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Article

The Suitability of Several Grasses for the Remediation of Hotspots Affected by Cadmium Contamination

by
Jolanta Korzeniowska
* and
Ewa Stanislawska-Glubiak
Department of Weed Science and Tillage Systems in Wroclaw, Institute of Soil Science and Plant Cultivation-State Research Institute in Pulawy, Orzechowa 61, 50-540 Wroclaw, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(7), 1127; https://doi.org/10.3390/agriculture14071127
Submission received: 7 May 2024 / Revised: 3 July 2024 / Accepted: 10 July 2024 / Published: 11 July 2024
(This article belongs to the Section Agricultural Soils)
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Abstract

:
Areas contaminated with cadmium require remediation because it is a highly toxic element. The aim of this study was to assess the Cd tolerance of four grass species (Poa pratensis, Lolium perenne, Festuca rubra, and Festuca pratensis) and to identify the most useful grass for the phytostabilization of areas with extremely high Cd content in the soil. Additionally, the relationship between grass tolerance to Cd and the glutathione (GSH) content in shoots was examined. Two series of pot experiments were carried out using soil artificially contaminated with Cd. Three levels of contamination were used—30, 60, and 130 mg kg−1 Cd—against a control. The plants were cut down 2 months after sowing. At the Cd1 level, L. perenne showed the highest tolerance to Cd (tolerance index TI = 86), while P. pratensis had the lowest tolerance (TI = 65). At Cd2, the TIs ranged from 52 to 59, indicating a similar tolerance of all species. Cd3 was most harmful to L. perenne (TI = 24), while P. pratensis was the most tolerant (TI = 31). Grassroots accumulated much more Cd than shoots. L. perenne showed the greatest increase in root Cd at each contamination level, followed by F. pratensis and then P. pratensis and F. rubra. It is noteworthy that the tolerance of grasses to Cd3 was related to the GSH content in shoots. P. pratensis and F. rubra increased the GSH content 4.6 and 3.6 times, respectively, while L. perenne and F. pratensis only increased it 2.3 times compared to the control plants.

1. Introduction

Cadmium (Cd) is toxic to plants, animals, and humans due to its ability to disrupt the function of many enzymes, leading to protein damage [1]. It is a heavy metal with relatively high mobility. When present in the soil, it can easily enter plant cover, threatening the entire food chain [2].
Excessive accumulation of Cd in the soil is the result of human activity. The largest amounts of Cd can be attributed to mining and smelting activities [3,4]. In addition, the burning of fossil fuels and rubbish is a source of cadmium, as are phosphate fertilizers, sewage sludge, and industrial waste [5].
There is no consensus in the EU on acceptable limits for cadmium in soil. Member states take different approaches to setting toxicity thresholds, which usually depend on land use and soil features [6]. This creates differences in the level of acceptable limits. For example, the limit value for Cd in agricultural soils varies between 0.4 and 1.0 mg kg−1 in Slovakia and between 2 and 5 mg kg−1 in Poland [7,8]. At the same time, the value limit for industrial areas varies from 15 mg kg−1 in Italy, through 20 mg kg−1 in Poland, to 30 mg kg−1 Cd in Belgium and Slovakia [9].
Despite the low recommended limits for Cd in soil, there are places in the world with very high Cd contamination. This is especially true for mining areas and areas near smelters. Mineral extraction and the metallurgical industry destroy the natural structure of the soil and pollute the environment with toxic metals through exhaust emissions and the storage of sewage, slag, and tailings [10]. In recent years, works in the literature have reported the significant contamination of soil by heavy metals, including Cd, in China. This has been caused by the rapid development of China’s industry over the past two decades. Wu et al. [11] studied toxic metals in agricultural soils near Pb-Zn mining and smelting areas in southwestern China and found that the Cd concentrations there ranged from 1.02 to 109 mg kg−1. Zhang et al. [12] noted that the Cd levels in arable soil around other mining and smelting sites in China were as high as 153 mg kg−1. Zeng et al. [4] showed that soil near one of China’s zinc smelters had extremely high Cd content; the average for the 323 samples was 798 mg kg−1 Cd. High cadmium contamination of industrial soils is also encountered in other countries. Citeau et al. [13] recorded 109 mg kg−1 Cd in soil from an agricultural area of a former industrial complex in northern France. According to Tosha et al. [14] and Chrastný et al. [15], the soils around a zinc smelter near Olkusz in Poland contained 64–153 mg kg−1 Cd. Additionally, a study by Stefanowicz et al. [3] showed that historical Zn and Pb mining areas in southern Poland are contaminated with Cd. In the 73 old dumps from this area studied, the Cd levels ranged from 5 to 522 mg kg−1.
Cd-contaminated areas require necessarily remediation. Plants growing in contaminated areas can take up and accumulate significant amounts of cadmium in their tissues, which is highly dangerous for animal consumers [16]. Various remediation techniques are used to exclude heavy metals from the soil. The use of plants for this purpose is called phytoremediation. This technique is distinguished by its lack of negative impact on the structure, biological activity, and fertility of the soil and its low cost [17]. Among phytoremediation techniques, two of the most popular are phytoextraction and phytostabilization. The first involves taking metals from the soil and translocating them to the above-ground parts of plants, which are then removed from the contaminated area. Plants used for this purpose should be characterized by rapid growth, high biomass, and high tolerance to heavy metals [18]. This technique is not very effective and a positive effect can only be achieved after a long time [19]. The second technique, phytostabilization, involves the immobilization and reduced mobility of heavy metals. Metals can be accumulated by the roots absorbed on their surface or precipitated in the rhizosphere. Plants ideal for phytostabilization should have a well-developed root system and be tolerant of high concentrations of heavy metals. It is also important that they are characterized by a high accumulation of metals in the roots and a low translocation from roots to shoots [20,21]. Phytostabilization can be successfully applied to Cd-contaminated soils [22,23,24].
The effectiveness of phytostabilization depends on the tolerance of plants to contaminants. Plants have developed different adaptation mechanisms to defend themselves against metal toxicity. These involve eliminating the stress factor by reducing the uptake of metal from the soil or the uptake of the metal and its detoxification inside the plant [25]. Plants use different defense strategies for different metals, as well as multiple strategies simultaneously for a single metal [26,27].
The primary method for metal detoxification within a plant is the metals’ chelation by various chemical compounds and transportation to cellular structures, where they become metabolically inactive. Cd ions accumulated by the plant are detoxified by phytochelatins (PCs), which are synthesized from the tripeptide glutathione (GSH) [28]. PCs form complexes with Cd ions, which move into the vacuole, where they pose no threat to the plant. This mechanism indicates a primary role for GHS in Cd detoxification in plants [29,30].
Grasses may be useful for the phytostabilization of heavy-metal-contaminated sites [31,32]. They are characterised by rapid growth, high biomass, a well-developed root system and a perennial growth pattern. In addition, they can accumulate large amounts of metals in both roots and shoots [33,34,35]. The literature reports the suitability of grasses of the genera Lolium and Festuca for this purpose [36,37,38].
The aim of the study was to assess the tolerance of four grass species to Cd and to identify the grass most suitable for the phytostabilization of this metal in the soil on the basis of its accumulation in roots and transfer to shoots. An additional objective was to test the relationship between grass tolerance to Cd and GSH content in shoots.

