Assessing the Effects of Varying Lead Concentrations on Tomato Plant Growth and Physiological Parameters

Introduction

Soil pollution with poisonous metals has gotten to be a critical natural concern because of its potentially harmful effects on natural habitats. Raised hazardous heavy metals can be credited to range of human intervention and industrial regular activities, for example, rock mining, oil refining, electroplating, the combustion of coal, and creation of lead-infused fuel production.¹ The toxic effects observed in plants in the presence of elevated heavy metal concentrations could stem from various interactions at cellular scale ^[2]. Toxicity may arise when metals interact with sulphydryl groups in proteins, leading to the loss of biological function or structural integrity.³ For optimal plant growth, soil should contain between 3%and 6% organic matter, which boosts nutrient content and stabilizes soil pH.^4,5 The ideal P^H of the agricultural lands ought to be between 6.5 and 7.5. In later a long time soil pollution by heavy metals such as zinc (Zn), chromium (Cr), copper (Cu), cadmium (Cd), and nickel (Ni) can lead to their accumulation in the soil, causing the P^H shift by 2-3 units- either increasing or decreasing thus making the soil more alkaline or acidic.^{6, 7}

Lead directly or indirectly influences photosynthesis, nutrient absorption by plants, seedling growth, protein function, water regulation, and membrane permeability.^8-10 By inhibiting the enzymes necessary for chlorophyll production, CO₂ obsession, and the protein-bound pigment the complexation of photosynthesis process, Pb disrupts the regular operation of chloroplasts that at elevated concentrations.¹¹ By impeding the enzyme activities linked to CO₂ fixation, pigment protein complex aggregation in photosynthesis, and chlorophyll formation, a elevated concentration of lead in the photosynthetic organelle may disrupt chloroplast function.¹²

The hazardous nature of Pb heavy metals and their propensity to bioaccumulate in the environment pose a major threat to the safety of living organisms. In a way, heavy metals can be transformed into less harmful species, but unlike organic contaminants, they cannot be broken down by chemical or biological processes. The selection of any plant for heavy metal phytoextraction mostly depends on the biomass and tolerance potential of the chosen plant because plants have a delayed potential to collect heavy metals.^13,14 The high levels of metal particles removed from the treated soil coexisted with a high biomass of plants. In this mechanism, plant roots particularly remove heavy metals from water.¹⁵ Using aquatic species or hydroponically, plants are grown directly in the water or in water-rich surfaces like sand.¹⁶

As the second-most important vegetable crop in the world, tomatoes have a tendency to accumulate heavy metals including arsenic, cadmium, and lead.¹⁷ Heavy metals contaminated groundwater and soil can cause these metals to be accumulated by the plant, affecting its roots, branches, leaves, and fruits, among other components.

In plants, exposure leads to a decline in germination capacity, suppression of root and shoot elongation, disruption of mitotic spindle formation, induction of foliar chlorosis, impairment of photosynthetic machinery, decreased ion and nutrients assimilation and structural alteration in plasma membrane integrity and permeability.^18-21 It may disrupt the cellular a redox state in the plants, resulting in the production of reactive oxygen species (ROS)²² including hydrogen peroxide (H₂O₂), hydroxyl radical (OH^.) and superoxide anions (O₂^.) are generated under stress conditions and contribute to cellular damage through oxidative mechanism increased ROS production results in oxidative stress, which damages nucleic acids, oxidized proteins, inhibits enzymes, and promotes lipid peroxidation. These molecules trigger programmed cell death (PCD) and ultimately result in cell lysis.^23-26 Tomatoes that accumulate heavy metals may experience detrimental effects on plant physiology, including reduced photosynthesis, altered enzyme activity, and stunted development.²⁷ These metal-induced stresses can lead to morphological changes, such as stunted growth and leaf chlorosis. Heavy metal contamination in tomatoes moreover postures a potential hazard to human wellbeing when consumed.^28-30

Lead (Pb) toxicity is widely recognized to have adverse effects on brain development, potentially leading to cognitive impairment, reduced IQ, and behavioral disorders.In adults, it is associated with hypertension, renal dysfunction, and reproductive complications.³¹

