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Full Research Article

Effects of Salt Stress on Seed Germination and Embryo Growth of Oxytropis coerulea

Qin Yuao1, Ma Ruixin2, Wang Zixuan1, Liu Zhen3, Chen Liuqian1, Han Qiqi1, Liu Zhongkuan4,*, Liu Guixia1,*
1College of Life Science, Engineering Research Center of Ecological Safety and Conservation in Beijing-Tianjin-Hebei (Xiong’an New Area) of MOE, Key Laboratory of Microbial Diversity Research and Application of Hebei Province, Hebei University, Baoding 071 002, China.
2Weixian No.6 Primary School, Handan 054 799, China.
3College of Environmental Science and Engineering, North China Electric Power University, Beijing, 102 206, China.
4Institute of Agro-resources and Environment, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang 050 051, China.

  • Submitted30-05-2024|

  • Accepted06-09-2024|

  • First Online 15-10-2024|

  • doi 10.18805/LRF-818

ABSTRACT

Background: Oxytropis coerulea is considered to be an exceptional forage. The salinization of soil is a prevalent ecological issue worldwide. In order to study the effects of saline solution on seed germination and embryo growth of O. coerulea.

Methods: An experiment was carried out using the culture dish filter paper method. Three salt stresses, namely, Na2CO3, NaCl and double salt were set, each of which was set to 0%, 0.3%, 0.6% and 0.9% concentration.

Result: The results indicated that as the concentration of salt increased, there was a decrease in the germination rate, germination index and embryo growth. The activities of SOD, POD and CAT, as well as soluble protein content, initially increased and then decreased with increasing salt stress. The toxic effects of the three salts ranged from strong to weak as Na2CO3 > double salt > NaCl. The salt resistance indexes of 0.3% Na2CO3, NaCl and double salt were 53.87, 57.00 and 38.73, respectively and the salt resistance index of 0.6% NaCl was 50.21, indicating a high salt-tolerant degree. It showed certain resistance to 0.3% Na2CO3, 0.6% NaCl and 0.3% double salt. In short, the various soluble mechanisms of O. coerulea in different stages of salt stress and different salt stress levels have different reaction mechanisms, which reflect the salt stress of O. coerulea seeds. O. coerulea seeds can be planted in a suitable concentration of saline-alkali land, which can utilize the feed value and medicinal value of O. coerulea to improve economic benefits and utilize saline soil to improve the ecological environment.

INTRODUCTION

Salinization of soil is a worldwide ecological problem. Soil salinity affects approximately 800 million hectares of arable land worldwide (Yuan et al., 2016). The total saline land is about 1125 million hectares in the world (Hossain, 2019). China is one of the world’s largest saline-alkali land. The saline-alkali lands are about 9.913.7×107 hm2 (Zhang and Wang, 2021), of which the saline-alkali cultivated land is about 6.6×106 hm2 and there is also a 2.0×107 hm2 saline-alkali wasteland waiting to be utilized (Liu and Wang, 2021). Salinity is the most important abiotic stress factor that negatively affects agricultural production and quality (Majeed and Muhammad, 2019). Some crop varieties are difficult to exert their yield potential due to salt damage of salinized soil. Therefore, it is a long-term economic benefit to study the salt tolerance and salt tolerance mechanism of plants and the selection of plant varieties resistant to salt.
       
