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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Nickel accumulation by Alyssum serpyllifolium subsp. lusitanicum (Brassicaceae) from serpentine soils of Bragança and Morais (Portugal) ultramafic massifs: plant–soil relationships and prospects for phytomining

I. Morais A D , J. S. Campos A D , P. J. C. Favas B D E , J. Pratas A D , F. Pita A and M. N. V. Prasad C
+ Author Affiliations
- Author Affiliations

A University of Coimbra, Faculty of Sciences and Technology, Department of Earth Sciences, 3001-401 Coimbra, Portugal.

B University of Trás-os-Montes e Alto Douro, UTAD, School of Life Sciences and the Environment, Quinta de Prados, 5000-801 Vila Real, Portugal.

C University of Hyderabad, Department of Plant Sciences, Hyderabad 500046, India.

D IMAR–CMA Marine and Environmental Research Centre/MARE – Marine and Environmental Sciences Centre, Faculty of Sciences and Technology, University of Coimbra, 3004-517 Coimbra, Portugal.

E Corresponding author. Email: pjcf@utad.pt

Australian Journal of Botany 63(2) 17-30 https://doi.org/10.1071/BT14245
Submitted: 19 September 2014  Accepted: 19 March 2015   Published: 5 May 2015

Abstract

The aim of the present study was to evaluate the possibility of using Alyssum serpyllifolium Desf. susbp. lusitanicum T.R.Dudley & P.Silva (Brassicaceae) for phytomining nickel (Ni)-rich bio-ore from serpentine soils. This species is endemic to serpentine soils of the Bragança and Morais massifs and is a Ni hyperaccumulator, containing more than 7000 mg kg–1 (dry weight) of this element. The variability of the Ni concentrations contained in the plant at different locations was verified as was its relationship with the total Ni contained in the soil or with the bioavailable Ni fraction extracted with ammonium acetate. We evaluated the biomass produced under natural conditions, and, on the basis of these values, we estimated the amount of Ni that can be removed per unit area. The results showed that considering only the aerial parts of the plant, the biomass varies between 7.04 and 9.37 t ha–1, containing a range of 0.12–0.70% Ni, allowing a withdrawal of between 12.2 and 44.0 kg Ni ha–1 per crop under natural conditions.

Additional keywords: Alyssum pintodasilvae, hyperaccumulation, Ni-hyperaccumulator species, phytoextraction, phytotechnology, serpentine flora.


References

Adriano DC (2001) ‘Trace elements in terrestrial environments: biogeochemistry, bioavailability and risks of metals.’ 2nd edn. (Springer-Verlag: New York)

Agroconsultores, COBA (1991) ‘Carta dos solos, carta do uso actual da terra e carta da aptidão da terra do nordeste de Portugal.’ (Universidade de Trás-os-Montes e Alto Douro: Vila Real, Portugal)

Aguiar C, Monteiro-Henriques T, Coutinho XP, Sánchez-Mata D (2011a) Flora. In ‘Flora and vegetation of Iberian ultramafics. Excursion guide’. (Eds A Asensi, C Aguiar, D Sánchez-Mata, TM Henriques) pp. 30–40. (Instituto Politécnico de Bragança and Universidade de Coimbra: Bragança, Coimbra, Portugal)

Aguiar C, Monteiro-Henriques T, Sánchez-Mata D (2011b) Vegetation. In ‘Flora and vegetation of Iberian ultramafics. Excursion guide’. (Eds A Asensi, C Aguiar, D Sánchez-Mata, TM Henriques) pp. 40–54. (Instituto Politécnico de Bragança and Universidade de Coimbra: Bragança, Coimbra, Portugal)

Aguiar C, Monteiro-Henriques T, Sánchez-Mata D (2013) New contributions on flora and vegetation of northeastern Portugal ultramafic outcrops. Lazaroa 34, 141–150.
New contributions on flora and vegetation of northeastern Portugal ultramafic outcrops.Crossref | GoogleScholarGoogle Scholar |

Alves S, Nabais C, Gonçalves MLS, Santos MMC (2011a) Nickel speciation in the xylem sap of the hyperaccumulator Alyssum serpyllifolium ssp. lusitanicum growing on serpentine soils of northeast Portugal. Journal of Plant Physiology 168, 1715–1722.
Nickel speciation in the xylem sap of the hyperaccumulator Alyssum serpyllifolium ssp. lusitanicum growing on serpentine soils of northeast Portugal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFGiurk%3D&md5=7107cefaf97c2caa0194e96d9ba70e59CAS | 21664714PubMed |