2. Methods

To investigate the responses of grasses to soil contamination with Cd, two series of pot experiments were performed in the greenhouse, one in spring (III–V) and one in autumn (IX–X). In both series, pots were filled with 2 kg of the same soil, brought from a field located in Jelcz-Laskowice near Wroclaw, Poland. Soil with a relatively low pH and low sorption complex was used in the experiments to increase Cd mobility (Table 1).
Before sowing grasses, the experimental soil was artificially contaminated with cadmium in the form of CdCl2, resulting in 4 levels of Cd in the soil: 0 (uncontaminated control), 0.7 mg kg−1; Cd1, 31 mg kg−1; Cd2, 62 mg kg−1; and Cd3, 130 mg kg−1. Four grass species were used as test plants: Poa pratensis L. (cv. Niweta), Lolium perenne L. (cv. Kinga), Festuca rubra L. (cv. Adio), and Festuca pratensis Huds. (cv. Fantasia). As a result, 16 experimental treatments (4 Cd levels × 4 grasses) were tested in a single experiment, each in 4 replications.
The grass seed came from the Nieznanice Breeding and Production Plant, part of the Malopolska Plant Breeding company. Grasses were sown 2 weeks after the introduction of Cd into the soil. Initially, more seeds were sown and after about 2 weeks, 30 individuals per pot were left. Three weeks after sowing, NPK fertilization was applied at a rate of 50 mg N as NH4NO3, 8.5 mg P as NaH2PO4·H2O, and 27.5 mg K as KCl per pot by watering the plants with the fertiliser solution. Plants were harvested 2 months after sowing. Grass shoots were cut 5 mm above the ground. The roots were removed from the pots, cleaned of soil, and washed thoroughly with tap water, followed by a 2-h rinse in distilled water using a rotary stirrer. Shoots and roots were dried (24 h at 50 °C and 3 h at 100 °C, respectively), carefully weighed, finely ground, and chemically analyzed.
All chemical analyses were performed at the Main Laboratory of the Institute of Soil Science and Plant Cultivation in Puławy, accredited by the Polish Centre for Accreditation (certificate number AB 339, based on the PN-EN ISO/IEC 17025 standard) [39].
The Cd content in the soil was determined using the FAAS method after digestion in aqua regia [40] The total organic carbon (TOC) content was determined with the Thiurin method using potassium dichromate [41], pH using the potentiometric method in 1 mol KCl dm−3 [42], and texture with the aerometric method [43]. In addition, the contents of available phosphorus and potassium were determined in the soil using the Enger–Riehm method [44,45], respectively) and magnesium with the Schachtschabel method [46]. Cd in shoots and roots was determined using the FAAS method, having first dry-ashed the material in a muffle furnace and digested it with 20% nitric acid [47]. A standard reference material IPE 952 (International Plant-Analytical Exchange) from Wageningen (The Netherlands) was used for quality control purposes.
The glutathione content in plant material was determined by derivatization with DTNB (5.5-dithio-bis-(2-nitrobenzoic acid)). After crushing the sample, previously frozen in liquid nitrogen, it was ground in phosphate buffer medium (pH = 7.5) with the addition of DTNB solution, while cooling with liquid nitrogen. The obtained extract was centrifuged and then purified by double filtration. The purified sample was analyzed by HPLC.
In order to compare the tolerance of the tested grasses to excess cadmium, a tolerance index (TI) was calculated according to the Wilkins formula [48]. This index expresses the ratio of the biomass of plants on the contaminated treatment to that of the plants on the control treatment:
T I = C d   b i o m a s s g C o n t r o l   b i o m a s s   ( g ) × 100
In order to compare metal accumulation in plants, bioaccumulation factors (BF) were calculated for shoots and roots using the following formulas, according to Melo et al. [49]:
B F s h o o t = C d   c o n c e n t r a t i o n   i n   s h o o t s   ( m g / k g ) C d   c o n c e n t r a t i o n   i n   s o i l   ( m g / k g )
B F r o o t = C d   c o n c e n t r a t i o n   i n   r o o t s m g / k g C d   c o n c e n t r a t i o n   i n   s o i l m g / k g
The translocation of cadmium from roots to aboveground parts (shoots) was determined based on the translocation factor (TF) expressed by the following formula [49]:
T F = C d   c o n c e n t r a t i o n   i n   s h o o t s   ( m g / k g ) C d   c o n c e n t r a t i o n   i n   r o o t s   ( m g / k g )
As the results of the spring and autumn experiments were very similar to each other, it was decided to average them. All results of plant biomass and Cd concentration in shoots and roots were given as the means from these two experiments. ANOVA calculations were performed using the Statgraphics v5.0 software (StatPoint Technologies, Inc., Warrenton, VA, USA). Multiple comparisons among groups were made with Tukey’s honest significant difference test (p < 0.05).