Oxytropis coerulea is a perennial herb of the family Leguminosae. It is cold-tolerant and drought-tolerant with thick roots, abundant leaf content, high nutritional value and strong regenerative capacity. It can be used repeatedly during the growing season and it has good palatability as a high-quality forage (Fan et al., 1999). In addition, its plants also have medicinal value of qi-fixing, detoxification and dehydration. The flowers are fresh and elegant with a long flowering period and they also have high ornamental value. In recent years, wild flowers have been widely used in garden landscaping due to the unique ornamental effect, leading to an increase in research on the ecological value and appreciation of O. coerulea (Dong et al., 2016). It can be concluded that O.coerulea can effectively maintain the carbon-oxygen balance of the garden environment if it is distributed with large-sized trees. O. coerulea is a grazing type grass that is tolerant to grazing, trampling and has strong regeneration ability. It can be used multiple times during the growing season. O. coerulea has good palatability and is often selected from grass herds for grazing by cattle, sheep and horses. They are considered as fattening forage. The thick, fleshy main roots of O. coerulea contain abundant nutrients. Cultivating on barren gravel slopes is a promising forage for improving degraded mountain grasslands. In the rainy season, whether it is shallow sowing in ditches or driven by sheep and trampling after sowing, seedlings are easy to emerge and the germination rate of seeds is generally above 40%.
       
However, the salt tolerance of O. coerulea has not been previously reported. In comparison to other stages of plants life, plant seeds exhibit lower resistance and tolerance to environmental stress during the germination stage. The germination performance of seeds and the protective enzyme system within the plant are crucial indicators that determine the ability of plants to survive and establish themselves in a new environment (Zhou, 2001). Therefore, this experiment aimed to investigate the tolerance of O. coerulea to various concentrations of salt solution and provide a theoretical foundation for the future cultivation of O. coerulea under saline conditions.

MATERIALS AND METHODS

Seed source
 
This experiment utilized wild O. coerulea seeds that were collected from Laiyuan County of Baoding City, Hebei Province in October 2021. Following the cleaning process, the seeds were stored in a refrigerator at a temperature of 4°C. Thousand seed weight was measured to be 2.3 g and the germination rate was determined to be 93.5%.
 
Test design and method
 
An experiment was carried out using the culture dish filter paper method. The seeds of O. coerulea were soaked in hot water at 98°C for 30 minutes to remove the hard seeds. The 2% sodium hypochlorite solution was sterilized for 10 minutes, then washed with sterile deionized water. 50 pieces of O. coerulea seeds with the same size were placed in a petri dish with double-layered sterile filter paper and 5 ml of different salt solutions were added respectively. Na2CO3, NaCl and double salt (main components are 50% NaCl, 30% Na2SO4, 10% NaHCO3, 10% Na2CO3) were used as three salt stresses, each set at 0%, 0.3%, 0.6% and 0.9% concentration. This resulted in a total of 10 treatments, with 4 replicates per treatment. The seeds of O. coerulea were placed in a 25±5°C incubator, with a light intensity set to 6000 lux. The day and night periods were each 12 hours long. The number of seeds germinated for each treatment was observed and recorded every day and the water in the petri dish was supplemented for 3 consecutive days until the seeds no longer continued to germinate. On the 7th and 13th day after seed germination, the antioxidant enzyme activity, MDA content, soluble protein content and cell membrane permeability were measured. After seed germination, several indicators were measured, including the length of the germ, hypocotyl and radicle, as well as 100 grains of fresh weight and relative chlorophyll content.
 
Indicators and methods
 
          (Riis et al., 1995) 

          (Murillo et al., 2002)
 
Gi = Σ(Gt/Dt)
 
Gt: Number of germinated seeds per day.
Dt: Corresponding sprouting days) (Carpıcı et al., 2009).
 
Vi = S• Gi
 
S: Average fresh weight of 100 seeds.
Gi: Germination index) (Zhang et al., 2015).
 
GV = Σ(Gt•Dt)/SGt
 
Gt: Number of seeds germinated.
Dt: Corresponding germination days) (Kaya and Day, 2008).
SPAD: SPAD-502 Plus Portable chlorophyll meter.
 
Antioxidant activity
 
Determination of superoxide dismutase activity by nitroblue tetrazolium (NBT) method; determination of peroxidase activity by guaiacol method; reaction solution for determination of catalase activity including 25 mmol/L phosphoric acid Buffer (pH = 7.0), 10 mmol/L H2O2 and enzyme extract were determined by UV spectrophotometry at 240 nm (Patra et al., 1978).
 
