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Article

Dopamine and 24-Epibrassinolide Upregulate Root Resilience, Mitigating Lead Stress on Leaf Tissue and Stomatal Performance in Tomato Plants

by
Lohana Ribeiro Prestes
1,
Madson Mateus Santos da Silva
1,
Sharon Graziela Alves da Silva
1,
Maria Andressa Fernandes Gonçalves
1,
Bruno Lemos Batista
2,
Ivan Becari Viana
3 and
Allan Klynger da Silva Lobato
1,*
1
Núcleo de Pesquisa Vegetal Básica e Aplicada, Universidade Federal Rural da Amazônia, Paragominas 68627-451, PA, Brazil
2
Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, Santo André 09280-560, SP, Brazil
3
Departamento de Ciências Biológicas, Universidade do Estado de Minas Gerais—Unidade Carangola, Carangola 36800-000, MG, Brazil
*
Author to whom correspondence should be addressed.
Agronomy 2025, 15(1), 239; https://doi.org/10.3390/agronomy15010239
Submission received: 27 October 2024 / Revised: 10 January 2025 / Accepted: 13 January 2025 / Published: 18 January 2025
(This article belongs to the Special Issue Regulatory Mechanism of Growth Regulators on Crop Growth and Development: 2nd Edition)
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Abstract

:
Soil contamination linked to anthropogenic activities has become a serious environmental problem on a global scale. It is caused by heavy metals, such as lead (Pb). Dopamine (DOP) is a biogenic amine that acts as a neurotransmitter. It is found in plant organs and induces tolerance against abiotic stresses, including contamination. 24-epibrassinolide (EBR) stimulates metabolism, positively impacting flowering and production. This research aimed to evaluate whether EBR and DOP, applied alone or combined, can mitigate the impacts caused by Pb on roots and leaves by measuring root and leaf structures and stomatal behavior. For roots, both plant growth regulators maximized the epidermis, with increases in treatments Pb2+ − DOP + EBR (45%), Pb2+ + DOP − EBR (24%), and Pb2+ + DOP + EBR (36%), when compared with equal treatment without Pb2+. To leaves, the tested molecules improved the leaf structures, significantly increasing palisade parenchyma and spongy parenchyma. Parallelly, stomatal performance was boosted after treatments with EBR and DOP, confirmed by increments in stomatal density. Our study proved that EBR and DOP, alone or combined, mitigated the damages to leaves and roots exposed to Pb stress, but better results were found when EBR was applied alone.

