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Article

Foliar Methyl Jasmonate Application Activates Antioxidant Mechanisms to Counteract Water Deficits and Aluminum Stress in Vaccinium corymbosum L.

by
Cristina Cáceres
1,
Crystal Cazor-Curilef
2,
Patricio Delgado-Santibañez
2,
Mariana Machado
3,
Mabel Delgado
4,
Alejandra Ribera-Fonseca
4,5,
Claudio Inostroza-Blancheteau
6,7,
Leon A. Bravo
4,8,
Jorge González-Villagra
6,7,
Adriano Nunes-Nesi
3 and
Marjorie Reyes-Díaz
4,9,*
1
Programa de Doctorado en Ciencias de Recursos Naturales, Universidad de La Frontera, Temuco P.O. Box 54-D, Chile
2
Carrera de Bioquímica, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco P.O. Box 54-D, Chile
3
National Institute of Science and Technology on Plant Physiology under Stress Conditions, Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa 36570-900, MG, Brazil
4
Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN-UFRO), Universidad de La Frontera, Temuco P.O. Box 54-D, Chile
5
Centro de Fruticultura, Facultad de Ciencias Agropecuarias y Medioambiente, Campus Andrés Bello, Universidad de La Frontera, Temuco P.O. Box 54-D, Chile
6
Núcleo de Investigación en Producción Alimentaria, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco P.O. Box 15-D, Chile
7
Laboratorio de Fisiología y Biotecnología Vegetal, Departamento de Ciencias Agropecuarias y Acuícolas, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco P.O. Box 15-D, Chile
8
Laboratorio de Fisiología y Biología Molecular Vegetal, Departamento de Ciencias Agronómicas y Recursos Naturales, Facultad de Ciencias Agropecuarias y Medioambiente, Universidad de La Frontera, Temuco P.O. Box 54-D, Chile
9
Laboratorio de Ecofisiología Molecular y Funcional de Plantas, Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco P.O. Box 54-D, Chile
*
Author to whom correspondence should be addressed.
Horticulturae 2024, 10(11), 1172; https://doi.org/10.3390/horticulturae10111172
Submission received: 30 September 2024 / Revised: 31 October 2024 / Accepted: 2 November 2024 / Published: 6 November 2024
(This article belongs to the Special Issue Effects of Biostimulants on the Growth and Development of Horticultural Crops)
Browse Figures
Versions Notes

Abstract

:
Due to climate change, water deficits (WDs) and aluminum (Al) toxicity are increasing, affecting plants, especially crops such as blueberries (Vaccinium corymbosum L.). The application of methyl jasmonate (MeJA) could mitigate these effects. This work aimed to evaluate the effective MeJA dose to overcome oxidative stress provoked by combined WD+Al stress in blueberries. Plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars were exposed to control (Al at 65 mg/Kg, 80% field capacity), WD+Al (50% field capacity; Al at 1665 mg/Kg), and WD+Al treatment with different foliar MeJA doses (10, 50, and 100 μM) during 7 and 21 days. Data revealed that plants exposed to WD+Al and treated with 50 µM MeJA reduced Al up to 3.2-fold in roots and 2.7-fold in leaves and improved water potential (Ψw) up to 2.5-fold. The sensitive cultivar decreased the relative growth rate under WD+Al, increasing by 1.9-fold with 50 µM MeJA. Under WD+Al stress, all MeJA doses mitigated the decrease in relative water content in Al-resistant cultivars, restoring values like control plants. In the sensitive cultivar, 50 µM MeJA increased photosynthesis (1.5-fold) and stomatal conductance (1.4-fold), without changes in transpiration. Lipid peroxidation decreased (1.2-fold) and increased antioxidant activity (1.8-fold), total phenols (1.6-fold), and superoxide dismutase activity (3.3-fold) under WD+Al and 50 µM-MeJA. It was concluded that the most effective dose to alleviate the WD+Al stress was 50 µM MeJA due to the activation of antioxidants in blueberry plants. Therefore, the MeJA application could be a potential strategy for enhancing the resilience of V. corynbosum exposed to WD+Al stress.