Malondialdehyde content
 
Thiobarbituric acid method (Soleimanzadeh et al., 2010).
 
Soluble  protein content
 
Coomassie brilliant blue solution (Doganlar et al., 2010).
 
Cell Membrane Permeability
 
Conductivity Method (Wiser and Blom, 2016).



 
Statistical analysis
 
The experimental data were recorded by Microsoft Excel software and plotted into a histogram. All data were subjected to a one-way analysis of variance and the mean differences were compared by the lowest significant difference (LSD). Comparisons with p<0.05 were considered significantly different.

RESULTS AND DISCUSSION

Effect of salt stress on germination rate of O. coerulea Seeds
 
The germination rate of O. coerulea seeds decreased with the increase in salt solution concentration (Fig 1). The germination rate decreased sharply when treated with 0.6% Na2CO3 or 0.9% double salt. The germination rate has dropped steadily by NaCl treatment increased with concentration. The germination rate of O. coerulea seeds were significantly inhibited by the concentration of 0.6%, 0.9% Na2CO3 and double salt. When the salt concentration is the same, the order of germination rate from high to low is NaCl > double salt > Na2CO3.
 

Fig 1: Effects of Na2CO3, NaCl and double salt on germination percentage of Oxytropis coerulea at four different concentrations.


 
Germination potential, germination index, germination vitality index, average germination days
 
The germination potential, germination index and germination vigor index of the seeds all decreased with the increase in the concentration of each salt stress (Table 1). Seed treatment with 0.6% Na2CO3 or 0.9% NaCl and double salts significantly declined the germination index. Under the same concentration of different salt treatment groups, the germination index seems to be highest in NaCl treatment followed by double salt and Na2CO3. The germination toxicity of Na2CO3 treatment was significantly greater than other salt treatments. The average germination days of O. coerulea seeds increased with increasing levels of salinity and the difference in salt treatment of the same concentration was not significant.
 

Table 1: Effects of Na2CO3 , NaCl and double salt on germination emergence (GE), Germination index (GI), germination vitality index (GVI) and average germination days/d at four different concentrations of Oxytropis coerulea seeds.


 
Embryo length, 100 fresh weight and relative chlorophyll content
 
The germ, hypocotyl, radicle length, 100-gravity fresh weight and relative chlorophyll content of O. coerulea seeds decreased with increasing treatment concentration (Table 2). The seeds of O. coerulea treated with 0.6%, 0.9% Na2CO3 and 0.9% double salt declined in germination index, were significantly affected by salt stress and the leaves were fragile. After washing, they were broken and some indicators could not be measured. Under the same concentration of different salt treatment groups, the experimental index seems to be the highest in NaCl treatment, followed by double salt and Na2CO3. It indicated that the normal growth and development of seeds were seriously hindered by the high concentration of Na2CO3. The 0.3% NaCl treatment was not significant when compared to the control and the damage caused by NaCl was the smallest among the three salts.
 

Table 2: Effects of Na2CO3, NaCl and Double salt on shoot length(cm), hypocotyl length (cm), radicle length (cm), hundred kernel fresh weight (g) and relative chlorophyll content/SPAD at four different concentrations of Oxytropis coerulea Seeds.


 
Antioxidant enzyme activity
 
Superoxide dismutase (SOD) activity
 
The SOD activity of the three salt-treated O. coerulea seeds gradually decreased as the germination time increased (Fig 2). The SOD activity of Na2CO3 and double salt treatment initially increased and then decreased with increasing concentration. On the 7th day of germination, the activity of SOD was the highest when the double salt concentration of Na2CO3 was 0.3% and the activity became smaller as the concentration increased (Fig 2-A). Under 0.6% NaCl treatment, it can react to produce higher SOD. On the 13th day of germination, the activity of Na2CO3 and NaCl was the highest at the concentration of 0.3% and the activity of Na2CO3 and double salt was the highest at the concentration of 0.6% (Fig 2-B). The SOD treatment at 0.9% Na2CO3 was less than the control, which indicated that the range of protective enzyme tolerance of O. coerulea seeds may have been exceeded.
 

