Effects of salt concentration, pH, and their interaction on plant growth, nutrient uptake, and photochemistry of alfalfa (Medicago sativa) leaves

Guo Kaiwen; Xu Zisong; Huo Yuze; Sun Qi; Wang Yue; Che Yanhui; Wang Jiechen; Li Wei; Zhang Huihui

doi:10.1080/15592324.2020.1832373

. 2020 Oct 19;15(12):1832373. doi: 10.1080/15592324.2020.1832373

Effects of salt concentration, pH, and their interaction on plant growth, nutrient uptake, and photochemistry of alfalfa (Medicago sativa) leaves

Guo Kaiwen ^a,^*, Xu Zisong ^a,^*, Huo Yuze ^a, Sun Qi ^a, Wang Yue ^b, Che Yanhui ^b, Wang Jiechen ^b, Li Wei ^a, Zhang Huihui ^a,^b,^✉

PMCID: PMC7671061 PMID: 33073686

ABSTRACT

In order to explore the main limiting factors affecting the growth and physiological function of alfalfa under salt and alkali stress, the effect of the salt and alkali stress on the growth and physiological function of alfalfa was studied. The results showed that effects of the excessive salt concentration (100 and 200 mM) on the growth and physiological characteristics were significantly greater than that of pH (7.0 and 9.0). Under 100 mM salt stress, there was no significant difference in the growth and photosynthetic function between pH 9.0 and pH 7.0. Under the 200 mM salt concentration the absorption of Na⁺ by alfalfa treated at the pH 9.0 did not increase significantly compared with absorption at the pH 7.0. However, the higher pH directly reduced the root activity, leaf’s water content, and N-P-K content also decreased significantly. The PSII and PSI activities decreased with increasing the salt concentration, especially the damage degree of PSI. Although the photoinhibition of PSII was not significant, PSII donor and electron transfer from the Q_A to Q_B of the PSII receptor sides was inhibited. In a word, alfalfa showed relatively strong salt tolerance capacity, at the 100 mM salt concentration, even when the pH reached 9.0. Thus, the effect on the growth and photosynthetic function was not significant. However, at 200 mM salt concentration, pH 9.0 treatment caused damage to root system and the photosynthetic function in leaves of alfalfa was seriously injured.

KEYWORDS: Salt and alkali stress, alfalfa, plant growth, photochemistry activity, photoinhibition

The regular salt is an important component of the soil, and it is also an essential nutrient element for plant growth. However, excessive amount of the salt will not only directly affect growth of the plants (through ion toxicity or interfering in ion balance),¹^,2 but will also indirectly cause an osmotic stress and affect the water absorption in the plants.^3,4 Under the salt stress, excessive amount of Na⁺ ions will disrupt the balance of plant metabolism, disturb the normal physiological activities of the plants, lead to the inhibition of plant’s growth,⁵ weakening of the photosynthesis and respiration processes, induce an accumulation of reactive oxygen species (ROS), and even cause death of the plants [^{6, 2009b}]. The main salts in nature include the neutral salts, such as NaCl and NaSO₄, and the alkaline salts (Na₂CO₃ and NaHCO₃).^7–9 In addition to the toxic effect of Na⁺, the damaging effects of the alkaline salt (with higher pH values) on the plants is more serious than that of the neutral salts [^10–12,], i.e. the effect of the alkaline salt stress on the seed germination,^13,14 root’s growth,^15,16 nutrient’s absorption,¹⁷ ion balance,^18,19 ROS metabolism [^{Zhang and Mu, 2009b; 20,21}], and other processes. Therefore, it is of great significance for vegetation restoration to study the damage mechanism of the alkaline salts on plants.

Photosynthesis is the basic mechanism in the plants for obtaining material and energy. More than 90% of a dry matter in plants directly comes from photosynthesis. However, it is also one of the processes sensitive to the stress, especially salt stress. Excessive salt concentration will affect the synthesis of photosynthetic pigment or accelerate their degradation.^20,22,23 In such a case, the absorption and utilization of light energy in PSII and PSI reaction center will be reduced,²⁴ the electron transfer will be blocked,²⁵ and carbon assimilation ability will be limited.^26,27 Alfalfa (Medicago sativa) is a perennial leguminous plant. Because of its beneficial characteristics, such as high yield, good quality, tolerance to frequent cutting, and good durability; it is known as “the king of forages.” This plant has the longest history of cultivation and the largest planting area in the world of the leguminous forages.^14,28 Songnen Plain is located in the “golden milk source” area, which is one of the main alfalfa producing areas in China. However, the alkaline salt (pH > 8.5), which is mainly due to the presence of NaHCO₃, is one of the most important limiting factors in alfalfa production.²⁹ Salt alkali stress will directly reduce the alfalfa yield and quality.^30,31 At the present time, there are many studies about the effects of single neutral salt (NaCl) and alkaline salt (NaHCO₃ or Na₂CO₃) on the growth and physiological characteristics of alfalfa.^32–36 Yet, there are only few about the interaction of salt concentration and pH value on the growth and physiological characteristics, especially on the photosynthetic function. Therefore, this experiment applied the method of solution culture to study the influence of different salt concentration (100 mM and 200 mM) and different pH values (7.0 and 9.0) on alfalfa plant growth, root activity, water and nutrient absorption, and leaf PSII and PSI function, in order to reveal the main limiting factors of alfalfa’s growth and physiological function under salt and alkali conditions. Theoretical basis for the promotion and reasonable planting of alfalfa in salt and alkali soil was also provided.

1. Materials and methods

1.1. Experimental design

The experiment was carried out in the Soil Science Laboratory of Northeast Agricultural University in 2019. The tested plant species was Medicago sativa CV. Zhaodong. The seeds were provided by the Crop Research Institute of Heilongjiang Academy of Land Reclamation Sciences. Mature, full-bodied, and similarly sized seeds were place in a cultivation dish for germination. After the germ grew to approximately 0.5 cm, germinated seeds with the relatively uniform growth were selected and grew in a 1:1:1 volume mixture of peat, perlite and vermiculite. The culture was carried out in an incubator with a temperature of 25°C, an illumination intensity of 400 μmol·m⁻³⁷·s,⁻¹ and in a photoperiod of 12/12 h (light/dark).

When the seedlings were about 15 cm, they were pulled out of the culture medium, carefully washed the culture medium on the surface of the root system, and then hydroponically treated the alfalfa seedlings. The used nutrient solution was Hoagland nutrient solution. The hydroponics box was black and opaque, with 30 cm in length, width, and height. Six alfalfa plants were fixed in each hydroponics box. The nutrient solution was continuously ventilated by electric courage pump to ensure proper supply of the oxygen. After 15 days of seedling culture, different concentrations of salt and alkali treatment were carried out, in which NaCl solution was selected for pH 7.0 salt treatment, and NaCl:NaHCO₃:Na₂CO₃ mixed salt solution with the ratio of 2:1:1 was selected for pH 9.0 salt and alkali treatment The concentration of salt solutions with different pH values were set to 100 mmol·L⁻¹ and 200 mmol·L⁻¹ (100 mM and 200 mM), respectively, with the normal Hoagland nutrient solution as the control (CK). 36 seedlings of each treatment were repeated. The salt concentration and pH value’s range were simulated according to the types and contents of main salt in saline alkali soil of Songnen Plain in China. The growth and physiological indexes were measured after 10 days after the treatment with the different concentrations of saline alkali.

