Salt stress changes biochemical, physiological and photosynthetic attributes of Satureja spicigera
Subject Areas : Stress Physiology
Hoshangh Rahmati
1
,
Borzou Yousefi
2
1 -
2 -
Keywords: Antioxidant activity, Medicinal plants, Photosynthesis, Salt stress ,
Abstract :
We investigated the effect of salt stress on photosynthetic, physiological, and biochemical traits of Satureja spicigera (C. Koch) Boiss., a medicinal plant used in edible products and healthcare industries. The experiment was designed in a randomized complete block design (RCB) with three replications in a greenhouse. The salt treatments included four levels of NaCl (0, 50, 100, and 150 mM). Results showed that salinity levels caused a significant reduction in some photosynthetic, morpho-physiological, physiological, and biochemical characteristics; however, it boosted antioxidant activity. Salinity levels significantly reduced leaf fresh weight (12.56%), leaf dry weight (18.53%), relative water content (11.94%), chlorophyll a (33.33%), chlorophyll b (15.62%), chlorophyll a+b (29.24%), and carotenoid content (42.46%). However, salinity significantly boosted the antioxidant activity of superoxide dismutase (236.50%), peroxidase (85.67%), and catalase (82.78%) on average. Salt stress also significantly increased proline content (373.33%), protein content (84.49%), and leaf electrical conductivity (333.26%) on average. Results confirm that S. spicigera tolerates NaCl concentrations below 100 mM; however, it is highly sensitive to NaCl concentrations above 100 mM, so that a salinity of 150 mM causes a dramatic decrease in photosynthesis and growth. Therefore, we do not recommend the cultivation of this plant in highly saline and semi-saline soils.
Afridi, M. S., T. Mahmood, A. Salam, T. Mukhtar, S. Mehmood, J. Ali, Z. Khatoon, M. Bibi, M. T. Javed and T. Sultan. 2019. Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: Involvement of ACC deaminase and antioxidant enzymes. Plant Physiology and Biochemistry, 139, 569-577.
Ahad, B., W. Shahri, H. Rasool, Z. Reshi, S. Rasool and T. Hussain. 2021. Medicinal plants and herbal drugs: An overview. Medicinal and aromatic plants: healthcare and industrial applications, 1-40.
Athar, H.-U.-R., F. Zulfiqar, A. Moosa, M. Ashraf, Z. U. Zafar, L. Zhang, N. Ahmed, H. M. Kalaji, M. Nafees and M. A. Hossain. 2022. Salt stress proteins in plants: An overview. Frontiers in Plant Science, 13, 999058.
Balasubramaniam, T., G. Shen, N. Esmaeili and H. Zhang. 2023. Plants’ response mechanisms to salinity stress. Plants, 12, (12) 2253.
Bates, L. S., R. Waldren and I. Teare. 1973. Rapid determination of free proline for water-stress studies. Plant and soil, 39, 205-207.
Beauchamp, C. and I. Fridovich. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical biochemistry, 44, (1) 276-287.
Bian, S. and Y. Jiang. 2009. Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Scientia Horticulturae, 120, (2) 264-270.
Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72, (1-2) 248-254.
Chance, B. and A. Maehly. 1955. [136] Assay of catalases and peroxidases.
Fabriki, O. S. and P. S. Mehrabad. 2016. The effects of drought and salt stresses on some morphological and biochemical parameters of savory (Satureja hortensis L.), 23-35.
Garcia-Caparros, P., L. De Filippis, A. Gul, M. Hasanuzzaman, M. Ozturk, V. Altay and M. T. Lao. 2021. Oxidative stress and antioxidant metabolism under adverse environmental conditions: a review. The Botanical Review, 87, 421-466.
Ghanbari, F., M. Bag-Nazari and A. Azizi. 2023. Exogenous application of selenium and nano-selenium alleviates salt stress and improves secondary metabolites in lemon verbena under salinity stress. Scientific Reports, 13, (1) 5352.