1. Introduction

The tomato crop (Solanum lycopersicum L.) has great potential for growth in the world market [1]. Generally, the focus is on fruit with a vibrant color and excellent flavor [2], nutritionally presenting vitamins, antioxidant substances, and fiber, including vitamins C, A, and K [3,4]. This plant is considered a model frequently used in research to develop plants tolerant to biotic and abiotic stresses [5,6,7].
Soil contamination linked to anthropogenic activities has become a serious environmental problem on a global scale [8]. Pollution in agricultural soils caused by heavy metals, such as lead (Pb), cadmium (Cd), mercury (Hg), arsenic (As), copper (Cu), and nickel (Ni) results in negative impacts on the soil and plants, reducing yield in arable areas [9]. Several industrial sectors use Pb in their production processes, including the mining, petroleum refinery, paint, pigment, metal coating, glass, ceramics manufacturing, and steel industries, as well as coal and energy plants as battery storage [10].
Pb contamination can harm human health [11] due to ingesting contaminated food or inhalation [12]. This heavy metal triggers harmful effects in plants, degrading pigments, inhibiting gas exchange, and promoting ionic imbalance, resulting in lower growth and biomass accumulation [13,14]. On the other hand, strategies based on the use of exogenous molecules using clean and safe technologies aimed at maximizing stress plant tolerance are efficient and cost-effective [15], including brassinosteroids (BRs) and neurotransmitters (NTs) [16,17].
Plants endogenously synthesize steroids, including BRs [18], with molecules detected in various organs and tissues [19,20]. The literature mentions the identification of more than 70 BRs that can be classified according to the number of carbons in the side chain [21]. Located at carbon number 17 of the main chain, 24-epibrassinolide (EBR) [22] is highlighted as the BR that is more biologically active, representative, and synthesized in plants [23]. EBR stimulates metabolism, including higher electron transport and carbon dioxide fixation, maximizes anatomical structures, and improves nutrient uptake, positively impacting flowering and production [24,25].
Dopamine (DOP) is classified as biogenic amines that act as a neurotransmitter belonging to the catecholamine group and is extensively present in plant organs [26]. These catecholamines were detected in various plant tissues, proving the biosynthesis of catecholamines in higher plants [27]. DOP is a water-soluble molecule containing carbon (C), nitrogen (N), and the chemical formula C8H11NO2 [28]. DOP roles in plants are intrinsically related to tolerance mechanisms to biotic and/or abiotic stresses, specifically, its modulatory function in physiological responses, the redox system, hormonal metabolism, and ionic homeostasis [29]. The exogenous application of DOP stimulates the antioxidant defense, increasing the tolerance of plants exposed to drought, salinity, and nutritional deficiency [30] because DOP alleviates oxidative stress due to higher activities of antioxidant enzymes [31].
The available literature does not contain research on the combined action of EBR and DOP in plants stressed by Pb, revealing a recent, modern, and unpublished approach using neurotransmitters and brassinosteroids. Our hypothesis also considers that EBR stimulates the growth and accumulation of biomass [32], while DOP reduces oxidative stress [33]. This research aimed to evaluate whether EBR and DOP, applied alone or combined, can mitigate the impacts caused by Pb on roots and leaves by measuring root and leaf structures and stomatal behavior.

2. Materials and Methods

2.1. Location and Growth Conditions

The experiment was performed at the Campus of Paragominas of the Universidade Federal Rural da Amazônia, Paragominas, Brazil (2°55′ S, 47°34′ W). The study was conducted in a greenhouse with controlled temperature and humidity. The minimum, maximum, and median temperatures were 23.6, 31.7, and 26.8 °C, respectively. The relative humidity during the experimental period varied between 60% and 80%.

2.2. Plants, Containers, and Acclimation

Seeds of Solanum lycopersicum L. cv Santa Clara were germinated using vegetable substrate and transplanted on the 15th day into 1.2 L pots filled with a mixed substrate of sand and vermiculite at a ratio of 3:1. Plants were cultivated under semi-hydroponic conditions containing 500 mL of nutritive solution. A nutritive solution was used as a source of nutrients [34]; the ionic strength started at 50% and was modified to 100% after two days.

2.3. Experimental Design

Experimental design had eight randomized treatments: control − DOP − EBR (1), control − DOP + EBR (2), control + DOP − EBR (3), control + DOP + EBR (4), Pb2+ − DOP − EBR (5), Pb2+ − DOP + EBR (6), Pb2+ + DOP − EBR (7), and Pb2+ + DOP + EBR (8). Five replicates for each one of the eight treatments were conducted and used in the experiment, a total of 40 experimental units, with one plant in each unit.

2.4. Dopamine (DOP) and 24-Epibrassinolide (EBR) Preparations and Applications

Dopamine (DOP) solution with 100 µM (Sigma-Aldrich, St. Louis, MO, USA) was prepared [35]. A 100 nM 24-epibrassinolide (EBR) (Sigma-Aldrich, USA) solution was used [36]. Fifteen-day-old plants were sprayed with single and combined applications of DOP and EBR at 7 d intervals until day 45. The concentrations of DOP and EBR were selected based on the research conducted by Pontes et al. [37] and Guedes et al. [32], respectively.