3. Results

3.1. Biomass

Significant differences were observed in the biomass yields of the studied grass species on control treatments without Cd. P. pratensis and F. rubra are smaller grasses that produced biomass of 2.15 and 2.07 g pot−1, respectively. In contrast, the larger grasses, L. perenne and F. pratensis, produced 3.48 and 3.43 g pot−1. Therefore, it was not possible to compare grass responses to toxic Cd based on absolute biomass yields and relative biomass yields were used for this purpose (Figure 1).
All tested grass species reduced shoot biomass with increasing Cd in the soil. However, differences between species in their tolerance of Cd were observed (Figure 1).
At the lowest level of contamination (Cd1), the reduction in shoot biomass relative to the control was arranged as follows: L. perenne (15%), F. pratensis (23%), F. rubra (25%), and P. pratensis (31%). Cd2 contamination reduced the shoots of Festucas by 39% and L. perenne and P. pratensis by 45%. At the highest level of Cd3 contamination, biomass decreased to a similar level in all grasses, ranging from 66 to 72%, with the lowest biomass loss in P. pratensis.
The plants also responded with a reduction in root growth (Figure 1). A similar decrease in their biomass was found compared to shoots, with a tendency toward a greater reduction in roots than in shoots. At the Cd1 level, the order of grass species for root reduction was the same as for shoots and was as follows: L. perenne (13%), F. pratensis (20%), F. rubra (36%), and P. pratensis (39%). At the Cd2 level, there was a 43% root reduction in F. pratensis and a 52% reduction in the other species. The highest level of Cd3 soil contamination resulted in an 82% root reduction in L. perenne and 74% in the other grasses.

3.2. Tolerance Index

The tolerance of the tested grasses to soil Cd contamination was determined by the average reduction in biomass of the shoots and roots (Table 2). The mean TI for the four grasses decreased with increasing soil contamination levels and was 75 for Cd1, 54 for Cd2, and 28 for Cd3. At the Cd1 level, L. perenne was the most tolerant, with a TI of 86, while P. pratensis proved to be the most sensitive to the presence of this metal in the soil, as indicated by a TI of 65. At Cd2, the TIs ranged from 52 to 59, indicating a similar tolerance across all species. The highest level of Cd3 contamination was most damaging to L. perenne, which had a TI of 24. At the same time, P. pratensis on Cd3 had the highest tolerance, with a TI of 31.

3.3. Cd Concentration in Soil

Post-harvest soil at control treatments contained between 0.6 and 0.9 mg kg−1 Cd, depending on the grass species (Figure 2). At the Cd1 level, 30–32 mg kg−1 Cd was recorded in the soil, while at the Cd2 and Cd3 levels, these concentrations ranged from 56 to 64 and 120 to 137, respectively.

3.4. Cd Concentration in Plants

In the control soil, uncontaminated with Cd, all grasses had similar concentrations of this element in shoots, ranging from 1.0 to 1.7 mg kg−1 Cd (Table 3). As soil contamination increased, there was a gradual increase in Cd in the shoots of all grasses, with species varying in concentration levels.
In comparison with the control, the concentration of Cd in shoots on Cd1 treatment increased 34–41 times, depending on the grass species. For Cd2 treatment, 71–81 times more Cd was found compared to the control and, in the case of Cd3 treatment, a 163–167-fold increase in Cd was observed. The two species L. perenne and F. pratensis were found to be identical with regard to the increase in Cd at successive levels of soil contamination relative to the control. Furthermore, these grasses, compared to the other two species, had the lowest increase in Cd in shoots relative to the control on Cd1 and, at the same time, the highest increase when on Cd3.
The roots of the grasses accumulated significantly more Cd than the shoots. Between 6.4 and 12.9 d mg kg−1 Cd was found in the roots of plants from the control treatments, depending on the grass species (Table 3). With respect to the control, the Cd concentration in roots on Cd1 increased by 102–186 times. Cd2 showed a 171–423-fold increase in Cd in roots and Cd3 exhibited the greatest difference among species. Cd in roots increased 248–713 times compared to the control. The largest relative increase in Cd in roots, at any level of Cd contamination, was recorded in L. perenne, followed by F. pratensis, while P. pratensis and F. rubra always showed a much smaller increase in Cd in roots.

3.5. Cd Distribution in Plants

The grass species tested accumulated Cd primarily in the roots, as evidenced by bioaccumulation factors several 10 s of times higher for roots (BFroot) compared to those for shoots (BFshoot). Depending on the grasses, BFroot, calculated as the mean for Cd1, Cd2, and Cd3, ranged from 23 to 49, while BFshoot ranged from 1.3 to 2.1 (Table 4).
At the same time, very little Cd transport from the roots to the shoots was found in all grasses. The TF, calculated as the mean of the three Cd levels, ranged from 0.03 to 0.09. This means that only 3–9% of the Cd was accumulated in the shoots compared to the amount accumulated in the roots (Table 4). P. pratensis was characterized by the lowest BFroot, which was very similar at each Cd level. At the same time, this grass, compared to the others, transported the most Cd from the roots to the shoots. L. perenne, on the other hand, had the highest BFroot, especially at the Cd2 level, and the lowest TF. On the other hand, in Festuca grasses, a decrease in BFroot was observed with increasing levels of soil contamination and, at the same time, a trend toward increasing TF.

3.6. Glutathione Content in Plants

The grasses tested on Cd-uncontaminated soil differed in their shoot glutathione (GSH) content, which is probably a species feature (Table 5). While P. pratensis, F. rubra, and F. pratensis had similar levels of GSH, L. perenne contained about four times less of it than the above-mentioned grasses. In response to Cd stress, an increase in shoot GSH was observed in all species. On Cd3 treatment, P. pratensis and F. rubra increased their GSH content by 4.6 and 3.6 times, respectively, compared to plants from the uncontaminated treatment. In L. perenne and F. pratensis, only 2.3 times more GSH was found on Cd3 treatment than under uncontaminated soil conditions.

