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Article

Physiological and Biochemical Responses of Apple (Malus domestica Borkh.) to Biostimulants Application and Substrate Additives under Salinity Stress

by
Louloudia Koulympoudi
1,*,
Christos Chatzissavvidis
1 and
Anastasia Evripidis Giannakoula
2
1
Laboratory of Pomology, Vegetable Crop Production and Floriculture, Department of Agricultural Development, Democritus University of Thrace, 68200 Orestiada, Greece
2
Laboratory of Plant Physiology, Department of Agriculture, International Hellenic University, Sindos, 54700 Thessaloniki, Greece
*
Author to whom correspondence should be addressed.
Appl. Sci. 2023, 13(3), 1290; https://doi.org/10.3390/app13031290
Submission received: 29 November 2022 / Revised: 15 January 2023 / Accepted: 16 January 2023 / Published: 18 January 2023
(This article belongs to the Section Food Science and Technology)
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Abstract

:
The issue of high concentration of salt in soil is not restricted to coastal areas, but also expands to cultivated lands, complicating, or even intercepting, the growth of plants. The objective of this paper is to study the effect of zeolite, compost and effective microorganisms (EM), seaweed extract, and ceramic powder on MM106 apple (Malus domestica Borkh.) plants in normal and saline conditions. More specifically, the weight of the dry matter of the plants, physiological parameters, proline, carbohydrate, carotenoid, phenolic, and flavonoid concentrations in leaf tissues and antioxidant capacity were determined. At the end of the experiment, it was ascertained that the plants of the treatments which included zeolite or EM exhibited the highest dry matter weight of the leaves in normal (5.07 g and 4.68 g, respectively) and saline conditions (4.14 g and 3.02 g, respectively), while the leaf dry weight in the control treatment was 4.37 g in the absence and 2.34 g in the presence of NaCl. Furthermore, these treatments resulted in significantly higher proline concentration in plant leaves under salinity with values of 5.63 in the EM treatment, 2.44 in the zeolite treatment, and 0.75 μmol/g of leaf fresh weight in the control. At the same time, the application of ceramic powder in combination with effective microorganisms led to the highest rate of photosynthesis in salinity conditions (12.8 μmol CO2/m2s), while the seaweed extract spraying was associated with low stomatal conductance in all treatments (0.09–0.13 mol H2O/m2s). Overall, the application of effective microorganisms appeared to associate more with plant vigor in both normal and salinity conditions. In this context, the implementation of EM could improve the growth of potted plants, but it could also be used in orchards before and after their establishment.

1. Introduction

Salinity constitutes a severe constraining factor of plant growth since it is associated with a combination of osmotic, ionic and, secondarily, oxidative stress [1]. Various undesirable effects appear because of high salt concentration. Salt stress alters the structure and composition of cell plasma membrane, especially lipid and protein contents, as well as cell plasma membrane cytoplasmic viscosity and composition [2,3]. Moreover, ion imbalance is one of the major consequences. A high concentration of Na and Cl ions, as an example, can lead to biochemical processes which can prove to be fatal for the plants [4,5,6]. Sodium and chloride toxicity not only induce nutritional disorders but also cause physiological drought by lowering the osmotic potential of the soil solutions [7]. Soil salinity prevents the plant from taking up water from the soil, resulting in a decline in cellular water, thus affecting cell turgor. Soil salinity also adversely affects photosynthetic activity in the plant and encourages the production of reactive oxygen species (ROS), thus reducing plant growth [8,9]. Gas exchange is inversely related to the concentration of Na and Cl ions [10,11], and parameters such as photosynthesis, stomatal conductance, and transpiration tend to be negatively influenced by saline treatments [12,13]. Moreover, higher salt levels are also known to alter photosynthesis via non-stomatal limitations, including variations in photosynthetic enzyme activity and changes in the concentration of chlorophyll and carotenoids [14,15,16].
In parallel, soil salinization evolves into a crucial matter which leads to land degradation [17], while there are estimations that about 20% (45 million ha) of irrigated land worldwide is affected by salinity [18]. Consequently, large areas are kept out of the production process rendering the necessity to improve this situation of vital meaning for the survival of the rapidly increasing population of Earth [19].
Temperate fruit trees, including apples, are salt-sensitive plants [20]. Apple cultivation under salt stress may result in a decline of fruit yield and quality. Several researchers suggest that salt stress impedes apple plant growth by decreasing water uptake, inhibition of photosynthesis, and by closing stomatal apertures [21,22].
Various strategies have been proposed in order to moderate the negative impact of problematic soils on plant cultivation, such as the use of biostimulants and soil amendments (substrate additives). According to Du Jardin [23], “a plantbiostimulant is any substance or microorganism applied to plants with the aim to enhance nutrition efficiency, abiotic stress tolerance and/or crop quality traits, regardless of its nutrients content”. Thus, photosynthetic bacteria have been extensively used in agriculture to improve plant growth and production quality [24], while it has been found that spraying Rhodopseudomonas palustris GJ-22 strain on tobacco leaves can protect plants from tobacco mosaic virus infection [25]. Other microorganisms, such as plant growth promoting bacteria (PGPB), also have the capacity to increase yield and reduce biotic and abiotic plant stress without conferring pathogenicity [26,27]. Additionally, products with lactic acid bacteria (LAB) are a common alternative in agricultural systems for improving soils and enhancing plant growth [28].
Regarding crop yield, seaweed extracts represent another perspective seeing that in many countries they are used as fertilizers [29]. It has been deemed that their effect derives from a combination of several constituents encompassing a number of macro- and micronutrients, plant growth regulators, and quaternary ammonium compounds [30,31], while many studies have shown that the implementation of seaweed extracts contributed to better crop performance and elevated resistance to abiotic stress [32]. In this direction, betaines contained in seaweed products serve as a compatible solute that alleviates osmotic stress of plants induced by salinity and drought stress [30]. Furthermore, the use of zeolite is a different approach to manage degraded soils. Soil amendments are generally used to improve conditions for plant growth [33]. Zeolites are hydrated aluminosilicates that are distinguished for their infinite three-dimensional structure of silicon tetraoxide (SiO4) and aluminum tetraoxide (AlO4) [10], their high ability to lose and gain water [34], and high cation-exchange capacity (CEC) [35]. Zeolites are considered to improve many soil physicochemical properties. They increase soil infiltration rate, saturated hydraulic conductivity, water holding capacity, aeration, and many others [34,36,37,38,39]. Various researchers reported that zeolite increases soil cation exchange capacity and water retention in the root zone [40,41], decreases mineral components leaching [37,42], and traps significant amounts of heavy metals and organic pollutants in contaminated soils [43,44]. Its use with fertilizers can help buffer soil pH levels, thus reducing the need for lime application [45,46]. Zeolites’ action as slow-release fertilizers are reported as well [34]. Unlike other soil amendments (e.g., lime), zeolite does not break down over time but remains in the soil to improve nutrient retention. Therefore, its addition to soil significantly reduces water and fertilizer costs by retaining beneficial nutrients in the root zone [36,47].
In parallel, an alternative strategy to decrease the oxidative damage on plants is to use silicon (Si) fertilization, the principal component of ceramic powder, in plants subjected to environmental stresses [48]. Therefore, Si has been shown to be able to improve early growth and establishment of plants under stressful conditions through increasing antioxidant enzymes, photosynthetic capacity, and low transpiration coefficient [49,50].
Currently, industrial agricultural practices are affecting the demotion of nodal ecological processes that maintain life on Earth, leading to climate change, loss of biosphere integrity, and destructive land system changes [51,52,53,54]. On the contrary, recent research has shown that agroecological farming systems based on the application of ecological principles to the design and management of agricultural ecosystems are capable of meeting global food needs sustainably and efficiently [54], whereas it has been demonstrated that beneficial microorganisms contribute to productivity improvement maintaining an ecological balance, especially where they help host plants to survive in arid environments [55]. The objective of this study was to investigate (i) the contribution of zeolite and effective microorganisms to the growth of apple plants under normal conditions and (ii) the possibility of compensating for the negative effects of salt stress on the growth of apple plants when using zeolite, effective microorganisms (Saccharomyces sp., photosynthetic and lactic acid bacteria), algal extract, and ceramic powder. The potential improvement of physiological and biochemical parameters of young plants exposed or not to salinity conditions by adding these inexpensive, abundant, and environmentally friendly materials as additives or substrates could be a significant benefit derived from the present study.