Lead toxicity interferes with chlorophyll production, decreases the proficiency of the photosynthetic machinery, and leads to lower rates of photosynthesis.³² This disturbance not only reduces the energy available for plant growth but also affects the overall metabolic processes, potentially leading to hindered plant development, decreased biomass, and lower yields. Studies have shown that elevated lead levels can cause oxidative stress, affecting various cellular components involved in photosynthesis and overall plant wellbeing.³³

Phytoremediation, the use of plants to assimilate, degrade, or stabilize toxins from the environment, has gained recognition as an effective and environmentally friendly approach for mitigating heavy metal contamination, such as Pb. Tomato plants (lycopersicon esculentum) are especially suitable for phytoremediation due to their capacity to collect Pb in their roots, stems, and leaves.³⁴

Method and Materials 

Culture Condition (soil preparation)

The experiment was carried out in clay pots, where tomato seeds (lycopersicon esculentum) were grown in distinctive soil treatments. A compost and soil blend was arranged by combining compost with soil in a 3:1 proportion. This blend was at that point set in clay pots for tests. Tomato seeds were to begin with disinfected by dousing them in 20% H₂O₂ solution(v/v), followed by rinsing with the water and soaking for 5 days in between temperature 23-27˚C to keep up moisture.³⁵ After this the seeds were sprinkled into the nursery soil in clay pots and permitted to grow for 15 days. When the third leaf appeared on the tomato seedlings, they were first transplanted into control soil, followed by transplantation into contaminated soil of Pb (50, 70 and 90 mg/ kg soil), to evaluate the impacts of the compost blend and Pb contamination on plants growth. The lead metal concentrations (Pb) in the treatments were recorded in triplicates as takes after: (a) Pb concentration in the compost-treated soil (50 mg/kg), (b) Pb concentration in sullied soil (70mg/kg), and (c) Pb concentration in sullied soil (90 mg/kg).Soil examinations were performed at indicated days after sowing (DAS), such as 0, 18, 36, and 54 DAS, to monitor variation in Pb level and theire in impact on morphological and physiological parameters off plants.³⁶

Analysis of Parameters

Morphological Parameters

Plant height, number of leaves, shoot length, number of flowers, number of fruits, biomass accumulation, and moisture content were recorded. The impact of lead (Pb) contamination on leaf area index (LAI) of tomato plants was assessed at three developmental stages: 18, 36, and 54 DAS. The soil was artificially contaminated with Pb at three concentrations (50, 70, and 90 mg/kg of soil). A control group with uncontaminated soil was maintained for comparison. Each treatment was replicated three times.

Physiological Parameters

Coordinate Strategy for Measuring Leaf Area Index

 The grid method was used to measure the leaf area index (LAI) of tomato plants at 18, 36, and 54 days after sowing (DAS), this method gives a coordinate and reliable approach for determining leaf area and has been broadly utilized in agricultural research, fully expanded takes off from three arbitrarily chosen plants per treatment were carefully withdrawn for investigation and brought to the laboratory. Amid collection, safety measure were taken to minimize leaf harm and guarantee precision in ensuing estimations. A transparent grid sheet with known grid cell measurements (1cm x 1 cm) was used to measure the leaf area.³⁷ The grid was put on a level surface beneath legitimate light to ensure the perceivability of the leaf outlines during the measurements process. Individual leaves were placed beneath the grid, completely spread and smoothed to avoid covering. The number of gride cells covered by each leaf was counted. Mostly secured grid cell were included proportionally in the total number, with the half cell covered being counted as 0.5 cm².

The total leaf area was calculated utilizing the equation:

Leaf Area Index= Number of Grid Cell Secured x Area of One Grid Cell

The leaf area index (LAI) was at that point decided by dividing the total leaf area by the ground area possessed by the plant:

The strategy was repeated for three plants per treatment to guarantee reliability, and the average LAI for each treatment was calculated at 18, 36, and 54DAS.

Relative Growth Rate

 To analyze the relative growth rate (RGR) of tomato plants with respect to the weight at 18, 36, and 54 days after sowing (DAS), randomly selected plants were collected for quantifications. Plants were carefully evacuated to maintain a strategic distance from harm to the roots, and soil tenderly washed away using water. After washing, the plants were blotted with paper towels to evacuate surface moisture before measuring their fresh weight using a precision analytical digital balance.