4. Discussion

The limits of acceptable Cd concentration in soil adopted in different countries vary from a few to several 10 s of mg kg−1 depending on the land use and type of soil. The aim of our study was to test the feasibility of using grasses for the phytoremediation of areas with very high levels of this metal, generally near industrial areas. For the study, we used soil artificially contaminated with doses of 30, 60, and 130 mg kg−1 Cd. Similar levels of soil contamination, such as 25, 50, and 100 mg kg−1 Cd, were used in a pot experiment by Kumar and Fulekar [50]. In the study by Sukario et al. [51], the Cd doses were even higher, ranging from 170 to 250 mg kg−1 depending on the soil texture.
Plants suitable for the phytostabilization of heavy-metal-contaminated areas should have a bioaccumulation factor for roots (BFroot) > 1 and a metal translocation factor from roots to shoots (TF) < 1 [52,53]. All the grasses studied showed a high capacity to accumulate Cd in the roots and reduced the transportation of this element to the shoots. BFroot values ranged from 23 to 60 and depended on the grass species and the level of soil Cd contamination. At the same time, TFs did not exceed a value of 0.1. Although, based on BFroot and TF, all four tested types of grass can be considered useful for the phytostabilization of Cd-contaminated soil; the tested species defended themselves against Cd in the soil in different ways, which can be assessed based on the mass of shoots and roots produced. The tolerance of grasses to Cd, as expressed by the tolerance index (TI), decreased with increasing Cd contamination of the soil; however, there were differences between species within each Cd level.
P. pratensis and L. perenne differed the most from each other. At 30 mg kg−1 Cd in the soil, the highest tolerance to this metal was found in L. perenne and the lowest in P. pratensis. At 60 mg kg−1 Cd, both grasses showed equal TI. At 130 mg kg−1 Cd, the highest tolerance was observed in P. pratensis and the lowest in L. perenne, which was the opposite of the findings at Cd1. The tolerance indices for grasses of the genus Festuca took intermediate values between the TI for P. pratensis and L. perenne, except at the contamination level of 60 mg kg−1, where the tolerance of F. rubra and F. pratensis was slightly better than the above-mentioned species.
The variation in tolerance of grasses to soil Cd contamination can be linked to the fact that different species have developed different defense mechanisms against the toxic effects of this metal. One strategy is to exclude the uptake of Cd from the soil by binding it into inaccessible forms through various chemical compounds secreted by the roots.
The defense mechanism of P. pratensis seemed to be related to the avoidance of Cd uptake. The BFroot value for P. pratensis was consistent regardless of the Cd level and was the lowest of all grasses. This may indicate that Cd uptake is blocked due to its excess level in the soil. Cd uptake may be blocked through root secretions of plants growing in contaminated areas. Pinto et al. [54] observed a significant decrease in bioavailable Cd in soil as a result of the complexation of this metal by organic compounds secreted by roots. Sun et al. [55] and Huang et al. [56] showed that Cd significantly alters the composition and content of root secretions. Lapi et al. [57] found that many compounds secreted by roots modify the speciation and dynamics of Cd in soil, which may play a role in plant tolerance to this metal.
In addition to blocking Cd uptake, P. pratensis had the highest Cd transfer from roots to shoots, regardless of the Cd level, compared to other species. Furthermore, at 130 mg kg−1 Cd, the GSH concentration in the shoots of P. pratensis was higher than in other grasses. This may indicate a greater involvement of this metabolite in Cd detoxification in P. pratensis shoots compared to the other studied species. Cd sequestration involving GSH, as a precursor of PCs, can occur in both shoots and roots [58,59,60]. This process involves the deposition of chelated forms of Cd in cellular structures, such as vacuoles or cell walls, where the metal does not interfere with metabolic reactions [25,61,62].
In contrast to P. pratensis, the defense mechanism of L. perenne was probably to accumulate Cd in the roots and limit the transfer of this metal to the shoots, thus protecting the photosynthetic apparatus from damage. This is confirmed by the BFroot values, which were the highest at each Cd level compared to other grasses. Moreover, they were 2–2.5 times larger compared to P. pratensis. At the same time, Cd transfer from the roots to the shoots of L. perenne was three to four times lower and the glutathione concentration in the shoots was two times lower than in P. pratensis. This suggests that, in L. perenne, Cd detoxification occurred mainly in the roots. This conclusion is supported by the study by Jiang et al. [38]. The authors found that Cd accumulation by L. perenne occurred mainly in the roots and that Cd tolerance improved with increasing GSH and PCs. Cd accumulation in the roots of L. perenne was also confirmed by the study by Lambrechts et al. [63].
According to Bali et al. [64], Cd in root cells is transported mainly to vacuoles. Metallothioneins, PCs, and organic acids play a key role in this transportation. Parotta et al. [65] demonstrate that Cd can also be retained in the cell wall as a result of proteins or phosphates bound to the cell wall. Secondary modifications of the cell wall, e.g., by lignin deposition, may be an additional barrier.
A similar mechanism to L. perenne for Cd accumulation in roots, with reduced transfer of this metal to shoots, was shown by grasses of the genus Festuca. However, the BFroot values of these grasses were lower and TF values higher than for L. perenne. Some differences were noted between F. rubra and F. pratensis. At contaminations of 60 and 130 mg kg−1 Cd, F. rubra accumulated less Cd in the roots and transferred more to the shoots than F. pratensis. Moreover, at 130 mg kg−1 Cd in the soil, the GSH content in F. rubra shoots was higher than in F. pratensis.
It was observed that at the lowest level of Cd contamination (30 mg kg−1), a better defense strategy was to accumulate the metal in the roots and limit its transfer to the aboveground parts, rather than blocking its uptake from the soil. This mode of Cd detoxification was demonstrated by L. perenne and grasses of the genus Festuca, which had a higher tolerance index compared to P. pratensis. In contrast, the defense mechanism of P. pratensis in blocking Cd uptake from the soil was more effective under conditions with the highest soil Cd content (130 mg kg−1).