Hao, S., Y. Wang, Y. Yan, Y. Liu, J. Wang and S. Chen. 2021. A review on plant responses to salt stress and their mechanisms of salt resistance. Horticulturae, 7, (6) 132.
Harati, E., B. Kashefi and M. Matinzadeh. 2015. Investigation reducing detrimental effects of salt stress on morphological and physiological traits of (Thymus vulgaris) by application of salicylic acid. Iranian Journal of Plant Physiology, 5, (3) 1383-1391.
Hernández-Adasme, C., R. Palma-Dias and V. H. Escalona. 2023. The effect of light intensity and photoperiod on the yield and antioxidant activity of beet microgreens produced in an indoor system. Horticulturae, 9, (4) 493.
Jan, R., S. Asaf, M. Numan, Lubna and K.-M. Kim. 2021. Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy, 11, (5) 968.
Jini, D. and B. Joseph. 2017. Physiological mechanism of salicylic acid for alleviation of salt stress in rice. Rice Science, 24, (2) 97-108.
Kulak, M. 2020. Recurrent drought stress effects on essential oil profile of Lamiaceae plants: An approach regarding stress memory. Industrial Crops and Products, 154, 112695.
Kumar, R., A. Bohra, A. K. Pandey, M. K. Pandey and A. Kumar. 2017. Metabolomics for plant improvement: status and prospects. Frontiers in Plant Science, 8, 1302.
Kumar, S., M. A. Ahanger, H. Alshaya, B. L. Jan and V. Yerramilli. 2022. Salicylic acid mitigates salt induced toxicity through the modifications of biochemical attributes and some key antioxidants in Capsicum annuum. Saudi Journal of Biological Sciences, 29, (3) 1337-1347.
Lichtenthaler, H. K. and A. R. Wellburn. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Ltd.
Mohammadi, H., S. Hazrati and L. Parviz,2019. Morphophysiological and biochemical response of savory medicinal plant using silicon under salt stress. Proc. Annales Universitatis Mariae Curie-Sklodowska, sectio C–Biologia, 72:29-40:
Reddy, A. R., K. Chaitanya, P. Jutur and K. Sumithra. 2004. Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environmental and experimental botany, 52, (1) 33-42.
Saadatfar, A. and S. H. Jafari. 2024. Application of 24-epibrassinolide as an Environmentally Friendly Strategy Alleviates Negative Effects of Salinity Stress in Satureja khuzistanica Jamzad. Journal of Rangeland Science, 14, (3).
Shanker, A. K., D. Gunnapaneni, D. Bhanu, M. Vanaja, N. J. Lakshmi, S. K. Yadav, M. Prabhakar and V. K. Singh. 2022. Elevated CO2 and water stress in combination in plants: brothers in arms or partners in crime? Biology, 11, (9) 1330.
Sheldon, A. R., R. C. Dalal, G. Kirchhof, P. M. Kopittke and N. W. Menzies. 2017. The effect of salinity on plant-available water. Plant and Soil, 418, 477-491.
Sinha, A. K. 1972. Colorimetric assay of catalase. Analytical biochemistry, 47, (2) 389-394.
Srivastava, S. and P. Sharma. 2021. Effect of NaCl on chlorophyll fluorescence and thylakoid membrane proteins in leaves of salt sensitive and tolerant rice (Oryza sativa L) varieties. Journal of Stress Physiology & Biochemistry, 17, (2) 35-44.
Wang, Y., W. Ma, H. Fu, L. Li, X. Ruan and X. Zhang. 2023. Effects of salinity stress on growth and physiological parameters and related gene expression in different ecotypes of Sesuvium portulacastrum on Hainan Island. Genes, 14, (7) 1336.
Zarei, B., A. Fazeli and Z. Tahmasebi. 2019. Salicylic acid in reducing effect of salinity on some growth parameters of Black cumin (Nigella sativa). Journal of Plant Process and Function, 8, (29) 287-298.
Zhang, M., Y. Fang, Y. Ji, Z. Jiang and L. Wang. 2013. Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. South African journal of botany, 85, 1-9.
