Energy Potential of Zea mays Grown in Cadmium-Contaminated Soil

Abstract

Cadmium is a non-essential element for proper plant growth and development and is highly toxic to humans and animals, in part because it inters with calcium-dependent processes in living organisms. For this reason, a study was conducted to assess the potential for producing maize (Zea mays) biomass in cadmium-contaminated soil for energy purposes. The energy potential of Zea mays was evaluated by determining the heat of combustion (Q), heating value (Hv), and the amount of energy produced from the biomass. Starch, compost, fermented bark, humic acids, molecular sieve, zeolite, sepiolite, expanded clay, and calcium carbonate were assessed as substances supporting biomass production from Zea mays. The accumulation and redistribution of cadmium in the plant were also investigated. The study was conducted in a vegetation hall as part of a pot experiment. Zea mays was grown in uncontaminated soil and in soil contaminated with 15 mg Cd²⁺ kg⁻¹. A strong toxic effect of cadmium on the cultivated plants was observed, causing a 62% reduction in the biomass of aerial parts and 61% in the roots. However, it did not alter the heat of combustion and heating value of the aerial part biomass, which were 18.55 and 14.98 MJ kg⁻¹ d.m., respectively. Of the nine substances tested to support biomass production, only four (molecular sieve, compost, HumiAgra, and expanded clay) increased the yield of Zea mays grown in cadmium-contaminated soil. The molecular sieve increased aerial part biomass production by 74%, compost by 67%, expanded clay by 19%, and HumiAgra by 15%, but none of these substances completely eliminated the toxic effects of cadmium on the plant. At the same time, the bioaccumulation factor (BAF) of cadmium was higher in the roots (0.21–0.23) than in the aerial parts (0.04–0.03), with the roots showing greater bioaccumulation.

1. Introduction

With the growing demand for renewable energy sources and the need to reduce greenhouse gas emissions, plant biomass is an important element in sustainable energy development strategies [1,2]. In this context, plant biomass harvested from degraded and polluted areas is particularly valuable, as it can be toxic to humans and animals [3,4]. It is therefore reasonable to use biomass containing heavy metals for energy purposes, in the sense of a closed-loop economy [5,6,7]. The implementation of such a practice is environmentally and socially acceptable, and the inclusion of this type of plant biomass in renewable energy sources represents an opportunity for the use of plants on a global scale [8,9]. Plant biomass produced on marginal, degraded, contaminated, or abandoned land that has not previously been used for food production fits into the concept described in the RED III Directive [10], which mandates the phasing out of biofuels with “high ILUC risk” (Indirect Land Use Change) after 2023 in favor of fuels derived from biomass with “low ILUC risk”. Sumfleth et al. [11] and Sandford et al. [12] note that fuels derived from biomass with “low ILUC risk” are being promoted under the European Union’s renewable energy policy because they reduce negative environmental impacts.

Research into the feasibility of growing energy crops on degraded soils or heavy metal contaminated soils is becoming increasingly important [13,14]. Cadmium contamination of soils, due to its mobility, toxicity, persistence in the environment, and tendency to bioaccumulate in food webs, is a significant environmental problem [15]. The metal is on the EU’s list of critical raw materials [16] that are at high risk of extraction [17]. However, it should be emphasized that geogenic sources determine the actual amount of cadmium in the environment, while its increasing pollution is directly related to anthropogenic activities. These include industrial emissions, mainly from the burning of fossil fuels, the production of phosphate fertilizers and pesticides, and mining [18].

Cadmium poses a high risk to organisms at all trophic levels. The bioaccumulation and biomagnification of cadmium in the food chain has implications for human and animal health [19,20]. Cadmium has been categorized as a carcinogen for humans by the International Agency for Research on Cancer [21]. It can enter the human body by inhalation, ingestion, and through the skin. It accumulates mainly in the liver, kidneys, but also in bones and other organs, causing irreversible multisystem damage [22,23]. Public concern about cadmium is compounded by the fact that it has been implicated in diseases, neurodegenerative diseases such as amyotrophic lateral sclerosis (ALS), multiple sclerosis (MS), and the now common Alzheimer’s or Parkinson’s diseases, referred to as the diseases of the 21st century [24]. This is partly due to the fact that cadmium is very slowly excreted from the body, with a biological half-life of 10–30 years [25]. Therefore, an increased scientific interest in the effects of cadmium on humans [25,26,27], animals [19], plants [28,29], and the soil [30,31,32] and water microbiome [33,34] is warranted. This is reflected in the number of scientific articles published in recent years, as pointed out by Liu et al. [28] and Irfan et al. [35]. In addition, predictive models are increasingly being constructed to predict heavy metal concentrations in the environment, which is essential for identifying public health risks. They are also helpful in selecting an appropriate remediation strategy for soils contaminated with these metals [36].

The relatively high mobility of cadmium in the environment predisposes this element to excessive accumulation in plants [37]. In the soil, cadmium binds to soil colloids, is then sorbed to the root surface, and is transported across the cell membrane into plant root cells [23,38]. The process of cadmium uptake from the soil by plant roots is first mediated by apoplasts (passive transport) and symplasts (active transport), and is then translocated via xylem and phloem to the aerial parts of the plant [39]. The process of cadmium uptake and translocation in plants is regulated by protein-coding genes, such as the Low-Affinity Cation Transporter1 (LCT1) gene, heavy metal ATPase 3 (HMA3), P1B2-ATPase, among others [40]. Finally, cadmium can accumulate in various plant organs [41]. The use of plants to remediate cadmium-contaminated soils is referred to as green remediation [42], which, depending on the mechanism, can be classified as phytostimulation [43,44], phytoextraction [38,45], phytostabilization [44,46], phytofiltration (including rhizofiltration, blastofiltration and caulofiltration [47]) and phytotransformation [44]. Sharma et al. [48] point out that using plants to clean heavy metal-contaminated soils is four to six times cheaper than physical remediation. Therefore, it is highly reasonable to exploit the biomass energy potential of these plants, and in this respect, the selection of plants in cadmium-contaminated areas is crucial [48,49]. It is reasonable to utilize plants that are distinguished by their extensive distribution range, substantial root system (which serves to impede the dissemination of heavy metals within the environment), abbreviated life cycle, and elevated biomass yield. These characteristics render them a compelling raw material for the bioenergy sector [13]. At the same time, these plants should have a high capacity to accumulate this heavy metal [50,51]. The Zea mays is one of these plants [52,53]. It is currently grown over about 194 million hectares in 170 countries [54,55]. A major advantage is its high yield potential, due in part to an efficient C4-type photosynthetic mechanism [14]. In addition, Zea mays has a good ability to tolerate certain levels of cadmium in the soil [52], and the biomass extracted from such areas can be used for energy purposes [9,56]. As reported by Elik et al. [29], maize demonstrates phytoremediation potential as evidenced by both changes in antioxidant enzyme activity and tissue water content or electrical conductivity resulting from Cd accumulation in Zea mays roots and leaves. Under good growth and development conditions, maize yields in Poland usually range from 30 to 50 tons of fresh weight per hectare. Under poorer, shaded growth conditions (with 26% shading), maize also has higher methane yields than a cereal monoculture for biogas purposes, which produces 3200 to 4500 m³ ha⁻¹ of methane [57,58,59]. According to Schulz et al. [60], taking into account the high biomass yield of Zea mays, biogas production of as much as 7500 to 10,200 m³ ha⁻¹ can be achieved, making it one of the most efficient feedstocks for biogas production. A new trend in the production of biomass for energy purposes is to grow it on marginal land and to support plant growth and development with different types of fertilizer [18,61]. This approach involves the addition of chemicals to the soil that can moderate the availability and mobility of cadmium in contaminated soils [61,62]. For example, the amendment of cadmium-contaminated soils with organic matter can enhance the formation of stable cadmium complexes, thereby decreasing its bioavailability [18] and ultimately improving soil fertility [63,64]. In addition, the application of mineral-based soil amendments and liming can promote the formation of insoluble cadmium compounds, effectively limiting its uptake by plants [65]. Petruzzelli et al. [66] and Barbafieri et al. [67] refer to the phenomenon of assisted phytoextraction, where mobilizing agents are applied to contaminated soils to promote the release of metals from the solid to the liquid phase, thereby increasing the bioavailability and uptake of metals by plants.

