Open AccessArticle

Photosynthetic and Physiological Characteristics of Three Common Halophytes and Their Relationship with Biomass Under Salt Stress Conditions in Northwest China

Xi Zhang

^1,2,3

Tao Lin

^2,4,

Hailiang Xu

^1,2,*,

Guaikui Gao

^1,2 and

Haitao Dou

^1,2

State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China

Engineering Technology Innovation Centre for Desert-Oasis Ecological Monitoring and Restoration, Ministry of Natural Resources, Urumqi 830011, China

College of Geographic Science and Tourism, Xinjiang Normal University, Urumqi 830054, China

⁴

Xinjiang Uygur Autonomous Region Comprehensive Land Management Centre, Urumqi 830011, China

Author to whom correspondence should be addressed.

Appl. Sci. 2024, 14(24), 11890; https://doi.org/10.3390/app142411890

Submission received: 12 October 2024 / Revised: 13 December 2024 / Accepted: 17 December 2024 / Published: 19 December 2024

(This article belongs to the Special Issue Recent Advances in Halophytes Plants)

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Abstract

Three different types of common halophytes (Haloxylon ammodendron, Tamarix chinensis, and Phragmites australis) in northwest China were used in this study. A field experiment approach was adopted, involving five solutions with different salt concentrations (0, 150, 200, 250, and 300 mmol·L⁻¹) for salt stress treatment. The changes in photosynthetic characteristics and physiological characteristics of three different types of halophytes and their relationship with biomass were measured and analyzed. The results showed that (1) with the increase in salt concentration, the plant height, stem diameter, and biomass of three halophytes showed a downward trend. (2) The chlorophyll a, chlorophyll b, and total chlorophyll contents of Haloxylon ammodendron and Tamarix chinensis first increased and then decreased with the increase in salt concentration. Phragmites australis showed a decreasing trend. The malondialdehyde content of three halophytes showed a clear increasing trend. (3) Under different salt concentrations, the diurnal changes in the net photosynthetic rate, transpiration rate, stomatal conductance, and water use efficiency of three different types of halophytes all showed an “M” trend. The diurnal variation in intercellular carbon dioxide concentration showed a “W” trend. (4) With the increase in salt concentration, the daily average values of the net photosynthetic rate, transpiration rate, and stomatal conductance of three different types of halophytes showed a downward trend. The daily average value of intercellular carbon dioxide concentration showed a “V”-shaped trend of first decreasing and then increasing. The daily average value of water use efficiency showed a “single peak” trend of first increasing and then decreasing. Haloxylon ammodendron and Phragmites australis were mainly limited by stomata at a salt concentration of 0~200 mmol·L⁻¹ and were mainly limited by non-stomata at a salt concentration of 250~300 mmol·L⁻¹. Tamarix chinensis is mainly limited by stomata at a salt concentration of 0~250 mmol·L⁻¹ and is mainly limited by non-stomata at a salt concentration of 300 mmol·L⁻¹. Compared with Haloxylon ammodendron and Phragmites australis, Tamarix chinensis has better water use efficiency, salt tolerance, and adaptability. (5) Meteorological factors, growth morphological factors, physiological factors, photosynthetic factors, and salt concentration have higher explanatory degrees, which have significant effects on the biomass of halophytes. Among them, salt concentration and growth morphological factors have direct core driving effects on the biomass of three different types of halophytes, while meteorological factors, photosynthetic factors, and physiological factors have different effects due to the differences in and complexity of halophytes. This study can provide a theoretical basis for further revealing the adaptation mechanism of different halophytes to salt stress.

Keywords:

salt stress; halophytes; ecological factors; biomass; ecological recovery

1. Introduction

Salinization is one of the main causes of land desertification and land degradation. At present, salinization has become a global ecological and resource problem and a major ecological crisis facing mankind [1]. According to FAO statistics, saline soil is distributed in more than 100 countries and regions around the world, and the total area of saline soil in the world has reached 954 million hm². In the above total saline soil area, Oceania accounts for about 37.5%, Asia for about 33.3%, America for about 15.4%, Africa for about 8.5%, and Europe for about 5.3% [2]. With climate change and the unsustainable development and utilization of resources by human beings, the area of salinized land is gradually expanding. At present, the area of salinized land worldwide is increasing at a rate of 1–1.5 million hm² per year. The salinized land in China accounts for 10.38% of the total salinized soil area worldwide. The saline land in the northwest region alone accounts for 69.03% of the total saline land area in China, accounting for a large proportion [3]. Salinization has become one of the main limiting factors of ecological construction in northwest China, which seriously restricts the development and utilization of agricultural and forestry resources in this area.

Many scholars from different countries have conducted extensive research on soil salinization. In the last century, Kovda et al. found that groundwater and arid climate play an important role in the formation of saline soil [4]. Gkiougkis et al. analyzed the salinized soil in eastern Greece and found that the salt content of the soil could be reduced using the pipe drainage method [5]. Nematollahi et al. improved the saline soil in northern Iran through deep tillage measures and found that although the vertical distribution of soil salt was changed after deep tillage, the overall soil salt did not decrease [6]. Many studies have found that planting halophytes is an economical and effective method for improving land salinization [7]. Researchers in India and African countries have successfully cultivated many salt-tolerant plants by planting and developing them on saline soil and successfully applied them to land salinization improvement [8]. Barrett not only cultivated halophytes with strong salt tolerance but also successfully improved land salinization in southern Australia using halophytes [9]. There are about 1560 species of halophytes worldwide, among which there are 300~400 species of halophytes with certain economic value. There are many kinds of halophytes, but the types of halophytes differ due to variations in environmental factors such as soil and climate in different regions. On the basis of previous studies, Breckle classified halophytes into three different types according to the transport, storage, and secretion characteristics of salt ions in halophytes: euhalophytes, recreteohalophytes, and pseudohalophytes, with each type of halophyte having a unique morphological structure and physiological functions [10].

Photosynthesis and physiological functions are fundamental to ensuring yield formation in the process of plant growth and development. When soil salinization occurs, plants will be subjected to osmotic stress, which will inhibit photosynthesis and the physiological functions of plants [11]. Zhang et al. found that salt stress clearly inhibited the photosynthesis of Morus alba seedlings [12]. Different halophytes differ in sensitivity and tolerance to salt, and the effects of salt stress on their photosynthetic characteristics and physiological characteristics also differ [13]. For example, Xiao et al., focusing on the Yinbei area in Ningxia, found that salt stress has a great influence on photosynthesis and the physiological function of Festuca ovina but little influence on Helianthus annuus as a whole [14]. Although the northwest of China has a dry climate, scarce precipitation, and a large area of salinized land, there are still many different kinds of halophytes that can continue to grow under such harsh environmental conditions. The mechanism of salt tolerance is worthy of further study. Based on this, this study is based on three different types of common halophytes; for each halophyte type, 4 common plants were selected (12 plants in total, 100 replicates in each plant, and 1200 samples in total). From 2021 to 2023, long-term field planting monitoring was carried out in the northwest of China. Finally, a representative halophyte with the best growth state and survival rate was selected from each type of halophyte as the research object of this experiment (Figure A1). Haloxylon ammodendron is the representative plant with the best growth state and survival rate in euhalophytes. Tamarix chinensis is the representative plant with the best growth state and survival rate in recretohalophytes. Phragmites australis is the representative plant with the best growth state and survival rate in pseudohalophytes. At present, few studies have been conducted on the salt tolerance of different types of halophytes in the northwest of China, and the salt tolerance mechanism is still unclear. Therefore, in this study, Haloxylon ammodendron, Tamarix chinensis, and Phragmites australis were taken as research objects to explore the photosynthetic physiological characteristics of three different types of common halophytes under salt stress, as well as their relationship with biomass and related effects. The purpose of this study is to provide practical scientific guidance for soil and farmland improvement in salinized areas and to provide a theoretical basis for understanding the salt tolerance mechanism of halophytes.

2. Materials and Methods

2.1. Overview of the Study Area

The study area is located in the central part of Yizhou District, Hami City, Xinjiang, China, with relatively flat terrain between the Tianshan Mountains in the north and the Gobi Desert in the south. The geographical coordinates are 93°15′00″ E~93°05′30″ E and 42°25′15″ N~42°16′45″ N (Figure 1a). There are many remnant mounds in the study area, which are rounded and flat at the top. The arid valleys between the residual hills are broadly developed, and the surface is covered with rock debris, sand, and gravel, typical of the Gobi landscape (Figure 1b). With long, cold winters; hot and dry summers; large annual and daily temperature differences; and year-round drought with little rain, it has a temperate continental arid climate [15]. With long light hours and high solar radiation, the total annual solar radiation can reach 6397.35 MJ/m². The average annual wind speed is 3 m/s~4 m/s, the average annual temperature is 3 °C~17 °C, the average annual precipitation is 50.78 mm, and the average annual evaporation is 3064.13 mm. The soil types in the study area are mainly desert soils with very high salt content, and the soil specifics are shown in Table 1.