1405
Salt stress changes biochemical, physiological and photosynthetic attributes of Satureja spicigera
Hoshang Rahmati*1 and Borzou Yousefi2
1.Department of Agriculture, Technical and Engineering Faculty, Payam Noor University, Tehran, Iran,
2.Kermanshah Agricultural and Natural Resources Research and Education Center, Kermanshah, Iran
________________________________________________________________________________
Abstract
We investigated the effect of salt stress on photosynthetic, physiological, and biochemical traits of Satureja spicigera (C. Koch) Boiss., a medicinal plant used in edible products and healthcare industries. The experiment was designed in a randomized complete block design (RCB) with three replications in a greenhouse. The salt treatments included four levels of NaCl (0, 50, 100, and 150 mM). Results showed that salinity levels caused a significant reduction in some photosynthetic, morpho-physiological, physiological, and biochemical characteristics; however, it boosted antioxidant activity. Salinity levels significantly reduced leaf fresh weight (12.56%), leaf dry weight (18.53%), relative water content (11.94%), chlorophyll a (33.33%), chlorophyll b (15.62%), chlorophyll a+b (29.24%), and carotenoid content (42.46%). However, salinity significantly boosted the antioxidant activity of superoxide dismutase (236.50%), peroxidase (85.67%), and catalase (82.78%) on average. Salt stress also significantly increased proline content (373.33%), protein content (84.49%), and leaf electrical conductivity (333.26%) on average. Results confirm that S. spicigera tolerates NaCl concentrations below 100 mM; however, it is highly sensitive to NaCl concentrations above 100 mM, so that a salinity of 150 mM causes a dramatic decrease in photosynthesis and growth. Therefore, we do not recommend the cultivation of this plant in highly saline and semi-saline soils.
Keywords: Antioxidant activity, Medicinal plants, Photosynthesis, Salt stress.
Abbreviation: C: control; Car: carotenoid; CAT: catalase; Chl: chlorophyll; LFW: leaf fresh weight; LDW: leaf dry weight; LTW: Leaf turgor weight; OD: optical density; POD: peroxidase; Pro: proline; ROS: reactive oxygen species; RWC: relative water content; SOD: superoxide dismutase.
Rahmati, H. and B. Yousefi, 2024. Salt stress changes biochemical, physiological and photosynthetic attributes of Satureja spicigera. Iranian Journal of Plant Physiology 14 (4), 5257- 5264.
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____________________________________ * Corresponding Author E-mail Address hoshang.rahmatipnu@pnu.ac.ir Received: May, 2024 Accepted: August, 2024
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Materials and Methods
Experimental Design and Treatments
A greenhouse experiment with three replications, based on a randomized complete block design (RCB), was carried out at the Research Center for Agricultural and Natural Resources in Kermanshah, Iran. Seeds were disinfected with 0.5% sodium hypochlorite, washed, and dried. They were planted in a peat moss bed and watered by sprinkling. The seedlings were transferred to plastic pots (one seedling per pot), filled with a mixture of farm soil, sand, and composted cow manure. The plants were maintained under a 17-hour light photoperiod with 300 μmol/m²s (equivalent to 110 lux of light intensity), followed by 7 hours of darkness (Hernández-Adasme et al., 2023), with a relative humidity of 50-60%. Each pot was irrigated twice a week with 2500 ml of well water. Four treatments were implemented, involving irrigation (250 ml per pot, twice a week) with 0, 50, 100, and 150 mM NaCl (Kumar et al., 2022). We removed the accumulated salts from the pots with distilled water after every four irrigations with the NaCl treatments.
