Nickelophilous plants and their significance in phytotechnologies

Plantas niquelófilas e sua importância em fitotecnologias

TOXIC METALS IN PLANTS

Nickelophilous plants and their significance in phytotechnologies

Plantas niquelófilas e sua importância em fitotecnologias

Majeti Narasimha Vara Prasad

Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad 500046 AP, India. Email: [e-mail]

ABSTRACT

Nickeliferous soils are invaded predominantly by members of the Brassicaceae, Cyperaceae, Cunoniaceae, Caryophyllaceae, Fabaceae, Flacourtiaceae, Euphorbiaceous, Lamiaceae, Poaceae and Violaceae, and many of these plants are metal tolerant. About 300 Ni hyperaccumulating plants been identified. These members exhibit unusual appetite for toxic metals and elemental defense. Hyperaccumulators provide protection against fungal and insect attack. Investigations suggested that Ni-hyperaccumulation has a protective function against fungal and bacterial pathogens in Streptanthus polygaloides and Thlaspi montanum. Significance of nickelophilous plants and their significance in phytotechnologies are discussed in this paper.

Key words: heavy metal, hyperaccumulators, nickel, phytomanagement, tolerance.

RESUMO

Solos ricos em Ni, niquelíeros, são invadidos predominantemente por membros de Brassicaceae, Cyperaceae, Cunoniaceae, Caryophyllaceae, Fabaceae, Flacourtiaceae, Euphorbiaceous, Lamiaceae, Poaceae e Violaceae, e muitas dessas plantas são tolerantes e metais. Aproximadamente 300 plantas que superacumulam Ni (hiperacumuladoras) já foram identificadas. Estas plantas apresentam capacidade não usual de acumular metais tóxicos e defesa contra eles. O acúmulo excessivo de metais fornece proteção contra o ataque de insetos e fungos. Investigações sugerem que a hiperacumulação de Ni tem como função a proteção contra fungos e bactérias patogênicos em Streptanthus polygaloides e Thlaspi montanum. A importância de plantas niquelíferas e a sua significância em fitotecnologias são discutidas nesta revisão.

Palavras-chave: fitomanejo, metal pesado, níquel, plantas hiperacumuladoras, tolerância.

INTRODUCTION

Serpentine soils, "hotspots" of metallophyte endemics are a rich source of toxic trace elements. Serpentinized rocks are distributed all over the world viz., western north America; Newfoundland, Mount Albert in eastern Canada; Lizard peninsula, Wales and Scotland; north-east Cuba; Portugal; Italy; Balkan peninsula; Turkey; topical far east; Central Brazil; New Caledonia; south east Asia; Philippines; Japan; Zimbabwe; eastern Transvaal Loweveld of South Africa, New Zealand; greenstone belts of western Australia. (Proctor and Woodell, 1975; Sequeira et al., 1991).

Serpentine soils contain heavy metals including nickel (averaging 10 mg per gram soil), cobalt and chromium, both of the latter being present at lower levels than nickel. Serpentine soils are also characterized by high concentrations of iron and magnesium and low nutrient levels. An interesting ecosystem is established in these biotopes driven by a nickel cycle, in which hyperaccumulating trees extract nickel from deep soil and rock layers and subsequently store it in their leaves (up to 1 % Ni in leaf dry matter). When the leaves are shed from the trees, the nickel is leached out into the surrounding topsoil. The solubilized metal exerts a localized selective pressure on the topsoil microflora, which acquire resistance to high levels of nickel (> 20 mM), as well as on other plant species, which are susceptible to toxic levels of Ni. Interestingly, the microflora which was not found directly beneath the canopy but in the same soil, showed tolerance to lower levels of nickel (3 mM) compared to the resistant population. Thus, the nickel selection pressure exists as a gradient around the hyperaccumulator plants and has a dramatic effect on the composition of the local microbial population (Prasad, 2001).

