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Phytoremediation of heavy metals using poplars (Populus Spp.): A glimpse of the plant responses to Copper, Cadmium and Zinc stress.
Abstract and Figures
Heavy metals (HMs) as such as cadmium (Cd), copper (Cu) and zinc (Zn) have been widespread in soils by human activities (for example, mining, smelting and agriculture). These metals can affect the environmental quality and the health of people. The risk associated to their occurrence and the possibility to cleanup them using phytoremediation systems are increasing the interest for understanding the biological basis of metal tolerance and accumulation process in plants.
Species belonging to genus Populus (poplars) are suitable candidates for phytoremediation. These trees have a high biomass production, extensive roots, high rates of transpiration and easy propagation. Also, the wide genetic diversity comprised within genus and the development of multiple biotechnologies and information resources allow a genetic improvement based on traditional and biotechnological approaches. Studies carried out in different experimental conditions show that poplars exposed to Cu, Cd and Zn exhibit distinct tolerance levels and metal accumulation patterns. This response is dependant on specific genotypes (species/hybrids and clones). Some of them have been proposed as candidate for phytostabilization and phytoextraction.
Exposition of poplars to toxic concentrations of Cd, Cu and Zn triggers different effects on growth, biomass partitioning, metal allocation, photosynthesis, carbohydrate and nitrogen metabolism, reactive oxygen species (ROS) production, among others. Plants dispose different homeostatic mechanisms for coping with metal excess. These operate at different levels and their regulation determinates the ability of plant to restrict the metal uptake and/or root to shoot transport, and compartmentalization. Biological mechanisms underlying metal homeostasis and tolerance in poplars and other tree species are only partially understood. Metal uptake in roots can be regulated by the exudation of organic acid anions, the binding effect of the cell wall and the flux of ions through plasmalem metal transporters.
In cytoplasm, metals are chelated and/or transported toward organelles by peptidic chelators. Simultaneously, excesses of metallic ions can be directed to vacuole or apoplast by membrane transporters. Metals are mobilized through the xylem from roots to aerial structures in a process driven by transpiration. Inside leaf cells, a regulated network of membrane transporters and chelators directs metals to their final destination. A further defensive line against metal induced ROS involves enzymes and reducing metabolites. Response to metal stress also includes expression of general defense proteins and signaling elements as such as calcium and ethylene.
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... Previous studies have shown that autochthonous, long-living woody species characterised by high below-and above-ground biomass and rapid growth, as well as the ability to reproduce vegetatively and capacity to tolerate various stressors, are best suited to stabilising FA landlls and reducing health problems associated with FA while restoring ecosystem functions (Carlson and Adriano, 1991;Pietrzykowski et al., 2018;Kostićet al., 2022b). Species from the Salicaceae family stand out when it comes to being used for the phytoremediation and revitalisation of polluted habitats, and in particular those from the Populus genus, which is characterised by high tolerance to a variety of environments (Zacchini et al., 2009;Guerra et al., 2011). However, species of Populus, as a thoroughly mapped genus, differ widely in their uptake patterns, as well as adaptation abilities under varying abiotic conditions (Dos Santos Utmazian et al., 2007;Zacchini et al., 2009;Di Lonardo et al., 2011;Tőzseŕ et al., 2023). ...
