Growth and metabolic functions of Schizolobium amazonicum subjected to nickel doses

Crescimento e funções metabólicas de Schizolobium amazonicum submetido a doses de níquel

Abstract

Anthropic activities such as industries, agriculture and mining has generated public concern for its numerous irregular disposals of its waste, the incorrect deposition of heavy metals such as nickel (Ni) has caused the degradation and contamination of groundwater and water. Studies that point out cheap and efficient solutions have been an obstacle to the advancement of solutions for degraded area recovery programs. For this, a vegetable home experiment was developed, with an entirely randomized design with 5 treatments being a control (no metal) and 4 nickel concentrations (200 μM/L; 400 μM/L; 600 μM/L and 800 μM/L) with 6 repetitions. The variables analyzed were growth and biochemical activity. Plant height and diameter were not affected by increasing nickel concentrations and this response was due to the low leaf and leaflet production capacity of the species under these conditions, consequently reducing biomass production. Metabolic parameters such as sucrose, carbohydrates, proline and glycine increase under stressful conditions, which does not occur for nutritional configurations that decrease with increasing nickel stress.

Keywords:
contamination; trace element; Paricá; recovery

Resumo

Atividades antrópicas como das indústrias, agricultura e mineração têm gerado preocupação publica por seus consideráveis ​​descartes irregulares de resíduos, a deposição incorreta de metais pesados ​​como o níquel (Ni) por exemplo, tem causado a degradação e contaminação de áreas e águas subterrâneas. Estudos que apontem soluções baratas e eficientes têm sido buscados para o avanço das soluções nos programas de recuperação de áreas degradadas. Para isso, foi desenvolvido um experimento em casa de vegetação, com um delineamento inteiramente casualizado, sendo 5 tratamentos, um controle (sem metal) e 4 concentrações de níquel (200 μM/L; 400 μM/L; 600 μM/L e 800 μM/L) e 6 repetições. As variáveis analisadas foram crescimento e atividade bioquímica. A altura e o diâmetro das plantas não foram afetados com o aumento das concentrações de níquel e essa resposta foi devido à baixa capacidade de produção de folhas e folíolos da espécie nessas condições, consequentemente reduzindo a produção de biomassa. Parâmetros metabólicos como sacarose, carboidratos, prolina e glicina aumentam em condições estressantes, o que não ocorre para configurações nutricionais que diminuem com o aumento do estresse por níquel.

Palavras-chave:
contaminação; elemento traço; Paricá; recuperação

1. Introduction

The world over decades has been undergoing increasing processes of urbanization and industrialization, actions such as these inevitably lead to environmental pollution, areas contaminated by heavy metals are already from 50% which come from various sources, such as industrial residual materials, sewage, Agriculture and Mining Waste. In part, this is due to the lack of legislation and investment for the correct disposal, even though they are most of these areas located in developed countries (Khalid et al., 2017).

One of the heavy contaminating metals is nickel (Ni), widely used in the manufacturing industry of different equipment and utensils, such as corrosion -resistant metal alloys and stainless steel, batteries, cables, ignition devices, cutlery and textiles (Kumar et al., 2021). The increase in Ni concentration in the environment is also naturally, through erosion, weathering of rocks and volcanic eruption (Khan et al., 2019). Excess Ni causes seed germination inhibition, decreased seedling growth (Aqeel et al., 2022), cell division inhibition (Banerjee and Roychoudhury, 2020), chlorosis, necrosis and reduction of root growth, implying less development of the plant (Merlot, 2020). At the molecular level, the toxicity for ni causes disturbance in photosystems and the Calvin-Benson cycle, inhibiting the electron transport chain and, consequently, the accumulation of ATP and NADPH for the ineffectiveness of biochemical reactions of photosynthesis (Pardo-Hernández et al., 2021).

Paricá (Schizolobium Amazonicum Huber Ex. Ducke), Fabaceae - Caesalpinioideae, is a large tree species that can reach up to 40 m high and 100 cm in diameter, and can be found in the Brazilian Amazon, Venezuelan, Colombian, Peruvian and Boliviana (Carvalho et al., 2019). It has been widely used in the recovery of degraded areas, because it has excessively fast growth (Benjamim et al., 2021).