Despite the many advantages of green remediation, both classical and assisted, it also carries risks, as the plant biomass that is extracted by this process can be toxic to humans and animals [3,4]. The choice of natural adsorbents was highly justified. Starch is a polysaccharide, the most abundant in nature, whose glycosidic structure with hydroxyl groups allows interactions with xenobiotics with different degrees of hydrophilicity [68]. It should also be noted that its production in the European Union (EU) was 9.2 million tons in 2023 [69]. Compost is an important source of organic matter fractions and reducing oxides that contribute to the immobilization of heavy metals in the soil, reducing their mobility and bioavailability [70]. The bark of Pinus elliottii was found by Junior et al. [71] to be an effective organic adsorbent of heavy metals, including cadmium, absorbing it at a level of 90%. Humic acids contain functional groups responsible for the formation of humates, which induce the sequestration of cadmium from soils [72]. Their ability in targeted soil remediation is demonstrated by an efficiency of 96.18% in the removal of this metal [73]. The sorption potential of the molecular sieve, on the other hand, is related to the presence of sodium ions (Na⁺), due to which metal ions are immobilized in the sieve structure as a result of ion exchange [74]. The choice of zeolite was determined not only by its annual production of 4 million tons per year, but mainly by its effectiveness in improving the sorption properties of soils [75,76]. Sepiolite, on the other hand, is characterized by its high availability, natural origin, and low cost, which ranges from USD 32 to USD 1000 per ton, depending on its use and degree of processing [77]. Interest in expanded clay arose, as with the above sorbents, from its particular sorption capacity [78,79]. The selection of calcium carbonate was related to the fact that in soils with a high CaCO₃ content, heavy metals are often precipitated as carbonates, which limits their mobility and availability to plants [80].

In view of the above considerations, and given that cadmium contamination of soil poses a significant threat to the environment, the present study adopted a balanced approach aimed at evaluating the suitability of Zea mays biomass cultivated in cadmium-contaminated soil for energy production. Furthermore, the study compared the effectiveness of various organic (starch, compost, fermented bark, and humic acids) and mineral (molecular sieve, zeolite, sepiolite, expanded clay, and calcium carbonate) production-enhancing substances, in order to select the most effective ones. The innovative nature of the research, achieved by combining the phytoremediation of cadmium-exposed soil with the assessment of the energy value of Zea mays, is also evident in this. This aligns with current research directions on the cultivation of energy crops in soils degraded or contaminated with heavy metals, while identifying the most effective sorbents among nine substances that support the remediation process. It was hypothesized that excessive cadmium in the soil may influence the yield of Zea mays and the accumulation of this element in plant tissues. It may also affect the energy value of the biomass and consequently alter the potential for energy production. These differences can be reduced by introducing substances into the soil that mitigate the toxic effects of cadmium on plants.

Therefore, the overall objective of this study was to evaluate the energy potential of Zea mays cultivated in cadmium-contaminated soil with regard to its applicability for sustainable biomass energy production. The analysis included both the accumulation of heavy metals in the plant and their redistribution. The specific objectives were as follows: (1) to assess the feasibility of Zea mays biomass production in cadmium-contaminated soil; (2) to evaluate the heat of combustion, heating value, and energy output of Zea mays biomass; (3) to examine the effects of various production-enhancing substances (starch, compost, fermented bark, humic acids, molecular sieve, zeolite, expanded clay, and calcium carbonate) on reducing cadmium toxicity and enhancing the energy value of Zea mays.

2. Materials and Methods

2.1. The Scope of the Study

The scope of the study was Zea mays grown in uncontaminated soil (sandy loam) and soil contaminated with cadmium at 15 mg kg⁻¹ d.m. of soil. Zea mays was selected for this study due to its widespread cultivation and proven capacity to tolerate and extract heavy metals from contaminated soils. Cadmium was used in the form of 3CdSO₄ × 8H₂O (Manufacturer: Sigma-Aldrich, Saint Louis, MO, USA). Nine remediators, including five of mineral origin (molecular sieve, Zeolite Bio.Zeo.S.01, sepiolite, expanded clay, and calcium carbonate) and four of organic origin (starch, compost, fermented bark, and HumiAgra), were used to offset the negative effects of cadmium on plants. The control was soil without production-enhancing substances. The characteristics of the soil and production-enhancing substances used in the study are shown in

Table 1. The characteristics of the material used in the study.

Type	Abbreviation	Characteristics
Soil
Sandy loam	SL	Content (%): sand (0.05–2 mm)—63.61, silt (0.002–0.05 mm)—32.68, clay (<0.002 mm)—3.71. Content (g kg−1 of soil dry matter): Corg—10.00 and Ntotal—0.83. Content (mg kg−1 of soil dry matter): Cd2+—0.142. pH in 1 mol KCl dm−3—4.40, pH in H2O dm−3—5.52. Hydrolytic acidity—26.10 mM(+) kg−1 d.m. of soil, exchangeable base cations—63.60 mM(+) kg−1 d.m. of soil, cation exchange capacity—89.70 mM(+) kg−1 d.m. of soil, alkaline cation saturation—70.90%.
Plant
Zea mays	Zm	Variety DS1897B. It is a crop suitable for grain, silage, and energy purposes. It is a plant adapted to existence in various conditions. It tolerates both low-fertility and high-fertility soils well.
Mineral substances for biomass production enhancement
Molecular sieve	MS	Silosiv A3 is a white, hydrated aluminosilicate characterized by a micropore diameter of 0.3 nm and a pHKCl value of 8.5. Its maximum volatile content at 950 °C does not exceed 2.5%. Manufacturer: Sylosiv, (Columbia, MD, USA).
Zeolite Bio.Zeo.S.01	Z	Aluminosilicate mineral of volcanic origin containing 60% clinoptilolite, 33% Si, 3.26% Al, 1.17% K, 2.44% Ca, 0.56% Mg, 0.52% Fe. Manufacturer: BioDrain (Rzeszow, Poland).
Sepiolite	S	Hydrated magnesium silicate (Mg4 [Si6O15(OH)2] × 6H2O), having a pore diameter of 1.4 nm, fibrous texture, and a pH KCl = 7.1. Manufacturer: Sepiolsa Minersa Group (Guadalajara, Spain).
Expanded clay	E	A lightweight ceramic aggregate formed by firing clay at a temperature of about 1200 °C, with a particle size of 75 to 710 μm, and a pHKCl 7.1. Manufacturer: GardenGURU, Piła, Poland.
Calcium carbonate	Ca	White powder (CaCO3) with a molar mass of 100.09 g mol−1. Manufacturer: Chempur (Piekary Śląskie, Poland).
Organic substances for biomass production enhancement
Starch	St	White powder (C6H10O5) with a molar mass of 162.1 g mol−1, and solubility in water of 50 g dm−3 (90 °C, pH 6.0–7.5). Manufacturer: Chempur (Piekary Śląskie, Poland).
Compost	K	Compost prepared from composted grasses. pH in 1 mol KCl dm−3—6.1. Content (g kg−1 of soil dry matter): Corg—146.61, Ntotal—20.18. Content (mg kg−1 of soil dry matter): P—3.41, K—9.25, and Mg—5.69.
Fermented bark	B	Fermented bark of coniferous trees with bark flake size of 20–50 mm. Content of dry matter ≥30%, organic matter ≥50%, and pH H2O ≤6.0. Manufacturer: Athena Bio-Produkty Sp. z o.o. (Golczewo, Poland).
HumiAgra	H	Ecological product (powder) of dark brown color, pH 8–10. Contains 90% humic acids, with a humic-to-fulvic acid ratio of 1:1, 8% K2O, and 3% S. Manufacturer: AgraPlant (Kielce, Poland).