2.5. Plant Nutrition and Pb Treatment

The plants received the following macro and micronutrients [38]. To induce Pb stress, PbCl2 was used at concentrations of 0 and 200 µM Pb and was applied over 10 days (days 35–45 after the start of the experiment), being these concentrations chosen according to the literature [38]. During the study, the nutrient solutions were changed at 07:00 h at 3-day intervals, with the pH adjusted to 5.5 using HCl or NaOH. On day 45 of the experiment, physiological and morphological parameters were measured for all plants, and tissues were harvested for anatomical, biochemical, and nutritional analyses.

2.6. Pb Determination

Milled samples (100 mg) of leaf tissue were pre-digested in conical tubes (50 mL) with 2 mL of sub-boiled HNO3. Subsequently, 8 mL of a solution containing 4 mL of H2O2 (30% v/v) and 4 mL of ultra-pure water was added and transferred to a Teflon digestion vessel [39]. Determination of Pb was performed using an inductively coupled plasma mass spectrometer (model ICP-MS 7900; Agilent, Santa Clara, CA, USA).

2.7. Measurements of Anatomical Parameters

Samples were collected from the middle region of the leaf limbs of fully expanded leaves of the third node and roots 4 cm from the root apex. Subsequently, all collected botanical material was fixed in FAA 70 [40] for 24 h and dehydrated in ethanol for embedding in methacrylate resin (Leica Historesin, Nussloch/Heidelberg, Germany). Transverse sections with a thickness of 7 μm were obtained with a rotating microtome (model YD 315, American MasterTech Scientific, Lodi, CA, USA), stained with toluidine blue, pH 4.7 [41], and mounted onto slides with synthetic resin (Permount-Fischer, Waltham, MA, USA). For stomatal characterization, the epidermal impression method was used [42]. The slides were observed and photomicrographed under an optical microscope (Primostar 3, Zeiss, Oberkochen, Germany) coupled to a digital camera (Axiocam ERc 5s, Zeiss, Oberkochen, Germany). The images were analyzed with Image-Pro Plus previously calibrated with a micrometer slide from the manufacturer.

2.8. Data Analysis

The data were subjected to an analysis of variance, and significant differences between the means were determined using the Scott-Knott test at a probability level of 5% [43]. Standard deviations were calculated for each treatment.

3. Results

3.1. Dopamine and 24-Epibrassinolide Protect Root Against Lead Excess

Pb excess was confirmed (Figure 1), and significant decreases in Pb contents were detected in the leaves with isolated DOP (47%), EBR (70%), and both molecules (58%). Plants subjected to excess Pb2+ had damages to anatomical structures of root tissue (Table 1 and Figure 2). However, the application of 100 µM DOP in plants exposed to excess Pb promoted significant increases in values of the RET (24%), RDT (16%), RCT (21%), VCD (10%), and RMD (5%), compared to plants with excess Pb and without treatment with DOP and EBR. Similarly, the use of 100 nM EBR in treatments under Pb excess resulted in increases (p < 0.05) to the RET (45%), RDT (38%), RCT (34%), VCD (36%), and RMD (23%). Additionally, the combination of DOP and EBR maximized the RET, RDT, RCT, VCD, and RMD by 36%, 28%, 29%, 25%, and 14%, respectively, concerning equal treatment with Pb excess and without DOP or EBR.

3.2. Growth Regulators Minimized the Harmful Effects Linked to Lead on Leaf Tissue

Pb excess caused deleterious effects on leaf anatomy (Table 2 and Figure 3). The application of DOP promoted increases (p < 0.05) of 16%, 21%, 10%, and 12% in the ETAd, ETAb, PPT, and SPT, respectively, and a reduction in the PPT/SPT (2%), when compared to treatment with Pb without DOP. Spraying EBR on tomato plants under Pb2+ excess mitigated the damages, maximizing the variables ETAd, ETAb, PPT, and SPT by 46%, 41%, 21%, and 42%, respectively, and a decrease in the PPT/SPT (14%), compared to treatment with Pb and without EBR. For the leaf cross-section, plants exposed to excess Pb2+ presented mesophyll with a compact arrangement. Additionally, the combined application of DOP and EBR induced increases of 23%, 35%, 15%, and 25% in the ETAd, ETAb, PPT, and SPT, respectively, with a decrease in the PPT/SPT (8%) in comparison with plants exposed to Pb2+ without the DOP and EBR.