Alves S, Trancoso MA, Gonçalves MLS, Santos MMC (2011b) A nickel availability study in serpentinised areas of Portugal. Geoderma 164, 155–163.
A nickel availability study in serpentinised areas of Portugal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps1yhu7c%3D&md5=a0e3aa8c6dc0c12417e69d8b2f9b7396CAS |

Anacker BL (2011) Phylogenetic patterns of endemism and diversity. In ‘Serpentine: evolution and ecology in a model system’. (Eds SP Harrison, N Rajakaruna) pp. 49–79. (University of California Press: Berkeley, CA)

Anderson CWN, Brooks RR, Chiarucci A, LaCoste CJ, Leblanc M, Robinson BH, Simcock R, Stewart RB (1999) Phytomining for nickel, thallium and gold. Journal of Geochemical Exploration 67, 407–415.
Phytomining for nickel, thallium and gold.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVKjsw%3D%3D&md5=ec880093e030ceecd0493fc405847cbbCAS |

Arianoutsou M, Rundel PW, Berry WL (1993) Serpentine endemics as biological indicators of soil elemental concentrations. In ‘Plants as biomonitors. Indicators for heavy metals in the terrestrial environment’. (Ed. B Markert) pp. 179–189. (VCH-Publisher: Weinheim, Germany)

Baker AJM (1981) Accumulators and excluders: strategies in the response of plants to heavy metals. Journal of Plant Nutrition 3, 643–654.
Accumulators and excluders: strategies in the response of plants to heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlemsb8%3D&md5=9707e416a2ab60f6f789d040320dd3dcCAS |

Ball PW, Dudley TR (1993) Alyssum L. In ‘Flora Europaea, Vol. 1’ 2nd edn. (Eds TG Tutin, VH Heywood, NA Burges, DM Moore, DH Valentine, SM Walters, DA Webb) pp. 359–369. (Cambridge University Press: Cambridge, UK)

Bani A, Echevarria G, Sulçe S, Morel JL, Mullaj A (2007) In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant and Soil 293, 79–89.
In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlaktL0%3D&md5=14fd63f81a76edc8e269c0d283d74ba0CAS |

Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulçe S (2010) Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Botanica Serbica 34, 3–14.

Bani A, Echevarria G, Montargès-Pelletier E, Gjoka F, Sulçe S, Morel JL (2014) Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence. Environmental Monitoring and Assessment 186, 4431–4442.
Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmt1GnsLg%3D&md5=a44702c18cf3e638bff66e751c33bb39CAS | 24718927PubMed |

Bani A, Echevarria G, Sulçe S, Morel JL (2015) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. International Journal of Phytoremediation 17, 117–127.
Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvV2ltrY%3D&md5=c499c4b8185f53d4d75f485a3cdeb312CAS | 25237722PubMed |

Barbaroux R, Mercier G, Blais JF, Morel JL, Simonnot MO (2011) A new method for obtaining nickel from the hyperaccumulator plant Alyssum murale. Separation and Purification Technology 83, 57–65.
A new method for obtaining nickel from the hyperaccumulator plant Alyssum murale.Crossref | GoogleScholarGoogle Scholar |

Barbaroux R, Plasari E, Mercier G, Simonnot MO, Morel JL, Blais JF (2012) A new process for nickel ammonium disulfate production from ash of the hyperaccumulating plant Alyssum murale. The Science of the Total Environment 423, 111–119.
A new process for nickel ammonium disulfate production from ash of the hyperaccumulating plant Alyssum murale.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvVOmur8%3D&md5=2b6e7b458caef579914fbd441c3d5bacCAS | 22405560PubMed |

Batianoff GN, Reeves RD, Specht RL (1990) Stackhousia tryonii Bailey: a nickel-accumulating serpentine-endemic species of central Queensland. Australian Journal of Botany 38, 121–130.
Stackhousia tryonii Bailey: a nickel-accumulating serpentine-endemic species of central Queensland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpslKr&md5=8d269244e7ee1612e002dc17232f8797CAS |