.

For a detailed characterization of the production-enhancing substances used in the study, see our previous work: molecular sieve, sepiolite, expanded clay [81,82], zeolite [83,84], compost [85], fermented bark [86], and HumiAgra [6].

2.2. Vegetation Experiment

The study was conducted in a vegetation hall located in northeastern Poland (53°45′36″ N 20°27′15″ E). The experiments were carried out in four replicates, in polyethylene pots with the following dimensions: 16 cm (height), 17 cm (diameter at the base). The procedure for conducting the experiment began with the selection of the soil. It was decided to use loamy sand, which is characteristic of the Mazurian Lake District (Poland). In the first step, a portion of the soil was prepared, dried, and sieved through a 5 mm mesh sieve, to which aqueous solutions of mineral fertilizers were added to meet the nutrient requirements of the test plant, Zea mays. Nitrogen (150 mg N kg⁻¹ of soil) was applied in the form of CO(NH₂)₂, phosphorus (50 mg P kg⁻¹ of soil) in the form of KH₂PO₄, potassium (150 mg K kg⁻¹ of soil) in the form of KH₂PO₄ + KCl, and magnesium (20 mg Mg kg⁻¹ of soil) in the form of MgSO₄ × 7H₂O. The soil was divided into two series. One series was uncontaminated soil, and the other was contaminated with cadmium at a dose of 15 mg Cd kg⁻¹ d.m. of soil. The respective biomass production-enhancing substances, as described in Table 1, were then applied to both series. These substances were added both to the uncontaminated and contaminated soil. Molecular sieve, zeolite SO1, sepiolite, and expanded clay were applied at 20 g kg⁻¹ d.m. of soil and calcium carbonate at 1.96 g kg⁻¹, corresponding to 1.5 hydrolytic acidity. Starch, HumiAgra, compost, and fermented bark were applied at 3 g C kg⁻¹ of soil. A total of 80 pots were used in the study, i.e., 10 soil amendments (control—no soil amendments, molecular sieve, Zeolite Bio.Zeo.S.01, sepiolite, expanded clay, calcium carbonate, starch, compost, fermented bark, and HumiAgra) × 2 doses of cadmium (0 and 15 g kg⁻¹ d.m. of soil) × 4 replicates. The soil prepared in this manner was placed in suitable pots, moistened to 60% of the maximum water capacity, and retained in this moistened state throughout the growing season (55 days). On the day the soil was packed in the pots, Zea mays (Zm) was sown at 8 seeds. Ultimately, 4 plants were placed in each pot after emergence. When the Zm panicle began to appear (according to the International System of Classification of the Development Stages of Crop Plants, this was the 51st stage of the BBCH—Biologische Bundesanstalt, Bundessortenamt, and Chemical Scale), the leaf green index (SPAD) was measured using a chlorophyll meter from Spectrum Technologies, Inc. (KONICA MINOLTA, Inc., Chiyoda, Japan), and then the aerial parts and roots of the plants were harvested and soil samples were also taken for subsequent analysis.

2.3. Laboratory Analysis Methodology

Soil samples were air-dried in the open air, while the biomasses of shoots and leaves as well as roots of Zea mays were dried in a Binder D-78532 dryer (Binder GmbH, Tuttlingen, Germany) at a temperature of 60 °C. Prior to the initiation of the experiment, soil grain size was determined in air-dried samples passed through a 2 mm mesh sieve using a Malvern Mastersizer 3000 Laser Diffraction (Malvern, Worcestershire, UK); soil organic carbon and total nitrogen contents were determined using a Vario MaxCube CN macroanalyzer (Hanau, Germany); soil pH was measured in 1 mol of KCl and H₂O using a pH meter HI 2221 (Hanna Instruments, Washington, UK); hydrolytic acidity and total alkaline exchangeable cation contents were determined using methods described in our previous study [56]. In order to ascertain the cadmium content of soil and plants, samples of soil, aerial part biomass and root biomass were mineralized in a microwave mineralizer (UltraWAVE Milestone, Sorisole, Italy). Prior to mineralization, plant samples were dried at 65 °C and subsequently ground. Soil samples were air-dried, ground using a mortar, and sieved through a 2 mm mesh. For mineralization, 5 cm³ of 65% HNO₃ solution was used per 0.5 g of sample. The mineralized material was diluted with demineralized water to a volume of 100 cm³. An inductively coupled plasma emission spectrometer (iCAP 7000 Series ICP-OES, Thermo Scientific, Newington, CT, USA) was used to determine cadmium content. All analyses were performed in 4 replicates. To ensure the accuracy of cadmium determinations by ICP-OES, instrument calibration was performed using a certified multi-element standard solution (Certipur^®, Merck, Darmstadt, Germany) containing 24 elements, including cadmium. The limit of detection (LOD) for cadmium was established at 0.001 ppm. Additionally, in accordance with PN–EN 14780:2017 [87] and PN–EN ISO 18125:2017 [88], the heat of combustion (Q) was determined in the biomass of the aerial parts. An IKA WERKE C2000 calorimeter (IKA, Cincinnati, OH, USA) was used for this purpose. The heating value (Hv) and energy content (Y_EP) of Zea mays biomass, both from uncontaminated and cadmium-contaminated soils, were then calculated. The detailed procedure for these determinations, along with the formulas used for the calculations, can be found in our previous research [6,51].

2.4. Preparation of Results

Statistica 13.3 software [89] was used to analyze the data. A two-factor analysis of variance (ANOVA) was used (factor I—the degree of cadmium contamination of the soil, factor II—the type of remediating substance) with a significance level of p = 0.01. Homogeneous groups were identified using Tukey’s HSD test, and the η² coefficient, which determines the contribution of individual independent variables to shaping the results of the study, was calculated using the ANOVA method of analysis of variance. In addition, r-Pearson correlation coefficients (p < 0.01) were calculated between the study variables. The heat of combustion (Q), the heating value (Hv) and the amount of energy extracted from Zea mays biomass (Y_EP) were presented in heat maps using RStudio 2023.06.0 software [90,91,92]. The coefficients determining the contribution of each independent variable to the shaping of the study results (η²) were illustrated in a pie chart created using the Circos package 8 [93].