3.3. Dopamine and 24-Epibrassinolide Positively Regulated Stomatal Characteristics in Lead-Stressed Plants

Stomatal characteristics were affected by Pb excess (Table 3 and Figure 3). On the adaxial face, plants exposed to Pb2+ stress and pretreated with DOP had significant increases of 31%, 3%, and 16% in the SD, SF, and SI, respectively, but also showed decreases in the PDS and EDS of 11% and 14%, in this order, comparing with plants under Pb2+ and without the use of neurotransmitters or brassinosteroids. Plants under Pb2+ toxicity and treated with EBR had significant increases in the SD (68%), SF (8%), and SI (40%) and decreases in the PDS (24%) and EDS (30%). The simultaneous use of DOP and EBR promoted substantial increases (p < 0.05) of 41%, 7%, and 29% in the SD, SF, and SI, in this order, when compared to treatment with plants exposed to Pb without pre-treatment with DOP or EBR. On the abaxial face, plants exposed to Pb and DOP (pre-treatment) had increases (p < 0.05) in the SD (54%) and SI (29%); however, there were reductions in the PDS (3%) and EDS (5%). Additionally, EBR provoked increases in the SD (76%), SF (4%), and SI (45%) and a reduction in the PDS (14%) and EDS (18%) when in a combined application (DOP and EBR) in plants under Pb excess; the SD, SF, and SI had maximizations of 66%, 3%, and 35%, respectively, and reductions in the PDS (7%) and EDS (9%) when compared to treatment with Pb2+ excess and without DOP or EBR.