2. Materials and Methods

One-year-old, bare-rooted, decapitated at a height of 15 cm, apple Malling Merton 106 (Malus domestica Borkh.; MM106) plants were used. All lateral shoots were removed, and the plants were planted in 4 L plastic pots. The experiment was conducted at the Department of Agricultural Development of the Democritus University of Thrace, Orestiada (longitude: 26°31′, latitude: 41°29′), Greece, under natural lighting.
There were three substrate mixtures (treatments) derived from the application of different substrate additives in each treatment from the beginning of the experiment. More specifically, the substrate mixtures included: (i) sand + perlite (1:1—control), (ii) sand + perlite + zeolite (1:1:1—zeolite) and (iii) sand + perlite (1:1) + 100 mL compost (effective microorganisms, EM). All plants were irrigated with 0.2 L of Hoagland 50% nutrient solution modified as described by Chatzissavvidis et al. [56] every two days, except those of the treatment with compost and microorganisms. The plants of the treatment in question (3rd case) were irrigated with water, while every seven days they received 0.2 L of aqueous solution with photosynthetic bacteria, Saccharomyces sp. and lactic acid bacteria (effective micoorganisms). Every treatment was divided into four subtreatments: (I) no addition of NaCl, (II) addition of NaCl 50 mM, (III) NaCl 50 mM and seaweed extract spraying solution, and (IV) addition of NaCl 50 mM and ceramic powder (silica (SiO2) 80%, alumina (Al2O3) 20% and fermented by effective microorganisms) spraying. All subtreatments comprised four plant replicates each. The irrigation of the plants with NaCl and the application of the seaweed extract and the ceramic powder solution began 20 days after the establishment of the plants in the pots. Moreover, the plants received distilled water every 15 days to wash away salts. The experiment lasted 76 days until the first severe symptoms of salinity were observed (marginal necrosis of basal leaf blades).
At the end of the experiment, the weight of leaf, stem, and root dry matter was measured, while the relative growth rate was calculated based on the initial and finalheight of the plants. Additionally, the chlorophyll was determined in chlorophyll content index (CCI) units (Opti-Sciences, CCM-200, Hudson, NH, USA) in mature top leaves. In order to estimate the leaf concentration of carbohydrates, anthrone (9(10H)-Anthracenone) and sulfuric acid (H2SO4) were used, according to the Fales [57] method, while the measurement was carried out in a Shimadzu spectrophotometer at 625 nm. The concentration of proline in the leaves was determined by the acidic ninhydrin reaction assay, using the Bates et al. [58] method, and measurements were conducted photometrically at 518 nm. The rate of photosynthesis, the rate of transpiration, the stomatal conductance, and the internal CO2 concentration in the leaves were determined by a LC Pro+ device (ADC, Bioscientific Ltd., Hertfordshire, UK). Furthermore, phenols were extracted from 0.1 g of leaf fresh matter in 80% methanol, assayed using the Folin–Ciocalteu reagent following the method of Scalbert et al. [59,60], and expressed as mg of gallic acid equivalents (GAE) per g of leaf fresh weight (FW), which was used for standard curve with a range of 0–125 μΜ. Flavonoids were extracted from 0.3 g of fresh matter in 80% methanol and determined colorimetrically [61] with some modifications. Rutin was used as the standard compound for the quantification of total flavonoids. All values were expressed as mg of rutin fresh matter weight (FW). The reported data are the means of four replicates. In order to determine antioxidant capacities in apple plants, two methods were used: (i) 2,2-diphenyl-1-picryl hydrazil (DPPH) [62] and (ii) ferric reducing antioxidant potential (FRAP) [63].
The JMP 8 (SAS Institute) and IBM SPSS Statistics 21 statistical softwarewere used for the statistical processing of the data. All data were subjected to analysis of variance (ANOVA) and presented as treatment means ± standard error (SE), while Tukey’s and Duncan’s tests were used.