The enormous quantities of fly ash (FA) produced by thermal power plants is a global problem and safe, sustainable approaches to reduce the amount and its toxic effects are still being sought. Vegetation cover comprising long-living species can help reduce FA dump-related environmental health issues. However, the synergistic effect of multiple abiotic factors, like drought, low organic matter content, a deficit of essential nutrients, alkaline pH, and phytotoxicity due to high potentially toxic element (PTE) and soluble salt content, limits the number of species that can grow under such stressful conditions. Thus, we hypothesised that Populus alba L., which spontaneously colonised two FA disposal lagoons at the ‘Nikola Tesla A’ thermal power plant (Obrenovac, Serbia) 3 years (L3) and 11 years (L11) ago, has high restoration potential thanks to its stress tolerance. We analysed the basic physical and chemical properties of FA at different weathering stages, while the ecophysiological response of P. alba to multiple stresses was determined through biological indicators [the bioconcentration factor (BCF) and translocation factor (TF) for PTEs (As, B, Cr, Cu, Mn, Ni, Se, and Zn)] and by measuring the following parameters: photosynthetic efficiency and chlorophyll concentration, non-enzymatic antioxidant defence (carotenoids, anthocyanins, and phenols), oxidative stress (malondialdehyde (MDA) concentrations), and total antioxidant capacity (IC50) to neutralise DPPH free radical activity. Unlike at L3, toxic As, B, and Zn concentrations in leaves induced oxidative stress in P. alba at L11, shown by the higher MDA levels, lower vitality, and reduced synthesis of chlorophyll, carotenoids, and total antioxidant activity, suggesting its stress tolerance decreases with long-term exposure to adverse abiotic factors. Although P. alba is a fast-growing species with good metal accumulation ability and high stress tolerance, it has poor stabilisation potential for substrates with high As and B concentrations, making it highly unsuitable for revitalising such habitats.
... Poplar species, known as deep-rooted plants with high transpiration rates (Guerra, Gainza-Cortéa, Pérez-Castro, & Zamadio, 2011), can effectively decrease the risk of contaminant leaching from surface water into groundwater (Bolan, Park, Robinson, Naidu, & Huh, 2011; Poplar as a woody model for the phytomanagement of trace element contaminated soils Ciadamidaro et al., 2014), tolerates high TE concentrations and accumulates TE in its tissues without showing toxic effects (Domínguez, Maranon, Murillo, Schulin, & Robinson, 2008). For all these reasons, this woody species has been extensively used for revegetation of land heavily contaminated with TE and so far for the use for phytoremediation purposes (Villette et al., 2019). ...
... Many aromatic plants remain unexplored for its potential in phyto-strategies and biological effects. Poplars are tree species that have favorable characteristics for phytoremediation strategies that include quick establishment, fast growth, large biomass accumulation, extensive and deep root systems, high rates of transpiration, ease asexual propagation, grow effortlessly on marginal lands, are not edible and can live for long [126]. Such plants should be investigated more for both their phytoremediation potential and biological properties. ...
Crop diseases due to fungal pathogens cause significant resulting economic losses in agriculture. For management of crop diseases, farmers use synthetic pesticides. However, the frequent application of these chemicals leads to accumulation in soil and therefore presenting pollution problems. Essential oils (EOs) sourced from aromatic plants are safer alternatives and are effective against a variety of crops pathogens. In addition to their role as the sources of EOs, aromatic plants are gaining much attention in rehabilitation strategies. In phytoremediation processes, suitable plants species are used to clean-up polluted sites. Mining activities and electricity generation processes have resulted in significant amounts of tailings and coal fly ash. Mine tailings and coal fly ash are disposed in dumpsites, converting productive lands to unusable waste sites. These solid waste materials contain toxic metals and therefore posing serious risks to the health of the environment. Aromatic plants can be cultivated in contaminated sites and therefore be used for restoration of polluted lands. The EOs can be sourced from these aromatic plants as they are free from metal-toxicity and can therefore be used to generate revenues. This review highlights the role of aromatic plants in the control of crops pathogens and also their application in phytoremediation processes.