4. Discussion

Growth regulators (DOP and EBR) reduced the adverse effects of Pb2+ on the RET, RDT, RCT, VCD, and RMD. The cumulative effects using DOP and EBR indicate that these molecules had a positive interaction and stimulated the tissue barrier linked to the root defense against the excess of this toxic metal, clearly evidenced after pretreatment with DOP and EBR, maximizing the RET. The epidermis is a tissue responsible for protecting the root because it makes intense contact with the environment and it induces interactions with the substrate [44]. Our data corroborate the study examining the toxic effects of Cd and Cr on the morphoanatomical characteristics of wheat, detecting reductions in the thickness of the root epidermis [45].
This research revealed increases in the VCD and RMD caused by the application of DOP, suggesting that this neurotransmitter promoted increases in anatomical structures [17,31], being intrinsically related to higher rates of cell divisions in vascular tissues and improving the absorption and ion influx through the symplastic pathways in the VCD and RMD [46,47]. However, the heavy metal studied reduced these structures, impairing the cell selectivity and differentiation in the metaxylem, which is responsible for transporting water and nutrients. In the literature, research demonstrates that DOP can interact with growth regulators, including auxin and ethylene, boosting root growth, and mitigating the negative impacts caused by heavy metals [26].
EBR caused an increase in the RDT, indicating that this growth regulator caused changes in the ionic selection that interact with the meristematic tissue, aiming to mitigate the transport of Pb2+ ions and improve tolerance to the heavy metal [48]. Similar increases occur in the RCD and RCT, associated with organ elongation. However, Pb caused reductions in these structures. Root formation depends on the anatomical architecture’s quality, which is essential for the absorption of water and ions during plant growth and development [49].
DOP application in plants under Pb excess maximized the epidermis, suggesting that the neurotransmitter improved leaf protection and epidermis functionality. The epidermis is a structure composed by a cell wall and often develops mechanical support and protective functions in leaf tissue, also contributing to essential processes, including transpiration and thermoregulation. ETAd and ETAb are structures with a protective function that can contribute to thermoregulation and gas exchange. A study with tomato plants revealed that the epidermis was modified by Pb intoxication, causing excessive water loss through transpiration [38]. A research evaluating Pb excess in leaves revealed that this heavy metal causes deleterious effects on leaf anatomy when compared to the control treatment [50].
Treatment with EBR alleviated the harmful effects caused by Pb2+ on leaf anatomy, making it possible to detect higher benefits of this treatment. Research suggests that increases in SPT can improve CO2 diffusion through intercellular spaces [51]. The increases in the PPT and SPT in plants pretreated with DOP and EBR exposed to excess Pb indicate that the mesophyll became thicker (PPT + SPT), suggesting better gas transport and radiation absorption capacity. PPT and SPT are structures responsible for transporting O2 and CO2, being gases necessary for photosynthesis and respiration [52].
The combined application of DOP and EBR positively regulated stomatal characteristics in plants under Pb excess. Stomata are specialized epidermal structures that regulate gas exchange between plants and the environment [53]. The opening in the epidermis is called the ostiole, communicating the mesophyll with the outside [54]. DOP is a neurotransmitter in the plant and animal kingdoms [55] and has recently been used to induce plant tolerance to stress situations [56]. Studies by [57] reveal that the exogenous application of DOP in apple plants under saline stress (100 mM) can improve SF, increasing stomatal opening and mitigating the deleterious effects on growth.
In this research, there were reductions in PDS and EDS (adaxial and abaxial sides) in plants under pre-treatment with DOP and excess Pb2+. PDS and EDS are relevant variables that reflect the stoma’s size and can vary depending on environmental conditions and plant characteristics. The stomatal complex may present variations according to polar and equatorial measurements in which more elliptical stomata are more efficient during the gas exchange [58]. Therefore, the decrease in PDS and EDS values contributes to the increase in SD, confirmed in this research after DOP treatment, suggesting that stomata are more elliptical.
Plants sprayed with EBR suffered less deleterious effects linked to Pb2+, improving the stomatal performance of tomato plants and, more specifically, increasing the SD, SF, and SI (on both leaf surfaces). The SD is a relevant indicator with a strong relationship with gas exchange [59]: a frequently high number of stomata per unit area on the leaf surfaces facilitates stomatal conductance, amplifying intercellular spaces and favoring the CO2 absorption during the photosynthetic process. Another aspect considered is SF, which is extremely important because stomata regulate gas exchange. Increase in the SF favors PN, as the stomata absorb CO2 and diffuse O2 and H2O [60]. Research with tomato plants under the exogenous application of EBR provided several benefits, including higher membrane integrity, relative water content, and increased biomass [61].

5. Conclusions

Our study proved that EBR and DOP, alone or combined, mitigated the damages to leaves and roots exposed to Pb stress, but better results were found when EBR was applied alone. For roots, both plant growth regulators maximized the epidermis, indicating higher root protection. For leaves, the molecules tested improved the leaf structures, significantly increasing palisade parenchyma and spongy parenchyma. Parallelly, the stomatal performance was boosted after treatments with EBR and DOP, confirmed by increments in the stomatal density and suggesting benefits on gas exchange in plants under Pb excess.

Author Contributions

A.K.d.S.L. advised this project, planned all phases of the research, and critically revised the manuscript. L.R.P., M.M.S.d.S., S.G.A.d.S. and M.A.F.G. conducted the experiment and wrote and edited the manuscript. I.B.V. performed anatomical determinations. B.L.B. carried out the nutritional determinations. All authors have read and agreed to the published version of the manuscript.

Funding

This research had financial support from Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA/Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil), and Universidade Federal Rural da Amazônia (UFRA/Brazil) to A.K.S.L. L.R.P., M.M.S.S., and S.G.A.S. were supported with scholarships from Programa de Educação Tutorial (PET/Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil), and Universidade Federal Rural da Amazônia (UFRA/Brazil), respectively.