Therefore, the general hypothesis of this work is that Schizolobium amazonicum seedlings can adapt to soils with increasing doses of nickel. The general objective of this study was to evaluate the effects of nickel on the growth, biochemical and nutritional characteristics of young S. amazonicum plants subjected to toxic levels of nickel.

2. Material and Methods

2.1. Experimental conduction and plant material

The experiment was carried out in a greenhouse at the Institute of Agricultural Sciences (ICA), belonging to the Federal Rural University of the Amazon (UFRA), located in the municipality of Belém, Pará, whose geographic coordinates are 01° 27’ 21” S and 48° 30’ 16” W. The seeds used were of the tree species known as Paricá and scientific name Schizolobium amazonicum, supplied by AIMEX (Association of Wood Exporting Industries of the State of Pará), subjected to an average temperature of 26.8 °C, with relative air humidity of 95%.

To produce seedlings, the paricá seeds were initially mechanically scarified with 80 mm sandpaper and submerged in cold water for a period of 24 hours, aiming to absorb water to facilitate the breaking of dormancy. After this period, the seeds were placed in 4.6l Leonard-type pots, adapted with PET bottles containing washed and autoclaved sand, with three seeds per pot. After 15 days of sowing, Sarruge’s (1975) nutrient solution was applied to accelerate its growth. 60 days after sowing, dosages of nickel chloride (NiCl₂) were applied together with the SARRUGE nutrient solution (1875). The nickel dosages applied were based on scientific work, at the following concentrations: NiCl₂ 200 μM/L; NiCl₂ 400 μM/L; NiCl₂ 600 μM/L; NiCl₂ 800 μM/L. The solutions were renewed weekly and the pH was maintained between 5.8 and 6.0.

2.2. Experimental design and material collection and storage

To order the treatments, a completely randomized experimental design (CRD) was used, which consisted of 5 treatments, control plants (without nickel) and 4 doses of nickel chloride (NiCl₂ 200 μM/L; NiCl₂ 400 μM/L; NiCl₂ 600 μM/L; NiCl₂ 800 μM/L) in 6 replicates, totaling 30 experimental units. The choice of these doses was based on the alert and intervention values ​​recommended by Conama Resolution No. 420 of 2009. Uniform plants regarding the morphology of the aerial part, characterized by height, stem diameter, number of leaves and number of leaflets were selected for application of the treatments.

After 15 days of application of NiCl₂, the seedlings showed signs of toxicity (chlorosis, epinasty and leaf senescence) and were collected for analysis, separating the leaves, stems and roots and storing them in paper bags and placed in a forced air ventilation greenhouse. at 65 °C for a period of 48 hours. After drying, the separated parts were ground and stored.

2.3. Growth variables and biochemistry analyzed

The growth variables analyzed were height (measured from the soil surface to the apex of the plant, using a millimeter ruler), stem diameter (measured using a 200mm digital caliper), number of leaves, leaflets and the dry matter of the root (DMR), the shoot (DMS) and the total dry matter (TDM) were quantified after drying in an oven with air circulation at 65 °C.

The biochemical variables were sucrose (van Handel, 1968); total soluble carbohydrates (Dubois et al., 1956); reducing sugars (Rinner et al., 2012), nitrate (Cataldo et al., 1975); activity of the Nitrate Reductase enzyme (Hageman and Hucklesby, 1971); Free Ammonium (Weatherburn, 1967); Total Soluble Amino Acids (Peoples et al., 1989); Total Soluble Proteins (Bradford, 1976); Proline (Bates et al., 1973); and Glycine-betaine (Grieve and Grattan, 1983).

2.4. Determination of macronutrient content

The macronutrient analyzes of the aerial part and roots were sent to the chemistry laboratory at the Museu Paraense Emílio Goeldi. To determine the nitrogen (N), phosphorus (P) and potassium (K) contents, they were analyzed according to the methodology proposed by Tedesco et al. (1995). The magnesium (Mg), calcium (Ca) and sulfur (S) contents were determined according to the methodology described by Miyazawa and Madari (2009).