Phytoremediation is a cost-effective and environmentally friendly approach to reclaim heavy metal-contaminated soils. The phytoremediation using tree species has been preferred over annual crops as they produce higher biomass and accumulate heavy metals for prolonged period. Toona ciliata M. Roem is a large perennial tree, known to produce high biomass in short rotation, can be used for phytoremediation experiments due to their alternative use in versatile timber production and absence of linkage with food chain. Thus, present investigations were conducted to untap the potential of T. ciliata grown on lead and cadmium contaminated soils during two constitutive years 2020–21. Regarding T. ciliata raised on soils treated with different concentrations of Pb, Cd, and their combinations for six months, the results depicted that plants accumulated higher concentrations of metals in shoots than roots having bioconcentration factor (BCF) and translocation factor (TF) more than one, indicating that plants have efficient metal translocation and accumulation capability. Further, heavy metal tolerance index and survival percentage (> 85%) denote the plant’s ability to tolerate heavy metals up to 300 mgPb/kg and 25 mgCd/kg. Anatomical changes induced due to heavy metals include reduced root area as well as vascular bundle area as compared to control, also reduced stomatal pore size and increased stomatal index and trichome density suggesting the plant’s adaptive response under heavy metal stress. Furthermore, distinct accumulation patterns of lead (Pb) and cadmium (Cd) in various tissues of both leaves and roots were meticulously identified and validated through the use of cutting-edge techniques like Field Emission Scanning Electron Microscopy and Energy-Dispersive X-ray Spectroscopy (FESEM-EDS), which reflects that plant had strong enrichment ability for Pb accumulation in roots and more Cd translocation, accumulation and sequestration in aerial tissues. Hence, the present study reflects that Toona ciliata had great phytoextraction efficiency for reclaiming Pb- and Cd-contaminated soils.
The growing risk of soil cadmium (Cd) pollution calls for creative approaches to environmental remediation. The critical role that biotechnology plays in mitigating Cd pollution and cleaning up contaminated places is examined in this chapter. A thorough understanding of several biotechnology techniques, such as genetic engineering, phytoremediation, and microbial remediation, is given. The ability of microorganisms, including fungus and bacteria, to remove, change, or immobilize Cd from soil matrices is being investigated. This chapter emphasizes how important plants are for collecting and storing Cd, particularly hyperaccumulators, which help restore damaged ecosystems. Recent advancements in genetic engineering have led to the creation of plant and species variants that are tolerant of cadmium (Cd), enhancing their effectiveness in environmental cleanup procedures. The difficulties and constraints posed by biotechnology applications are discussed, taking into account ecological elements, site-specific characteristics, and regulatory requirements. This chapter promotes integrated strategies that combine traditional remediation techniques with biotechnology to achieve effective and sustainable Cd remediation. To sum up, this chapter is an invaluable tool for scholars, environmental scientists, and decision-makers. It supports ongoing initiatives to preserve ecosystems, advance sustainable agriculture, and defend human health from Cd pollution by investigating environmentally beneficial tactics. The application of biotechnology presents viable paths toward the creation of efficient and ecologically responsible ways to lessen the effects of Cd pollution.
This study investigates the phytoremediation potential of non-productive seedlings of Ailanthus altissima, Acer pseudoplatanus, and Fraxinus excelsior for lead, cadmium, and zinc accumulation in contaminated soils of Zanjan Province, an industrial area with significant pollution. The evaluation employed a completely randomized design, with three treatment levels for each element, alongside a control treatment, replicated three times over a two-year period. A total of 810 one-year-old seedlings from the three species were involved in the study. Soil contamination levels, ranging from 0 to 2000 mg/kg for lead and zinc and from 0 to 200 mg/kg for cadmium, were administered through soil pot irrigation. Sampling of seedling stems and pot soils was conducted in November of 2021 and 2022. The absorption levels of elements in the samples were determined using the dry acid digestion method and an ICP-OES atomic absorption spectrometer. Results indicate species-specific variations in metal absorption, with Ailanthus showing the highest accumulation rates. Findings suggest Ailanthus as a promising candidate for soil improvement in polluted environments, particularly in contaminated soils of Zanjan Province.
Environment and human health might be adversely affected by different organic and inorganic contaminants in the soil brought on by human ventures such as mining, waste disposal, industrial discharge, and agriculture. Various soil remediation techniques such as soil encapsulation, soil washing, chemical soil stabilisation and bioremediation, and phytoremediation have been recognised as effective, affordable, and sustainable approaches for the treatment of areas polluted with heavy metal contamination and organic pollutants. With this approach, hazardous chemicals in the soil are cleaned up using plants, the main characteristics required for plants to be suitable for phytoremediation are rapid growth and high biomass, profound root system, easily harvestable, the accumulation of high levels of contaminant in shoots, and resistant to high levels of toxicity. Mainly aromatic plants, fibrous plants, woody plants, herbaceous plants, etc., are considered as these are not directly consumed by humans and assist in revenue generation compared to edible crops. Although phytoremediation is an effective method for reducing soil contaminants, it has limitations. One of the main challenges with this technique is the disposal of metal-contaminated biomass. This chapter offers comprehensive information on the plant species used for soil contaminant reduction and the management of contaminated biomass.