2.2. Experimental Design

2.2.1. Research Objectives

The research focuses on three different types of halophytes common in northwest China: euhalophytes (Haloxylon ammodendron (hereinafter referred to as Ha)), recreteohalophytes (Tamarix chinensis (hereinafter referred to as Tc)), and pseudohalophytes (Phragmites australis (hereinafter referred to as Pa)). Ha is a perennial plant of the Amaranthaceae Haloxylon, mainly found in Central Asia. It is the main establishment species of desert vegetation in the arid zone, i.e., salt- and drought-tolerant and can not only grow in sand dunes with a high-water table but can also survive normally in saline soils. Tc is a perennial plant of the Tamaricaceae family, Tamarix, mainly found in northwestern China. The root system is well developed, with strong sprouting ability, and is salt, cold, and drought resistant. It is not demanding in terms of climate and soil conditions, allowing it to grow in harsh environments. Phragmites (Pa) is a perennial plant of the Poaceae family and is widely distributed throughout. It is highly environmentally adaptable and can not only form dominant species in riverine areas but can also grow normally in sand dunes and saline soils.

2.2.2. Experimental Program

From January 2021 to January 2023, early monitoring of halophyte planting was carried out. The research objects suitable for this experiment were selected through a comprehensive evaluation. In mid-February, 2023, this experiment was carried out in the middle of Yizhou District. Three different types of halophytes were planted randomly. Five large sample plots of 20 m × 20 m were set for each halophyte. In order to avoid the interaction of different salt solutions between large sample plots, a 5 m buffer zone was set between large sample plots. A 5 m × 5 m small sample plot was set at five positions in the four corners and center of each large sample plot. When the spacing between plants is too small, it will affect the balance between the promotion and competition between plants. To provide plants with a better living space, through many experiments and comparisons, the optimal spacing between halophytes was finally determined to be 2 m [16]. Therefore, one plant was planted in the four corners and five positions in the center of each plot, and the spacing between plants was 2 m. In total, there were 15 large plots, 75 small plots, and 375 samples in this experiment. After three different types of halophytes were planted in the small sample plot, fresh water was used for drip irrigation. After all three different types of halophytes had grown normally for 30 days, salt stress treatment was carried out again. Through the investigation of different areas in the study area, the lowest salt concentration of groundwater in the study area was found to be 150 mmol·L⁻¹, and the highest was 300 mmol·L⁻¹, under natural conditions. In order to simulate the common salt concentration levels in this study area, we designed five salt solutions with different concentrations, namely, 150 mmol·L⁻¹, 200 mmol·L⁻¹, 250 mmol·L⁻¹, and 300 mmol·L⁻¹, with 0 mmol·L⁻¹ as the control (Table 2). Irrigation was carried out using drip irrigation. Five plots of each halophyte were irrigated with the above five salt solutions with different concentrations, and the period of drip irrigation was once every 7 days. The experiment was completed in mid-August, 2023, and the indexes were determined.

2.3. Measurement Indicators and Methods

2.3.1. Measurement of Meteorological Factors

Meteorological factors were monitored using automatic meteorological stations in the vicinity of the study area, and changes in meteorological factors were recorded every hour. The meteorological factors measured include the atmospheric temperature (°C), relative humidity (%), and atmospheric carbon dioxide concentration (μmol·mol⁻¹). The daily variation in meteorological factors in the study area is shown in Figure 2. Atmospheric temperatures showed a significant upward trend from 07:00 to 11:00 and reached a maximum at 13:00 with temperatures up to 39 °C, followed by a slow downward trend. The trends in relative humidity and atmospheric carbon dioxide concentration were consistent. Both the relative humidity and atmospheric carbon dioxide concentration were the highest in the early morning. They showed a gradual decreasing trend from 7:00 to 11:00 and reached a minimum at 13:00 with 18% and 330 μmol·mol⁻¹, respectively. This was followed by a slow upward trend in relative humidity and atmospheric carbon dioxide concentration as the atmospheric temperature decreased.

2.3.2. Measurement of Growth Indicators

At the end of the experiment, ten plants with relatively uniform growth were selected for each halophyte under different concentrations of salt solution treatments for the determination of growth indexes. Plant height was determined using a tape measure (accuracy: 0.1 cm). The stem diameter of the plants was determined using vernier calipers (accuracy: 0.01 mm) at a distance of 5 cm from the ground surface. The selected plants were removed whole, washed with deionized water, placed in an oven, and dried at 105 °C for 30 min and then at 85 °C for 48 h until constant weight, then weighed using an electronic balance (accuracy: 0.001 g) and recorded as total biomass.

2.3.3. Measurement of Physiological Indicators

At the end of the experiment, fresh leaves from the middle of each halophyte were selected for physiological indexes under different concentrations of salt solution treatments. The malondialdehyde content was determined with reference to the method of Zhang [17]. A measure of 0.3 g of fresh leaves was weighed in a mortar, and 2 mL of 5% trichloroacetic acid was added; they were ground, and then the solution was extracted using centrifugation at 3000 r/min for 10 min; finally, the malondialdehyde content was determined using the thiobarbituric acid method. The chlorophyll content was determined with reference to the method of Gao [18]. A measure of 0.5 g of fresh leaves was weighed and ground into powder, and then the solution was extracted with a 95% ethanol–acetone mixture. The absorbance values of the extracted solution at 645 nm and 663 nm were determined spectrophotometrically, and the contents of chlorophyll a, chlorophyll b, and total chlorophyll were calculated. The formulae are as follows:

C h l o r o p h y l l a = (12.7 D_{663 n m} - 2.69 D_{645 n m}) \times [V / (1000 \times W)]

(1)

C h l o r o p h y l l b = (22.9 D_{645 n m} - 4.68 D_{663 n m}) \times [V / (1000 \times W)]

(2)

T o t a l c h l o r o p h y l l = C h l a + C h l b

(3)

In the formula: D is the absorbance value, V is the total volume of leaf extract (mL), and W is the mass of leaf (g).

2.3.4. Measurement of Photosynthetic Parameters

Photosynthetic parameters were measured in the middle leaves of each halophyte under different salt solution treatments using the LI-6400 Convenient Photosynthesis Measurement System analyzer from LI-COR, Lincoln city, NE, USA, on a sunny day. Measurements were taken every 2 h from 07:00 to 19:00. The light intensity of the photosynthesis measurement system analyzer was set at 1000 μmol·m⁻²·s⁻¹, the carbon dioxide concentration was set at 400 μmol·mol⁻¹, the flow rate was set at 500 μmol·s⁻¹, the humidity was set at 20% to 30%, and the temperature of the control leaf chamber was set at 25 °C. The net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular carbon dioxide concentration (Ci), and transpiration rate (Tr) of leaves were measured. Also, the water use efficiency (Wue) of leaves was calculated using the following equation:

W u e = P n / T r

(4)

2.4. Redundancy Analysis

Redundancy analysis (RDA) is a method based on constraint analysis, which is mainly used to analyze the relationship between ecological factors and species change. Redundancy analyses allow the selection of ecological factors with greater explanatory power from all of them, thus revealing the causes of species change. A detrended correspondence analysis (DCA) was first performed, and redundancy analysis was selected if the analysis showed that the maximum value in the sorting axis was less than 3. If greater than 4, canonical correspondence analysis (CCA) is selected. If it is between 3 and 4, both analyses are possible [19]. The results of this study, analyzed by detrending correspondence, show that the maximum values in the sorting axis are all less than 3. Therefore, in this study, a redundancy analysis based on linear models was chosen to analyze the relationship between different ecological factors and halophyte biomass.

