Hyperaccumulator

{{Short description|Category of plant}} [[File:Gelbes Galmeiveilchen (viola lutea ssp. calaminaria).jpg|thumb|''Viola lutea subsp. calaminaria'', also known as the zinc violet, grows in soils high in zinc.]] A '''hyperaccumulator''' is a category of metallophyte that is capable of growing in soil or water with a higher concentration of metals, absorbing the metals through its roots and storing it in its foliage.<ref name="Rascio2">{{cite journal |last=Rascio |first=Nicoletta |author2=Navari-Izzo, Flavia |date=1 February 2011 |title=Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? |journal=Plant Science |volume=180 |issue=2 |pages=169–181 |bibcode=2011PlnSc.180..169R |doi=10.1016/j.plantsci.2010.08.016 |pmid=21421358 |s2cid=207387747}}</ref><ref>{{Cite journal |last1=Rajput |first1=Vishnu |last2=Minkina |first2=Tatiana |last3=Semenkov |first3=Ivan |last4=Klink |first4=Galya |last5=Tarigholizadeh |first5=Sarieh |last6=Sushkova |first6=Svetlana |date=2021-04-01 |title=Phylogenetic analysis of hyperaccumulator plant species for heavy metals and polycyclic aromatic hydrocarbons |url=https://doi.org/10.1007/s10653-020-00527-0 |journal=Environmental Geochemistry and Health |language=en |volume=43 |issue=4 |pages=1629–1654 |bibcode=2021EnvGH..43.1629R |doi=10.1007/s10653-020-00527-0 |issn=1573-2983 |pmid=32040786 |url-access=subscription}}</ref><ref name=":02" /> The metals are concentrated at levels that are toxic to closely related species not adapted to growing on the metalliferous soils. Approximately 85-90% of hyperaccumulators are obligate metallophytes.<ref name=":5">{{Cite journal |last=Pollard |first=A. Joseph |last2=Reeves |first2=Roger D. |last3=Baker |first3=Alan J. M. |date=2014-03-01 |title=Facultative hyperaccumulation of heavy metals and metalloids |url=https://www.sciencedirect.com/science/article/pii/S0168945213002574 |journal=Plant Science |volume=217-218 |pages=8–17 |doi=10.1016/j.plantsci.2013.11.011 |issn=0168-9452|url-access=subscription }}</ref>

Compared to non-hyperaccumulating species, hyperaccumulator roots extract the metal from the soil at a higher rate, transfer it more quickly to their shoots, and store large amounts in leaves and roots.<ref>{{cite journal |last=Hossner |first=L.R. |author2=Loeppert, R.H. |author3=Newton, R.J. |author4=Szaniszlo, P.J. |year=1998 |title=Literature review: Phytoaccumulation of chromium, uranium, and plutonium in plant systems |journal=Amarillo National Resource Center for Plutonium, TX (United States) Technical Report}}</ref> The ability to hyperaccumulate toxic metals compared to related species has been shown to be due to differential gene expression and regulation of the same genes in both plants.<ref name="Rascio2" /> Hyperaccumulators are regularly discussed within the context of phytoremediation, although their commercialization remains aspirational. 450 plant species, including the model organisms ''Arabidopsis'' and Brassicaceae, have demonstrated the capacity to uptake and sequester metals such as Arsenic (As), Cobalt (Co), Iron (Fe), Copper (Cu), Cadmium (Cd), Lead (Pb), Mercury (Hg), Selenium (Se), Manganese (Mn), Nickel (Ni),<ref>{{Cite journal |last=Brooks |first=R.R. |year=1977 |title=Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants |url=https://core.ac.uk/download/pdf/39880595.pdf |journal=Journal of Geochemicul Exploration |volume=7 |pages=49–57 |bibcode=1977JCExp...7...49B |doi=10.1016/0375-6742(77)90074-7}}</ref> Zinc (Zn), and Molybdenum (Mo) in 100–1000 times the concentration found in sister species or populations.<ref name="Rascio2" />

== Metallophytes == A '''metallophyte''' is a type of plant capable of surviving in metal-rich soil. <ref>{{Cite journal |last=Alford |first=Élan R. |last2=Pilon-Smits |first2=Elizabeth A. H. |last3=Paschke |first3=Mark W. |date=2010-12-01 |title=Metallophytes—a view from the rhizosphere |url=https://doi.org/10.1007/s11104-010-0482-3 |journal=Plant and Soil |language=en |volume=337 |issue=1 |pages=33–50 |doi=10.1007/s11104-010-0482-3 |issn=1573-5036|url-access=subscription }}</ref> Metallophytes are classified as metal indicators, excluders, or hyperaccumulators.<ref name=":02">{{Cite journal |last=Awa |first=Soo Hui |last2=Hadibarata |first2=Tony |date=2020-01-21 |title=Removal of Heavy Metals in Contaminated Soil by Phytoremediation Mechanism: a Review |url=https://doi.org/10.1007/s11270-020-4426-0 |journal=Water, Air, & Soil Pollution |language=en |volume=231 |issue=2 |pages=47 |doi=10.1007/s11270-020-4426-0 |issn=1573-2932|url-access=subscription }}</ref> Such plants range between obligate metallophytes and facultative metallophytes.<ref name=":12">CRC dictionary of agricultural sciences, Robert Alan Lewis, CRC Press, 2001, {{ISBN|0-8493-2327-4}}</ref> '''Obligate''' metallophytes can only survive in the presence of heavy metals while '''facultative''' metallophytes can tolerate such conditions but are not confined to them.<ref name=":12" />