Data Availability Statement

Data are available upon request to the corresponding author.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Agronomy 15 00239 g001
Figure 1. Pb content in tomato plants treated with single and combined DOP and EBR exposed to Pb excess. Columns with different letters indicate significant differences from the Scott-Knott test (p < 0.05). Columns corresponding to means from five repetitions and standard deviations.
Figure 1. Pb content in tomato plants treated with single and combined DOP and EBR exposed to Pb excess. Columns with different letters indicate significant differences from the Scott-Knott test (p < 0.05). Columns corresponding to means from five repetitions and standard deviations.
Agronomy 15 00239 g001
Agronomy 15 00239 g002
Figure 2. Root cross-sections in tomato plants treated with single and combined DOP and EBR exposed to Pb excess. –Pb2+ − DOP − EBR (a), –Pb2+ − DOP + EBR (b), –Pb2+ + DOP − EBR (c), –Pb2+ + DOP + EBR (d), +Pb2+ − DOP − EBR (e), +Pb2+ − DOP + EBR (f), +Pb2+ + DOP − EBR (g), and +Pb2+ + DOP + EBR (h). Legends: RE = root epidermis; RC = root cortex; RD = root endodermis; VC = vascular cylinder; RM = root metaxylem. Black bars = 50 µm.
Figure 2. Root cross-sections in tomato plants treated with single and combined DOP and EBR exposed to Pb excess. –Pb2+ − DOP − EBR (a), –Pb2+ − DOP + EBR (b), –Pb2+ + DOP − EBR (c), –Pb2+ + DOP + EBR (d), +Pb2+ − DOP − EBR (e), +Pb2+ − DOP + EBR (f), +Pb2+ + DOP − EBR (g), and +Pb2+ + DOP + EBR (h). Legends: RE = root epidermis; RC = root cortex; RD = root endodermis; VC = vascular cylinder; RM = root metaxylem. Black bars = 50 µm.
Agronomy 15 00239 g002
Agronomy 15 00239 g003
Figure 3. Leaf cross-sections in tomato plants treated with single and combined DOP and EBR exposed to Pb excess. –Pb2+ − DOP − EBR (a), –Pb2+ − DOP + EBR (b), –Pb2+ + DOP − EBR (c), –Pb2+ + DOP + EBR (d), +Pb2+ − DOP − EBR (e), +Pb2+ − DOP + EBR (f), +Pb2+ + DOP − EBR (g), and +Pb2+ + DOP + EBR (h). Legends: EAd = adaxial epidermis; EAb = abaxial epidermis; PP = palisade parenchyma; SP = spongy parenchyma. Black bars = 10 µm.
Figure 3. Leaf cross-sections in tomato plants treated with single and combined DOP and EBR exposed to Pb excess. –Pb2+ − DOP − EBR (a), –Pb2+ − DOP + EBR (b), –Pb2+ + DOP − EBR (c), –Pb2+ + DOP + EBR (d), +Pb2+ − DOP − EBR (e), +Pb2+ − DOP + EBR (f), +Pb2+ + DOP − EBR (g), and +Pb2+ + DOP + EBR (h). Legends: EAd = adaxial epidermis; EAb = abaxial epidermis; PP = palisade parenchyma; SP = spongy parenchyma. Black bars = 10 µm.
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Table 1. Root anatomy in tomato plants treated with single and combined DOP and EBR exposed to Pb excess.
Table 1. Root anatomy in tomato plants treated with single and combined DOP and EBR exposed to Pb excess.
Pb2+DOPEBRRET (µm)RDT (µm)RCT (µm)VCD (µm)RMD (µm)
−−−9.81 ± 0.48 e9.69 ± 0.12 c103.41 ± 5.14 e88.37 ± 2.71 d45.73 ± 2.03 d
−−+13.19 ± 0.64 a12.11 ± 0.54 a135.86 ± 5.62 a114.35 ± 3.98 a68.02 ± 2.57 a
−+−11.39 ± 0.23 c10.59 ± 0.29 b116.01 ± 2.74 c96.46 ± 1.83 c55.09 ± 2.58 c
−++12.44 ± 0.31 b11.74 ± 0.28 a127.23 ± 1.08 b105.61 ± 2.99 b60.33 ± 3.78 b
+−−7.12 ± 0.43 g7.70 ± 0.37 e91.20 ± 5.51 f69.53 ± 1.57 f32.60 ± 1.65 g
+−+10.30 ± 0.12 d10.62 ± 0.37 b122.64 ± 6.85 c94.69 ± 3.79 c39.96 ± 1.51 e
++−8.80 ± 0.31 f8.93 ± 0.32 d110.78 ± 5.54 d76.31 ± 3.91 e34.13 ± 1.15 g
+++9.69 ± 0.42 e9.83 ± 0.48 c117.74 ± 6.75 c86.69 ± 1.63 d37.01 ± 1.10 f
