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Article

Physiological Responses of Salinized Fenugreek (Trigonellafoenum-graecum L.) Plants to Foliar Application of Salicylic Acid

by
Reda E. Abdelhameed
1,*,
Arafat Abdel Hamed Abdel Latef
2,* and
Rania S. Shehata
1,3
1
Botany and Microbiology Department, Faculty of Science, Zagazig University, Zagazig 44519, Egypt
2
Department of Biology, Turabah University College, Turabah Branch, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia
3
Biology Department, Faculty of Science, Jazan University, Jizan 45142, Saudi Arabia
*
Authors to whom correspondence should be addressed.
Plants 2021, 10(4), 657; https://doi.org/10.3390/plants10040657
Submission received: 24 February 2021 / Revised: 23 March 2021 / Accepted: 29 March 2021 / Published: 30 March 2021
(This article belongs to the Special Issue The Role of Salicylic Acid in Mitigating Plant Stress and Its Application in Agriculture)
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Abstract

:
Considering the detrimental effects of salt stress on the physiological mechanisms of plants in terms of growth, development and productivity, intensive efforts are underway to improve plant tolerance to salinity. Hence, an experiment was conducted to assess the impact of the foliar application of salicylic acid (SA; 0.5 mM) on the physiological traits of fenugreek (Trigonella foenum-graecum L.) plants grown under three salt concentrations (0, 75, and 150 mM NaCl). An increase in salt concentration generated a decrease in the chlorophyll content index (CCI); however, the foliar application of SA boosted the CCI. The malondialdehyde content increased in salt-stressed fenugreek plants, while a reduction in content was observed with SA. Likewise, SA application induced an accumulation of proline, total phenolics, and flavonoids. Moreover, further increases in total free amino acids and shikimic acid were observed with the foliar application of SA, in either control or salt-treated plants. Similar results were obtained for ascorbate peroxidase, peroxidase, polyphenol oxidase, and catalase with SA application. Hence, we concluded that the foliar application of SA ameliorates salinity, and it is a growth regulator that improves the tolerance of fenugreek plants under salt stress.

1. Introduction

Abiotic stresses have been documented as the chief threat to agricultural efficiency all over the world. Anthropogenic activities in the developmental era have intensified the degradation of the agricultural system and its productivity due to the foremost abiotic stresses, such as extreme temperatures, salinity, drought, nutrients (deficiency and excess), metals/metalloids, and UV radiation [1,2,3,4], which can potentially influence almost all plant metabolic processes and which may negatively affect 70% of crops’ yields [5]. One of these abiotic stresses is salinity, which threatens the agricultural system and affects all physiological processes, from seed germination to plant development, leading to reduced growth and yield [6,7,8]. The detrimental effects of salinity on plant physiology are associated with specific low water potential in soil solution (drought stress), ion effects, nutritional disparities, forwarding of energy from growth to pull out pure water from the saline water and to create defensive chemicals, or a combination of these altered factors [9,10].
Sensitivity to salt stress is mainly due to oxidative stress, which arises from a disturbance of the balance between the production and elimination of reactive oxygen species (ROS) such as superoxide, hydrogen peroxide, and hydroxyl radicals [11]. Furthermore, lipids, specifically polyunsaturated fatty acids, are sensitive to deterioration by ROS, inducing changes in the structural and functional properties of the cells [12,13]. Previous studies have confirmed the accumulation of lipid peroxidation products in salt-stressed plants, and the leakiness of membranes [14,15].
Recently, great efforts have been exerted to increase the protective mechanisms of plants against salt stress. One of these promising efforts is the application of phytohormones, such as salicylic acid (SA), which is a phenolic phytohormone that acts as a signaling molecule [16]. SA plays an essential function in the regulation of seed germination and plant growth and development [17]. Ion uptake and transport, stomatal conductance, the photosynthetic rate, and transpiration [18,19] could also be affected by SA application. Exogenous SA application to stressed plants, either through seed soaking, adding to the nutrient solution, irrigation, or spraying, has been reported to augment stress tolerance-mechanisms [20,21] against metals [22], salinity [13], drought [23], and heat stress [24]. A direct physiological impact of SA is the modification of antioxidant enzyme actions to increase plant responses to these stresses [25]. Moreover, SA increases plant growth under salt stress, which could be attributed to considerable enhancement in the net photosynthetic rate [26]. El-khodary [27] observed a considerable enhancement in growth characteristics, pigment contents, photosynthetic rate, and carbohydrate content in maize sprayed with SA. Additionally, SA has been shown to ameliorate salt stress in seedlings of cucumbers [28] and cowpea plants [14].
With the purpose of improving whole-plant performance under amplified severity of salt stress, more information is required about the contribution of SA to salt stress tolerance in plants at the physiological level. Among the various plants tested, fenugreek (Trigonella foenum gracium L.) is an annual leguminous herb regarded as a multi-purpose crop, that is extensively cultivated in most regions of the world for its medicinal value [29]. The use of different parts of the fenugreek plant as flavoring agents, stabilizers, adhesives, or for cosmetics, papers, and paints has also been documented [30]. It is considered a salt-sensitive plant species which is harmfully affected by salt stress in terms of physiology and growth [31,32]. Therefore, this experiment aimed to determine whether exogenous SA application could convey salt tolerance to fenugreek plants at the physiological level, based on various biochemical parameters, osmolytes, and antioxidative enzymes.

2. Results

2.1. Chlorophyll Content Index

The results in Table 1 reveal that CCI decreased with increasing salt concentration; however, the foliar application of SA had prominent effects, and an increase in the CCI of fenugreek leaves was observed.

2.2. Total Soluble Carbohydrates

Table 1 shows carbohydrates accumulation in NaCl-treated fenugreek plants, compared to the control. Further accumulation of carbohydrates was detected in NaCl-treated and non-treated plants with foliar application of SA, but in salinized plants (75 and 150 mM NaCl) this accumulation was significantly higher relative to the control. Indeed, with SA application, a significant increase by 8.4% and 7.8% in carbohydrate content was observed in plants grown under 75 and 150 mM NaCl, respectively, as compared with salinized plants only.