3. Results

The measurements of the dry matter weight (DW) of plants which were carried out at the end of the experiment showed that the corresponding values differ among the treatments (Table 1). In general, the leaf DW reached the highest values when no NaCl was added in all treatments and it was lower in the corresponding control subtreatment (I). On the other hand, irrigation with NaCl led to the decline of the parameter in question, whereas the statistically significantly lowest value was found in the control subtreatment in which only NaCl was added (II). It is noteworthy that the application of the ceramic powder or the seaweed extract spray solution on the plants of the control subtreatments, which were irrigated with NaCl (IV and III, respectively), favored the leaf DW, contributing to the reduction in the statistically significant differences. In contrast, NaCl irrigation did not cause a significant reduction in leaf dry matter weight compared with normal conditions in the zeolite treatment, while no significant changes in leaf DW were observed when plants in this treatment were sprayed with seaweed extract (III) or ceramic powder (IV). In the EM treatment, salinity negatively affected leaf DW leading to a statistically significantly lower value compared with the subtreatment in which plants were not irrigated with NaCl (I). However, the spraying with seaweed extract of plants and the application of the ceramic powder spray solution in the subtreatments III and IV of the EM treatment favored the leaf DW, ranking its values at the same level as in normal conditions. Overall, both zeolite and the combination of compost and effective microorganisms had a statistically significant positive effect on leaf DW under salinity conditions compared with the corresponding control subtreatment (II). In addition, spraying with algal extract (III) or ceramic powder (IV) favored leaf dry matter weight in the presence of salinity in the zeolite or EM treatments leading to significantly higher values than those of the corresponding control subtreatments (Table 1).
Regarding the shoot DW, it did not show a statistically significant difference between the control and the other two treatments under normal conditions. Furthermore, the addition of salinity did not significantly alter the aforementioned parameter of the control (subtreatment II), but neither did spraying with algae or ceramic powder solution in the presence of salinity (III and IV). Irrigation with NaCl (II) resulted in a statistically significant decrease in shoot dry matter weight in the zeolite treatment compared with the value of this parameter in the absence of salinity (I). However, the application of the algal extract or the ceramic powder (III or IV) appeared to help bridge the difference, bringing the shoot DW back to higher values. At the same time, the subtreatment in which NaCl was administered, in the EM treatment, did not demonstrate a significant change in shoot DW compared with normal conditions. However, a decrease in shoot dry matter weight was found when plants were sprayed with seaweed extract in the presence of salinity (III), while spraying with ceramic powder solution (IV) had no significant effect on the value of the parameter (Table 1).
Furthermore, root DW showed the greatest values in the zeolite treatment and in the EM treatment in the absence of salinity compared with the control, although this fact was not accompanied by a statistically significant difference. Irrigation with NaCl and application of algal extract or ceramic powder in the presence of salinity did not cause significant changes in root dry matter weight both between and within treatments. An exception was the subtreatment III, in which the plants were sprayed with seaweed solution in the presence of salinity, in the EM treatment. In this subtreatment, the DW of the roots was significantly lower compared with that of the normal conditions subtreatment (I) (Table 1).
Overall, the presence of salinity affected the leaf DW of plants in the control treatment, but not the shoot or root DW, which did not show a significant difference due to salt addition. Both the addition of (i) zeolite and (ii) compost and effective microorganisms resulted in higher DW of leaves, shoots, and roots in normal conditions compared with the control. However, salinity conditions (II) were associated with statistically significantly lower shoot DW in the zeolite treatment and lower leaf DW in the EM treatment compared with normal conditions (I).
At the same time, the relative growth rate based on the initial and final height of the plants did not show statistically significant differences between and within the treatments. In this context, the relative growth rate of height ranged at similar levels in all treatments when NaCl was not administered to the plants. The addition of salt (II) contributed to the reduction in the aforementioned parameter in the control and in the EM treatment compared with normal conditions (I), while it was associated with an increase in the zeolite treatment. In addition, the subtreatment that included spraying the plants with algal solution in the presence of salinity (III) showed a greater relative height growth rate than the subtreatment in which plants received only NaCl (II) in the control treatment and the EM treatment, while the zeolite treatment had a lower rate. The application of ceramic powder appeared to have a positive effect on the relative growth rate of height compared with its values in subtreatment II of the control and EM treatments (Table 1).
The photosynthesis parameters also varied considerably depending on the treatment (Figure 1). Regarding the photosynthesis rate, the diverse substrate additives in normal conditions or the presence of salt, compared with normal conditions, did not provoke any statistically significant differences (Figure 1a). On the other hand, the application of the seaweed extract or the ceramic powder solution with the simultaneous administration of NaCl led to fluctuations of the photosynthesis rate, although not statistically significant in all treatments. Thus, the seaweed extract spraying contributed to statistically significantly lower photosynthetic rates in all treatments, with the lowest photosynthetic activity occurring in the subtreatment with zeolite, NaCl, and the seaweed extract solution (zeolite treatment—subtreatment III). The statistically significantly highest value was observed in the plants subjected to the combination of the compost, microorganisms, and ceramic powder spray solution under saline conditions (EM treatment—subtreatment IV). In contrast, in the subtreatment in which ceramic powder was applied (IV), the photosynthetic rate was maintained at similar levels to those of normal conditions in the control treatment; it was statistically significantly lower in the zeolite treatment, while it showed a significantly higher value in the EM treatment (Figure 1a).
The inclusion of zeolite in the substrate affected stomatal conductance, seeing that the statistically significantly highest value was noted in the respective treatment in normal conditions. On the other hand, when plants received compost and microorganisms, the stomatal conductance showed significantly lower values in the absence of salinity. However, the presence of NaCl was not associated with lower stomatal conductance in this experiment since no significant differences in stomatal conductance were recorded between normal and salinity subtreatments in any treatment. Conversely, the algal spraying (III) or the application of the ceramic powder spray solution (IV) led to significantly lower values of the aforementioned parameter in the control or zeolite treatments. The application of algae solution or ceramic powder had no apparent negative effect on the stomatal conductance of the EM-treated plants (Figure 1b).