== Hyperaccumulators == {{see|List of hyperaccumulators}} === Table on Hyperaccumulators === {| class="wikitable" |+ !Plant Species !Common Name !Metal Accumulated !Obligate or Facultative |- |''Alyssum murale'' |Yellow Tuft |Ni<ref name=":02" /> |Facultative<ref name=":5" /> |- |''Astragalus'' |Astragalus |Se<ref name=":3">{{cite journal |last1=Terry |first1=N. |last2=Zayed |first2=A. M. |last3=De Souza |first3=M. P. |last4=Tarun |first4=A. S. |date=2000 |title=Selenium in Higher Plants |journal=Annual Review of Plant Physiology and Plant Molecular Biology |volume=51 |pages=401–432 |doi=10.1146/annurev.arplant.51.1.401 |pmid=15012198}}</ref> | |- |''Biscutella laevigata'' |Buckler Mustard |Tl<ref name="LaCoste20062">{{cite journal |vauthors=LaCoste C, Robinson B, Brooks R, Anderson C, Chiarucci A, Leblanc M |year=2006 |title=The phytoremediation potential of thallium-contaminated soils using Iberis and Biscutella species |journal=International Journal of Phytoremediation |volume=1 |issue=4 |pages=327–338 |doi=10.1080/15226519908500023}}</ref> |Facultative<ref name=":5" /> |- |''Brassica juncea'' |Mustard Greens |Au,<ref name=":02" /> Pb<ref name=":4">{{Cite journal |last=Sikka |first=Rajeev |last2=Kalsi |first2=Arshdeep |last3=Kaur |first3=Paawan |date=2025-04-12 |title=Phytoremediation of Lead-Contaminated Soils Using Indian Mustard: Influence of Organic and Inorganic Amendments |url=https://doi.org/10.1007/s00128-025-04042-9 |journal=Bulletin of Environmental Contamination and Toxicology |language=en |volume=114 |issue=4 |pages=63 |doi=10.1007/s00128-025-04042-9 |issn=1432-0800|url-access=subscription }}</ref> | |- |''Deschampsia cespitosa'' |Tufted Hairgrass |Pb, Cd, Zn<ref name=":02" /> | |- |''Desert princesplume'' |Stanleya |Se<ref name=":3" /> | |- |''Eleocharis acicularis'' |Needle Spikerush |Cu, Zn, Cd, As<ref name=":02" /> | |- |''Erato polymnioides'' |Ghost Plant |Hg<ref name=":02" /> | |- |''Haumaniastrum robertii'' |Robert's Haumaniastrum |Co<ref name=":02" /> | |- |''Helianthus annus'' |Common Sunflower |Cd, Ni, Pb, Cr,<ref name=":4" /> As<ref name=":22">{{Citation |last1=Marchiol |first1=L. |title=Removal of trace metals by Sorghum bicolor and Helianthus annuus in a site polluted by industrial wastes: A field experience |journal=Plant Physiology and Biochemistry |volume=45 |issue=5 |pages=379–87 |year=2007 |bibcode=2007PlPB...45..379M |doi=10.1016/j.plaphy.2007.03.018 |pmid=17507235 |last2=Fellet |first2=G. |last3=Perosa |first3=D. |last4=Zerbi |first4=G.}}</ref> | |- |''Iberis intermedia'' |Candytuft |Tl<ref name="LaCoste20062" /> | |- |''Medicago sativa'' |Alfalfa |Au<ref name=":02" /> | |- |''Populus nigra'' |Poplar |Cd, Ni, Pb, Cr<ref name=":4" /> | |- |''Pteris vittata'' |Chinese Brake |Cr, Hg<ref name=":02" /> |Facultative<ref name=":5" /> |- |''Salix smithiana'' |Smith's Willow |Cd, Ni, Pb, Cr<ref name=":4" /> | |- |''Salix viminalis'' |Basket Willow |Cd, Zn, Cu<ref name="Greger2">{{Citation |last1=Greger |first1=M. |title=Using of Willow in Phytoextraction |journal=International Journal of Phytoremediation |volume=1 |issue=2 |pages=115–123 |year=1999 |bibcode=1999IJPhy...1..115G |doi=10.1080/15226519908500010 |name-list-style=amp |last2=Landberg |first2=T.}}.</ref> | |- |''Solanum lycopersicum'' |Tomato |Cr<ref>{{Cite journal |last1=Akhtar |first1=Ovaid |last2=Kehri |first2=Harbans Kaur |last3=Zoomi |first3=Ifra |date=2020-09-15 |title=Arbuscular mycorrhiza and Aspergillus terreus inoculation along with compost amendment enhance the phytoremediation of Cr-rich technosol by Solanum lycopersicum under field conditions |url=http://www.sciencedirect.com/science/article/pii/S0147651320307089 |journal=Ecotoxicology and Environmental Safety |language=en |volume=201 |article-number=110869 |bibcode=2020EcoES.20110869A |doi=10.1016/j.ecoenv.2020.110869 |issn=0147-6513 |pmid=32585490 |s2cid=220073862 |url-access=subscription}}</ref> | |- |''Virotia neurophylla'' | |Mn<ref name=":02" /> | |- |''Xylorhiza'' |Mojave-aster |Se<ref name=":3" /> | |- |''Zea mays'' |Maize |Cd, Ni, Pb, Cr<ref name=":4" /> | |} Note that it is under debate as to whether Allium, Amaranthus, Iris, Lonicera, Rorippa, Salsola and Solanum are truly hyperaccumulators or metallophytes at all as their hyperaccumulation was recorded in labs, not nature.<ref name=":5" /> {{Multiple image | align = left | direction = horizontal | total_width = 720 | image1 = | caption1 = ''Brassica juncea'', commonly known as mustard greens | image3 = Solanum Lycopersicum tomkin 1.jpg | caption3 = ''Solanum lycopersicum'', commonly known as tomato plant | image5 = Pteris vittata from Antalya city in Turkey 10.jpg | caption5 = ''Pteris vittata'', commonly known as the Chinese Brake | image6 = Xylorhiza tortifolia 1.jpg | caption6 = ''Xylorhiza'', commonly known as Mojave-aster }} {{Multiple image | align = left | direction = horizontal | total_width = 720 | image1 = Brassica juncea Flower.jpg | caption1 = ''Brassica juncea'', commonly known as Mustard Greens | image2 = Alyssum murale kz05 (2x3).jpg | caption2 = ''Alyssum murale'', commonly known as Yellow Tuft | image4 = Erato polymnioides (Asteraceae) (30361407622).jpg | caption4 = ''Erato polymnioides'', commonly known as Ghost Plant }}