Following this, the plants were placed in paper envelopes or weighing dishes and dried in an oven set at 45C for 72 hours, or until a steady weight accomplished. The dry weights of the plants were recorded.³⁸

Relative Growth Rate (day⁻¹), a measure of plant (without root) growth rate balanced to size, was estimated utilizing both dangerous and non-destructive (or image analysis based) methods.³⁹

RGR = (lnW₂-lnW₁)/ (T₂-T₁)

 In this condition, both W₁ and W₂ indicate the dry weight of the plants at time t₁ and t₂
, respectively, with t₁ and t₂ being the corresponding time points in days. This calculation enabled the assessment of growth elements between the progressive time intervals.

To ensure reliability, information was statistically analyzed utilizing methods such as ANOVA to detect significant distinction in RGR over the measured time intervals.

Pb Impacts on Photosynthesis and Chlorophyll Content

To analyze the chlorophyll content in tomato plants at 0, 18, 36, and 54 DAS, the process involves extracting chlorophyll utilizing 80% aqueous acetone and analyzing the extract by using UV-Visible spectroscopy.⁴⁰

To begin with, leaves from tomato plants at each specific time focuses (0, 18, 36, and 54 DAS) are collected. The leaves are rinsed with distilled water to evacuate any soil or contaminants at that point carefully blotted dry using tissue paper. Around 0.5 to 1 gm of leaf tissue is weighed from each time point. The tissue is the homogenized in 80% aqueous acetone utilizing a mortar and pestle or a homogenizer. After homogenization, the mixture is filtered or centrifuged to obtained the supernatant, with contains chlorophyll extract.

UV- Visible spectroscopy was used to measure absorption at two specific wavelengths: 645 nm and 663 nm for determination chlorophyll contents.

Chl. a=12.7⋅A₆₆₃​−2.69⋅A_645​

Chl. b= 22.9⋅A_645​−4.68⋅A₆₆₃​

A₆₄₅ and A₆₆₃ is absorption at 645nm and 663nm.

The total chlorophyll content (mg/ml) is the sum of chlorophyll a and chlorophyll b:

Total Chlorophyll=Chl. a+ Chl. b

Result and Discussion

The table below presents the impact of varying Pb concentrations on the morphological parameters of tomato plants at distinctive growth stages: 0, 18, 36, and 54 days after sowing (DAS). Pb concentrations in the soil were set at 50 mg/kg (low), 70 mg/kg (medium), and 90 mg/kg (high). The morphological parameters measured included plant height, shoot length, number of leaves, leaf area, and root biomass.

Table 1: Effect of Pb concentrations on morphological parameters of plants at 0, 18, 36, and 54 DAS.

The table shows a concentration dependent impact of lead (Pb) contamination on the development of tomato plants. At lower Pb concentration 50 mg/kg soil, plants exhibited irregular development characterized by critical increment in height, plants shoot length, number of branches, number of leaves, number of fruits, leaf area index, relative growth rate, and chlorophyll content compared to plants developed in control (Pb free) soil. This stimulatory impact at low Pb levels could be credited to a hormetic reaction, where a low measurements of Pb heavy metals induces beneficial impact on plant growth.

However as the Pb concentration expanded to intermediate (70 mg/kg) and high level (90 mg/kg), a articulated decay in all development parameters was watched. The decrease in plant height, shoot length, number of leaves, number of branches and number of fruits at these concentration show the inhibitory impacts of Pb toxicity, which is consist with its known impact on cellular processes such that photosynthesis, nutrient take-up, and enzyme activities.

Interestingly, at 18 days after sowing (DAS), plant in 50 mg/ kg treatment continued to exhibit enhanced growth compared to the control, while those in 70 and 90 mg/kg treatment showed significant growth retardation. However, at later development stages, even the plants in the 50 mg/kg treatment started to exhibit negative growth reactions, with reduce development parameters and productivity compared to control plants. This suggest that the initial positive impact of low Pb concentrations was transient and that prolonged exposure to Pb, even at low levels, ultimately has deleterious impacts on tomato plants growth.

Table 2: Effect of Pb concentrations on physiological parameters of plants at 0, 18, 36, and 54 DAS.

