Coordination in functional traits of Populus euphratica leaves under salt stress

Leaf functional traits allow plant survival and maintain their ecosystem function. Salinity affects leaf functional traits, but coordination among leaf functional traits is poorly known and may depend on salt severity. To increase our understanding of the coordination of leaf functional traits under salt stress, we determined hydraulic, gas exchange, and physiological and biochemical parameters in Populus euphratica Oliv. (P. euphratica) grown under salinity treatments, as well as gas exchange parameters under different CO₂ concentrations. We found that P. euphratica can reinforce its hydraulic capacity by increasing the water transfer efficiency of both its leaves and stems when a salinity threat occurs for a specific duration of stress. Its stems were more adaptable than leaves. The economic and hydraulic traits of P. euphratica leaves were consistent during the middle stages of salt stress, but inconsistent during the onset and late stages of salt stress. There was almost no biochemical limitation under severe salinity conditions, and CO₂ enrichment of P. euphratica had a greater effect on leaf economic traits. The mechanism of toxic ion exclusion based on water availability and intracellular mechanisms in leaves contributed to salt tolerance when P. euphratica was exposed to salinity stress. There was also a coordination mechanism for the plants during increasing salt stress. The leaf intracellular traits of P. euphratica can coordinate with the leaf economic and hydraulic traits and form a defense mechanism to reduce salt damage and guarantee growth under saline conditions. In conclusion, P. euphratica, the main constructional species of riparian forests, adapts to saline environments by adjustment and coordination of leaf functional traits, ensuring survival. These results provide a scientific basis for riparian forest restoration.

1. Introduction

The area of salinized soil accounts for 7.6% of the global land area, and China is one of the major keepers of salinized land, distributed in the arid northwestern part of the country. Salinity stress is an important environmental factor that interferes with plant productivity and growth, causing decreased growth, productivity, and even death (Shamsi et al., 2020; Yang et al., 2021). Salt stress develops as a result of salt accumulation to toxic concentrations through evapotranspiration in the soil surface layer, particularly in semi-arid and arid areas (Deinlein et al., 2014; Yu et al., 2020).

Downstream areas of river basins in the arid area of northwestern China are known as green corridors due to the lush cover of riparian forests that are several miles wide. Populus euphratica (P. euphratica) is one of the few tall tree species that form forests in semiarid areas and maintain ecosystem functions in vulnerable oases (Chen et al., 2012). P. euphratica is a tree species with an extremely strong adaption to growth under an adverse environment where it can persist for decades and centuries (Si et al., 2014). Increases in soil salinization could further inhibit tree growth and increase the risk of plant mortality; however, plants change their functional traits to adapt to the environment (Zhang C. et al., 2022).

Leaf functional traits are key to the understanding of tree internal coordination and adaptation mechanisms to the environment; thus, coordination of leaf functional traits plays a critical role in realizing the physiological, ecological, and survival strategies of plants (Derroire et al., 2018; Zhang C. et al., 2022). Recent studies on tree response processes in the environment highlight the importance of hydraulic functional integrity for tree survival and that hydraulic failure can lead to tree mortality across multiple tree taxa (Adams et al., 2017; Powers et al., 2020). Leaves are a vital hydraulic choke point in the hydraulic system of plants, in which hydraulic resistance accounts for approximately 30–80% of the whole-plant resistance (Liu et al., 2014; Pan et al., 2016; Li et al., 2019).

The hydraulic function of a leaf is very sensitive to soil water potential (Pan et al., 2016), resulting in changes with drought and salt stress. Therefore, leaf hydraulic traits are essential indices of water conduction in plants that reflect the water transfer efficiency and plant safety condition under various environmental stress conditions. In addition, the physiological cause of tree mortality is a fatal depletion of non-structural carbohydrates resulting from CO₂ fixation and carbon metabolism disorders, even carbon starvation (Anderegg et al., 2012). Moreover, the gas exchange level, a leaf economic trait, that reflects carbon investment and carbon allocation, can affect the construction of the hydraulic system (Petit et al., 2016; Dong and Jaume, 2018). It has been shown that organs with a short lifespan require lower economic investment and fewer resources, and thus, they could be easily rebuilt depending on the construction economics of plants (Pivovaroff et al., 2014). As stomata can link the water desorption and gas exchange processes, the leaf hydraulic and economic traits are associated at the leaf scale (Choat et al., 2018; Yin et al., 2018). There is a trade-off between the hydraulic and economic traits of trees at the leaf level, which affects plant survival and adaption to the environment (Liu et al., 2019; Yin et al., 2021). Therefore, leaf hydraulic and economic traits may exhibit coordination in adaption to saline environments.