Poplars have been identified as heavy metals hyperaccumulators and can be used for phytoremediation. We have previously established that their symbiosis with arbuscular mycorrhizal fungi (AMF) may alter their uptake, tolerance and distribution to excess concentrations of heavy metals in soils. In this study we hypothesised that mycorrhizal symbiosis improves the tolerance of poplars to lethal copper (Cu) concentrations, but this influence may vary among different AMF species. We conducted an experiment in a growth chamber with three Cu application levels of control (0 mg kg − 1), threshold-lethal (729 mg kg − 1) and supra-lethal (6561 mg kg − 1), and three mycorrhizal treatments (non-mycorrhizal, Rhizophagus irregularis, and Paraglomus laccatum) in a completely randomized design with six replications. The poplars did not grow after application of 729 mg Cu kg − 1 substrate, and mycorrhizal symbiosis did not help plants to tolerate this level of Cu. This can be explained by the toxicity suffered by mycorrhizal fungi. Translocation of Cu from roots to shoots increased when plants were colonised with R. irregularis and P. laccatum under threshold-lethal and supra-lethal applications of Cu, respectively. This result shows that mycorrhizal mediation of Cu partitioning in poplars depends on the fungal species and sub-strate Cu concentration. Multi-model inference analysis within each mycorrhizal treatment showed that in plants colonised with R. irregularis, a higher level of mycorrhizal colonisation may prevent Cu transfer to the shoots. We did not observe this effect in P. laccatum plants probably due to the relatively low colonisation rate (14%). Nutrient concentrations in roots and shoots were impacted by applied substrate Cu levels, but not by mycor-rhizas. Magnesium (Mg), potassium (K), and manganese (Mn) concentrations in roots reduced with enhancing applied substrate Cu due to their similar ionic radii with Cu and having common transport mechanism. Syner-gistic effect on shoot concentration between applied substrate Cu levels and Mg, K, calcium, iron (Fe), and zinc was observed. Root Cu concentration was inversely related with root K and Mn concentrations, and shoot Cu concentration had a positive correlation with shoot Fe and K concentrations. Overall, mycorrhizal symbiosis has the potential to enhance plant health and their resilience to Cu toxicity in contamination events. However, it is important to note that the effectiveness of this symbiotic relationship varies among different mycorrhizal species and is influenced by the level of contamination.
Concentrations of total nonstructural carbohydrates (TNC), soluble carbohydrates, starch, sucrose, glucose, fructose, raffinose, galactose, stachyose, mannitol and specific activities of soluble acid (AI) and neutral (NI) invertases, sucrose synthase (SuSy), hexokinase (HK), fructokinase (FK), glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and glucose 6-phosphate dehydrogenase (G6PDH) were analyzed in fine roots of Populus deltoides Bartr. ex Marsh growing at a polluted site (near copper smelters) and a control site (free from heavy pollution). Also chemical properties of the soil from both sites were assessed. In comparison with the control, fine roots from the polluted site contained greater concentrations of TNC, soluble sugars, starch and sucrose but less hexoses, so they had higher values of sucrolysis index (sucrose/hexoses). The activity of AI, NI and SuSy declined insignificantly, while specific activities of HK, FK, GAPDH and G6PDH were significantly inhibited. The results suggest that a long-term heavy metal stress leads to an accumulation of carbohydrates and altering activities of glycolysis and the oxidative pentose phosphate pathway in fine roots.
The use of plants (directly or indirectly) to remediate contaminated soil or water is known as phytoremediation. This technology has emerged as a more cost effective, noninvasive, and publicly acceptable way to address the removal of environmental contaminants. Plants can be used to accumulate inorganic and organic contaminants, metabolize organic contaminants, and encourage microbial degradation of organic contaminants in the root zone. Widespread utilization of phytoremediation can be limited by the small habitat range or size of plants expressing remediation potential, and insufficient abilities of native plants to tolerate, detoxify, and accumulate contaminants. A better understanding and appreciation of the potential mechanisms for removing contaminants from the root zone and the interaction between plants, microorganisms, and contaminants will be useful in extending the application of phytoremediation to additional contaminated sites.