Morpho-physiological Measurements
We measured leaf fresh weight (LFW), leaf turgor weight (LTW), and leaf dry weight (LDW) using 30 young leaves from each plant. These young leaves were immediately weighed with precision (0.0001 g) (LFW). The leaves were immersed in double-distilled water for 18 hours to reach full hydration (22 °C). After drying the leaf surfaces, they were weighed again (LTW). The leaves were then placed in an oven (70 °C, 48 h), and the leaf dry weight (LDW) was measured. The means of LFW and LDW were calculated in grams (g). RWC was calculated using the following formula (Bian and Jiang, 2009):
RWC (%) = (LFW–LDW)/(LTW–LDW)100
Photosynthetic Assays
Chlorophyll a, b, and carotenoid content were measured. The samples were centrifuged for 10 minutes (10000 rpm, 4 °C), and the supernatant was measured at 663, 646, and 470 nm using a microplate reader. The content of photosynthetic pigments (mg g⁻¹ FW) was calculated using the following formulas (Lichtenthaler and Wellburn, 1983):
Carotenoid = (1000 A470 – 3.27 [Chl a] – 104 [Chl b]/227)
Biochemical Assays
The extraction buffer and crude leaf extract were prepared (Reddy et al., 2004). The enzymatic
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activity rate of superoxide dismutase (SOD, EC 1.15.1.1) was measured based on the ability of SOD to stop the photochemical reduction of nitroblue tetrazolium (NBT) by superoxide radicals in the presence of riboflavin under light conditions (Beauchamp and Fridovich, 1971). The optical absorbance was read at 560 nm (one enzymatic unit equals 50% inhibition) using a microplate reader. The activity of SOD was calculated using the following formula:
where:
· OD control: absorbance of control at 560 nm
· OD sample: absorbance of samples at 560 nm
The peroxidase (POD; E.C. 1.11.1.7) activity was measured using a microplate reader and expressed in terms of H₂O₂ consumption (μmol min⁻¹ mg⁻¹ of soluble protein) (Chance and Maehly, 1955). The optical absorbance was recorded for 15 minutes at 30-second intervals at a wavelength of 470 nm, and calculated using the Beer-Lambert law (0.0266 M⁻¹cm⁻¹). The activity of catalase (CAT; E.C. 1.11.1.6) was measured (Sinha, 1972) with some modifications, using the Beer-Lambert law (extinction coefficient of 0.0394 M⁻¹cm⁻¹). Proline content was measured (Bates et al., 1973) as well as soluble protein concentration (mg g⁻¹ FW) (Bradford, 1976).
Statistical Analysis
Analysis of variance and Duncan's Test (p < 0.05) were performed using IBM SPSS Statistics 26 software. The charts were created using Excel software.
Results
The results of ANOVA revealed significant differences (p < 0.01) for chlorophyll a, b, carotenoid, chlorophyll a + b, proline, soluble protein, relative water content, and SOD, POD, and CAT activities (Table 1).
Photosynthetic Pigments
The highest chlorophyll a (12.90 mg g⁻¹ FW), b (3.67 mg g⁻¹ FW), a + b (15.86 mg g⁻¹ FW), and carotenoid (3.87 mg g⁻¹ FW) were observed in the non-NaCl-treated plants. Salinity treatments significantly decreased, on average, the amounts of chlorophyll a, b, carotenoid, and chlorophyll a + b by 33.33%, 15.62%, 42.46%, and 29.24%, respectively (Fig. I). The highest photosynthetic performance index (2.86) was observed in the control plants. Salt treatments significantly reduced this trait by an average of 35.31% (Fig. II).
Antioxidant Activity
The highest SOD (3.64 µmol min⁻¹ mg⁻¹ protein), POD (3.05 µmol min⁻¹ mg⁻¹ protein), and catalase
Fig I. Means comparison of chlorophyll a, chlorophyll b, carotenoid, and total chlorophyll (a + b) content in Satureja spicigera plants in response to different NaCl treatments. Columns with the same letters are not significantly different based on LSD test (Mean ± SD, p = 0.05).
Fig.II. Means comparison (LSD Means ±SD) for photosynthetic performance index, superoxide dismutase, peroxidase, and catalase activity of Satureja spicigera plants in response to different NaCl treatments. The same letters are not show significant difference (P= 0.05).
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II). Salinity levels significantly increased SOD, POD, and catalase activity, on average, by 236.50%, 85.67%, and 82.78%, respectively, compared to the control plants (Fig. II).