The observed decrease in growth parameters at higher Pb concentrations might be attributed to Pb- initiated disturbance in nutrient acquisition and oxidative stress in plants. Lead is known to interfere with the uptake and translocation of fundamental nutrients, leading to nutrients deficiencies and disabled metabolic functions. In addition, Pb aggregation in plant tissues can produce reactive oxygen species (ROS), causing oxidative disruption of cellular function, which likely to decline in growth matrices observed in this study.

Diminish in chlorophyll content with increasing Pb concentrations is a well documented phenomenon attributed to the disruption of chlorophyll biosynthesis and photosynthesis proficiency. Lead interferes with key enzymes, such as δ-aminolevulinic acid dehydratase, included in chlorophyll production, and disturbs the uptake of fundamental elements like magnesium and press, basic for chlorophyll arrangement (Sharma and Dubey, 2005).⁴¹ At lower concentrations (50 mg/kg), Pb might stimulate a hermetic reaction, temporarily enhancing physiological activities, including chlorophyll synthesis. However, at higher concentration (70 and 90 mg/kg), Pb toxicity generates oxidative stress, leading to chlorophyll degradation and damage to the photosynthetic device.⁴²

Similarly, the decrease in LAI with expanding Pb concentrations is connected to reduced leaf expansion and senescence due to the inhibitory impacts of Pb on cell division and turgor maintenance. Higher Pb levels impede water and nutrient uptake, which directly impacts leaf development and area, further reducing the plant’s photosynthetic efficiency (Gopal & Rizvi, 2008).⁴³

Table 3: Chemical analysis of heavy metals in parts of tomato plants by Atomic Absorption Spectroscopy.

 Study indicate that the lead (Pb) aggregation in plants increments with higher soil Pb concentrations, predominantly localizing in roots, followed by stem, leaves, and negligibly in natural products. This dispersion recommends restricted translocation of Pb of roots to airborne parts. Pb uptake occurs through root absorption, where it binds to cell wall components, limiting its development tp shoots and clears out. Lifted Pb levels can disturb water adjust, supplement take-up, and chemical exercises, driving to oxidative stretch and disabled plant development.⁴⁴ Among plants parts, the accumulation followed the trend: root>stem>leaf>fruit. According to this research showing that Pb accumulated mostly in roots because of its poor mobility throughout plants, this pattern emphasizes the limited transfer of Pb from root to aerial regions.⁴⁵ Roots act as the essential site of Pb aggregation because Pb strongly ties to cell wall components and is sequestered in vacuoles, limiting its translocation by means of the xylem. The relatively lower aggregation of lead (Pb) in stems and leaves suggests the activation of defense mechanism, such as chelation and compartmentalization, which help mitigate Pb toxicity in aerial parts.⁴⁶ However, even trace amounts of Pb in fruits are concerning due to the potential risks to human health, as Pb is a non-essential and highly harmful element. Elevated Pb levels in plant tissues disturb physiological processes, including nutrient uptake, photosynthesis, and oxidative stress management, contributing to in general development restraint.⁴⁷

Conclusion
In this study, we highlight the concentration – dependent impacts of lead (Pb) contamination on the growth and development of tomato plants at different time intervals. At lower concentrations (50 mg/kg), Pb shown a hormetic impacts, briefly enhancing the growth parameters such as plant height, plant’s shoot length, numbers of branches, number of leaves, number of fruit, leaf area index, relative growth rate, and chlorophyll content compared to control plants. In any case as the concentration of lead increased (70and 90 mg/kg), these growth parameters were altogether diminished, demonstrating the poisonous impacts of Pb on plants physiological and morphological capacities. Lead harmfulness postures significant challenges to plant development, affecting physiological, biochemical, and morphological traits. However, plants exhibit various resistance and detoxification mechanisms.

The finding emphasize the dual role of Pb as potential development stimulant at trace levels and severe phytotoxic agent at higher concentrations or with the prolonged exposure. These result emphasize the require for careful monitoring of Pb defilement in rural soil to moderate its unfavorable impacts on edit efficiency and guarantee nourishment security.

Acknowledgment

The authors are grateful to their supervisor, and Ewing Christian College, Prayagraj (University of Allahabad), for their invaluable support throughout the course of this research. Special thanks are extended to the college for providing laboratory space for cultivation of tomato plants in clay pots and access to essential instrumentation, including UV- Visible spectroscopy, which significantly contribute to the success of this study.