Bennett FA, Tyler EK, Brooks RR, Gregg PEH, Stewart RB (1998) Fertilisation of hyperaccumulators to enhance their potential for phytoremediation and phytomining. In ‘Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining’. (Ed. RR Brooks) pp. 249–259. (CAB International: Wallingford, UK)

Boas LV, Gonçalves SC, Portugal A, Freitas H, Gonçalves MT (2014) A Ni hyperaccumulator and a congeneric non-accumulator reveal equally effective defences against herbivory. The Science of the Total Environment 466–467, 11–15.
A Ni hyperaccumulator and a congeneric non-accumulator reveal equally effective defences against herbivory.Crossref | GoogleScholarGoogle Scholar |

Brooks RR (1983) ‘Biological methods of prospecting for minerals.’ (Wiley: New York)

Brooks RR (1987) ‘Serpentine and its vegetation: a multidisciplinary approach.’ (Dioscorides Press: Portland, OR)

Brooks RR (1998a) Biogeochemistry and hyperaccumulators. In ‘Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining’. (Ed. RR Brooks) pp. 95–118. (CAB International: Wallingford, UK)

Brooks RR (1998b) Geobotany and hyperaccumulators. In ‘Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining’. (Ed. RR Brooks) pp. 55–94. (CAB International: Wallingford, UK)

Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proceedings of the Royal Society of London. Series B, Biological Sciences 200, 217–224.
Nickel accumulation by European species of the genus Alyssum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtFOrs7w%3D&md5=19ab16d38a3f9b9cfd5ecb266e041c8dCAS |

Brooks RR, Robinson BH (1998a) Aquatic phytoremediation by accumulator plants. In ‘Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining’. (Ed. RR Brooks) pp. 203–226. (CAB International: Wallingford, UK)

Brooks RR, Robinson BH (1998b) The potential use of hyperaccumulators and other plants for phytomining. In ‘Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining’. (Ed. RR Brooks) pp. 327–356. (CAB International: Wallingford, UK)

Brooks R, Lee J, Reeves R, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. Journal of Geochemical Exploration 7, 49–57.
Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXkt1KhsL8%3D&md5=0c18d4fa860a65a0ff100bc0e7f9c7cbCAS |

Brooks RR, Shaw S, Marfil AA (1981) Some observations on the ecology, metal uptake and nickel tolerance of Alyssum serpyllifolium subspecies from the Iberian peninsula. Plant Ecology 45, 183–188.
Some observations on the ecology, metal uptake and nickel tolerance of Alyssum serpyllifolium subspecies from the Iberian peninsula.Crossref | GoogleScholarGoogle Scholar |

Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends in Plant Science 3, 359–362.
Phytomining.Crossref | GoogleScholarGoogle Scholar |

Brooks RR, Robinson BH, Howes AW, Chiarucci A (2001) An evaluation of Berkheya coddii Roessler & Alyssum bertolonii Desv. for phytoremediation and phytomining of nickel. South African Journal of Science 97, 558–560.

Cabello-Conejo MI, Becerra-Castro C, Prieto-Fernández A, Monterroso C, Saavedra-Ferro A, Mench M, Kidd PS (2014) Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Plant and Soil 379, 35–50.
Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1Kms78%3D&md5=130eb2721620cad9f372f4670590814eCAS |

Cecchi L, Colzi I, Coppi A, Gonnelli C, Selvi F (2013) Diversity and biogeography of Ni-hyperaccumulators of Alyssum section Odontarrhena (Brassicaceae) in the central western Mediterranean: evidence from karyology, morphology and DNA sequence data. Botanical Journal of the Linnean Society 173, 269–289.
Diversity and biogeography of Ni-hyperaccumulators of Alyssum section Odontarrhena (Brassicaceae) in the central western Mediterranean: evidence from karyology, morphology and DNA sequence data.Crossref | GoogleScholarGoogle Scholar |

Centofanti T, Siebecker MG, Chaney RL, Davis AP, Sparks DL (2012) Hyperaccumulation of nickel by Alyssum corsicum is related to solubility of Ni mineral species. Plant and Soil 359, 71–83.
Hyperaccumulation of nickel by Alyssum corsicum is related to solubility of Ni mineral species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGmsr7I&md5=5788178d1364b893972cfdd1a2e044deCAS |

Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. Journal of Environmental Quality 36, 1429–1443.
Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtV2nsL%2FE&md5=6dd23f826db1e55bbee2e2b2306a93b6CAS | 17766822PubMed |

Chen M, Ma LQ (2001) Comparison of three aqua regia digestion methods for twenty Florida soils. Soil Science Society of America Journal 65, 491–499.
Comparison of three aqua regia digestion methods for twenty Florida soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1Ol&md5=974cc3e46ae4001b43d26a3705ea3ddaCAS |

Díez Lázaro J, Kidd PS, Monterroso Martínez C (2006) A phytogeochemical study of the Trás-os-Montes region (NE Portugal): possible species for plant-based soil remediation technologies. The Science of the Total Environment 354, 265–277.
A phytogeochemical study of the Trás-os-Montes region (NE Portugal): possible species for plant-based soil remediation technologies.Crossref | GoogleScholarGoogle Scholar | 16399000PubMed |

Dold B (2003) Speciation of the most soluble phases in a sequential extraction procedure adapted for geochemical studies of copper sulfide mine waste. Journal of Geochemical Exploration 80, 55–68.
Speciation of the most soluble phases in a sequential extraction procedure adapted for geochemical studies of copper sulfide mine waste.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltlGhtbY%3D&md5=bd1c97b2e7eb3d8b992c30f4ab9a7341CAS |

Dudley TR (1967) A new Portuguese subspecies of Alyssum serpyllifolium Desfontaines. Agronomia Lusitanica 28, 69–76.

Dudley TR (1986a) A new nickelophilous species of Alyssum (Cruciferae) from Portugal: Alyssum pintodasilvae T.R.Dudley. Feddes Repertorium 97, 135–138.

Dudley TR (1986b) A nickel hyperaccumulating species of Alyssum (Cruciferae) from Spain: Alyssum malacitanum (Rivas-Goday) T.R. Dudley. Feddes Repertorium 97, 139–141.

Escande V, Garoux L, Grison C, Thillier Y, Debart F, Vasseur JJ, Boulanger C, Grison C (2014) Ecological catalysis and phytoextraction: symbiosis for future. Applied Catalysis B: Environmental 146, 279–288.
Ecological catalysis and phytoextraction: symbiosis for future.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXms1yrtbw%3D&md5=c7b49a916ea3f690160103009928c32aCAS |

Favas PJC, Pratas J, Prasad MNV (2012) Accumulation of arsenic by aquatic plants in large-scale field conditions: opportunities for phytoremediation and bioindication. The Science of the Total Environment 433, 390–397.
Accumulation of arsenic by aquatic plants in large-scale field conditions: opportunities for phytoremediation and bioindication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFOqsbnP&md5=db1bf50f1af3bdba6a2d311e4fddbf24CAS |

Favas PJC, Pratas J, Varun M, D’Souza R, Paul MS (2014a) Accumulation of uranium by aquatic plants in field conditions: prospects for phytoremediation. The Science of the Total Environment 470–471, 993–1002.
Accumulation of uranium by aquatic plants in field conditions: prospects for phytoremediation.Crossref | GoogleScholarGoogle Scholar |

Favas PJC, Pratas J, Varun M, D’Souza R, Paul MS (2014b) Phytoremediation of soils contaminated with metals and metalloids at mining areas: potential of native flora. In ‘Environmental risk assessment of soil contamination’. (Ed. MC Hernández-Soriano) pp. 485–517. (Intech: Rijeka, Croatia) Available at http://www.intechopen.com/articles/show/title/phytoremediation-of-soils-contaminated-with-metals-and-metalloids-at-mining-areas-potential-of-nativ. [Verified 28 June 2014]

Freitas H, Prasad MNV, Pratas J (2004) Analysis of serpentinophytes from north-east of Portugal for trace metal accumulation: relevance to the management of mine environment. Chemosphere 54, 1625–1642.
Analysis of serpentinophytes from north-east of Portugal for trace metal accumulation: relevance to the management of mine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVWgsbg%3D&md5=e7e4fbbc52e5b7880b636cb9c420fad1CAS | 14675842PubMed |

Gall JE, Rajakaruna N (2013) The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In ‘Brassicaceae: characterization, functional genomics and health benefits’. (Ed. M Lang) pp. 121–148. (Nova Science Publishers: New York)