=== Applications of Hyperaccumulators === [[File:Phytoextraction diagram.svg|thumb|Cartoon for phytoremediation of metal-contaminated soil (violet and yellow = heavy metals) by a hyperaccumulator. The metal ions are moved from the soil to the leaves of the plant. In the case of phytomining, the leaves would be harvested to recover the valuable metals.]]

==== Phytoremediation ==== Hyperaccumulating plants are of interest in the context of phytoremediation: to detoxify contaminated soils.<ref name="Rascio">{{cite journal|last=Rascio|first=Nicoletta|author2=Navari-Izzo, Flavia|title=Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting?|journal=Plant Science|date=1 February 2011|volume=180|issue=2|pages=169–181|doi=10.1016/j.plantsci.2010.08.016|pmid=21421358|bibcode=2011PlnSc.180..169R |s2cid=207387747}}</ref><ref>{{Cite journal |last1=Awa |first1=Soo Hui |last2=Hadibarata |first2=Tony |date=2020-01-21 |title=Removal of Heavy Metals in Contaminated Soil by Phytoremediation Mechanism: a Review |journal=Water, Air, & Soil Pollution |language=en |volume=231 |issue=2 |page=47 |doi=10.1007/s11270-020-4426-0 |issn=1573-2932}}</ref> '''Phytoextraction''' is a subprocess of phytoremediation in which plants remove metal ions from soil or water.<ref name="Rascio" /> Phytoextraction could in principle be used to remove contaminants from an ecosystem.<ref>Guidi Nissim W., Palm E., Mancuso S., Azzarello E. (2018) "Trace element phytoextraction from contaminated soil: a case study under Mediterranean climate". Environmental Science and Pollution Research https://doi.org/10.1007/s11356-018-1197-x {{Webarchive|url=https://web.archive.org/web/20211006204029/https://link.springer.com/article/10.1007%2Fs11356-018-1197-x |date=2021-10-06 }}</ref> For example, water hyacinth have been demonstrated to remove arsenic from water.<ref>Misbahuddin, M., and A. Fariduddin. "Water Hyacinth Removes Arsenic from Arsenic-Contaminated Drinking Water." Archives of Environmental Health 57.6 (2002): 516-8. SCOPUS. Web. 26 September 2011.</ref> Cadmium accumulation has also received attention as this metal is usually toxic.<ref>{{cite book |last1=Küpper |first1=Hendrik |last2=Leitenmaier |first2=Barbara |editor=Astrid Sigel, Helmut Sigel and Roland K. O. Sigel |title=Cadmium: From Toxicology to Essentiality |series=Metal Ions in Life Sciences |volume=11 |year=2013 |publisher=Springer |pages=373–413 |chapter=Chapter 12. Cadmium-accumulating plants |doi=10.1007/978-94-007-5179-8_12|pmid=23430779 |isbn=978-94-007-5178-1 }}</ref><ref>Han F., Shan X.Q., Zhang S.Z., Wen B. & Owens G. (2006) Enhanced cadmium accumulation in maize roots – the impact of organic acids. Plant and Soil 289, 355–368.</ref><ref>K.B. Axelsen and M.G. Palmgren, Inventory of the superfamily of P-Type ion pumps in Arabidopsis. Plant Physiol., 126 (1998), pp. 696–706.</ref>

Caesium-137 and strontium-90 were removed from a pond using sunflowers after the Chernobyl accident.<ref>{{cite magazine |url=http://findarticles.com/p/articles/mi_m1200/is_n3_v150/ai_18518620/?tag=content;col1 |title=Botanical cleanup crews: using plants to tackle polluted water and soil |author=Adler, Tina |magazine=Science News |date=July 20, 1996 |access-date=2010-09-03 |archive-url=https://web.archive.org/web/20110715211727/http://findarticles.com/p/articles/mi_m1200/is_n3_v150/ai_18518620/?tag=content;col1 |archive-date=July 15, 2011 }}</ref>

The remediation of metal-contaminated soils recognizes that metals cannot be degraded, they must be removed. Organic pollutants can be, and are generally the major targets for phytoremediation. Field trials support the feasibility of using plants for environmental cleanup.<ref name="Salt1998">{{cite journal |vauthors=Salt DE, Smith RD, Raskin I |title=Phytoremediation |journal=Annual Review of Plant Physiology and Plant Molecular Biology |volume=49 |pages=643–668 |year=1998 |pmid=15012249 |doi=10.1146/annurev.arplant.49.1.643 |s2cid=241195507 }}</ref><ref>{{Cite book |last=Linacre |first=J. Scott Angle and Nicholas A. |url=https://books.google.com/books?id=rQO75ucv4fUC&dq=%22phytomining%22%7C%22phytominings%22&pg=PA14 |title=Ecological Risks of Novel Environmental Crop Technologies Using Phytoremediation as an Example |date=2005 |publisher=Intl Food Policy Res Inst |language=en}}</ref>