Taking into account the yield of dry matter of Zea mays shoots and leaves (Y_A) and roots (Y_R); the heat of combustion of Zea mays (Q); and the cadmium content of soil (Cd_S), the shoots and leaves (Cd_A) and roots (Cd_R) were calculated:

• The heating value of the dry matter of shoots and leaves of Zea mays is expressed as Hv (MJ kg⁻¹) and is calculated as follows: $\mathrm{H}\mathrm{v}={\displaystyle \frac{\mathrm{Q}\left(100-\mathrm{M}\mathrm{c}\right)}{100}}-\mathrm{M}\mathrm{c}$ × 0.0244, where Q—heat of combustion of the dry matter of shoots and leaves of Zea mays; M_C—moisture content of the biomass (%); and 0.0244—correction coefficient for the enthalpy of water evaporation (MJ kg⁻¹).
• The energy yield of the dry matter of shoots and leaves of Zea mays is expressed as Y_EP (kJ) and is calculated as follows: Y_EP = Hv × Y, where Hv—the heating value of the dry matter of the shoots and leaves of Zea mays (MJ kg⁻¹); and Y—the dry matter of the shoots and leaves of Zea mays produced from 1 kg of soil.
• Cadmium uptake by Zea mays (U) is expressed as the sum of the uptake by the leaves (U_A) and by the roots (U_R) of the plants: U = U_A + U_R, where U_A = Y_A × Cd_A and U_R = Y_R × Cd_R. Cadmium uptake by Zea mays expressed in μg Cd per pot. Y_A indicates shoots and leaves yield; Y_R—root yield; Cd_A—cadmium content in shoots and leaves of Zm; and Cd_R—cadmium content in the roots of Zm.
• The indices of cadmium uptake in shoots and leaves (RI_A) and in roots (RI_R) are calculated according to the formulas: ${\mathrm{R}\mathrm{I}}_{\mathrm{A}}={\displaystyle \frac{{\mathrm{U}}_{\mathrm{A}}}{{{\mathrm{U}}_{\mathrm{A}}+\mathrm{U}}_{\mathrm{R}}}}\times 100$%; ${\mathrm{R}\mathrm{I}}_{\mathrm{R}}={\displaystyle \frac{{\mathrm{U}}_{\mathrm{R}}}{{{\mathrm{U}}_{\mathrm{A}}+\mathrm{U}}_{\mathrm{R}}}}\times 100$%.
• The cadmium bioaccumulation index in shoots and leaves (BAF_A) and in roots (BAF_R) of Zea mays was calculated according to the following equation: ${\mathrm{B}\mathrm{A}\mathrm{F}}_{\mathrm{A}}={\displaystyle \frac{{\mathrm{C}\mathrm{d}}_{\mathrm{A}}}{{\mathrm{C}\mathrm{d}}_{\mathrm{S}}}}$ and ${\mathrm{B}\mathrm{A}\mathrm{F}}_{\mathrm{R}}={\displaystyle \frac{{\mathrm{C}\mathrm{d}}_{\mathrm{R}}}{{\mathrm{C}\mathrm{d}}_{\mathrm{S}}}}$, where Cd_A denotes the cadmium content of the shoots and leaves of Zm; Cd_R denotes the cadmium content of the roots of Zm; and Cd_S is the cadmium content of the soil, of course, in comparable units.

3. Results

3.1. Impact of Cadmium on Zea mays Biomass

3.1.1. Yield and SPAD

The elevated cadmium levels in the soil clearly inhibited the growth of Zea mays (Figure 1a,c and Figure 2a,c). Not all the substances tested that were applied to the soil had a clear effect on the aerial biomass of maize (Figure 1a,b). In cadmium-uncontaminated soil, molecular sieve, zeolite, bark, HumiAgra, and expanded clay did not modify the biomass of aerial parts, whereas sepiolite, starch, and liming reduced it by 13%, 24%, and 11%, respectively, and compost increased it by 14%. The negative effect of sepiolite, starch, and CaCO₃ intensified after their application to cadmium-contaminated soil. In this series of experiments, these substances exacerbated the biomass regression caused by cadmium by 52%, 31%, and 37%, respectively, whereas molecular sieve, compost, HumiAgra, and expanded clay resulted in an increase of 80%, 68%, 17%, and 19%, respectively. However, they did not completely eliminate the toxic effects of cadmium on the development of aerial parts of Zea mays, but only reduced their size.

On average, the molecular sieve increased the aerial part yield by 25%, compost by 29%, while starch, zeolite, and liming decreased it by 26%, 24%, and 18%, respectively, regardless of the cadmium content in the soil (Figure 1b). In contrast, the molecular sieve increased root yield by 16%, zeolite by 22%, and compost by 24%, while starch decreased it by 16% (Figure 2b). The other substances had no significant effect on the biomass of the Zea mays rootstock. When comparing the effects of all soil remediation enhancers on the roots and aerial parts, there is a clear positive evaluation of molecular sieve and compost in this enhancement. Both substances can be considered for use in the remediation of soils with elevated cadmium levels and for growing energy crops in them. This is especially important given that the potency of the effect of cadmium on the aerial parts and roots was similar, as evidenced by the average biomass results obtained from all sites, regardless of the substances used to offset the toxic effects of cadmium on Zea mays. Indeed, the biomass of aerial parts decreased by 58% under the effect of cadmium (Figure 1c), and comparatively, that of the roots decreased by 54% (Figure 2c). The dry matter content of maize was not affected by the applied substances or the cadmium concentration in the soil (

Table 2. Dry matter content of Zea mays biomass, %.

Treatment	Dose Cd, mg kg−1
	0	15	Average
Shoots and leaves
Control	12.43 ± 0.23 a	12.45 ± 0.71 a	12.44 A
Molecular sieve	12.20 ± 0.60 a	12.55 ± 0.73 a	12.38 A
Zeolite	12.29 ± 0.54 a	12.73 ± 0.45 a	12.51 A
Sepiolite	12.43 ± 0.33 a	12.62 ± 1.01 a	12.53 A
Expanded clay	12.45 ± 0.25 a	12.55 ± 0.58 a	12.50 A
Calcium carbonate	12.46 ± 0.42 a	12.23 ± 0.82 a	12.37 A
Starch	12.50 ± 0.71 a	12.76 ± 0.83 a	12.63 A
Compost	12.48 ± 0.12 a	12.66 ± 0.44 a	12.58 A
Fermented bark	12.22 ± 0.19 a	12.91 ± 0.98 a	12.58 A
HumiAgra	12.11 ± 0.40 a	12.61 ± 0.42 a	12.36 A
Average	12.36 I	12.61 I
Source of variation (F statistic and probability level): Cd dose: F—15,187.19 (p < 0.01); Treatment: F—315.07 (p < 0.01); Cd dose × Treatment: F—48.71 (p < 0.01)
Roots
Control	12.13 ± 0.56 a	11.41 ± 0.87 a	11.77 A
Molecular sieve	10.68 ± 0.35 a	11.04 ± 0.75 a	10.86 A
Zeolite	11.96 ± 0.72 a	11.68 ± 0.07 a	11.82 A
Sepiolite	11.65 ± 0.48 a	11.53 ± 0.91 a	11.59 A
Expanded clay	11.48 ± 0.37 a	11.93 ± 0.94 a	11.71 A
Calcium carbonate	11.91 ± 0.87 a	11.48 ± 0.68 a	11.69 A
Starch	11.76 ± 0.50 a	11.53 ± 0.79 a	11.65 A
Compost	11.60 ± 0.68 a	11.71 ± 1.02 a	11.66 A
Fermented bark	11.58 ± 0.80 a	11.46 ± 0.81 a	11.52 A
HumiAgra	12.30 ± 0.87 a	11.74 ± 0.88 a	12.02 A
Average	11.71 I	11.55 I
Source of variation (F statistic and probability level): Cd dose: F—2605.51 (p < 0.01); Treatment: F—24.95 (p < 0.01); Cd dose × Treatment: F—16.72 (p < 0.01)

Statistical calculations were made separately for shoots and leaves and roots. Values marked with a lowercase letter (a) form homogeneous groups for dry matter content of shoots and leaves and roots, values marked with an uppercase letter (A) indicate significance for production-enhancing substances, and values marked (I) indicate significance for cadmium doses, p < 0.010, N = 4 for each standard deviation.