2.3. Total Free Amino Acid Content

Figure 1A reveals a significant (p ≤ 0.05) increase in the total free amino acid content due to NaCl treatment and SA application, compared to control. Although salt stress increased the free amino acid content in fenugreek leaves, this increase was more conspicuous with SA application, realizing a maximum (7.920 mg g−1 DW) increase at 150 mM NaCl treatment over salinized plants only (5.999 mg g−1 DW).

2.4. Proline Content

The results in Figure 1B indicate that the proline content increased in response to NaCl stress, and the proline level was augmented with increasing salt concentration compared to control. Furthermore, with SA application, a significant increase (p ≤ 0.05) in proline content in salt-stressed fenugreek plants at the levels of 75 and 150 mM NaCl concentration was detected, when compared with their respective salinized plants only.

2.5. Total Phenolics and Flavonoids

The data of the total phenolic and flavonoid contents in the fenugreek leaves are shown in Figure 2. With increasing salt concentration, there was a considerable increase in total phenolic and flavonoid contents in the fenugreek leaves. Further increases in their contents were observed with SA application, in either control or salt-treated plants. For instance, at 150 mM NaCl, the total phenolic content was about 2-fold (4.716 mg g−1 DW) higher than that of the control (2.473 mg g−1 DW) due to SA spraying (Figure 2A). In plants challenged by 75 and 150 mM NaCl, the increases in the flavonoid content were 59.3% and 101%; these percentages were boosted by 65.3% and 122%, respectively, with SA application versus control in untreated plants only (Figure 2B).

2.6. Lipid Peroxidation

Results of the present study revealed significant changes in MDA content in salt-stressed fenugreek leaves, influenced by SA application (Figure 3A). It was noted that with SA application, MDA content was significantly lower than in non-SA applied plants. On the other hand, there was a significant (p ≤ 0.05) increase in MDA content with increasing salt concentrations. In non-SA applied plants, an increase by 93.6% and 173.9% in MDA content was observed at 75 and 150 mM NaCl, respectively. Conversely, a lower MDA content was detected with SA spraying (by 32.2% and 23.1%) at 75 and 150 mM, respectively, versus salinized plants only.

2.7. Shikimic Acid Content

Among the tested parameters observed under stress conditions, the highest fluctuations in values of shikimic acid content were observed as a response to salt treatment. The increase in shikimic acid content ranged from 0.553 to 0.589 mg g−1 DW at 75 and 150 mM NaCl, compared to control (0.487 mg g−1 DW, Figure 3B). Of particular note, a further increase in its content was observed with foliar application of 0.5 mM SA, either in control or salt-treated plants. However, in salt-treated plants, this enhancement was significantly greater relative to the control realizing 0.586 to 0.713 mg g−1 DW at 75 and 150 mM NaCl. Further, in terms of two-way ANOVA results (Table 2) for shikimic acid content in the leaves of fenugreek plants, significant changes were observed between salt, SA treatment, and their interactions.

2.8. Antioxidative Enzymes

Salt stress significantly induced an increase in the enzymatic antioxidant profiles of fenugreek leaves, including POD, CAT, PPO, and APX activities (Figure 4). Moreover, the application of SA significantly (p ≤ 0.05) improved their activities (Figure 4A–D), either in control or NaCl-stressed fenugreek plant leaves. Under normal conditions, SA application significantly increased APX and POD activities (by 27.6% and 53.5%, respectively) in comparison with control. At 150 mM NaCl, SA application significantly augmented the activities of POD, APX, and PPO in fenugreek leaves by 42.1%, 8.1% and 14.1%, respectively, as compared to NaCl-treated plants alone. Most interestingly, based on two-way ANOVA results (Table 2), significant differences were established among salt, SA treatment, and their interactions in the antioxidant enzymes of fenugreek plant leaves.