==== Phytomining ==== [[File:Alyssum obovatum 38030702.jpg|thumb|''Odontarrhena'' plants are hyperaccumulators of nickel]]

'''Phytomining''', sometimes called '''agromining''',<ref name="Dang">{{Cite journal |last1=Dang |first1=P. |last2=Li |first2=C. |date=2022-12-01 |title=A mini-review of phytomining |journal=International Journal of Environmental Science and Technology |language=en |volume=19 |issue=12 |pages=12825–12838 |doi=10.1007/s13762-021-03807-z |bibcode=2022JEST...1912825D |issn=1735-2630 }}</ref> is the concept of extracting heavy metals from the soil using hyperaccumulating plants.<ref>{{Cite journal |last1=Brooks |first1=Robert R |last2=Chambers |first2=Michael F |last3=Nicks |first3=Larry J |last4=Robinson |first4=Brett H |date=1998-09-01 |title=Phytomining |url=https://www.sciencedirect.com/science/article/pii/S1360138598012837 |journal=Trends in Plant Science |volume=3 |issue=9 |pages=359–362 |doi=10.1016/S1360-1385(98)01283-7 |bibcode=1998TPS.....3..359B |issn=1360-1385 |url-access=subscription}}</ref> Once the hyperaccumulation has proceeded to some extent, the metals are collected from the plant matter and then refined for sale or disposed of.<ref name="leaders">{{Cite web |date=2021-02-11 |title=Leaders of the energy transition are calling for a sustainable source of critical metals – is phytomining the answer? |url=https://smi.uq.edu.au/leaders-energy-transition-sustainable-source-critical-metals-phytomining |access-date=2023-10-09 |website=smi.uq.edu.au |language=en}}</ref><ref>{{Cite journal |last1=Tangahu |first1=Bieby Voijant |last2=Sheikh Abdullah |first2=Siti Rozaimah |last3=Basri |first3=Hassan |last4=Idris |first4=Mushrifah |last5=Anuar |first5=Nurina |last6=Mukhlisin |first6=Muhammad |date=2011-08-16 |editor-last=Bart |editor-first=Hans-Jörg |title=A Review on Heavy Metals (As, Pb, and Hg) Uptake by Plants through Phytoremediation |journal=International Journal of Chemical Engineering |language=en |volume=2011 |issue=1 |article-number=939161 |doi=10.1155/2011/939161 |doi-access=free |issn=1687-806X}}</ref><ref name="pr">{{Cite journal|last1=Ali|first1=Hazrat|last2=Khan|first2=Ezzat|last3=Sajad|first3=Muhammad Anwar|title=Phytoremediation of heavy metals—Concepts and applications|journal=Chemosphere|volume=91|issue=7|pages=869–881 |doi=10.1016/j.chemosphere.2013.01.075 |pmid=23466085|year=2013 |bibcode=2013Chmsp..91..869A}}</ref>

Phytomining typically follows three steps: 1) Phytoextraction, where metals are sequestered from soil into plants; 2) Enrichment, where plant biomass is eliminated and heavy metals are enriched as solids; 3) Extraction, where the solid remains are processed into more accessible forms.<ref>{{Cite journal |last=Kovacs |first=Helga |date=2025-12-01 |title=Extraction of noble metals and rare earth elements using plants |url=https://www.sciencedirect.com/science/article/pii/S2211339825001042 |journal=Current Opinion in Chemical Engineering |volume=50 |article-number=101192 |doi=10.1016/j.coche.2025.101192 |issn=2211-3398|doi-access=free }}</ref>

Phytomining would, in principle, minimize environmental effects compared to conventional mining. Phytomining could also remove low-grade heavy metals from mine waste.<ref name="leaders" /> A 2021 review concluded that the commercial viability of phytomining was "limited"<ref name="Dang" /> because it is a slow and inefficient process. Its purpose is either: (i) gathering the metals for economic use (ii) gathering toxic metals to improve the soil.

Phytomining was proposed in 1983 by Rufus Chaney, a USDA agronomist.<ref name="fp">{{Cite news |last=Morse |first=Ian |date=2020-02-26 |title=Down on the Farm That Harvests Metal From Plants |language=en-US |work=The New York Times |url=https://www.nytimes.com/2020/02/26/science/metal-plants-farm.html |access-date=2023-10-09 |issn=0362-4331}}</ref> He and Alan Baker, a University of Melbourne professor, first tested it in 1996.<ref name="fp" /> They, as well as Jay Scott Angle and Yin-Ming Li, filed a patent on the process in 1995 which expired in 2015.<ref>{{Cite patent|number=US5711784A|title=Method for phytomining of nickel, cobalt and other metals from soil|gdate=1998-01-27|invent1=Chaney|invent2=Angle|invent3=Baker|invent4=Li|inventor1-first=Rufus L.|inventor2-first=Jay Scott|inventor3-first=Alan J. M.|inventor4-first=Yin-Ming|url=https://patents.google.com/patent/US5711784A/en}}</ref>