Fig 2: Effects of the 7th day (A) and 13th day (B) on SOD activity of Oxytropis coerulea seeds.


 
Peroxidase (POD) activity
 
 The POD activity of O. coerulea seeds treated with double salt and Na2CO3 generally decreased with the prolongation of germination time (Fig 3). On the 7th day of germination, the activity of POD in Na2CO3 and double salt treatment first increased and then decreased with the increase of concentration (Fig 3-A). The concentration of NaCl was lower than that of the control. The POD concentration was highest when the concentration was 0.3% under Na2CO3 and double salt treatment. When the concentration was 0.9%, the POD activity of NaCl was the highest at the same concentration. On the 13th day of germination, the activity of POD in NaCl and double salt treatment first increased and then decreased with the increase of concentration (Fig 3-B). The treatment of 0.3%-0.9% Na2CO3 was smaller than the control value and decreased continuously with increasing concentration. At concentrations of 0.3%-0.6%, the POD activity of NaCl and double salt treatment was significantly higher than that of Na2CO3. At a concentration of 0.9%, the POD activity of NaCl treatment was significantly higher than other treatments and the order of POD activity was NaCl > double salt > Na2CO3.
 

Fig 3: Effects of the 7th day(A) and 13th day (B) on POD activity of Oxytropis coerulea seeds.


       
Activity of catalase (CAT): The CAT activity and the SOD activity of the three salt-treated O. coerulea seeds were nearly identical (Fig 4). On the 7th day of germination, the CAT activity was highest under the salt stress treatments when the concentration was 0.3%. When the concentration was 0.6% and 0.9%, the CAT activity was highest under NaCl treatment. On the 13th day of germination, the CAT activity of 0.6%-0.9% Na2CO3 treatment was lower than the control value, suggesting that the tolerance range of O. coerulea seed protective enzymes may have been exceeded at this time. When the concentration of each salt was between 0.3% and 0.9%, the CAT activity of NaCl and double salt treatment was significantly higher than that of Na2CO3.
 

Fig 4: Effects of the 7th day(A) and 13th day (B) on CAT activity of Oxytropis coerulea seeds.


 
Malondialdehyde content
 
On the 7th day of O. coerulea seed germination, the malondialdehyde (MDA) content of O. coerulea seeds increased with the increase of Na2CO3 concentration. Additionally, it increased initially and then decreased with the increase of NaCl and double salt concentration (Fig 5-A). On the 13th day of O. lanceolata seed germination, the MDA content increased with the increase of Na2CO3 and NaCl concentrations. However, the double salt concentration initially decreased and then increased (Fig 5-B)., the difference between the NaCl and double salt results was not significant when compared to the control. Furthermore, the MDA content of O. coerulea seeds in the Na2CO3 treatment group increased significantly over time.
 

Fig 5: Effects of the 7th day (A) and 13th day (B) on MDA activity of Oxytropis coerulea seeds.


 
Soluble protein content
 
On the 7th day of seed germination, the soluble protein content increased as the salt concentration increased (Fig 6-A). When the concentration was the same, the NaCl treatment had the highest soluble protein content. On the 13th day of O. coerulea seed germination, the soluble protein content of O. coerulea seeds decreased with the increasing Na2CO3 concentration and increased with increasing NaCl and double salt concentration (0.3%-0.6%). The soluble protein content of NaCl and 0.3% double salt was lower than that of the control group (Fig 6-B). Comparing the data on the 7th day and the 13th day of O. coerulea seed germination in the figure, it can be observed that the protein content of O. coerulea seeds in 0.9% Na2CO3, 0.3%-0.9% NaCl and 0.3% double salt treatment groups decreased over time.
 