3. Discussion

Chlorophyll content is widely used as an indicator of abiotic tolerance in plants, as changes in chlorophyll content are linked to visual symptoms of plant illness and photosynthetic efficiency [33]. A decline in chlorophyll content in salt-applied fenugreek plants might be ascribed to the possible oxidation of chlorophyll and other chloroplast pigments, coupled with the instability of the pigment-protein complex under salt stress [34]. Similar results were obtained in cowpea plants by [14] and [35] under salt stress conditions. Reduction in the chlorophyll content can be reversed back to a similar level as the control by the foliar application of SA, which might account for the induction of Rubisco activity and synthesis of more carbohydrates in treated plants [24]. SA application may also inhibit the production and accumulation of ROS in plant tissues, which negatively affects the photosynthetic unit.
The increase in carbohydrate content in fenugreek plants grown in soil treated with 75 and 150 mM NaCl could be related to the major role of these carbohydrates in stress alleviation, involving osmoprotectants, carbon storage, and signal molecules. It was reported that carbohydrates such as sugars (e.g., glucose, fructose, fructans, and trehalose) and starch are involved in the response to several stresses, and act as nutrient and metabolite signaling molecules [36,37]. Additionally, the high carbohydrate accumulation helps to prevent oxidative losses by scavenging ROS and maintaining protein structure during salt stress. Moreover, the marked increase in carbohydrate levels in fenugreek leaves following SA application corroborated the findings of [27,38,39]. SA application deranges the enzymatic system of polysaccharide hydrolysis, which stimulates the hydrolysis of insoluble sugars and creates an osmotic source that is important to osmotic regulation. Interestingly, it can be concluded that SA application ameliorates salinity stress by increasing photosynthetic carbohydrates.
Amino acids are essential molecules that shuttle organic nitrogen through the plant, and play several critical roles in plants, from providing the building blocks of proteins to their central role in cellular and plant physiology [40,41]. The increase in amino acid content in fenugreek plants as a result of salt stress and SA application may be attributed to the changes produced by stress promoting the synthesis of amino acids, inhibiting amino acid degradation, and inhibiting protein synthesis and protein degradation [42]. Moreover, amino acids are involved in glutathione and phytochelatin synthesis, which play roles in metal binding and synthesis of polyamines, acting as signaling molecules and antioxidants [43]. Therefore, it could be hypothesized that amino acids contribute to maintaining the cellular osmotic potential, and may have an important role in tolerance to salt stress.
Generally, proline accumulation is an important physiological index for plant response to salt stress and is supposed to correlate with adaptation to salinity [44]. The obtained result of increasing proline content in fenugreek leaves supports earlier reports by [45], in which salinity displayed a conspicuous increase in compatible solutes, such as proline. Hence, the accumulated proline level under salt stress may be due to the activation of proline biosynthesis, which enhances protein turnover [30]. A noteworthy finding from our study is that the use of the plant-growth-hormone (SA) significantly increased the proline content in fenugreek plants under both saline and non-saline conditions, as previously reported by [46] in chickpea plants. Plants require a greater accumulation of energy-rich compounds under a saline soil environment. From these compounds, proline serves as a nitrogen and/or carbon source, or as a building block for peptide and protein synthesis [47]. Moreover, proline acts as a scavenger of free radicals [48], and a cytoplasmic osmolyte that reduces the osmotic potential of the cell and the uptake of toxic ions [49].
Similarly, phenolic compounds, a group of secondary metabolites, have different biological activities, and their most important capability is their antioxidant activity in plants [50,51]. Our study indicated the role of SA application in minimizing the harmful effects of salt stress, with evidence of an increase in the protective effects of these compounds against salt stress, supporting plants to maintain ROS levels under detrimental conditions, and facilitating rapid elimination so that metabolism remains stable.
Moreover, the results of a flavonoid increase in fenugreek leaves agreed with earlier studies of [52] on artichoke (Cynara scolymus L.) leaves, which may be explained by the finding that enzymes of the flavonoid biosynthesis pathway, such as phenylalanine ammonia-lyase and chalcone synthase, increase under stress [53]. Additionally, flavonoids directly scavenge ROS, including H2O2, O2− and OH− radicals. Furthermore, flavonoids were found to enrich plant tolerance against salinity by regulating K+ maintenance and Na+ elimination from leaf mesophyll in broad beans and quinoa [54].
Lipid peroxidation is the process whereby free radicals steal electrons from the lipids in cell membranes, leading to a free radical chain reaction mechanism that indicates the magnitude of the oxidative stress, resulting in cell damage and the formation of MDA [55,56,57]. The accumulation of MDA in fenugreek leaves subjected to salt stress was ascribed to the production of ROS in cells, which causes peroxidation in membranous lipids and the formation of MDA. The reduction in its content in fenugreek plants following SA application could be attributed to the fact that SA supports plants to produce antioxidative compounds and/or enzymes that diminish ROS before peroxidation [14].
Interestingly, the increase in shikimic acid in fenugreek leaves subjected to salt stress and sprayed with SA was in agreement with the previously observed results of [58,59, 60] for maize, Eucalyptus and carrot, respectively, under different stress conditions. It was proven that the accumulation of shikimic acid depends on the rate of ongoing metabolic processes [61], which leads to the synthesis of plant phenolic compounds via the shikimic acid pathway. This pathway simply converts simple carbohydrate precursors derived from glycolysis and the pentose phosphate pathway into aromatic amino acids, including the SA precursor phenylalanine [62], which could be correlated with the pivotal effect that SA exerts during the plant response to salinity.
The increase in antioxidant enzyme activity in fenugreek plant leaves under salt stress confirms earlier reports [38]. Salinity led to a prominent increase in antioxidant enzymes, which may be due to the reality that ROS are produced in response to different environmental stresses, including salt stress [63,64].
Of particular note, a significant (p ≤ 0.05) increase in antioxidant enzyme activity following SA application could be the sign of buildup of a protective means to lessen the oxidative damage induced by salt stress. A similar observation was recorded by [65] on soybean plants under the combination of salt stress and SA application, and by [66] under Cd stress. The augmentation of oxidative stress caused by salinity may be overwhelmed by this enzymatic system, and this explains our previously mentioned result of a decrease in MDA content in SA applied fenugreek plants.

4. Materials and Methods

4.1. Soil, Seed, and Growth Conditions

The experimental soil was collected from the top layer (0–20 cm) from Sharkia Governate, Egypt. Physicochemical attributes and nutritional status of the experimental soil are recorded in Table 3. Fenugreek seeds (Trigonella foenum-graecum L.) (var. Giza 30; procured from Agricultural Research Centre, Giza, Egypt) were surface disinfected with 5% sodium hypochlorite for 10 min, then subsequently washed with distilled water and sown in plastic pots (25 cm diam.) filled with 2 kg of the collected soil. The experiments were kept under controlled conditions (10 h light/14 h dark cycle at 20/15 °C (day/night), moistened repeatedly with water, and thinned to five germinated seeds per pot after 10 days of germination.

4.2. Salt and Salicylic Acid Application

Salt solutions were applied after one month from sowing at the levels of 0, 75 and 150 mM NaCl, then SA was applied after finishing the salt addition by spraying the fenugreek plant leaves with 0.5 mM SA solution, versus no SA (control sprayed with distilled water) in the early morning for seven successive days. Hence, there were six treatments (2 × 3), and each treatment was replicated three times (2 × 3 × 3). The plant samples from all treatments were collected after 4 weeks from SA application and kept in labeled bags for different analysis.

4.3. Physiological Evaluation

4.3.1. Estimation of Chlorophyll

The chlorophyll content index (CCI) in fenugreek leaves was estimated by the CCM-200 plus Chlorophyll Content Meter (Opti-Sciences, Inc., Hudson, NH, USA). CCI results are the mean of the data recorded at different positions along the length of the leaf.

4.3.2. Estimation of Carbohydrate Content

Carbohydrates were estimated by the phenol sulphuric acid technique, as confirmed by [67]. A known weight of dried fenugreek leaves was extracted with 2.5 N HCl. The absorbance was read at 490 nm.

4.3.3. Determination of Total Free Amino Acids and Proline Content

The total free amino acid content of fenugreek leaf tissue was assessed quantitatively in an alcoholic extract by the method of [68]. Ninhydrin solution, citrate buffer, glycerol (55%), and 0.5 mL of sample solution were mixed subsequently, and the volume was brought up to 5 mL by distilled water. After heating in a boiling water bath for half an hour, the mixture was then cooled under tap water and gently shaken. The absorbance was read at 570 nm.
The proline content of fresh leaves was extracted in 3% aqueous sulphosalicylic acid, and the homogenate was filtered. Two mL of glacial acetic acid and 2 mL of acid ninhydrin were added to 2 mL of the filtrate in a glass test tube and heated in a boiling water bath for 1 h, and then were placed in an ice bath. Four mL of toluene was added to the reaction mixture and stirred well for 20–30 s. The optical density of the produced color was measured at 520 nm [69].