1.2. Determination of parameters and methods

Determination of chlorophyll fluorescence parameters: Fully unfolded leaves of alfalfa in each treatment were selected and treated with dark adaptation clip for 30 min. OJIP curves and modulated reflection at 820 nm (MR₈₂₀) of leaves in each treatment were measured by M-PEA (Multi-Function Plant Efficiency Analyzer, Hansatech) after dark adaptation. F_v/F_m and ΔI/I_o were used to characterize the photochemical activity of PSII and PSI, respectively, of which F_v/F_m = (F_m-F_o)/F_m, where F_m and F_o are the relative fluorescence intensities of P point (1000 ms) and O point (0.01 ms) on the OJIP curve, I_o represents the maximum value of the MR₈₂₀ signal, and ΔI represents the difference between the maximum and the minimum of the MR₈₂₀ signal .³⁸ Relative fluorescence intensity of the O point in the OJIP curve was defined as 0, while in the case of P point and J point (2 ms) was defined as 1. The OJIP curve was standardized according to the formulas V_O-P = (F_t-F_o)/(F_m-F_o) and V_O-J = (F_t-F_o)/(F_J-F_o) to obtain the relative variable fluorescence V_J at J point (2 ms) in V_O-P curve and relative variable fluorescence V_K at K point (0.3 ms) in V_O-J curve. The standardized V_O-P and V_O-J curves of alfalfa leaves at different saline alkali stress were compared with those of CK and the differences were denoted as ΔV_O-P and ΔV_O-J, respectively. Five repetitions were carried out for each treatment.

Determination of physiological indexes of alfalfa plants: after measuring the chlorophyll fluorescence parameters, the root tips of differently treated alfalfa were used in TTC method to measure the root activity.³⁹ After the harvesting of aboveground and underground of differently treated alfalfa respectively, the fresh weight of the aboveground and underground were obtained. Parts were drying at 80°C in order to obtain the biomass. The aboveground water content = (aboveground fresh weight – aboveground biomass)/aboveground biomass. The aboveground and underground parts of differently treated alfalfa were ground down and sieved using 40 meshes. After digesting the aboveground and underground samples using H₂SO₄-H₂O₂, nitrogen content was determined by the Micro-Kjeldahl method, phosphorus content was measured by UV-visible spectrophotometry method, and potassium and natrium contents were determined by the flame photometric method.^37,40 All measurements were performed in triplicate (biological experiments).

1.3. Data analysis

Excel (2003) and SPSS (22.0) software were used to conduct statistical analyses on the measured data. The data in the figures were denoted as mean ± standard deviation (SE). A two-way analysis of variance (two-way ANOVA) and least significant difference (LSD) test were adopted to compare the difference between the treatments.

2. Results and analysis

2.1. Plant growth parameters, leaf water content and root activity

As shown in Table 1, the effects of salt concentration on the fresh weight and biomass of alfalfa was significant (P < .01), but the effects of pH on the growth was not significant. There was also no significant interaction between salt concentration and pH. The effects of the salt concentration on the leaf water content and root activity was significant. The effects of the pH on the root activity of alfalfa was also significant, but on the leaf water content was not significant, salt concentration× pH on the leaf water content and root activity of alfalfa was not significant.

Table 1.

Two-way ANOVAs examining the effects of salt concentration, pH and their interaction (salt concentration× pH) on fresh weight and biomass in aboveground and underground

	Salt concentration		pH		Salt concentration×pH
	F	P	F	P	F	P
Aboveground fresh weight (g)	29.79	< 0.01	2.419	0.14	0.868	0.44
Underground fresh weight (g)	15.94	< 0.01	1.788	0.20	0.687	0.52
Aboveground biomass (g)	17.07	< 0.01	1.048	0.32	0.829	0.46
Underground biomass (g)	39.57	< 0.01	1.983	0.18	1.662	0.23
Aboveground water content (%)	10.237	< 0.05	0.351	0.56	0.196	0.82
Root activity	17.132	< 0.05	10.8	< 0.05	2.902	0.09

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The findings in Figure 1 showed that at 100 mM salt concentration, there was no significant difference between the above-mentioned growth parameters compared to the CK, but when the salt concentration increased to 200 mM, the growth parameters were significantly lower than CK. At the 100 mM salt concentration, there was no significant difference in the growth parameters of alfalfa treated with pH 7.0 and pH 9.0. When the salt concentration increased to 200 mM, the aboveground fresh weight, underground fresh weight, aboveground biomass, and underground biomass of alfalfa treated with pH 9.0 were lower than those of pH 7.0 by 24.45% (P > .05), 20.79% (P > .05), 26.88% (P > .05), and 40.85% (P < .05), respectively. At the 100 mM salt concentration, the leaf’s water content and root activity were slightly lower than CK. The difference was not significant, but they were significantly lower in the case when the salt concentration increased to 200 mM. The root activity treated with pH 9.0 was 25.82% (P < .05) and 45.29% (P < .05) lower than that of treated with pH 7.0 at 100 and 200 mM salt concentrations, respectively, but the difference of leaf’s water content was not significant under the different pH treatments.

2.2. N, P, K and Na content

The effect of the salt concentration on the content of N and P in aboveground and underground of the alfalfa was very significant, while pH showed a significant effect on the content of N in aboveground of alfalfa. There was no significant interaction between the salt concentration and pH on the content of N and P in alfalfa. the effects of the salt concentration on the K and Na contents in the aboveground and underground were extremely significant. The pH showed a significant effect only on the K content in the underground of the alfalfa, but there is no significant interaction between them (Table 2).

Table 2.

Two-way ANOVAs examining the effects of salt concentration, pH, and their interaction (salt concentration× pH) on N, P, K, and Na content in aboveground and underground

	Salt concentration		pH		Salt concentration×pH
Content (mg·g⁻¹DW)	F	P	F	P	F	P
Aboveground nitrogen	22.16	< 0.01	5.21	< 0.05	2.87	0.09
Underground nitrogen	40.08	< 0.01	1.19	0.29	3.31	0.07
Aboveground phosphate	26.89	< 0.01	2.94	0.11	1.41	0.27
Underground phosphate	15.34	< 0.01	1.05	0.32	0.26	0.77
Aboveground potassium	10.65	< 0.01	2.83	0.11	1.45	0.27
Underground potassium	44.94	< 0.01	7.00	< 0.05	2.14	0.16
Aboveground sodium	100.19	< 0.01	0.13	0.72	0.09	0.90
Underground sodium	139.68	< 0.01	0.19	0.66	0.05	0.94

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As shown in Figure 2, at 100 mM salt concentration, there was no significant difference in N and P content in aboveground and underground, but P content decreased significantly in underground. At the 200 mM salt concentration, the content of N and P in aboveground and underground decreased significantly. The contents of N and P in aboveground and underground at pH 9.0 treatment were significantly lower than that of pH 7.0 treatment. With the increase in the salt concentration, the K content in the aboveground and underground of alfalfa decreased, while the Na content increased significantly. At the 100 mM salt concentration, the K content in the aboveground and underground showed no significant difference at both pH 7.0 and 9.0 treatment, but when the salt concentration increased to 200 mM, the K content in the aboveground and underground at pH 9.0 treatment was lower than that of pH 7.0 treatment by 33.33% (P < .05) and 35.21% (P < .05), respectively, There was no significant difference in the Na content between the aboveground and underground of alfalfa treated with both pH 7.0 and 9.0.