2.5. Statistical analysis of data

Statistical analysis of variables and generation of graphs was carried out using the R Studio software version 1.3.1093 using the ExpDes.pt library and the “dic” function, which already performs analysis of normality of residuals using the Shapiro-Wilk test and equality of variances using the Bartlett test, also using ANOVA and subsequently Tukey's Post-Hoc test, for all analyzes a significance level of 5% was considered.

3. Results and Discusion

3.1. Growth variables

The results showed that there was no increase in the height and diameter variables of paricá seedlings with increasing nickel concentrations (Figure 1a and 1b). It was observed in the height variable that from the concentration of 400 µM of Ni, significant differences occurred when compared to the control treatment. In the case of the diameter variable, this difference occurred after 600 µM of Ni.

Figure 1
Height and diameter of parica plants as a function of increasing nickel concentrations. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

The presence of toxic elements such as heavy metals affect the root system as seen in Figure 2, causing disturbances in protein structures and membrane permeability, inhibiting cell elongation and increasing lignification of cell walls, which results in plants with reduced growth (Shawai et al., 2017; Zhang et al., 2019). Furthermore, metals can also affect the production of carbohydrates, which are essential for plant growth, given that toxic levels of metals cause damage to the photosynthetic process, causing destabilization of reactions and carbon assimilation, a process that reduces height and the diameter of the seedlings (He et al., 2018).

Figure 2
Dry mass of roots, stem ad leaves of parica plants as a function of increasing nickel concentrations. Nickel concentration averages in the root and leaf. followed by the same letter. do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

The results showed a reduction in the leaves and leaflets of the plants subjected to the metal when compared to the control plants. The variable number of leaves, for example, presented a statistical difference in the 400 µM (2.33) and 800 µM (2.40) treatments, with reductions of 31.47% and 29.41%, respectively, when compared to the control plants (3.40) (Figure 3a). In the case of the number of leaflets, this statistical difference occurred in the 400 µM (12.0), 600 µM (20.20) and 800 µM (11.25) treatments, with reductions of 51.02%, 17.55% and 54.08%, respectively, when compared to the control (24.50) (Figure 3b).

Figure 3
Number of leaves and leaflets of paricá plants as a function of increasing nickel concentrations. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

The reductions in the number of leaves and leaflets in the growth plate can be explained by the low nitrogen concentration in the roots (Figure 4a), considering that this macronutrient plays an important role in the initiation and expansion rates of this organ (Lambers and Oliveira, 2019). Another possible consequence is the inhibition of chlorophyll biosynthesis, which resulted in disturbance of photochemical or biochemical activity, inducing its degradation, since the phytotoxic activity of this metal affects the chloroplastic structures of leaf cells, which may have influenced the amount of starch granules, due to the low photosynthetic activity, affecting the production of leaf biomass (Adrees et al., 2015a).

Figure 4
Nitrogen, phosphorus and potassium concentrations in paricá plants as a function of increasing nickel concentrations. Nickel concentration averages in the root and leaf. followed by the same letter. do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

The results regarding the dry mass of the root, stem and leaves showed variations with the application of the metal. When analyzing the data on root dry mass, there was a decrease in all treatments, with reductions of 40.15% (1.52), 31.89% (1.73), 53.15% (1.19) and 37.40% (1.59), leading to statistical differences when compared to the control plants (2.54). For the dry mass of the stem, it was noted that only the treatments of 200 μM (1.86) and 600 μM (2.05) of Ni presented statistical difference when compared to the control plants (2.52), with reductions of 26.19% and 18.65% respectively (Figure 2). In relation to the leaves, the lowest dry mass index occurred at the doses of 400 (2.42) and 800 µM (2.15) Ni, with reductions of 20.13% and 29.04% when compared to the control treatment (3.03).

The reduction in biomass caused by nickel can be justified by the denaturation of organic macromolecules and interference in the metabolism of fundamental nutrients such as Fe, Zn and Mg (Figure 4b), replacing them due to chemical affinity, especially with regard to lower dry weight of the roots due to the toxicity (Rehman et al., 2016).