5. Conclusions

All four types of grass tested met the basic requirement for phytostabilization, BFroot > 1 and TF < 1, but differed in their tolerance to Cd, as measured by biomass production. Under the conditions of the experiment, their suitability for phytostabilization depended on the level of soil contamination:
−
At a level of 30 mg kg−1 Cd, L. perenne was definitely the most efficient. This grass accumulated the most Cd in the roots, transferred the least Cd to the shoots, and showed the highest tolerance compared to the other grasses tested;
−
At a level of 60 mg kg−1 Cd, F. pratensis was the most effective. This grass produced more biomass than the other grasses and had low Cd transfer from roots to shoots;
−
At a level of 130 mg kg−1 Cd, P. pratensis could be used. Although it accumulated less Cd in the roots and transferred most Cd to the shoots, its Cd tolerance was higher than that of the other grasses. In the phytostabilization process, with such high contamination, survival and the production of a lot of biomass were most important. The distribution of Cd between roots and shoots was less important, especially since TF was 10 times lower than the required value of this parameter for phytostabilization (TF < 1).
A defense mechanism such as accumulating Cd in the roots and blocking its transfer to the shoots was effective at contamination levels of 30 and 60 mg kg−1 Cd. In contrast, at contamination levels of 130 mg kg−1, the stress factor exclusion strategy used by P. pratensis through blocking Cd uptake from the soil was superior.
The tolerance of grasses to Cd at the highest level of contamination was related to the GSH content of the shoots. P. pratensis had the highest tolerance and, at the same time, the highest increase in GSH compared to the control.
Our research has shown that grasses can be used for the phytoremediation of areas with extreme levels of Cd contamination. The next research challenge is to deepen our understanding of defense mechanisms against Cd stress. In addition, the suitability of other grass species for phytoremediation should be determined. A comparison of cultivar tolerance within a single species would also be needed.