). In the aerial parts, it ranged from 12.36% (0 mg Cd dose) to 12.61% (15 mg Cd dose), and in the roots, from 11.71% to 11.55%, respectively. These differences were not statistically significant.

Cadmium had a negative effect on the greenness index (SPAD) of Zea mays leaves (

Table 3. Zea mays leaf greenness index (SPAD).

Treatment	Dose Cd, mg kg−1
	0	15	Average
Control	35.61 ± 1.91 a–c	32.02 ± 2.00 c–g	33.82 AB
Molecular sieve	35.90 ± 0.69 a–c	32.09 ±1.53 b–g	34.00 A
Zeolite	35.08 ± 2.12 a–d	32.63 ± 0.50 b–f	33.86 A
Sepiolite	37.82 ±2.29 a	34.97 ± 2.38 a–e	36.40 A
Expanded clay	27.48 ± 1.55 gh	30.53 ± 1.72 d–g	29.01 CD
Calcium carbonate	32.08 ± 1.95 b–g	29.70 ± 089 f–h	30.89 BC
Starch	28.21 ± 2.91 f–h	25.24 ± 1.13 h	26.72 D
Compost	36.78 ± 2.74 ab	30.64 ± 1.44 d–g	33.71 AB
Fermented bark	30.05 ± 1.74 fg	28.94 ± 0.94 f–h	29.49 CD
HumiAgra	30.30 ± 0.85 efg	29.29 ± 2.03 f–h	29.80 C
Average	32.93 I	30.61 II
Source of variation (F statistic and probability level): Cd dose: F—33.65 (p < 0.01); Treatment: F—22.59 (p < 0.01); Cd dose × Treatment: F—3.54 (p < 0.01)

Values marked with the same lowercase letters (a–h) form homogeneous groups for the greenness index, values marked with uppercase letters (A–D) denote significance for production-enhancing substances, and values marked (I,II) denote significance for cadmium doses, p < 0.010, N = 4 for each standard deviation.

). The average SPAD index, in the series without the addition of cadmium to the soil, was 32.93, while after its application it decreased to 30.61, but it was not only this element that reduced the SPAD value, as starch, bark, HumiAgra and expanded clay also contributed to lowering its value. The extent of SPAD reduction by the aforementioned materials was, on average regardless of the amount of cadmium in the soil, 21%, 13%, 12% and 14%, respectively. The other substances (molecular sieve, sepiolite, zeolite, compost and CaCO₃) did not significantly change the greenness index.

3.1.2. The Energy Value of Zea mays

The heat of combustion (Q) of Zea mays produced in cadmium-uncontaminated soil ranged from 17.99 MJ kg⁻¹ d.m. to 18.65 MJ, and in contaminated soil from 17.82 MJ to 18.55 MJ (Figure 3). In the control object, without production-enhancing substances, the Q value was constant, regardless of the cadmium contamination in the soil. On the other hand, the addition of sepiolite, compost, starch, HumiAgra, and zeolite to uncontaminated soil significantly reduced Q, the addition of expanded clay increased it from 18.54 MJ to 18.65 MJ, and the application of bark and calcium carbonate caused no significant changes. On the other hand, for Zea mays grown in soil containing 15 mg Cd kg⁻¹, all fertilizers except zeolite contributed to a reduction in Q. The molecular sieve had the greatest effect, reducing Q from 18.55 MJ to 17.82 MJ.

The dependence of the heating value (Figure 4) of Zea mays on the independent variables was identical to that of the heat of combustion (Figure 3), except that the values documenting the heating value (Hv) were lower than those representing the heat of combustion. The Hv values ranged from 14.52 MJ kg⁻¹ to 15.06 MJ for Zea mays grown in uncontaminated soil and from 14.37 MJ kg⁻¹ to 14.98 MJ for those grown in contaminated soil. In both sets of experiments, Zea mays grown on molecular sieve amended soil had the lowest heating value.

Energy production (Yep) from Zea mays biomass was significantly affected by the conditions under which the crop was grown (Figure 5). The value of Yep in the series of the experiment where the soil was not contaminated with cadmium ranged from 164 kJ kg⁻¹ to 245 kJ kg⁻¹, while in the series with contaminated soil, it ranged from 40 kJ kg⁻¹ to 145 kJ kg⁻¹, depending on the remediating substance used. The results demonstrate the significant negative effect of increased cadmium content in the soil on Yep. On average, this metal caused a 57% reduction in Yep. But it was not only cadmium that contributed to the reduction in Yep. This was also caused by some substances applied to the soil, such as sepiolite, starch, and calcium carbonate. The analyzed parameter was positively affected by the compost added to the soil in both experimental series and, in the series with increased cadmium content, also by the molecular sieve. The other substances introduced into the soil did not significantly affect the value of Yep.

3.1.3. Cadmium Content of Zea mays

The cadmium content in the aerial parts and roots of Zea mays was related to its concentration in the soil (

Table 4. Cadmium content in soil and Zea mays biomass, mg Cd kg⁻¹ d.m.