The highest leaf fresh weight (12.31 mg) and leaf dry weight (2.45 mg) were observed in the plants treated with 50 mM NaCl (Fig. III a). The highest RWC (89.13%) was observed in the non-NaCl-treated plants; however, the highest LEC (378.23 µS cm⁻¹) was observed in the plants treated with 150 mM NaCl (Fig. III b). Salinity significantly decreased the leaf fresh weight by 12.56%, leaf dry weight by 18.53%, and leaf relative water content by 11.94% in the salt-treated plants compared to the control (Fig. III a, b). Salinity significantly increased LEC by 333.26% in the salt-treated plants compared to the control (Fig. III b).
Morpho-Physiological and Physiological Attributes
Fig III. Means comparison (LSD Mean’s ± SD): (a) leaf fresh weight and leaf dry weight, (b) relative water content (RWC) and leaf electrical conductivity (LEC) of Satureja spicigera plants in response to different NaCl treatments. The same letters are not show significant difference (P= 0.05).
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The relationship between the leaf relative water content and the electrical conductivity is inverse. Its trend can be seen in Fig. IV. This relationship shows that under salinity stress greater than 50 mM, the relative water content decreases with a gentle and uniform slope, but the electrical conductivity increases with a very steep slope.
Fig IV. Relationship between relative water content (RWC) and leaf electrical conductivity (LEC) of Satureja spicigera plants during enhancement NaCl concentration.
Fig. V. Means comparison (LSD Mean’s ± SD) leaf proline content and leaf protein content of Satureja spicigera plants in response to different NaCl treatments. The same letters are not show significant difference (P= 0.05). |
Biochemical Traits
Salt levels severely increased proline content. The highest proline (1.08 µg g⁻¹ FW) was observed in 150 mM NaCl (Fig. V). Salt levels significantly increased proline content by 373.33% on average. The 50 and 100 mM NaCl treatments caused a severe rise in protein content (112% on average) compared to the control; however, 150 mM NaCl improved the protein content by 30.23% compared to the control (Fig. V).
Discussion
In salt-sensitive plants, chlorophyll concentration decreases significantly at high levels of NaCl; however, in salt-resistant plants, the concentration of chlorophyll is less affected by salt stress(Srivastava and Sharma, 2021). In the present study, different NaCl levels caused a significant decrease in Chl a, Chl b, total Chl, carotenoid content, and the performance index of photosynthesis. Similar to our findings, salinity significantly decreased chlorophyll a and b in Satureja hortensis (Mohammadi et al., 2019)and Satureja khuzestanica (Saadatfar and Jafari, 2024), as well as carotenoid content in Satureja hortensis (FABRIKI and MEHRABAD, 2016).
Under oxidative stress, enzymatic antioxidant activity increases and scavenges excessive ROS. These enhanced enzymatic activities ameliorate oxidative damage caused by stressful agents (Garcia-Caparros et al., 2021). In the present research, the antioxidant activity of SOD, POD, and CAT significantly increased in response to NaCl concentrations. In S. khuzestanica, different NaCl levels significantly increased the activity of SOD, POD, and CAT (Saadatfar and Jafari, 2024). These results confirm our findings.
In plants under osmotic stress, the accumulation of proline and other osmoprotectants increases. In the present research, the proline content significantly augmented in response to salt levels. Similar to our findings, salinity levels significantly increased the proline content in Satureja hortensis (Mohammadi et al., 2019), Satureja khuzestanica
(Saadatfar and Jafari, 2024), and Thymus danensis (Harati et al., 2015).
Low salt levels stimulate plant growth and cause the synthesis of de novo proteins; however, high salinity levels reduce the synthesis of proteins (Zhang et al., 2013). Also, a part of the proteins is decomposed in response to high salt (Hao et al., 2021). Different salt levels caused a significant increase in the protein content; however, this increase was limited at 150 mM NaCl compared to the other NaCl treatments. Similar to these results, low salinity treatments increased soluble protein, while high levels of NaCl significantly declined it in Thymus vulgaris (Harati et al., 2015).
