Home Physio-biochemical analyses in seedlings of sorghum-sudangrass hybrids that are grown under salt stress under in vitro conditions
Article Publicly Available

Physio-biochemical analyses in seedlings of sorghum-sudangrass hybrids that are grown under salt stress under in vitro conditions

  • Ramazan Beyaz ORCID logo EMAIL logo and Hakan Kır ORCID logo
Published/Copyright: November 14, 2019
Download Article (PDF)
Turkish Journal of Biochemistry
From the journal Turkish Journal of Biochemistry Volume 45 Issue 2

Abstract

Objective

This study was conducted to analyze the physio-biochemical responses of two sorghum-sudangrass (Sorghum bicolor × Sorghum Sudanese Stapf.) hybrid (“Aneto” and “Sugar Graze”) seedlings exposed to salt stress.

Materials and methods

Sorghum-sudangrass hybrid seeds sown in MS medium containing 50 and 100 mM NaCl. The activity of antioxidant enzymes (SOD, CAT, GR, APX), chlorophyll (a, b, and total), malondialdehyde (MDA), and proline levels measured in 14 days old seedlings.

Results

As a result of the study, the activity of antioxidant enzymes (CAT, SOD, APX, and GR), malondialdehyde (MDA), proline and chlorophyll contents of seedlings of cv. “Aneto” increased. On the other hand, SOD activity, proline, and chlorophyll content increased while CAT, APX, GR activity, and malondialdehyde (MDA) content decreased in seedlings of cv. “Sugar graze”.

Conclusion

Overall, the results showed that the cv. “Aneto” was less affected by the adverse effects of salt stress than the cv. “Sugar graze”. This study is essential for revealing biochemical responses of 14 days old Sorghum-Sudanese hybrid seedlings against salt stress. These study findings can use in breeding programs for sorghum plants.

Öz

Amaç

Bu çalışma, tuz stresine maruz burakılan iki sorgum-sudangrass (Sorghum bicolor ×Sorghum sudanense Stapf.) hibrit (“Aneto” ve “Sugar Graze”) fidelerinin fizyo-biyokimyasal tepkilerini analizi için yapılmıştır.

Gereç ve Yöntem

Sorgum-sudangrass hibrid tohumları içerisinde 50 ve 100 mM NaCl içeren MS ortamlarına ekilmiştir. 14 günlük fidelerde, antioksidant enzimlerin aktivitleri (SOD, CAT, GR, APX), klorofil (a, b ve toplam), malondialdehit (MDA) ve prolin seviyeleri ölçülmüştür.

Bulgular

Çalışma sonucunda, “Aneto” çeşidinin fidelerinde, antioksidant enzimlerin (CAT, SOD, APX ve GR) aktivitesi, malondialdehit (MDA), prolin ve klorofilin içerikleri artmıştır. Diğer taraftan, “Sugar graze” çeşidin fidelerinde, SOD aktivitesi, prolin ve klorofil içeriği artarken, CAT, APX, GR aktivitesi ve malondialdehit (MDA) içeriği azalmıştır.

Sonuç

Genel olarak, sonuçlar tuz stresinin olumsuz etkilerinden “Sugar graze” çeşidi ile kıyaslandığında “Aneto” çeşidinin daha az etkilendiği göstermiştir. Bu çalışma, 14 günlük Sorgum-Sudanotu melez fidelerin tuz stresine karşı biyokimyasal tepkilerini ortaya çıkarması bakımından önemlidir. Sorgum bitki için ıslah programlarında bu çalışma bulguları kulanılabilir.

Keywords: Salt (NaCl) stress; Antioxidant enzymes; Proline; Malondialdehyde (MDA); Chlorophyll
Anahtar kelimeler: Tuz (NaCL) stresi; aktioksidan enzimler; prolin; malondialdehid (MDA); klorofil

Introduction

Salinity is a major problem in agriculture and crop production [1]. It is known to limit plant performance through a decrease in plant growth and yield [2]. More 6% of the land in the entire world (more than 800 million ha of land) is affected by salt [3]. Wang et al. [4] and Jha et al. [5] highlighted emphasized the increasing ratios of salt-stressed areas and predicted an almost 30% loss in land based on salt stress in the next 25 years. Therefore, this environmental stress factor continuously increases its impact. Although there are many ways to fight this stress factor, the farming salt-tolerant plants has been considered as the most economical and effective way to utilize saline-alkali land. Salinity stress influences a plant at its all stages of growth; however, for most plants, stages of seed germination and seedling growth are known to be more susceptible [6], [7]. Moreover, the stages of germination and early seedling are indications of plant growth reactions to salt stress [6]. Salt tolerance in plants is a complicated issue that is dependent on several associated factors regarding biochemical and physiological processes [8]. Therefore, revealing the physio-biochemical mechanism of salt tolerance is needed to improve the tolerance of plants to salt stress [9]. Salinity influences many aspects of plant physio-biochemical processes including antioxidant enzymes’ activities, proline accumulation and photosynthesis. Many studies showed that these physio-biochemical processes are related to salt tolerance in many plants, and they affect the plant’s acclimation in saline environments [6], [10], [11].