A saline environment can have direct harmful effects on cell growth and intracellular traits; past research has shown that a physiological cause of tree mortality is lethal tissue dehydration with no shrinking ability (Anderegg et al., 2012). Osmotic adjustment is a common response to osmotic stress induced by high ion accumulation, which affects plant cell systolic traits involved in counteracting the loss of turgor by maintaining or increasing bulk intracellular compatible solutes (Per et al., 2017; Meena et al., 2019; Moukhtari et al., 2020). The contents of proline and soluble sugars, as vital intracellular compatible solutes in plants, are closely related to osmotic adjustment and the converse-succession-resistant capability of plants (Shamsi et al., 2020; Zelm et al., 2020; Afefe et al., 2021). In addition, the formation of reactive oxygen species (ROS) within plant cells caused by ion accumulation under salinity compromises cell contractility and disrupts the metabolic processes (Flowers and Colmer, 2015; Hussain et al., 2015; Ma et al., 2019). Plants can protect themselves from ROS-induced oxidative damage through enzymatic defense mechanisms, and the activation of antioxidant enzymes is critical for suppressing toxic ROS levels within cells (Hishida et al., 2014; You and Chan, 2015; AbdElgawad et al., 2016). Therefore, intracellular regulatory mechanisms including enzymatic defense and osmotic adjustment are important to the understanding of leaf intracellular traits.

Earlier studies showed that leaf hydraulic traits are under the influence of changes in cell shrinkage, including permeability of extravascular water pathways (Pou et al., 2013; Scoffoni et al., 2014). In addition, stomatal behavior affects not only gas exchange and water desorption but also osmotic regulation and ROS accumulation (Cao et al., 2014; Hartmann and Trumbore, 2016; Karst et al., 2017). Therefore, there appears to be a coordination of leaf hydraulic, economic, and intracellular traits for plant acclimatization to saline environments. Understanding the coordination of leaf functional traits in saline environments is essential for a holistic perception of plant resistance mechanisms to adverse conditions.

Differences in the physiological and biochemical responses of riparian plants to salt stress shed light on adaptive traits (Li et al., 2013, 2019; Si et al., 2014; Rajput et al., 2015; Pan et al., 2016) and help reveal the mechanisms of the converse-succession-resistant capability of P. euphratica. Some reports indicate that P. euphratica has the physiological ability to tolerate salinity stresses, but little is known about the physiological aspects and coordination among leaf functional traits to adapt to salt stress. The growth mechanisms of P. euphratica under such conditions are not fully explained because leaf functional traits have not been addressed in previous research studies. Nevertheless, P. euphratica survives saline conditions and forms forests, indicating that its leaf functional traits adapt to stressful environments. Therefore, a greater understanding of the adaptation and coordination of leaf functional traits in P. euphratica is essential for understanding salt stress adaptation. The goal of the present study is to elucidate the effects of salinity stress on the leaf hydraulic, economic, and intracellular traits and salt tolerance of P. euphratica. Specifically, we aimed to answer the following questions: (1) how do the leaf hydraulic traits of P. euphratica respond to changes in a salinity gradient and stress duration? (2) how do the leaf economic traits of P. euphratica respond to changes in a salinity gradient and stress duration? and (3) how do intracellular traits of P. euphratica respond to changes in a salinity gradient and stress duration?

2. Materials and methods

2.1. Study sites

The study was carried out in the Alxa Desert Eco-Hydrology Experimental Research Station in Ejina oasis in northwestern China (41°40′ N−42°40′ N, 100°15′ E−101°15′ E), which is a part of the Heihe River Basin and located downstream (Figure 1). In this area, 75% of precipitation occurs during June, July, and August, and the annual precipitation averages 38 mm. Evaporation is very strong at 3,390 mm annually, exceeding precipitation by more than 90 times. The area belongs to the extremely arid regions in China, with an annual average temperature of 8.2°C and high temperatures usually occurring from June to August (Si et al., 2014). Local groundwater is the main source of water for plants in this region and it is derived mostly from the discharge in the middle and upper streams of the Heihe River (Zhou et al., 2013). The soil in this region originates from fluvial sediments; the soil salinity is up to 33% (Si et al., 2014).