2.5. Structural Equation Modeling

Structural equation modeling (SEM) is a comprehensive statistical and analytical method of data analysis based on the covariance matrix of variables to analyze the relationship between different variables. This model integrates regression analysis, causal analysis, path analysis, and other analytical methods, which can not only represent the complex variable relationship network intuitively with the model but can also discern the strength of the relationship between the variables and test the direct and indirect relationships between the variables [20]. To further determine the effects of different ecological factors on halophytes, this study used structural equation modeling to analyze and quantify the direct and indirect effects of different ecological factors on the biomass of each halophyte. Direct effects refer to the effects of different ecological factors on biomass directly, while indirect effects refer to the effects of different ecological factors on biomass indirectly by influencing other ecological factors later. Due to the large number of variables in the structural equation model, the fitness of the model can be tested using several key indices to determine the goodness of fit of the model. These indices include the chi-square (χ²), degrees of freedom (df), p-value of the chi-square (p), standardized fit indicator (CFI), root mean square of approximation error (RMSEA), and goodness of fit indicator (GFI). When 1 < χ²/df < 3, p > 0.05 indicates that the model has good confidence. When the CFI and GFI are greater than 0.9, it indicates a good model fit. When the RMSEA is less than 0.08, it indicates a good model fit.

2.6. Data Processing and Statistical Analysis

Microsoft Excel 2022 software was used for basic data statistics and processing. One-way ANOVA, regression analysis, and mean comparison testing (expressed by mean standard deviation) were carried out using IBMSPSS statistics 25.0 software. The LSD method of DPS 7.05 software was used to test the significance of differences. Redundancy analysis was performed using Canoco 5.0 software. The structural equation modeling was conducted in R 4.3.1 using the “piecewise SEM package”. Mapping was carried out using ArcGIS 10.8 and Origin 2022 software.

3. Results

3.1. Effects of Different Salt Concentration Treatments on the Growth of Halophytes

With increasing salt concentration, the plant height and stem diameter of all three halophytes were inhibited to varying degrees (Figure 3). The plant heights of Ha, Tc, and Pa were highest at a salt concentration of 0 mmol·L⁻¹, which were 158.3 cm, 131.9 cm, and 91.1 cm, respectively. The plant height of Ha and Tc at a salt concentration of 150 mmol·L⁻¹ decreased compared with the control, but the difference was not significant (p > 0.05). Compared with the control, the plant height of Ha at a salt concentration of 200~300 mmol·L⁻¹ decreased by 13%, 33.2%, and 45.5%, respectively, and there were significant differences between them and the control (p < 0.05). Compared with the control, the plant height of Tc decreased by 9.7%, 27.7%, and 38.5%, respectively, at a salt concentration of 200~300 mmol·L⁻¹, and there were significant differences between them and the control (p < 0.05). Pa plant height at salt concentrations of 150~300 mmol·L⁻¹ was reduced by 6%, 32.6%, 53.3%, and 65.8%, respectively, and all of them were significantly different (p < 0.05) from the control.

The highest stem diameters of 6.3, 4.8, and 0.7 cm were recorded for Ha, Tc, and Pa, respectively, under the treatment with a salt concentration of 0 mmol·L⁻¹. Stem diameter of Ha at a salt concentration of 150 mmol·L⁻¹ was reduced compared with the control, but the difference was not significant (p > 0.05). The stem diameter of Ha at salt concentrations of 200~300 mmol·L⁻¹ was reduced by 51%, 56.7%, and 64.9%, respectively, and all of them were significantly different (p < 0.05) from the control. The stem diameter of Tc at salt concentrations of 150~200 mmol·L⁻¹ was not significantly different (p > 0.05) from that of the control, although it was slightly reduced. The stem diameter of Tc at salt concentrations of 250~300 mmol·L⁻¹ was reduced by 18.2% and 40.2%, respectively, compared with the control, and both were significantly different (p < 0.05) from the control. Stem diameter of Pa under different salt concentration treatments was not found to be significantly different between treatments (p > 0.05), although it was reduced compared to the control.

3.2. Effects of Different Salt Concentration Treatments on Physiological Indexes of Halophytes

As can be seen in Figure 4, different salt concentration treatments had significant effects on the physiological indices of the three plants. The chlorophyll a, chlorophyll b, and total chlorophyll contents of Ha and Tc showed a trend of increasing and then decreasing with increasing salt concentration, both reaching a maximum at 150 mmol·L⁻¹ salt concentration and a minimum at 300 mmol·L⁻¹ salt concentration. Chlorophyll a, chlorophyll b, and total chlorophyll contents of Ha increased by 14.9%, 11.5%, and 14.6%, respectively, whereas Tc increased by 9.4%, 7.1%, and 9.4%, respectively, at a salt concentration of 150 mmol·L⁻¹ compared with the control but were not significantly different (p > 0.05) from the control. At a salt concentration of 300 mmol·L⁻¹, the chlorophyll a, chlorophyll b, and total chlorophyll contents of Ha and Tc were significantly lower than those of the control (p < 0.05), by 29.3%, 67.6%, and 32.5% for Ha and by 16.3%, 48.3%, and 22.2% for Tc, respectively. It is noteworthy that the chlorophyll a, chlorophyll b, and total chlorophyll contents of Pa all showed a gradual decrease with increasing salt concentration. The levels of the three at a salt concentration of 300 mmol·L⁻¹ were significantly lower than those of the control (p < 0.05), with reductions of 38.7%, 67.9%, and 45.3%, respectively, compared with the control.

Under normal conditions, malondialdehyde levels were low in the three halophytes. The malondialdehyde content of the three halophytes also showed a significant increasing trend with increasing salt concentration, and all of them reached a maximum at a salt concentration of 300 mmol·L⁻¹. At a salt concentration of 300 mmol·L⁻¹, the malondialdehyde content of Ha, Tc, and Pa was 6.95, 10.20, and 16.3 μmol·g⁻¹, respectively, which increased by 15.7%, 13.9%, and 21.8%, respectively, compared with the control and was significantly different from the control in all cases (p < 0.05).

3.3. Characteristics of Changes in Photosynthetic Parameters of Halophytes Under Different Salt Concentration Treatments

3.3.1. Characteristics of Daily Changes in Net Photosynthetic Rate (Pn) of Halophytes Under Different Salt Concentration Treatments

Under different salt concentration treatments, the daily changes in Pn of the three halophytes showed a “bimodal” trend of increasing, then decreasing, then increasing, and then decreasing, with the peaks occurring at 11:00 and 17:00, respectively (Figure 5). The maximum value of Pn appeared at 11:00 for all three halophytes. The maximum values of Pn in Ha were 32.40, 25.73, 22.30, 18.47, and 14.73 μmol·m⁻²·s⁻¹ at salt concentrations ranging from approximately 0 to 300 mmol·L⁻¹ treatment, respectively. The Pn maxima for Tc were 28.47, 24.13, 20.80, 17.73, and 14.23 μmol·m⁻²·s⁻¹, respectively. The Pn maxima for Pa were 23.83, 19.30, 15.97, 11.70, and 8.67 μmol·m⁻²·s⁻¹, respectively.

The daily mean Pn values of the three halophytes decreased with increasing salt concentration. The daily mean values of Pn for Ha, Tc, and Pa were all highest at a salt concentration of 0 mmol·L⁻¹ and were 21.55, 15.03, and 14.29 μmol·m⁻²·s⁻¹, respectively. Both Ha and Pa showed a significant decreasing trend (p < 0.05) in the daily mean Pn at salt concentrations of 150~300 mmol·L⁻¹ compared with the control. Ha decreased by 15.11%, 29.42%, 44.74%, and 57.15%, while Pa decreased by 19.62%, 34.88%, 50.31%, and 67.61%, respectively. The daily mean Pn of Tc at a salt concentration of 150 mmol·L⁻¹ was not significantly different (p > 0.05) from that of the control but was significantly different (p < 0.05) from that of the control at salt concentrations of 200~300 mmol·L⁻¹.

3.3.2. Characteristics of Daily Changes in Transpiration Rate (Tr) of Halophytes Under Different Salt Concentration Treatments

As can be seen from Figure 6, the daily variation in Tr of the three halophytes was consistent with the daily variation in net photosynthetic rate and also showed a “bimodal” trend. Tr peaked at 11:00 and 17:00 for all three halophytes and was significantly higher at 11:00 than at 17:00. The Tr maxima of Ha were 8.23, 6.37, 5.30, 4.80, and 4 mmol·m⁻²·s⁻¹ at salt concentrations ranging from approximately 0 to 300 mmol·L⁻¹ treatment, respectively. The Tr maxima for Tc were 9.63, 7.87, 7.24, 6.30, and 5.71 mmol·m⁻²·s⁻¹, respectively. The Tr maxima for Pa were 9.03, 6.73, 4.87, 4.57, and 4.03 mmol·m⁻²·s⁻¹, respectively.