At the same time, the transpiration rate was higher in the zeolite treatment and in the EM treatment compared with the control under normal conditions. Administration of NaCl contributed to an increase in the transpiration rate in all treatments, but was not associated with significant differences between treatments. In addition, the subtreatment in which plants were sprayed with algal extract in the presence of salinity (III) showed similar transpiration rates in all treatments, which were also not significantly different from the corresponding subtreatments in which plants were given NaCl only (II). The control subtreatment in which the plants had ceramic powder applied in the presence of salinity (IV) showed a significantly higher transpiration rate compared with the normal conditions subtreatment (I), but a similar difference was not found in the other two treatments (Figure 1c).
As far as the concentration of internal CO2 is concerned, there were no significant differences among the treatments in normal conditions and between normal and saline conditions in all treatments. The implementation of seaweed extract under salinity (III) had a positive effect on the internal CO2 concentration in all treatments, while the application of ceramic powder (IV) was associated with a significantly lower concentration of CO2 compared with normal conditions in zeolite treatment (Figure 1d).
In general, proline concentration ranged at a similar statistical level among the plants of all treatments in normal conditions, although the plants in the EM treatment had the lower concentration (Table 2). The administration of NaCl alone (II) led to a decrease in proline concentration in the control treatment, while in the other two treatments proline concentration in the presence of salinity increased. In fact, the corresponding subtreatment (II) in the EM treatment demonstrated a statistically significantly higher concentration of proline compared with all the subtreatments of control or zeolite treatment. In the subtreatments in which either seaweed extract or ceramic powder solution was applied to the plants (III or IV), an increase in proline concentration was observed in the control, but in the zeolite and EM treatments, a decrease in proline concentration was found in the aforementioned subtreatments. However, the plants of the effective microorganisms treatment, when sprayed with algal solution with simultaneous salt administration, showed a higher proline concentration compared with the corresponding subtreatments of the other treatments.
The concentration of carbohydrates in leaves did not display significant differences among the treatments (Table 2). The carbohydrate concentration was heightened in the presence of salt (II) in the control treatment but it was diminished in the respective subtreatment when zeolite was implemented as a substrate additive. On the contrary, the combination of compost and microorganisms led to consistent carbohydrate concentrations in both normal and saline conditions. Moreover, the spraying with the algal extract (III) provoked shrinkage to the carbohydrate content of leaves, while the ceramic powder spray solution (IV) resulted in higher values, compared with the application of seaweed solution, in all cases.
In order to estimate antioxidant capacities in apple plants, both the 2,2-diphenyl-1-picryl hydrazil (DPPH) method [62] and the ferric reducing antioxidant potential (FRAP) method [63] were used. The first method showed that there were statistically significant differences in antioxidant capacity among the treatments (Figure 2a). In the subtreatments where no NaCl was administered to the plants (I), no significant differences were recorded in the antioxidant capacity between the various treatments, and also no differences were found in the sub-treatments where only NaCl was administered (II). Nevertheless, the antioxidant capacity of plants was lower in normal conditions than when the irrigation with salt took place in all substrate additives, while in the case of zeolite the aforementioned parameter reached the highest value. However, the application of seaweed extract under saline conditions overturned the previous picture, leading to the statistically significantly lowest antioxidant capacities in zeolite and in the EM treatment.
The antioxidant capacity did not demonstrate any significant fluctuations when it was assessed with the ferric reducing antioxidant potential (FRAP) method. The highest value was recorded in plants that were grown in zeolite under saline conditions (Figure 2b).
Furthermore, no significant variations were observed in the concentration of phenolic compounds in the leaves among the treatments in this study (Figure 2c). The phenolic concentration ranged at the same level in all substrate additives without NaCl (I). Nonetheless, the addition of salt (II) brought about a decline in phenols in the control treatment, while a rise in these compounds occurred in the zeolite treatment. Irrigation with NaCl slightly increased the concentration of phenolics in the subtreatment with compost and microorganisms. In the meantime, the implementation of seaweed extract solution under saline conditions (III) improved the content of phenols compared with the administration of NaCl alone (subtreatment II) in the control and EM treatment.
The concentration of flavonoids in leaves did not present statistically significant differences (Figure 2d). Plants in the control treatment displayed the lowest flavonoid concentration in normal conditions (I), but the addition of NaCl (II) increased the corresponding value. In contrast, the plants which received NaCl in the treatment with the combination of compost and microorganisms had a lower content of flavonoids compared with those which were grown without NaCl. Furthermore, the spraying with the seaweed extract solution (III) caused a reduction in flavonoid concentration in the control treatment, while it did not significantly change the concentration of flavonoids in the other two treatments.
The determination of the concentration of carotenoids revealed that the irrigation with salt and the different biostimulants and substrate additives affected this parameter in a variety of ways (Table 2). In normal conditions, the control plants demonstrated the lowest carotenoid concentration compared with the other treatments. The addition of NaCl (II) in the control treatment improved the carotenoid concentration, driving it close to the highest values. Simultaneously, the presence of NaCl significantly decreased the carotenoid concentration in the respective subtreatment of zeolite treatment, while there were not any notable fluctuations between normal and saline conditions in the EM treatment. However, despite any differences in carotenoids induced by NaCl administration within treatments, no significant differences were observed between treatments when plants were grown in saline conditions. Furthermore, it was ascertained that the implementation of the seaweed extract in the presence of NaCl (III) was to the detriment of the carotenoid concentration in the zeolite and EM treatments, whereas the last case showed the statistically significantly lowest value. On the other hand, the ceramic powder spraying of the plants (subtreatment IV) related to an augmentation of the carotenoid concentration compared with the application of seaweed solution in all treatments.