Fig 6: Effects of the 7th day(A) and 13th day (B) on soluble protein content of Oxytropis coerulea seeds.


 
Cell membrane permeability
 
The electrical conductivity of O. coerulea seeds increased with increasing concentration and prolonged stress time. On the 7th day, the seed conductivity of 0.9% Na2CO3 treatment increased greatly (Fig 7-A). On the 13th day, the seed conductivity of different concentrations of Na2CO3 treatment increased significantly and the conductivity value of NaCl treatment was small and stable (Fig 7-B).
 

Fig 7: Effects of the 7th day(A) and 13th day (B) on conductivity of Oxytropis coerulea seeds.


 
Salt tolerance evaluation
 
As can be seen from Table 3, the salt tolerance index of the same salt solution decreased as the concentration increased. Na2CO3 has the largest reduction between 0.3% and 0.6%, NaCl has the largest reduction between 0.6% and 0.9% and the double salt has the largest reduction between 0.6% and 0.9%. Under the salt stress of different concentrations, the salt tolerance index of NaCl was the largest. The salt tolerance index is 0.97 for 0.9% Na2CO3 and 57.00 for 0.3% NaCl.
 

Table 3: Effects of salt stress on Oxytropiscoerulea and its salt tolerance.


       
The salt-alkali damage index of the same salt solution increased with increasing concentration. The highest salt tolerance index is 96.00% at 0.9% Na2CO3 and the smallest is 3.25% at 0.3% NaCl. The salt tolerance index of O. coerulea seeds was classified according to the salinity index (Table 4). The salt-tolerant grade 1 (high-resistance) included 0.3% Na2CO3, NaCl, double salt and 0.6% NaCl. The salt-tolerant grade 2 (resistance) included 0.9% NaCl and the salt-tolerant grade 3 (moderate-resistance) included 0.6% double salt. The remaining salt and alkali resistance grade is 5 (sensitive).
 

Table 4: Saline-alkaline stress damage grading table.


       
Through the salt stress of different species and different concentrations of O. coerulea seeds, the experimental results and application suggestions for germination index, enzyme activity, physiological index and physiological salt tolerance range were discussed.
1. The germination rate reflects the germination ability of the seed. The higher the salt concentration, the lower the germination rate of the seed. When the salt concentration is the same, the germination rate may be the highest in NaCl treatment, followed by double salt and Na2CO3. This is similar to the test results on Brassica Napus (Kandil et al., 2012) and Canola seed germination (Bybordi, 2010).
2. The germination potential and germination index decreased as the increase of salt concentration increased. The average germination days of O. coerulea seeds also increased with the increase in salt concentration. However, there was no significant difference in the salt treatment with the same concentration, suggesting that the average germination days were mainly affected. This finding is consistent with the research results to Anbarasu Mariyappillai on on Vigna mungo under NaCl stress (Mariyappillai and Kulanthaivel, 2024). The seed germination rate of Vicia sativa also decreased with the increase of salt concentration (Zhao et al., 2022) The embryo length of O. coerulea treated with 0.3% and 0.6% NaCl was greater than that of the control group. Further verification is needed to determine whether the low concentration of NaCl solution has the effect of increasing the length of the germ.
3. Under unfavorable conditions, the active oxygen species generated by plants have a detrimental impact on the cell membrane. This, in turn, triggers the activation of the protective enzyme system to eliminates surplus free radicals from the body. SOD, POD and CAT are crucial elements of antioxidant defense systems and can be used as indicators of tissue damage (Kumar et al., 2021).
       