4.3.4. Determination of Total Phenolic and Flavonoid Contents

Total phenolic content in fenugreek leaves was determined [70] after 95% ethanol extraction; then, 1 mL from the extract was mixed with 1 mL of Folin reagent and 1 mL of Na2CO3 (20%). The absorbance was computed at 650 nm.
Total flavonoid content in fenugreek leaves was assayed according to [71], using the aluminum chloride colorimetric method. A 100 μL aliquot of the alcoholic extract was added to 4 mL of distilled water. At zero time, 0.3 mL 5% sodium nitrite was added. After 5 min, 0.3 mL of 10% aluminum chloride was added. After 6 min, 2 mL of 1 M sodium hydroxide was added to the mixture. Absorbance was measured at 510 nm.

4.3.5. Determination of Malondialdehyde (MDA) Content

Lipid peroxidation rates in fresh fenugreek leaves were determined by measuring the MDA content according to the method of [72], using thiobarbituric acid. Absorbance was determined at 450, 532, and 600 nm, respectively, using a spectrophotometer, and its content was estimated based on the following formula:
MDA (μm/L) = 6.45(A532 − A600) − 0.56 A450

4.3.6. Shikimic Acid Content

Fresh fenugreek leaves were homogenized in 0.25 M HCl (1 mL/100 mg biomass) [73] and centrifuged at 3000 rpm for 30 min. Then, 0.5 mL of 1% periodic acid was added to 50 µL of supernatant and left for 3 h at room temperature. After that, 0.5 mL of 1 M sodium hydroxide and 0.3 mL of 0.1 M glycine were added, and the samples were centrifuged again. The absorbance of the samples was read at 380 nm.

4.3.7. Estimation of the Antioxidant Enzymes

A known shoot fresh weight of fenugreek was ground in 0.05 M phosphate buffer (pH 7.0) containing 1 mM EDTA (Ethylene Diamine Tetra Acetic Acid), and centrifuged at 10,000 rpm for 10 min. The supernatant was finalized to a total known volume and used as an enzyme source. An assay of catalase activity (CAT) was undertaken in line with the method of [74]. Peroxidase activity (POD) was estimated based on information from [75], wherein 5 mL of the assay mixture, comprising 300 µM phosphate buffer (pH 6.8), 50 µM catechol, 50 µM H2O2 and 1 mL of enzyme extract, was prepared. The optical density was measured at 430 nm.
An assay of polyphenol oxidase activity (PPO) was performed according to [76], wherein 5 mL of assay mixture comprising 125 µM of phosphate buffer (pH 6.8), 100 µM of pyrogallol, and 1 mL of enzyme extract were prepared. The optical density of the produced color was measured at 430 nm. Ascorbate peroxidase (APX) activity was prepared and assayed according to [77].

4.4. Statistical Analysis

Origin 2017 was used for data processing and forming figures. The data were subjected to statistical studies using a two-way analysis of variance (ANOVA), using the Statistical Package for the Social Science (SPSS) version 15.0. The data are presented as the means ± standard errors of at least three replicates per treatment (n = 3), and the different letters indicate the statistical differences at p < 0.05 using the post hoc test (Tukey’s test).

5. Conclusions

It may be concluded from our results that NaCl had damaging effects on the chlorophyll content and biochemical parameters of fenugreek plants. SA application alleviates the devastating effects generated by salt stress, and this was evidenced by the increase in CCI, carbohydrates, phenolics, flavonoids, and total free amino acids. Increases in shikimic acid, proline, and antioxidant enzyme activity, and a lower MDA content, were also detected with SA application. Thus, it may be concluded that exogenous SA application might act as a powerful tool in enhancing physiological parameters and protecting plants from abiotic stresses, such as salt stress.