Sorghum is a C4 plant, known by its high photosynthetic capacity and high yield and its high tolerance of stressors (drought, radiation and solar heat), including salt [2], [12]. However, salt stress gravely influences the growth and development of sorghum, which is a significant plant grown in arid and semiarid regions [13]. Sorghum’s tolerance to high-salinity conditions appears to differ based on the genotype [14]. Salt stress tolerance in types (grain sorghum, forage or sweet sorghum, sudangrass and sorghum-sudangrass hybrids) of sorghum plants has been investigated in previous studies by Chaugool et al. [14], de Lacerdaa et al. [15], Yan et al. [16] and Patane et al. [17]. However, there is limited information about the physio-biochemical responses of sorghum-sudangrass hybrids to salt stress. Therefore, here, the effects of salt (NaCl) stress on physio-biochemical variables were characterized on two sorghum-sudangrass hybrids’ seedlings under in vitro conditions. The significance of this study was that it revealed the physio-biochemical responses of Sorghum-Sudangrass hybrids’ seedlings in their early growth stage to salt stress.

Materials and methods

Plant materials

Seeds of two sorghum-sudangrass hybrids (“Aneto” and “Sugar graze”) (Sorghum bicolor×Sorghum sudanense Stapf.) were utilized as plant material in this study. The seeds were obtained from the Field Crop Central Research Institute (Ankara, Turkey) and the Ulusoy Seed Company (Ankara, Turkey).

Seed surface sterilization, germination of seeds in in vitro conditions, in vitro application of salt stress

The sorghum (cv. “Aneto” and cv. “Sugar graze”) seeds were kept in a 50% commercial bleach solution (ACE-Turkey, containing 5% sodium hypochlorite) for 20 min for surface sterilization and then rinsed thrice by sterile distilled water. The sterilized samples were planted into an MS (Murashige and Skoog) [18] basal medium containing 3% sucrose and 50 and 100 mM of sodium chloride (NaCl). It was solidified by 0.65% agar. All the cultures were kept under white fluorescent light (27 μmol m−2 s−1) in a light-dark cycle of 16 h of light and 8 h of dark at 24±1°C.

Biochemical analysis

Contents of chlorophyll and malondialdehyde (MDA) proline, and activities of antioxidative enzymes (CAT, SOD, GR and APX) were evaluated in the shoot tissues of 14-day-old sorghum seedlings (Figure 1).

Figure 1: The 14-day-old sorghum hybrids seedlings that exposed to salt (NaCl) stress (0, 50, and 100 mM) under in vitro condititons.
Figure 1:

The 14-day-old sorghum hybrids seedlings that exposed to salt (NaCl) stress (0, 50, and 100 mM) under in vitro condititons.

Chlorophyll content

The protocol proposed by Curtis and Shetty [19] was used to determine the chlorophyll a, chlorophyll b and total chlorophyll compositions of the shoot of the plants on which different doses of NaCl were applied. By following the protocol, 50mg of green material was added into 3mL of methanol and stored at 23°C in darkness for 2 h to allow the chlorophyll in the green material to dissolve into the methanol. Then, the optic density (OD) of 1.5mL of the liquid part (the chlorophyll-containing methanol) was determined at 650 and 665nm using a spectrophotometer, and the chlorophyll a, chlorophyll b and total chlorophyll quantities were determined in units of “μg chlorophyll/g of fresh tissue”.

Measurement proline and lipid peroxidation (MDA content)

Drawing on Lutts et al.’s [20] method, the malondialdehyde (MDA) contents were identifined. Five milliliter of trichloroacetic acid (TCA) (0.1%) was added onto 200 mg of green leaves as a specimen, and later, centrifuged at 12,500 rpm for around 20 min. Three milliliter of the supernatant was obtained from 5 mL of each extract. Three milliliter of 0.1% thiobarbituric acid mixed with 20% trichloroacetic acid (w/v) was complemented to the same amounts of all supernatants. The A-absorbance of the specimens was measured spectrophotometrically at 532 and 600 nm using a spectrophotometer.

Following the method described by Bates et al. [21], using 3% sulfosalicylic acid to break fresh plant specimens, a proline assay was performed. The ninhydrin reagent was put to the tubes that had the crushed specimens, and then, put in a water bath at the temperature of 100°C for almost an hour. Following a cool-down process, 4 mL of toluene was put into each specimen. The specimens were examined at 520 nm.