Author Contributions

Conceptualization, J.K. and E.S.-G.; investigation, J.K. and E.S.-G.; methodology, J.K. and E.S.-G.; writing—original draft, J.K. and E.S.-G.; writing—review and editing, J.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Polish Ministry of Agriculture and Rural Development under 4.12: Scientific Research Program of the Institute of Soil Science and Plant Cultivation in Pulawy.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Kabata-Pendias, A.; Mukherjee, A.B. Trace Elements from Soil to Human, 1st ed.; Springer: New York, NY, USA, 2007. [Google Scholar]
  2. Sterckeman, T.; Thomine, S. Mechanisms of cadmium accumulation in plants. Crit. Rev. Plant Sci. 2020, 39, 322–359. [Google Scholar] [CrossRef]
  3. Stefanowicz, A.M.; Woch, M.W.; Kapusta, P. Inconspicuous waste heaps left by historical Zn–Pb mining are hot spots of soil contamination. Geoderma 2014, 235, 1–8. [Google Scholar] [CrossRef]
  4. Zeng, J.; Ke, W.; Deng, M.; Tan, J.; Li, C.; Cheng, Y.; Xue, S. A practical method for identifying key factors in the distribution and formation of heavy metal pollution at a melting site. J. Environ. Sci. 2023, 127, 552–563. [Google Scholar] [CrossRef]
  5. McLaughlin, M.J.; Smolders, E.; Zhao, F.J.; Grant, C.; Montalvo, D. Managing cadmium in agricultural systems. Adv. Agron. 2021, 166, 1–129. [Google Scholar]
  6. Ballabio, C.; Jones, A.; Panagos, P. Cadmium in topsoils of the European Union—An analysis based on lucas topsoil database. Sci. Total Environ. 2024, 912, 168710. [Google Scholar] [CrossRef]
  7. Carlon, C. Derivation Methods of Soil Screening Values in Europe. A Review and Evaluation of National Procedures Towards Harmonization; European Commission, Joint Research Centre: Ispra, Italy, 2007; EUR 22805-EN. [Google Scholar]
  8. Regulation of the Minister of the Environment of 1 September 2016 on the Method of the Contamination Assessment of the Earth Surface. In Journal of Laws of 2016; Item 1395; Minister of the Environment: Warsaw, Poland, 2016. Available online: https://isap.sejm.gov.pl/isap.nsf/DocDetails.xsp?id=wdu20160001395 (accessed on 8 July 2024). (In Polish)
  9. Baritz, R.; Amelung, W.; Antoni, V.; Boardman, J.; Hijbeek, R.; Horn, R.; Prokop, G.; Römbke, J.; Romkens, P.; Steinhoff-Knopp, B.; et al. Soil Monitoring in Europe—Indicators and Thresholds for Soil Health Assessments; EEA Report No 08/2022; European Environment Agency: Copenhagen, Denmark, 2023. [Google Scholar]
  10. Zhang, X.; Yang, L.; Li, Y.; Li, H.; Wang, W.; Ye, B. Impacts of lead/zinc mining and smelting on the environment and human health in China. Environ. Monit. Assess. 2011, 184, 2261–2273. [Google Scholar] [CrossRef]
  11. Wu, J.; Long, J.; Liu, L.; Li, J.; Liao, H.; Zhang, M.; Zhao, C.; Wu, Q. Risk assessment and source identification of toxic metals in the agricultural soil around a Pb/Zn mining and smelting area in Southwest China. Int. J. Environ. Res. Public Health 2018, 15, 1838. [Google Scholar] [CrossRef]
  12. Zhang, X.; Chen, D.; Zhong, T.; Zhang, X.; Cheng, M.; Li, X. Assessment of cadmium (Cd) concentration in arable soil in China. Environ. Sci. Pollut. Res. 2015, 22, 4932–4941. [Google Scholar] [CrossRef]
  13. Citeau, L.; Lamy, I.; Van Oort, F.; Elsass, F. Colloidal facilitated transfer of metals in soils under different land use. Colloids Surface A 2003, 217, 11–19. [Google Scholar] [CrossRef]
  14. Tosza, E.; Dumnicka, E.; Niklińska, M.; Rożen, A. Enchytraeid and earthworm communities along a pollution gradient near Olkusz (southern Poland). Eur. J. Soil Biol. 2010, 46, 218–224. [Google Scholar] [CrossRef]
  15. Chrastný, V.; Čadková, E.; Vaněk, A.; Teper, L.; Cabala, J.; Komárek, M. Cadmium isotope fractionation within the soil profile complicates source identification in relation to Pb–Zn mining and smelting processes. Chem. Geol. 2015, 405, 1–9. [Google Scholar] [CrossRef]
  16. Baldantoni, D.; Morra, L.; Zaccardelli, M.; Alfani, A. Cadmium accumulation in leaves of leafy vegetables. Ecotox. Environ. Safe 2016, 123, 89–94. [Google Scholar] [CrossRef]
  17. Kanwar, V.S.; Sharma, A.; Srivastav, A.L.; Rani, L. Phytoremediation of toxic metals present in soil and water environment: A critical review. Environ. Sci. Pollut. Res. 2020, 27, 44835–44860. [Google Scholar] [CrossRef]
  18. Marques, A.P.G.C.; Rangel, A.O.S.S.; Castro, P.M.L. Remediation of heavy metal contaminated soils: Phytoremediation as a potentially promising clean-up technology. Crit. Rev. Environ. Sci. Technol. 2009, 39, 622–654. [Google Scholar] [CrossRef]
  19. Van Nevel, L.; Mertens, J.; Oorts, K.; Verheyen, K. Phytoextraction of metals from soils: How far from practice? Environ. Pollut. 2007, 150, 34–40. [Google Scholar] [CrossRef]
  20. Korzeniowska, J.; Stanislawska-Glubiak, E.; Igras, J. Applicability of energy crops for metal phytostabilization of soils moderately contaminated with copper, nickel and zinc. J. Food Agric. Environ. 2011, 9, 693–697. [Google Scholar]
  21. Korzeniowska, J.; Stanisławska-Glubiak, E. Phytoremediation potential of Phalaris arundinacea, Salix viminalis and Zea mays for nickel-contaminated soils. Int. J. Environ. Sci. Technol. 2019, 16, 1999–2008. [Google Scholar] [CrossRef]
  22. Phusantisampan, T.; Meeinkuirt, W.; Saengwilai, P.; Pichtel, J.; Chaiyarat, R. Phytostabilization potential of two ecotypes of Vetiveria zizanioides in cadmium-contaminated soils: Greenhouse and field experiments. Environ. Sci. Pollut. Res. 2016, 23, 20027–20038. [Google Scholar] [CrossRef]
  23. Taeprayoon, P.; Homyog, K.; Meeinkuirt, W. Organic amendment additions to cadmium-contaminated soils for phytostabilization of three bioenergy crops. Sci. Rep. 2022, 12, 13070. [Google Scholar] [CrossRef]
  24. Zgorelec, Z.; Bilandzija, N.; Knez, K.; Galic, M.; Zuzul, S. Cadmium and mercury phytostabilization from soil using Miscanthus× giganteus. Sci. Rep. 2020, 10, 6685. [Google Scholar] [CrossRef]
  25. Dubey, S.; Shri, M.; Gupta, A.; Rani, V.; Chakrabarty, D. Toxicity and detoxification of heavy metals during plant growth and metabolism. Environ. Chem. Lett. 2018, 16, 1169–1192. [Google Scholar] [CrossRef]
  26. Hossain, M.A.; Piyatida, P.; da Silva, J.A.T.; Fujita, M. Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012, 2012, 1–37. [Google Scholar] [CrossRef]
  27. Stanislawska-Glubiak, E.; Korzeniowska, J. Effect of salicylic acid foliar application on two wheat cultivars grown under zinc stress. Agronomy 2022, 12, 60. [Google Scholar] [CrossRef]