Referee: Professor Alan J.M. Baker, School of Botany, The University of Melbourne, VIC 3010, Australia A relatively small yet diverse group of plants are capable of sequestering metals in their shoot tissues at remarkably high concentrations that would be toxic to most organisms. This process, known as metal hyperaccumulation, is of interest for several reasons, including its relevance to the phytoremediation of metalpolluted soils. Most research on hyperaccumulators has focused on the physiological mechanisms of metal uptake, transport, and sequestration, but relatively little is known regarding the genetic basis of hyperaccumulation. There are no known cases of major genetic polymorphisms in which some members of a species are capable of hyperaccumulation and others are not. This is in contrast to the related phenomenon of metal tolerance, in which most species that possess any metal tolerance are polymorphic, evolving tolerance only in local populations on metalliferous soil. However, although some degree of hyperaccumulation occurs in all members of the species that can hyperaccumulate, there is evidence of quantitative genetic variation in ability to hyperaccumulate, both between and within populations. Such variation does not appear to correlate positively with either the metal concentration in the soil or the degree of metal tolerance in the plant. Studies using controlled crosses, interspecific hybrids, and molecular markers are beginning to shed light on the genetic control of this variation. As molecular physiology provides greater insights into the specific genes that control metal accumulation, we may learn more about the genetic and regulatory factors that influence variable expression of the hyperaccumulation phenotype.
The use of plants (directly or indirectly) to remediate contaminated soil or water is known as phytoremediation. This technology has emerged as a more cost effective, noninvasive, and publicly acceptable way to address the removal of environmental contaminants. Plants can be used to accumulate inorganic and organic contaminants, metabolize organic contaminants, and encourage microbial degradation of organic contaminants in the root zone. Widespread utilization of phytoremediation can be limited by the small habitat range or size of plants expressing remediation potential, and insufficient abilities of native plants to tolerate, detoxify, and accumulate contaminants. A better understanding and appreciation of the potential mechanisms for removing contaminants from the root zone and the interaction between plants, microorganisms, and contaminants will be useful in extending the application of phytoremediation to additional contaminated sites.
We Studied the effects of a 2-day exposure to aluminum (Al), copper (Cu) and zinc (Zn) stress on root exudates and root apices of aseptically grown poplar (Populus tremula L.) cuttings. Aluminum induced root exudation of oxalate and citrate, Cu induced root exudation of oxalate, malate and formate, and Zn induced root exudation of formate. The threshold treatment concentrations were 100 mu M for Cu and 500 mu M for Al and Zn, corresponding to about 30 mu M C mu(2+), 140 mu M Al3+ and 290 mu M Zn2+. Simultaneous with the increase in organic acid anion exudation, sulfate and the nutrient cations K+, Ca2+ and Mg2+, were released into the solutions. Significant positive correlations between the organic acid anions and the cations indicate possible co-release. Toxicity symptoms of the poplar roots included browning of the root apices, which occurred at Cu concentrations of 50 mu M and above, at Zn concentrations of 500 mu M and above, and at an Al concentration of 1000 mu M, and callose formation, which was observed solely in response to Al concentrations of 500 mu M or higher. The results indicate that the composition of the exuded organic acid anions from poplar roots and the toxicity symptoms are specific to each of the applied heavy metals.
Silene vulgaris ssp. humilis, a heavy metal tolerant plant growing on the polluted soil of a medieval copper mining dump, accumulates considerable amounts of heavy metals (HM) in its roots and shoots. The intracellular distribution of HMs in the leaves was investigated by conventional and analytical (EDX, ESI, EELS) electron microscopy. Part of the HMs, Fe, Cu, and Zn occur as crystalline compounds on the surface of the leaves. The epidermal cell walls accumulate Fe, Ni, Cu, AI, Sn, and Zn. Cu within the cell walls is tightly bound to a protein with oxalate oxidase activity, evidencing a high homology to germin. Zn and Sn are accumulated in the cell walls as silicate. Cytoplasm and organelles contain only traces of Cu and Sn, while in the vacuoles no HMs are detected. In the epidermal cell walls, intercellular spaces, and in vacuoles there are high concentrations of Si, forming crystal-like structures. EELS and quantum-chemical calculations reveal these structures as SiO2. The role of Si in the HM-tolerance of Silene is discussed.