Antioxidant enzyme analyses

To find out the effects of the enzyme in plants under high-salinity conditions, almost 0.5g of fresh shoot specimens in liquid nitrogen were powdered in porcelain mortars and homogenized with 8mL of a 50-mM phosphate buffer solution, which had 0.1mM of Na-EDTA (pH of 7.6). The homogenized specimens were centrifuged at 15,000g for 15 min, and the precipitates that were formed were utilized in the enzyme analyses. The specimens were stored at +4°C up to the point the enzyme analyses were conducted. In enzyme measurements, the ultimate volume values were received by utilizing the buffer solution.

Superoxide dismutase (SOD) activity

Following the methods described by Çakmak and Marschner and Çakmak et al., we examined the superoxide dismutase (SOD) activity [22], [23] through the decrease of NBT (nitro blue tetrazolium chloride) by O 2 − in light. All mixtures were introduced to the reaction medium. 0.1mM of Na-EDTA, including a 50 mM (pH: 7.6) phosphate (P) buffer. The enzyme extract (25 to 100μL) before 0.5mL of 50mM Na2CO3 (pH of 10.2), 0.5mL of 12mM of L-methionine, 0.5mL and 75μM of p-nitro blue tetrazolium chloride (NBT) and 10μm of riboflavin were all put into the medium. Hence, the ultimate volume of the medium reached 5mL. The specimens were in light under light for around 15 min, and calculations were performed at the wavelength of 560nm.

Ascorbate peroxidase (APX) activity

The ascorbate peroxidase (APX) activity was calculated [22], [23] by focusing on the oxidation of ascorbate at 290nm (E=2.8mMcm−1). The ultimate volume of the reaction medium was set at 1mL by adding 0.1mM of EDTA including a 50-mM phosphate buffer (pH of 7.6), 0.1mL and 10mM of EDTA including 12mM of H2O2, 0.1mL and 0.25mM of L-ascorbic acid and enzyme extract within the medium. Afterwards, the ascorbate contents were was calculated spectrophotometrically at 290nm.

Glutathione reductase (GR) activity

The glutathione reductase (GR) activity was calculated using the technique proposed by Çakmak and Marschner [22] and Çakmak et al. [23], and the oxidation process of NADPH at the wavelength of 340nm (E=6.2mMcm−1). The ultimate volume of the reaction medium was set at 1mL by introducing 0.1mM of EDTA that included a 50-mM phosphor buffer (pH of 7.6), 0.1mL and 0.5mM of oxidized glutathione (GSSG), 0.1mL and 0.12mM of NADPH and enzyme extract within the medium. The level of NADPH oxidation was calculated spectrophotometrically at the wavelength of 340nm.

Catalase (CAT) activity

The catalase activity (CAT) was measured based on the degradation rate of H2O2 at 240nm (E=39.4mMcm−1) [22], [23]. In this enzyme analysis, the ultimate volume of the reaction medium was set at 1mL through introducing 0.1mM of EDTA which had a 50-mM phosphate buffer (pH of 7.6), 0.1mL and 100mM of H2O2 and enzyme extract within the reaction medium.

Statistical analysis

The experiment was conducted according to the “Completely Randomized Block Design” concept. One-way ANOVA (Analysis of Variance) was performed on each experiment, and the mean values were compared using Duncan’s multi-range tests with the “SPSS for Windows” software.

Results

The responses of antioxidant enzymes (CAT, SOD, GR and APX) in the shoot tissues of 14-day-old seedlings of cv. “Sugar graze” are presented in Table 1. The activity of antioxidant enzymes was significantly (p<0.01) affected by salt stress in cv. “Sugar graze” seedlings. Our results showed that CAT, APX and GR activities reduced by 2.67, 1.31 and 1.04-fold, respectively. Moreover, SOD activity increased by 1.08-fold in comparison to the control group with the highest degree (100 mM) of salt treatment (Table 1). The contents of proline and chlorophyll (chl. a, and total chl.) significantly (p<0.01) increased by 9.16, 3.12, and 1.66-fold in the highest degree (100 mM) of salt stress treatment in comparison to the control group. Furthermore, compared the highest degree (100 mM) of salt treatment, MDA and chl. b contents were reduced by 1.31 and 1.05-fold, respectively.

Table 1:

Physio-biochemical responses of 14-day-old seedlings of sorghum (cv. “Sugar graze”) to salt (NaCl) stress.