Several startups are investigating the process for mining surface-available heavy metals. In 2025, Genomines received 45 million dollars of Series A funding to commercialize nickel phytomining from mine tailings.<ref>{{Cite news |last=Peters |first=Adele |date=2025-09-19 |title=This startup grows plants instead of digging mines to extract a critical mineral |url=https://www.fastcompany.com/91406694/this-startup-uses-plants-not-a-huge-mine-to-pull-a-critical-mineral-out-of-the-ground |archive-url=https://web.archive.org/web/20251010150743/https://www.fastcompany.com/91406694/this-startup-uses-plants-not-a-huge-mine-to-pull-a-critical-mineral-out-of-the-ground |archive-date=2025-10-10 |access-date=2025-11-10 |work=Fast Company |language=en-US}}</ref> The French company Econick and the Albanian company MetalPlant both have nickel phytomining projects. As of mid-2024, MetalPlant had extracted less than a kilo of usable nickel, using ''Odontarrhena'' plants.<ref>{{cite web |last1=Dinneen |first1=James |title=Flower farm could supply nickel for electric vehicle batteries |url=https://www.newscientist.com/article/2438399-flower-farm-could-supply-nickel-for-electric-vehicle-batteries/ |publisher=New Scientist |access-date=29 December 2025 |date=4 July 2024}}</ref>

=== Physiological advantage for hyperaccumulation === The biological advantage of hyperaccumulation may be that the toxic levels of heavy metals in leaves deter herbivores or increase the toxicity of other anti-herbivory metabolites.<ref name="Rascio" /><ref>{{Cite journal|last1=Goolsby|first1=Eric W.|last2=Mason|first2=Chase M.|date=2015-01-30|title=Toward a more physiologically and evolutionarily relevant definition of metal hyperaccumulation in plants|journal=Frontiers in Plant Science|volume=6|page=33|doi=10.3389/fpls.2015.00033|issn=1664-462X|pmc=4311607|pmid=25688255|bibcode=2015FrPS....6...33G |doi-access=free}}</ref> The plant defense hypothesis, "the elemental defense hypothesis", provided by Poschenrieder, suggested that the expression of these genes assist in antiherbivory or pathogen defenses by making tissues toxic to organisms attempting to feed on that plant.<ref name="Poschenrieder C. 2006" /> Another hypothesis, "the joint hypothesis", provided by Boyd, suggests that expression of these genes assists in systemic defense.<ref name="Boyd R. S. 2012">{{Cite journal |last=Boyd |first=Robert S. |date=October 2012 |title=Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses |journal=Plant Science|volume=195 |pages=88–95 |doi=10.1016/j.plantsci.2012.06.012 |issn=1873-2259 |pmid=22921002 |bibcode=2012PlnSc.195...88B }}</ref> The benefit for a plant to hyperaccumulate may be that root-to-shoot transport system drives hyper-accumulation by creating a metal deficiency response in roots.<ref name="hanik">{{cite journal|last1=Hanikenne |first1=Marc |last2=Talke |first2=Ina N. |last3=Haydon |first3=Michael J. |last4=Lanz |first4=Christa |last5=Nolte |first5=Andrea |last6=Motte |first6=Patrick |last7=Kroymann |first7=Juergen |last8=Weigel |first8=Detlef |last9=Krämer |first9=Ute |title=Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4 |journal=Nature |date=2008 |volume=453 |issue=7193 |pages=391–395 |doi=10.1038/nature06877 |pmid=18425111 }}</ref>

===T. caerulescens=== As a hyperaccumulator variously of Cd, Pb, and Zn, ''T. caerulescens'', pennycress, has received particular attention. Its leaves accumulate up to 380 mg/kg Cd.<ref name=penny>{{cite journal|volume=137|year=2006|pages=19–32|journal=Geoderma|title=Review:Cadmium in Plants on Polluted Soils: Effects of Soil Factors, Hyperaccumulation, and Amendments|author=M.B.Kirkham|doi= 10.1016/j.geoderma.2006.08.024}}</ref> On the other hand, the presence of copper seems to impair its growth. It is found mostly in Zn/Pb-rich soils, as well as serpentines and non-mineralized soils.<ref>{{Cite journal|last1=Baker|first1=A. J. M.|last2=Reeves|first2=R. D.|last3=Hajar|first3=A. S. M.|date=1994|title=Heavy metal accumulation and tolerance in British populations of the metallophyte ''Thlaspi caerulescens'' J. & C. Presl (Brassicaceae)|journal=New Phytologist|language=en|volume=127|issue=1|pages=61–68|doi=10.1111/j.1469-8137.1994.tb04259.x|pmid=33874394|bibcode=1994NewPh.127...61B |issn=1469-8137|doi-access=free}}</ref> When grown on mildly polluted soils, a closely related species, ''Thlaspi ochroleucum'', is a heavy metal-tolerant plant, but it accumulates much less Zn in the shoots than ''T. caerulescens''. Thus, ''T. ochroleucum'' is a non-hyperaccumulator and of the same family ''T. caerulescens'' is a hyperaccumulator. The transfer of Zn from roots to shoots varied significantly between these two species. ''T. caerulescens'' had much higher shoot/root Zn concentration levels than ''T. ochroleucum'', which always had higher Zn concentrations in the roots. When Zn was withheld, the amount of Zn previously accumulated in the roots in ''T. caerulescens'' decreased even more than in ''T. ochroleucum'', with a concomitantly greater rise in the amount of Zn in the shoots. The decreases in Zn in roots may be mostly due to transport to shoots, since the volume of Zn in shoots increased during the same time span.<ref>{{Cite journal|last=Mathys|first=Werner|date=1977|title=The Role of Malate, Oxalate, and Mustard Oil Glucosides in the Evolution of Zinc-Resistance in Herbage Plants|url=https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1399-3054.1977.tb01509.x|journal=Physiologia Plantarum|language=en|volume=40|issue=2|pages=130–136|doi=10.1111/j.1399-3054.1977.tb01509.x|bibcode=1977PPlan..40..130M |issn=1399-3054|url-access=subscription}}</ref>