1. Introduction

Acid soils occupy about 40% of the land surface and approximately 70% of potentially arable land [1,2]. Despite the remarkable amount of nutrients in these soils, they present significant restrictions for agricultural production due to the decrease in the availability of some nutrients and the increase in toxic elements such as aluminum (Al) [3,4]. The Al prevails in its phytotoxic ionic forms (Al+, Al2+, and Al3+), in acid soil, with Al3+ being the most abundant and detrimental to plants [3,4]. In addition, drought episodes have increased due to climate change, which has conditioned plants to water deficit (WD) stress, causing an overall reduction in total crop yield by 40–60% [5]. When drought episodes occur in acid soils, Al toxicity and WD stresses can overlap and strongly intervene in normal plant growth and development [6]. The interaction between WD and Al stress is more detrimental than the individual stresses, limiting crop yield and productivity to a greater extent [7,8,9,10]. For this reason, despite the few studies with combined stresses, there has been increasing interest in studying the sensitivity and resistance responses of various plant species.
Highbush blueberry (Vaccinium corymbosum L.) is a shrub from the Ericaceae family, originally from North America and introduced to Chile in the 1980s, which is currently experiencing stress due to both WD and Al stress [11]. Unlike other species of the genus Vaccinium, this species is highly sensitive to WD stress because of its shallow and extended root systems, which make its water conduction systems relatively inefficient [12,13]. V. corymbosum plants thrive in acid soils with a pH between 4.4 and 5.5, making them ideal for cultivation in Andisol soils. However, acid soils with high Al3+ availability significantly reduce crop yield and fruit quality [14,15]. Although the impacts of individual WD stress and Al3+ stress on V. corymbosum have been reported, no studies have been reported on the combined effects of these stresses on this species.
It has been reported that V. corymbosum plants subjected to WD decreased their relative water content (RWC), triggering stomatal closure and decreasing CO2 assimilation [11,16,17]. At the biochemical level, V. corymbosum plants subjected to WD exhibited an imbalance in their photosynthetic performance, increasing the reactive oxygen species (ROS) biosynthesis [13,16]. The high ROS level damages plasma membranes by enhancing lipid peroxidation [16]. It is worth noting that the impacts of WD stress on V. corymbosum plants become noticeable after they have been subjected to water stress for a minimum of 3 weeks [11,16,17]. On the other hand, negative effects have been reported on plant growth in V. corymbosum plants subjected to Al [3,18,19]. It has been reported that Al reduced root growth, leading to a decrease in water and nutrient uptake, negatively affecting other physiological processes such as photosynthesis [3,18,20]. It is crucial to note that V. corymbosum plants exposed to Al toxicity stress respond more quickly than those experiencing WD, as the effects of Al toxicity become evident after just one week of treatment [3,18,21].
Studies showed that several V. corymbosum cultivars exhibit varying degrees of resistance to individual WD and Al stress [3,11,18,21,22]. Thus, cv. Elliot and cv. Biloxi have been reported to be WD-resistant, while cv. Brigitta was reported as WD-sensitive [11,16,17]. Regarding Al, some studies revealed that cv. Brigitta, cv. Legacy, cv. Camellia, and cv. Cargo are classified as Al-resistant, while cv. Bluegold and cv. Star are Al-sensitive [19,22,23]. However, few reports have been found about combined WD and Al stress, which are mainly crops like Hordeum vulgare L., where plants have tolerated individual stresses of WD and Al and also demonstrated resistance to the combined stress of WD and Al (WD+Al) [7].
The foliar application of phytohormones, such as methyl jasmonate (MeJA), has been reported as an important tool to prevent individual stresses due to WD and Al [19,24,25,26,27,28]. Thus, some studies have demonstrated that MeJA at doses of 10, 50, and 100 µM increased the enzymatic and non-enzymatic antioxidant mechanisms, as well as increasing osmoregulatory compounds such as proline and soluble carbohydrates, reducing lipid peroxidation, and improving resistance mechanisms in V. corymbosum, Zea mays L., Triticum sativum, Citrus sp. cv. Huangguogan, and Glycine max L. plants subjected to WD [24,26,27,28,29]. Thus, Ulloa-Inostroza et al. [19,25,28] reported that V. corymbosum plants exposed to individual WD and Al revealed that the 10 µM dose was the most effective in mitigating damage and inducing resistance mechanisms. However, the effects of MeJA on V. corymbosum plants subjected to WD+Al stress remain unclear. Cáceres et al. [10] reported a comprehensive review of the phytohormonal response to WD and Al individually, suggesting that in plants facing WD+Al stress, jasmonates (JAs) could activate resistance mechanisms such as increased antioxidant activity.
Based on the information, we hypothesize that V. corymbosum cultivars are sensitive and resistant to Al and will also be sensitive and resistant to combined WD+Al stress. The resistant cultivar is expected to activate its antioxidant system more rapidly in response to the combined WD+Al stress. Additionally, we expected that the effective dose of MeJA to mitigate damage and activate the antioxidant system against the combined WD+Al stress in V. corymbosum plants would be higher than the doses used for individual stresses previously reported for this species. Therefore, this study aimed to determine the effective MeJA dose to mitigate damage and activate the antioxidant system against the combined WD+Al stress in two cultivars of V. corymbosum with contrasting Al resistance. The findings from this research will be a valuable contribution toward understanding the behavior of WD stress and Al stress interaction while also highlighting the efficacy of MeJA as a valuable agronomic tool for mitigating the adverse effects of this interaction.

2. Materials and Methods

2.1. Soil Properties and Preparation

The soil used in this study is classified as the Lastarria series (Andisol), procured from Lastarria, La Araucanía Region, Chile [30]. To achieve a high Al concentration in soil (1665 mg kg−1), 10 mL of 18% AlCl3 (Winkler LTDA, Santiago, Chile) per kg of soil was used to irrigate at the onset of treatments. A control treatment was the soil without AlCl3 supplementation (65 mg kg−1).

2.2. Plant Material and Growing Conditions

Two highbush blueberry (V. corymbosum) cultivars with contrasting Al resistance were used in this study: Star (Al-sensitive) and Legacy (Al-resistant). Plants were obtained from Viveros Global Seedling SpA. in the Maule region, Chile. Plants of uniform size (between 30 and 40 cm) were placed in plastic pots containing 1 kg of soil (with low Al saturation) and conditioned in a greenhouse for two weeks (temperature of 25 ± 2 °C, relative humidity between 60% and 70%, and photosynthetic photon flux density (PPFD) of 500 μmol photons m−2 s−1 as a mean of the day). Moisture sensors were used to monitor the plants daily. These sensors were calibrated to measure moisture levels consistent with field capacity (FC), allowing us to maintain irrigation at 80% of the same level. To determine field capacity, we employed the cylindrical sand bath method proposed by Brischke and Wegener [31].

2.3. Treatments

After two weeks of conditioning, plants corresponding to the control were kept irrigated at 80% FC, and the other plants were suspended irrigation until reaching 50% FC, which corresponds to WD conditions as described by Almutairi et al. [32]. After the plants reached 50% FC, 10 mL per kg of soil of 18% AlCl3 was applied to reach 1665 mg/kg of Al; this was applied as irrigation as described by Slugeňová et al. [33]. For determining the effective MeJA dose, five treatments were applied. (1) Control: plants irrigated at 80% FC with 65 mg/kg of Al, and no MeJA application; (2) plants subjected to WD+Al stress: irrigated at 50% FC, 1665 mg/kg of Al, and no MeJA application; (3) plants subjected to WD+Al stress and 10 µM MeJA; (4) plants subjected to WD+Al stress and 50 μM MeJA; (5) plants subjected to WD+Al stress and 100 μM MeJA. The MeJA (Sigma-Aldrich, St. Louis, MO, USA) was prepared with 0.05% tween 80 (Sigma-Aldrich, St. Louis, MO, USA) and applied foliarly to the stressed plants after applying Al to the soil. Leaves and roots were collected on the morning of the 7th and 21st days of the experiment. Fifteen biological replicates per treatment were considered, of which five plants were separated for chemical and biomass analysis, five plants for photosynthetic and plant water status parameters, and five plants for biochemical analysis.

2.4. Leaf and Root Aluminum Concentration

The Al concentration was analyzed in leaves and roots. Each sample was dried in an oven at 70 °C for 24 h and then incinerated at 500 °C for 8 h. Following this, the sample was treated with 2M HCl and filtered. The Al concentration was determined using atomic absorption spectrophotometry (model 969; UNICAM, Cambridge, UK) with nitrous oxide-acetylene flame by direct aspiration at 324.7 nm [34].