Gonçalves MT, Gonçalves SC, Portugal A, Silva S, Sousa JP, Freitas H (2007) Effects of nickel hyperaccumulation in Alyssum pintodasilvae on model arthropods representatives of two trophic levels. Plant and Soil 293, 177–188.
Effects of nickel hyperaccumulation in Alyssum pintodasilvae on model arthropods representatives of two trophic levels.Crossref | GoogleScholarGoogle Scholar |

Grison C (2015) Combining phytoextraction and ecocatalysis: a novel concept for greener chemistry, an opportunity for remediation. Environmental Science and Pollution Research 22, 5589–5591.
Combining phytoextraction and ecocatalysis: a novel concept for greener chemistry, an opportunity for remediation.Crossref | GoogleScholarGoogle Scholar | 24946705PubMed |

Jaffré T, Schmid M (1974) Accumulation du nickel par une Rubiacée de Nouvelle Calédonie: Psychotria douarrei (G. Beauvisage) Däniker. Comptes Rendus de l’Academie des Sciences de Paris Série D 278, 1727–1730.

Jaffré T, Brooks R, Lee J, Reeves R (1976) Sebertia acuminata a nickel-accumulating plant from New Caledonia. Science 193, 579–580.
Sebertia acuminata a nickel-accumulating plant from New Caledonia.Crossref | GoogleScholarGoogle Scholar | 17759588PubMed |

Kabata-Pendias A (2011) ‘Trace elements in soils and plants.’ 4th edn. (CRC Press: Boca Raton, FL)

Kay KM, Ward KL, Watt LR, Schemske DW (2011) Plant speciation. In ‘Serpentine: evolution and ecology in a model system’. (Eds SP Harrison, N Rajakaruna) pp. 71–95. (University of California Press: Berkeley, CA)

Kidd PS, Monterroso C (2005) Metal extraction by Alyssum serpyllifolium ssp. lusitanicum on mine-spoil soils from Spain. The Science of the Total Environment 336, 1–11.
Metal extraction by Alyssum serpyllifolium ssp. lusitanicum on mine-spoil soils from Spain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKqtLrE&md5=445a6e3f7cb44d7cd779306a15160adaCAS | 15589245PubMed |

Krämer U (2010) Metal hyperaccumulation in plants. Annual Review of Plant Biology 61, 517–534.
Metal hyperaccumulation in plants.Crossref | GoogleScholarGoogle Scholar | 20192749PubMed |

Kruckeberg AR (1984) ‘California serpentines: flora, vegetation, geology, soils and management problems.’ (University of California Press: Berkeley, CA)

Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. Journal of Environmental Quality 33, 2090–2102.
The effect of pH on metal accumulation in two Alyssum species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVegs7vE&md5=de3115e8f7d536f4c60b6110798dc2d7CAS | 15537931PubMed |

Kumar A, Maiti SK (2013) Availability of chromium, nickel and other associated heavy metals of ultramafic and serpentine soil/rock and in plants. International Journal of Emerging Technology and Advanced Engineering 3, 256–268.

Li Y-M, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003a) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant and Soil 249, 107–115.
Development of a technology for commercial phytoextraction of nickel: economic and technical considerations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVyrs74%3D&md5=0708e75b82b0162996210868f5a224c2CAS |

Li Y-M, Chaney RL, Brewer EP, Angle JS, Nelkin J (2003b) Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel-contaminated soils. Environmental Science & Technology 37, 1463–1468.
Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel-contaminated soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslSls7g%3D&md5=133c31dab250e455d75549f4f2ead6a8CAS |

Liu X, Li X, Chermaine Ong SM, Chu Z (2013) Progress of phytoremediation: focus on new plant and molecular mechanism. Journal of Plant Biology & Soil Health 1, 5

Lombini A, Dinelli E, Ferrari C, Simoni A (1998) Plant–soil relationships in the serpentinite screes of Mt Prinzera (northern Apennines, Italy). Journal of Geochemical Exploration 64, 19–33.
Plant–soil relationships in the serpentinite screes of Mt Prinzera (northern Apennines, Italy).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXis1yntA%3D%3D&md5=afdc054ea4fe4942b435faf0e21a1323CAS |

