Nickel Hyperaccumulator Research Articles

Assessing Plant Phytoextraction Potential Through Mathematical Modeling

ABSTRACT One of the most serious and long-term consequences of environmental pollution is heavy metal contamination of soils. Elements such as zinc, cadmium, lead, nickel, and chromium are being released into the environment by many industrial processes and have now reached concentrations that are of concern. Phytoremediation is a new, low-cost, and environmentally friendly technique that relies on the natural properties of some plants to clean-up the ground through their ability to take up metals from the soil. Hyperaccumulator plants, capable of accumulating metals far in excess of any normal physiological requirement, represent a most promising tool for metal phytoextraction, but the in field establishment of their conditions for utilization needs a long period because of the plant life-cycle. The use of a mathematical model is proposed to process growth and uptake data from in vitro experiments for a rapid assessment of the time and concentration parameters for the deployment of hyperaccumulator plants for phytoextraction purposes. This preliminary research has been carried out using Alyssum bertolonii Desv., a nickel hyperaccumulator endemic to Italian serpentine soils.

Seedling mortality of metal hyperaccumulator plants resulting from damping off by Pythium spp.

Seedling mortality of Alyssum serpyllifolium ssp. lusitanicum and A. murale, both nickel hyperaccumulators, was reduced by increasing concentrations of metal within plant tissues when inoculated with the fungi Pythium mamillatum or P. ultimum, both of which cause damping-off disease of seedlings. Pythium mamillatum, isolated from nickel-rich serpentine soil, was more tolerant of nickel than P. ultimum, isolated from low-metal control soil, and was more pathogenic than P. ultimum towards seedlings containing high concentrations of metal. These results support the hypothesis that metal hyperaccumulation by plants is closely linked to increased protection against disease.

Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae).

Plants use chemical defences to reduce damage from herbivores and the effectiveness of these defences can be altered by biotic and abiotic factors, such as herbivory and soil resource availability. Streptanthus polygaloides, a nickel (Ni) hyperaccumulator, possesses both Ni-based defences and organic defences (glucosinolates), but the extent to which these defences interact and respond to environmental conditions is unknown. S. polygaloides plants were grown on high-Ni and low-Ni soil and concentrations of Ni and glucosinolates were compared with those of the congeneric non-hyperaccumulator, S. insignus spp. insignus, grown under the same conditions. Ni contents were highest (4000 μg g-1 dry tissue) in S. polygaloides plants grown on high-Ni soil. Glucosinolate content was significantly higher in S. insignus than in S. polygaloides suggesting that plants defended by Ni produce a lower concentration of organic defences. In a separate experiment, high-Ni S. polygaloides plants were exposed to simulated herbivory or live folivores to determine the inducibility of Ni-based and organic defences. Contents of Ni were not affected by either herbivory treatment, whereas glucosinolate concentrations were >30% higher in damaged plants. We concluded that the Ni-based defence of S. polygaloides is not induced by herbivory.

Soil Amendments Affecting Nickel and Cobalt Uptake by Berkheya coddii: Potential Use for Phytomining and Phytoremediation

Plants with inordinately high concentrations of heavy metals (‘hyperaccumulators’) can be used for phytoremediation (removal of contaminants from soils) or phytomining (growing a crop of plants to harvest the metals). Pot trials were used to investigate the effects of MgCO3, CaCO3, sulphur, chelating agents (NTA, DTPA, EDTA) and acid mine tailings on nickel and cobalt uptake by the South African nickel hyperaccumulator Berkheya coddii. Plants were grown in a nickel-rich ultramafic (‘serpentine’) soil diluted with pumice. Both MgCO3and CaCO3caused significant decreases in the uptake of both metals, as well as decreasing their solubility in the soil. After the addition of MgCO3,there was a significant increase in soil pH, so the reduction in plant-metal uptake could not be solely attributed to the action of magnesium alone. Since CaCO3had no significant effect on soil pH, this indicated that calcium inhibits the uptake of both cobalt and nickel. All three chelating agents caused a significant reduction in plant uptake of nickel, despite increasing the solubility (plant availability) of these elements in the soil. Cobalt uptake was unaffected. Sulphur, and the addition of acid mine tailings, caused a highly significant increase in nickel and cobalt uptake, relative to the controls. Sulphur could be used as a low-cost soil amendment to enhance the metal uptake of crops grown on ultramafic soils. Thus, land management procedures would enhance phytoremediation and phytomining operations for nickel and cobalt.