  28. Grill, E.; Löffler, S.; Winnacker, E.L.; Zenk, M.H. Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc. Natl. Acad. Sci. USA 1989, 86, 6838–6842. [Google Scholar] [CrossRef]
  29. Delalande, O.; Desvaux, H.; Godat, E.; Valleix, A.; Junot, C.; Labarre, J.; Boulard, Y. Cadmium–glutathione solution structures provide new insights into heavy metal detoxification. FEBS J. 2010, 277, 5086–5096. [Google Scholar] [CrossRef]
  30. Luo, J.S.; Zhang, Z. Mechanisms of cadmium phytoremediation and detoxification in plants. Crop J. 2021, 9, 521–529. [Google Scholar] [CrossRef]
  31. Abaga, N.O.Z.; Dousset, S.; Mbengue, S.; Munier-Lamy, C. Is vetiver grass of interest for the remediation of Cu and Cd to protect marketing gardens in Burkina Faso? Chemosphere 2014, 113, 2–47. [Google Scholar]
  32. Rabêlo, F.H.S.; Borgo, L. Changes caused by heavy metals in micronutrient content and antioxidant system of forage grasses used for phytoremediation: An overview. Ciência Rural 2016, 46, 1368–1375. [Google Scholar] [CrossRef]
  33. Korzeniowska, J.; Stanislawska-Glubiak, E. Phytoremediation potential of Miscanthus× giganteus and Spartina pectinata in soil contaminated with heavy metals. Environ. Sci. Pollut. Res. 2015, 22, 11648–11657. [Google Scholar] [CrossRef]
  34. Xu, P.; Wang, Z. Physiological mechanism of hypertolerance of cadmium in Kentucky bluegrass and tall fescue: Chemical forms and tissue distribution. Environ. Exp. Bot. 2013, 96, 35–42. [Google Scholar] [CrossRef]
  35. Zhang, S.; Lin, H.; Deng, L.; Gong, G.; Jia, Y.; Xu, X.; Li, T.; Li, Y.; Chen, H. Cadmium tolerance and accumulation characteristic Siegesbeckia orientalis L. Ecol. Eng. 2013, 51, 133–139. [Google Scholar] [CrossRef]
  36. Antonkiewicz, J.; Jasiewicz, C.; Koncewicz-Baran, M.; Sendor, R. Nickel bioaccumulation by the chosen plant species. Acta Physiol. Plant 2016, 38, 40–51. [Google Scholar] [CrossRef]
  37. Gawryluk, A.; Wyłupek, T.; Wolański, P. Assessment of Cu, Pb and Zn content in selected species of grasses and in the soil of the roadside embankment. Ecol. Evol. 2020, 10, 9841–9852. [Google Scholar] [CrossRef] [PubMed]
  38. Jiang, N.; Li, Z.; Yang, J.; Zu, Y. Responses of antioxidant enzymes and key resistant substances in perennial ryegrass (Lolium perenne L.) to cadmium and arsenic stresses. BMC Plant Biol. 2022, 22, 145. [Google Scholar] [CrossRef] [PubMed]
  39. ISO/IEC 17025; General Requirements for the Competence of Testing and Calibration Laboratories. Polish Committee for Standardization: Warsaw, Poland, 2018. (In Polish)
  40. PN-ISO 11047:2001; Soil Quality: Determination of Cadmium, Chromium, Cobalt, Copper, Lead, Manganese, Nickel and Zinc in Aqua Regia Extracts of Soil—Flame and Electrothermal Atomic Absorption Spectrometric Methods. Polish Committee for Standardization: Warsaw, Poland, 2013. (In Polish)
  41. PN-ISO 14235:2003; Soil Quality: Determination of Organic Carbon in Soil by Sulfochromic Oxidation. Polish Committee for Standardization: Warsaw, Poland, 2003. (In Polish)
  42. PN-EN ISO 10390:2022-09; Soil, Treated Biowaste and Sludge—Determination of pH (ISO 10390:2021). Polish Committee for Standardization: Warsaw, Poland, 2022. (In Polish)
  43. PN-R-04033:1998; Soil and Mineral Soil Materials—Particle Size Distribution on Soil Classes. Polish Committee for Standardization: Warsaw, Poland, 1998. (In Polish)
  44. PN-R-04023:1996; Agrochemical Soil Analyse–Determination of Assimilated Phosphorus Contents. Committee for Standardization: Warsaw, Poland, 1996. (In Polish)
  45. PN-R-04022:1996; Agrochemical Soil Analyse—Determination of Assimilated Potassium Content. Committee for Standardization: Warsaw, Poland, 1996. (In Polish)
  46. PN-R-04020:1994; Agrochemical Soil Analyse—Determination of Assimilated Magnesium Content. Committee for Standardization: Warsaw, Poland, 1994. (In Polish)
  47. PN-R-04014:1991; Agrochemical Plant Analyse—Methods of Mineralization of Plant Material for Determination Macro- and Microelements. Polish Committee for Standardization: Warsaw, Poland, 1991. (In Polish)
  48. Wilkins, D.A. The measurement of tolerance to edaphic factors by means of root growth. New Phytol. 1978, 80, 623–633. [Google Scholar] [CrossRef]
  49. Melo, E.E.C.; Costa, E.T.S.; Guilherme, L.R.G.; Faquin, V.; Nascimento, C.W.A. Accumulation of arsenic and nutrients by castor bean plants grown on an As-enriched nutrient solution. J. Hazard. Mater. 2009, 168, 479–483. [Google Scholar] [CrossRef]
  50. Kumar, P.; Fulekar, M.H. Cadmium phytoremediation potential of Deenanath grass (Pennisetum pedicellatum) and the assessment of bacterial communities in the rhizospheric soil. Environ. Sci. Pollut. Res. 2022, 29, 2936–2953. [Google Scholar] [CrossRef] [PubMed]
  51. Sukarjo, S.; Zulaehah, I.; Purbalisa, W. The critical limit of cadmium in three types of soil texture with shallot as an indicator plant. AIP Conf. Proc. 2019, 2120, 040012. [Google Scholar]
  52. Roccotiello, E.; Manfredi, A.; Drava, G.; Minganti, V.; Mariotti, M.; Berta, G.; Cornara, L. Zinc tolerance and accumulation in the ferns Polypodium cambricum L. and Pteris vittata L. Ecotoxicol. Environ. Saf. 2010, 73, 1264–1271. [Google Scholar] [CrossRef]
  53. Cheraghi, M.; Lorestani, B.; Khorasani, N.; Yousefi, N.; Karami, M. Findings on the phytoextraction and phytostabilization of soils contaminated with heavy metals. Biol. Trace Elem. Res. 2011, 144, 1133–1141. [Google Scholar] [CrossRef]
  54. Pinto, A.P.; Sim[otilde]es, I.; Mota, A.M. Cadmium impact on root exudates of sorghum and maize plants: A speciation study. J. Plant Nutr. 2008, 31, 1746–1755. [Google Scholar] [CrossRef]
  55. Sun, L.; Cao, X.; Tan, C.; Deng, Y.; Cai, R.; Peng, X.; Bai, J. Analysis of the effect of cadmium stress on root exudates of Sedum plumbizincicola based on metabolomics. Ecotoxicol. Environ. Safe 2020, 205, 111152. [Google Scholar] [CrossRef] [PubMed]
  56. Huang, H.; Lu, R.; Zhan, J.; He, J.; Wang, Y.; Li, T. Role of Root Exudates in Cadmium Accumulation of a Low-Cadmium-Accumulating Tobacco Line (Nicotiana tabacum L.). Toxics 2023, 11, 141. [Google Scholar] [CrossRef] [PubMed]
  57. Lapie, C.; Leglize, P.; Paris, C.; Buisson, T.; Sterckeman, T. Profiling of main metabolites in root exudates and mucilage collected from maize submitted to cadmium stress. Environ. Sci. Pollut. Res. 2019, 26, 17520–17534. [Google Scholar] [CrossRef] [PubMed]