The daily mean Tr values of all three halophytes showed a gradual decreasing trend with increasing salt concentration. The daily mean values of Tr for Ha, Tc, and Pa were all highest at a salt concentration of 0 mmol·L⁻¹ and were 5.82, 7.57, and 6.21 mmol·m⁻²·s⁻¹, respectively. It decreased to a minimum at a salt concentration of 300 mmol·L⁻¹, where Ha, Tc, and Pa decreased by 50.98, 44.51, and 55.73%, respectively, compared with the control. At salt concentrations of 150~300 mmol·L⁻¹, the daily means of Tr for Ha, Tc, and Pa were all significantly different from the control (p < 0.05).

3.3.3. Characteristics of Daily Changes in Stomatal Conductance (Gs) of Halophytes Under Different Salt Concentration Treatments

Under the treatment of different salt concentrations, the daily change pattern of Gs of the three halophytes was shown in Figure 7, which showed a trend of increasing, then decreasing, then increasing, and then decreasing, which was basically consistent with the daily change pattern of the net photosynthetic rate. The maximum value of Gs was observed at 11:00 for all three halophytes. The maximum values of Gs for Ha were 0.81, 0.68, 0.57, 0.46, and 0.37 mmol·m⁻²·s⁻¹ at salt concentrations ranging from approximately 0 to 300 mmol·L⁻¹ treatment, respectively. The Gs maxima for Tc were 0.73, 0.59, 0.50, 0.36, and 0.30 mmol·m⁻²·s⁻¹, respectively. The maximum values of Gs for Pa were 0.57, 0.40, 0.32, 0.27, and 0.20 mmol·m⁻²·s⁻¹, respectively.

The daily mean values of Gs for the three halophytes decreased with increasing salt concentration. The daily means of Gs for Ha, Tc, and Pa were all highest at a salt concentration of 0 mmol·L⁻¹ and were 0.54, 0.41, and 0.34 mmol·m⁻²·s⁻¹, respectively. Compared with the control, the daily mean values of Gs for Ha, Tc, and Pa at salt concentrations ranging from approximately 150 to 300 mmol·L⁻¹ showed a significant decrease (p < 0.05). Ha decreased by 19.70%, 33.95%, 46.17%, and 59.72%, respectively. Tc was reduced by 12.37%, 26.59%, 38.73%, and 48.21%, respectively. Pa was reduced by 22.66%, 38.74%, 51.05%, and 67.83%, respectively.

3.3.4. Characteristics of Daily Changes in Intercellular Carbon Dioxide Concentration (Ci) in Halophytes Under Different Salt Concentration Treatments

Under different salt concentration treatments, the daily changes in Ci in the three halophytes showed a “W” trend of decreasing, then increasing, then decreasing, and then increasing, with the lowest values occurring at 11:00 and 17:00, respectively (Figure 8). The Ci of Ha decreased to a minimum of 219 μmol·mol⁻¹ at 11:00 under the treatment with a salt concentration of 0 mmol·L⁻¹. In contrast, the Ci of Ha was minimized at 17:00 under salt concentration treatments ranging from approximately 150 to 300 mmol·L⁻¹: 172.33, 121.33, 280, and 315.33 μmol·mol⁻¹, respectively. Similarly, the lowest values of Ci for Tc and Pa were observed at 17:00 under the treatment with salt concentrations ranging from 0~300 mmol·L⁻¹. The lowest values of Ci for Tc were 244, 184.67, 145, 118.67, and 274.33 μmol·mol⁻¹, respectively. The lowest values of Ci for Pa were 174, 150.33, 107.67, 239.67, and 270.67 μmol·mol⁻¹, respectively.

With the increase in salt concentration, the daily mean Ci values of the three halophytes showed a trend of decreasing and then increasing. Ha and Pa were minimized at a salt concentration of 200 mmol·L⁻¹, whereas Tc was minimized at a salt concentration of 250 mmol·L⁻¹. Compared with the control, the daily mean values of Ci for Ha showed a significant (p < 0.05) decrease at salt concentrations of 150~200 mmol·L⁻¹ by 13.89% and 33.86%, respectively. A significant increasing trend (p < 0.05) was observed at salt concentrations of 250~300 mmol·L⁻¹, which increased by 12.71% and 27.97%, respectively.

Notably, although the daily mean values of Ci at salt concentrations of 150 mmol·L⁻¹ for Tc and Pa were reduced compared with the control, the difference was not significant (p > 0.05). The daily mean Ci values of Tc at salt concentrations of 200~250 mmol·L⁻¹ showed a significant (p < 0.05) decrease compared with the control, by 25.67% and 35.33%, respectively. A significant increasing trend (p < 0.05) was observed at a salt concentration of 300 mmol·L⁻¹, which increased by 13.16%. The daily mean Ci of Pa showed a significant (p < 0.05) decrease of 39.18% at a salt concentration of 200 mmol·L⁻¹ treatment compared with the control. A significant increasing trend (p < 0.05) was observed at salt concentrations of 250~300 mmol·L⁻¹, which increased by 14.38% and 26.07%, respectively.

3.3.5. Characteristics of Daily Changes in Water Use Efficiency (Wue) of Halophytes Under Different Salt Concentration Treatments

As can be seen in Figure 9, under different salt concentration treatments, the daily changes in Wue of three kinds of halophytes showed different regular trends, and the overall “double-peak” trend of first increasing, then decreasing, then increasing, and then decreasing was presented. The Wue of Ha appeared to be at its maximum at 15:00 with 4.27, 4.65, and 4.90 μmol·mol⁻¹ at salt concentrations ranging from approximately 0 to 200 mmol·L⁻¹, respectively. However, the Wue of Ha showed a maximum value of 3.96 μmol·mol⁻¹ at 9:00 when treated with a salt concentration of 250 mmol·L⁻¹. The Wue of Ha showed a maximum value of 3.70 μmol·mol⁻¹ at 17:00 under treatment with a 300 mmol·L⁻¹ salt concentration. The Wue of Tc appeared to be at its maximum at 11:00 with 2.96, 2.81, 2.87, 3.07, and 2.49 μmol·mol⁻¹ under the treatment of salt concentration from approximately 0 to 300 mmol·L⁻¹, respectively. The Wue of Pa appeared to be at its maximum at 17:00 with 2.66 and 2.39 μmol·mol⁻¹ at salt concentrations of 0~250 mmol·L⁻¹ treatments, respectively. However, at salt concentrations of 150~200 mmol·L⁻¹ and 300 mmol·L⁻¹ treatments, the Wue of Pa showed a maximum at 11:00, which was 2.87, 3.30, and 2.22 μmol·mol⁻¹, respectively.

With the increase in salt concentration, the daily mean of Wue and the daily mean of intercellular carbon dioxide concentration of the three halophytes showed the opposite trend of “single-peak” change, which first increased and then decreased. Ha and Pa rose to a maximum at a salt concentration of 200 mmol·L⁻¹, whereas Tc rose to a maximum at a salt concentration of 250 mmol·L⁻¹. The daily means of Wue for Ha and Pa at a salt concentration of 150 mmol·L⁻¹ were increased compared with the control, but the difference was not significant (p > 0.05). At a salt concentration of 200 mmol·L⁻¹, the daily means of Wue for Ha and Pa were significantly increased by 11.7% and 22.6%, respectively, compared with the control (p < 0.05). However, the daily mean values of Wue for Ha were significantly reduced by 4.3% and 12.8%, respectively, at salt concentrations ranging from approximately 250 to 300 mmol·L⁻¹ compared with the control. The daily mean values of Wue for Pa decreased significantly by 12.1% and 28.4%, respectively (p < 0.05). Importantly, although the daily mean of Wue for Tc increased at salt concentrations of 150~250 mmol·L⁻¹ compared with control, the difference was not significant (p > 0.05). In contrast, at a salt concentration of 300 mmol·L⁻¹, the daily mean Wue of Tc was significantly decreased by 11.8% (p < 0.05) compared with the control.

3.4. Relationship Between Ecological Factors and Biomass of Halophytes Under Salt Stress Conditions

3.4.1. Effect of Different Salt Concentration Treatments on Biomass of Halophytes

The biomass of all three halophytes was affected to varying degrees with increasing salt concentration. As can be seen in Figure 10, the biomasses of Ha, Tc, and Pa all showed a decreasing trend with increasing salt concentration. The biomasses of Ha, Tc, and Pa were highest in the treatment with a salt concentration of 0 mmol·L⁻¹ and decreased to a minimum at a salt concentration of 300 mmol·L⁻¹. The biomasses of Ha, Tc, and Pa were 50.60, 31.70, and 18.00 g, respectively, at a salt concentration of 0 mmol·L⁻¹ treatment. The biomasses of Ha, Tc, and Pa were reduced by 64.9%, 41.2%, and 83%, respectively, at a salt concentration of 300 mmol·L⁻¹ treatment compared with the control. Biomass was analyzed by regression for salt concentration treatments and three halophytes. The fitted R² for biomasses of Ha, Tc, and Pa were found to be 0.663, 0.708, and 0.597, respectively, which were all greater than 0.5, providing a good fit (Table 3). Meanwhile, significant correlation (p < 0.05) was found between salt concentration treatments and biomass of all three halophytes through ANOVA testing.