FIGURE 1

Figure 1. Location and elevation of the study area in the Heihe River Basin in the arid inland region of China.

2.2. Plant materials

P. euphratica saplings were cultivated on the local forest farm in Ejina Banner for 2 years before transplantation. A total of 100 P. euphratica saplings were transplanted into pots for this study and placed outdoors in the natural environment in early April. We selected healthy, straight, non-stressed, and well growing saplings as samples for salt treatments when saplings grew in pots for more than 3 months. Samples were assigned to one of several salt treatments, each with four replications. The salinity gradient included NaCl at concentrations of 100, 200, 300, and 400 mmol/L. Each salt concentration treatment was given for the following durations: CK (0 days salinity), 7 days (salinity period lasted for 7 days), 14 days (salinity period lasted for 14 days), and 21 days (salinity period lasted for 21 days). The volume of the solution was 3 L per pot, which was poured at one time into pots for all treatments; subsequently, all treated pots were watered every 7 days for the rest of the time. All saplings were measured at once after the salt treatments. The starting day of treatment was varied to ensure that the required salinity duration was met on the same day for each group to avoid growth-induced differences in different salt treatments.

2.3. Measurement of hydraulic conductance

A high-pressure flow meter (HPFM-GEN3, Dynamax Inc., Houston, TX, USA) was used for determining the original hydraulic conductance using the water perfusion method (Tyree et al., 1995). Briefly, HPFM pushes distilled water into certain parts of plants and determines a homologous flow rate. As a result, the original hydraulic conductance is obtained from the relationship between flow rate and imposed pressure. Measurements of the original hydraulic conductance in shoots were determined with imposed pressure of approximately 300–350 kPa until the rate of water flow was stable. The determinations took approximately 10 min, and the original values had to be corrected to the values at 25°C to make up for water viscosity variations during each measurement.

The original hydraulic conductance of roots and shoots was determined as above and the specific steps were as follows: First, the stalk was excised from the main root at 3–4 cm above the soil surface. The original hydraulic conductance was obtained by attaching the ends of whole roots/shoots to the instrument for testing. In vitro measurement was performed for the whole shoot system, while in situ measurement was performed for the whole root system. Then, new values were obtained by removing the leaves—the original hydraulic conductance of the stem and then the original hydraulic conductance of the leaves were determined from the hydraulic pressure analog based on Ohm’s law (Alsina et al., 2011). Finally, the water transfer efficiency of different plant parts was expressed using the leaf-specific hydraulic conductance values—the hydraulic conductance per leaf area (K, kg m^–2 s^–1 MPa^–1) was obtained from the corrected original hydraulic conductance that was adjusted for the leaf area. The hydraulic contribution of specific parts was reflected in the hydraulic resistance ratio through hydraulic segmentation, which was determined using the hydraulic resistance (the reciprocal of original hydraulic conductance) of specific parts relative to the whole plant, and expressed as a percentage. The formula for the relations among leaf-specific hydraulic conductance of different tissues is as follows:

${\mathrm{K}}_{\text{leaf}}={(K_{\text{twig}}{}^{-1}-K_{\text{stem}}{}^{-1})}^{-1},$

where K_leaf is the leaf-specific hydraulic conductance of leaves, K_twig is the leaf-specific hydraulic conductance of a fully-leaved twig, and K_stem is the leaf-specific hydraulic conductance of the bare stem.

2.4. Total leaf area

A total of 5–10 leaves per sapling from each group were placed on a grid paper and the edges were traced to obtain the leaf area. The total number of grids was counted in which the leaves occupied more than 50% of the grid; then, the area of a grid was multiplied by the number of square grids to obtain the leaf area. Subsequently, the leaves were washed and dried at 80°C and weighed to obtain biomass. The SLW (specific leaf weight) values of each sapling were calculated by dividing the leaf area by biomass. Fresh leaves were also stored in liquid nitrogen for measurements of physiological and biochemical parameters and their leaf area was measured as mentioned previously. The area of the remaining leaves was obtained from the dry weight divided by the SLW values, based on the assumption of the same SLW per sapling. The leaf area of the whole plant was obtained by adding the three parts of the leaf area calculated before.