NaCl concentration (mM) Activity of antioxidant enzymes
 Content of (μmol/g of fresh tissue)
 Content of chlorophyll (μg/g fresh tissue)
CAT** (μmol min–1 mg–1 FW) SOD* (U min–1 mg–1 FW) APX** (μmol min–1 mg–1 FW) GR** (μmol min–1 mg–1 FW) MDA* Proline** a** b** Total**
0 155.35±0.0a 330.15±2.5b 50.89±1.7a 171.02±1.2a 13.08±1.2a 2.16±0.4c 224.99±1.9c 226.82±2.4a 327.94±4.4c
50 119.12±1.8b 154.41±2.1c 32.60±2.1b 157.68±2.2c 10.60±1.0a,b 9.03±1.7b 588.44±2.9b 160.02±1.7c 440.61±3.6b
100 58.20±1.9c 358.60±6.7a 38.89±6.0b 164.53±4.5b 9.91±1.5b 19.87±4.1a 699.23±1.3a 214.20±1.5b 546.72±2.6a

  1. MDA, Malondialdehyde; SOD, superoxide dismutase; CAT, catalase; APX, ascorbate peroxidase; GR, glutathione reductase. The values indicated in each column with a different letter were statistically significant at **p<0.01 and *p<0.05 levels. The values represent the mean±SD calculated on the basis of results of three replicate experiments.

The changing in antioxidant enzyme (CAT, SOD, GR and APX) activities of the shoot tissues of 14-day-old seedlings of cv. “Aneto” are shown in Table 2. The salt stress significantly (p<0.01, and p<0.05 for CAT) affected the antioxidant enzyme activities in the seedlings of cv. “Aneto”. It was found that 1.31, 1.95, 1.96 and 1.04-fold increasing in CAT, SOD, APX and GR activities, respectively, in comparison to the control group with the highest degree (100 mM) of salt treatment (Table 2). In terms of MDA, proline and chlorophyll contents (chl. a, chl. b and total chl.), 1.30, 3.31, 1.96, 1.29 and 1.62-fold increases were, respectively, in comparison to the control group with the highest degree (100 mM) of salt treatment.

Table 2:

Physio-biochemical responses of 14-day-old seedlings of sorghum (cv. “Aneto”) to salt (NaCl) stress.

NaCl concentration (mM) Activity of antioxidant enzymes
 Content of (μmol/g of fresh tissue)
 Content of chlorophyll (μg/g fresh tissue)
CAT* (μmol min–1 mg–1 FW) SOD** (U min–1 mg–1 FW) APX** (μmol min–1 mg–1 FW) GR** (μmol min–1 mg–1 FW) MDA* Proline** a** b** Total**
0 41.19±2.0b 151.36±7.2b 27.31±6.7b 170.48±2.5b 7.26±2.2b 1.71±0.0b 246.63±4.8c 108.08±1.7b 224.16±0.7b
50 54.28±6.2a 96.50±4.0c 52.22±4.2a 171.20±0.8b 17.17±3.5a 2.98±0.1b 303.00±8.8b 60.08±4.5c 145.49±1.0c
100 54.14±1.6a 295.61±4.3a 53.52±0.9a 177.68±0.4a 9.47±2.6b 5.67±1.9a 470.17±11.7a 140.67±2.3a 364.39±5.1a

  1. MDA, Malondialdehyde; SOD, superoxide dismutase; CAT, catalase; APX, ascorbate peroxidase; GR, glutathione reductase. The values indicated in each column with a different letter were statistically significant at **p<0.01 and *p<0.05 levels. The values represent the mean±SD calculated on the basis of results of three replicate experiments.

Discussion

The influence of various contents of NaCl (50 and 100 mM) was investigated on physio-biochemical changes in two sorghum-sudangrass (Sorghum bicolor×Sorghum sudanense Stapf.) hybrids’ (“Aneto” and “Sugar graze”) seedlings under in vitro conditions. The findings of present study show that the physio-biochemical responses of these hybrids to salt concentrations were different.

Activity of antioxidant enzymes

Abiotic stresses (including salt stress) lead to harm in plants in part by stimulating excessive production of reactive oxygen species (ROS), which causes cellular damage and prevention of physiological functions in plants. Collection of ROS such as hydroxyl radicals (HO˙) and singlet oxygen (1O2) in the cell end up with oxidation of different biochemical substances: lipids, proteins, DNA and RNA [24]. On the other hand, plants have developed antioxidative processes to survive ROS production and accumulation processes. One of such processes is enzymatic components including catalase (CAT), superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione reductase (GR).

When exposed to salt stress, the antioxidative enzyme system (CAT, SOD, APX, and GR) increased in comparison to the control group with the highest degree (100 mM) of salt treatment seemed to function better in cv. “Aneto” than in cv. “Sugarcane” (Tables 1 and 2). Meanwhile, the decreased activities of CAT, APX and salt-treated GR in cv. “Sugar graze” indicated that these enzymes might not have an indispensable part for scavenging superoxide radicals under salt stress. Similarly, decreases in the activity of some antioxidant enzymes such as SOD and CAT were shown by Reddy et al. [13] and Sundar et al. [25] in sorghum plants that were exposed to salt and water stress, respectively. Dugasa et al. [26] reported that SOD, APX and CAT activity increased in wheat that combined species of sorghum genotypes. Sen and Alikamanoglu [27] stated that functions of the antioxidant enzymes SOD, CAT and POD increased in salt stress conditions in all wheat varieties. Reddy et al. [13] noted that SOD, CAT and GR activity increased in transgenic sorghum under salt stress. Additionally, Elsawy et al. [28] observed that salt treatment causes elevated antioxidant enzyme (CAT, APX, sPOD, GR and SOD) activities in barley cultivars.