Funding Sources

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Conflict of Interest

The author(s) do not have any conflict of interest.

Data Availability Statement

This statement does not apply to this article.

References

1. Eichler, A., Gramlich, G., Kellerhals, T., Tobler, L., & Schwikowski, M.. Pb pollution from leaded gasoline in South America in the context of a 2000-year metallurgical history. Science Advances, 1(2), (2015), https://doi.org/10.1126/sciadv.1400196
   CrossRef
2. Rehman, A. U., Nazir, S., Irshad, R., Tahir, K., Rehman, K. U., Islam, R. U., & Wahab, Z.. Toxicity of heavy metals in plants and animals and their uptake by magnetic iron oxide nanoparticles. Journal of Molecular Liquids, (2021), 321, 114455.
   CrossRef
3. Ajsuvakova, O. P., Tinkov, A. A., Aschner, M., Rocha, J. B., Michalke, B., Skalnaya, M. G., … & Bjørklund, G.. Sulfhydryl groups as targets of mercury toxicity. Coordination Chemistry Reviews, (2020), 417, 213343.
   CrossRef
4. Van Straaten, P.. Human exposure to mercury due to small scale gold mining in northern Tanzania. Science of the Total Environment, (2000), 259(1–3), 45–53. https://doi.org/10.1016/S0048-9697(00)00548-9
   CrossRef
5. Botta, C., Iarmarcovai, G., Chaspoul, F., Sari-Minodier, I., Pompili, J., Orsière, T., … & De Méo, M.. Assessment of occupational exposure to welding fumes by inductively coupled plasma-mass spectroscopy and by the alkaline Comet assay. Environmental and Molecular Mutagenesis, (2006), 47(4), 284–295. https://doi.org/10.1002/em.20205
   CrossRef
6. Khan, A., Khan, S., Khan, M. A., Qamar, Z., & Waqas, M.. The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environmental Science and Pollution Research, (2015), 22(18), 13772–13799. https://doi.org/10.1007/s11356-015-4881-0
   CrossRef
7. Xiang, M., et al.. Heavy metal contamination risk assessment and correlation analysis of heavy metal contents in soil and crops. Environmental Pollution, (2021), 278(11), 6911. https://doi.org/10.1016/j.envpol.2021.116911
   CrossRef
8. Sharma, P., & Dubey, R. S.. Lead toxicity in plants. Brazilian Journal of Plant Physiology, (2005), 17(1), 35–52.
   CrossRef
9. Shahid, M., Pinelli, E., Pourrut, B., Silvestre, J., & Dumat, C.. Lead-induced genotoxicity to Vicia faba roots in relation with metal cell uptake and initial speciation. Ecotoxicology and Environmental Safety, (2011), 74, 78–84.
   CrossRef
10. Kumar, A., Prasad, M. N. V., & Sytar, O.. Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere, (2012), 89, 1056–1065.
    CrossRef
11. Sharma, P., & Dubey, R. S. . Lead toxicity in plants. Brazilian Journal of Plant Physiology, (2005), 17(1), 35–52.
    CrossRef
12. Sharma, P., & Dubey, R. S.. Lead toxicity in plants. Brazilian Journal of Plant Physiology, (2005), 17(1), 35–52.
    CrossRef
13. Kacalkova, L., Tlustos, P., & Szakova, J.. Phytoextraction of risk elements by willow and poplar trees. International Journal of Phytoremediation, (2015), 17, 414–421.
    CrossRef
14. PP, S., & Puthur, J. T.. Heavy metal phytoremediation by bioenergy plants and associated tolerance mechanisms. Soil and Sediment Contamination, (2021), 30(3), 253–274.
    CrossRef
15. Yedjou, C. G., Tchounwou, C. K., Haile, S., Edwards, F., & Tchounwou, P. B.. N-acetylcysteine protects against DNA damage associated with lead toxicity in HepG2 cells. Ethnicity & Disease, (2010), 20(1 Suppl 1), S1.
16. Maucieri, C., Nicoletto, C., Van Os, E., Anseeuw, D., Van Havermaet, R., & Junge, R.. Hydroponic technologies. Aquaponics Food Production Systems, (2019), 10, 978–3.
    CrossRef