2.5. Gas exchange

An LI-6400 portable photosynthesis system (LI-COR, Lincoln, NE, USA) was used to determine transpiration (E, mmolH₂O⋅m^–2⋅s^–1), net photosynthetic rate (P_N, μmolCO₂⋅m^–2⋅s^–1), and stomatal conductance (g_s, molH₂O⋅m^–2⋅s^–1). Water use efficiency (WUE, μmolCO₂⋅mmolH₂O^–1) was determined as the ratio of the net photosynthetic rate and the transpiration rate. Three or four fully expanded leaves from 3 to 4 branches on the top of each shoot system were used for the measurement. The LI-COR settings were 1,200 μmol m^–2 s^–1 for light intensity (with a 6400-02B red-blue LED Light Source) and 400 μmol mol^–1 and 600 μmol mol^–1 for CO₂ concentration (using 6400-01 CO₂ mixer). These measurements were conducted immediately after the salt treatments.

2.6. Physiological and biochemical parameters

Testing kits (Comin Biotechnology Co., Ltd., Suzhou, China) were used for measuring malondialdehyde content (MDA) and the activities of superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT). A 0.1 g sample was ground in liquid nitrogen before weighing using an analytical balance. Then, the sample was homogenized in phosphate buffer with a pH of 7.8. Then MDA, SOD, POD, and CAT analyses were conducted after the homogenate was centrifuged at 12,000 rpm at 4°C for 15 min. The resulting supernatant was used for the determination of SOD, POD, and CAT activity by thiobarbituric acid chronometry, nitroblue tetrazolium, and guaiacol staining methods, respectively. MDA content was determined using ammonium molybdate colorimetry. After grinding in liquid nitrogen, a 0.1 g sample was weighed and extracted with 5 ml of 3% sulfosalicylic acid. The homogenate was placed in a centrifuge tube and extracted by vibrating in a hot water bath for 10 min at 95°C. After the homogenate was centrifuged at 10,000 rpm at 25° for 10 min, the content of proline was determined by colorimetry with acid ninhydrin a cooled homogenate. Then, 0.1–0.2 g samples were weighed and then ground with a small amount of distilled water. The volume of the homogenates was filled to 10 ml with deionized water and heated in a hot water bath for 30 min at 95°C; the supernatant was obtained by centrifuging at 3,000 rpm. Then, the anthrone colorimetric method was used for soluble sugar content determination in the supernatant.

2.7. Data treatment and statistical analysis

Analysis of variance (ANOVA) was used to test for differences in hydraulic values, net photosynthetic rate, stomatal conductance, water use efficiency, SOD activity, POD activity, CAT activity, MDA content, proline content, and soluble sugar content among different salinity treatments. We used the least significant difference test (LSD) based on post-hoc means. Pearson Product Moment Correlation was used to test the statistical significance of the correlations. A probability value of p < 0.05 was used to indicate statistically significant differences. Data were presented as means with standard error and statistically analyzed using SPSS 19.0. The figures were plotted using Origin 8.0.

3. Results

3.1. Variability in hydraulic characteristics

At the same concentration, leaf-specific hydraulic conductance in twigs (K_twig) significantly increased with salinity duration from CK to 14 days for NaCl concentrations of 100, 200, and 300 mmol/L. The maximum values were 4.13 × 10^–3, 3.54 × 10^–3, and 3.33 × 10^–3 kg m^–2 s^–1 MPa^–1, respectively, at increasing concentrations. Subsequently, K_twig significantly decreased when salinity stress lasted for 21 days and was 3.03, 1.59, and 1.11 times the value of CK treatment (no salt), respectively. The K_twig value increased gradually to 1.36 × 10^–3 kg m^–2 s^–1 MPa^–1 with an increase in salinity duration from CK to 14 days, and then significantly decreased when the salt stress lasted for 21 days at a concentration of 400 mmol/L NaCl. Moreover, the K_twig value decreased with increasing NaCl concentrations for the same duration (Figure 2A).