Ma Y, Rajkumar M, Freitas H (2009) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75, 719–725.
Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVChur4%3D&md5=228efb25f3252beb3375d3a0879cf05aCAS | 19232424PubMed |

Marques FO (2011) Geology of the ultramafic area of the Trás-os-Montes. Geology of the Bragança massif. In ‘Flora and vegetation of Iberian ultramafics. Excursion guide’. (Eds A Asensi, C Aguiar, D Sánchez-Mata, TM Henriques) pp. 22–24. (Instituto Politécnico de Bragança and Universidade de Coimbra: Bragança, Coimbra, Portugal)

Marques FO, Ribeiro A, Munhá JM (1996) Geodynamic evolution of the continental allochthonous terrane (CAT) of the Bragança Nappe Complex, NE Portugal. Tectonics 15, 747–762.
Geodynamic evolution of the continental allochthonous terrane (CAT) of the Bragança Nappe Complex, NE Portugal.Crossref | GoogleScholarGoogle Scholar |

McGrath SP (1998) Phytoextraction for soil remediation. In ‘Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining’. (Ed. RR Brooks) pp. 261–287. (CAB International: Wallingford, UK)

Minguzzi C, Vergnano O (1948) Il contenuto di nichel nelle ceneri di Alyssum bertolonii. Atti della Società Toscana di Scienze Naturale 55, 49–74.

Morais I, Campos JS, Pratas J, Pita F (2012) Estudo preliminar de fitomineração utilizando Alyssum serpyllifolium Desf. subsp. lusitanicum (Dudley & P. Silva) em solos serpentiníticos dos maciços de Bragança e de Morais (Nordeste de Portugal). In ‘Para desenvolver a Terra. Memórias e notícias de geociências no espaço lusófono’. (Coords M Quinta-Ferreira, MT Barata, FC Lopes, AI Andrade, MH Henriques, R Pena dos Reis, E Ivo Alves) pp. 341–350. (Imprensa da Universidade de Coimbra: Coimbra, Portugal)

Morrison RS, Brooks RR, Reeves RD (1980) Nickel uptake by Alyssum species. Plant Science Letters 17, 451–457.
Nickel uptake by Alyssum species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhs1Slsb4%3D&md5=2600870ccab7b2054c6005f6295c0b4bCAS |

Nicks LJ, Chambers MF (1998) A pioneering study of the potential of phytomining for nickel. In ‘Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining’. (Ed. RR Brooks) pp. 313–325. (CAB International: Wallingford, UK)

O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In ‘Serpentine: evolution and ecology in a model system’. (Eds SP Harrison, N Rajakaruna) pp. 97–137. (University of California Press: Berkeley, CA)

Oliveira DPS, Santana HMCV, Guimarães CAMF (2009) The Bragança podiform chromite field in NE Portugal. In ‘Smart science for exploration and mining. Proceedings of the 10th biennial SGA meeting. Vol. 1’. (Ed. PJ Williams) pp. 158–160. (Economic Geology Research Unit, James Cook University: Townsville, Qld)

Oze C, Skinner C, Schroth AW, Coleman RG (2008) Growing up green on serpentine soils: biogeochemistry of serpentine vegetation in the Central Coast Range of California. Applied Geochemistry 23, 3391–3403.
Growing up green on serpentine soils: biogeochemistry of serpentine vegetation in the Central Coast Range of California.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWms73F&md5=a2fe112a83373de9cb2d5eb664b63a74CAS |

Pereira E (2011) Geology of the ultramafic area of the Trás-os-Montes. Morais massif. In ‘Flora and vegetation of Iberian ultramafics. Excursion guide’. (Eds A Asensi, C Aguiar, D Sánchez-Mata, TM Henriques) pp. 18–21. (Instituto Politécnico de Bragança and Universidade de Coimbra: Bragança, Coimbra, Portugal)

Peterson LR, Trivett V, Baker AJM, Aguiar C, Pollard AJ (2003) Spread of metals through an invertebrate food chain as influenced by a plant that hyperaccumulates nickel. Chemoecology 13, 103–108.