Aphids are unaffected by the elemental defence of the nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae)

Nickel hyperaccumulation, resulting in plant Ni contents of >1000 mg kg−1 dry mass, has been shown to defend plants against folivorous herbivores. We determined whether this elemental defence tactic protected hyperaccumulating plants from attack by a phloem-feeding herbivore. We used the pea aphid, Acyrthosiphon pisum, and the Ni-hyperaccumulating plant Streptanthus polygaloides. Aphids were allowed to colonize mixed arrays of S. polygaloides in which plants either were hyperaccumulating Ni, not hyperaccumulating Ni and treated with a systemic insecticide, or not hyperaccumulating Ni. Aphid numbers g−1 dry mass of plant biomass were lowest for the insecticide treatment, intermediate for low-Ni plants, and highest for plants hyperaccumulating Ni. Artificial liquid aphid diet, amended with varying levels of Ni, resulted in decreased aphid survival at 2500 mg kg−1 Ni dry mass (or 5.03 mM Ni). We concluded that Ni levels in the phloem of hyperaccumulating plants of S. polygaloides were < 5.03 mM and, as a result, were not effective in defending plants against aphid attack.

Nickel Hyperaccumulation in the Serpentine Flora of Cuba

Extraordinary uptake (hyperaccumulation) of nickel (Ni), reaching concentrations of 0.1–5.0%, about 1000-times greater than those usually found in flowering plants, has been reported over the period 1948–1996 in about 190 species that grow on Ni-rich serpentine soils derived from ultramafic rocks in various parts of the world. A recent study of the families Buxaceae and Euphorbiaceae identified a further 80 Ni hyperaccumulators from the very large ultramafic flora of Cuba, the largest number found to date in any one country. A much wider investigation of the elemental content of plants from the Cuban ultramafic flora, reported here with representative analyses of the corresponding soils, has revealed Ni hyperaccumulation in an additional 50 taxa (in 16 genera and eight families). The number of hyperaccumulators is greatest on the oldest serpentine soils, which are believed to have been available for colonization for the last 10–30 million years. Both Ni hyperaccumulators, and serpentine endemic species generally, are much more frequent on these old soils, occurring in the eastern and western extremities of Cuba, than on those developed within the last million years in the central part of the country. Hyperaccumulating plants of the families Acanthaceae, Asteraceae, Clusiaceae, Myrtaceae, Ochnaceae, Oleaceae, Rubiaceae and Tiliaceae are discussed.

Plant–soil relationships in the serpentinite screes of Mt. Prinzera (Northern Apennines, Italy)

Relations between `bioavailable' metals in serpentinite soils and metal content of plants living on the serpentinite outcrop of Mt. Prinzera (Italy) were investigated. The taxa considered were Alyssum bertolonii Desv., Minuartia laricifolia subsp. ophiolitica (L.) Sch. et Th., Cerastium arvense subsp. suffruticosum (L.) Nym., Biscutella laevigata subsp. prinzerae Raffaelli et Baldoin, Dianthus sylvestris Wulfen group and Silene armeria L. Plants and soils from their rhizospheres were sampled in 1994 and 1995. The soils are enriched in Fe, Al, Cr, Co and Zn as compared to fresh rocks. `Bioavailable' fractions, evaluated by extractions with 0.02 M EDTA and 0.005 M DTPA, show enrichment in Fe, Co and Ni. Metal distribution in plants did not show significant changes between 1994 and 1995, even though different analytical strategies were applied. Our data confirm Alyssum bertolonii as a nickel hyperaccumulator, and the other serpentinophyte Minuartia laricifolia subsp. ophiolitica yielded relatively high metal contents. The determination of nickel distribution between shoots and roots enabled the identification of different strategies of plant adaptation to high Ni concentration in soil: hyperaccumulators, taxa with moderate levels of Ni, taxa with low translocation of Ni, taxa with low metal absorption. These groups can be generalized since the taxa studied all grow on similar soils, and metal availability strongly depends on the degree of weathering of serpentinite. Other metals, such as Cu and Zn, are actively absorbed by plants, both because of relatively high availability in the soil environment and for the active biological role they have.

Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait

Adaptations to particular stresses may occur only in populations experiencing those stresses or may be widespread within a species. Nickel hyperaccumulation is viewed as an adaptation to high-Ni (serpentine) soils, but few studies have determined if hyperaccumulation ability is restricted to populations from high-Ni soils or if it is a constitutive trait found in populations on both high- and low-Ni soils. We compared mineral element concentrations of Thlaspi montanum var. montanum plants grown on normal and high-Ni greenhouse soils to address this question. Seed sources were from four populations (two serpentine, two non-serpentine) in Oregon and northern California, USA. Plants from all populations were able to hyperaccumulate Ni, showing Ni hyperaccumulation to be a constitutive trait in this species. Populations differed in their ability to extract some elements (e.g., Ca, Mg, P) from greenhouse soils. We noted a negative correlation between tissue concentrations of Ni and Zn. We suggest that the ability to hyperaccumulate Ni has adaptive value to populations growing on non- serpentine soil. This adaptive value may be a consequence of metal-based plant defense against herbivores/pathogens, metal- based interference against neighboring plant species, or an efficient nutrient scavenging system. We suggest that the Ni hyperaccumulation ability of T. montanum var. montanum may be an inadvertent consequence of an efficient nutrient (possibly Zn or Ca) uptake system.

Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata

The nickel content in different parts of the hyperaccumulating tree Sebertia acuminata was analysed by atomic absorption spectroscopy. Nickel was found to be mainly located in laticifers. The total nickel content of a single mature tree was estimated to be 37 kg. By gel filtration and NMR spectroscopy, citric acid was unequivocally identified as counter ion for about 40% of this metal present. Nitrate was assumed to be a further partner for a complete ionic balance. Phytochelatins were not found to be involved in nickel detoxification in Sebertia. The localization of nickel complexes inside the laticifers was demonstrated by light microscopy as well as by scanning electron microscopy in combination with an EDX system for the analysis of elements. A repellent effect of the plant sap was observed on the fruit fly Drosophila melanogaster indicating that in hyperaccumulating plants nickel functions as an agent to prevent predation.

The Role of Metal Transport and Tolerance in Nickel Hyperaccumulation by Thlaspi goesingense Halacsy.

Metal hyperaccumulators are plants that are capable of extracting metals from the soil and accumulating them to extraordinary concentrations in aboveground tissues (greater than 0.1% dry biomass Ni or Co or greater than 1% dry biomass Zn or Mn). Approximately 400 hyperaccumulator species have been identified, according to the analysis of field-collected specimens. Metal hyperaccumulators are interesting model organisms to study for the development of a phytoremediation technology, the use of plants to remove pollutant metals from soils. However, little is known about the molecular, biochemical, and physiological processes that result in the hyperaccumulator phenotype. We investigated the role of Ni tolerance and transport in Ni hyperaccumulation by Thlaspi goesingense, using plant biomass production, evapotranspiration, and protoplast viability assays, and by following short- and long-term uptake of Ni into roots and shoots. As long as both species (T. goesingense and Thlaspi arvense) were unaffected by Ni toxicity, the rates of Ni translocation from roots to shoots were the same in both the hyper- and nonaccumulator species. Our data suggest that Ni tolerance is sufficient to explain the Ni hyperaccumulator phenotype observed in hydroponically cultured T. goesingense when compared with the Ni-sensitive nonhyperaccumulator T. arvense.

The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining

Pot trials and tests in outside plots were carried out on the South African Ni hyperaccumulator plant Berkheya coddii in order to establish its potential for phytoremediation of contaminated soils and for phytomining of Ni. Outside trial plots showed that a dry biomass of 22 t/ha could be achieved after moderate fertilisation. Pot trials with varying soil amendments with nitrogen and phosphorus fertilisers showed enhanced uptake of Ni with increasing nitrogen addition, though there was no reaction to phosphorus. The Ni content of the plant was directly related to the ammonium acetate extractable fraction of Ni in a wide range of natural and artificial substrates. Excision of shoots induced a dramatic increase in the Ni content in the new growth (5500 μg/g compared with 1800 μg/g Ni). When plants were grown in pots with Ni added to the substrate (0–1%), the Ni content of the plants rose to a maximum value of about 1% dry mass. The data from this last experiment were used to calculate the probable Ni yield (kg/ha) of plants grown in nickel-rich soils in different parts of the world. It was calculated that moderately contaminated soils (100 μg/g Ni) could be remediated with only two crops of Berkheya coddii. The potential of this species for phytomining has also been evaluated and it is proposed that a yield of 100 kg/ha of Ni should be achievable at many sites worldwide. Phytomining is also discussed in general terms for other metals as well as Ni.