  58. Tian, S.; Xie, R.; Wang, H.; Hu, Y.; Hou, D.; Liao, X.; Brown, P.H.; Yang, H.; Lin, X.; Labavitch, J.M.; et al. Uptake, sequestration and tolerance of cadmium at cellular levels in the hyperaccumulator plant species Sedum alfredii. J. Exp. Bot. 2017, 68, 2387–2398. [Google Scholar] [CrossRef] [PubMed]
  59. Wang, K.; Yu, H.; Ye, D.; Wang, Y.; Zhang, X.; Huang, H.; Zheng, Z.; Li, T. The critical role of the shoot base in inhibiting cadmium transport from root to shoot in a cadmium-safe rice line (Oryza sativa L.). Sci. Total Environ. 2021, 765, 142710. [Google Scholar] [CrossRef] [PubMed]
  60. Gao, Y.; Li, H.; Song, Y.; Zhang, F.; Yang, Z. The response of thiols to cadmium stress in spinach (Spinacia oleracea L.). Toxics 2022, 10, 429. [Google Scholar] [CrossRef]
  61. Viehweger, K. How plants cope with heavy metals. Bot. Stud. 2014, 55, 35. [Google Scholar] [CrossRef] [PubMed]
  62. Kumar, R.; Mishra, R.K.; Mishra, V.; Qidwai, A.; Pandey, A.; Shukla, S.K.; Pandey, M.; Pathak, A.; Dikshit, A. Detoxification and tolerance of heavy metals in plants. In Plant Metal Interaction; Elsevier: Amsterdam, The Netherlands, 2016; pp. 335–359. [Google Scholar]
  63. Lambrechts, T.; Lequeue, G.; Lobet, G.; Godin, B.; Bielders, C.L.; Lutts, S. Comparative analysis of Cd and Zn impacts on root distribution and morphology of Lolium perenne and Trifolium repens: Implications for phytostabilization. Plant Soil 2014, 376, 229–244. [Google Scholar] [CrossRef]
  64. Bali, A.S.; Sidhu, G.P.S.; Kumar, V. Root exudates ameliorate cadmium tolerance in plants: A review. Environ. Chem. Lett. 2020, 18, 1243–1275. [Google Scholar] [CrossRef]
  65. Parrotta, L.; Guerriero, G.; Sergeant, K.; Cai, G.; Hausman, J.F. Target or barrier? The cell wall of early-and later-diverging plants vs cadmium toxicity: Differences in the response mechanisms. Front. Plant Sci. 2015, 6, 123937. [Google Scholar] [CrossRef] [PubMed]
Agriculture 14 01127 g001
Figure 1. Relative biomass of shoots and roots of grasses (control as 100%). Values marked with different lowercase letters within one species and values marked with uppercase letters within one Cd dose are significantly different according to the Tukey test (p < 0.05).
Figure 1. Relative biomass of shoots and roots of grasses (control as 100%). Values marked with different lowercase letters within one species and values marked with uppercase letters within one Cd dose are significantly different according to the Tukey test (p < 0.05).
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Agriculture 14 01127 g002
Figure 2. Cd concentration in the soil after harvest. Values marked with different lowercase letters within one species and values marked with uppercase letters within one Cd dose were significantly different according to the Tukey test (p < 0.05).
Figure 2. Cd concentration in the soil after harvest. Values marked with different lowercase letters within one species and values marked with uppercase letters within one Cd dose were significantly different according to the Tukey test (p < 0.05).
Agriculture 14 01127 g002
Table 1. Properties of soils used in the experiment.
Table 1. Properties of soils used in the experiment.
Soil FeaturepHTOCP2O5K2OMgCdSandSiltClay
%mg kg−1%
Value5.40.66237 1159 165 20.7 374233
Sand: 2.0–0.05 mm, silt: 0.05–0.002 mm, clay: <0.002 mm diameter, TOC—total organic carbon, 1 Enger–Rhiem, 2 Schachtschabel, 3 aqua regia.
Table 2. Tolerance index (TI) of grasses.
Table 2. Tolerance index (TI) of grasses.
Grass Cd1 Cd2 Cd3
ShootsRootsMeanShootsRootsMeanShootsRootsMean
P. pratensis696165 Ac554852 Ab342831 Ca
L. perenne858786 Dc554852 Ab301824 Aa
F. rubra756470 Bc614855 Ab312729 BCa
F. pratensis778079 Cc615759 Bb282527 Ba
Mean777375585054312528
Values marked with different lowercase letters within one species and values marked with uppercase letters within one Cd dose are significantly different according to the Tukey test (p < 0.05).
Table 3. Cd concentration in shoots and roots.
Table 3. Cd concentration in shoots and roots.
GrassTreatmentShootsRoots
Cd mg kg−1Increase *Cd mg kg−1Increase *
01.6 Ca-6.4 Aa-
P. pratensisCd166 Cb41708 Ab111
Cd2129 Cc811466 Ac229
Cd3261 Cd1632710 Ad423
01.0 Aa-7.9 Ba-
L. perenneCd134 Ab341470 Cb186
Cd272 Ac723345 Dc423
Cd3167 Ad1675631 Dd713
01.7 Ca-12.9 Ca-
F. rubraCd170 Cb411319 Bb102
Cd2121 Cc712207 Bc171
Cd3219 Bd1293197 Bd248
01.4 Ba-8.1 Ba-
F. pratensisCd148 Bb341226 Bb151
Cd299 Bc712862 Cc353
Cd3234 Bd1674994 Cd617
(*) Increase compared to the control treatment. Values marked with different lowercase letters within one species and values marked with uppercase letters within one Cd dose are significantly different according to the Tukey test (p < 0.05).
Table 4. Bioaccumulation (BF) and translocation factors (TF).
Table 4. Bioaccumulation (BF) and translocation factors (TF).
GrassCd LevelBFshootBFrootTF
P. pratensisCd12.122.30.09
Cd22.023.00.09
Cd32.222.60.10
Mean Cd1–Cd32.122.70.09
L. perenneCd11.145.90.02
Cd21.359.60.02
Cd31.344.90.03
Mean Cd1–Cd31.348.90.03
F. rubraCd12.343.60.05
Cd21.934.80.05
Cd31.623.60.07
Mean Cd1–Cd31.829.30.06
F. pratensisCd11.641.30.04
Cd21.645.50.03
Cd31.736.50.05
Mean Cd1–Cd31.739.60.04
Table 5. Glutathione concentration in shoots.
Table 5. Glutathione concentration in shoots.
GrassWithout Cd (0)Cd3 LevelGlutathione Increase
µg kg−1
P. pratensis1272 Ba5916 Db4.6
L. perenne251 Aa580 Ab2.3
F. rubra1109 Ba3964 Cb3.6
F. pratensis1177 Ba2693 Bb2.3
Values marked with different lowercase letters within one species and values marked with uppercase letters within one Cd dose are significantly different according to the Tukey test (p < 0.05).
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Korzeniowska, J.; Stanislawska-Glubiak, E. The Suitability of Several Grasses for the Remediation of Hotspots Affected by Cadmium Contamination. Agriculture 2024, 14, 1127. https://doi.org/10.3390/agriculture14071127

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Korzeniowska J, Stanislawska-Glubiak E. The Suitability of Several Grasses for the Remediation of Hotspots Affected by Cadmium Contamination. Agriculture. 2024; 14(7):1127. https://doi.org/10.3390/agriculture14071127

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Korzeniowska, Jolanta, and Ewa Stanislawska-Glubiak. 2024. "The Suitability of Several Grasses for the Remediation of Hotspots Affected by Cadmium Contamination" Agriculture 14, no. 7: 1127. https://doi.org/10.3390/agriculture14071127

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