17. Piscitelli, C., Lavorgna, M., De Prisco, R., Coppola, E., Grilli, E., Russo, C., & Isidori, M.. Tomato plants (Solanum lycopersicum) grown in experimental contaminated soil: Bioconcentration of potentially toxic elements and free radical scavenging evaluation. PLOS ONE, (2020), 15(8), e0237031. https://doi.org/10.1371/journal.pone.0237031
    CrossRef
18. Gupta, D. K., Nicoloso, F. T., Schetinger, M. R. C., Rossato, L. V., Pereira, L. B., Castro, G. Y., … & Tripathi, R. D.. Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. Journal of Hazardous Materials, (2009) 172, 479–484. https://doi.org/10.1016/j.jhazmat.2009.06.141
    CrossRef
19. Hadi, F., & Aziz, T.. A mini review on lead (Pb) toxicity in plants. Journal of Biology and Life Sciences, (2015), 6, 91–101.
    CrossRef
20. Maodzeka, A., Hussain, N., Wei, L., Zvobgo, G., Mapodzeke, J. M., Adil, M. F., … & Shamsi, I. H.. Elucidating the physiological and biochemical responses of different tobacco (Nicotiana tabacum) genotypes to lead toxicity. Environmental Toxicology and Chemistry, (2016), 36, 175–181. https://doi.org/10.1002/etc.3522
    CrossRef
21. Tupan, C. I., & Azrianingsih, R.. Accumulation and deposition of lead heavy metal in the tissues of roots, rhizomes and leaves of seagrass Thalassia hemprichii. Aquaculture, Aquarium, Conservation & Legislation, (2016), 9.
22. Shahid, M., Dumat, C., Pourrut, B., Silvestre, J., Laplanche, C., & Pinelli, E.. Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba Journal of Soils and Sediments, (2014), 14, 835–843. https://doi.org/10.1007/s11368-013-0724-0
    CrossRef
23. Shah, K., Kumar, R. G., Verma, S., & Dubey, R. S.. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Science, (2001), 161, 1135–1144. https://doi.org/10.1016/s0168-9452(01)00517-9
    CrossRef
24. Mittler, R.. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, (2002), 7, 405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
    CrossRef
25. Sharma, P., & Dubey, R. S.. Lead toxicity in plants. Brazilian Journal of Plant Physiology, (2005), 17(1), 35–52.
    CrossRef
26. Srivastava, S., & Dubey, R. S.. Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regulation, (2011), 64, 1–16. https://doi.org/10.1007/s10725-010-9526-1
    CrossRef
27. Asati, A., Pichhode, M., & Nikhil, K.. Effect of heavy metals on plants: an overview. International Journal of Application or Innovation in Engineering & Management, (2016) 5(3), 56-66.
28. Jabeen, F., Farid, M., Malik, R. N., & Li, J.. Heavy metals in the soil-plant system. Environmental Pollution, (2018), 243, 195–207. https://doi.org/10.1016/j.envpol.2018.08.021
    CrossRef
29. Akinola, M. O., Olayanju, T. M. A., Ajayi, A. R., & Omoike, A.. Impact of heavy metal contamination in vegetables and fruits. Environmental Monitoring and Assessment, (2020), 192(9), 585. https://doi.org/10.1007/s10661-020-08185-1
30. Khan, S., Rehman, M. S. U., Imran, M., & Shah, Z.. The impact of heavy metals on the growth and metabolism of tomato plants. Environmental Science and Pollution Research, (2019), 26, 23253–23263. https://doi.org/10.1007/s11356-019-05348-9
31. Jayarathne, A., Egodawatta, P., Ayoko, G. A., & Goonetilleke, A.. Assessment of ecological and human health risks of metals in urban road dust based on geochemical fractionation and potential bioavailability. Science of The Total Environment, (2018), 635, 1609–1619.
    CrossRef
32. Cunha, A. R. D., Ambrósio, A. D. S., Wolowski, M., Westin, T. B., Govêa, K. P., Carvalho, M., … & Barbosa, S.. Negative effects on photosynthesis and chloroplast pigments exposed to lead and aluminum: A meta-analysis. Cerne, (2020), 26(2), 232–237.