FIGURE 2

Figure 2. Changes in the leaf-specific hydraulic conductance values of whole twig (A), leaf (B), and stem (C) under different salinity concentrations and durations of stress. Different lower-case letters denote significance levels based on analysis of variance (ANOVA) post-hoc means with least significant difference test (LSD) analysis (p < 0.05). Data are means with standard error.

The trend in leaves was the same as that in whole twigs. At the same concentration, leaf-specific hydraulic conductance in leaves (K_leaf) significantly increased from CK to 14 days and then decreased from 14 to 21 days for all NaCl concentrations. The values of K_leaf at 21 days were 2.43, 1.99, 1.67, and 1.18 times the value of CK treatment, respectively, for increasing concentrations. This trend of changes showed that leaves enhanced water transfer efficiency under salt stress. The K_leaf values decreased gradually with the increase in NaCl concentration for the same duration. The results exhibited that the water transfer efficiency of leaves was significantly reduced by salinity stress for the same duration (Figure 2B).

The maximum values of leaf-specific hydraulic conductance in stems (K_stem) were 9.31 × 10^–3, 9.68 × 10^–3, 9.29 × 10^–3, and 3.56 × 10^–3 kg m^–2 s^–1 MPa^–1 at the salinity duration of 14 days, respectively, at increasing concentrations. At the same salinity duration, the values of K_stem increased initially and then decreased with the increase in NaCl concentrations, differing from those of K_twig and K_leaf. Moreover, the maximum values of K_stem were higher at all other concentrations but sharply reduced for the concentration of 400 mmol/L NaCl. This indicated that stems were more adaptable than leaves under mild and moderate salt stress conditions (Figure 2C). This illustrated that both the leaves and stems of P. euphratica could enhance the water transfer efficiency upon increased durations of salt stress.

The leaf hydraulic resistance was 64% relative to that of the whole twig in the CK treatment. The values of leaf hydraulic resistance relative to that of the whole twig decreased from 71.4 to 64.5% after the 7 days treatment with increasing NaCl concentrations. The leaf hydraulic resistance ratio declined from 70.6 to 56.2% after the 14 days treatment with increasing NaCl concentrations. There was a significant decline in the leaf hydraulic resistance ratio from 67.5 to 39.4% after the 21 days treatment with increasing NaCl concentrations. This indicated that the hydraulic contribution of leaves in twigs was significantly enhanced by salinity stress over the same duration. The hydraulic resistance in leaves accounted for 39.4% of the whole twigs in the treatment for 21 days with 400 mmol/L NaCl, which was lower than that of bare stems for the first time (Figure 3). This showed that the hydraulic contribution of leaves in twigs was more than half.

FIGURE 3

Figure 3. Changes in the leaf hydraulic resistance ratio under different salinity concentrations. Different lower-case letters denote significance levels based on ANOVA post-hoc means with LSD analysis (p < 0.05). Data are means with standard error.

At the same concentration, the leaf hydraulic resistance ratio first increased and then decreased with an increase in salinity duration for all NaCl concentrations. The leaf hydraulic resistance ratio values obtained at 21 days were not statistically significantly different from those obtained after the CK treatment for the 100 and 200 mmol/L NaCl concentrations, but were 13.6 and 38.4% lower for the concentrations 300 and 400 mmol/L NaCl (Figure 3). The decrease in the proportion of hydraulic resistance represents the increase in hydraulic transport contribution. This indicated that the hydraulic contributions of leaves in whole twigs first enhanced and then decreased depending on salinity duration for the same NaCl concentrations. The more severe the stress is, the greater the impact is.

3.2. Variability in gas-exchange characteristics

At the same concentrations, there was a sharp decline in the net photosynthetic rate (P_N) between CK and 7 days of treatment, ranging from 50.8 to 8.6% of the value in CK, with increasing concentrations. This indicated that the higher the initial salt concentration, the greater the P_N decreased in the short term. Subsequently, the value of P_N significantly increased, indicating an adaptation to salt stress. Meanwhile, the more severe the salinity stress, the smaller the values of P_N for the same duration (Figure 4A).