4. Discussion

Soil salinity stresses plants either because high concentrations of salts in the soil make it difficult for roots to extract water or because high concentrations of salts within plants can be toxic [64]. In this study, salinity resulted in lower leaf dry matter weight compared with normal conditions in the control treatment, but not lower shoot and root DW or relative growth rate of apple plants in terms of height. A rise in the salinity of soil is connected with a decreased rate of leaf growth owing to the osmotic effect of salt in the rhizosphere and consequently, leaf cells lose water. However, the loss of cell volume and turgor is transient, since these properties recur due to osmotic adjustment within hours, a finding which is not valid for cell elongation rates [65,66,67]. Decreases in cell elongation and cell division lead to a slower leaf emergence and a smaller final size over time [64].
At the same time, in the present experiment, no statistically significant differences in photosynthetic parameters were found between salinity and non-salinity conditions in the control treatment. Stable photosynthesis rates per unit leaf area in plants treated with salt is a frequent occurrence, whereas the changes in cell anatomy, the emergence of smaller, thicker leaves, and the resulting higher chloroplast density per unit leaf area could provide a possible explanation [68]. Petridis et al. [69] showed that mild water deficits had no effect on leaf gas exchange parameters in olive trees and, hence, suggested that their photosynthetic apparatus is very resistant to the stress in question. Pezeshki et al. [70] also concluded that the leaf internal CO2 concentrations in flooded Taxodium distichum seedlings remained relatively unchanged by different salt concentrations in the floodwater, despite reductions in stomatal conductance and photosynthesis.
Organic solutes that are compatible with metabolic activity, even at high concentrations, accumulate in the cytosol and organelles, in order to compensate for the osmotic pressure of the ions of Na and Cl, which are confined in the vacuole in plants exposed to saline conditions [71,72]. The compounds that have been associated with abiotic stress conditions and accumulate most commonly in plant tissues are sucrose, proline, and glycine betaine [64,73,74]. In plants under water deficit, proline often acts as an osmoprotectant that protects enzymes and proteins from denaturation [75]. However, in our study, a slight decrease, although not statistically significant, in proline concentration was observed in plants exposed to salinity compared with those grown under normal conditions in the control treatment.
In glycophytes, the concentrations of the accumulating compatible solutes are in the order of 10 mM, on a tissue water basis. However, their potential compartmentalization exclusively to the cytoplasm could cause a significant osmotic pressure and an osmolyte function [64]. In parallel, it is considered that the compatible solutes either contribute to the conservation of the tertiary structure of proteins or function as osmoprotectants at low concentrations [76]. Nevertheless, the concentration of carbohydrates in leaves did not display significant differences among the treatments in our experiment, which complies with the assumption that some plants can adapt to salinity if exposed to low concentrations of salt. Casas et al. [77] found that unadapted to salt, Atriplex nummularia cell cultures showed a dose-dependent inhibition of DW increase in the presence of 50–350 mM NaCl, and cells adapted to 342 or 428 mM NaCl were capable of sustained growth in the presence of salt.
In parallel, the dwindling leaf area, which is associated with exposure to salinity, entails that the photosynthesis capability per plant is reduced resulting in a rise in the formation of reactive oxygen species (ROS) and of the activity of the respective detoxifying enzymes [78,79]. Thus, the process of acclimation to stress conditions leads the plants to adjustments regarding leaf morphology, chloroplast pigment composition, and the activity of biochemical processes that prevent photosystems from oxidative damage [64]. Moreover, it is accepted that several environmental conditions, such as drought [80] and salinity [81], which engender oxidative stress in plants, are connected with the induction of phenylpropanoid metabolism, a finding that mirrors the role of phenolics in protecting the cells under the aforementioned abiotic stress conditions [82]. Additionally, flavonoids are regarded as photosynthetic apparatus protectants as they partly prevent DNA from the harmful effects of UV radiation [83,84], while carotenoids constitute a factor of the antioxidant mechanism, which coordinates a plant’s defense against ROS composed under stress conditions [85]. In the present work, a slight increase in antioxidant capacity estimated with the DPPH method and carotenoid concentration of the control plants grown under salinity conditions was found compared with normal conditions, but no increase in phenolic, flavonoid, and antioxidant capacity estimated with the FRAP method were observed. Salt stress is thought to be one of those important factors which restrict the development of apple in some regions. However, salt tolerance of some apple rootstocks was previously evaluated and showed large differences among species [21].
Regarding the addition of zeolite to the substrate, it was associated with higher values of leaf, stem, and root DW, transpiration rate, stomatal conductance and internal CO2 concentration, carotenoid concentration, and antioxidant capacity assessed with the DPPH method in the apple plants of zeolite treatment grown in the absence of salinity compared with the corresponding control plants, although there was not in all cases a statistically significant difference. Noori et al. [86] concluded that the application of zeolite in normal soil improved its ability to retain nutrients in the root zone without affecting its ability to drain, while previous research has shown that the use of zeolite in normal conditions contributed to a higher root DW of bean plants [87]. Gül et al. [88], also, observed that zeolite exceeded perlite, since the first increased the growth of crisp-head lettuces.
In addition, when plants grown under salinity conditions of the zeolite and the control treatment were compared, it was found that the application of zeolite contributed to greater leaf DW, relative growth rate, transpiration rate, proline concentration, phenolic concentration, and antioxidant capacity when measured by the DPPH or FRAP method, but not always with significant difference. Zeolite, due to its structure rich in micropores and physicochemical properties, can act as a trap for positive cations, such as ammonium and potassium [86]. At the same time, Na+ and Cl− ions can be absorbed in the network of cavities, which helps the improvement of soil properties. Thus, with the use of zeolite, both the improvement of soil fertility and the gradual release of nutrients are achieved [86]. In this direction, Aboul-Magd et al. [89] reported a positive effect of zeolite application on maize plants grown under saline conditions, as plant nutrient uptake was improved, while Al-Busaidi et al. [90] found that zeolite led to a substantial increase in barley biomass when plants were exposed to salinity. In addition, Al-Busaidi et al. [90] noticed that zeolite enhanced the water and salt holding capacity of soil. During the growth of plants in salinity conditions, zeolite on the one hand significantly increases the availability of nitrogen in plants, thereby enhancing the synthesis of chlorophyll, antioxidant enzymes, and other structural components of the plant and, on the other hand, significantly contributes to increasing the relative water content of stressed plants by increasing water availability and its uptake by roots [91]. Zeolite application has been reported to reduce leaf senescence in salinity-stressed sorrel plants by increasing leaf chlorophyll content and reducing its degradation [92]. The implementation of zeolite can also indirectly enhance the photosynthetic rate of stressed plants, as it improves water and nutrient availability owing to its high adsorption capacity [93]. In our study, zeolite did not seem to have any positive effect on shoot and root DW, carotenoid concentration, photosynthetic parameters, and carbohydrate and flavonoid concentrations under saline conditions.