3.2. Biochemical metabolism

Carbohydrate concentrations in leaves increased with increasing nickel concentrations, with the highest result observed at the dose of 800 µM (6.0) with a 97.36% increase in relation to the control plants (3.04). In the case of roots, the treatments of 200 µM (3.06) and 400 µM (3.33) presented higher carbohydrate concentrations, with increases of 36% and 48%, showing a significant difference with the control (2.25) (Figure 5a). The synthesis or degradation of carbohydrates works as a defense mechanism carried out by plants and called osmoregulation, being present in stress conditions such as the presence of heavy metals, which increases the concentration of carbohydrates in the plant (Sanches et al., 2017; Raza et al., 2022). This is observed in the leaf system of these vegetables. Sugars provide greater resistance to stress by maintaining redox reactions and membrane structure, the integrity of the cell wall and other molecules (Siddiqui et al., 2020).

Figure 5
Total soluble carbohydrates, sucrose and reducing sugars in parica plants as a function of increasing nickel concentrations. Nickel concentration averages in the root and leaf, followed by the same letter, do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

Sucrose concentrations (Figure 5b) increased in both roots and leaves with increasing metal doses. For leaves, statistical differences occurred in treatments 200 (13.78), 400 (15.82) and 600 (20.23) µM Ni, with increases of 30.61%, 49.95% and 91.75% in relation to the control (10.55). For roots, statistical differences occurred in treatments 200 (19.57), 600 (20.88) µM Ni, with 51% and 61.11% increases in relation to the control (12.96). Therefore, sucrose, the main form of carbohydrate transport, provides energy to maintain the osmotic balance of cells, seeking to increase resistance to this stress (Li et al., 2022), a fact that corroborates the data presented, denoting a possible induction of resistance of Paricá plants when in contact with the metal. The sucrose formed in the leaves is transported by the vascular tissues to other organs, acting as a source of energy for growth, or is stored in the form of reserve polysaccharides. The increase in sucrose may be related to the accumulation of hexoses that are used in the osmotic adjustment process, as the water molecules in the leaf bind to them to maintain the water level in the leaf and induce an osmotic adjustment in the stressed plant.

The increase in nickel dosages caused a decrease in reducing sugars (Figure 6a) in the roots, with lower results at doses of 400 (0.20) µM and 800 (0.20) µM Ni, 41.17% lower than in the control plants (0.34). In relation to the leaves, there was a significant increase in the concentration of sugars at the metal concentrations (200 (0.44) µM and 800 (0.77) µM nickel), presenting a statistical difference between the control treatments (0.19), with increases of 131.57% and 305.19%. The accumulation of reducing sugars in the aerial part, especially at the highest dose of the metal, is related to the maintenance of cellular respiration and photosynthetic metabolism, as protection and osmotic regulation, in order to maintain metabolic activities (Singh et al., 2016). However, in relation to the low concentration of reducing sugars in the roots, it can be indicated the inhibitory effect of metal toxicity in reducing root growth (Figure 2), which causes limitations in the translocation of carbohydrates, indicating the action of nickel in the transport of assimilates for this organism (Shah et al., 2017).

Figure 6
Reducing sugars in parica plants as a function of increasing nickel concentrations. Nickel concentration averages in the root and leaf. followed by the same letter. do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

Nitrate concentrations increased in paricá roots with increasing nickel concentrations, especially at the dose of 400 µM (0.076), causing a significant difference of 25% when compared to control plants (0.057). However, in the leaves this increase was not significant (Figure 7a). The activity of the nitrate reductase enzyme decreased with increasing nickel, with the lowest result observed at the highest dose of 800 µM (2.0), with a reduction of 46.8%, compared to control plants (3.76). The same behavior can be observed in ammonium concentrations in the roots that decreased 71.17% at the dose of 800 µM (2.28) in relation to control plants (7.91) (Figures 7b and 7c). The enzyme activity in the leaves was less significant and the treatments with nickel stress at doses of 400, 600 and 800 µM showed significant difference when compared to the control treatments. The ammonium concentrations in the leaves increased in the plants under stress, the opposite of the roots, and there was a significant difference when compared to the control plants in all treatments.