Treatment	Dose Cd, mg kg−1
	0	15	Average
Soil
Control	0.115 ± 0.002 d	14.029 ± 0.489 b	7.072 C
Molecular sieve	1.619 ± 0.115 c	14.160 ± 0.577 b	7.890 AB
Zeolite	0.276 ± 0.012 d	14.395 ± 0.157 b	7.336 BC
Sepiolite	0.228 ± 0.026 d	14.510 ± 0.349 b	7.369 BC
Expanded clay	0.211 ± 0.016 d	14.874 ± 0.605 b	7.543 A–C
Calcium carbonate	0.225 ± 0.005 d	14.456 ± 0.247 b	7.341 BC
Starch	0.222 ± 0.036 d	14.238 ± 0.159 b	7.230 C
Compost	0.189 ± 0.012 d	15.980 ± 1.155 a	8.085 A
Fermented bark	0.194 ± 0.006 d	14.931 ± 0.297 b	7.563 A–C
HumiAgra	0.165 ± 0.007 d	14.663 ± 0.491 b	7.414 BC
Average	0.344 II	14.624 I
Source of variation (F statistic and probability level): Cd dose: F—28,615.14 (p < 0.01); Treatment: F—5.18 (p < 0.01); Cd dose × Treatment: F—9.27 (p < 0.01)
Shoots and leaves
Control	0.015 ± 0.001 l	0.030 ± 0.004 i	0.023 I
Molecular sieve	0.011 ± 0.000 jk	0.094 ± 0.001 h	0.053 H
Zeolite	0.010 ± 0.000 jk	0.718 ± 0.001 b	0.364 B
Sepiolite	0.010 ± 0.001 jk	0.378 ± 0.001 f	0.194 F
Expanded clay	0.009 ± 0.001 kl	0.572 ± 0.005 c	0.291 C
Calcium carbonate	0.003 ± 0.000 l	0.305 ± 0.001 g	0.154 G
Starch	0.010 ± 0.001 jk	0.833 ± 0.007 a	0.422 A
Compost	0.005 ± 0.001 kl	0.445 ± 0.009 e	0.225 E
Fermented bark	0.008 ± 0.001 kl	0.829 ± 0.002 a	0.419 A
HumiAgra	0.003 ± 0.001 l	0.474 ± 0.002 d	0.239 D
Average	0.008 II	0.468 I
Source of variation (F statistic and probability level): Cd dose: F—621,495.70 (p < 0.01); Treatment: F—22,934.70 (p < 0.01); Cd dose × Treatment: F—23,196.00 (p < 0.01)
Roots
Control	0.050 ± 0.004 h	5.512 ± 0.096 a	2.781 A
Molecular sieve	0.037 ± 0.008 h	0.743 ± 0.016 g	0.390 G
Zeolite	0.034 ± 0.002 h	3.170 ± 0.007 c	1.602 C
Sepiolite	0.051 ± 0.001 h	2.893 ± 0.005 e	1.472 E
Expanded clay	0.043 ± 0.002 h	3.535 ± 0.008 b	1.789 B
Calcium carbonate	0.034 ± 0.001 h	2.012 ± 0.004 f	1.023 F
Starch	0.052 ± 0.002 h	3.569 ± 0.009 b	1.811 B
Compost	0.039 ± 0.012 h	2.884 ± 0.079 e	1.462 E
Fermented bark	0.060 ± 0.002 h	3.001 ± 0.009 d	1.531 D
HumiAgra	0.056 ± 0.003 h	3.003 ± 0.012 d	1.530 D
Average	0.050 II	3.030 I
Source of variation (F statistic and probability level): Cd dose: F—152,384.40 (p < 0.01); Treatment: F—2489.80 (p < 0.01); Cd dose × Treatment: F—2457.70 (p < 0.01)

Statistical calculations were made separately for soil, shoots and leaves, and roots. Values marked with the same lowercase letters form homogeneous groups for cadmium content in soil (a–d), shoots and leaves (a–l), and roots (a–h); values marked with uppercase letters indicate significance for production-enhancing substances for cadmium content in soil (A–C), shoots and leaves (A–I), and roots (A–G); and values marked (I,II) indicate significance for cadmium doses, p < 0.010, N = 4 for each standard deviation.

). At all sites where cadmium was added to the soil, its accumulation in the plant increased. In the series of experiments with uncontaminated soil, the average cadmium content in aerial parts was 0.008 mg kg⁻¹ d.m., and in roots 0.05 mg kg⁻¹ d.m., while in the series of experiments with soil contaminated with this element, 0.468 mg Cd accumulated in 1 kg d.m. of aerial parts, and 3.03 mg Cd in roots. All the treatments applied reduced the cadmium content in the aerial parts of Zea mays grown in soil not contaminated with this element and increased its amount in the plant grown in contaminated soil. A different pattern was observed in the roots. In these organs, none of the treatments significantly changed the amount of Cd in the plant grown in uncontaminated soil, and all of them reduced its amount in the plant grown in soil supplemented with 15 g Cd kg⁻¹ d.m. of soil. The molecular sieve soil amendment and CaCO₃ did this to the greatest extent.

The average value of the cadmium bioaccumulation index (BAF) in shoots and leaves of Zea mays grown in soil uncontaminated with this element was 0.040, and in contaminated soil it was 0.032, while in roots it was 0.225 and 0.208, respectively (

Table 5. Bioaccumulation index (BAF) of cadmium Zea mays.

Treatment	Dose Cd, mg kg−1
	0	15	Average
Shoots and leaves
Control	0.130 ± 0.009 a	0.002 ± 0.000 l	0.066 A
Molecular sieve	0.007 ± 0.001 l	0.007 ± 0.001 l	0.007 H
Zeolite	0.036 ± 0.002 fg	0.050 ± 0.001 cd	0.043 CD
Sepiolite	0.044 ± 0.005 d–f	0.026 ± 0.001 h–j	0.035 E
Expanded clay	0.043 ± 0.003 d–f	0.038 ± 0.002 fg	0.041 D
Calcium carbonate	0.013 ± 0.002 k	0.021 ± 0.001 i–k	0.017 G
Starch	0.045 ± 0.004 d–f	0.059 ± 0.001 b	0.052 B
Compost	0.026 ± 0.002 h–j	0.028 ± 0.002 hi	0.027 F
Fermented bark	0.041 ± 0.003 ef	0.056 ± 0.001 bc	0.048 C
HumiAgra	0.018 ± 0.001 jk	0.032 ± 0.001 gh	0.025 F
Average	0.040 I	0.032 II
Source of variation (F statistic and probability level): Cd dose: F—173.17 (p < 0.01); Treatment: F—287.80 (p < 0.01); Cd dose × Treatment: F—428.28 (p < 0.01)
Roots
Control	0.435 ± 0.032 a	0.393 ± 0.017 b	0.414 A
Molecular sieve	0.023 ± 0.002 j	0.052 ± 0.003 j	0.038 H
Zeolite	0.123 ± 0.005 i	0.220 ± 0.003 d–g	0.172 F
Sepiolite	0.224 ± 0.026 d–f	0.199 ± 0.005 fg	0.212 DE
Expanded clay	0.204 ± 0.016 e–g	0.238 ± 0.010 de	0.221 D
Calcium carbonate	0.151 ± 0.003 hi	0.139 ± 0.003 i	0.145 G
Starch	0.234 ± 0.027 de	0.251 ± 0.002 d	0.242 C
Compost	0.206 ± 0.010 e–g	0.180 ± 0.009 gh	0.193 EF
Fermented bark	0.309 ± 0.010 c	0.201 ± 0.004 fg	0.255 BC
HumiAgra	0.339 ± 0.015 c	0.205 ± 0.007 e–g	0.272 B
Average	0.225 I	0.208 II
Source of variation (F statistic and probability level): Cd dose: F—29.71 (p < 0.01); Treatment: F—399.78 (p < 0.01); Cd dose × Treatment: F—79.62 (p < 0.01)

Statistical calculations were made separately for shoots and leaves and roots. Values marked with the same lowercase letters form homogeneous groups for cadmium bioaccumulation index (BAF) in shoots and leaves (a–l) and in roots (a–j), values marked with uppercase letters indicate significance for production-enhancing substances for BAF in shoots and leaves (A–H) and in roots (A–H), and values marked (I,II) indicate significance for cadmium doses, p < 0.010, N = 4 for each standard deviation.

). All the applied fertilizers caused a reduction in BAF values in both aerial parts and roots. This is reflected in the average results obtained, regardless of the cadmium content in the soil. The highest value of the bioaccumulation index occurred in Zea mays grown in the control object without the application of fertilizers. It was 0.066 in the aerial parts, and 0.414 in the roots. The average results analyzed were significantly influenced by the different effects of production-enhancing substances on uncontaminated and contaminated soil on the bioaccumulation capacity of cadmium by the tested plant. After the application of production-enhancing substances, the bioaccumulation of cadmium in Zea mays grown in uncontaminated soil decreased in both in aerial parts and roots, whereas in Zea mays grown in contaminated soil, it increased in aerial parts and decreased in roots.