2.3. OJIP curve, MR₈₂₀ curve and photochemistry activity

As shown in Figure 3-A, the OJIP curve and MR₈₂₀ curves of alfalfa leaves were significantly changed at different salt concentration and pH values. At different salt and pH treatment, the changes of O-point relative fluorescence intensity (F_o) was negligible, but with the increase in salt concentration, the P-point relative fluorescence intensity (F_m) showed a significant downward trend. The F_m at the pH 9.0 treatment was not significantly higher than that of pH 7.0 treatment. As can be seen in Figure 3-B, with the increase in salt concentration, the amplitude of MR₈₂₀ curve decreased significantly, and the decrease amplitude at pH 9.0 treatment was greater than that of pH 7.0 treatment, especially at 200 mM salt concentration.

In Tab. 3, the effects of salt concentration on F_v/F_m and ΔI/I_o were significant, while the effects of salt concentration on F_v/F_m and ΔI/I_o were extremely significant. In Fig. 5-C and 5-D, there was no significant difference between F_v/F_m and ΔI/I_o and CK at the 100 mm salt concentration. When the salt concentration increased to 200 mM, F_v/F_m and ΔI/I_o were significantly lower than CK, while F_v/F_m and ΔI/I_o treated with pH 9.0 were lower than those of treated with pH 7.0 by 2.60% (P < .05) and 27.35% (P < .05), respectively.

Table 3.

Two-way ANOVAs examing the effects ofsalt concentration, pH, and their interaction (salt concentration× pH) on F_v/F_m and ΔI/I_o.

	Salt concentration		pH		Salt concentration×pH
	F	P	F	P	F	P
F_v/F_m	12.60	< 0.01	8.62	<0.05	3.20	0.07
ΔI/I_o	12.35	< 0.01	21.56	<0.05	14.25	<0.05

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2.4. Standardized OJIP curve and relative variable fluorescence

In Figure 4-A and 4-B, V_J on the V_O-P curve and V_K on the V_O-J curve of alfalfa leaves at different salt concentrations and pH treatments showed the significant changes. The difference between V_O-P and V_O-J curves under the different treatments and CK might be seen in the presented curves for ΔV_O-P and ΔV_O-J (Fig. 5-C and 5-D). At the 200 mM salt stress, the increase in V_J and V_K was significantly greater than that at 100 mM salt stress.

As shown in Table 4, the effects of the salt concentration on V_J and V_K were very significant, effect of the pH on V_J and V_K was also very significant, but their interaction had no significant effect on V_J. On the other hand, interaction showed a significant effect on V_K. In Fig. 6-E and 6-F, at 100 and 200 mM salt concentrations, V_J and V_K increased significantly compared to the CK. At 100 mM salt concentration, V_J and V_K treated with pH 9.0 increased to different degrees compared with those at the pH 7.0. However, only V_K showed significant difference. At 200 mM salt concentration, V_J and V_K treated with pH 9.0 increased by 14.85% (P < .05) and 20.80% (P < .05) respectively compared with pH 7.0.

Table 4.

Two-way ANOVAs examing the effects of salt concentration, pH, and their interaction (salt concentration× pH) on V_J andV_K.

	Salt concentration		pH		Salt concentration×pH
	F	P	F	P	F	P
V_J	19.69	<0.01	7.54	<0.05	3.60	0.06
V_K	11.38	<0.01	28.69	<0.01	9.24	<0.01

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3. Discussion

Plant’s root system is the part with direct exposure to the salt and alkali stress, and it is also one of the parts which is sensitive to the salt and alkali stress.⁴¹ The damage of plant’s root system will directly lead to the limitation of plant’s water and nutrient absorption.²⁴ This experiment showed that the fresh weight and biomass of the alfalfa’s root (underground) were not significantly lower than CK at the 100 mM salt stress, and there was no significant difference between treatment at pH 9.0 and pH 7.0. But at the 200 mM salt stress, the fresh weight and biomass of alfalfa’s root were significantly lower than CK, and effects of the treatment at the pH 9.0 were significant. In addition, at the different salt concentrations, the root activity under pH 9.0 treatment was significantly lower than that of pH 7.0. This indicated that the damage of alfalfa’s root system was intensified at the high pH level. Higher salt concentration in the soil, especially alkaline salt, will reduce the availability of nutrients in it.³⁰ In this experiment, with the increase in the salt concentration, the fresh weight and biomass of the aboveground and the NPK content decreased, but the differences of other growth parameters and NPK content with CK at the 100 mM salt stress were not significant. The biomass accumulation, NPK content and the water content of the aboveground of alfalfa at the 200 mM salt stress were significant. At the 100 mM salt stress, higher pH inhibited the root activity, but it had less effect on the growth and NPK nutrient absorption of alfalfa. At the 200 mM salt stress, the interaction effect of the salt concentration and pH was enhanced. The higher pH restricted further absorption of the nutrients and inhibited the growth of alfalfa. The toxicity of the salt stress toward the plant’s growth is mainly related to the excessive absorption of Na⁺ ions.^1,42 The results showed that, although the Na content in the aboveground and underground increased significantly with the increase the in salt concentration, there was no significant difference in the Na content between the aboveground and underground in the case of pH 9.0 and pH 7.0 treatments at the different salt concentrations. Therefore, the reason why the higher concentrations of alkaline salt show a greater inhibition on alfalfa’s growth is not due to the increase of Na⁺ absorption. This could be mainly related to the greater damage of higher pH level on alfalfa’s roots, thus limiting the absorption of the water and nutrients by root system.