The results indicated that the SOD, POD and CAT of O. coerulea seeds exhibited regular changes under different salt stresses. In the various salt treatments, the SOD activity in a low concentration NaCl solution was lower than that in the control in the short term, specifically under the 0.6% treatment. It was significantly higher than other concentrations, suggesting that a short-term treatment of 0.3% NaCl concentration, is insufficient to cause damage to plant cells. The SOD activity increased in the other treatments at a low concentration of 0.3% and then steadily decreased steadily with an increase in concentration. This indicates that the seeds initially caused damage to the cells under the stress of other low-concentration salts, triggering the defense system and increasing SOD activity to limit the damage caused by free radicals to cells. Under long-term salt stress, the SOD activity decreased. When the concentration of Na2CO3 was 0.9%, the SOD activity decreased significantly, indicating that the damage to cells exceeded its self-protection range, resulting in irreparable damage to the plant body (Sinky et al., 2024).
       
The changes in POD and CAT activities were almost identical to those of SOD activity. Under long-term treatment stress with a NaCl solution, the activity of POD increased significantly over time, possibly due to an increasing ability to protect itself as salt stress accumulated. During long-term stress, the CAT activity in the seed increased significantly with increasing of concentration and then decreased significantly below the control level. This indicates that in extreme environment, the seed can quickly react and activate its protective system, but when the stress exceeds its tolerance range, its CAT activity drops rapidly. Therefore, in the long-term evolution of plants, peroxidase in the defense system plays a role in maintaining the dynamic balance of the intracellular environment and improving the ability of seeds to resist external environmental disturbances.
       
Under salt stress, plant growth inhibition is related to the destruction of the cell membrane system. The change in plasma membrane permeability can be measured to determine the extent of cell membrane damage (Mansour, 2013). Malondialdehyde is a product of membrane lipid peroxidation in plant cells and can be used as an indicator of plant aging and stress (Hnilickova et al., 2021). As time and concentration increase, the MDA content and cell membrane permeability of O. coerulea seeds in treatment group significantly increase. The results indicate that Na2CO3 causes the greatest damage to O. coerulea seed and the NaCl damage was the smallest, which was the result of germination. This result is similar to the study of Lycium barbarum (Zhang et al., 2019).
       
Most of the soluble proteins in plants are enzymes that participate in metabolic activities and their content reflects the overall metabolic activity of plant tissues (Taffouo et al., 2017). In the short-term, exposure to Na2CO3, NaCl and double salt stress can increase the protein content and increase the intracellular osmotic potential by promoting the synthesis of new resistance protein. However, in the long-term Na2CO3 stress, O. coerulea seeds may inhibit protein synthesis. The storage of proteolysis is accelerated to enhance salt resistance and has this process operates through different mechanisms depending on the type of salt.
       
The test measures only the growth index of the seed during germination. The salt tolerance of the plant was fully reflected during the growth process. Therefore, it is necessary to comprehensively judge a number of biological indicators at different growth stages. In the future, several concentration gradients and various salt solutions may be set. It is also necessary to study other salt types such as potassium salts and salt damage to plants. It is also possible to investigate the recovery of germination ability after seed salt stress is relieved.

CONCLUSION

The results showed that all three salts at different concentrations inhibited seed germination of O. coerulea. In this study, it was further confirmed that the tolerance degree to three kinds of salt stress in the germination stage of O. coerulea seed was Na2CO3, double salt and NaCl in order from large to small. With the increase of salt concentration, the physiological indexes and growth indexes of O. coerulea seeds generally showed a downward trend. During the germination, they changed the antioxidant enzyme activity and protein content in different periods and different salt stresses. The reaction mechanism works together to resist salt stress

ACKNOWLEDGEMENT

This work was supported by the Hebei Grass Industry Innovation team of Modern Agricultural Industry Technology System (HBCT 2023160203). This study was funded by the Engineering Research Center of Ecological Safety and Conservation in Beijing-Tianjin-Hebei (Xiong’an New Area) of MOE, China. This study was also supported by the Key Laboratory of Microbial Diversity Research and Application of Hebei Province, College of Life Sciences, Hebei University.

CONFLICT OF INTEREST

All authors declare that they have no conflict of interest.

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