Pilon-Smits E, Pilon M (2002) Phytoremediation of metals using transgenic plants. Critical Reviews in Plant Sciences 21, 439–456.
Phytoremediation of metals using transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlKitro%3D&md5=5031fbe457313dd5bed566ae2762526eCAS |

Pin C, Paquette JL, Ábalos B, Santos FJ, Gil Ibarguchi JI (2006) Composite origin of an early Variscan transported suture: ophiolitic units of the Morais Nappe Complex (north Portugal). Tectonics 25, TC5001
Composite origin of an early Variscan transported suture: ophiolitic units of the Morais Nappe Complex (north Portugal).Crossref | GoogleScholarGoogle Scholar |

Pinto da Silva AR (1968) A flora e a vegetação das áreas ultrabásicas do Nordeste Transmontano. Agronomia Lusitana 30, 175–364.

Pollard AJ, Smith JAC (2014) Population-level variation in nickel tolerance and hyperaccumulation in Alyssum serpyllifolium from the Iberian Peninsula. Paper 40. In ‘Abstracts of the 8th international conference on serpentine ecology’. p. 71. (Kota Kinabalu, Sabah, Malaysia)

Prasad MNV (2005) Nickelophilous plants and their significance in phytotechnologies. Brazilian Journal of Plant Physiology 17, 113–128.
Nickelophilous plants and their significance in phytotechnologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVWrsLg%3D&md5=1737f1414162732435c8e816784f14a7CAS |

Prasad MNV, Freitas HMO (1999) Feasible biotechnological and bioremediation strategies for serpentine soils and mine spoils. Electronic Journal of Biotechnology 2, 36–50.

Rajakaruna N (2004) The edaphic factor in the origin of species. International Geology Review 46, 471–478.
The edaphic factor in the origin of species.Crossref | GoogleScholarGoogle Scholar |

Reeves RD (1992) The hyperaccumulation of nickel by serpentine plants. In ‘The ecology of ultramafic serpentine soils’. (Eds AJM Baker, J Proctor, RD Reeves) pp. 253–277. (Intercept: Andover, UK)

Reeves RD, Baker AJM, Borhidi A, Berazain R (1996) Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytologist 133, 217–224.
Nickel-accumulating plants from the ancient serpentine soils of Cuba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFKlsLc%3D&md5=fd3caffb6a094cdb888125308d3bafd7CAS |

Robinson BH, Chiarucci A, Brooks RR, Petit D, Kirkman JH, Gregg PEH, Dominicis VD (1997) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. Journal of Geochemical Exploration 59, 75–86.
The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlWmsrs%3D&md5=ec723413861966e5e4b337909ce5dd45CAS |

Robinson BH, Brooks RR, Gregg PEH, Kirkman JH (1999) The nickel phytoextraction potential of some ultramafic soils as determined by sequential extraction. Geoderma 87, 293–304.
The nickel phytoextraction potential of some ultramafic soils as determined by sequential extraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXos1GktA%3D%3D&md5=7ec2697b00c02bd9544072293cddec0eCAS |

Roger F, Matte Ph (2005) Early Variscan HP metamorphism in the western Iberian Allochthon: a 390 Ma U-Pb age for the Bragança eclogite (NW Portugal). International Journal of Earth Sciences 94, 173–179.
Early Variscan HP metamorphism in the western Iberian Allochthon: a 390 Ma U-Pb age for the Bragança eclogite (NW Portugal).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFCjt7c%3D&md5=82f4942160e992ca871d9acb4c4af940CAS |

Rout GR, Samantaray S, Das P (2000) Effects of chromium and nickel on germination and growth in tolerant and non-tolerant populations of Echinochloa colona (L.) Link. Chemosphere 40, 855–859.
Effects of chromium and nickel on germination and growth in tolerant and non-tolerant populations of Echinochloa colona (L.) Link.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXht1ygsLw%3D&md5=60dd374b91d6fb60c74905823e30ce7bCAS | 10718579PubMed |

Sequeira EM (1969) Toxicity and movement of heavy metals in serpentinic soils (north-eastern Portugal). Agronomia Lusitana 30, 115–154.