=== Genetic basis of hyperaccumulation === An overexpression of a Zn transporter gene, ZNT1, in root and shoot tissue is an essential component of the Zn hyperaccumulation trait in ''T. caerulescens''.<ref>{{Cite journal|last1=Pence|first1=Nicole S.|last2=Larsen|first2=Paul B.|last3=Ebbs|first3=Stephen D.|last4=Letham|first4=Deborah L. D.|last5=Lasat|first5=Mitch M.|last6=Garvin|first6=David F.|last7=Eide|first7=David|last8=Kochian|first8=Leon V.|author-link8=Leon Kochian|date=2000-04-25|title=The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens|journal=Proceedings of the National Academy of Sciences|language=en|volume=97|issue=9|pages=4956–4960|doi=10.1073/pnas.97.9.4956|issn=0027-8424|pmid=10781104|pmc=18339|bibcode=2000PNAS...97.4956P|doi-access=free}}</ref> This increased gene expression has been shown to be the basis for increased Zn<sup>2+</sup> uptake from the soil in ''T. caerulescens'' roots, and it is possible that the same process underpins the enhanced Zn<sup>2+</sup> uptake into leaf cells.The proteins are coded by genes in the ZIP family, however other families such as the HMA (heavy metal ATPase<ref name=hanik/>), MATE, YSL and MTP families have also been observed to be involved. The ZIP gene family encodes Cd, Mn, Fe and Zn transporters. The ZIP family plays a role in supplying Zn to metalloproteins.<ref name="Poschenrieder C. 2006">{{Cite journal |last1=Poschenrieder |first1=Charlotte |last2=Tolrà |first2=Roser |last3=Barceló |first3=Juan |date=June 2006 |title=Can metals defend plants against biotic stress? |journal=Trends in Plant Science |volume=11 |issue=6 |pages=288–295 |doi=10.1016/j.tplants.2006.04.007 |issn=1360-1385 |pmid=16697693 |bibcode=2006TPS....11..288P }}</ref><ref>{{Cite journal|last1=Pollard|first1=A. Joseph|last2=Powell|first2=Keri Dandridge|last3=Harper|first3=Frances A.|last4=Smith|first4=J. Andrew C.|date=2002-11-01|title=The Genetic Basis of Metal Hyperaccumulation in Plants|journal=Critical Reviews in Plant Sciences|volume=21|issue=6|pages=539–566|doi=10.1080/0735-260291044359|bibcode=2002CRvPS..21..539P |s2cid=17553966|issn=0735-2689}}</ref>

In one study on ''Arabidopsis'', it was found that the metallophyte ''Arabidopsis halleri'' expressed a member of the ZIP family that was not expressed in a non-metallophyte sister species. This gene was an iron-regulated transporter (IRT-protein) that encoded several primary transporters involved with cellular uptake of cations above the concentration gradient. When this gene was transformed into yeast, hyperaccumulation was observed.<ref name="Becher, Martina 2004">{{Cite journal |last1=Becher |first1=Martina |last2=Talke |first2=Ina N. |last3=Krall |first3=Leonard |last4=Krämer |first4=Ute |date=January 2004 |title=Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri |journal=The Plant Journal: For Cell and Molecular Biology |volume=37 |issue=2 |pages=251–268 |doi=10.1046/j.1365-313x.2003.01959.x |issn=0960-7412 |pmid=14690509}}</ref> This suggests that overexpression of ZIP family genes that encode cation transporters is a characteristic genetic feature of hyperaccumulation. Another gene family that has been observed ubiquitously in hyperaccumulators are the ZTP and ZNT families. A study on ''T. caerulescens'' identified the ZTP family as a plant specific family with high sequence similarity to other zinc transporter. Both the ZTP and ZNT families, like the ZIP family, are zinc transporters.<ref name="Persans, Michael W. 2001">{{Cite journal |last1=Persans |first1=M. W. |last2=Nieman |first2=K. |last3=Salt |first3=D. E. |date=2001-08-14 |title=Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense |journal=Proceedings of the National Academy of Sciences of the United States of America |volume=98 |issue=17 |pages=9995–10000 |doi=10.1073/pnas.171039798 |doi-access=free |issn=0027-8424 |pmc=55566 |pmid=11481436 |bibcode=2001PNAS...98.9995P}}</ref> It has been observed in hyperaccumulating species, that these genes, specifically ZNT1 and ZNT2 alleles are chronically overexpressed.<ref name="Assunção, A. G. L. 2001">{{Cite journal |last1=Assunção |first1=A. G. L. |last2=Martins |first2=P. Da Costa |last3=De Folter |first3=S. |last4=Vooijs |first4=R. |last5=Schat |first5=H. |last6=Aarts |first6=M. G. M. |date=February 2001 |title=Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens |url=https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2001.00666.x |journal=Plant, Cell & Environment |language=en |volume=24 |issue=2 |pages=217–226 |doi=10.1111/j.1365-3040.2001.00666.x |bibcode=2001PCEnv..24..217A |issn=0140-7791 |url-access=subscription}}</ref>