3.4.2. Redundancy Analysis of Different Ecological Factors with Halophytes Biomass

In RDA ordination diagrams, ecological factors are generally represented by hollow arrows. The length of the arrow connecting the lines represents the magnitude of correlation of an ecological factor with the analyzed indicator. Redundancy analysis of the ecological factors with the biomass of halophytes showed that 71.53% and 12.17% were explained by the first and second sorting axes, respectively, i.e., the total explanation of the two sorting axes was 83.7%. It indicates that the first two axes can effectively reflect the relationship between ecological factors and halophyte biomasses, and the ordering is good (Figure 11a). As can be seen from the figure, the longer connecting lines for salt concentration, plant height, malondialdehyde, chlorophyll a, intercellular carbon dioxide concentration, stem diameter, chlorophyll b, atmospheric temperature, net photosynthetic rate, stomatal conductance, and relative humidity indicate a greater correlation between these ecological factors and the biomass of halophytes. The degree of interpretation of the biomass of halophytes by different ecological factors is shown in Figure 11b. From the figure, it can be seen that salt concentration, plant height, malondialdehyde, chlorophyll a, intercellular carbon dioxide concentration, stem diameter, chlorophyll b, atmospheric temperature, net photosynthetic rate, stomatal conductance, and relative humidity were more highly interpreted compared with the other ecological factors, and all of them could significantly affect the biomass of the halophytes (p < 0.05).

3.4.3. Structural Equation Modeling of Different Ecological Factors and Halophytes Biomass

Structural equation modeling allows the visualization of the relationships between different indicators, calculation of path coefficients between indicators, and comparison of the magnitude of impact. However, since the measures vary from indicator to indicator, the same type of indicator needs to be downscaled to extract the new variables and then analyzed using structural equation modeling. Redundancy analysis revealed that salt concentration, plant height, malondialdehyde, chlorophyll a, intercellular carbon dioxide concentration, stem diameter, chlorophyll b, atmospheric temperature, net photosynthesis rate, stomatal conductance, and relative humidity had longer line segments, which were more correlated with the biomass of the halophytes, so the above metrics were selected for the downscaling process. According to relevant professional knowledge, the variables of the “meteorological factor” are extracted from the atmospheric temperature and relative humidity. The “growth morphological factors” variable was extracted from plant height and stem diameter. Regarding the extraction of “physiological factors” variables from chlorophyll a, chlorophyll b, and malondialdehyde, the “photosynthetic factors” variable was extracted from the net photosynthetic rate, stomatal conductance, and intercellular carbon dioxide concentration. Salt concentration was then used as a separate variable. From Figure 12a–c, it can be seen that the results of structural equation modeling analysis of different ecological factors with a halophyte biomass of χ²/df were all in the range of 1 to 3, with a p value greater than 0.05, CFI and GFI greater than 0.9, RMSEA below 0.08, and good overall model fit.

A comprehensive analysis of the structural equation model results of three different types of halophytes shows that different ecological factors play different roles in different halophytes. In the structural equation model of Ha, salt concentration and growth morphological factors play a core driving role in biomass, among which salt concentration has a highly significant negative impact, and the path coefficient is −0.86 (p < 0.001). Although the growth morphological factors were influenced by salt concentration, meteorological factors, photosynthetic factors, and physiological factors, the growth morphological factors still showed a highly significant positive impact on Ha biomass, with a path coefficient of 0.72 (p < 0.001). The influence of meteorological factors on Ha biomass was not significant (p > 0.05). Under the influence of salt concentration and meteorological factors, photosynthetic factors and physiological factors have positive effects on biomass, but photosynthetic factors have more obvious effects on Ha biomass, and the path coefficient is 0.50 (p < 0.05). In the structural equation model of Tc, salt concentration, growth morphological factors, and meteorological factors all have effects on biomass, among which salt concentration has a very significant negative effect, and the path coefficient is −0.67 (p < 0.01). Meteorological factors showed a significant negative impact, and the path coefficient was −0.55 (p < 0.05). Under the influence of different ecological factors, the growth morphological factors had a significant positive effect on the biomass of Tc, and the path coefficient was 0.65 (p < 0.05). Under the influence of salt concentration and meteorological factors, although photosynthetic factors and physiological factors had positive effects on Tc biomass, the effects were not significant (p > 0.05). In the structural equation model of Pa, salt concentration, meteorological factors, photosynthetic factors, physiological factors, and growth morphological factors all have obvious effects on biomass. Among them, the salt concentration showed a highly significant negative impact, and the path coefficient was −0.72 (p < 0.001). Meteorological factors showed a significant negative impact, and the path coefficient was −0.39 (p < 0.05). Under the influence of different ecological factors, the growth morphological factors had a very significant positive effect on the biomass of Pa, and the path coefficient was 0.62 (p < 0.01). Under the influence of salt concentration and meteorological factors, photosynthetic factors had a significant positive effect on the biomass of Pa, and the path coefficient was 0.38 (p < 0.05). However, physiological factors had a very significant positive effect on the biomass of Pa, and the path coefficient was 0.46 (p < 0.01).

As can be seen from the figure, because the growth morphological factors have a direct impact on the biomass of three different types of halophytes, there is no indirect impact on the growth morphological factors. At the same time, as can be seen from Figure 12d–f, compared with other ecological factors, the direct effects of salt concentration and growth morphology factors on the biomass of three different types of halophytes are more obvious. The direct effects of salt concentration, meteorological factors, photosynthetic factors, physiological factors, and growth morphological factors on Ha were −0.86, −0.17, 0.50, 0.25, and 0.72, respectively, and the indirect effects were −0.67, 0.48, 0.29, and 0.13, respectively. The direct effects of salt concentration, meteorological factors, photosynthetic factors, physiological factors, and growth morphological factors on Tc were −0.67, −0.55, 0.22, 0.20, and 0.65, respectively, and the indirect effects were −0.68, 0.43, 0.33, and 0.34, respectively. The direct effects of salt concentration, meteorological factors, photosynthetic factors, physiological factors, and growth morphological factors on Pa were −0.72, −0.39, 0.38, 0.46, and 0.62, respectively, and the indirect effects were −1.07, 0.29, 0.16, and 0.13, respectively.

4. Discussion

4.1. Response of Growth Morphology of Halophytes to Salt Stress

Plants undergoing adverse stress can reduce the harm of adversity to themselves in different ways. Three different types of halophytes have special plant organs, which can be adjusted by their own organs to survive in the face of salt stress. (i) Euhalophytes: Haloxylon ammodendron. Salt can be accumulated in the vacuoles of green tissue cells through the regionalization of salt ions, thus reducing the salt in the body. (ii) Recreteohalophytes: Tamarix chinensis. Salt glands, or salt vesicles, can be used to directly excrete excessive salt ions from the body, thus avoiding salt damage. (iii) Pseudohalophytes: Phragmites australis. Salt can be accumulated in vacuoles of parenchyma or parenchyma of root xylem, which reduces the upward transport of ions and reduces the salt in the body [10]. The environment in the northwest of China is harsh, and the salinity is high. When halophytes are stressed by adversity, their external morphology will change to adapt to the harm caused by the harsh environment [21]. Plant height, stem diameter, and biomass are all significant indicators that can directly reflect plant growth and are also the most direct basis for evaluating plant salt tolerance. Although euhalophytes, recretohalophytes, and pseudohalophytes all have special plant organs, when the salt concentration is too high, they will still have a direct impact on the growth of three different types of plants. In this study, with the increase in salt concentration, the plant height, stem diameter, and biomass of three different types of halophytes were inhibited to varying degrees, showing a decreasing trend. However, Zhi et al. found that with the increase in salt concentration, the biomass of five garden salt-tolerant plants not only showed an upward trend but also made the soil desalination rate of saline–alkali land reach 31%, and according to this result, the environmental greening and landscape restoration effects in saline–alkali areas were improved [22]. This may be due to the different plants studied and the different salt concentration ranges, leading to different research conclusions. At present, many studies show that with the increase in salt concentration, the growth of plants will be clearly inhibited, which is consistent with the conclusion of this study. For example, Shannon et al. analyzed the salt tolerance of Oryza sativa in California and found that with the increase in salt concentration, the growth rate of Oryza sativa gradually decreased [23]. Flower’s research in Brighton shows that the plant height of crops will be notably shortened when it is stressed by salt [24]. Garima et al. found in India that with the increase in salt concentration, the biomass of Brassica juncea decreased gradually, and the salt tolerance of different varieties of Brassica juncea was different [25]. Liu et al. also found that when the salt concentration was high, the biomass of Coleus hybridus also showed a downward trend [26]. This is because when the salt concentration is high, osmosis, ion stress, and oxidation stress are enhanced, and plants absorb a lot of harmful ions, which hinders cell division and destroys metabolism, thus affecting the absorption and utilization of water and nutrients in plants, then leading to plant growth damage and slow development.