Hyperaccumulator plants are geographically distributed and are found throughout the plant kingdom (Brooks, 1998; Chaney et al., 1995). To date approximately 450 taxa, ranging in growth habit from annual herbs to perennials are known. Hyperaccumulator plants have been identified on all continents, both in temperate and tropical environments (table 1). Natural occurrences of hyperaccumulators for Ni include New Caledonia, Cuba, Southeast Asia, Brazil, southern Europe and Asia Minor; for Zn and Pb include northwest Europe; and for Cu and Co include south-central Africa. Some families and genera are particularly well documented as Ni hyperaccumulators [Brassicaceae (Alyssum and Thlaspi), Euphorbiaceae (Phyllanthus, Leucocroton) and Asterceae, Zn Brassicaceae (Thlaspi), and Cu and Co (Lamiaceae, Scrophulariaceae) (Brooks, 1998). There are not many Cr hyperaccumulators in nature, but there are numerous Ni hyperaccumulators. A few Cr hyperaccumulators have been identified, partly because Cr exists predominantly in the 3⁺ oxidation state and is very insoluble and much less available for plant uptake.

Some metals may interact competitively for accumulation (e.g., Zn and Ni in calamine and serpentine soils). The number of Ni hyperaccumulator taxa are more than 300 in 35 families (table 1). They commonly have 3-4 % Ni in the dry matter of leaves. Alyssum betolonii, which is endemic to serpentine soils, is known for its high concentration of Ni (> 10,000 mg.kg^-1 in leaves). The fact that serpentine (ultramafic) soils also contain other elements such as Cr has led to the assumption that the preferential accumulation of Ni in many species of Alyssum is due to a selective uptake mechanism. Brassica juncea (Indian mustard) - a high-biomass producing plant that can accumulate Pb, Cr(VI), Cd, Cu, Ni, Zn, 90 Sr, B, and Se (Palmer et al., 2001; Prasad, 2001) produces biomass of over 20 times that of Thlaspi caerulescens (Salt et al., 1998). Brassica juncea had the best ability to transport lead to the shoots. Except for sunflower (Helianthus annuus) and tobacco (Nicotiana tabacum), other non-Brassica plants had phytoextraction coefficients less than one. B. juncea cultivars varied widely in their ability to accumulate Pb, with different cultivars ranging from 0.04 % to 3.5 % Pb accumulation in the shoots and 7 to 19% in the roots (Kumar et al., 1995).

Nickel hyperaccumulators - environmental implications

One of the most persuasive ecological explanations for hyperaccumulation of Ni and other toxic metals appears to be the defensive role against herbivores or pathogens (Dudley, 1986; Boyd and Martens, 1988, 1994). This function, which might be similar in other hyperaccumulators, can be improved if the metal is localized in the outer layers of leaves and roots. Like in other Ni accumulators, such as Hybantus floribundus, Senecio coronatus and Thlaspi montanum variety siskiyouense, and A. bertolonii, Ni has been evidenced in leaf epidermal cells as a red-stained nickel-dimethylglyoxime complex (Boyd, 1988; Farago et al., 1988; Mesjasz-Przybylowicz et al., 1994; Heath et al., 1997; Sanita Di Toppi, 2001). Furthermore, microprobe analysis has shown that leaf hairs have the highest nickel concentrations (Vergano, 1967). Similarly, in A. lesbiacum, using a micro-PIXE technique, Ni was found in the epidermis and in leaf trichomes (Gabrielle et al., 1997). The Ni hyperaccumulator T. montanum var. siskiyouense accumulates the highest Ni concentration at the leaf surface, particularly in the subsidiary cells surrounding the guard cells, and in other elongate epidermal cells, a characteristic that supports the defense hypothesis (Heath et al., 1997; Pollard and Baker, 1997).