The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel

Experiments were carried out in Italy on the potential use of the hyperaccumulator Alyssum bertolonii in phytomining of ultramafic soils for Ni. In situ experimental plots at Murlo, Tuscany were fertilized with various regimes during a 2-year period. The best fertilizer treatment (N + K + P) gave a threefold increase of the biomass of reproductive matter to 9.0 t/ha without dilution of the unfertilized Ni content. A Ni content of 0.8% in dry matter (11% in ash), would give a Ni yield of 72 kg/ha without need of resowing for a further crop. There was no correlation between the age of a plant and its Ni content. The long-term cropping sustainability of the soils was simulated by sequential extractions with KH phthalate solutions at pH 2, 4 and 6 that showed a limiting available Ni content of 768 μg/g. Thus just over seven croppings at pH 6 in the rhizosphere would reduce the available Ni pool by 30%. A proposed model for phytomining involves harvesting the crop after 12 months and burning the material to produce a sulphur-free bio-ore with about 11% Ni. Utilising the energy of combustion is also discussed. It is considered that Alyssum bertolonii or other Alyssum species might be used for phytomining throughout the Mediterranean area including Anatolia, as well as in Western Australia and the western United States. The economic limits of phytomining are proposed and at current world prices, the technique would only be feasible for Ni and Co with plants of at least the same biomass as Alyssum. Plants of higher biomass and similar uptake potential as for Ni, could extend the limits to other elements.

Effects of heavy metals on the growth and mineral composition of a nickel hyperaccumulator

Abstract Alyssum pintodasilvae Dudley is a nickel (Ni) hyperaccumulator endemic to serpentine soils of north‐east Portugal. In one experiment, the effects of cadmium (Cd), chromium (Cr), copper (Cu), Ni, lead (Pb), and zinc (Zn) on the growth and mineral composition of this species were evaluated. The growth of A. pintodasilvae, measured by dry matter accumulation, was not influenced by the presence of Cr, Cu, Pb, Ni, or Zn in the soil, but Cd applications led to significant decreases in dry matter yield. The addition of heavy metals to the soil resulted in increased uptake and translocation by A. pintodasilvae but only Ni was accumulated to high levels. In a second experiment, two cuts of A. pintodasilvae, grown on a Ni‐enriched soil, were compared. Nickel concentrations were higher in the second cut, suggesting the possibility of continued growth and harvest of this plant to detoxify Ni‐contaminated soils.

Free histidine as a metal chelator in plants that accumulate nickel

A NUMBER of terrestrial plants accumulate large quantities of metals such as zinc, manganese, nickel, cobalt and copper in their shoots1. The largest group of these so-called 'metal hyperaccumulators' is found in the genus Alyssum, in which nickel concentrations can reach 3% of leaf dry biomass2,3. Apart from their intrinsic interest, plants exhibiting this trait could be of value in the decontamination of metal-polluted soils4–6. However, the biochemical basis of the capacity for metal accumulation has not been elucidated. Here we report that exposing hyperaccumu-lator species of Alyssum to nickel elicits a large and proportional increase in the levels of free histidine, which is shown to be coordinated with nickel in vivo. Moreover, supplying histidine to a non-accumulating species greatly increases both its nickel tolerance and capacity for nickel transport to the shoot, indicating that enhanced production of histidine is responsible for the nickel hyperaccumulation phenotype in Alyssum.

The ecological significance of nickel hyperaccumulation: a plant chemical defense.

Nickel hyperaccumulating plants have more than 1000 mg Ni kg-1 dry weight when grown on nickel-bearing soils. We hypothesized that Ni hyperaccumulation could serve as a chemical defense against herbivores In feeding experiments with potential insect herbivores and Ni hyperaccumulating plants, only those inseets fed leaves from plants grown on non-nickel-bearing soil survived or showed a weight gain. Among chemical parameters measured, only Ni content of plants was sufficient to explain this result. When subjected to herbivory by lepidopteran larvae, plants grown on Ni-amended soil showed greater survival and yield than plants on unamended soil. Ni hyperaccumulation may be an effective plant chemical defense against herbivores because of its high lethality, apparent low cost, and broad spectrum of toxicity.