The application of compost combined with the administration of effective microorganisms contributed to a higher root DW, transpiration rate, carotenoid concentration, and antioxidant capacity compared with the control under normal conditions. Previous research has shown that LAB, as biofertilizers, can improve nutrient availability from compost and other organic material, while PGPB increase nutrient uptake and plant biomass production [94]. Most composts are presumed to provide a “warm” growing medium, which promotes root growth [95]. Several previous studies have shown that inoculation with photosynthetic bacteria can increase plant production [96]. Purple non-sulfur bacteria (PNSB), a major group of photosynthetic bacteria containing Rhodopseudomonas spp. and Rhodobacter spp. [97], are able to transform atmospheric molecular nitrogen into ammonia (NH3) or ammonium (NH4+) with a specific nitrogenase enzyme, thereby making this nitrogen available for absorption by plants [98,99]. Furthermore, PNSB has been reported to improve the nitrogen use efficiency of plants [100].
At the same time, the EM treatment apple plants grown in the presence of salinity showed higher leaf DW, proline concentration, concentration of phenolic compounds, and antioxidant capacity assessed with the DPPH method compared with the corresponding control plants, while the combination of compost and effective microorganisms did not appear to induce a significant increase in shoot and root DW, relative height growth rate, and carotenoid, carbohydrate, and flavonoid concentrations, and photosynthetic parameters of plants exposed to NaCl. Plant biostimulants are considered as one of the most promising and efficient strategies for maintaining yield stability [101]. In this context, many PNSBs, such as Rhodopseudomonas palustris, Rhodobacter sphaeroides, and Rhodovulum sp. have been identified as potential 5-aminolevulinic acid (5-ALA) producers [102,103,104], which is abundant in bacteria, algae, plants, and constitutes a plant growth regulator and confers tolerance to plants of various abiotic stresses [105]. On account of the additional nutrient release from the disintegrating organic components, the resistance to abiotic stresses could be amplified with the use of organic ingredients in growing media [95]. Moreover, it has been noted that LAB, as biostimulants, are in a position to directly promote the alleviation of various abiotic stresses [28]. Several strains of plant-growth-promoting bacteria, such as Burkholderia [106], Arthrobacter, and Bacillus [107] amplify proline synthesis in stressed plants, which conduces to preserving the cell water status, contributing in this way to the plant coping with the saline conditions [108]. The stabilization of the cell environment, as far as pH is concerned, and the maintenance of antioxidant activity through the removal of reactive oxygen species (ROS) by proline, could improve the activity of various enzymes [109].
Spraying plants with algal extract under salinity generally favored leaf dry matter weight, relative plant growth rate, internal CO2 concentration, and phenolic concentration. On the grounds that liquid fertilizers deriving from seaweeds through the extraction method exhibit a high content of organic matter, micro and macroelements, vitamins, fatty acids, and growth regulators, they are found to be superior to chemical fertilizers [110]. Since several polysaccharides present in seaweed extracts constitute effective elicitors of plant defense against plant diseases, marine algae can serve as an important source of such stimulants [30,111]. Ramkissoon et al. [112] noticed an increase in the total phenolic contents in tomato plants treated with seaweed extract, which could possibly be due to elicitor activity of the seaweed extract components. The Sargassum latifolium or Ulva lactuca algal extract has been associated with both the induction of antioxidant activity and the mitigation of the harmful effects of drought on the vegetative stage of Triticum aestivum. Hence, Kasim et al. [113] presumed that seaweed extracts compete against the consequences of drought directly with the activation of the antioxidative system and with the supply of phytohormones and micro-nutrients essential for wheat growth. In our study, the implementation of seaweed extract on apple plants exposed to salinity was not associated with significant enhancement of shoot and root dry weight, photosynthetic rate, transpiration rate, stomatal conductance, concentrations of proline, sugars, and carotenoids, concentration of flavonoids, and antioxidant capacity of plants grown under saline conditions in most cases.
The ceramic powder applied to the experimental plants consisted of 80% silicon and 20% aluminum, and was fermented with effective microorganisms. When ceramic powder was administered to plants, they showed improvement in their leaf and shoot DW, relative height growth rate, and carotenoid concentration under salinity conditions in almost all treatments. Silicon is considered a non-essential (or quasi-essential) element for plant growth [114], which contributes to plant vigor and resistance to abiotic stresses when added to the growth medium [115]. Previous studies have suggested that Si(OH)4 acts as a trigger for plants, priming defense responses, which are fully activated when the plant is exposed to stress [116]. It has also been hypothesized that it constitutes a second messenger by binding to the hydroxyl groups of the proteins involved in cell signaling [117]. Furthermore, two main processes have been proposed by which silicon contributes to plant resistance to stresses: (1) a physical and mechanical protection afforded by SiO2 deposits and (2) a metabolic response that triggers metabolic changes [116]. Silicon also enhances the tolerance to UV radiation either due to the protective effect of its deposits on the leaf epidermis [118] or due to the reduction of UVB damage to the membranes [119]. Moreover, it affects water relations in drought-stressed plants, as it induces the formation of a silica cuticle double layer under the leaf epidermis which reduces water losses through cuticular transpiration [120]. Recent research has demonstrated that Si is associated with the regulation of antioxidant enzymes [121], increase in synthesis of endogenous antioxidants leading to mitigation of oxidative stress [50], maintenance of net photosynthesis through the stabilization of chloroplast structures, PSII integrity, and increased pigment concentration [122,123] when plants are subjected to heavy metal treatment [116]. Something else worth noting is that since the ceramic powder had previously been fermented with photosynthetic bacteria, it would also bring products of their metabolism. Older studies have shown that the application of photosynthetic bacteria enhanced the carotenoid content of citrus, spinach, and tomato plants [96], which could be related to the enhancement of photosynthetic pigments derived from indole-3-acetic acid (IAA) produced by PGPR [124,125].
Simultaneously, in the present experiment, ceramic powder did not contribute to the increase in root DW, proline and carbohydrate concentrations, and photosynthetic parameters when plants were exposed to salinity conditions, with the exception of the photosynthetic rate in the active EM treatment and transpiration rate in the control treatment. As mentioned above, IAA produced by PGPR improves photosynthetic parameters and alleviates the abiotic stress of plants, such as that due to drought and saline [124,125]. Miao et al. [126] reported that foliar spraying of PNSB under low temperatures improved the chlorophyll content and photosynthetic rate in yellow-skinned watermelon, while it has also been observed that foliar inoculation with Rhodopseudomonas sp. ISP-1 may have improved net photosynthesis of stevia plants in pot experiments [127].
Finally, the treatment that appeared to associate more to the vigor of apple plants in both normal and salinity conditions was the combination of compost and effective microorganisms. The application of EM contributed to the improvement of the dry weight of the plants in normal conditions compared with the control plants, while at the same time it led to higher dry weights of the plants in salinity conditions compared with the other two treatments, offering growth stability in the studied salinity regimes. In addition, this treatment was characterized by consistently high concentrations of carotenoids, proline, carbohydrates, and phenolic substances, which did not occur to the same extent in the other two treatments. Moreover, in the apple plants of the EM treatment exposed to salinity conditions, a lower stomatal conductance was observed compared with the control and zeolite treatment, while, in parallel, the photosynthesis rate did not show a significant difference from the aforementioned treatments.