2.5. Physiological Analyses

2.5.1. Plant Growth

The relative growth rate (RGR) was measured to determine plant growth. For this, the protocol proposed by Hoffmann and Poorter [35] was used, based on dry weight (DW) transformed into a natural logarithm according to equation 1, where W1 corresponds to the DW at the beginning, W2 corresponds to the DW after 21 days, t1 corresponds to 0 days, and t2 corresponds to 21 days. Five biological replicates were considered, and after drying the samples in an oven at 72 °C for three days, we recorded their dry weight.
RGR = (ln W2 − ln W1)/(t2 − t1)

2.5.2. Plant Water Status

Stem water potential (Ψw) was measured using a Scholander Model 1000 chamber (PMS, Instruments Co., Corvallis, OR, USA), according to the Begg and Turner [36] protocol. A branch was used for the measurement, which was covered with aluminum foil and a plastic bag 90 min before the measurement. The Ψw was determined on days 7 and 21 of the experiment.
The relative water content (RWC) was determined according to Rahimi et al. [37]. For this, five leaves were removed from three different plants per treatment, weighed to obtain the fresh weight (FW), and then immersed in double-distilled water for 24 h. The leaves were then reweighed to obtain the turgor weight (TW) and oven-dried to a constant weight at 60 °C. Finally, the leaves were weighed again to obtain the dry weight (DW). The RWC was calculated using Equation (2).
RWC = [(FW − DW)/(TW − DW)] × 100

2.5.3. Photosynthetic Parameters

Gas exchange measurements were performed using a portable infrared gas analyzer (IRGA) (Li-6400; LI-COR Inc., Lincoln, NE, USA). Net photosynthesis (Pn), stomatal conductance (gs), and the transpiration rate (E) were assessed in leaves taken from the second to the third shoot node within the light period (08:00 to 10:00 AM) at days 7 and 21 of treatment, following the protocol of Reyes-Díaz et al. [38]. The gas analyzer maintained controlled environmental conditions, a light intensity of 500 μmol m−2 s−1, a temperature of 20 °C, relative humidity of 70%, and a CO2 concentration of 360 ppm, with a flow rate of 200 mL min−1 [38].

2.6. Biochemical Analyses

2.6.1. Lipid Peroxidation Determination

Lipid peroxidation (LP) was evaluated in leaves and roots by monitoring the levels of substances that react with thiobarbituric acid (TBARS), as an indicator of oxidative damage [39]. The absorbance was determined at 532, 600, and 440 nm wavelengths to correct for interferences caused by TBARS-sugar complexes through an UV/Vis Unico SpectroQuest 2800 spectrophotometer (United Products & Instruments Inc., Dayton, NJ, USA). This method identifies the presence of malondialdehyde (MDA) as a secondary by-product derived from the oxidation of polyunsaturated fatty acids that can react with TBARS. The LP was expressed in terms of malondialdehyde content equivalents (nmol MDA g−1 DW).

2.6.2. Non-Enzymatic Antioxidants

Total antioxidant capacity (AC) was measured following the 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radical scavenging (Sigma-Aldrich, St. Louis, MO, USA) method proposed by Chinnici et al. [40]. Ethanol extracts were derived from both leaf and root samples. The absorbance was determined spectrophotometrically at 515 nm. Trolox (Sigma-Aldrich, St. Louis, MO, USA) was used as the reference standard and expressed as mg of Trolox equivalent (TE) g−1 DW. Total phenols (TP) were assessed by the Folin–Ciocalteu reagent (Merck KGaA, Darmstadt, Germany), following the Slinkard and Singleton [41] method. The absorbance was measured at 765 nm (UV/Vis Unico SpectroQuest 2800 spectrophotometer, United Products & Instruments Inc., Dayton, NJ, USA). The TP concentration was expressed as μg of chlorogenic acid (Sigma-Aldrich, St. Louis, MO, USA) equivalent (GAE) g−1 DW.

2.6.3. Enzymatic Antioxidants

The antioxidant activity of the superoxide dismutase (SOD) enzyme was measured on leaves and roots. The extraction and analysis of SOD activity was carried out as described by Giannopolitis and Ries [42] by monitoring the superoxide radical-induced reduction of nitroblue tetrazolium (NBT) (Winkler LTDA, Santiago, Chile) at 560 nm by an UV/Vis Unico SpectroQuest 2800 spectrophotometer (United Products & Instruments Inc., Dayton, NJ, USA). The SOD activity was expressed as U mg−1 protein.

2.7. Statistical Analysis

The experiment considered two cultivars, two harvest times, and five treatments. Each experimental unit comprised 5 biological replicates, and all analyzed data successfully passed the Shapiro–Wilk normality test for normality and homogeneity of variance. Data were analyzed by three-way ANOVA, where the factors were cultivars, harvest time, and treatments. Tukey’s multiple comparison test p ≤ 0.05 was used. SigmaPlot 12.0 software was used for statistical data analysis, and GraphPad Prism 10.1.2 was used for graphing. Principal component analysis (PCA) was necessary to equalize the magnitude of the variables. Thus, each response was divided by the median of the entire data set. Then, the data were subjected to the Z-score transform. Thus, the data were subjected to a principal component analysis (PCA) using the pcaMethods package in the R software 4.2.3 version [43].

3. Results

3.1. MeJA Application Effects on Leaf and Root Aluminum Concentration of V. corymbosum Under Combined WD+Al Stress

The Al concentration in leaves and roots of V. corymbosum exhibited a noteworthy interplay between cultivar, time, and treatment, p < 0.001 (Figure 1). In both cultivars, a significant increase in Al concentration was observed in both leaves and roots in plants treated with WD+Al with respect to the control at 7 and 21 days of the experiment (Figure 1A,B). The most significant increase was observed in the roots of the Al-sensitive cultivar at day 7 in the WD+Al stressed plants, which were 9.9 times greater than the control. It is also important to note that the Al-sensitive cultivar accumulated 1.8 times more Al than the Al-resistant cultivar. Both cultivars exhibited a decrease in roots Al concentration after 7 and 21 days of foliar MeJA application, compared to WD+Al stressed plants without MeJA application (Figure 1B). The 50 µM dose of the MeJA application displayed the greatest reduction in Al concentration in roots with a 3.2 times lower rate in the Al-sensitive cultivar at 7 days (Figure 1B). Similarly, a decline in foliar Al concentration was observed in MeJA-treated plants after 21 days of treatment, compared to plants grown under WD+Al treatment. The 50 µM dose produced the most significant decrease in foliar Al concentration, with levels up to 2.7 times lower than plants stressed by WD+Al in Al-resistant cultivar (Figure 1A).