4.2. Responses of Physiological Functions of Halophytes to Salt Stress

Chlorophyll is an important carrier for light energy aggregation and transmission, and it is one of the important physiological indexes for measuring the stress resistance of plants; its content can also reflect the growth status of plants [27]. Many studies have found that the chlorophyll content of plants can reflect the salt tolerance of plants to a certain extent [28]. Mandhania et al. found in Haryana, India, that the chlorophyll content of Triticum aestivum has a clear correlation with the degree of salt stress [29]. Sogoni et al. found in South Africa that with an increase in salt concentration, the chlorophyll content of Tetragonia decumbens showed a “single peak” pattern change trend [30]. In this study, with the increase in salt concentration, the chlorophyll content of Ha, Tc, and Pa showed different changes. The contents of chlorophyll a, chlorophyll b, and total chlorophyll in Ha and Tc increased first and then decreased, and the turning point was a salt concentration of 150 mmol·L⁻¹. However, Pa shows a decreasing trend. This may be because Ha is composed of euhalophytes and Tc is composed of reteohalophytes. When the salt concentration is low, the special organ structure of Ha and Tc enables them to adapt to adversity and promote the increase in chlorophyll. However, when the salt concentration is too high, too many harmful ions enter the plant body, causing damage to the grana lamella and thylakoid structure in chloroplasts, which makes the salt-discharging ability of Ha and Tc reach the limit. Therefore, the chlorophyll leading to Ha and Tc reached the highest when the salt concentration was 150 mmol·L⁻¹ and then gradually decreased [31]. Pa is composed of pseudohalophytes. The absorption of salt can be limited by the suberization in the roots. However, on the one hand, the soil salinity in the study is high. On the other hand, on this basis, plants are irrigated with high-salt-concentration solutions, which enhances the negative impact on plant leaves and leads to salt gradually entering plants. When the salt in plants is too high, some toxic substances, such as cadaverine and putrescine, are often produced. However, the characteristics of Pa, such as impermeability to water and air, make it difficult to discharge toxic substances from plants, so the chlorophyll of Pa gradually decreases [32]. Different from Ha and Tc, which can actively excrete salt in the body, Pa’s salt rejection mechanism is passive, so chlorophyll shows a downward trend.

Salt stress can make plants produce reactive oxygen species, lower cell membrane integrity, and cause membrane lipid peroxidation. Malondialdehyde is the main product of membrane lipid peroxidation, which can directly reflect the damage degree of the plant cell membrane. The higher the content, the more serious the cell membrane damage and the weaker the stress resistance [33]. In this study, with the increase in salt concentration, the malondialdehyde content of three different types of halophytes showed an obvious increasing trend. This is the same as the research findings of Lee et al. in Korea that, with the increase in salt concentration, the synthetase activity of Oryza sativa decreased continuously and the malondialdehyde content increased continuously [34]. This is because with the gradual increase in salt concentration, whether it is Ha, Tc, or Pa, the dynamic equilibrium state in the body is broken and the physiological metabolism process is destroyed. Once the physiological metabolism process and cell membrane of plants are damaged, the cell membrane permeability of plants will continue to increase, and the membrane lipid peroxidation will gradually strengthen, so the malondialdehyde content of Ha, Tc, and Pa will gradually increase [35].

4.3. Response of Photosynthesis of Halophytes to Salt Stress

Photosynthesis is the process of converting light energy into chemical energy, and it is also the main source of plant matter and energy, which is of great significance to plant growth and ecological adaptation. Under salt stress, there are generally four types of diurnal variation in photosynthesis in plants, namely the “single peak” type, the “bimodal” type, the “W” type, and the changeable type [36]. João et al. found that in southern Portugal, with the increase in salt stress, the diurnal variation in stomatal conductance of Atriplex portulacoides showed a “single peak” trend [37]. In Iran, Kafi et al. found that the diurnal variation in photosynthesis of Triticum aestivum showed a changeable trend [38]. In this study, under different salt concentrations, the diurnal changes in net photosynthetic rate, transpiration rate, and stomatal conductance of Ha, Tc, and Pa, as well as the water use efficiency of Tc and Pa, all showed a “double peak” pattern, with the peak values appearing around 11:00 and 17:00, respectively, and the lowest value appearing around 13:00. The diurnal changes in intercellular carbon dioxide concentrations of Ha, Tc, and Pa all showed a “W” shape, with the lowest values appearing around 11:00 and 17:00, respectively, and the maximum values appearing around 13:00. It is worth noting that compared with Tc and Pa, the first peak in daily variation in water use efficiency of Ha appears around 9:00. This is because Ha belongs to euhalophytes. At 9:00, the stomata of Ha gradually opened, and there was more water in the plant vacuole. Therefore, Ha can maintain higher photosynthesis through a lower transpiration rate, which makes the numerical ratio of net photosynthetic rate and transpiration rate quite different. Therefore, the value of water use efficiency calculated according to formula (4) is large. In this study, the first extreme values of the net photosynthetic rate, transpiration rate, stomatal conductance, and intercellular carbon dioxide concentration of Ha, Tc, and Pa all appeared at 11:00. This is because at 11:00, the northwest of China has strong evaporation, high temperature, strong solar radiation, and the most active photosynthesis, so the net photosynthetic rate, transpiration rate, stomatal conductance, and intercellular carbon dioxide concentration all appear to have extreme values. At 13:00, the temperature in the study area reached the highest, and three different types of halophytes had different degrees of “lunch break” in order to prevent themselves from being harmed by excessive temperature. The phenomenon of “lunch break” refers to the fact that at noon, the light intensity is the highest, the temperature is the highest, and the humidity is the lowest. In order to protect themselves from external damage, plants will take the initiative to close their stomata and reduce photosynthesis. After noon, the light and temperature gradually decrease, the humidity increases, the plants will open their stomata again, and photosynthesis will pick up. And with the gradual entry into the evening, the light gradually weakens, and plants can no longer carry out photosynthesis, so photosynthesis will decrease again [39,40]. When plants carry out photosynthesis, they will gradually consume intercellular carbon dioxide in the body, and when plant photosynthesis stops gradually, intercellular carbon dioxide will gradually increase. Therefore, the change trend in intercellular carbon dioxide concentration is the opposite of other photosynthetic parameters [41]. This is the same as Liu et al.’s research conclusion on the changes in photosynthesis in Medicago sativa [42].