The cadmium uptake (Ua) by Zea mays (Table S1) and the uptake index (RI) calculated from the uptake depended on the content of this element in the soil and the fertilizers used (Figure 6). Under the influence of a dose of 15 mg Cd kg⁻¹ soil, its value decreased on average from 40.98% to 34.91% in the aerial parts, while in the roots it increased from 59.02% to 65.09%. All fertilizers reduced the magnitude of this index in the roots of Zea mays grown in soil supplemented with 15 mg Cd kg⁻¹. In this series of experiments, the highest index (97.75%) was recorded in the roots of the plant grown on unfertilized control soil, and the lowest in the bark-fertilized soil (45.66%). Conversely, the value of this index per aerial parts was arranged inversely, as the highest index was recorded after bark fertilization (54.34%), and the lowest in the control object. The positive effect of the other applied fertilizers on the Cd uptake index in the aerial parts is also favorable, as it provides the possibility of clearing the soil of this element, provided that the biomass of the aerial parts is used for energy purposes.

3.1.4. Interdependencies Between Quantitative Variables

Soil contamination with cadmium determined the results to a greater extent than the production-enhancing substances used (Figure 7). The function of this contaminant was the Y_A at 82% and Y_R at 86%; the cadmium content of Y_A at 60% and Y_R at 77%; the uptake of cadmium by Y_A at 56% and Y_R at 78%; and the amount of Yep at 82%. Its effect on the Q and Hv of the biomass was relatively small at only 7%. In contrast to cadmium, the soil improvers had the greatest effect on Zea mays leaf greenness index (62%), BAF in the plant (39–87%) and biomass Hv 77%. They also had a relatively high effect on cadmium redistribution in the plant (38%) and bioaccumulation (39–87%).

The Y_A and Y_R of Zea mays was positively correlated with the value of the SPAD greenness index and the redistribution of cadmium to aerial parts, as well as the amount of Yep, and negatively correlated with the cadmium content of the soil and the plant, and the uptake of cadmium from the soil (Figure 8). In contrast, there was no significant correlation between the yield of Zea mays and its Q, Hv, and BAF of this element in the plant. Soil and plant cadmium content was negatively correlated, not only with plant yield, but also with SPAD and Yep value, and positively correlated with soil cadmium uptake. In addition, root cadmium content was significantly positively correlated with the RI_R and negatively correlated with the RI_A. The correlation between the energy indices Q, Hv and Yep and the other parameters studied is interesting. In fact, Q and Hv were only positively related to BAF in roots and aerial parts of Zea mays. They were not determined by the other properties studied. On the other hand, Yep was significantly positively related to Y_A and Y_R and to the redistribution of cadmium to RI_A, and negatively related to the cadmium content in the environment (soil, plant).

The first principal component reproduced the primary variables to the greatest extent (Figure 9a). However, the yield of Zea mays (Y_A, Y_R) and the amount of biomass energy produced (Yep) were negatively related to this component, whereas the cadmium content in the plant (Cd_A, Cd_R) and in the soil (Cd_S) and its uptake by Zea mays (U_A, U_R) were positively related to this component. This means that increased cadmium content in the soil decreased the values of negatively correlated dependent variables and increased the values of positively correlated dependent variables (Figure 9b). In addition, the spatial distribution of the results demonstrates significant differences between the results obtained on uncontaminated and cadmium-contaminated soil. On the other hand, Q, Hv, BAF_R, and RI_R were quite strongly negatively correlated with the second principal component (Figure 9a). However, the RI_A was positively correlated with the described variable. Practically, the BAF_A was not correlated with any of the principal components discussed, while the SPAD was partially correlated only with the first principal component.

4. Discussion

Growing energy crops such as Zea mays in soils polluted with heavy metals is part of the idea of sustainable biomass production. This process combines the simultaneous extraction of renewable energy sources with soil remediation, leading to improved soil health [94]. Such a solution, which is a cornerstone of sustainable development strategies, promotes the rational use of degraded land, reduces greenhouse gas emissions, and reduces the need for fossil fuels. It is clear that, in order to define strategies for utilizing this pool of plant resources, it is necessary to assess the magnitude of the effects of cadmium interference on the growth and development of plants, including Zea mays, which sheds light on its energy potential despite the pressure of this xenobiotic. This is also an appropriate line of research as it indirectly indicates the changes occurring in the soil [18,95,96]. According to Raza et al. [97], exposure to cadmium can cause stunted growth both of roots and of shoots and leaves, resulting in reduced plant yields and causing economic losses. These reports correspond with our results. In our study, the weight of roots of Zea mays growing in soil contaminated with cadmium at 15 mg Cd kg⁻¹ d.m. of soil was 60.75% lower than in uncontaminated soil, and the aerial parts were 61.61% lower, respectively (Figure 1 and Figure 2). Plant biomass was characterized by a relatively stable dry matter content (Table 2). The negative effect of cadmium on plant growth and development is due to its easy penetration into the roots and subsequent transport to the aerial parts. This, in turn, reduces the efficiency of photosynthesis and the uptake of water and essential macro- and micronutrients, interfering with their proper assimilation and distribution in the plant [98,99]. Cadmium photoactivates photosystem II (PSII) [100]. Induced oxidative stress in plants generates the overproduction of reactive oxygen species (ROS), which can cause disorders in cellular metabolism, including lipid peroxidation, protein oxidation, mitochondrial membrane depolarization, DNA damage, and apoptosis [101,102]. It also interferes with oxidative phosphorylation and reduces ATP synthesis [99]. Subsequently, as a result of the impaired division of mitotic processes in plants, there is deformation of the root system, inhibition of lateral root formation [103], reduced transpiration, and leaf chlorosis [104], which ultimately reduces plant growth and development [31,105]. The reduced biomass of roots as well as shoots and leaves correlates with photosynthetic disorders, as confirmed by our study, since the SPAD of Zea mays leaves decreased from 32.93 to 30.61 under the effect of cadmium (Table 3).

Obviously, the biomass from plants used in green remediation should be used for energy purposes. Such a sustainable approach is all the more reasonable as the Q (Figure 3) and Hv (Figure 4) of Zea mays biomass were stable and not altered by cadmium. In the tested samples, the highest values defining the Q of Zea mays grown in cadmium-uncontaminated soil reached the highest values of 18.65 MJ, while in cadmium-contaminated soil it was 18.55 MJ (Figure 3). In contrast, the highest values for the Hv were 15.06 MJ for Zea mays grown in uncontaminated soil and 14.98 MJ for Zea mays grown in cadmium-contaminated soil (Figure 4). These values were comparable to those obtained in our previous studies on soils affected by other contaminants (

Table 6. Heating value of Zea mays (Hv) grown under stress conditions, MJ kg⁻¹ air-dry matter plants.

Development Stage of Zea mays	Type of Contamination	Dose per kg of Soil d.m.	Heating Value	References
BBCH 51 phase	Cr6+	0 mg 60 mg	14.80 14.85	[6]
BBCH 51 phase	Unleaded gasoline 95	0 cm3 24 cm3	15.12 15.34	[106]
BBCH 51 phase	Diesel oil	0 cm3 24 cm3	15.12 15.04	[107]
BBCH 39 phase	Ni2+	0 mg 400 mg	14.79 14.95	[108]
BBCH 39 phase	Co2+	0 mg 80 mg	14.79 14.91	[108]
BBCH 39 phase	Pb2+	0 mg 800 mg	16.48 16.54	[109]
BBCH 39 phase	Ash from Salix viminalis	0 mg 20 g	16.50 15.93	[56]
BBCH 39 phase	Ash from Carpinus betulus	0 mg 20 g	16.29 16.07	[110]

).