3.2. Plant Growth of V. corynbosum Under Combined WD+Al Stress and MeJA Application

The relative growth rate (RGR) significantly decreased in Al-sensitive and Al-resistant cultivars subjected to combined WD+Al stress compared to control plants. The RGR decreased by 1.7-fold in the Al-sensitive cultivar, while the Al-resistant cultivar experienced a 1.8-fold decrease (Table 1; Figure S1). When plants were subjected to foliar application of MeJA, plants exhibited a substantial increase in RGR under the combined WD+Al stress condition, reaching levels comparable to those of control plants in both cultivars. In the case of the Al-sensitive cultivar, this effect was observed at a dose of 100 µM (Figure S1), while in the sensitive cultivar, the increase was observed at a dose of 50 µM (Table 1).

3.3. Plant Water Status of V. corymbosum Under WD+Al Stress and MeJA Application

A reduction in water potential (Ψw) was observed in both cultivars subjected to the WD+Al treatment compared to the control plants (Table 2). The decrease was significantly greater after 21 days of treatment, reaching levels 3.6 times lower in the Al-sensitive cultivar and 3-fold lower in the Al-resistant cultivar compared to the control. Regarding the effective MeJA dose, it was observed that doses of 10 and 50 µM were effective in mitigating the decrease in Ψw of the Al-sensitive cultivar after 21 days of treatment. In the case of the 50 µM dose, the decrease in Ψw was up to 2.5 times lower than the combined WD+Al stress without MeJA. In both cultivars, there was a significant reduction in RWC (Table 2). The Al-sensitive cultivar experienced a 6% decrease compared to the control plants after 7 days of treatment, while the Al-resistant cultivar showed a 10% decrease compared to the control plants after 21 days of treatment. The application of MeJA mitigated the reduction in RWC for both cultivars. In the Al-sensitive cultivar, MeJA doses of 50 and 100 µM restored values similar to those of the control plants, while in the Al-resistant cultivar, all MeJA doses mitigated the decrease in RWC, resulting in values similar to those of the control plants.

3.4. Leaf Gas Exchange Parameters in V. corymbosum Under WD+Al Stress and MeJA Application

The photosynthetic parameters revealed that the Al-sensitive cultivar exhibited significant differences under the WD+Al stress treatment (Table 2). Following 21 days of treatment, a 1.5-fold reduction in photosynthesis (Pn) and stomatal conductance (gs) was observed, along with a 1.2-fold decrease in transpiration (E) in comparison to the control plants. The application of MeJA, particularly at concentrations of 10 µM and 50 µM, led to a notable enhancement in these parameters, bringing them closer to the control levels. Applying 10 µM of MeJA resulted in a 1.41-fold increase in Pn, while gs and E exhibited no significant alterations. The application of 50 µM MeJA resulted in a 1.46-fold increase in Pn, a 1.41-fold increase in gs, and no significant change in E. The application of MeJA at a concentration of 100 µM did not result in any notable enhancements, exhibiting values that remained comparable to those observed in the combined WD+Al stress treatment without the addition of MeJA.

3.5. Effects of MeJA on Lipid Peroxidation of V. corymbosum Under Combined WD+Al Stress

Lipid peroxidation showed a significant interaction among cultivar, time, and treatment factors (p < 0.001). Lipid peroxidation significantly increased the leaves and roots of both cultivars subjected to WD+Al stress compared to the control plants after 7 and 21 days of treatment (Figure 2). In our study, an Al-resistant cultivar showed a significant increase in lipid peroxidation in leaves, which was 2.7-fold higher in WD+Al-stressed plants than in control plants. By contrast, Star, an Al-sensitive cultivar, showed a higher lipid peroxidation in roots, 1.6 times higher in WD+Al-stressed plants than in control plants. Interestingly, all MeJA doses reduced oxidative damage in the Al-sensitive cultivar exposed to WD+Al stress, particularly with the 50 µM MeJA, which showed similar results to the control plants in leaves and roots after 7 days of treatment. After 21 days, the 10 µM and 50 µM MeJA in leaves were effective, showing levels comparable to the control plant. Regarding the Al-resistant cultivar, the 50 µM MeJA dose reduced oxidative damage in leaves after 7 and 21 days of treatment. In roots, all MeJA treatments counteracted the oxidative damage caused by WD+Al stress, even reaching levels comparable to those of control plants with doses of 100 and 50 µM after 7 and 21 days of treatment.

3.6. Effects of WD+Al Stress on Non-Enzymatic Antioxidants in V. corymbosum

Following a 7-day treatment period, an increase in antioxidant activity was observed in plants grown under WD+Al treatment, both in leaves and roots of the Al-sensitive and Al-resistant cultivars, in comparison to control plants (Figure 3A,B). However, after 21 days of treatment, this same result was only observed in the leaves of the Al-sensitive cultivar and the roots of the Al-resistant cultivar. Regarding the foliar application of MeJA, a significant increase in AC was only observed in combined WD+Al-stressed plants in the Al-resistant cultivar. This increase was observed in leaves after 7 days of treatment with all MeJA doses, and the 50 µM dose of MeJA was up to 1.8 times higher than plants grown under WD+Al treatment. After 21 days of treatment, this increase was observed in both the leaves and roots, but only with the 50 µM MeJA dose, with a 1.6-fold increase in leaves compared to combined WD+Al stressed plants and a 1.3-fold increase in roots. A significant increase in polyphenol concentration was observed in the combined WD+Al stressed plants compared to the control plants, both in the leaves and roots of the Al-sensitive cultivar and in the leaves of the Al-resistant cultivar after 7 days of treatment (Figure 3C,D). However, this significant increase was only visible in the leaves of the Al-resistant cultivar after 21 days of treatment. When a foliar application of MeJA was performed, a significant increase in total polyphenols was recorded in the leaves of the Al-sensitive cultivar after 7 days of treatment with doses of 10 and 50 µM, exceeding combined WD+Al stressed plants levels up to 1.3-fold with the 50 µM dose (Figure 3C). In contrast, in the Al-resistant cultivar, this significant increase was observed after 21 days with the same MeJA doses, exceeding combined WD+Al stressed plant levels up to 1.6-fold with the 50 µM dose. As for polyphenols in roots (Figure 3D), the Al-sensitive cultivar showed an increase in their concentration only after 21 days of treatment with 50 and 100 µM doses, compared to combined WD+Al stressed plant levels. On the other hand, roots of the cultivar Al-resistant showed an increase at 7 days with all MeJA doses and at 21 days only with the 50 µM dose.