PSII and PSI are sensitive to the salt stress. Salt stress often leads to the decrease in the PSII and PSI activity, and even photoinhibition.²⁵ F_v/F_m and ΔI/I_o are very important indexes capable to characterize the photochemical activities of PSII and PSI, respectively.^43,44 In this experiment, at the 100 mM salt stress, F_v/F_m and ΔI/I_o of alfalfa’s leaves were slightly reduced, but the difference was not significant compared to the CK. At the 200 mM salt stress, F_v/F_m and ΔI/I_o were significantly reduced, and the decrease in ΔI/I_o was larger than of F_v/F_m, indicating that PSI of alfalfa’s leaves was more sensitive to the salt stress than PSII. Although there was no significant difference between F_v/F_m and ΔI/I_o in the treatment with pH 7.0 and pH 9.0 at the 100 mM salt stress, F_v/F_m and ΔI/I_o in the treatment with pH 9.0 were significantly lower than those at the pH 7.0 at the 200 mM salt stress. This means that higher pH increased the photoinhibition of both PSII and PSI in alfalfa’s leaves at the high concentration of the salt. Further analysis of the reason for the decrease in PSII activity showed that with the increase of the salt concentration, V_J in the V_O-P curve and V_K in the V_O-J curve of alfalfa’s leaves increased significantly. The increase in V_J indicated that the electron transfer from Q_A to Q_B in the photosynthetic electron transport chain was blocked, while the increase in V_K was considered as a specific marker of the damage to the activity of oxygen-evolving complex on the PSII electron donor side.^45,46 Therefore, the main reason for decrease of the PSII activity in alfalfa’s leaves under the salt and alkali stress is an obstruction of the electron supply and transmission in the both donor and the receptor side of the PSII. However, at the 100 mM salt stress, V_K of alfalfa’s leaves treated with pH 9.0 was significantly higher than that treated with pH 7.0, but the difference for V_J was not significant. It has been found that in the process of electronic transfer, when the upstream electronic supply is restrained, the electronic pressure in the downstream electron transporter will be reduced.⁴⁷ Therefore, in this experiment, there was no significant difference in the inhibition degree of PSII receptor side electron transfer of alfalfa leaves under 100 mM salt stress between pH 7.0 and 9.0 treatments. This may be due to the fact that pH 9.0 treatment showed less damaging effect toward the PSII receptor side of alfalfa’s leaves, but it may also be due to the inhibition of OEC activity at the pH 9.0 treatment. The specific reasons need to be studied more extensively. However, at the 200 mM salt stress, V_K and V_J of alfalfa’s leaves treated with pH 9.0 were significantly higher than those of treated with the pH 7.0. At high salt concentration, the donor side and recipient side of unrecognized PSII were significantly affected.

4. Conclusion

Although the Na content of alfalfa plants increased significantly at the 100 mM salt concentration, the biomass accumulation, root activity, N-P-K content (except for P content in the underground), and water content in the aboveground were not significantly affected. The electronic supply and transmission of the PSII donor and receptor sides of alfalfa’s leaves were inhibited, but the activities of the PSII and PSI were not significantly reduced. Different pH treatments at 100 mM salt concentration had no significant effect on alfalfa. However, at the 200 mM salt concentration, the growth and the absorption of nutrients and water, as well as the activities of the PSII and PSI were significantly inhibited. It is worth mentioning that the inhibition in the case of pH 9.0 treatment was more significant. The main reason for the higher pH to intensify the growth and photosynthesis inhibition were not caused by the absorption of more Na⁺. It might be concluded that the higher pH led to the decrease of the root activity, which restricted the absorption of water and nutrients.

Funding Statement

This research was supported by ‘Young Talents’ Project of Northeast Agricultural University [18QC12] and The National Natural Science Fund [31901088].