Sequeira EM (2011) Soils. In ‘Flora and vegetation of Iberian ultramafics. Excursion guide’. (Eds A Asensi, C Aguiar, D Sánchez-Mata, TM Henriques) pp. 24–29. (Instituto Politécnico de Bragança and Universidade de Coimbra: Bragança, Coimbra, Portugal)

Sequeira EM, Pinto da Silva AR (1992) The ecology of serpentinized areas of north-east Portugal. In ‘The ecology of areas with serpentinized rocks. A world review’. (Eds BA Roberts, J Proctor) pp. 169–197. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Severne B, Brooks R (1972) A nickel-accumulating plant from Western Australia. Planta 103, 91–94.
A nickel-accumulating plant from Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xht1Gkurk%3D&md5=907a2b76d2d2ba825f1a799ffe12a364CAS | 24481475PubMed |

Shah MT, Begun S, Khan S (2010) Pedo and biogeochemical studies of mafic and ultramafic rocks in the Mingora and Kabal areas, Swat, Pakistan. Environmental Earth Sciences 60, 1091–1102.
Pedo and biogeochemical studies of mafic and ultramafic rocks in the Mingora and Kabal areas, Swat, Pakistan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptFKgtLc%3D&md5=7165778721c868871d8ba57859aa3da8CAS |

Shah MT, Ara J, Muhammad S, Khan S, Asad SA, Ali L (2014) Potential heavy metals accumulation of indigenous plant species along the mafic and ultramafic terrain in the Mohmand Agency, Pakistan. CLEAN – Soil, Air, Water 42, 339–346.
Potential heavy metals accumulation of indigenous plant species along the mafic and ultramafic terrain in the Mohmand Agency, Pakistan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtleku7bP&md5=9aff93f14e1bc8ec636e61e42f088168CAS |

Sheoran V, Sheoran AS, Poonia P (2009) Phytomining: a review. Minerals Engineering 22, 1007–1019.
Phytomining: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXps1Wqtbo%3D&md5=fbd504856e0563dc0dc89034dd3d72f9CAS |

Sheoran V, Sheoran AS, Poonia P (2010) Role of hyperaccumulators in phytoextraction of metals from contaminated mining sites: a review. Critical Reviews in Environmental Science and Technology 41, 168–214.
Role of hyperaccumulators in phytoextraction of metals from contaminated mining sites: a review.Crossref | GoogleScholarGoogle Scholar |

van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013a) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant and Soil 362, 319–334.
Hyperaccumulators of metal and metalloid trace elements: facts and fiction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2ks7bF&md5=bee356700f51fe2ae7218429ac2a5674CAS |

van der Ent A, Baker AJM, Van Balgooy MMJ, Tjoa A (2013b) Ultramafic nickel laterites in Indonesia (Sulawesi, Halmahera): mining, nickel hyperaccumulators and opportunities for phytomining. Journal of Geochemical Exploration 128, 72–79.
Ultramafic nickel laterites in Indonesia (Sulawesi, Halmahera): mining, nickel hyperaccumulators and opportunities for phytomining.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjt1Sgu7w%3D&md5=b69d9aea1cf8b76b4ad464d9558b4d87CAS |

van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL, Echevarria G, Fogliani B, Rongliang Q, Mulligan DR (2015) Agromining: farming for metals in the future? Environmental Science & Technology 49, 4773–4780.
Agromining: farming for metals in the future?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtV2ntrk%3D&md5=620d62e89a2db74f4eade1f1f0ea2f06CAS |

Vithanage M, Rajapaksha AU, Oze C, Rajakaruna N, Dissanayake CB (2014) Metal release from serpentine soils in Sri Lanka. Environmental Monitoring and Assessment 186, 3415–3429.
Metal release from serpentine soils in Sri Lanka.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht12jsL0%3D&md5=6fdc44a6057a8a0746022f272fe8038bCAS | 24464398PubMed |

Wilson-Corral V, Anderson CWN, Rodriguez-Lopez M (2012) Gold phytomining. A review of the relevance of this technology to mineral extraction in the 21st century. Journal of Environmental Management 111, 249–257.
Gold phytomining. A review of the relevance of this technology to mineral extraction in the 21st century.Crossref | GoogleScholarGoogle Scholar | 22940825PubMed |

Zhang X, Houzelot V, Bani A, Morel JL, Echevarria G, Simonnot MO (2014) Selection and combustion of Ni-hyperaccumulators for the phytomining process. International Journal of Phytoremediation 16, 1058–1072.
Selection and combustion of Ni-hyperaccumulators for the phytomining process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtV2ltLzP&md5=4056ee5606a4078fb8ce086eb90af0e4CAS | 24933902PubMed |