5. Conclusions

The results of the present study show that the application of zeolite or effective microorganisms contributed to the improvement of plant growth in both normal and salinity conditions, while the findings after spraying with algal extract or ceramic powder when NaCl was added were similar. Photosynthesis rate, stomatal conductance, and internal CO2 concentration did not show a significant difference between normal and saline conditions, but the application of seaweed extract or ceramic powder caused significant variations among treatments. Effective microorganisms and zeolite resulted in a significantly higher proline concentration compared with the control with the addition of NaCl. Furthermore, the application of zeolite improved the antioxidant capacity of plants under salinity conditions, while spraying with ceramic powder led to a higher concentration of carotenoids compared with the algal extract. The application of effective microorganisms contributed to a greater stability of plant growth in both normal and saline conditions.

Author Contributions

Conceptualization, L.K.; methodology, L.K., C.C. and A.E.G.; software L.K., C.C. and A.E.G.; validation, L.K., C.C. and A.E.G.; formal analysis, L.K., C.C. and A.E.G.; investigation, L.K., C.C. and A.E.G.; resources, L.K., C.C. and A.E.G.; data curation, L.K., C.C. and A.E.G.; writing—original draft preparation, L.K. and C.C.; writing—review and editing, L.K. and C.C.; data interpretation and valuable insights, L.K., C.C. and A.E.G.; supervision, C.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are available on request.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 13 01290 g001a 550Applsci 13 01290 g001b 550
Figure 1. (a) Photosynthesis rate, (b) stomatal conductance, (c) transpiration rate, and (d) internal CO2 concentration in leaves of the apple plants. All the values are averages of four replications ± standard error. The different letters in the same column show statistically significant differences among the twelve subtreatments according to the Duncan test (p ≤ 0.05) with the larger values corresponding to the letter “a”. I: no NaCl, II: NaCl 50 mM, III: NaCl 50 mM + seaweed extract spraying, IV: NaCl 50 mM + ceramic powder spraying. EM treatment included compost addition.
Figure 1. (a) Photosynthesis rate, (b) stomatal conductance, (c) transpiration rate, and (d) internal CO2 concentration in leaves of the apple plants. All the values are averages of four replications ± standard error. The different letters in the same column show statistically significant differences among the twelve subtreatments according to the Duncan test (p ≤ 0.05) with the larger values corresponding to the letter “a”. I: no NaCl, II: NaCl 50 mM, III: NaCl 50 mM + seaweed extract spraying, IV: NaCl 50 mM + ceramic powder spraying. EM treatment included compost addition.
Applsci 13 01290 g001aApplsci 13 01290 g001b
Applsci 13 01290 g002a 550Applsci 13 01290 g002b 550
Figure 2. (a) DDPH, (b) FRAP, (c) phenolic compounds, and (d) flavonoid concentration in leaves of the apple plants. All the values are averages of three replications ± standard error. The different letters in the same column show statistically significant differences among the nine subtreatments, according to the Tukey test (p ≤ 0.05) with the larger values corresponding to the letter “a”. I: no NaCl, II: NaCl 50 mM, III: NaCl 50 mM + seaweed extract spraying. EM treatment included compost addition.
Figure 2. (a) DDPH, (b) FRAP, (c) phenolic compounds, and (d) flavonoid concentration in leaves of the apple plants. All the values are averages of three replications ± standard error. The different letters in the same column show statistically significant differences among the nine subtreatments, according to the Tukey test (p ≤ 0.05) with the larger values corresponding to the letter “a”. I: no NaCl, II: NaCl 50 mM, III: NaCl 50 mM + seaweed extract spraying. EM treatment included compost addition.