Mitigation of oxidative harm by scavenging ROS by utilizing antioxidant enzymes is a significant tactic of plants for raising their tolerance to stress [13]. Kholova et al. [29] reported that functions of superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT) and glutathione reductase (GR) rose depending on salt stress levels in maize genotypes. The results suggested that the CAT-SOD-APX-GR system protects cv. “Aneto” from oxidative damage under salinity stress conditions, while these protections systems (except, SOD) are invalid for cv. “Aneto”. Elsawy et al. [28] observed that antioxidant activity in general was higher in tolerant cultivars than sensitive varieties in barley (Hordeum vulgare L.) under salt stress. Molazem and Bashirzadeh [30] stated that antioxidant enzyme activity such as SOD in salinity-resistant varieties of maize increased sharply. In this study, the results showed that antioxidant enzymes (CAT, SOD, APX and GR) seem to be more active in cv. “Aneto” than in cv. “Sugar graze” under salt stress. Therefore, it may be speculated that cv. “Aneto” might be a salt tolerant hybrid due to a strong antioxidant mechanism.

Contents of proline, MDA and chlorophyll

Among the osmoprotectants, proline (Pro) is one of the more efficient osmolytes used for improving salt tolerance in crops [31]. In this study, the results clearly showed that proline accumulation significantly (p<0.01) increased in both hybrids’ (“Aneto” and “Sugar graze”) seedlings under salt stress. However, the accumulation of proline was greater in cv. “Sugar graze”. Bavei et al. [32] reported that proline contents increase with the increasing salt stress in different sorghum varieties. Colmer et al. [33] stated that salt stress causes effects on the contents of proline in Sorghum bicolor (cv. “Hegari”) seedlings. The findings that were reached here were also in parallel to those obtained by Luo et al. [34] and Wang et al. [35] who emphasized increased proline accumulation in maize that combined species of sorghum under salt stress. Proline also interacts with cellular macromolecules including substances like enzymes/proteins and stabilizes the structure and function of such substances under stressors’ effects, including NaCl [13], [29], [36]. Therefore, it may be speculated that the high proline accumulation in the seedlings of cv. “Sugar graze” was due to low activity of antioxidant enzymes like CAT, APX and GR in salinity stress conditions. On the other hand, the low proline accumulation in the seedlings of cv. “Aneto” was due to high activity of all antioxidant enzymes.

The primary marker of oxidative stress in plants is MDA, which is a degradation product of polyunsaturated fatty acids of bio-membranes [37]. MDA is considered as a suitable marker for membrane lipid peroxidation. In this study, the results showed that the MDA contents increased in cv. “Aneto” while decreasing in cv. “Sugarcane” in comparison to the control group with the highest degree (100 mM) of salt stress (Tables 1 and 2). Du et al. [38] reported that proline contents had negative correlations with MDA contents under water deficits. Therefore, this may explain the decreasing MDA contents in the seedlings of cv. “Sugar graze” with high proline accumulation (Table 1). On the other hand, increasing the MDA contents in cv. “Aneto” seedlings might explain the insufficient degree of proline accumulation. Maswada et al. [39] stated that MDA contents increase in sorghum seedlings under salt stress (150 mM).

Photosynthesis is tightly associated with the yield of plants but prone to be influenced by salt stress. Decline of photosynthetic capacity prevalently occurred in plants under salt stress, but the underlying processes are complicated and not clear. In this study, interestingly, chlorophyll contents (except, chl b. in cv. “Sugar graze”) increased in both hybrid leaves under salt stress (Tables 1 and 2). Shah et al. [40] reported that salinity-induced increases in pigment contents were enhanced in wheat. On the other hand, Yan et al. [16] reported that during salt treatment with 50 and 150 mM NaCl, the photosynthetic rate (Pn) decreased in sorghum. However, several studies have shown that salinity stress decreased the concentrations of chlorophyll contents in maize that combined species of sorghum under salt stress [29], [30]. The reasons for increased chlorophyll content in seedling might be as a part of the adaptive mechanism of sorghum hybrids. In this study, the chlorophyll contents seemed to have a higher in cv. “Aneto” than in cv. “Sugar graze” under salt stress. Therefore, it might be speculated that cv. “Aneto” is a more tolerant hybrid against salt stress.