Figure 7
Concentrations of nitrate, nitrate reductase enzyme and free ammonium in parica plants as a function of increasing nickel concentrations. Nickel concentration averages in the root and leaf. followed by the same letter. do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

Nitrate absorption in roots occurs by cortical cells, through nitrate transport proteins (Dai et al., 2013), and the results of this study probably indicate that this transport protein was not affected, even with an increase in nickel concentration, due to there being a large absorption of nitrate by the roots (Figure 7a). However, nickel may be interfering with the nitrate translocation process to the aerial part, due to the low concentration of this substrate in the leaves. This can be proven by Reis et al. (2014) who state that nickel alters the activity of the nitrate reductase enzyme, influencing its translocation to the leaves. The low activity of the nitrate reductase enzyme, as well as the low concentration of nitrate in the leaves, may be the answer to the increase in ammonium in this organ.

The concentrations of amino acids and proteins in the leaves and roots decreased with increasing nickel concentrations, showing a statistical difference in all treatments, with the lowest result for amino acids in the roots observed at the dose of 600 µM and for proteins at the dose of 800 µM (Figure 8a and 8b). The accumulation of amino acids and proteins occurred in the paricá leaves when compared to the roots.

Figure 8
Concentrations of total soluble amoniacids. total soluble proteins in parica plants as a function of increasing nickel concentrations. Nickel concentration averages in the root and leaf. followed by the same letter. do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

The reduction of amino acids in plants exposed to nickel may be associated with changes in transcriptional levels that compile enzymes involved in metabolism (He et al., 2013). One of these enzymes is Glutamine Synthetase (GS), this enzyme is a precursor in the formation of amino acids (Sarangthem et al., 2017). Therefore, nickel may have reduced the level of GS transcription and contributed to reductions in the concentration of total soluble amino acids in Paricá plants.

For total soluble proteins, Wu et al. (2015) state that heavy metals cause a decline in protein content and a corresponding increase in the activity of hydrolytic enzymes such as proteases. Thus, the results suggest that nickel promoted the activation of proteolytic enzymes that degraded total soluble proteins, releasing amino acids used in the biosynthesis of specific amino acids such as proline (Figure 9). Another possible argument would be that Ni caused the denaturation of enzymes involved in protein synthesis (Singh et al., 2016) and induced the fragmentation of proteins due to the toxic effects of reactive oxygen species (ROS), causing a reduction in protein content (Anand et al., 2017).

Figure 9
Glycine betaine and proline concentrations in paricá plants as a function of increasing nickel concentrations. Nickel concentration averages in the root and leaf. followed by the same letter. do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

Glycine is considered a stress osmoregulator, showing a 47.54% increase in the concentration of this amino acid at a dose of 400 μM (142.4) as nickel stress increases, compared to the control treatment (74.69) (Figure 9a). Statistically, both roots and leaves showed significant differences when compared to control plants. The nickel doses that caused the greatest increases in this amino acid in root and leaf organs were 400 and 600 μM, respectively. The proline concentration increased linearly with increasing stress, with the last dose of 800 μM nickel showing the highest concentration of this amino acid. Statistically, there was a difference in all stress treatments when compared to control plants (Figure 9b).

In the presence of heavy metals, proline acts as a metal chelator, an antioxidant defense molecule and a messenger molecule (Hayat et al., 2012). The accumulation of proline and glycine may be contributing to the osmotic adjustment of these paricá plants at the cellular level in enzymatic protection, stabilization of the membrane structure, macromolecules and organelles (Wang et al., 2016). Proline is one of the main non-enzymatic agents of the antioxidant machinery (Sachdev et al., 2021), this amino acid aims to reestablish cellular homeostasis from the detoxication exposed by nickel, from the sequestration or degradation of these and, thus, prevents possible cellular damage.