References

1.Ali S, Rizwan M, Qayyum MF, Ok YS, Ibrahim M, Riaz M, Arif MS, Hafeez F, Al-Wabel MI, Shahzad AN, et al. Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review. Environ Sci Pollut Res Int. 2017;24(14):1–9. doi: 10.1007/s11356-017-8904-x. [DOI] [PubMed] [Google Scholar]
2.Yan SH, Ji J, Wang G.. Effects of salt stress on plants and the mechanism of salt tolerance. World Sci-Technol Res Dev. 2006;28:70–76. [Google Scholar]
3.Forni C, Duca D, Glick BR.. Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil. 2017;410(1–2):335–356. doi: 10.1007/s11104-016-3007-x. [DOI] [Google Scholar]
4.Munns R, James RA, Läuchli A.. Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot. 2006;57(5):1025–1043. doi: 10.1093/jxb/erj100. [DOI] [PubMed] [Google Scholar]
5.Munns R, Tester M. Mechanisms of Salinity Tolerance. Annu Rev Plant Biol. 2008;59(1):651–681. doi: 10.1146/annurev.arplant.59.032607.092911. [DOI] [PubMed] [Google Scholar]
6.Zhang JT, Mu CS. Effeets of saline and alkaline stresses on the germination, growth, photosynthesis, ionic balance and anti-oxidant system in an alkali-tolerant Leguminou Forage Lathyrus quinquenervius. Soil Sci Plant Nutr. 2009a;55:685–697. doi: 10.1111/j.1747-0765.2009.00411.x. [DOI] [Google Scholar]
7.Yang C, Chong J, Li C, Kim C, Shi D, Wang D. Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil. 2007;294(1–2):263–276. doi: 10.1007/s11104-007-9251-3. [DOI] [Google Scholar]
8.Zhang HH, Li X, Guan YP, Li MB, Wang Y, An MJ, Zhang Y H, Liu GJ, Xu N, Sun GY. Physiological and proteomic responses of reactive oxygen species and antioxidant machinery in leaves of mulberry (Morus alba L.) to NaCl and NaHCO₃ stress. Ecotoxicol Environ Saf. 2020a;193:110259. doi: 10.1016/j.ecoenv.2020.110259. [DOI] [PubMed] [Google Scholar]
9.Zhang HH, Wang Y, Li X, Guoqiang H, Yanhui C, Zhiyuan T, Jieyu S, Nan X, Guangyu S. Chlorophyll synthesis and the photoprotective mechanism in leaves of mulberry (Morus alba L.) seedlings under NaCl and NaHCO₃ stress revealed by TMT-based proteomics analyses. Ecotoxicol Environ Saf. 2020b;190:110164. doi: 10.1016/j.ecoenv.2020.110164. [DOI] [PubMed] [Google Scholar]
10.Xiao CX, Cui XL, Lu HY, Han L, Liu S, Zheng Y, Wang H, Wang H, Yang C. Comparative adaptive strategies of old and young leaves to alkali-stress in hexaploid wheat. Environ Exp Bot. 2020;171:103955. doi: 10.1016/j.envexpbot.2019.103955. [DOI] [Google Scholar]
11.Yang CW, Jianar A, Li CY, Shi DC, Wang DL. Comparison of the effects of salt-stress and alkali-stress on photosynthesis and energy storage of an alkali-resistant halophyte Chloris virgata. Photosynthetica. 2008;46(2):273–278. doi: 10.1007/s11099-008-0047-3. [DOI] [Google Scholar]
12.Zhao Z, Liu J, Jia R, Bao S, Chen X. Physiological and TMT-based proteomic analysis of oat early seedlings in response to alkali stress. J Proteomics. 2019;193:10–26. doi: 10.1016/j.jprot.2018.12.018. [DOI] [PubMed] [Google Scholar]
13.Liu Y, Wang Q, Zhang Y, Cui J, Chen G, Xie B, Wu C, Liu H. Synergistic and antagonistic effects of salinity and pH on germination in switchgrass (Panicum virgatum L.). Plos One. 2014;9(1):e85282. doi: 10.1371/journal.pone.0085282. [DOI] [PMC free article] [PubMed] [Google Scholar]
14.Zhang HH, Li X, Xu N, Sun GY, Sun ML, Cai DJ, Gu SY. Alkalinity and salinity tolerance during seed germination and early seedling stages of three alfalfa (Medicago sativa L.) cultivars. Legume Res. 2017a;40(5):853–858. [Google Scholar]
15.Jia X-M, Wang H, Svetla S, Zhu Y-F, Hu Y, Cheng L, Zhao T, Wang Y-X. Comparative physiological responses and adaptive strategies of apple Malus halliana to salt, alkali and saline-alkali stress. Sci Hortic (Amsterdam). 2019;245:154–162. doi: 10.1016/j.scienta.2018.10.017. [DOI] [Google Scholar]
16.Rui G, Shi LX, Yang YF. Germination, growth, osmotic adjustment and ionic balance of wheat in response to saline and alkaline stresses. Soil Sci Plant Nutr. 2009;55(5):667–679. doi: 10.1111/j.1747-0765.2009.00406.x. [DOI] [Google Scholar]
17.Sarkar AN, Wynjones RG. Effect of rhizosphere pH on the availability and uptake of Fe, Mn and Zn. Plant Soil. 1982;66(3):361–372. doi: 10.1007/BF02183802. [DOI] [Google Scholar]
18.Guo R, Shi LX, Ding XM, Hu Y, Tian S, Yan D, Shao S, Gao Y, Liu R, Yang Y, et al. Effects of Saline and Alkaline Stress on Germination, Seedling Growth, and Ion Balance in Wheat. Agron J. 2010;102(4):1252–1260. doi: 10.2134/agronj2010.0022. [DOI] [Google Scholar]
19.Wang X, Geng S, Ri YJ, Cao D, Liu J, Shi D, Yang C. Physiological responses and adaptive strategies of tomato plants to salt and alkali stresses. Sci Hortic (Amsterdam). 2011;130(1):248–255. doi: 10.1016/j.scienta.2011.07.006. [DOI] [Google Scholar]
20.Gong B, Wen D, Vandenlangenberg K, Wei M, Yang F, Shi Q, Wang X. Comparative effects of NaCl and NaHCO₃ stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hortic (Amsterdam). 2013;157:1–12. doi: 10.1016/j.scienta.2013.03.032. [DOI] [Google Scholar]
21.Guan Q, Liao X, He M, Li X, Wang Z, Ma H, Yu S, Liu S. Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO₃ stress. Plos One. 2017;12(10):e0186052. doi: 10.1371/journal.pone.0186052. [DOI] [PMC free article] [PubMed] [Google Scholar]
22.Dąbrowski P, Baczewska AH, Pawluśkiewicz B, Paunov M, Alexantrov V, Goltsev V, Kalaji MH. Prompt chlorophyll a, fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in Perennial ryegrass. J Photochem Photobiol Biol. 2016;157(7):22–31. doi: 10.1016/j.jphotobiol.2016.02.001. [DOI] [PubMed] [Google Scholar]
23.Jin X, Liu T, Xu J, Gao Z, Hu X. Exogenous GABA enhances muskmelon tolerance to salinity-alkalinity stress by regulating redox balance and chlorophyll biosynthesis. BMC Plant Biol. 2019;19(1):48. doi: 10.1186/s12870-019-1660-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
24.Zhang HH, Shi GL, Shao JY, Xin L, Ma-bo L, Liang M, Nan X, Guang-yu S. Photochemistry and proteomics of mulberry (Morus alba L.) seedlings under NaCl and NaHCO₃ stress. Ecotoxicol Environ Saf. 2019;184(30):109624. doi: 10.1016/j.ecoenv.2019.109624. [DOI] [PubMed] [Google Scholar]
25.Zhang HH, Li X, Zhang SB, Yin Z, Zhu W, Li J, Meng L, Zhong H, Xu N, Wu Y, et al. Rootstock alleviates salt stress in grafted mulberry seedlings: physiological and PSII Function responses. Front Plant Sci. 2018a;9:1806. doi: 10.3389/fpls.2018.01806. [DOI] [PMC free article] [PubMed] [Google Scholar]
26.Takahashi M, Shigeto J, Sakamoto A, Morikawa H. Selective nitration of PsbO1, PsbO2, and PsbP1 decreases PSII oxygen evolution and photochemical efficiency in intact leaves of Arabidopsis. Plant Signal Behav. 2017;12(10):e1376157. doi: 10.1080/15592324.2017.1376157. [DOI] [PMC free article] [PubMed] [Google Scholar]
27.Xu N, Zhang HH, Zhong HX, Wu YN, Li JB, Li X, Yin ZP, Zhu WX, Qu Y, Sun GY. The response of photosynthetic functions of F₁ cutting seedlings from Physocarpus amurensis Maxim (♀) × Physocarpus opulifolius “Diabolo” (♂) and the parental leaves to salt stress. Front Plant Sci. 2018;9:714. doi: 10.3389/fpls.2018.00714. [DOI] [PMC free article] [PubMed] [Google Scholar]
28.Huang Z, Liu Y, Cui Z, Fang Y, He H, Liu B-R, Wu G-L. Soil water storage deficit of alfalfa (Medicago sativa) grasslands along ages in arid area (China). Field Crops Res. 2018;221:1–6. doi: 10.1016/j.fcr.2018.02.013. [DOI] [Google Scholar]
29.Wang L, Seki K, Miyazaki T, Ishihama Y. The causes of soil alkalinization in the Songnen Plain of Northeast China. Paddy Water Environ. 2009;7(3):259–270. doi: 10.1007/s10333-009-0166-x. [DOI] [Google Scholar]
30.He H, Peng Q, Wang X, Fan C, Pang J, Lambers H, Zhang X. Growth, morphological and physiological responses of alfalfa (Medicago sativa) to phosphorus supply in two alkaline soils. Plant Soil. 2017;416(1–2):565–584. doi: 10.1007/s11104-017-3242-9. [DOI] [Google Scholar]
31.Ruicai L, Mingna L, Tiejun Z, Junmei K, Yan S, Lili C, Yanli G, Fengqi L, Qingchuan Y. Comparative proteomic analysis reveals differential root Proteins in Medicago sativa and Medicago truncatula in response to salt stress. Front Plant Sci. 2016;7:424. [DOI] [PMC free article] [PubMed] [Google Scholar]
32.Lei Y, Xu Y, Hettenhausen C, Lu C, Shen G, Zhang C, Li J, Song J, Lin H, Wu J, et al. Comparative analysis of alfalfa (Medicago sativa L.) leaf transcriptomes reveals genotype-specific salt tolerance mechanisms. BMC Plant Biol. 2018;18(1):35. doi: 10.1186/s12870-018-1250-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
33.Tingting S, Huihui X, Na S, Jiang L, Tian P, Yong Y, Yang W, Cai H, Cui G. Metabolomic Analysis of alfalfa (Medicago sativa L.) root-symbiotic rhizobia responses under alkali stress. Front Plant Sci. 2017;8:1208. doi: 10.3389/fpls.2017.01208. [DOI] [PMC free article] [PubMed] [Google Scholar]
34.Wang ZY, Song FB, Cai H, Zhu YM, Bai X, Ji W, Li Y, Hua Y. Over-expressing GsGST14 from glycine soja enhances alkaline tolerance of transgenic Medicago sativa. Biol Plant. 2012;56(3):516–520. [Google Scholar]
35.Yunting L, Qing L, Christian H, Guoyan C, Qing T, Weiye Z, Honghui L, Jianqing W. Salt-tolerant and -sensitive alfalfa (Medicago sativa) cultivars have large variations in defense responses to the lepidopteran insect Spodoptera litura under normal and salt stress condition. Plos One. 2017;12(7):e0181589. doi: 10.1371/journal.pone.0181589. [DOI] [PMC free article] [PubMed] [Google Scholar]
36.Zhao Y, Zhu YM, Bai X, JI W, WU J, TANG -L-L, CAI H. Over-expressing GsCBRLK/SCMRP Enhances Alkaline Tolerance and Methionine Content in Transgenic Medicago sativa. Acta Agronomica Sinica. 2014;40(3):431. doi: 10.3724/SP.J.1006.2014.00431. [DOI] [Google Scholar]
37.Ashrafi E, Razmjoo J, Zahedi M. Effect of salt stress on growth and ion accumulation of alfalfar (Medicago sativa L.) cultivars. J Plant Nutr. 2018;41(7):1–14. [Google Scholar]
38.Schansker G, Srivastava A, Strasser RJ. Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol. 2003;30(7):785–796. doi: 10.1071/FP03032. [DOI] [PubMed] [Google Scholar]
39.Shao XJ, Yang HQ, Qiao HT, Zhang L, You SZ. Effects of CdCl₂ on grape root mitochondrial characteristics and root activity. Chin J Appl Ecol. 2009;20(6):1390–1394. [PubMed] [Google Scholar]
40.Bao SD. Soil analysis. Beijing, China: China agriculture press; 2005. [Google Scholar]
41.Zhao Q, Suo J, Chen S, Jin Y, Ma X, Yin Z, Zhang Y, Wang T, Luo J, Jin W, et al. Na₂CO₃-responsive mechanisms in halophytePuccinellia tenuifloraroots revealed by physiological and proteomic analyses. Sci Rep. 2016;6:32717. doi: 10.1038/srep32717. [DOI] [PMC free article] [PubMed] [Google Scholar]
42.Martinez JP, Kinet JM, Bajji M, Lutts S. NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. J Exp Bot. 2005;56(419):2421–2431. doi: 10.1093/jxb/eri235. [DOI] [PubMed] [Google Scholar]
43.Zhang HH, Li X, Xu ZS, Wang Y, Teng ZY, An MJ, Zhang YH, Zhu WX, Xu N, Sun GY. Toxic effects of heavy metal Pb and Cd on mulberry (Morus alba L.) leaves: photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicol Environ Saf. 2020c;195:110469. doi: 10.1016/j.ecoenv.2020.110469. [DOI] [PubMed] [Google Scholar]
44.Zhang HH, Xu ZS, Huo YZ, Guo K, Wang Y, He G, Sun H, Li M, Li X, Xu N, et al. Overexpression of Trx CDSP32 gene promotes chlorophyll synthesis and photosynthetic electron transfer and alleviates cadmium-induced photoinhibition of PSII and PSI in tobacco leaves. J Hazard Mater. 2020d;397:122899. doi: 10.1016/j.jhazmat.2020.122899. [DOI] [PubMed] [Google Scholar]
45.Strasser RJ, Srivastava A, Govindjee G. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol. 1995;61(1):32–42. doi: 10.1111/j.1751-1097.1995.tb09240.x. [DOI] [Google Scholar]
46.Zhang HH, Xu ZS, Guo KW, Huo Y, He G, Sun H, Guan Y, Xu N, Yang W, Sun G, et al. Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicol Environ Saf. 2020e;202:110856. doi: 10.1016/j.ecoenv.2020.110856. [DOI] [PubMed] [Google Scholar]
47.Zhang ZS, Jin LQ, Li YT, Tikkanen M, Li Q-M, Ai X-Z, Gao H-Y. Ultraviolet-B radiation (UV-B) relieves chilling-light-induced PSI photoinhibition and accelerates the recovery of CO₂ assimilation in cucumber (Cucumis sativus L.) leavesl. Sci Rep. 2016;6:34455. doi: 10.1038/srep34455. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0001] 1.Ali S, Rizwan M, Qayyum MF, Ok YS, Ibrahim M, Riaz M, Arif MS, Hafeez F, Al-Wabel MI, Shahzad AN, et al. Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review. Environ Sci Pollut Res Int. 2017;24(14):1–9. doi: 10.1007/s11356-017-8904-x. [DOI] [PubMed] [Google Scholar]