3.7. Influence of MeJA Application on Enzymatic Antioxidants in V. corymbosum Under WD+Al Stress

As for enzymatic antioxidants, it can be observed that SOD activity significantly increased with the foliar application of MeJA, exceeding the values obtained in the plants grown under WD+Al treatment. The increase in SOD activity in leaves was especially significative at the 50 µM dose, being up to 2.1 times higher than the combined WD+Al stressed plants in the Al-sensitive cultivar after 7 and 21 days of treatment and 3.3 times higher than the combined WD+Al stressed plants in Al-resistant after 21 days of treatment (Figure 4). In the roots, the significant increase in SOD activity was less pronounced and was only observed after 7 days of treatment, in the Al-sensitive cultivar with the 50 µM and 100 µM doses and in Al-resistant with the 50 µM dose.

3.8. Multivariate Analysis

The principal component analysis (PCA) was based on leaf and root data collected at 7 days (A) and 21 days (B) into the experiment. The physiological and metabolic data indicated that between 52.47% (at 7 days) and 53.58% (at 21 days) of the variance was explained by the two principal components, PC1 and PC2 (refer to Figure 5). At both 7 and 21 days of treatment, observable trends emerged, differentiating the two cultivars and their respective tissues. Following 7 days of treatment (Figure 5A), there was a tendency to form three groups: (1) a cluster comprising leaves and roots of the Al-sensitive cultivar; (2) a cluster consisting of leaves of the Al-resistant cultivar; and (3) a cluster comprising roots of the Al-resistant cultivar. Al-resistant plants separated leaves and root samples influenced by PC1, mainly due to lipid peroxidation and total antioxidant variables. After 21 days of treatment (Figure 5B), the observed trends manifested in four groups: (1) a cluster of leaves of the Al-resistant cultivar; (2) a cluster of leaves of the Al-sensitive cultivar; (3) a cluster of roots of the Al-resistant cultivar; and (4) a cluster of roots of the Al-sensitive cultivar. Although root samples were separated for each cultivar, both (Al-resistant and Al-sensitive) were influenced to separate from the leaves samples of each cultivar by PC1 specifically due to Al content and total antioxidant. Furthermore, root samples from Al-sensitive and Al-resistant cultivars are separate from each other and influenced by lipid peroxidation. On the other hand, the leaf samples of the Al-sensitive and Al-resistant cultivars are separated and influenced by PC2, mainly due to the variables phenols, transpiration, and RWC.

4. Discussion

4.1. Aluminum Accumulation Restricts Growth and Water Uptake in V. corymbosum Under Combined WD+Al Stress

This study examines the impact of WD and Al stress on V. corymbosum, a species vulnerable to both but which has not been investigated under their combined influence [12,15,16,17]. The results of this study indicate that V. corymbosum is adversely affected by the combined WD+Al stress. This is evidenced by a significant increase in Al accumulation (Figure 1) and a significant decrease in relative growth rate (RGR) (Table 1), stem water potential (Ψw) (Table 2), and relative water content (RWC) (Table 2) in plants exposed to combined WD+Al stress, as compared to control plants. These results align with observations made by other researchers on different plants exposed to combined WD+Al stress, indicating that significant increases in Al content are directly associated with a decrease in RGR, Ψw, and RWC [9,44,45,46,47]. According to Yang et al. [45], under combined WD+Al stress, Al primarily contributes to decreased water and nutrient uptake. This is because Al leads to a decline in water potential and, upon entering the plant, reduces the porosity of cell walls and plasma membranes in the meristem and root elongation zones, crucial areas for water and nutrient absorption. Additionally, Al interferes with pectin distribution in the cell wall, impeding root elongation [48].
Prior research has indicated that when combined, plants maintain their sensitivity or resistance to individual WD and Al stresses [7,47]. Our findings also support this trend, noting that the increase in Al concentration and decrease in Ψw were significantly more pronounced in the sensitive cultivar (Figure 1 and Table 2). Our results agree with previous studies on V. corymbosum and Hordeum vulgare under Al toxicity and combined WD+Al stress. These studies reported elevated levels of Al accumulation in stressed plants, with Al-sensitive cultivars showing the highest sensibility to WD and Al stress [3,7,23,47]. Furthermore, these findings align with observations made by Slugeňová et al. [33], who reported a decrease in Ψw in Picea abies plants subjected to combined WD+Al stress. Hence, these results suggest that the Al-sensitive cultivar (Star) is more susceptible to combined WD+Al stress than the Al-resistant cultivar (Legacy).

4.2. The MeJA 50 µM Dose Is the Effective Dose for Mitigation of Combined WD+Al Stress

Foliar application of MeJA on plants with combined WD+Al stress significantly reduced Al concentration and increased RGR, Ψw, and RWC compared to plants not treated with MeJA. It has been established that MeJA acts as a signal molecule that induces the biosynthesis of compounds that limit Al uptake and increase Ψw and RWC [10]. Thus, studies in Pinus massoniana suggest that jasmonate accumulation increases the expression of the transcription factor WRKY, which positively regulates the malate transporter ALMT, exuding malate into the soil to form complexes with Al and reduce its uptake by the plant [49]. However, the exact mechanism by which MeJA limits Al uptake under these conditions remains unknown.
Studies performed in V. corymbosum, Brassica oleracea, and Beta vulgaris plants exposed to individual WD and Al stresses indicated that the effective dose of MeJA to mitigate WD or Al damage is 10 µM, with this dose significantly reducing Al accumulation and increasing biomass over individual stresses without MeJA application [25,28,50,51]. This issue supports the hypothesis that higher doses of MeJA are required in combined WD+Al stresses.