Comparison of the chemical changes in the rhizosphere of the nickel hyperaccumulator Alyssum murale with the non-accumulator Raphanus sativus

Changes in pH and redox potential were studied in the rhizosphere soil of a nickel hyperaccumulator plant (Alyssum murale) and of a crop plant, radish (Raphanus sativus). Differences in rhizosphere pH and reducing activity were found between the lateral and the main roots of both species, but the pH changes in the rhizosphere were similar in both species. Changes in pH were associated with the relative uptakes of cations and anions; whether the concentrations of heavy metals in the growth medium did not have any effect on the rhizosphere pH. The source of nitrogen (ammonium or nitrate) was the major factor determining the pH of the rhizosphere of both species. The redox potential of the rhizosphere was influenced by both the N-source and the concentrations of heavy metals. When heavy metals were not present in the growth medium, and nitrate was the N-source, the reducing capacity of A. murale roots was enhanced. However, the reducing activity of A. murale was always smaller than that of radish. Therefore, the mechanism of metal solubilization by the hyperaccumulator plant does not involve either the reduction of pH in the rhizosphere or the release of reductants from roots. The acidification and reducing activity of the roots of A. murale was always smaller than that of R. sativus.

Serpentinite, Harzburgite, and Vegetation on Subantarctic Macquarie Island

Macquarie Island (54°35′S, 158°55′E) is a subantarctic island composed of oceanic crustal rocks lifted above sea level during the middle to late Pleistocene. The northern third of its plateau contains large areas of serpentinite and harzburgite. Outcrops of basalt rich in phenocrysts of olivine and pyroxine occur farther south. Where large enough to influence soil formation all these areas are marked by sparse vegetation cover with small, apparently slow-growing plants and a high percentage of bare ground, in sharp contrast to adjacent areas. Soils and plants on serpentinite and harzburgite areas contain high nickel and magnesium, and have lowered calcium/magnesium ratios. There are no species confined to the serpentinite and harzburgite rocks and none is a hyperaccumulator of nickel, presumably because of the short time with respect to evolution that the island has been above sea level.

Comparative studies of nickel, cobalt, and copper uptake by some nickel hyperaccumulators of the genus Alyssum

The uptake of Ni, Co, and Cu by the nickel hyperaccumulator Alyssum troodii Boiss and the non-accumulator Aurinia saxatilis (L.) Desv. were studied in pot trials using artificial rooting media with varying concentrations of the metals added as soluble salts, singly and in combination. The ability of five other Ni hyperaccumulating species of Alyssum to hyperaccumulate Co was also investigated.

Accumulation mechanisms and heavy metal tolerance of a nickel hyperaccumulator

Abstract Alyssum bertoionii Desv., a crucifer which grows only in Tuscany on serpentine soil, is characterized by high Ni concentration in its leaves and a high tolerance to this element. In this research, the Co and Zn tolerance of A. bertolonii has been tested and compared with that of Ni. Although the Zn concentration in the serpentine soil on which the plant grows is lower than that of Co, root growth showed no significant difference for these two elements. In excised roots, on the other hand, Co and Zn compete with Ni uptake and accumulation. Seedlings do not show any inhibition in the translocation of these three elements. They are all rapidly carried to and accumulate in the shoots, but the uptake and traslocation of Zn does not show the saturation trend found for Ni and Co. The same gel filtration fractions contain the three elements in association with malic acid, involved in Ni tolerance.

Characterization of the nickel-rich extract from the nickel hyperaccumulator Dichapetalum gelonioides

Abstract Following the discovery of the hyperaccumulation of nickel by the Philippine plant Dichapetalum gelonioides subsp. tuberculatum , the nature of the nickel in aqueous plant extracts has been investigated by gel chromatography, ion exchange chromatography, high voltage electrophoresis and GC-MS. The purified extract contained 18% Ni, 24% citric acid and 43% malic acid(mole ratio 1:0.4:1), the remainder consisting of small amounts of Ca, Mg, K, Na and a trace of tartaric acid. Experimental observations are discussed in terms of the stabilities of complexes of citrate and malate with Ni. By using X-ray crystallography it was shown that crystals obtained from a Ni-citrate-malate solution simulating the extract, contain Ni exclusively in the form of an anionic Ni(II)-citrato complex.