[cit0002] 2.Yan SH, Ji J, Wang G.. Effects of salt stress on plants and the mechanism of salt tolerance. World Sci-Technol Res Dev. 2006;28:70–76. [Google Scholar]

[cit0003] 3.Forni C, Duca D, Glick BR.. Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil. 2017;410(1–2):335–356. doi: 10.1007/s11104-016-3007-x. [DOI] [Google Scholar]

[cit0004] 4.Munns R, James RA, Läuchli A.. Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot. 2006;57(5):1025–1043. doi: 10.1093/jxb/erj100. [DOI] [PubMed] [Google Scholar]

[cit0005] 5.Munns R, Tester M. Mechanisms of Salinity Tolerance. Annu Rev Plant Biol. 2008;59(1):651–681. doi: 10.1146/annurev.arplant.59.032607.092911. [DOI] [PubMed] [Google Scholar]

[cit0006] 6.Zhang JT, Mu CS. Effeets of saline and alkaline stresses on the germination, growth, photosynthesis, ionic balance and anti-oxidant system in an alkali-tolerant Leguminou Forage Lathyrus quinquenervius. Soil Sci Plant Nutr. 2009a;55:685–697. doi: 10.1111/j.1747-0765.2009.00411.x. [DOI] [Google Scholar]

[cit0007] 7.Yang C, Chong J, Li C, Kim C, Shi D, Wang D. Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil. 2007;294(1–2):263–276. doi: 10.1007/s11104-007-9251-3. [DOI] [Google Scholar]

[cit0008] 8.Zhang HH, Li X, Guan YP, Li MB, Wang Y, An MJ, Zhang Y H, Liu GJ, Xu N, Sun GY. Physiological and proteomic responses of reactive oxygen species and antioxidant machinery in leaves of mulberry (Morus alba L.) to NaCl and NaHCO₃ stress. Ecotoxicol Environ Saf. 2020a;193:110259. doi: 10.1016/j.ecoenv.2020.110259. [DOI] [PubMed] [Google Scholar]