4.3. The MeJA Improves Photosynthetic Performance and Limits Transpirational Water Loss Under Combined WD+Al Stress

Plants exposed to combined WD+Al stress as well as individual stresses have shown increases in Al concentrations and decreases in Ψw, associated with reduced parameters such as Pn, gs, and E [24,29,33,49]. The results of this study reflect this phenomenon, particularly in the Al-sensitive cultivar, where a significant decrease in photosynthetic parameters, including Pn, gs, and E, was observed in plants subjected to combined WD+Al stress compared to control plants after 21 days of treatment (Table 1). These findings are consistent with those in H. vulgare plants under combined WD+Al stress, which showed a significant reduction in the same photosynthetic parameters when compared to the control plants [7]. Regarding MeJA application, doses of 10 µM and 50 µM were observed to significantly enhance Pn and gs, thereby bringing them closer to the control levels. However, no significant changes were noted in the case of E. These findings are consistent with previous studies on the effects of individual WD stresses and Al toxicity, which have demonstrated that MeJA can prevent the decline in Pn under these conditions but does not mitigate the decline in E [25,28]. This is primarily because MeJA may act synergistically with abscisic acid (ABA) to regulate stomatal closure as a resistance mechanism to prevent water loss through transpiration [52]. These findings demonstrate that MeJA at moderate doses (10 µM and 50 µM) can enhance photosynthetic parameters such as Pn and gs, thereby enabling plants to maintain equilibrium between stomatal aperture and photosynthetic efficiency under combined WD+Al stress conditions, which in turn allows to keep a better plant water status.

4.4. MeJA Decreases Oxidative Damage by Inducing the Accumulation of Non-Enzymatic Antioxidants Under Combined WD+Al Stress

A reduction in photosynthetic activity can result in excess light excitation energy, leading to overexcitation of photosynthetic pigments and an increased accumulation of ROS, resulting in a significant increase in lipid peroxidation, producing oxidative stress in plants [16,18,25]. The results of our research align with this finding, demonstrating a significant increase in lipid peroxidation in the leaves and roots of both cultivars under combined WD+Al stress. Our PCA analysis indicates that this is the primary factor influencing the behavior of the roots in the sensitive cultivar after 21 days of treatment (Figure 5). Additionally, our PCA analysis suggests that the 50 µM dose of MeJA has the least impact on lipid peroxidation in the roots of Al-sensitive cultivars after 21 days of WD+Al treatment. These findings are consistent with those presented in Figure 2, which illustrate that the 50 µM MeJA dose results in the most significant reduction in oxidative damage caused by WD+Al stress in both roots and leaves of both cultivars after 7 and 21 days of treatment. In a study conducted by Allagulova et al. [26] on Triticum aestivum under water deficit conditions, it was noted that the application of MeJA had a beneficial impact on both gene expression and dehydrin accumulation. This protein plays a crucial role in preserving the structural integrity of the plasma membrane and is actively involved in alleviating oxidative damage resulting from lipid peroxidation during dehydration conditions [26].
In conjunction with the increase in lipid peroxidation in plants exposed to combined WD+Al stress, a significant increase in both enzymatic and non-enzymatic antioxidant content was observed (Figure 2, Figure 3 and Figure 4), which was particularly pronounced in the leaves of the Al-resistant cultivar. The results of the PCA analysis indicated that the non-enzymatic antioxidants had the most significant impact on the leaves of the Al-resistant cultivar. The total antioxidants were the most relevant at 7 days, while polyphenols exerted the most significant influence at 21 days (Figure 3 and Figure 5). An increase in polyphenols is linked to a decrease in lipid peroxidation, as polyphenols contain multiple hydroxyl (OH) groups that can donate electrons to neutralize free radicals such as the hydroxyl radical (OH-), which is the primary radical involved in the lipid peroxidation of cell membranes [53,54]. Hence, this helps to reduce oxidative stress caused by factors such as WD and Al. Numerous studies have also extensively examined the role of polyphenols as chelating agents. These compounds bind Al in the cell wall or create complexes with the metal, rendering it inactive within the plant symplast or vacuole [1,55]. Polyphenols bind aluminum ions through their hydroxyl and carboxyl groups, reducing cell availability and preventing oxidative damage [56]. These findings suggest that aluminum-resistant cultivars can alleviate oxidative damage associated with water deficit and aluminum stress by activating their non-enzymatic antioxidant system, mainly by accumulating polyphenols.
Applying MeJA on the leaves of V. corymbosum plants under combined WD+Al stress increased enzymatic and non-enzymatic antioxidant concentrations. PCA analysis indicated that the 50 µM dose had the most significant impact on the rise of polyphenols in leaves of the Al-resistant cultivar after 21 days under combined WD+Al stress (Figure 3 and Figure 5). The results agree with previous studies on the response of V. corymbosum to Al toxicity and MeJA treatments. Those studies found increased levels of polyphenols such as chlorogenic acid, caffeic acid, ferulic acid, and myricetin in plants subjected to combined Al+MeJA treatment. These increased polyphenol levels were associated with the greater Al resistance observed in the Al-resistant cultivar [19]. A recent study demonstrated that MeJA induces polyphenol accumulation by regulating the expression of genes encoding enzymes involved in the phenylpropanoid pathway, including phenylalanine ammonium lyase (PAL), 4-cinnamic hydroxylase (C4H), and 4-coumarate:coenzyme A ligase (4CL) [57]. This suggests that 50 µM MeJA can enhance polyphenol accumulation by potentially up-regulating genes related to the phenylpropanoid pathway.

5. Conclusions

According to the evidence presented, the hypotheses have been successfully addressed. Our findings confirm that the cultivars exhibiting sensitivity or resistance to Al toxicity stress also demonstrate resistance to the combined WD+Al stress. The results of our PCA analysis indicate that the parameters responsible for the Al-sensitive cultivar’s sensitivity to the combined WD+Al stress are the accumulation of Al and lipid peroxidation in roots, as evidenced by higher levels compared to the Al-resistant cultivar. In contrast, the Al-resistant cultivar demonstrates resistance to the combined WD+Al stress through the induction of non-enzymatic antioxidant activity, particularly the accumulation of total polyphenols in leaves. This phenomenon is accompanied by a notable reduction in oxidative damage, as evidenced by a significant correlation between these two variables. Secondly, we have determined that the effective MeJA dose for alleviating the combined WD+Al stress was 50 µM, which is higher than the dosage used for treating individual WD and Al toxicity stresses (MeJA 10 µM). The 50 µM dose was found to be the most effective in reducing the concentration of Al and oxidative damage in the roots of the sensitive cultivar. Furthermore, it resulted in the greatest accumulation of polyphenols in the tissues of the Al-resistant cultivar. These findings have significant implications for agricultural practices, particularly in regions with acidic soils and constrained water resources. They suggest a potential strategy for enhancing the resilience of V. corymbosum by combining WD+Al stress through the application of MeJA.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/horticulturae10111172/s1: Figure S1: Pictures of cv. Star plants from different treatments at 21 days. Table S1: Component loading table derived from data of leaves and roots harvested in 7 days and 21 days of experiment.

