterial merA/merB genes” to the paper. The paper does not mention merA or merB; the bacterial mercury transgenes it discusses are MerP (from Bacillus megaterium; Hsieh et al. 2009, cited) and MerC (in a MerC-SYP121 fusion construct; Uraguchi et al. 2019, cited per Table 2). Corrected.
• Prior revision asserted “HMA3 and HMA4 are central to Cd and Zn vacuolar compartmentalization and phloem loading, respectively.” The paper’s HMA discussion is rice-specific: OsHMA3 for vacuolar Cd sequestration and OsHMA2 for root-to-shoot Cd translocation. The HMA3/HMA4 phloem-loading framing is a general Arabidopsis literature claim not made in this paper. Corrected to match what Sharma et al. actually state.
• Prior revision included a “Crop selection for contaminated land” section asserting “The principle is the same as described in Khan et al. 2015 and Guan et al. 2014” and adding mechanistic claims about “reduced phloem loading of Cd, immobilization in root apoplast for Pb, and competition with silicon for As entry in rice varieties with higher silicon uptake.” None of those mechanisms in that combination appear in Sharma et al. 2023. The Khan/Guan comparison is a Part 2 firewall violation (synthesis across sources at the source-page level). Removed the section; crop-specific MBP findings now sit in their own faithful section sourced to what the paper actually says.
• Prior revision included a “Strategic relevance to the wiki” framing section. Removed — source pages report what the paper says, not how the wiki plans to use it.
• Prior revision linked [[supply-chain/soil]] in both Implications and Wiki pages updated on ingest. That page does not exist; removed both references.
• Added Key numbers section drawing from Tables 1, 2, 3 and in-text quantitative figures, with page-number citations.
• Added Methods (brief) section explicitly noting this is a non-systematic narrative review.
• Replaced defective raw_handle: papers-cube with stable raw_handle: PCMF_article-1-copy-8.
• Added access_url (DOI link) and raw_sha256 provenance fields.
• Added water to matrices to cover the rhizofiltration and aquatic-plant content.
• Audit subagent (2026-05-18) flagged the Key numbers wording on the Lu et al. 2017 biochar entry as conflating two adjacent paper sentences — verified against page 7: the 38–42% figure refers to the proportion of total Pb²⁺ adsorbed via biochar functional-group contact, NOT to the Lu et al. 2017 four-metal reduction (which has no per-metal percentage in the source). Corrected: Lu et al. 2017 entry now reports the 5% (w/w) amendment without a percentage, and the 38–42% Pb²⁺ figure is given separately as a mechanism statement.
• Audit subagent (2026-05-18) flagged plant-tissue as a possibly non-vocabulary matrix slug — verified against wiki/sources/: the slug is in active use in multiple existing source pages, so it is a recognized matrix value not a vocabulary defect. False positive; no change.
• Audit subagent (2026-05-18) flagged [[mitigation/agronomic]] as possibly a missing page — verified wiki/mitigation/agronomic.md exists in the repo. False positive; no change.

Page history

The five most recent substantive edits to this page. The full version history lives in git; when DOI minting comes online (see schema docs), each entry below will also link to a version-pinned DataCite DOI.