Author Contributions

Conceptualization, R.E.A.; Methodology, R.E.A.; Validation, R.E.A., A.A.H.A.L.; Formal analysis, R.E.A.; Investigation, R.E.A.; Data curation, R.E.A.; Funding acquisition, A.A.H.A.L., R.S.S., Writing, R.E.A., Review and editing, A.A.H.A.L., Supervision, A.A.H.A.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Taif University Researchers Supporting Project number (TURSP-2020/72), Taif University, Taif, Saudi Arabia.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Abdel Latef, A.A.; Zaid, A.; Abo-Baker, A.B.E.; Salem, W.; Abu Alhmad, M.F. Mitigation of copper stress in maize by inoculation with Paenibacillus polymyxa and Bacillus circulans. Plants 2020, 9, 1513. [Google Scholar] [CrossRef] [PubMed]
  2. Osman, M.S.; Badawy, A.A.; Osman, A.I.; Abdel Latef, A.A. Ameliorative impact of an extract of the halophyte Arthrocnemum macrostachyum on growth and biochemical parameters of soybean under salinity stress. J. Plant Growth Regul. 2020. [Google Scholar] [CrossRef]
  3. Qi, Z.Y.; Ahammed, G.J.; Jiang, C.Y.; Li, C.X.; Zhou, J. The E3 ubiquitin ligase gene SlRING1 is essential for plant tolerance to cadmium stress in Solanum lycopersicum. J. Biotechnol. 2020, 324, 239–247. [Google Scholar] [CrossRef] [PubMed]
  4. Dawood, M.F.A.; Tahjib-Ul-Arif, M.; Sohag, A.A.; Abdel Latef, A.A.; Ragaey, M.M. Mechanistic insight of allantoin in protecting tomato plants against ultraviolet C stress. Plants 2021, 10, 11. [Google Scholar] [CrossRef]
  5. Mantri, N.; Patade, V.; Penna, S.; Ford, R.; Peng, E. Abiotic stress responses in plants: Present and future. In Abiotic Stress Responses in Plants; Ahmad, P., Prasad, M.N.V., Eds.; Springer: New York, NY, USA, 2012; pp. 1–19. [Google Scholar] [CrossRef]
  6. Chinnusamy, V.; Jagendorf, A.; Zhu, J.-K. Understanding and improving salt tolerance in plants. Crop. Sci. 2005, 45, 437–448. [Google Scholar] [CrossRef] [Green Version]
  7. Abdel Latef, A.A.; Alhmad, M.F.A.; Kordrostami, M.; Abo–Baker, A.B.A.E.; Zakir, A. Inoculation with Azospirillum lipoferum or Azotobacter chroococcum reinforces maize growth by improving physiological activities under saline conditions. J. Plant Growth Regul. 2020, 39, 1293–1306. [Google Scholar] [CrossRef]
  8. Al-Elwany, O.A.A.I.; Mohamed, G.F.; Abdurrahman, H.A.; Rady, M.M.; Abdel Latef, A.A. Exogenous glutathione-mediated tolerance to deficit irrigation in salt-affected Capsicum frutescence (L.) plants is connected with higher antioxidant content and ionic homeostasis. Not. Bot. Horti Agrobot. Cluj Napoca 2020, 48, 1957–1979. [Google Scholar] [CrossRef]
  9. Munns, R.; Tester, M. Mechanism of salinity tolerance. Annu. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef] [Green Version]
  10. Abdel Latef, A.A.; Srivastava, A.K.; Abdel-sadek, M.S.; Kordrostam, M.; Tran, L.S.P. Titanium dioxide nanoparticles improve growth and enhance tolerance of broad bean plants under saline conditions. Land Degrad. Dev. 2018, 29, 1065–1073. [Google Scholar] [CrossRef]
  11. Dief, H.; Hashem, E.A.; Fawzan, S.; El-Sayed, A.S. Alleviation of salt stress in Triticum aestivum by biopriming with Phanerochaete chrysosporium. J. Crop. Sci. Biotechnol. 2021, 24, 103–116. [Google Scholar] [CrossRef]
  12. Chandrakar, V.; Dubey, A.; Keshavkant, S. Modulation of antioxidant enzymes by salicylic acid in arsenic exposed Glycine max L. J. Soil Sci. Plant Nutr. 2016, 16, 662–676. [Google Scholar] [CrossRef] [Green Version]
  13. Abdel Latef, A.A.; Kordrostami, M.; Zakir, A.; Zaki, H.; Saleh, O.M. Eustress with H2O2 facilitates plant growth by improving tolerance to salt stress in two wheat cultivars. Plants 2019, 8, 303. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Abdelhameed, R.E.; Metwally, R.A. Mitigation of salt stress by dual application of arbuscular mycorrhizal fungi and salicylic acid. Agrochimica 2018, 62, 353–366. [Google Scholar] [CrossRef]
  15. Ahammed, G.J.; Li, Y.; Li, X.; Han, W.-Y.; Chen, S. Epigallocatechin-3-Gallate Alleviates Salinity-Retarded Seed Germination and Oxidative Stress in Tomato. J. Plant Growth Regul. 2018, 37, 1349–1356. [Google Scholar] [CrossRef]
  16. Per, T.S.; Fatma, M.; Asgher, M.; Javied, S.; Khan, N.A. Salicylic Acid and Nutrients Interplay in Abiotic Stress. In Salicylic Acid: A Multifaceted Hormone; Nazar, R., Iqbal, N., Khan, N., Eds.; Springer Nature: Singapore, 2017. [Google Scholar] [CrossRef]
  17. Koo, Y.M.; Heo, A.Y.; Choi, H.W. Salicylic Acid as a Safe Plant Protector and Growth Regulator. Plant Pathol. J. 2020, 36, 1–10. [Google Scholar] [CrossRef] [PubMed]
  18. Hayat, Q.; Hayat, S.; Irfan, M.; Ahmad, A. Effect of exogenous salicylic acid under changing environment: A review. Environ. Exp. Bot. 2010, 68, 14–25. [Google Scholar] [CrossRef]
  19. Li, X.; Zhang, L.; Ahammed, G.J.; Li, Y.-T.; Wei, J.-P.; Yan, P.; Zhang, L.-P.; Han, X.; Han, W.-Y. Salicylic acid acts upstream of nitric oxide in elevated carbon dioxide-induced flavonoid biosynthesis in tea plant (Camellia sinensis L.). Environ. Exp. Bot. 2019, 161, 367–374. [Google Scholar] [CrossRef]
  20. Palma, F.; López-Gómez, M.; Tejera, N.A.; Lluch, C. Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Sci. 2013, 208, 75–82. [Google Scholar] [CrossRef]
  21. Babar, S.; Siddiqi, E.H.; Hussain, I.; Bhatti, K.H.; Rasheed, R. Mitigating the Effects of Salinity by Foliar Application of Salicylic Acid in Fenugreek. Physiol. J. 2014, 2014, 1–6. [Google Scholar] [CrossRef] [Green Version]
  22. Zhang, Y.; Xu, S.; Yang, S.; Chen, Y. Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 2015, 252, 911–924. [Google Scholar] [CrossRef]
  23. Fayez, K.A.; Bazaid, S.A. Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J. Saudi Soc. Agric. Sci. 2014, 13, 45–55. [Google Scholar] [CrossRef] [Green Version]