Conclusions

In this study, the two sorghum-sudangrass hybrids reacted differently to different concentrations of NaCl. According to physio-biochemical responses, cv. “Aneto” seemed to be more tolerant to oxidative damage provoked by salt stress than cv. “Sugar graze.” Based on the results of this study, SOD, proline and chlorophyll contents seem to be reliable physio-biochemical parameters in determining tolerant or susceptible hybrids in sorghum plants under salt stress.

Acknowledgements

The authors thank the Biotechnology Institute of Ankara University (Turkey) for using their facility for conducting the laboratory work.

References

1. Forghanı AH, Almodares A, Ehsanpour AA. Potential objectives for gibberellic acid and paclobutrazol under salt stress in sweet sorghum (Sorghum bicolor [L.] Moench cv. Sofra). Appl Biol Chem 2018;61:113–24.10.1007/s13765-017-0329-1Search in Google Scholar

2. Desokya ES, Merwadb AR, Rady MM. Natural biostimulants ımprove saline soil characteristics and salt stressed-sorghum performance. Commun Soil Sci Plant Anal 2018;49: 967–83.10.1080/00103624.2018.1448861Search in Google Scholar

3. Saddıqe Z, Javerıa S, Khalıd H, Farooq A. Effect of salt stress on growth and antioxidant enzymes in two cultivars of maize (Zea Mays L.). Pak J Bot 2016;48:1361–70.Search in Google Scholar

4. Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 2003;218:1–14.10.1007/s00425-003-1105-5Search in Google Scholar PubMed

5. Jha UC, Bohra A, Jha R, Parida SK. Salinity stress response and ‘omics’ approaches for improving salinity stress tolerance in major grain legumes. Plant Cell Reports 2019;38:255–77.10.1007/s00299-019-02374-5Search in Google Scholar PubMed

6. Cuartero J, Bolarin MC, Asins MJ, Moreno V. Increasing salt tolerance in the tomato. J Exp Bot 2006;57:1045–58.10.1093/jxb/erj102Search in Google Scholar PubMed

7. Bybordı A. The ınfluence of salt stress on seed germination, growth and yield of canola cultivars. Not Bot Hort Agrobot Cluj 2010;38:128–33.Search in Google Scholar

8. Ashraf M. Effect of sodium chloride on water relations and some organic osmotica in arid zone plant species Melilotus indica (L.) All. Tropenlandwir 1993;94:95–102.Search in Google Scholar

9. Yang Z, Wang Y, Weı X, Zhao X, Wang B, Suı N. Transcription profiles of genes related to hormonal regulations under salt stress in sweet sorghum. Plant Mol Biol Rep 2017;35:586–99.10.1007/s11105-017-1047-xSearch in Google Scholar

10. Ghaderı N, Hatamı M, Mozafarı A, Sıosehmardeh A. Change in antioxidant enzymes activity and some morphophysiological characteristics of strawberry under long-term salt stress. Physiol Mol Biol Plants 2018;24:833–43.10.1007/s12298-018-0535-2Search in Google Scholar PubMed PubMed Central

11. Uzal Ö. The effect of GA3 applications at different doses on lipidperoxidation, chlorophyll, and antioxidant enzyme activities in pepper plants under salt stress. Fresen Envıron Bull 2017;26:5283–8.Search in Google Scholar

12. Zhang H, Xu N, Wu X, Wang J, Ma S, Lı X, et al. Effects of four types of sodium salt stress on plant growth and photosynthetic apparatus in sorghum leaves. J Plant Interact 2018;13:506–13.10.1080/17429145.2018.1526978Search in Google Scholar

13. Reddy PS, Jogeswar G, Rasınenı GK, Maheswarı M, Reddy AR, Varshney RK, et al. Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 2015;94:104–13.10.1016/j.plaphy.2015.05.014Search in Google Scholar PubMed

14. Chaugool J, Naıto H, Kasuga S, Ehara H. Comparison of young seedling growth and sodium distribution among sorghum plants under salt stress. Plant Prod Sci 2013;16:261–70.10.1626/pps.16.261Search in Google Scholar

15. Lacerdaa CF, Cambraıab J, Olıva MA, Ruız HA. Changes in growth and in solute concentrations in sorghum leaves and roots during salt stress recovery. Environ Exper Bot 2005;54:69–76.10.1016/j.envexpbot.2004.06.004Search in Google Scholar

16. Yan K, Chen P, Shao H, Zhao S, Zhang L, Zhang L, et al. Responses of photosynthesis and photosystem II to higher temperature and salt stress in sorghum. J Agronomy Crop Science 2013;198:218–26.10.1111/j.1439-037X.2011.00498.xSearch in Google Scholar