Peterson et al. (2003) studied plants, soil, and invertebrates from Portuguese serpentine outcrops whose vegetation is dominated by the Ni hyperaccumulator Alyssum pintodasilvae. Peterson et al. (2003) concluded that grasshoppers, spiders, and other invertebrates that fed on these hyperaccumulators spread metals through food chain

Hyperaccumulation of metals is known for about 450 species of flowering plants, which take up, transport and sequester metallic elements, achieving tissue concentrations that are toxic to most organisms (Baker et al., 2000; Reeves and Baker, 2000). Several hypotheses have been advanced to explain the evolution of this trait (Boyd and Martens, 1992), with most attention focused on the hypothesis that hyperaccumulated metals may act as defenses against herbivory (Boyd, 1998; Boyd and Martens, 1998; Pollard, 2000; Pollard et al., 2000). With the exception of recent work by Wall and Boyd (2002), most studies to date have considered interactions between individual plants and herbivores, with little attention being paid to the effects of hyperaccumulators on their communities or ecosystems.

The broader environmental consequences of hyperaccumulation are of practical importance because of developing technologies that would use metal-accumulating plants to cleanse contaminated soil, termed phytoremediation (Schwitzguébel et al., 2002). A relatively unexplored risk of these techniques is that metals sequestered in plant tissues could be consumed by herbivores and thus mobilized into food chains (Chaney et al., 2000). One way to investigate the possibility of such mobilization is through studies of natural ecosystems whose vegetation is dominated by hyperaccumulating plants.

High Ni concentrations in both grasshoppers and spiders suggest that the presence of hyperaccumulating plants affects the flux of Ni to both herbivore and carnivore trophic levels. This parallels findings recently published by Boyd and Wall (2001) showing that Ni accumulated by a herbivore feeding on hyperaccumulating plants can be passed on to carnivores. In one case, Boyd and Wall (2001) reported the Ni concentration in wild-caught crab spiders (Misumena vatia, Araneae: Thomisidae) from Streptanthus polygaloides growing on California serpentines.

The consequences and ecological role of metal hyperaccumulation is expanding rapidly. Hyperaccumulation is known for aluminium, copper, cobalt, manganesium, Ni and zinc (Baker and Brooks, 1989). Caledonia, Sebertia acuminata, (a tree Sapotaceae) is the classic example capable of concentrating Ni up to 26 % (on a dry matter basis) in the xylem tissue. In Portuguese serpentine ecosystems, Alyssum serpyllifolium, a dominant weed, accumulates up to 10,000 ppm of Ni in the leaves. The objective of this paper is to highlight the scope and limitations of Ni tolerant plants and Ni accumulators and their role in promoting phytotechnologies for the environmental cleanup of heavy metals and radionuclides. The below and above-ground biodiversity of Ni tolerant plants/Ni accumulators (alien/indigenous) of metalliferous substrates, is becoming increasingly considered for the phytomanagement of metal contaminated and polluted ecosystems. The Ni tolerant plants/Ni accumulators that accumulate and/or exclude metals have tremendous potential for moving phytoremediation forward. Therefore, for phytomanagement metal-accumulating plants are seeded or transplanted into metal-polluted soil/water. If metal availability were not adequate for sufficient plant uptake, the substrate would require amendment to release or arrest the mobility of metals in the substrate. Synthetic cross-linked polyacrylates (hydrogels) have protected plant roots from heavy metal toxicity and prevented the entry of toxic metals into roots. After sufficient plant growth and metal accumulation, the above-ground portions of the plant are harvested and removed, resulting in the permanent removal of metals from the site. The retention of metals by soil organic matter is also weaker at low pH, resulting in more available metal in the soil solution for root absorption. It is suggested that the phytoextraction process is enhanced when metal availability to plant roots is facilitated through the addition of acidifying agents to the soil. Several researchers have screened fast-growing, high-biomass producing plants (e.g. Poaceae) for their ability to tolerate and accumulate metals in their shoots. The solubilized metal exerts a localized selective pressure on the topsoil microflora, which acquire resistance to high levels (e.g. Ni > 20 mM). Thus, knowledge of how plants can specifically accumulate or exclude essential elements and toxic metals, particularly of Ni tolerant plants or Ni accumulators, is fundamental for selecting species that can be utilized for phytomanagement. This includes knowledge on bioavailability of metals in rhizospheric processes as well as translocation and processing/storage in the above-ground parts of the plant.