  24. Khan, M.I.R.; Iqbal, N.; Masood, A.; Per, T.S.; Khan, N.A. Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal. Behav. 2013, 8, e26374. [Google Scholar] [CrossRef] [Green Version]
  25. Alsahli, A.; Mohamed, A.-K.; Alaraidh, I.; Al-Ghamdi, A.; Al-Watban, A.; El-Zaidy, M.; Alzahrani, S.M. Salicylic acid alleviates salinity stress through the modulation of biochemical attributes and some key antioxidants in wheat seedlings. Pak. J. Bot. 2019, 51, 1551–1559. [Google Scholar] [CrossRef]
  26. Noreen, S.; Ashraf, M. Alleviation of adverse effects of salt stress on sunflower (Helianthus annuus L.) by exogenous application of salicylic acid: Growth and photosynthesis. Pak. J. Bot. 2008, 40, 1657–1663. [Google Scholar]
  27. El-khodary, S.F.A. Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt stressed maize plants. Int. J. Agric. Biol. 2004, 6, 5–8. [Google Scholar]
  28. Shim, I.S.; Momose, Y.; Yamamoto, A.H.; Kim, D.W.A.; Usui, K. Inhibition of catalase activity by oxidative stress and its relationship to salicylic acid accumulation in plants. Plant Growth Regul. 2003, 39, 285–292. [Google Scholar] [CrossRef]
  29. Petropoulos, G.A. Fenugreek—The Genus Trigonella, 1st ed.; Taylor and Francis: London, UK; New York, NY, USA, 2002; pp. 1–127. [Google Scholar]
  30. Ahmad, A.; Alghamdi, S.; Mahmood, K.; Afzal, M. Fenugreek a multipurpose crop: Potentialities and improvements. Saudi J. Biol. Sci. 2016, 23, 300–310. [Google Scholar] [CrossRef] [Green Version]
  31. Abdel Latef, A.A.; Abu Alhmad, M.F.A.; Ahmad, S. Foliar application of fresh moringa leaf extract overcomes salt stress in fenugreek (Trigonella foenum-graecum) plants. Egypt. J. Bot. 2017, 57, 157–179. [Google Scholar] [CrossRef]
  32. Metwally, R.A.; Abdelhameed, R.E. Synergistic effect of arbuscular mycorrhizal fungi in growth and physiology of salt-stressed Trigonella foenum-graecum plants. Biocatal. Agric. Biotechnol. 2018, 16, 538–544. [Google Scholar] [CrossRef]
  33. Selem, E.E.; Abdelhameed, R.E.; Kamel, H.A.; Hegazy, S.H. Physiological and Biochemical Response of Gamma Irradiated Sesamum indicum L. Seed Grown in Heavy Metal Contaminated Soil. Biosci. Res. 2018, 15, 1063–1072. [Google Scholar]
  34. Shi, Q.; Bao, Z.; Zhu, Z.; Ying, Q.; Qian, Q. Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul. 2006, 48, 127–135. [Google Scholar] [CrossRef]
  35. Abdel-Fattah, G.M.; Rabie, G.H.; Lamis, D.S.; Metwally, R.A. The impact of arbuscular mycorrhizal fungi on growth and physiological parameters of cowpea plants grown under salt stress conditions. Int. J. Appl. Sci. Biotechnol. 2016, 4, 372–379. [Google Scholar] [CrossRef] [Green Version]
  36. Couée, I.; Sulmon, C.; Gouesbet, G.; El Amrani, A. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J. Exp. Bot. 2006, 57, 449–459. [Google Scholar] [CrossRef] [PubMed]
  37. Abdel Latef, A.A.; Abu Alhmad, M.F.A.; Abdelfattah, K.E. The possible roles of priming with ZnO nanoparticles in mitigation of salinity stress in lupine (Lupinus termis) plants. J. Plant Growth Regul. 2017, 36, 60–70. [Google Scholar] [CrossRef]
  38. Fahad, S.; Bano, A. Effect of salicylic acid on physiological and biochemical characterization of maize grown in saline area. Pak. J. Bot. 2012, 44, 1433–1438. [Google Scholar]
  39. Jini, D.; Joseph, B. Physiological Mechanism of Salicylic Acid for Alleviation of Salt Stress in Rice. Rice Sci. 2017, 24, 97–108. [Google Scholar] [CrossRef]
  40. Hernandez-Montes, G.; Diaz-Mejia, J.J.; Perez-Rueda, E.; Segovia, L. The hidden universal distribution of amino acid biosynthetic networks: A genomic perspective on their origins and evolution. Genome Biol. 2008, 9, R95. [Google Scholar] [CrossRef] [Green Version]
  41. Abdel Latef, A.A.; Srivastava, A.K.; Saber, H.; Alwaleed, E.A.; Tran, L.S.P. Sargassum muticum and Jania rubens regulate amino acid metabolism to improve growth and alleviate salinity in chickpea. Sci. Rep. 2017, 7, 10537. [Google Scholar] [CrossRef] [Green Version]
  42. Mansour, M.M. Nitrogen containing compounds and adaptation of plants to salinity stress. Biol. Plant. 2000, 43, 491–500. [Google Scholar] [CrossRef]
  43. Sharma, S.S.; Dietz, K.J. The significance of amino acids and amino acid-derived molecules in plant responces and adaptation to heavy metal stress. J. Exp. Bot. 2006, 57, 711–726. [Google Scholar] [CrossRef] [Green Version]
  44. Ashraf, M.; Harris, P.J.C. Potential biochemical indicators of salinity tolerance in plants. Plant Sci. 2004, 166, 3–16. [Google Scholar] [CrossRef]
  45. Khan, M.N.; Siddiqui, M.H.; Mohammad, F.; Naeem, M.; Khan, M.M.A. Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol. Plant. 2010, 32, 121–132. [Google Scholar] [CrossRef]
  46. Asadi, M.; Heidari, M.A.; Kazemi, M.; Filinejad, A.R. Salicylic acid induced changes in some physiological parameters in chickpea (Cicer arietinum L.) under salt stress. J. Agric. Technol. 2013, 9, 311–316. [Google Scholar]
  47. El Moukhtari, A.; Cabassa-Hourton, C.; Farissi, M.; Savouré, A. How Does Proline Treatment Promote Salt Stress Tolerance During Crop Plant Development? Front. Plant Sci. 2020, 11, 1127. [Google Scholar] [CrossRef] [PubMed]
  48. Trotel, P.; Bouchereau, A.; Niogret, M.F.; Larher, F. The fate of osmo-accumulated proline in leaf discs of Rape (Brassica napus L.) incubated in a medium of low osmolarity. Plant Sci. 1996, 118, 31–45. [Google Scholar] [CrossRef]
  49. Woodward, A.J.; Bennett, I.J. The effect of salt stress and abscisic acid on proline production, chlorophyll content and growth of in vitro propagated shoots of Eucalyptus camaldulensis. Plant Cell Tissue Organ Cult. 2005, 82, 189–200. [Google Scholar] [CrossRef]
  50. Zlatić, N.; Jakovljević, D.; Stanković, M. Temporal, Plant Part, and Interpopulation Variability of Secondary Metabolites and Antioxidant Activity of Inula helenium L. Plants 2019, 8, 179. [Google Scholar] [CrossRef] [Green Version]