17. Patane C, Saıta A, Sortıno O. Comparative effects of salt and water stress on seed germination and early embryo growth in two cultivars of sweet sorghum. Agro Crop Sci 2013; 199:30–7.10.1111/j.1439-037X.2012.00531.xSearch in Google Scholar

18. Murashıge T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 1962;15:473–97.10.1111/j.1399-3054.1962.tb08052.xSearch in Google Scholar

19. Curtıs OF, Shetty K. Growth medium effects on vitrification, total phenolics, chlorophyll, and water content of in vitro propagated oregano clones. Acta Horticulture 1996;426:498–503.10.17660/ActaHortic.1996.426.53Search in Google Scholar

20. Lutts S, Kıne JM, Bouharmont J. NaCl-ınduced senesence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 1996;78:389–98.10.1006/anbo.1996.0134Search in Google Scholar

21. Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water stress studies. Plant Soil 1973;39:205–7.10.1007/BF00018060Search in Google Scholar

22. Cakmak I, Marschner H. Magnesium defficiency and higlight ıntensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol 1992;98:1222–6.10.1104/pp.98.4.1222Search in Google Scholar

23. Çakmak I, Atlı M, Kaya R, Evliya H, Marschner H. Association of high light and zinc deficiency in cold-ınduced leaf chlorosis in grapefruit and mandarin trees. J Plant Physiol 1995;146: 355–60.10.1016/S0176-1617(11)82068-7Search in Google Scholar

24. Tripathy BC, Oelmüller R. Reactive oxygen species generation and signaling in plants. Plant Signal Behav 2012;7:1621–33.10.4161/psb.22455Search in Google Scholar PubMed PubMed Central

25. Sundar D, Perıanayaguy B, Reddy R. Localization of antioxidant enzymes in the cellular compartments of sorghum Leaves. J Plant Growth Regul 2004;44:157–63.10.1023/B:GROW.0000049418.92833.d6Search in Google Scholar

26. Dugasa MT, Cao F, Ibrahim W, Wu F. Differences in physiological and biochemical characteristics in response to single and combined drought and salinity stresses between wheat genotypes differing in salt tolerance. Physiol Plant 2019;165: 134–43.10.1111/ppl.12743Search in Google Scholar

27. Şen A, Alikamanoğlu S. Effect of salt stress on growth parameters and antioxidant enzymes of different wheat (Triticum Aestivum L.) varieties on ın vitro tissue culture. Fresen Envıron Bull 2011;20:489–95.Search in Google Scholar

28. Elsawy HI, Mekawy AM, Elhity MA, Abdel-Dayem SM, Abdelaziz MN, Assaha DV, et al. Differential responses of two Egyptian barley (Hordeum vulgare L.) cultivars to salt stress. Plant Physiol Biochem 2018;127:425–35.10.1016/j.plaphy.2018.04.012Search in Google Scholar

29. Kholova J, Saıram RK, Meena RC. Osmolytes and metal ions accumulation, oxidative stress and antioxidant enzymes activity as determinants of salinity stress tolerance in maize genotypes. Acta Physiol Plant 2010;32:477–86.10.1007/s11738-009-0424-ySearch in Google Scholar

30. Molazem D, Bashırzadeh A. Impact of salinity stress on proline reaction, peroxide activity, and antioxidant enzymes in maize (Zea mays L.). Pol J Environ Stud 2015;24: 597–603.10.15244/pjoes/29691Search in Google Scholar

31. Butt M, Ayyub CM, Amjad M, Ahmad R. Proline application enhances growth of chilli by ımproving physiological and biochemical attributes under salt stress. Pak J Agri Sci 2016;53:43–9.10.21162/PAKJAS/16.4623Search in Google Scholar

32. Bavei V, Shiran B, Arzani A. Evaluation of salinity tolerance in sorghum (Sorghum bicolor L.) using ion accumulation, proline and peroxidase criteria. Plant Growth Regul 2011;64:275–85.10.1007/s10725-011-9568-zSearch in Google Scholar

33. Colmer TD, Fan TW, Higashi RM, Läuchli A. Interactive effects of Ca2 and NaCl salinity on the ionic relations and proline accumulation in the primary root tip of Sorghum bicolor. Physiol Plant 1996;97:421–4.10.1111/j.1399-3054.1996.tb00498.xSearch in Google Scholar

34. Luo M, Zhao Y, Zhang R, Su A, Li C, Xiangpeng W, et al. Effect of saline stress on the physiology and growth of maize hybrids and their related inbred lines. Maydica 2017;62:1–8.Search in Google Scholar

35. Wang Y, Jia D, Guo J, Zhang X, Guo C, Yang Z. Antioxidant metabolism variation associated with salt tolerance of six maize (Zea mays L.) cultivars. Acta Ecol Sin 2017;37:368–72.10.1016/j.chnaes.2017.08.007Search in Google Scholar