Author Contributions

C.C. and M.R.-D. conceptualized, designed, and coordinated the experiment; M.R.-D. supervised; M.R.-D., C.I.-B., M.D. and A.N.-N. obtained funding acquisition; C.C., C.C.-C., P.D.-S. and J.G.-V. carried out the physiological and biochemical analysis; M.R.-D. and L.A.B. performed and analyzed the photosynthetic parameters; C.C., M.M. and A.N.-N. performed the statistical analyses; C.C., M.D. and M.R.-D. formulated the draft of the manuscript. C.C., M.M., M.D., A.R.-F., C.I-B., L.A.B., J.G.-V., A.N.-N. and M.R.-D. revised and improved the current version of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Agencia Nacional de Investigación y Desarrollo (ANID)/FONDECYT 1211856; ANID scholarship 21202370; ANID/FONDAP/15130015; ANID/FONDAP/1523A0001; ANID/Anillo ATE230007; PP23-0023 de la Dirección de Investigación UFRO; ANID/FONDECYT 1201749; ANID/FONDECYT 1210684; and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazil, Grant 407276/2021-1 and 406455/2022-8).

Data Availability Statement

All data supporting the findings of this study are available within the paper.

Acknowledgments

We would like to thank Ximena Garrido, Jessica Yañez, and Mariela Mora for technical support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Concentration of aluminum (Al) in the (A) leaves and (B) roots in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
Figure 1. Concentration of aluminum (Al) in the (A) leaves and (B) roots in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
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Figure 2. Lipid peroxidation in the (A) leaf and (B) root in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
Figure 2. Lipid peroxidation in the (A) leaf and (B) root in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
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Figure 3. Total antioxidant capacity and total polyphenols in leaves (A,C) and roots (B,D) in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
Figure 3. Total antioxidant capacity and total polyphenols in leaves (A,C) and roots (B,D) in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
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Figure 4. Superoxide dismutase (SOD) activity in (A) leaves and (B) roots in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
Figure 4. Superoxide dismutase (SOD) activity in (A) leaves and (B) roots in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and treated with different MeJA doses (10, 50, and 100 µM). Each value represents the mean ± SD of five replicates per treatment. Due to a lack of statistically significant differences among controls and start of the experiment (0 day), we considered the values at control as the average among the start of the experiment and the respective controls for each time point (7 and 21 days). Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
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Figure 5. Principal component analysis (PCA) scores and loading plot from physiologic and metabolic data derived from two V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars that were subjected to combined water deficit and Al stress (WD+Al) and treated with varying doses of MeJA at 10, 50, and 100 µM. The PCA is derived from data of leaves and roots harvested in (A) 7 days and (B) 21 days of the experiment, exhibiting 52.47% and 53.58% on variance explained, respectively, in the separation of groups in the two principal components. In the Loadings plot, font size is directly proportional to its importance in separating groups. PC1, principal component 1; PC2, principal component 2. Values of the loading plot are presented in Table S1.
Figure 5. Principal component analysis (PCA) scores and loading plot from physiologic and metabolic data derived from two V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars that were subjected to combined water deficit and Al stress (WD+Al) and treated with varying doses of MeJA at 10, 50, and 100 µM. The PCA is derived from data of leaves and roots harvested in (A) 7 days and (B) 21 days of the experiment, exhibiting 52.47% and 53.58% on variance explained, respectively, in the separation of groups in the two principal components. In the Loadings plot, font size is directly proportional to its importance in separating groups. PC1, principal component 1; PC2, principal component 2. Values of the loading plot are presented in Table S1.
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Table 1. Relative growth rate (RGR) at 21 days in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars treated with combined water deficit and Al stress (WD+Al) and with different doses of MeJA (10, 50, and 100 µM).
Table 1. Relative growth rate (RGR) at 21 days in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars treated with combined water deficit and Al stress (WD+Al) and with different doses of MeJA (10, 50, and 100 µM).
CultivarsTreatmentRGR of the Plant (mg DW d−1)
Al-sensitive
(cv. Star)		Control39.1 ± 4.2 Aa
WD+Al22.4 ± 3.6 Ab
WD+Al+MeJA10 27.9 ± 4.5 Ab
WD+Al+MeJA50 22.7 ± 3.8 Bb
WD+Al+MeJA10036.4 ± 4.7 Aa
Al-resistant
(cv. Legacy)		Control39.6 ± 1.7 Aa
WD+Al21.2 ± 4.3 Ac
WD+Al+MeJA1033.4 ± 1.1 Ab
WD+Al+MeJA5040.6 ± 0.2 Aa
WD+Al+MeJA10018.3 ± 4.9 Bc 1
1 Each value represents the mean ± SD of five replicates per treatment. Uppercase letters indicate significant differences (p ≤ 0.05) between cultivars of the same treatment and lowercase letters indicate significant differences (p ≤ 0.05) between treatments of the same cultivar, according to Tukey’s test.
Table 2. Net photosynthesis (Pn), stomatal conductance (gs), transpiration (E), water potential (Ψw), and relative water content (RWC) in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and different MeJA doses (10, 50, and 100 µM).
Table 2. Net photosynthesis (Pn), stomatal conductance (gs), transpiration (E), water potential (Ψw), and relative water content (RWC) in V. corymbosum plants of Al-sensitive (Star) and Al-resistant (Legacy) cultivars subjected to combined water deficit and Al stress (WD+Al) and different MeJA doses (10, 50, and 100 µM).
CultivarsTimeTreatmentΨw
(MPa)		RWC
(%)		Pn
(µmol CO2 m−2s−1)		gs
(mol H2O m−2s−1)		E
(mmol H2O m−2s−1)
Al-sensitive
(cv. Star)		7 daysControl−0.28 ± 0.08 Aa95.72 ± 1.21 Aa7.81 ± 0.33 Aa0.35 ± 0.01 Aa*1.62 ± 0.03 Aa*
WD+Al−1.07 ± 0.03 Ab90.08 ± 2.66 Bb*7.78 ± 0.23 Aa0.24 ± 0.02 Ab1.48 ± 0.07 Ab*
WD+Al+MeJA10 −1.12 ± 0.06 Ab87.08 ± 0.42 Bb7.97 ± 0.11 Aa0.22 ± 0.01 Bb*1.36 ± 0.09 Ab*
WD+Al+MeJA50 −1.12 ± 0.28 Ab96.26 ± 3.34 Aa8.06 ± 0.03 Aa0.21 ± 0.01 Bb*1.37 ± 0.11 Ab*
WD+Al+MeJA100 −1.83 ± 0.45 Ac*98.90 ± 4.23 Aa7.92 ± 0.26 Aa0.23 ± 0.01 Ab1.38 ± 0.06 Ab*
21 daysControl−0.77 ± 0.12 Ba97.51 ± 4.71 Aa7.81 ± 0.10 Aa0.33 ± 0.01 Aa*1.64 ± 0.03 Aa*
WD+Al−2.78 ± 0.20 Bd*95.86 ± 1.11 Aa*5.37 ± 0.26 Bb*0.22 ± 0.02 Ab*1.46 ± 0.11 Ab*
WD+Al+MeJA10−1.37 ± 0.23 Ab*96.51 ± 1.08 Aa7.59 ± 0.31 Aa0.25 ± 0.01 Ab1.38 ± 0.05 Ab*
WD+Al+MeJA50−1.10 ± 0.10 Ab*98.49 ± 1.69 Aa*7.86 ± 0.04 Aa0.31 ± 0.01 Aa*1.36 ± 0.05 Ab*
WD+Al+MeJA100−2.30 ± 0.20 Ac*96.05 ± 2.24 Aa5.98 ± 0.02 Bb*0.23 ± 0.03 Ab1.34 ± 0.05 Ab*
Al-resistant
(cv. Legacy)		7 daysControl−0.15 Aa97.32 ± 1.04 Aab8.18 ± 0.14 Aa0.28 ± 0.02 Aa*1.28 ± 0.03 Aa*
WD+Al−0.75 ± 0.13 Ab99.83 ± 1.76 Aa*8.07 ± 0.31 Aa0.27 ± 0.02 Aa1.24 ± 0.03 Aa*
WD+Al+MeJA10−1.28 ± 0.08 Ac97.90 ± 1.40 Aab8.05 ± 0.16 Aa0.28 ± 0.01 Aa*1.28 ± 0.11 Aa*
WD+Al+MeJA50−1.18 ± 0.16 Ac98.38 ± 0.52 Aab8.19 ± 0.17 Aa0.27 ± 0.01 Aa*1.29 ± 0.03 Aa*
WD+Al+MeJA100−0.75 ± 0.09 Ab*94.79 ± 2.66 Ab8.17 ± 0.17 Aa0.26 ± 0.02 Aa1.27 ± 0.04 Aa*
21 daysControl−0.55 ± 0.05 Ba96.79 ± 1.33 Aa8.20 ± 0.14 Aa0.28 ± 0.02 Aa*1.26 ± 0.06 Aa*
WD+Al−1.65 ± 0.05 Bb*86.92 ± 2.93 Bb*8.15 ± 0.11 Aa*0.29 ± 0.01 Aa*1.25 ± 0.03 Aa*
WD+Al+MeJA10−2.42 ± 0.25 Bc*97.03 ± 4.65 Aa8.14 ± 0.08 Aa0.28 ± 0.01 Aa1.26 ± 0.03 Aa*
WD+Al+MeJA50−2.32 ± 0.10 Bc*93.68 ± 2.98 Aa*8.19 ± 0.06 Aa0.28 ± 0.02 Aa*1.26 ± 0.03 Aa*
WD+Al+MeJA100−1.08 ± 0.19 Bb*94.76 ± 2.71 Aa8.12 ± 0.05 Aa*0.27 ± 0.01 Aa1.26 ± 0.02 Aa*1
1 Each value represents the mean ± SD of five replicates per treatment. Lowercase letters indicate significant differences (p ≤ 0.05) between treatments within the same harvest time and cultivar, uppercase letters indicate significant differences (p ≤ 0.05) between harvest times for each cultivar within the same treatment, and * represents significant differences (p ≤ 0.05) between cultivars within the same treatment and harvest time, according to Tukey’s test.
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Cáceres, C.; Cazor-Curilef, C.; Delgado-Santibañez, P.; Machado, M.; Delgado, M.; Ribera-Fonseca, A.; Inostroza-Blancheteau, C.; Bravo, L.A.; González-Villagra, J.; Nunes-Nesi, A.; et al. Foliar Methyl Jasmonate Application Activates Antioxidant Mechanisms to Counteract Water Deficits and Aluminum Stress in Vaccinium corymbosum L. Horticulturae 2024, 10, 1172. https://doi.org/10.3390/horticulturae10111172