Salinity reduces turgor pressure and interrupts the ionic balance between the plant and soil (Wang et al., 2023). Therefore, salinity strongly affects the plant's water status. The relative water content significantly decreased in response to different levels of NaCl; however, leaf electrical conductivity significantly increased. Similar to these findings, RWC significantly decreased in response to different salt concentrations in Lemon verbena (Ghanbari et al., 2023)and Oryza sativa (Jini and Joseph, 2017).
In the present study, NaCl caused a significant decrease in leaf fresh weight and leaf dry weight. A high salt concentration in the root zone reduces the osmotic potential of water in the surrounding roots. Therefore, the plant's access to water is reduced. A lack of water in the plant causes partial closure of the stomata, thus reducing the entry of CO₂ into the plant (Shanker et al., 2022). Reducing the absorption of CO₂ in plants diminishes photosynthesis and growth. Salinity causes ion toxicity (in the form of Na⁺ and Cl⁻). A high concentration of Na⁺ decreases nitrate reductase activity and inhibits the functioning of photosystem II ((Sheldon et al., 2017), which leads to a decrease in plant growth. Additionally, salinity causes nutrient deficiency (N, P, K, Zn, and Fe), which decreases plant growth and development (Sheldon et al., 2017).
The destruction of cell membranes due to salt is associated with a diminution in the absorption and transfer of nutrients through the roots, a decrease in the biosynthesis of chlorophyll, and an increase in the destruction of chlorophyllase due to salinity, which causes a decrease in plant growth and development.
Conclusion
The present study confirms that S. spicigera, to some extent, tolerates concentrations of less than 100 mM NaCl, but it is highly sensitive to concentrations greater than 100 mM NaCl, such that a salinity of 150 mM causes a significant decrease in photosynthesis and growth. Therefore, we do not recommend the cultivation of this plant in saline or semi-saline soil.
References
Afridi, M. S., T. Mahmood, A. Salam, T. Mukhtar, S. Mehmood, J. Ali, Z. Khatoon, M. Bibi, M. T. Javed and T. Sultan. 2019. Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: Involvement of ACC deaminase and antioxidant enzymes. Plant Physiology and Biochemistry, 139, 569-577.
Ahad, B., W. Shahri, H. Rasool, Z. Reshi, S. Rasool and T. Hussain. 2021. Medicinal plants and herbal drugs: An overview. Medicinal and aromatic plants: healthcare and industrial applications, 1-40.
Athar, H.-U.-R., F. Zulfiqar, A. Moosa, M. Ashraf, Z. U. Zafar, L. Zhang, N. Ahmed, H. M. Kalaji, M. Nafees and M. A. Hossain. 2022. Salt stress proteins in plants: An overview. Frontiers in Plant Science, 13, 999058.
Balasubramaniam, T., G. Shen, N. Esmaeili and H. Zhang. 2023. Plants’ response mechanisms to salinity stress. Plants, 12, (12) 2253.
Bates, L. S., R. Waldren and I. Teare. 1973. Rapid determination of free proline for water-stress studies. Plant and soil, 39, 205-207.
Beauchamp, C. and I. Fridovich. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical biochemistry, 44, (1) 276-287.
Bian, S. and Y. Jiang. 2009. Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Scientia Horticulturae, 120, (2) 264-270.
Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72, (1-2) 248-254.
Chance, B. and A. Maehly. 1955. [136] Assay of catalases and peroxidases.
Fabriki, O. S. and P. S. Mehrabad. 2016. The effects of drought and salt stresses on some morphological and biochemical parameters of savory (Satureja hortensis L.), 23-35.
Garcia-Caparros, P., L. De Filippis, A. Gul, M. Hasanuzzaman, M. Ozturk, V. Altay and M. T. Lao. 2021. Oxidative stress and antioxidant metabolism under adverse environmental conditions: a review. The Botanical Review, 87, 421-466.
Ghanbari, F., M. Bag-Nazari and A. Azizi. 2023. Exogenous application of selenium and nano-selenium alleviates salt stress and improves secondary metabolites in lemon verbena under salinity stress. Scientific Reports, 13, (1) 5352.