Cadmium and Zn were characterized in soils treated with 100 Mg ha-1 of an anaerobically digested sewage sludge from Chicago, IL. The four soils included a Chalmers silt loam (Typic Haplaquolls) (Indiana), Celina loam (Aquic Hapludalfs) (Michigan), Celina silt loam (Aquic Hapludalfs) (Ohio), and a Plano silt loam (Typic Aquidolls) (Wisconsin). The single application of sludge supplied 19 kg Cd ha-1 and 340 kg Zn ha-1. Four or five crops of barley (Hordeum vulgare L.) had been grown on each site prior to soil sampling. Soil solutions obtained by a centrifugation method contained Zn in the range of 1.4 to 10.5 μmol L-1 while Cd ranged from 18 to 135 nmol L-1. The addition of sludge increased the concentration of both metals in the soil solutions of all four soils. Evaluation of soil solution data with the computer program CEOCHEM showed that >85% of the total soluble Cd and >91% of the total soluble Zn existed as the free metal ion. Sludge addition increased the amount of Cd and Zn extracted by DTPA and 4 M HNO3. The relative increases in soil solution and extractable Cd and Zn were different in each of the four soils even though the same sludge was applied at the same rate. Diffusion coefficients measured with a cation exchange resin paper method (D(e)), ranged from 1.8 x 10-11 to 1.7 x 10-9 cm2 s-1 for Zn and from 5.2 x 10-11 to 3.2 x 10-10 cm2 s-1 for Cd. The application of sludge had little or no effect on the magnitude of D(e) for either Cd or Zn as measured by the resin paper method, but the diffusion coefficients for Zn were inversely related to soil pH. Increases in the flux of Cd and Zn to plant roots in sludge-treated soils will be a reflection of changes in soluble and extractable Cd and Zn.
The roots of six plant species, in three families, were exposed to 0, 3 and 9 μM CdCl2 for three days. The tops and roots were analyzed for total Cd. The roots were extracted with tris buffer at pH 7.2 and the extracts were analyzed for Cd and were also extracted with HAc-EDTA buffer and the extracts were analyzed for Cd, glutathione and SH compounds other than glutathione (SH-G). After exposure to Cd, the concentration of SH-G was highest in cucurbits, medium in grasses and lowest in legumes. Cd extracted from the roots at pH 7.2 increased with Cd treatment and correlated with SH-G in all families. This suggests that the Cd incorporated into the cells was detoxified by SH compounds produced in proportion to the degree of Cd incorporation. This may be one mechanism for tolerance in plants which accumulate Cd.
The percentages of Cd transported from roots to tops were highest in cucurbits and lower in grasses and legumes. Cd incorporated into the root cells (symplast), was transported to top through apoplast.
Foliar absorption of seven organic pollutants (acetone, acetonitrile, acrolein, methyl ethyl ketone (MEK), isobutyl methyl ketone (IBMK), chloroform, and benzene), and ozone was examined. Two woody species (Populus nigra and Camellia sasanqua ) were exposed to each pollutant at a concentration of 0.5 or 1.0 ppmv (μmol mol-1), and gas absorption and transpiration rates were measured simultaneously. Ozone and acrolein were effectively absorbed by both species. MEK was absorbed by C. sasanqua only. A model analysis of gas exchange rates revealed that foliar absorption of the three pollutants was predominantly through the stomata, and cuticular contribution on gas removal is, if any, very small. The plant leaves showed no detectable absorption of the other five organic pollutants. We conclude that plant leaves act as an effective sink for some organic pollutants but not for others. The factor that determines whether plant leaves can effectively absorb pollutants in this study seems to be whether the pollutant is effectively metabolized in the leaf cells.