AMA Style

Cáceres C, Cazor-Curilef C, Delgado-Santibañez P, Machado M, Delgado M, Ribera-Fonseca A, Inostroza-Blancheteau C, Bravo LA, González-Villagra J, Nunes-Nesi A, et al. Foliar Methyl Jasmonate Application Activates Antioxidant Mechanisms to Counteract Water Deficits and Aluminum Stress in Vaccinium corymbosum L. Horticulturae. 2024; 10(11):1172. https://doi.org/10.3390/horticulturae10111172

Chicago/Turabian Style

Cáceres, Cristina, Crystal Cazor-Curilef, Patricio Delgado-Santibañez, Mariana Machado, Mabel Delgado, Alejandra Ribera-Fonseca, Claudio Inostroza-Blancheteau, Leon A. Bravo, Jorge González-Villagra, Adriano Nunes-Nesi, and et al. 2024. "Foliar Methyl Jasmonate Application Activates Antioxidant Mechanisms to Counteract Water Deficits and Aluminum Stress in Vaccinium corymbosum L." Horticulturae 10, no. 11: 1172. https://doi.org/10.3390/horticulturae10111172

APA Style

Cáceres, C., Cazor-Curilef, C., Delgado-Santibañez, P., Machado, M., Delgado, M., Ribera-Fonseca, A., Inostroza-Blancheteau, C., Bravo, L. A., González-Villagra, J., Nunes-Nesi, A., & Reyes-Díaz, M. (2024). Foliar Methyl Jasmonate Application Activates Antioxidant Mechanisms to Counteract Water Deficits and Aluminum Stress in Vaccinium corymbosum L. Horticulturae, 10(11), 1172. https://doi.org/10.3390/horticulturae10111172

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