According to the theory of stomatal limitation, the reasons for the decrease in plant photosynthesis caused by salt stress are mainly divided into stomatal limitation and non-stomatal limitation [43]. Farquhar and others believe that if the net photosynthetic rate, stomatal conductance, and intercellular carbon dioxide concentration change in the same direction, the main reason for the decrease in photosynthetic parameters is stomatal limitation. If the change direction is opposite (net photosynthetic rate and stomatal conductance decrease, intercellular carbon dioxide concentration increases), then the main reason for the decrease in photosynthetic parameters is non-stomatal limitation [44]. Usually, stomatal limitation and non-stomatal limitation will work together to reduce plant photosynthesis. In this study, with the increase in salt concentration, the net photosynthetic rate, transpiration rate, and stomatal conductance of three different types of halophytes showed a decreasing trend. The daily average value of intercellular carbon dioxide concentration showed a trend of first decreasing and then increasing. Different plants have different critical concentrations of photosynthesis. Burchett et al. found in Australia that Avicennia marina has stronger salt tolerance and a higher critical concentration of photosynthetic rate of leaves than Aegiceras corniculatum [45]. In this study, the critical concentration of Ha and Pa is 200 mmol·L⁻¹, and the critical concentration of Tc is 250 mmol·L⁻¹. Before the critical concentration, in order to maintain cell water potential and self-growth, plants reduce stomatal conductance to prevent cells from losing water, which leads to a decrease in photosynthesis. At this time, stomatal limitation is the main limiting factor. However, when the salt concentration exceeds the critical concentration, with the increase in salt, the photosynthetic mechanism of plants is destroyed and the activity is compromised, and non-stomatal limitation becomes the main limiting factor [46]. It was found that the daily average water use efficiency of three different types of halophytes showed a trend of first increasing and then decreasing. The daily average water use efficiency of Ha and Pa is the highest at a salt concentration of 200 mmol·L⁻¹, while that of Tc is the highest at a salt concentration of 250 mmol·L⁻¹. This shows that compared with Ha and Pa, Tc has stronger water use efficiency, salt tolerance, and better adaptability. This is because the northwest of China is dry all year round, with high evaporation and scarce precipitation. Under this environment, Tc has gradually evolved and formed scaly leaves. The leaves tightly surround the stem, which greatly reduces the area of leaves exposed to the air and increases the utilization efficiency of water in the body. At the same time, Tc has a special salt-secreting halophyte structure—salt gland, which can directly excrete excess salt in cells, thus reducing the accumulation of salt in the body, and the salt discharge efficiency is high. Compared with Tc, in arid environments, Ha leaves gradually degenerate and form assimilated branches. The assimilation of vascular tissue in branches can improve the transportation efficiency of plants to organic matter. However, when the salt concentration is too high, the vascular tissue will deteriorate continuously, thus reducing the discharge efficiency of harmful ions in vacuoles. The root cortex of Pa is suberization, and there are suberin and casparian strip zones in the root cortex. Although it can prevent some harmful ions from entering plants, when the salt concentration is high, cell gap sealing of the suberin and casparian strip will also make it difficult to discharge harmful ions from plants. Therefore, compared with Ha and Pa, Tc has better salt tolerance and adaptability [47].

4.4. Relationship Between Halophyte Biomass and Ecological Factors

Plant biomass is the main indicator of overall plant growth and damage. In the natural environment, plant growth is not only affected by its own physiological effects and photosynthesis, but ecological factors such as light, water, and temperature also play an important role in the development and reproduction of plants [48]. The results of this study, through redundancy analysis, showed that meteorological factors (atmospheric temperature and relative humidity), growth morphological factors (plant height and stem diameter), physiological factors (chlorophyll a, chlorophyll b, and malondialdehyde), photosynthetic factors (net photosynthetic rate, stomatal conductance, and intercellular carbon dioxide concentration), and salt concentration all had a significant effect on the biomass of halophytes. In order to further investigate the complex correlations between various ecological factors and biomass and to analyze the main factors affecting the biomass of halophytes, a structural equation model was developed in this study. Structural equation modeling can not only clearly show the relationships and interactions between the variables but can also explain the direct and indirect effects between the variables. For example, Kang et al. used structural equations to accurately analyze the relationship between biomass and the climate and soil [49]. Huang et al. also used structural equations to analyze the association characteristics between productivity and stand factors in Cunninghamia lanceolata [50].

The present study, using structural equation modeling, revealed significant differences in the mechanism of influence of ecological factors on the biomass of different halophytes. Among them, salt concentration and growth morphological factors were central drivers of biomass in all three halophytes, and the direct and indirect effects were more pronounced. This may be due to ion imbalance and metabolic dysfunction in the plant when subjected to salt stress, and the plant mitigates the effects of salt damage by regulating its morphological growth. The effect of salt concentration and growth morphology factors on biomass was more pronounced as the plant morphology became progressively smaller with increasing salt concentration and eventually showed significant biomass suppression [51]. This is the same as the findings of Zhang et al., who found that the plant height and biomass of Platycodon grandiflorus gradually decreased with increasing salt concentration [52]. Meteorological factors, physiological factors, and photosynthetic factors vary according to the variability and complexity of halophytes. This is because the three plants belong to three different types of halophytes: Ha being euhalophytes, Tc being retretohalophytes, and Pa being pseudohalophytes. In response to salt stress, different types of halophytes also show different responses, such as ions and osmosis in their bodies [53]. Thus, meteorological factors, physiological factors, and photosynthetic factors have different effects on different halophytes.

5. Conclusions

Based on the previous field experiments, in this study, the photosynthetic physiological characteristics of three different types of common halophytes in northwest China under salt stress and their relationship with biomass were analyzed. The following conclusions were drawn: (1) With the increase in salt concentration, the plant height, stem diameter, and biomass of Haloxylon ammodendron (euhalophytes), Tamarix chinensis (recreteohalophytes), and Phragmites australis (pseudohalophytes) all showed a decreasing trend in different degrees. (2) Chlorophyll a, chlorophyll b, and total chlorophyll contents of Haloxylon ammodendron and Tamarix chinensis first increased and then decreased with the increase in salt concentration. Phragmites australis showed a decreasing trend. The malondialdehyde content of three different types of halophytes showed an obvious increasing trend with the increase in salt concentration. (3) Under different salt concentrations, the diurnal changes in the net photosynthetic rate, transpiration rate, stomatal conductance, and water use efficiency of three different types of halophytes showed a “double peak” trend. The diurnal variation in intercellular carbon dioxide concentration shows a “W” trend. (4) With the increase in salt concentration, the daily average values of the net photosynthetic rate, transpiration rate, and stomatal conductance of three different types of halophytes showed a downward trend. With the increase in salt concentration, the daily average value of intercellular carbon dioxide concentration showed a “V”-shaped trend of first decreasing and then increasing. The daily average value of water use efficiency showed a “single peak” trend of first increasing and then decreasing. Haloxylon ammodendron and Phragmites australis were mainly limited by stomata at the salt concentration of 0~200 mmol·L⁻¹ and were mainly limited by non-stomata at a salt concentration of 250~300 mmol·L⁻¹. Tamarix chinensis is mainly limited by stomata at a salt concentration of 0~250 mmol·L⁻¹ and is mainly limited by non-stomata at a salt concentration of 300 mmol·L⁻¹. Compared with Haloxylon ammodendron and Phragmites australis, Tamarix chinensis has better water use efficiency, salt tolerance, and adaptability. (5) Through the analysis of RDA and structural equation modeling, it is found that meteorological factors (atmospheric temperature and relative humidity), growth morphological factors (plant height and stem diameter), physiological factors (chlorophyll a, chlorophyll b, and malondialdehyde), photosynthetic factors (net photosynthetic rate, stomatal conductance, and intercellular carbon dioxide concentration), and salt concentration have higher explanatory degrees, which have significant effects on the biomass of halophytes. Among them, salt concentration and growth morphological factors have direct core driving effects on the biomass of three different types of halophytes, while meteorological factors, photosynthetic factors, and physiological factors have different effects due to the differences in and complexity of halophytes.

At present, the global salinized land area is expanding, and some soil improvement mechanisms are still unclear. Therefore, in this study, three different types of halophytes were planted in the saline–alkali land in the northwest of China, and then the change characteristics of the three different types of halophytes were monitored and analyzed through irrigation with a high-salt-concentration solution. The field ecological restoration effect of this study is significant (Figure A2). This study explored the salt resistance mechanism of three different types of halophytes in high-saline–alkali soil and high-salt-concentration solution, which provided a theoretical basis for ecological management and restoration of farmland and saline areas; it also provided a data basis for planting and screening halophytes. At the same time, this study is also applicable to the fields of environmental beautification and landscape restoration, which can provide a new technical reference for its ecological management.

Author Contributions

Conceptualization, H.X.; methodology, T.L. and G.G.; software, X.Z.; formal analysis, X.Z.; investigation, T.L. and X.Z.; data curation, G.G.; writing—original draft preparation, X.Z.; writing—review and editing, X.Z. and H.X.; visualization, H.D.; project administration, H.X. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the project “Popularization and Application of Key Technologies of Ecological Restoration in Mining Areas (Utilization of High Saline Water)” of Xinjiang Uygur Autonomous Region, China, with the support number JTZB(2023)-082. APC is funded by this project.

Data Availability Statement

The data presented in this study are available on request from the corresponding authors. These data are not publicly available due to ethical restrictions.

Acknowledgments

The main author of this paper thanks the support of the project “Popularization and Application of Key Technologies of Ecological Restoration in Mining Areas (Utilization of Saline Water)” in Xinjiang Uygur Autonomous Region, China, as well as the reviewers for reviewing the manuscript despite their busy schedules and Lu Zhuo for the cooperation. Finally, I would like to thank my mentor, HL. X. I thank him for his guidance and for supporting my research work.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Figure A1. Average survival rate of 12 different plants from 2021 to 2023.