  51. Metwally, R.A.; Abdelhameed, R.E. Impact of Ridomil, Bavistin and Agrothoate on arbuscular mycorrhizal fungal colonization, biochemical changes and potassium content of cucumber plants. Ecotoxicology 2019, 28, 487–498. [Google Scholar] [CrossRef]
  52. Rezazadeh, A.; Ghasemnezhad, A.; Barani, M.; Telmadarrehei, T. Effect of Salinity on Phenolic Composition and Antioxidant Activity of Artichoke (Cynara scolymus L.) Leaves. Res. J. Med. Plants 2012, 6, 245–252. [Google Scholar] [CrossRef] [Green Version]
  53. Li, J.; Ou-Lee, T.M.; Raba, R.; Amundson, R.G.; Last, R.L. Arabidopsis flavonoid mutants are hypersensitive to UV-B radiation. Plant Cell 1993, 5, 171–179. [Google Scholar] [CrossRef]
  54. Ismail, H.; Maksimovic, J.D.; Maksimovic, V.; Shabala, L.; Zivanovic, B.D.; Tian, Y.; Jacobsen, S.-E.; Shabala, S. Rutin, a flavonoid with antioxidant activity, improves plant salinity tolerance by regulating K+ retention and Na+ exclusion from leaf mesophyll in quinoa and broad beans. Funct. Plant Biol. 2016, 43, 75–86. [Google Scholar] [CrossRef]
  55. Neffati, M.; Sriti, J.; Hamdaoui, G.; Kchouk, M.E.; Marzouk, B. Salinity impact on fruit yield, essential oil composition and antioxidant activities of Coriandrum sativum fruit extracts. Food Chem. 2011, 124, 221–225. [Google Scholar] [CrossRef]
  56. Qureshi, M.I.; Abdin, M.Z.; Qadir, S.; Iqbal, M. Lead induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol. Plant. 2007, 51, 121–128. [Google Scholar] [CrossRef]
  57. Abdel Latef, A.A.; Mostofa, M.G.; Rahman, M.M.; Abdel-Farid, I.B.; Tran, L.S.P. Extracts from yeast and carrot roots enhance maize performance under seawater-induced salt stress by altering physio-biochemical characteristics of stressed plants. J. Plant Growth Regul. 2019, 38, 966–979. [Google Scholar] [CrossRef]
  58. Sicher, C.; Barnaby, J.Y. Impact of carbon dioxide enrichment on the responses of maize leaf transcripts and metabolites to water stress. Physiol. Plant. 2012, 144, 238–253. [Google Scholar] [CrossRef]
  59. Warren, C.; Aranda, I.; Cano, F.J. Metabolomics demonstrates divergent responses of two Eucalyptus species to water stress. Metabolomics 2012, 8, 186–200. [Google Scholar] [CrossRef] [Green Version]
  60. Becerra-Moreno, A.; Redondo-Gil, M.; Benavides, J.; Nair, V.; Cisneros-Zevallos, L.; Jacobo-Velázquez, D.A. Combined effect of water loss and wounding stress on gene activation of metabolic pathways associated with phenolic biosynthesis in carrot. Front. Plant Sci. 2015, 6, 837. [Google Scholar] [CrossRef] [Green Version]
  61. Matallo, M.B.; Almeida, S.D.B.; Franco, D.A.S.; Cerdeira, A.L.; Gazzeiro, D.L.P. Glyphosate as a tool to produce shikimic acid in plants. Planta Daninha 2014, 32, 601–608. [Google Scholar] [CrossRef] [Green Version]
  62. Herrmann, K.M.; Weaver, L.M. The shikmate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 473–503. [Google Scholar] [CrossRef] [PubMed]
  63. Jacobo-Velázquez, D.A.; Cisneros-Zevallos, L. Correlations of antioxidant activity against phenolic content revisited: A new approach in data analysis for food and medicinal plants. J. Food Sci. 2009, 74, 107–113. [Google Scholar] [CrossRef]
  64. Chen, Z.; Silva, H.; Klessig, D.F. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 1993, 262, 1883–1886. [Google Scholar] [CrossRef]
  65. Jaiswal, A.; Pandurangam, V.; Sharma, S.K. Effect of salicylic acid in soybean (Glycine max L. Meril) under salinity stress. Int. J. Life Sci. Res. 2014, 9, 671–676. [Google Scholar]
  66. Singh, S.; Singh, V.P.; Prasad, S.M.; Sharma, S.; Ramawat, N.; Dubey, N.K.; Tripathi, D.K.; Chauhan, D.K. Interactive Effect of Silicon (Si) and Salicylic Acid (SA) in Maize Seedlings and Their Mechanisms of Cadmium (Cd) Toxicity Alleviation. J. Plant Growth Regul. 2019, 38. [Google Scholar] [CrossRef]
  67. Dubois, M.; Gilles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, F. Calorimetric method for determination of sugars and related substances. Anal. Chem. 1956, 28, 350–356. [Google Scholar] [CrossRef]
  68. Lee, Y.P.; Takanashi, T. An improved colorimetric determination of amino acids with the use of ninhydrin. Anal. Biochem. 1966, 14, 71–77. [Google Scholar] [CrossRef]
  69. Bates, I.S.; Waldern, R.P.; Teare, I.D. Rapid determination of free proline for water stress studies. Plant Soil 1973, 39, 205–207. [Google Scholar] [CrossRef]
  70. Jindal, K.K.; Singh, R.N. Phenolic content in male and female Carica papaya: A possible physiological marker sex identification of vegetative seedlings. Physiol. Plant. 1975, 33, 104–107. [Google Scholar] [CrossRef]
  71. Zou, Y.; Lu, Y.; Wei, D. Antioxidant activity of flavonoid-rich extract of Hypericum perforatum L in vitro. J. Agric. Food Chem. 2004, 52, 5032–5039. [Google Scholar] [CrossRef]
  72. Heath, R.L.; Packer, L. Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 1968, 125, 189–198. [Google Scholar] [CrossRef]
  73. Zelya, I.A.; Anderson, J.A.H.; Owen, M.D.K.; Landes, R.D. Evaluation of spectrophotometric and HPLC methods for shikimic acid determination in plants: Models in glyphosate resistant and susceptible crops. J. Agric. Food Chem. 2011, 59, 2202–2212. [Google Scholar] [CrossRef] [PubMed]
  74. Aebi, H. Catalase. In Methods of Enzymatic Analysis; Bergmeyer, H., Ed.; Elsevier: Amsterdam, The Netherlands, 1983; pp. 273–286. [Google Scholar] [CrossRef]
  75. Maehly, A.C. Assay of catalases and peroxidases. In Methods of Biochemical Analysis; Glick, D., Ed.; Wiley: Hoboken, NJ, USA, 1955; Volume 2, pp. 764–775. [Google Scholar] [CrossRef]
  76. Kar, M.; Mishra, D. Catalase, peroxidase and polyphenol oxidase activities during rice leaf senescence. Plant Physiol. 1976, 57, 315–319. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Nakano, Y.; Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981, 22, 867–880. [Google Scholar] [CrossRef]