36. Smırnoff N, Cumbes QT. Hydroxyl radicals scavenging activity of compatible isolates. Phytochemistry 1989;28:1057–60.10.1016/0031-9422(89)80182-7Search in Google Scholar

37. Demıral T, Turkan I. Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 2005;53:247–57.10.1016/j.envexpbot.2004.03.017Search in Google Scholar

38. Du F, Shi H, Zhang X, Xu X. Responses of reactive oxygen scavenging enzymes, proline and malondialdehyde to water deficits among six secondary successional seral species in loess plateau. Plos One 2014;9:1–6.10.1371/journal.pone.0098872Search in Google Scholar PubMed PubMed Central

39. Maswada HF, Djanaguiraman M, Prasad PV. Seed treatment with nano-iron (III) oxide enhances germination, seeding growth and salinity tolerance of sorghum. J Agro Crop Sci 2018;204:577–87.10.1111/jac.12280Search in Google Scholar

40. Shah SH, Houborg R, Mccabe M. Response of measurement to salinity and nutrient stress in wheat (Triticum aestivum L.). Agronomy 2017;7:1–20.10.3390/agronomy7030061Search in Google Scholar
Received: 2019-01-11
Accepted: 2019-04-18
Published Online: 2019-11-14
Published in Print: 2020-04-28

©2019 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Review Article
  3. Lipidomics and cognitive dysfunction – A Narrative review
  4. Research Articles
  5. Effects of topiramate on adipocyte differentiation and gene expression of certain carbonic anhydrase isoenzymes
  6. Heterologous expression of a plant WRKY protein confers multiple stress tolerance in E. coli Bir bitkinin heterolog ifadesi WRKY proteini çoklu stres yaratır E. coli’de tolerans
  7. Cytogenetic impact of sodium chloride stress on root cells of Vigna radiata L. seedlings
  8. Understanding the impacts of self-shuffling approach on structure and function of shuffled endoglucanase enzyme via MD simulations
  9. Evaluation ofTrichoderma atroviride and Trichoderma citrinoviride growth profiles and their potentials as biocontrol agent and biofertilizer
  10. Physio-biochemical analyses in seedlings of sorghum-sudangrass hybrids that are grown under salt stress under in vitro conditions
  11. The structural diversity of ginsenosides affects their cholinesterase inhibitory potential
  12. Extracellular acidity and oxygen availability conjointly control eukaryotic cell growth via modulation of cytoplasmic translation
  13. Genome-wide identification, phylogeny and expression analysis of G6PC gene family in common carp, Cyprinus carpio
  14. The effect of Diplotaenia turcica root extract in streptozotocin-induced diabetic rats
  15. Letter to the Editor
  16. Metabolomics analysis of medicinal insect Protaetia brevitarsis after Bacillus subtilis fermentation
  17. Opinion Paper
  18. Identifying and solving scientific problems in the medicine: key to become a competent scientist
https://doi.org/10.1515/tjb-2018-0552
Keywords for this article
Salt (NaCl) stress; Antioxidant enzymes; Proline; Malondialdehyde (MDA); Chlorophyll

Articles in the same Issue

  1. Frontmatter
  2. Review Article
  3. Lipidomics and cognitive dysfunction – A Narrative review
  4. Research Articles
  5. Effects of topiramate on adipocyte differentiation and gene expression of certain carbonic anhydrase isoenzymes
  6. Heterologous expression of a plant WRKY protein confers multiple stress tolerance in E. coli Bir bitkinin heterolog ifadesi WRKY proteini çoklu stres yaratır E. coli’de tolerans
  7. Cytogenetic impact of sodium chloride stress on root cells of Vigna radiata L. seedlings
  8. Understanding the impacts of self-shuffling approach on structure and function of shuffled endoglucanase enzyme via MD simulations
  9. Evaluation ofTrichoderma atroviride and Trichoderma citrinoviride growth profiles and their potentials as biocontrol agent and biofertilizer
  10. Physio-biochemical analyses in seedlings of sorghum-sudangrass hybrids that are grown under salt stress under in vitro conditions
  11. The structural diversity of ginsenosides affects their cholinesterase inhibitory potential
  12. Extracellular acidity and oxygen availability conjointly control eukaryotic cell growth via modulation of cytoplasmic translation
  13. Genome-wide identification, phylogeny and expression analysis of G6PC gene family in common carp, Cyprinus carpio
  14. The effect of Diplotaenia turcica root extract in streptozotocin-induced diabetic rats
  15. Letter to the Editor
  16. Metabolomics analysis of medicinal insect Protaetia brevitarsis after Bacillus subtilis fermentation
  17. Opinion Paper
  18. Identifying and solving scientific problems in the medicine: key to become a competent scientist
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 25.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/tjb-2018-0552/html?lang=en
Scroll to top button