Hao, S., Y. Wang, Y. Yan, Y. Liu, J. Wang and S. Chen. 2021. A review on plant responses to salt stress and their mechanisms of salt resistance. Horticulturae, 7, (6) 132.
Harati, E., B. Kashefi and M. Matinzadeh. 2015. Investigation reducing detrimental effects of salt stress on morphological and physiological traits of (Thymus vulgaris) by application of salicylic acid. Iranian Journal of Plant Physiology, 5, (3) 1383-1391.
Hernández-Adasme, C., R. Palma-Dias and V. H. Escalona. 2023. The effect of light intensity and photoperiod on the yield and antioxidant activity of beet microgreens produced in an indoor system. Horticulturae, 9, (4) 493.
Jan, R., S. Asaf, M. Numan, Lubna and K.-M. Kim. 2021. Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy, 11, (5) 968.
Jini, D. and B. Joseph. 2017. Physiological mechanism of salicylic acid for alleviation of salt stress in rice. Rice Science, 24, (2) 97-108.
Kulak, M. 2020. Recurrent drought stress effects on essential oil profile of Lamiaceae plants: An approach regarding stress memory. Industrial Crops and Products, 154, 112695.
Kumar, R., A. Bohra, A. K. Pandey, M. K. Pandey and A. Kumar. 2017. Metabolomics for plant improvement: status and prospects. Frontiers in Plant Science, 8, 1302.
Kumar, S., M. A. Ahanger, H. Alshaya, B. L. Jan and V. Yerramilli. 2022. Salicylic acid mitigates salt induced toxicity through the modifications of biochemical attributes and some key antioxidants in Capsicum annuum. Saudi Journal of Biological Sciences, 29, (3) 1337-1347.
Lichtenthaler, H. K. and A. R. Wellburn. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Ltd.
Mohammadi, H., S. Hazrati and L. Parviz,2019. Morphophysiological and biochemical response of savory medicinal plant using silicon under salt stress. Proc. Annales Universitatis Mariae Curie-Sklodowska, sectio C–Biologia, 72:29-40:
Reddy, A. R., K. Chaitanya, P. Jutur and K. Sumithra. 2004. Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environmental and experimental botany, 52, (1) 33-42.
Saadatfar, A. and S. H. Jafari. 2024. Application of 24-epibrassinolide as an Environmentally Friendly Strategy Alleviates Negative Effects of Salinity Stress in Satureja khuzistanica Jamzad. Journal of Rangeland Science, 14, (3).
Shanker, A. K., D. Gunnapaneni, D. Bhanu, M. Vanaja, N. J. Lakshmi, S. K. Yadav, M. Prabhakar and V. K. Singh. 2022. Elevated CO2 and water stress in combination in plants: brothers in arms or partners in crime? Biology, 11, (9) 1330.
Sheldon, A. R., R. C. Dalal, G. Kirchhof, P. M. Kopittke and N. W. Menzies. 2017. The effect of salinity on plant-available water. Plant and Soil, 418, 477-491.
Sinha, A. K. 1972. Colorimetric assay of catalase. Analytical biochemistry, 47, (2) 389-394.
Srivastava, S. and P. Sharma. 2021. Effect of NaCl on chlorophyll fluorescence and thylakoid membrane proteins in leaves of salt sensitive and tolerant rice (Oryza sativa L) varieties. Journal of Stress Physiology & Biochemistry, 17, (2) 35-44.
Wang, Y., W. Ma, H. Fu, L. Li, X. Ruan and X. Zhang. 2023. Effects of salinity stress on growth and physiological parameters and related gene expression in different ecotypes of Sesuvium portulacastrum on Hainan Island. Genes, 14, (7) 1336.
Zarei, B., A. Fazeli and Z. Tahmasebi. 2019. Salicylic acid in reducing effect of salinity on some growth parameters of Black cumin (Nigella sativa). Journal of Plant Process and Function, 8, (29) 287-298.
Zhang, M., Y. Fang, Y. Ji, Z. Jiang and L. Wang. 2013. Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. South African journal of botany, 85, 1-9.