3.3. Nutritional assessments: macronutrients

The concentrations of nitrogen, phosphorus and potassium in the leaves showed significant differences from the concentrations of 600 µM nickel when compared to the control plants (Figure 4), since the presence of nickel can cause interference in the absorption of other nutrients, a fact that can be observed when analyzing the data of this study. Phosphorus in the roots showed differences among all treatments with metals, with reductions of 5.4% (1.75), 14.59% (1.58), 38.37% (1.14), 50.27% (0.92) compared to the control plants (1.85). For nitrogen in the root, there was a difference in the concentrations of 600 µM (11.04) and 800 µM nickel (9.92), with reductions of 21.59% and 29.54% in relation to the control treatment (14.08). In the case of potassium in the root, a statistical difference was noted in the concentrations of 400 µM (16.74), 600 µM (12.24) and 800 µM (11.15) of nickel, with reductions in the absorption of this nutrient of 8.02%, 32.74% and 38.73% compared to the control plants (18.20).

Plants that are exposed to heavy metal toxicity generally present symptoms that can affect their development, such as impaired growth and browning of roots, and subsequent decline and death (Öztürk et al., 2015). In environments with high nickel levels, symptoms such as necrosis, chlorosis and nutrient deficiencies and imbalances in the cell membrane are recurrent, factors that impair the normal growth and development of plants (Ghori et al., 2019).

For the concentrations of secondary macronutrients in the leaves and roots, a decreasing behavior can be observed as the nickel dosages increase (Figure 10). In addition, for calcium in the roots, a difference was noted in the concentrations of 400 µM (2.62), 600 µM (2.03) and 800 µM (1.62) of nickel, with reductions of 23.16%, 40.46% and 52.49% compared to the control (3.41). Magnesium showed a difference in the roots and leaves, in the concentrations of 400 µM, 600 µM and 800 µM of nickel, in the case of the leaves there were reductions of 18.48% (3.13), 33.3% (2.56) and 47.13% (2.03) when comparing the control plants (3.84). In the case of magnesium in the roots, these reductions were 26.59% (2.07), 49.29% (1.43) and 62.05% (1.07) in relation to the control treatment (2.82). For sulfur in the roots, all treatments differed from the control and in the leaves, a statistical difference was noted and decreases of 12.37%, 27.68% and 37.13% were observed in the concentrations of 400 µM (2.69), 600 µM (2.22) and 800 µM (1.93) of nickel, respectively, in comparison to the control plants (3.07).

Figure 10
Concentrations of calcium. magnesium and sulfur in parica plants as a function of increasing concentrations of nickel. Nickel concentration averages in the root and leaf. followed by the same letter. do not differ from each other using the F test. at a 5% probability level. Different lowercase letters indicate statistical difference by Tukey test (P<0.05), identical letters do not differ significantly from each other.

The presence of heavy metals causes a decrease in the concentration of important nutrients such as Ca and Mg, mainly in leaves, due to competition or antagonism between these ions (Marschner, 2012). Furthermore, high concentrations of heavy metals in the soil greatly affect the coordination mechanism between essential elements, resulting in stunted growth and failures in the metabolic processes of cultivated crops (Khan et al., 2015), which can interfere with root expansion and the absorption of macronutrients from the soil, which justifies the reduction in calcium, magnesium and sulfur concentrations.

4. Conclusion

The paricá seedlings were sensitive to the application of increasing doses of nickel, especially after 200 μM/L, manifested mainly by the reduction in their growth. The root system was the organ most affected by nickel concentrations, reducing its biochemical activities in almost all analyzed variables. The ormoregulatory system analyzed by the concentrations of amino acids proline and glycine increased significantly, contributing to the cellular protection of vegetables. Nutritional factors were affected by nickel toxicity, largely because the root system was greatly affected.

Acknowledgements

To the Federal Rural University of the Amazon and the research group on Biodiversity Studies in Higher Plants (EBPS).

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Publication Dates

• Publication in this collection
  17 Jan 2025
• Date of issue
  2024

History

• Received
  05 Feb 2024
• Accepted
  06 Aug 2024