AhHMHA3 is expressed in hyperaccumulating individuals. AhHMHA3 has been identified to be expressed in response to and aid of Zn detoxification.<ref name="C. Pagliano, 2006 pp. 70">{{Cite journal |last1=Pagliano |first1=Cristina |last2=Raviolo |first2=Marco |last3=Dalla Vecchia |first3=Francesca |last4=Gabbrielli |first4=Roberto |last5=Gonnelli |first5=Cristina |last6=Rascio |first6=Nicoletta |last7=Barbato |first7=Roberto |last8=La Rocca |first8=Nicoletta |date=2006-07-03 |title=Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.) |journal=Journal of Photochemistry and Photobiology B: Biology |volume=84 |issue=1 |pages=70–78 |doi=10.1016/j.jphotobiol.2006.01.012 |issn=1011-1344 |pmid=16540337 |bibcode=2006JPPB...84...70P }}</ref> In another study, using metallophytic and non-metallophytic ''Arabidopsis'' populations, back crosses indicated pleiotropy between Cd and Zn tolerances.<ref name="Bert, V. 2003">{{Cite journal |last1=Bert |first1=V. |last2=Meerts |first2=P. |last3=Saumitou-Laprade |first3=P. |last4=Salis |first4=P. |last5=Gruber |first5=W. |last6=Verbruggen |first6=N. |date=2003 |title=Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri |url=http://link.springer.com/10.1023/A:1022580325301 |journal=Plant and Soil |volume=249 |issue=1 |pages=9–18 |doi=10.1023/A:1022580325301 |bibcode=2003PlSoi.249....9B |url-access=subscription}}</ref> This response suggests that plants are unable to detect specific metals, and that hyperaccumulation is likely a result of an overexpressed Zn transportation system.<ref name="Pollard, A. J 1996">{{Cite journal |last1=Pollard |first1=A. Joseph |last2=Baker |first2=Alan J.M. |date=January 1996 |title=Quantitative genetics of zinc hyperaccumulation in Thlaspi caerulescens |url=https://nph.onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.1996.tb04515.x |journal=New Phytologist |language=en |volume=132 |issue=1 |pages=113–118 |doi=10.1111/j.1469-8137.1996.tb04515.x |pmid=33863047 |bibcode=1996NewPh.132..113P |issn=0028-646X}}</ref>

One of the most well-documented HMAs is HMA4, which belongs to the Zn/Co/Cd/Pb HMA subclass and is localized at xylem parenchyma plasma membranes.<ref name="Rascio"/> HMA4 is upregulated when plants are exposed to high levels of Cd and Zn, but it is downregulated in its non-hyperaccumulating relatives.<ref>A. Papoyan and L.V. Kochian, Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyper-accumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol., 136 (2004), pp. 3814–3823.</ref> Also, when the expression of HMA4 is increased there is a correlated increase in the expression of genes belonging to the ZIP (Zinc regulated transporter Iron regulated transporter Proteins) family.

=== Genetic Engineering of Hyperaccumulators === Genetic engineering has been used to research potential improvements towards hyperaccumulation efficiency and species resistance to biological side effects of metal uptake.<ref name=":0">{{Cite journal |last=Jassal |first=Prabhjot Singh |last2=Kudave |first2=Pratik Suryakant |last3=Wani |first3=Atif Khurshid |last4=Yadav |first4=Tusha |date=2025-08-24 |title=Prospects of phytoremediation in degradation of environmental contaminants: recent advances, challenges and way forward |url=https://www.tandfonline.com/doi/full/10.1080/15226514.2025.2500643 |journal=International Journal of Phytoremediation |language=en |volume=27 |issue=10 |pages=1442–1459 |doi=10.1080/15226514.2025.2500643 |issn=1522-6514|url-access=subscription }}</ref> Methods have included engineering overexpression of pollutant degrading enzymes or proteins associated with heavy metal transportation pathways, and transgenesis, where genes from hyperaccumulators are inserted into the genome of other hyperaccumulators to target specific metals or metals previously inaccessible to that species.

For example, ''Sedum plumbizinicicola'' is a hyperaccumulator of Cd using the heavy metal transporter genes SpHMA2, SpHMA3, and SpNramp6.<ref name=":2">{{Cite journal |last=Yang |first=Zi |last2=Wu |first2=Hai-Tao |last3=Yang |first3=Hao |last4=Chen |first4=Wan-Di |last5=Liu |first5=Jia-Lan |last6=Yang |first6=Fan |last7=Tai |first7=Li |last8=Li |first8=Bin-Bin |last9=Yuan |first9=Bo |last10=Liu |first10=Wen-Ting |last11=Zhang |first11=Yan-Feng |last12=Luo |first12=Yan-Rong |last13=Chen |first13=Kun-Ming |date=2023-05-05 |title=Overexpression of Sedum SpHMA2, SpHMA3 and SpNramp6 in Brassica napus increases multiple heavy metals accumulation for phytoextraction |url=https://www.sciencedirect.com/science/article/pii/S0304389423002522 |journal=Journal of Hazardous Materials |volume=449 |article-number=130970 |doi=10.1016/j.jhazmat.2023.130970 |issn=0304-3894|url-access=subscription }}</ref> In 2023, Yang et al. inserted these genes into ''Brassica napus'', or Rapeseed plants, resulting in high uptake efficiency and sequestration of Cd compared to the wild-type rapeseed.

Transgenic phytoextractors theoretically function to combine favorable traits like high biomass production with hyperaccumulation, showing the potential to improve the speed of phytoremediation. However, research reports often do not include long term data of artificial phytoextraction by transgenic plants to see if they can actually survive their entire life cycle intaking hyperaccumulator-levels of contaminants.<ref>{{Cite web |last=van der Ent |first=Anthony |last2=Rylott |first2=Elizabeth L. |date=March 2024 |title=Inventing hyperaccumulator plants: improving practice in phytoextraction research and terminology |url=https://www.tandfonline.com/action/cookieAbsent |access-date=2026-04-01 |website=www.tandfonline.com |doi=10.1080/15226514.2024.2322631 |pmc=11221517 |pmid=38437154}}</ref> Site implementation of transgenic plants for phytoremediation is also controversial, due to how these plants could negatively impact native biodiversity.<ref>{{Cite journal |last=Olabisi Onabanjo University, Ago Iwoye, Ogun State Nigeria |last2=Anifowose |first2=Oluwaseun |last3=Oyelana |first3=Oluwabori |last4=Olabisi Onabanjo University, Ago Iwoye, Ogun State Nigeria |date=2025-06-18 |title=Ethical Reflections on The Impact of Genetic Engineering on Biodiversity |url=https://journals.uni-vt.bg/ese/eng/vol3/iss1/art3 |journal=Ethics, Science, Education |volume=3 |issue=1 |pages=23–29 |doi=10.54664/CMGZ6373}}</ref>