Nickelophilous plants phytotechnologies – advantages and limitations

The importance of below and above ground biodiversity is increasingly considered for the phytomanagement of the metalliferous ecosystems. This subject is emerging as a cutting edge area of research and gaining considerable commercial significance in the contemporary field of environmental biotechnology. Globally, metal pollution has increased several thousand-fold (Adriano, 2001). Several microbes, including mycorrhizal and non-mycorrhizal fungi, agricultural and vegetable crops, ornamentals, and wild metal hyperaccumulators and excluders are being tested both under lab and field conditions for cleanup of the metalliferous substrates in the environment. Brassicaceae has the largest number of taxa viz. 11 genera and 87 species. Different genera of Brassicaceae are known to accumulate metals. Ni hyperaccumulation is reported in 7 genera and 72 species, and Zn in 3 genera and 20 species. Thlaspi species are known to hyperaccumulate more than one metal i.e T.caerulescence for Cd, Ni. Pb, and Zn; T. goesingense and T.ochroleucum for Ni and Zn and T.rotundifolium for Ni, Pb and Zn (Prasad and Freitas, 2003).

Plants that accumulate and exclude metals have tremendous potential for application in remediation of metals in the environment. Significant progress has been achieved in phytoremediation (Vangronsveld and Cunningham, 1998; Glass, 1999; Terry and Bañuelos, 2000; McCutcheon and Schnoor, 2003; Prasad, 2003, 2004a,b). This process involves raising plants hydroponically and transplanting them into metal-polluted waters where the plants absorb and concentrate the metals in their roots and shoots. As they become saturated with the metal contaminants, roots or whole plants are harvested for disposal. The phytoextraction process involves the use of plants to facilitate the removal of metal contaminants from a soil matrix. In practice, metal-accumulating plants are seeded or transplanted into metal-polluted soil and are cultivated using established agricultural practices. If metal availability in the soil is not adequate for sufficient plant uptake, chelates or acidifying agents would be applied to liberate them into the soil solution. Use of soil amendments such as synthetics (ammonium thiocyanate) and natural zeolites have yielded promising results. Synthetic cross-linked polyacrylates (hydrogels) have protected plant roots from heavy metals toxicity and prevented the entry of toxic metals into roots. After sufficient plant growth and metal accumulation, the above-ground portions of the plant are harvested and removed, resulting the permanent removal of metals from the site. Soil metals should also be bioavailable, or subject to absorption by plant roots. Chemicals that are suggested for this purpose include various acidifying agents, fertilizer salts and chelating materials. The retention of metals to by soil organic matter is also weaker at low pH, resulting in more available metal in the soil solution for root absorption. It is suggested that the phytoextraction process is enhanced when metal availability to plant roots is facilitated through the addition of acidifying agents to the soil. Chelates are used to enhance the phytoextraction of a number of metal contaminants including Cd, Cu, Ni, Pb, and Zn.

Ni tolerant plants/Ni accumulators either accumulate or exclude metals. Hence, plants with a reduced capacity to accumulate toxic metals if edible, should be a concern for human health. In contrast, plants with an enhanced capacity to accumulate toxic metals can help in phytoremediation technologies. Thus, knowledge of how plants can specifically accumulate or exclude essential elements and toxic metals, particularly in case of Ni tolerant plants or accumulators can be exploited for the selection of species that are appropriate for use in phytoremediation. This includes knowledge on bioavailability of metals, rhizospheric processes and root uptake, as well as on translocation to and processing/storage in the above-ground parts of the plant. Use of plants that hyperaccumulate specific metals and control and/or transform organic pollutants is gaining considerable significance in contemporary phytotechnology (table 2).

Ni tolerant plants and Ni accumulators have been found to be useful in phytotechnologies all over the word for transformation and containment of inorganic and organic pollutants including radionuclides (table 2). However, ecosystem design and management, investigations related to rhizosphere biotechnology, processes involved in the evolution of ecosystems and engineering of plant metabolism for enhancing the adaptive ecophysiology still remain a challenging task particularly with regard to the management of the phytomass and recycling (figures 2 and 3).

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Publication Dates

• Publication in this collection
  03 June 2005
• Date of issue
  Mar 2005