Applsci 13 01290 g002aApplsci 13 01290 g002b
Table
Table 1. Growth parameters of the apple plants at the end of the experiment.
Table 1. Growth parameters of the apple plants at the end of the experiment.
Treatments–Substrate AdditivesSub-
Treatments		Leaf DW (g)Stem DW (g)Root DW (g)Relative Growth Rate (Height–mm mm−1 d−1)
ControlI4.37 ± 0.36 ab14.93 ± 3.01 ab11.23 ± 1.66 ab0.0063 ± 0.002 a
II2.34 ± 0.16 d16.02 ± 2.47 ab13.19 ± 2.22 ab0.0033 ± 0.002 a
III3.51 ± 0.29 bc13.64 ± 2.90 ab11.00 ± 1.76 ab0.0063 ± 0.001 a
IV3.61 ± 0.24 bc15.59 ± 2.46 ab12.57 ± 2.85 ab0.0042 ± 0.001 a
ZeoliteI5.07 ± 0.55 a19.92 ± 3.19 a18.86 ± 4.32 a0.0055 ± 0.002 a
II4.14 ± 0.23 abc11.97 ± 1.39 b10.96 ± 2.14 ab0.0079 ± 0.001 a
III4.28 ± 0.03 ab13.25 ± 0.74 ab14.53 ± 1.50 ab0.0058 ± 0.002 a
IV4.57 ± 0.33 ab16.47 ± 1.59 ab11.77 ± 1.22 ab0.0064 ± 0.001 a
EMI4.68 ± 0.42 ab17.26 ± 0.95 ab18.32 ± 4.19 a0.0058 ± 0.002 a
II3.02 ± 0.60 cd15.14 ± 1.44 ab13.61 ± 0.96 ab0.0031 ± 0.001 a
III4.42 ± 0.44 ab12.28 ± 1.31 b9.56 ± 1.28 b0.0078 ± 0.001 a
IV3.99 ± 0.18 abc13.10 ± 1.30 ab11.73 ± 1.02 ab0.0051 ± 0.002 a
All the values are averages of four replications ± standard error. The different letters in the same column show statistically significant differences among the twelve subtreatments according to the test of Duncan (p ≤ 0.05) with the larger values corresponding to the letter “a”. I: no NaCl, II: NaCl 50 mM, III: NaCl 50 mM + seaweed extract spraying, IV: NaCl 50 mM + ceramic powder spraying. EM treatment included compost addition.
Table
Table 2. Proline, carbohydrate, and carotenoid concentration in leaves of the apple plants.
Table 2. Proline, carbohydrate, and carotenoid concentration in leaves of the apple plants.
Treatments–Substrate
Additives		Sub-TreatmentsProline
(μmol/g FW)		Carbohydrates (μmol/g FW)Carotenoids
(mg/g FW)
ControlI2.09 ± 0.82 bc59.97 ± 12.2 a564.13 ± 78.32 bcd
II0.75 ± 0.27 c69.20 ± 7.54 a687.04 ± 84.71 a–d
III1.07 ± 0.70 c43.56 ± 10.74 a687.78 ± 21.53 a–d
IV1.65 ± 0.55 bc57.66 ± 12.26 a823.88 ± 31.00 ab
ZeoliteI1.72 ± 0.45 bc71.97 ± 10.70 a847.60 ± 100.35 a
II2.44 ± 0.86 bc56.69 ± 12.73 a543.32 ± 79.53 cd
III1.33 ± 0.42 c39.45 ± 6.04 a524.13 ± 24.62 cd
IV1.09 ± 0.20 c59.21 ± 6.12 a736.79 ± 6.67 abc
EMI1.10 ± 0.39 c64.88 ± 2.96 a673.78 ± 47.16 a–d
II5.63 ± 0.54 a65.88 ± 12.76 a681.11 ± 18.51 a–d
III4.16 ± 0.63 ab48.34 ± 2.34 a430.80 ± 24.74 d
IV1.76 ± 0.30 bc55.48 ± 11.83 a602.32 ± 3.56 a–d
All the values are averages of three replications ± standard error. The different letters in the same column show statistically significant differences among the twelve subtreatments according to the Tukey’s test (p ≤ 0.05) with the larger values corresponding to the letter “a”. I: no NaCl, II: NaCl 50 mM, III: NaCl 50 mM + seaweed extract spraying, IV: NaCl 50 mM + ceramic powder spraying. EM treatment included compost addition.
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Koulympoudi, L.; Chatzissavvidis, C.; Giannakoula, A.E. Physiological and Biochemical Responses of Apple (Malus domestica Borkh.) to Biostimulants Application and Substrate Additives under Salinity Stress. Appl. Sci. 2023, 13, 1290. https://doi.org/10.3390/app13031290

AMA Style

Koulympoudi L, Chatzissavvidis C, Giannakoula AE. Physiological and Biochemical Responses of Apple (Malus domestica Borkh.) to Biostimulants Application and Substrate Additives under Salinity Stress. Applied Sciences. 2023; 13(3):1290. https://doi.org/10.3390/app13031290

Chicago/Turabian Style

Koulympoudi, Louloudia, Christos Chatzissavvidis, and Anastasia Evripidis Giannakoula. 2023. "Physiological and Biochemical Responses of Apple (Malus domestica Borkh.) to Biostimulants Application and Substrate Additives under Salinity Stress" Applied Sciences 13, no. 3: 1290. https://doi.org/10.3390/app13031290

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