=== Molecular pathway === Often hyperaccumulation is the result of promiscuous zinc binding, i.e. protein-based sequestrants, transporters, etc with a high affinity for zinc that will bind other metal ions. Metals ions in solution are susceptible to extraction.<ref>Misra V., Tiwari A., Shukla B. & Seth C.S. (2009) Effects of soil amendments on the bioavailability of heavy metals from zinc mine tailings. Environmental Monitoring Assessment 155, 467–475.</ref> For example, ligands secreted by plant - phytosiderophores, organic acids, or carboxylates -can selectively binds certain ions.<ref>Clemens S., Palmgren M.G. & Krämer U. (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends in Plant Science 7, 309–315.</ref><ref>Seth, C. S., et al. "Phytoextraction of Toxic Metals: A Central Role for Glutathione." Plant, Cell and Environment (2011)SCOPUS. Web. 16 October 2011.</ref>

== Metal Excluders == A '''metal excluder''' is a category of metallophyte that absorbs metals at only their roots.<ref name=":02" /> {| class="wikitable" !Plant Species !Common Name !Metal Accumulated |- |''Bidens pilosa'' |Cobblers Pegs |As, Cd<ref name=":02" /> |- |''Silene paradoxa'' |Dover Catchfly |As, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Zn<ref name=":02" /> |} {{Multiple image | align = left | direction = horizontal | total_width = 360 | image1 = Bidens pilosa-Silent Valley-2016-08-13-001.jpg | caption1 = The flowering plant ''Bidens pilosa'' of the daisy family Asteraceae | image2 = Silene paradoxa.jpg | caption2 = The flowering plant ''Silene paradoxa'', or Dover Catchyfly, of the Caryophyllaceae family | caption3 = ''Pistia stratiotes'', an example of a neuston, a plant that floats freely on the water surface }}

== Metal Indicators == A '''metal indicator''' is a metallophyte that accumulates heavy metal concentration in shoots and leaves.<ref name=":02" />While good at absorbing metals, they eventually succumb to the metals' toxicity.<ref name=":02" /> {| class="wikitable" !Plant Species !Common Name !Metal Accumulated |- |''Chara baltica'' |Stonewort |Pb, Cd, Hg, Ni<ref name=":02" /> |- |''Cladophora'' spp. |Blanket Weed |Pb, Cd, Hg, Ni<ref name=":02" /> |- |''Coccotylus truncatus'' | |Pb, Cd, Hg, Ni<ref name=":02" /> |- |''Fucus serratus'' |Toothed Wrack |Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn<ref name=":02" /> |- |''Furcellaria lumbricalis'' |Irish Moss |Pb, Cd, Hg, Ni<ref name=":02" /> |- |''Patella vulgata'' |Common Limpet |Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn<ref name=":02" /> |- |''Polysiphonia fucoides'' |Red Seaweed |Pb, Cd, Hg, Ni<ref name=":02" /> |- |''Ricinus communis'' |Castor Bean |Ni<ref name=":02" /> |- |''Stuckenia pectinata'' |Sago Pondweed |Pb, Cd, Hg, Ni<ref name=":02" /> |- |''Zannichellia palustris'' |Horned Pondweed |Pb, Cd, Hg, Ni<ref name=":02" /> |} {{Multiple image | align = left | direction = horizontal | total_width = 720 | image1 = Common limpets1.jpg | caption1 = ''Patella vulgata'', a species of sea snail commonly known as the common limpet of the family Patellidae | image2 = Polysiphonia fucoides Crouan.jpg | caption2 = ''Polysiphonia fucoides'', a small seaweed commonly known as red seaweed | image3 = Furcellaria lumbricalis - Tor Bay Provincial Park, Nova Scotia 2022-07-27.jpg | caption3 = ''Furcellaria lumbricalis'', a red algae commonly known as Irish Moss }} {{clear}}

== Other Examples == Alpine pennycress (''Thlaspi caerulescens''),<ref>{{Cite journal |last1=Shen |first1=Z. G. |last2=Zhao |first2=F. J. |last3=McGrath |first3=S. P. |date=1997 |title=Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum |journal=Plant, Cell & Environment |language=en |volume=20 |issue=7 |pages=898–906 |bibcode=1997PCEnv..20..898S |doi=10.1046/j.1365-3040.1997.d01-134.x |issn=1365-3040 |doi-access=}}</ref> the zinc violet (''Viola calaminaria''), spring sandwort (''Minuartia verna''), sea thrift (''Armeria maritima''), ''Cochlearia'', common bent (''Agrostis capillaris''), and plantain (''Plantago lanceolata'').<ref>''Ecosystems of Disturbed Ground'', Lawrence R Walker, Elsevier, 1999, {{ISBN|0-444-82420-0}}</ref>

==Further reading== *K.B. Axelsen and M.G. Palmgren, Inventory of the superfamily of P-Type ion pumps in Arabidopsis. Plant Physiol., 126 (1998), pp. 696–706.

==References== {{reflist}}

13. Souri Z, Karimi N, Luisa M. Sandalio. 2017. Arsenic Hyperaccumulation Strategies: An Overview. Frontiers in Cell and Developmental Biology. 5, 67. DOI: 10.3389/fcell.2017.00067.

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