Figure A2. Comparison of ecological restoration effect before and after. (a) Before ecological restoration; (b) after ecological restoration.

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Figure 1. Overview of the study area. (a) Geographical location of the study area; (b) topography of the study area.

Figure 2. Daily variation in meteorological factors in the study area.

Figure 3. Effects of different salt concentration treatments on the growth of halophytes. (a) Plant height. (b) Stem diameter. Different lowercase letters in the graphs indicate significant differences under different salt concentration treatments (p < 0.05). A total of 375 samples. Same as below.

Figure 4. Effect of different salt concentration treatments on the physiology of halophytes. (a) Contents of chlorophyll a and chlorophyll b. (b) Contents of total chlorophyll and malondialdehyde. The error bar above the graph represents the standard error. Different lowercase letters in the graphs indicate significant differences under different salt concentration treatments (p < 0.05).

Figure 5. Characteristics of daily changes in Pn of halophytes under different salt concentration treatments. (a) Ha. (b) Tc. (c) Pa. (d) Daily average of net photosynthetic rate. The error bar above the graph represents the standard error. The same below. Different lowercase letters in the graphs indicate significant differences under different salt concentration treatments (p < 0.05).

Figure 6. Characteristics of daily changes in Tr of halophytes under different salt concentration treatments. (a) Ha. (b) Tc. (c) Pa. (d) Daily average of transpiration rate. Different lowercase letters in the graphs indicate significant differences under different salt concentration treatments (p < 0.05).

Figure 7. Characteristics of daily changes in Gs of halophytes under different salt concentration treatments. (a) Ha. (b) Tc. (c) Pa. (d) Daily average of stomatal conductance. Different lowercase letters in the graphs indicate significant differences under different salt concentration treatments (p < 0.05).

Figure 8. Characteristics of daily changes in Ci of halophytes under different salt concentration treatments. (a) Ha. (b) Tc. (c) Pa. (d) Daily average of intercellular carbon dioxide concentration. Different lowercase letters in the graphs indicate significant differences under different salt concentration treatments (p < 0.05).

Figure 9. Characteristics of daily changes in Wue of halophytes under different salt concentration treatments. (a) Ha. (b) Tc. (c) Pa. (d) Daily average of water use efficiency. Different lowercase letters in the graphs indicate significant differences under different salt concentration treatments (p < 0.05).

Figure 10. Effect of different salt concentration treatments on biomass of halophytes. The error bar above the graph represents the standard error.

Figure 11. Relationship between different ecological factors and biomass of halophytes. (a) RDA ordination plot of ecological factors versus halophytes biomass; (b) degree of explanation of halophyte biomass by each ecological factor; “ACO2” is atmospheric carbon dioxide concentration. “Tr” is transpiration rate. “TChl” is total chlorophyll. “Wue” is water use efficiency. “Rh” is relative humidity. “Gs” is stomatal conductance. “Pn” is net photosynthetic rate. “Ta” is atmospheric temperature. “Cb” is chlorophyll b. “D” is stem diameter. “Ci” is intercellular carbon dioxide concentration. “Ca” is chlorophyll a. “MDA” is malondialdehyde. “H” is plant height. “Sc” is salt concentration. “TB” is total biomass. * represents p < 0.05.

Figure 12. Structural equation modeling of different ecological factors and biomass of halophytes. (a) Structural equation modeling of different ecological factors with Ha biomass; (b) structural equation modeling of different ecological factors with Tc biomass; (c) structural equation modeling of different ecological factors with Pa biomass; (d) direct and indirect effects of different ecological factors on Ha biomass; (e) direct and indirect effects of different ecological factors on Tc biomass; (f) direct and indirect effects of different ecological factors on Pa biomass; blue arrows in the figure represent positive correlations, and orange arrows represent negative correlations. A solid line indicates a significant effect, and a dashed line indicates a non-significant effect. The numbers next to the arrows are standardized path coefficients, which reflect the magnitude of the effect between the variables. The width of the arrows is proportional to the standardized path coefficient. * represents p < 0.05. ** represents p < 0.01. *** represents p < 0.001.

Table 1. Specific profile of soils in the study area.

Type	Organic Matter (g·kg⁻¹)	Total Nitrogen (g·kg⁻¹)	Total Phosphorus (g·kg⁻¹)	Total Potassium (g·kg⁻¹)	Available Nitrogen (mg·kg⁻¹)	Available Phosphorus (mg·kg⁻¹)	Available Potassium (mg·kg⁻¹)	Electrical Conductivity (ms·cm⁻¹)	pH	Salt Content (g·kg⁻¹)
Desert soil	1.17 ± 0.4	0.09 ± 0.03	0.30 ± 0.05	34.10 ± 7.7	31.10 ± 5.1	2.17 ± 0.6	61.30 ± 13.9	11.19 ± 4.4	7.78 ± 2.1	30.07 ± 6.3

Note: The data in the table are mean and standard deviation.

Table 2. Overview of different concentrations of salt solutions.

Salt Concentration (mmol·L⁻¹)	Water Soluble Salt (mg·L⁻¹)	Electrical Conductivity (ms·cm⁻¹)	pH	Cl⁻ (mg·L⁻¹)	${SO}_{4}^{2 -}$ (mg·L⁻¹)	Ca²⁺ (mg·L⁻¹)	K⁺ (mg·L⁻¹)	Mg²⁺ (mg·L⁻¹)	Na⁺ (mg·L⁻¹)	${H C O}_{3}^{-}$ (mg·L⁻¹)	${C O}_{3}^{2 -}$ (mg·L⁻¹)
0	—	0.1 ± 0.02	6.12 ± 0.5	—	12 ± 3.1	11 ± 2.6	0.7 ± 0.1	2 ± 1.5	—	17 ± 3.1	—
150	7064 ± 179	10 ± 1.5	7.63 ± 2.2	3079 ± 87	1005 ± 35	282 ± 19	9 ± 1.7	109 ± 11	1297 ± 77	41 ± 9	—
200	9773 ± 201	13 ± 1.0	7.86 ± 2.0	4251 ± 102	1338 ± 41	454 ± 16	11 ± 2.6	167 ± 16	2083 ± 64	68 ± 12	—
250	11,440 ± 65	15 ± 2.1	8.12 ± 2.5	4869 ± 96	1562 ± 89	535 ± 21	13 ± 1.2	235 ± 27	2900 ± 93	85 ± 11	—
300	13,323 ± 87	18 ± 1.9	8.57 ± 3.1	5903 ± 117	1754 ± 65	657 ± 12	18 ± 3.0	324 ± 18	4029 ± 126	106 ± 14	—

Note: “—” means that the ion content was not detected or the ion content was less than 0.03 mg·L⁻¹. The data in the table are means and standard deviations.

Table 3. Equations for fitting salt concentration treatments to halophyte biomasses.

Halophyte Species	Fitting Formula	R²	ANOVA Test
Haloxylon ammodendron	Y = −9.0108x + 62.415	0.663	p < 0.05
Tamarix chinensis	Y = −6.431x + 39.663	0.708	p < 0.05
Phragmites australis	Y = −3.5003x + 20.407	0.597	p < 0.05

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Zhang, X.; Lin, T.; Xu, H.; Gao, G.; Dou, H. Photosynthetic and Physiological Characteristics of Three Common Halophytes and Their Relationship with Biomass Under Salt Stress Conditions in Northwest China. Appl. Sci. 2024, 14, 11890. https://doi.org/10.3390/app142411890

AMA Style

Zhang X, Lin T, Xu H, Gao G, Dou H. Photosynthetic and Physiological Characteristics of Three Common Halophytes and Their Relationship with Biomass Under Salt Stress Conditions in Northwest China. Applied Sciences. 2024; 14(24):11890. https://doi.org/10.3390/app142411890

Chicago/Turabian Style

Zhang, Xi, Tao Lin, Hailiang Xu, Guaikui Gao, and Haitao Dou. 2024. "Photosynthetic and Physiological Characteristics of Three Common Halophytes and Their Relationship with Biomass Under Salt Stress Conditions in Northwest China" Applied Sciences 14, no. 24: 11890. https://doi.org/10.3390/app142411890

APA Style

Zhang, X., Lin, T., Xu, H., Gao, G., & Dou, H. (2024). Photosynthetic and Physiological Characteristics of Three Common Halophytes and Their Relationship with Biomass Under Salt Stress Conditions in Northwest China. Applied Sciences, 14(24), 11890. https://doi.org/10.3390/app142411890

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