RET = root epidermis thickness; RDT = root endodermis thickness; RCT = root cortex thickness; VCD = vascular cylinder diameter; RMD = root metaxylem diameter. Columns with different letters indicate significant differences from the Scott-Knott test (p < 0.05). Values correspond to means from five repetitions and standard deviations.
Table 2. Leaf anatomy in tomato plants treated with single and combined DOP and EBR exposed to Pb excess.
Table 2. Leaf anatomy in tomato plants treated with single and combined DOP and EBR exposed to Pb excess.
Pb2+DOPEBRETAd (µm)ETAb (µm)PPT (µm)SPT (µm)Ratio PPT/SPT
−−−5.06 ± 0.41 c4.71 ± 0.30 d23.71 ± 0.19 c29.39 ± 1.84 c0.80 ± 0.05 c
−−+6.40 ± 0.24 a6.64 ± 0.29 a25.79 ± 0.68 a35.97 ± 2.94 a0.72 ± 0.04 c
−+−5.81 ± 0.43 b5.41 ± 0.34 c24.40 ± 0.92 b31.23 ± 1.33 c0.78 ± 0.04 c
−++5.97 ± 0.41 b5.81 ± 0.34 b24.66 ± 0.99 b32.94 ± 1.17 b0.75 ± 0.02 c
+−−3.48 ± 0.30 e3.55 ± 0.18 f19.12 ± 0.45 f20.79 ± 0.74 f0.92 ± 0.03 a
+−+5.06 ± 0.26 c5.01 ± 0.37 d23.19 ± 0.67 c29.48 ± 1.30 c0.78 ± 0.04 c
++−4.04 ± 0.19 d4.31 ± 0.20 e20.95 ± 0.52 e23.30 ± 1.29 e0.90 ± 0.06 a
+++4.27 ± 0.18 d4.79 ± 0.19 d22.02 ± 0.88 d26.03 ± 0.96 d0.84 ± 0.05 b
ETAd = epidermis thickness from adaxial leaf side; ETAb = epidermis thickness from abaxial leaf side; PPT = palisade parenchyma thickness; SPT = spongy parenchyma thickness. Columns with different letters indicate significant differences from the Scott-Knott test (p < 0.05). Values correspond to means from five repetitions and standard deviations.
Table 3. Stomatal characteristics in tomato plants treated with single and combined DOP and EBR exposed to Pb excess.
Table 3. Stomatal characteristics in tomato plants treated with single and combined DOP and EBR exposed to Pb excess.
Pb2+DOPEBRSD (Stomata per mm2)PDS (µm)EDS (µm)SFSI (%)
Adaxial face
−−−530 ± 35 d13.62 ± 0.47 d10.11 ± 0.19 d1.35 ± 0.04 a8.17 ± 0.45 d
−−+630 ± 34 a11.78 ± 0.52 f8.57 ± 0.22 f1.38 ± 0.08 a11.36 ± 0.80 a
−+−570 ± 31 c12.66 ± 0.24 e9.31 ± 0.50 e1.36 ± 0.09 a9.62 ± 0.65 c
−++603 ± 33 b11.90 ± 0.67 f8.73 ± 0.39 f1.37 ± 0.08 a10.30 ± 0.62 b
+––272 ± 15 h17.82 ± 0.57 a14.58 ± 0.23 a1.22 ± 0.03 b5.69 ± 0.33 g
+–+457 ± 31 e13.59 ± 0.92 d10.28 ± 0.33 d1.32 ± 0.09 a7.95 ± 0.41 d
++–357 ± 16 g15.79 ± 0.38 b12.49 ± 0.23 b1.26 ± 0.04 b6.60 ± 0.37 f
+++384 ± 27 f14.94 ± 0.69 c11.39 ± 0.42 c1.31 ± 0.06 a7.31 ± 0.27 e
Abaxial face
–−−783 ± 36 c13.56 ± 0.41 e11.37 ± 0.37 d1.19 ± 0.04 a9.31 ± 0.24 d
–−+880 ± 29 a12.17 ± 0.69 f9.91 ± 0.65 f1.23 ± 0.10 a12.39 ± 0.45 a
–+−817 ± 24 b12.66 ± 0.24 f10.52 ± 0.30 e1.20 ± 0.03 a10.20 ± 0.49 c
–++854 ± 39 a12.33 ± 0.54 f10.12 ± 0.63 f1.22 ± 0.08 a11.67 ± 0.48 b
+––365 ± 9 g16.38 ± 0.45 a14.08 ± 0.56 a1.16 ± 0.03 a6.30 ± 0.11 f
+–+643 ± 36 d14.04 ± 0.39 d11.62 ± 0.49 d1.21 ± 0.06 a9.11 ± 0.50 d
++–561 ± 32 f15.93 ± 0.62 b13.37 ± 0.32 b1.19 ± 0.02 a8.15 ± 0.53 e
+++605 ± 27 e15.30 ± 0.18 c12.78 ± 0.44 c1.20 ± 0.03 a8.50 ± 0.24 e
SD = stomatal density; PDS = polar diameter of the stomata; EDS = equatorial diameter of the stomata; SF = stomatal functionality; SI = stomatal index. Columns with different letters indicate significant differences from the Scott-Knott test (p < 0.05). Values correspond to means from five repetitions and standard deviations.
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Prestes, L.R.; Silva, M.M.S.d.; Silva, S.G.A.d.; Gonçalves, M.A.F.; Batista, B.L.; Viana, I.B.; Lobato, A.K.d.S. Dopamine and 24-Epibrassinolide Upregulate Root Resilience, Mitigating Lead Stress on Leaf Tissue and Stomatal Performance in Tomato Plants. Agronomy 2025, 15, 239. https://doi.org/10.3390/agronomy15010239