[cit0009] 9.Zhang HH, Wang Y, Li X, Guoqiang H, Yanhui C, Zhiyuan T, Jieyu S, Nan X, Guangyu S. Chlorophyll synthesis and the photoprotective mechanism in leaves of mulberry (Morus alba L.) seedlings under NaCl and NaHCO₃ stress revealed by TMT-based proteomics analyses. Ecotoxicol Environ Saf. 2020b;190:110164. doi: 10.1016/j.ecoenv.2020.110164. [DOI] [PubMed] [Google Scholar]

[cit0010] 10.Xiao CX, Cui XL, Lu HY, Han L, Liu S, Zheng Y, Wang H, Wang H, Yang C. Comparative adaptive strategies of old and young leaves to alkali-stress in hexaploid wheat. Environ Exp Bot. 2020;171:103955. doi: 10.1016/j.envexpbot.2019.103955. [DOI] [Google Scholar]

[cit0011] 11.Yang CW, Jianar A, Li CY, Shi DC, Wang DL. Comparison of the effects of salt-stress and alkali-stress on photosynthesis and energy storage of an alkali-resistant halophyte Chloris virgata. Photosynthetica. 2008;46(2):273–278. doi: 10.1007/s11099-008-0047-3. [DOI] [Google Scholar]

[cit0012] 12.Zhao Z, Liu J, Jia R, Bao S, Chen X. Physiological and TMT-based proteomic analysis of oat early seedlings in response to alkali stress. J Proteomics. 2019;193:10–26. doi: 10.1016/j.jprot.2018.12.018. [DOI] [PubMed] [Google Scholar]

[cit0013] 13.Liu Y, Wang Q, Zhang Y, Cui J, Chen G, Xie B, Wu C, Liu H. Synergistic and antagonistic effects of salinity and pH on germination in switchgrass (Panicum virgatum L.). Plos One. 2014;9(1):e85282. doi: 10.1371/journal.pone.0085282. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0014] 14.Zhang HH, Li X, Xu N, Sun GY, Sun ML, Cai DJ, Gu SY. Alkalinity and salinity tolerance during seed germination and early seedling stages of three alfalfa (Medicago sativa L.) cultivars. Legume Res. 2017a;40(5):853–858. [Google Scholar]

[cit0015] 15.Jia X-M, Wang H, Svetla S, Zhu Y-F, Hu Y, Cheng L, Zhao T, Wang Y-X. Comparative physiological responses and adaptive strategies of apple Malus halliana to salt, alkali and saline-alkali stress. Sci Hortic (Amsterdam). 2019;245:154–162. doi: 10.1016/j.scienta.2018.10.017. [DOI] [Google Scholar]

[cit0016] 16.Rui G, Shi LX, Yang YF. Germination, growth, osmotic adjustment and ionic balance of wheat in response to saline and alkaline stresses. Soil Sci Plant Nutr. 2009;55(5):667–679. doi: 10.1111/j.1747-0765.2009.00406.x. [DOI] [Google Scholar]

[cit0017] 17.Sarkar AN, Wynjones RG. Effect of rhizosphere pH on the availability and uptake of Fe, Mn and Zn. Plant Soil. 1982;66(3):361–372. doi: 10.1007/BF02183802. [DOI] [Google Scholar]

[cit0018] 18.Guo R, Shi LX, Ding XM, Hu Y, Tian S, Yan D, Shao S, Gao Y, Liu R, Yang Y, et al. Effects of Saline and Alkaline Stress on Germination, Seedling Growth, and Ion Balance in Wheat. Agron J. 2010;102(4):1252–1260. doi: 10.2134/agronj2010.0022. [DOI] [Google Scholar]

[cit0019] 19.Wang X, Geng S, Ri YJ, Cao D, Liu J, Shi D, Yang C. Physiological responses and adaptive strategies of tomato plants to salt and alkali stresses. Sci Hortic (Amsterdam). 2011;130(1):248–255. doi: 10.1016/j.scienta.2011.07.006. [DOI] [Google Scholar]

[cit0020] 20.Gong B, Wen D, Vandenlangenberg K, Wei M, Yang F, Shi Q, Wang X. Comparative effects of NaCl and NaHCO₃ stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hortic (Amsterdam). 2013;157:1–12. doi: 10.1016/j.scienta.2013.03.032. [DOI] [Google Scholar]

[cit0021] 21.Guan Q, Liao X, He M, Li X, Wang Z, Ma H, Yu S, Liu S. Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO₃ stress. Plos One. 2017;12(10):e0186052. doi: 10.1371/journal.pone.0186052. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0022] 22.Dąbrowski P, Baczewska AH, Pawluśkiewicz B, Paunov M, Alexantrov V, Goltsev V, Kalaji MH. Prompt chlorophyll a, fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in Perennial ryegrass. J Photochem Photobiol Biol. 2016;157(7):22–31. doi: 10.1016/j.jphotobiol.2016.02.001. [DOI] [PubMed] [Google Scholar]

[cit0023] 23.Jin X, Liu T, Xu J, Gao Z, Hu X. Exogenous GABA enhances muskmelon tolerance to salinity-alkalinity stress by regulating redox balance and chlorophyll biosynthesis. BMC Plant Biol. 2019;19(1):48. doi: 10.1186/s12870-019-1660-y. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0024] 24.Zhang HH, Shi GL, Shao JY, Xin L, Ma-bo L, Liang M, Nan X, Guang-yu S. Photochemistry and proteomics of mulberry (Morus alba L.) seedlings under NaCl and NaHCO₃ stress. Ecotoxicol Environ Saf. 2019;184(30):109624. doi: 10.1016/j.ecoenv.2019.109624. [DOI] [PubMed] [Google Scholar]

[cit0025] 25.Zhang HH, Li X, Zhang SB, Yin Z, Zhu W, Li J, Meng L, Zhong H, Xu N, Wu Y, et al. Rootstock alleviates salt stress in grafted mulberry seedlings: physiological and PSII Function responses. Front Plant Sci. 2018a;9:1806. doi: 10.3389/fpls.2018.01806. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0026] 26.Takahashi M, Shigeto J, Sakamoto A, Morikawa H. Selective nitration of PsbO1, PsbO2, and PsbP1 decreases PSII oxygen evolution and photochemical efficiency in intact leaves of Arabidopsis. Plant Signal Behav. 2017;12(10):e1376157. doi: 10.1080/15592324.2017.1376157. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0027] 27.Xu N, Zhang HH, Zhong HX, Wu YN, Li JB, Li X, Yin ZP, Zhu WX, Qu Y, Sun GY. The response of photosynthetic functions of F₁ cutting seedlings from Physocarpus amurensis Maxim (♀) × Physocarpus opulifolius “Diabolo” (♂) and the parental leaves to salt stress. Front Plant Sci. 2018;9:714. doi: 10.3389/fpls.2018.00714. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0028] 28.Huang Z, Liu Y, Cui Z, Fang Y, He H, Liu B-R, Wu G-L. Soil water storage deficit of alfalfa (Medicago sativa) grasslands along ages in arid area (China). Field Crops Res. 2018;221:1–6. doi: 10.1016/j.fcr.2018.02.013. [DOI] [Google Scholar]