FIGURE 4

Figure 4. Changes in the net photosynthetic rate (A), stomatal conductance (B), and water use efficiency (C) under different salinity concentrations. Lowercase letters over the bars denote significance levels based on ANOVA post-hoc means using LSD analysis (p < 0.05).

At the same concentration, the trend in stomatal conductance (g_s) was the same as that in P_N but g_s decreased by day 7 of the treatment; the decreasing amplitude range was from 67.7 to 92.2% of the value in CK with increasing concentrations, which was higher than that of P_N. This indicated that the initial salt stress effect on g_s was even greater than that on P_N in the short term. Then g_s increased between 7 and 21 days, and this indicated that both g_s and P_N could be enhanced after a short-term adaptation for certain levels of salt stress. Meanwhile, the more severe the salinity stress, the smaller the values of g_s at the same duration. At day 21, the g_s values were significantly higher than those at CK for 100 mmol/L NaCl treatment. There was no significant difference between these values and those at CK for 200 and 300 mmol/L NaCl treatment. The g_s values were significantly lower than those at CK for 400 mmol/L NaCl treatment (Figure 4B). This indicated that the longer the stress duration, the slower the recovery of g_s with increasing salinity.

Although there was a sharp decline in both the P_N and g_s values at CK and at day 7, there was no significant difference in the water use efficiency (WUE) between day 7 of the treatment and at CK. The WUE trend was the same as that for stomatal conductance for 100 and 200 mmol/L NaCl treatments, which had the maximum value after 21 days. The WUE first increased at days 7 and 14 and then decreased for 300 and 400 mmol/L NaCl treatments. This was not significantly different from that in the CK group after 21 days (Figure 4C). This indicated that P. euphratica could maintain the efficient usage of water under salt stress for a long time.

All values of P_N increased when the CO₂ concentrations increased from 400 to 600 μmol mol^–1, which indicated that CO₂ provision could enhance photosynthesis in P. euphratica under salt stress. The values of P_N at days 7, 14, and 21 of the treatment increased by 37.9, 59.7, and 49.0%, respectively, with 100 mmol/L NaCl treatment (Figure 5A). They increased by 39.1, 43.1, and 33.1%, respectively, with 200 mmol/L NaCl treatment (Figure 5B) and by 75.5, 46.8, and 66.4%, respectively, with 300 mmol/L NaCl treatment (Figure 5C). The values increased by 97.5, 93.9, and 101.3%, respectively, with 400 mmol/L NaCl treatment (Figure 5D). This illustrated that the more severe the salt stress, the greater the enhancement effect of increased CO₂ on photosynthesis for the same salinity duration.

FIGURE 5

Figure 5. Changes in the net photosynthetic rate at 100 mmol/L NaCl (A), 200 mmol/L NaCl (B), 300 mmol/L NaCl (C), and 400 mmol/L NaCl (D) with the same CO₂ concentration. Lowercase letters denote significance levels based on ANOVA post-hoc means using LSD analysis (p < 0.05). Data are means with standard error.

3.3. Variability in physiological and biochemical substances

The SOD activity was 156.5 U⋅g^–1 at CK which increased with the durations of salt stress for all NaCl concentrations. Meanwhile, changes in salt stress during the early stages of salt stress were very slow with the durations of stress being relatively mild but rose rapidly under relatively severe salt stress. In addition, the SOD activity increased with increasing NaCl concentrations over the same salinity duration (Figure 6A).

FIGURE 6

Figure 6. Changes in the superoxide dismutase (SOD) (A), peroxidase (POD) (B), and catalase (CAT) (C) under different salinity concentrations. Lowercase letters denote significance levels based on ANOVA post-hoc means using LSD analysis (p < 0.05). Data are means with standard error.

The POD activity was 354.37 U⋅g^–1 at CK and it increased between CK and 14 days after the treatment and then decreased for all NaCl concentrations. The values ranged from 1.9 to 3.7 times the value during CK treatment and on day 21, respectively, with increasing concentrations. The POD activity enhanced with increasing NaCl concentrations over the same salinity duration (Figure 6B).