Therefore, the cultivation of crops on marginal land for energy production is justified in the context of reducing greenhouse gas emissions [111,112]. Biomass obtained indirectly from soils contaminated with various xenobiotics can be important in the energy balance. [113,114]. Therefore, the use of plants with remediation properties that combine the process of soil decontamination with bioenergy production has gained popularity in recent years [115]. According to Konieczna et al. [57], with an average fresh weight yield of Zea mays of 30–50 Mg ha⁻¹, 4050–6750 m³ ha⁻¹ of biogas can be expected to be produced, yielding 87–145 GJ ha⁻¹ of energy. In a study by Jankowski et al. [116], the energy gain of corn biomass was determined to be 172–265 GJ ha⁻¹. Its value was, on average, 34% higher than that of Sorghum saccharatum. It is also worth noting that corn straw can be a valuable feedstock for biogas production. The methane yield from this raw material ranges from 201 to 207 m³ Mg⁻¹ fresh weight, making it much more efficient than the traditionally used corn silage, for which this parameter settles at around 105 m³ Mg⁻¹ fresh weight [117]. In our study, the amount of energy obtained from Zea mays biomass was significantly correlated not only with the plant biomass, but also with the redistribution of cadmium to aerial parts and negatively with the cadmium content of the plant.

The results of our study showed that the content (Table 3), uptake (Table S1), and consequently the redistribution (Figure 6) of cadmium was significantly higher in the roots of Zea mays than in the aerial parts, confirming reports by other researchers [29,118].

The soil–plant interface plays an important function in the bioavailability of cadmium to plants [118], as plant roots are the first line of defense in the uptake of cadmium by plants [119]. The response to this relationship is root secretions consisting of low molecular weight (e.g., sugars, amino acids, and organic acids), multimolecular (e.g., proteins), and volatile organic compounds (e.g., carbon dioxide, alcohols, and aldehydes) that create a unique environment in the rhizosphere [120]. Yan et al. [41] note the role of root secretions acidifying the rhizosphere in the uptake of heavy metals. Phytosiderophores, carboxylates, and organic acids facilitate the chelation of heavy metals, increasing their solubility, mobility, and bioavailability. In addition, cadmium has a high mobility in soil compared to other heavy metals. It is rapidly taken up by the plant root system [23] and readily accumulated in plants [29,121]. The process of accumulation in the plant begins with the root uptake of cadmium via apoplasts, symplasts, or mineral transporters, followed by translocation to xylem and phloem tissues [122]. Tennakoon et al. [42] and Lin et al. [123] highlight specific genes that are responsible for cadmium uptake and translocation in plants. ZIP transporters, which are located in the cytoplasmic membrane, actively transport Cd2⁺ ions from the soil solution to the cytoplasm of the root cell, LCT transporters facilitate their transport to the aerial parts, and they regulate the transport and distribution of Cd²⁺ from the phloem to the stems and leaves. According to Kanwal et al. [124], Mn-Cd interactions and the regulation of NRAMP (Natural Resistance-Associated Macrophage Proteins) may limit the uptake and accumulation of cadmium in plants. ZmNRAMP2 is one of the Zea mays genes encoding the NRAMP2 protein. It is located in the tonoplasm, the central vacuole of the plant cell, suggesting that this protein may be involved in the transport of cadmium into the vacuole, among other things [125]. ATPases (P-type adenosine triphosphatases) known as heavy metal-associated (HMA) proteins also play an important role in this process [126].

Estimating the magnitude of the negative impact of cadmium on the growth and development of Zea mays, translated into its energy potential, leads to a discussion of the issue of the maximum efficiency of the soil-amendment substances used. It should be noted that the promotion of green remediation as a strategy to reduce cadmium contamination in soils is an effective treatment, provided that appropriate substances are selected to support the process [30,64,103,127]. Huang and Imran [65] point out two strategies used in the remediation of soils under cadmium pressure. The first is to enhance the mobilization of this element in the soil, and the second is to dynamize immobilization. In our study, molecular sieve and compost immobilized cadmium in the soil, thereby reducing its uptake by Zea mays and thus reducing its toxic effects on the plant. This resulted in a positive effect on the yield of Zea mays and the amount of energy obtained from its biomass. In turn, starch, zeolite, fermented bark, sepiolite, and expanded clay enhanced the mobilization process. The different effects of the soil-amendment substances studied on the persistence of cadmium in the soil are due to, among other things, their structure, their sorption properties, which mainly include organic substances that support bioremediation, and their ability to complex this element, attributed largely to mineral substances [128,129,130]. The sorptive properties of starch are mainly related to the polymers of its cross-linked form [131], and those of fermented bark to the complex structure of lignin, which enhances these interactions [132].

We demonstrated that, among the nine tested substances enhancing biomass production, molecular sieve and compost appear to be the most effective options for cadmium removal from soil. Both substances reduced the potency of cadmium toxicity on both roots and above-ground parts to the greatest extent (Figure 1 and Figure 2). The effectiveness of the molecular sieve in revitalizing cadmium-contaminated soil may be due to its homogeneous structure [133], although cadmium is also strongly immobilized by silanol groups (Si-O-H) which generate electrostatic interactions with metal cations, including Cd²⁺ [134]. In turn, compost enhances processes such as adsorption, complexation, precipitation, and redox reactions [135].

To summarize, using Zea mays biomass contaminated with this metal for energy production, the right next research step will be to conduct detailed analyses of the safety of the conversion processes and, above all, their environmental impact. Not to be overlooked, for example, is the issue of heavy metal accumulation in ash, which creates the necessity of its treatment to prevent secondary environmental pollution [136]. Therefore, further studies are needed to fully understand and optimize these processes. It should also be noted that studies conducted in pot experiments may not account for the natural heterogeneity of the soil, the presence of native soil microorganisms, or the variability of atmospheric conditions, all of which may affect the dynamics of soil processes and lead to differences between pot and field experiments.

5. Conclusions

The conducted studies demonstrate that elevated cadmium content in the soil negatively affects the growth and development of Zea mays. Cadmium reduces the biomass of aerial parts by 80% and roots by 68%. The yield of aerial parts and roots of Zea mays is positively correlated with the SPAD greenness index and the redistribution of cadmium to the aerial parts, as well as with the energy produced (Yep), whereas it is negatively correlated with the cadmium content in both the soil and the plant. The energy indices of Zea mays, including the heat of combustion (Q) and heating value (Hv), are positively related to cadmium bioaccumulation (BAF) in both roots and aerial parts. These indices are not influenced by the other properties tested. On the other hand, Yep is significantly positively correlated with the yield of both aerial parts and roots, as well as with the redistribution of cadmium to the aerial parts (RI_A), and negatively correlated with cadmium content in the environment (soil, plant). The heating value of Zea mays biomass obtained from cadmium-contaminated soil ranged from 17.82 MJ to 18.55 MJ. Cadmium exposure resulted in an average decrease in Yep by 57%. The above data prove that any substance that effectively reduces the toxic effects of cadmium on the plant is useful in supporting the phytoremediation of cadmium-contaminated soils, and such, effective materials should be sought. The studies performed indicate that molecular sieve and compost can play such a role. A prerequisite for the promotion of such a method of treating contaminated soil is the use of the plant biomass produced for energy purposes.