[cit0029] 29.Wang L, Seki K, Miyazaki T, Ishihama Y. The causes of soil alkalinization in the Songnen Plain of Northeast China. Paddy Water Environ. 2009;7(3):259–270. doi: 10.1007/s10333-009-0166-x. [DOI] [Google Scholar]

[cit0030] 30.He H, Peng Q, Wang X, Fan C, Pang J, Lambers H, Zhang X. Growth, morphological and physiological responses of alfalfa (Medicago sativa) to phosphorus supply in two alkaline soils. Plant Soil. 2017;416(1–2):565–584. doi: 10.1007/s11104-017-3242-9. [DOI] [Google Scholar]

[cit0031] 31.Ruicai L, Mingna L, Tiejun Z, Junmei K, Yan S, Lili C, Yanli G, Fengqi L, Qingchuan Y. Comparative proteomic analysis reveals differential root Proteins in Medicago sativa and Medicago truncatula in response to salt stress. Front Plant Sci. 2016;7:424. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0032] 32.Lei Y, Xu Y, Hettenhausen C, Lu C, Shen G, Zhang C, Li J, Song J, Lin H, Wu J, et al. Comparative analysis of alfalfa (Medicago sativa L.) leaf transcriptomes reveals genotype-specific salt tolerance mechanisms. BMC Plant Biol. 2018;18(1):35. doi: 10.1186/s12870-018-1250-4. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0033] 33.Tingting S, Huihui X, Na S, Jiang L, Tian P, Yong Y, Yang W, Cai H, Cui G. Metabolomic Analysis of alfalfa (Medicago sativa L.) root-symbiotic rhizobia responses under alkali stress. Front Plant Sci. 2017;8:1208. doi: 10.3389/fpls.2017.01208. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0034] 34.Wang ZY, Song FB, Cai H, Zhu YM, Bai X, Ji W, Li Y, Hua Y. Over-expressing GsGST14 from glycine soja enhances alkaline tolerance of transgenic Medicago sativa. Biol Plant. 2012;56(3):516–520. [Google Scholar]

[cit0035] 35.Yunting L, Qing L, Christian H, Guoyan C, Qing T, Weiye Z, Honghui L, Jianqing W. Salt-tolerant and -sensitive alfalfa (Medicago sativa) cultivars have large variations in defense responses to the lepidopteran insect Spodoptera litura under normal and salt stress condition. Plos One. 2017;12(7):e0181589. doi: 10.1371/journal.pone.0181589. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0036] 36.Zhao Y, Zhu YM, Bai X, JI W, WU J, TANG -L-L, CAI H. Over-expressing GsCBRLK/SCMRP Enhances Alkaline Tolerance and Methionine Content in Transgenic Medicago sativa. Acta Agronomica Sinica. 2014;40(3):431. doi: 10.3724/SP.J.1006.2014.00431. [DOI] [Google Scholar]

[cit0037] 37.Ashrafi E, Razmjoo J, Zahedi M. Effect of salt stress on growth and ion accumulation of alfalfar (Medicago sativa L.) cultivars. J Plant Nutr. 2018;41(7):1–14. [Google Scholar]

[cit0038] 38.Schansker G, Srivastava A, Strasser RJ. Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol. 2003;30(7):785–796. doi: 10.1071/FP03032. [DOI] [PubMed] [Google Scholar]

[cit0039] 39.Shao XJ, Yang HQ, Qiao HT, Zhang L, You SZ. Effects of CdCl₂ on grape root mitochondrial characteristics and root activity. Chin J Appl Ecol. 2009;20(6):1390–1394. [PubMed] [Google Scholar]

[cit0040] 40.Bao SD. Soil analysis. Beijing, China: China agriculture press; 2005. [Google Scholar]

[cit0041] 41.Zhao Q, Suo J, Chen S, Jin Y, Ma X, Yin Z, Zhang Y, Wang T, Luo J, Jin W, et al. Na₂CO₃-responsive mechanisms in halophytePuccinellia tenuifloraroots revealed by physiological and proteomic analyses. Sci Rep. 2016;6:32717. doi: 10.1038/srep32717. [DOI] [PMC free article] [PubMed] [Google Scholar]

[cit0042] 42.Martinez JP, Kinet JM, Bajji M, Lutts S. NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. J Exp Bot. 2005;56(419):2421–2431. doi: 10.1093/jxb/eri235. [DOI] [PubMed] [Google Scholar]

[cit0043] 43.Zhang HH, Li X, Xu ZS, Wang Y, Teng ZY, An MJ, Zhang YH, Zhu WX, Xu N, Sun GY. Toxic effects of heavy metal Pb and Cd on mulberry (Morus alba L.) leaves: photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicol Environ Saf. 2020c;195:110469. doi: 10.1016/j.ecoenv.2020.110469. [DOI] [PubMed] [Google Scholar]

[cit0044] 44.Zhang HH, Xu ZS, Huo YZ, Guo K, Wang Y, He G, Sun H, Li M, Li X, Xu N, et al. Overexpression of Trx CDSP32 gene promotes chlorophyll synthesis and photosynthetic electron transfer and alleviates cadmium-induced photoinhibition of PSII and PSI in tobacco leaves. J Hazard Mater. 2020d;397:122899. doi: 10.1016/j.jhazmat.2020.122899. [DOI] [PubMed] [Google Scholar]

[cit0045] 45.Strasser RJ, Srivastava A, Govindjee G. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol. 1995;61(1):32–42. doi: 10.1111/j.1751-1097.1995.tb09240.x. [DOI] [Google Scholar]

[cit0046] 46.Zhang HH, Xu ZS, Guo KW, Huo Y, He G, Sun H, Guan Y, Xu N, Yang W, Sun G, et al. Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicol Environ Saf. 2020e;202:110856. doi: 10.1016/j.ecoenv.2020.110856. [DOI] [PubMed] [Google Scholar]

[cit0047] 47.Zhang ZS, Jin LQ, Li YT, Tikkanen M, Li Q-M, Ai X-Z, Gao H-Y. Ultraviolet-B radiation (UV-B) relieves chilling-light-induced PSI photoinhibition and accelerates the recovery of CO₂ assimilation in cucumber (Cucumis sativus L.) leavesl. Sci Rep. 2016;6:34455. doi: 10.1038/srep34455. [DOI] [PMC free article] [PubMed] [Google Scholar]

PERMALINK

Effects of salt concentration, pH, and their interaction on plant growth, nutrient uptake, and photochemistry of alfalfa (Medicago sativa) leaves

Guo Kaiwen

Xu Zisong

Huo Yuze

Sun Qi

Wang Yue

Che Yanhui

Wang Jiechen

Li Wei

Zhang Huihui

ABSTRACT