The CAT activity significantly increased from 77.42 nmol⋅min^–1⋅g^–1 at CK to a maximum value at day 21 under the same salt stress duration for all NaCl concentrations. The CAT activity enhanced with increasing NaCl concentrations over the same salinity duration (Figure 6C). This indicated that SOD, POD, and CAT in the leaves of P. euphratica could provide strengthened defensive protection under salt stress conditions.

There were no significant differences in proline content over different salinity durations for 100 and 200 mmol/L NaCl treatment. The proline content increased gradually between CK and at day 21 from 29.85 to 35.62 μg⋅g^–1 for 300 mmol/L NaCl treatment and significantly from 29.85 to 45.89 μg⋅g^–1 for 400 mmol/L NaCl treatment. In addition, the proline content accumulated with increasing NaCl concentrations over the same salinity duration (Figure 7A).

FIGURE 7

Figure 7. Changes in proline (A) and soluble sugar (B) with different salinity concentrations. Lowercase letters denote significance levels based on ANOVA post-hoc means using LSD analysis (p < 0.05). Data are means with standard error.

The soluble sugar content was 18.85 mg⋅g^–1in CK, and it increased between CK and 21 days treatment at all NaCl concentrations. Meanwhile, changes in salt stress were very rapid and relatively mild with stress duration in the early stage but rose slowly under relatively severe salt stress. In addition, the soluble sugar content increased upon 100 to 200 mmol/L NaCl treatment and then decreased upon 200 to 400 mmol/L NaCl treatment under the same salinity duration (Figure 7B).

The MDA content was 37.64 nmol⋅g^–1 in CK and it significantly declined between CK and day 7 and then increased on day 21 upon 100 and 200 mmol/L NaCl treatments. The values significantly declined between CK and day 14 and then increased at day 21 upon 300 mmol/L NaCl treatment. The values gradually decreased until day 21 upon 400 mmol/L NaCl treatment and the minimum values were at day 21. The time node at which the minimum values occurred at different salt concentrations indicated that the lighter the salt stress, the faster the recovery of the MDA content. The minimum values of MDA content were approximately 88 to 81% of the value in CK treatment for 100 to 400 mmol/L NaCl treatment, respectively, (Figure 8). This demonstrated that the MDA content could be maintained at a low level under salt stress, reflecting relatively light stress-induced damage to cell membranes.

FIGURE 8

Figure 8. Changes in malondialdehyde (MDA) content under different salinity concentrations. Different lower-case letters denote the significance levels based on ANOVA post-hoc means with LSD analysis (p < 0.05). Data are means with standard error.

4. Discussion

4.1. Leaf hydraulic traits under salinity stress

The hydraulic capacities of both leaves and bare stems were higher than those of whole twigs as water in whole twigs needs to travel longer water channels. When the salt concentration did not exceed 400 mmol/L, the hydraulic conductance of both leaves and stems was enhanced with the duration of stress not exceeding 14 days. It showed that P. euphratica can reinforce its hydraulic capacity by increasing its water transfer efficiency when a salinity threat occurs for a specific duration. Meanwhile, the greater the salt concentration, the lower the increase in the hydraulic capacity of leaves over the same duration of stress. Our results also suggested that increasing salt concentrations attenuated the degree of enhanced water transport performance than prolonged stress durations for leaf hydraulic traits. Moreover, the salt concentration of 100 mmol/L made a great positive impact on the hydraulic capacity of leaves. In contrast, the salt concentrations of 200 and 300 mmol/L positively affected the hydraulic capacities of stems more than the 100 mmol/L concentration over the same duration of stress. These results indicated that stems in P. euphratica were more adaptable than leaves under mild and moderate salt stress, and the self-adaptive and regulatory capacity of water transfer was weakened under severe salt stress with a salt concentration of 400 mmol/L.

The construction costs in plants could be reflected in the values of hydraulic resistance, and it has been shown that organs with a short lifespan require lower economic investment owing to the stronger hydraulic resistance (Pivovaroff et al., 2014). Leaves with higher hydraulic resistance required higher construction costs than stems, and the leaf hydraulic resistance increased for all salt concentrations over a shorter duration, thus reflecting the decreased firmness of leaves. Zeng et al. (2009) showed that a salt elimination mechanism in P. euphratica operated by allocating large amounts of toxic salt ions into leaves that are ultimately abscised. There was also a significant decline ranging from 67.5 to 39.4% in leaf hydraulic resistance relative to that of whole twig under severe salinity stress over a longer duration, which was caused by the enhanced hydraulic resistance of the whole twig. These results also reflected weakened effectiveness of overall hydraulic capacity and decreased water availability ultimately. Our study revealed that the toxic ion exclusion mechanism in leaves was a contributing factor in salt tolerance based on water availability when P. euphratica was exposed to salinity stress.