AMA Style

Prestes LR, Silva MMSd, Silva SGAd, Gonçalves MAF, Batista BL, Viana IB, Lobato AKdS. Dopamine and 24-Epibrassinolide Upregulate Root Resilience, Mitigating Lead Stress on Leaf Tissue and Stomatal Performance in Tomato Plants. Agronomy. 2025; 15(1):239. https://doi.org/10.3390/agronomy15010239

Chicago/Turabian Style

Prestes, Lohana Ribeiro, Madson Mateus Santos da Silva, Sharon Graziela Alves da Silva, Maria Andressa Fernandes Gonçalves, Bruno Lemos Batista, Ivan Becari Viana, and Allan Klynger da Silva Lobato. 2025. "Dopamine and 24-Epibrassinolide Upregulate Root Resilience, Mitigating Lead Stress on Leaf Tissue and Stomatal Performance in Tomato Plants" Agronomy 15, no. 1: 239. https://doi.org/10.3390/agronomy15010239

APA Style

Prestes, L. R., Silva, M. M. S. d., Silva, S. G. A. d., Gonçalves, M. A. F., Batista, B. L., Viana, I. B., & Lobato, A. K. d. S. (2025). Dopamine and 24-Epibrassinolide Upregulate Root Resilience, Mitigating Lead Stress on Leaf Tissue and Stomatal Performance in Tomato Plants. Agronomy, 15(1), 239. https://doi.org/10.3390/agronomy15010239

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