Plants 10 00657 g001 550
Figure 1. Effect of NaCl concentrations and salicylic (SA) application on (A) total free amino acid content and (B) proline content of fenugreek plant leaves. Values represent the mean of three replicates. Different letters (a, b, c and d) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW—dry weight.
Figure 1. Effect of NaCl concentrations and salicylic (SA) application on (A) total free amino acid content and (B) proline content of fenugreek plant leaves. Values represent the mean of three replicates. Different letters (a, b, c and d) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW—dry weight.
Plants 10 00657 g001
Plants 10 00657 g002 550
Figure 2. Effect of NaCl concentrations and salicylic (SA) application on (A) phenolic content and (B) flavonoid content of fenugreek plant leaves. Values represent the mean of three replicates. Different letters (a, b, c, d and e) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW—dry weight.
Figure 2. Effect of NaCl concentrations and salicylic (SA) application on (A) phenolic content and (B) flavonoid content of fenugreek plant leaves. Values represent the mean of three replicates. Different letters (a, b, c, d and e) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW—dry weight.
Plants 10 00657 g002
Plants 10 00657 g003 550
Figure 3. Effect of NaCl concentrations and salicylic (SA) application on (A) malondialdehyde (MDA) content and (B) shikimic acid content of fenugreek plant leaves. Values represent the mean of three replicates. Different letters (a, b and c) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW; dry weight.
Figure 3. Effect of NaCl concentrations and salicylic (SA) application on (A) malondialdehyde (MDA) content and (B) shikimic acid content of fenugreek plant leaves. Values represent the mean of three replicates. Different letters (a, b and c) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW; dry weight.
Plants 10 00657 g003
Plants 10 00657 g004 550
Figure 4. Effect of NaCl concentrations and salicylic (SA) application on antioxidant enzymes activities; (A) peroxidase (POD), (B) catalase (CAT), (C) polyphenol oxidase (PPO) and (D) ascorbate peroxidase (APX), of fenugreek plants. Values represent the mean of three replicates. Different letters (a, b, c, d and e) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW; dry weight.
Figure 4. Effect of NaCl concentrations and salicylic (SA) application on antioxidant enzymes activities; (A) peroxidase (POD), (B) catalase (CAT), (C) polyphenol oxidase (PPO) and (D) ascorbate peroxidase (APX), of fenugreek plants. Values represent the mean of three replicates. Different letters (a, b, c, d and e) indicate statistical differences at 5% probability according to Tukey’s test. Error bars are standard errors of the mean. DW; dry weight.
Plants 10 00657 g004
Table
Table 1. Effect of NaCl concentrations and salicylic (SA) application on the chlorophyll content index (CCI) and carbohydrate content of fenugreek plant leaves.
Table 1. Effect of NaCl concentrations and salicylic (SA) application on the chlorophyll content index (CCI) and carbohydrate content of fenugreek plant leaves.
NaCl (mM)SA (mM)CCI% CCarbohydrates (mg g−1 DW)% C
0022.03 ± 0.91 ab11.379.2 ± 4.5 c4.3
0.524.51 ± 3.08 a82.6 ± 4.6 bc
75017.87 ± 1.11 b35.3 ↑91 ± 5.1 bc8.4 ↑
0.524.17 ± 4.61 a98.6 ± 5.5 ab
150013.27 ± 3.56 c32.1 ↑110.4 ± 6.1 a7.8 ↑
0.517.53 ± 3.65 b119 ± 7.3 a
Data shown in the table represent the mean ± standard error, followed by a small letter; similar letters indicate that means were not different significantly at 5%, probability based on Tukey’s test. %C means SA-treated plants expressed as % of their respective non-treated controls. DW— dry weight, ↑ means increase.
Table
Table 2. Analysis of variance of the effect of salt, salicylic (SA), and their interactions on some physiological parameters in fenugreek leaves, based on a two-way ANOVA analysis.
Table 2. Analysis of variance of the effect of salt, salicylic (SA), and their interactions on some physiological parameters in fenugreek leaves, based on a two-way ANOVA analysis.
Parameters SaltSASalt × SA
Chlorophyll content index ***
Carbohydrates*nsns
Lipid peroxidation***
Phenolics **ns
Flavonoids**ns
Shikimic acid***
Total free amino acids***
Proline***
POD**ns
CAT**ns
APX***
PPO***
ns (non-significant) and * (significant at the 5% probability level).
Table
Table 3. Physicochemical properties and nutritional status of the experimental soil before planting.
Table 3. Physicochemical properties and nutritional status of the experimental soil before planting.
PropertySand
(%)		Silt
(%)		Clay (%)Soil TextureSaturation Percent Electric
Conductivity		pHCaCO3 (%)Mineral Content Organic Matter
(mg/kg Soil)(%)
KMgCaTotal P(%)
Value13.927.458.7clay693.48.24.90.376.38.40.691.2
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Abdelhameed, R.E.; Abdel Latef, A.A.H.; Shehata, R.S. Physiological Responses of Salinized Fenugreek (Trigonellafoenum-graecum L.) Plants to Foliar Application of Salicylic Acid. Plants 2021, 10, 657. https://doi.org/10.3390/plants10040657

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Abdelhameed RE, Abdel Latef AAH, Shehata RS. Physiological Responses of Salinized Fenugreek (Trigonellafoenum-graecum L.) Plants to Foliar Application of Salicylic Acid. Plants. 2021; 10(4):657. https://doi.org/10.3390/plants10040657

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Abdelhameed, Reda E., Arafat Abdel Hamed Abdel Latef, and Rania S. Shehata. 2021. "Physiological Responses of Salinized Fenugreek (Trigonellafoenum-graecum L.) Plants to Foliar Application of Salicylic Acid" Plants 10, no. 4: 657. https://doi.org/10.3390/plants10040657

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