    CrossRef
33. Asati, A., Pichhode, M., & Nikhil, K.. Effect of heavy metals on plants: an overview. International Journal of Application or Innovation in Engineering & Management, (2016), 5(3), 56-66.
34. Piscitelli, C., Lavorgna, M., De Prisco, R., Coppola, E., Grilli, E., Russo, C., & Isidori, M.. Tomato plants (Solanum lycopersicum) grown in experimental contaminated soil: Bioconcentration of potentially toxic elements and free radical scavenging evaluation. PLOS ONE, (2020), 15(8), e0237031. https://doi.org/10.1371/journal.pone.0237031
    CrossRef
35. Ganiyu, S. A., Popoola, A. R., Imonmion, J. E., Uzoemeka, I. P., & Ojo, K. O.. Effect of three sterilizing agents on seed viability, seedling vigor and occurrence of seed-borne bacterial pathogens of two tomato cultivar. Nigerian Journal of Plant Protection, (2021), 35(1), 32–38.
36. Ashfaque, F., & Inam, A.. Accumulation of metals, antioxidant activity, growth and yield attributes of mustard (Brassica juncea) grown on soil amendments with fly ash together with inorganic nitrogen fertilizer. Acta Physiologiae Plantarum, (2020), 42, 1–13.
    CrossRef
37. Magistri, F., Chebrolu, N., Behley, J., & Stachniss, C.. Towards in-field phenotyping exploiting differentiable rendering with self-consistency loss. In 2021 IEEE International Conference on Robotics and Automation (ICRA) (2021, May), (pp. 13960–13966). IEEE.
    CrossRef
38. Latifah, E., Krismawati, A., Saeri, M., Arifin, Z., Warsiati, B., Setyorini, D., … & Maghfoer, M. D.. Analysis of plant growth and yield in varieties of tomato (Solanum lycopersicum) grafted onto different eggplant rootstocks. International Journal of Agronomy, (2021), 6630382.
    CrossRef
39. Li, C., Adhikari, R., Yao, Y., Miller, A. G., Kalbaugh, K., Li, D., & Nemali, K.. Measuring plant growth characteristics using smartphone-based image analysis technique in controlled environment agriculture. Computers and Electronics in Agriculture, (2020) 168, 105123.
    CrossRef
40. Ašimović, Z., Čengić, L., Hodžić, J., & Murtić, S.. Spectrophotometric determination of total chlorophyll content in fresh vegetables. LXI Broj, (2016) 66, 104–108.
41. Sharma, P., & Dubey, R. S.. Lead toxicity in plants. Brazilian Journal of Plant Physiology, (2005), 17(1), 35–52.
    CrossRef
42. Gopal, R., & Rizvi, A. H.. Excess lead alters growth, metabolism, and translocation of certain nutrients in radish. Chemosphere, (2008), 70(9), 1539–1544. https://doi.org/10.1016/j.chemosphere. 2007.08.046
    CrossRef
43. Ahmad, M. S. A., et al.. Lead (Pb)-induced regulation of growth, photosynthesis, and mineral nutrition in maize (Zea mays L.) plants at early growth stages. Biological Trace Element Research, (2011), 144, 1229–1239.
    CrossRef
44. Kumar, A., & Prasad, M. N. V.. Plant-lead interactions: transport, toxicity, tolerance, and detoxification mechanisms. Ecotoxicology and Environmental Safety, (2018) 166, 401–418.
    CrossRef
45. Pourrut, B., Shahid, M., Dumat, C., Winterton, P., & Pinelli, E.. Lead uptake, toxicity, and detoxification in plants. Reviews of Environmental Contamination and Toxicology, (2011), 213, 113–136. https://doi.org/10.1007/978-1-4419-9860-6_4
    CrossRef
46. Sharma, P., & Dubey, R. S.. Lead toxicity in plants. Brazilian Journal of Plant Physiology, (2005), 17(1), 35–52.
    CrossRef
47. Zulfiqar, U., Farooq, M., Hussain, S., Maqsood, M., Hussain, M., Ishfaq, M., … & Anjum, M. Z.. Lead toxicity in plants: Impacts and remediation. Journal of Environmental Management, (2019), 250, 109557.
    CrossRef