4.2. Leaf economic traits under salinity stress

Water use efficiency could reflect the amount of dry matter produced by plants per unit of water consumed, which was adversely affected by other physiological and biochemical processes, but not photosynthesis, during the onset of salt stress (Minh et al., 2016). Enhanced water use efficiency occurs in some tree species, while some plants exhibit low water use efficiency under salinity conditions (Li et al., 2022; Zhang Y. et al., 2022). In general, a reduction in photosynthesis is a response to an initial osmotic shock, caused by some degree of salt stress, resulting from stomata closure (Li et al., 2013). Although the photosynthetic rate decreased sharply in the early stage of salt stress, P. euphratica tried to alleviate salinity stress by decreasing its stomatal conductance and increasing WUE; this indicated that changes in stomatal performance had a greater effect on water loss and WUE than photosynthesis, in agreement with past research (Rajput et al., 2015). It has been pointed out that when plants are grown in a saline environment, improved WUE is favorable to the survival and development of the species (Rajput et al., 2015). The results showed that P. euphratica can reinforce its water use efficiency accompanied by an increase in water transfer efficiency when a salinity threat occurs at a specific duration of stress. Water use efficiency began to decline with stress duration at relatively high salinity gradients, and comprehensive physiological and biochemical processes could ameliorate the negative effects of salinity through decreased water use efficiency even in a long term.

A large number of studies have shown that stomatal conductance decreases due to stomatal closure, which restrains the availability of CO₂ and fixation of carbon in the leaves with an increase in salt concentration (Liu et al., 2014; Duan et al., 2018; Lawson and Matthews, 2020). Stomatal conductance was lower under saline conditions than in CK except for 100 mmol/L, which affected CO₂ diffusion in leaves pre-dominantly triggered by salt stress (Liu and Suarez, 2021). Past findings in woody plants also indicated that increasing CO₂ concentration in leaves and active sites of Rubisco ultimately enhanced light-saturated photosynthetic rates up to 2.8 times (Duan et al., 2015). Elevated CO₂ compensated for the reduction in CO₂ supply caused by stomatal limitation on leaf photosynthesis and improved leaf photosynthetic performance (Pérez-López et al., 2012; Eller et al., 2014). Our research showed that elevated CO₂ could improve photosynthesis, providing evidence that the main limitation was a reduction of CO₂ diffusion into leaves due to the stomatal effect rather than a biochemical limitation of CO₂ assimilation, even under the high salinity concentration of 400 mmol/L. As a result, CO₂ enrichment of P. euphratica had a greater effect on photosynthesis and leaf economic traits by CO₂ assimilation and carbon fixation.

The significantly lower stomatal conductance exhibited a higher stomatal limitation upon sudden increases in salt stress at day 7 when leaf photosynthesis was eliminated by at least half. This indicated that it would take more than 7 days to recover leaf photosynthesis although no biochemical limitation to photosynthesis was observed under the circumstances. Salt-stressed leaves required higher ambient concentrations of CO₂ to exhibit the same or higher photosynthesis than exhibited by leaves without salt stress at a maximum CO₂ assimilation rate; elevated CO₂ may render different results in different species under salt stress (Xu et al., 2016; Liu and Suarez, 2021). A 50% increase in carbon dioxide had a significant effect on photosynthesis in this study. In summary, the effects of salt stress on photosynthesis were eliminated by supplementing CO₂ to leaves; this was due to alleviating the diffusion resistance for CO₂ through reopened stomata or higher concentration gradient of atmospheric CO₂ for P. euphratica with improved salt tolerance. Moreover, CO₂ enrichment in P. euphratica under lower salt stress showed a relatively weak response but the effect was greater in plants in severe salinity conditions.

4.3. Coordination of hydraulic traits and economic traits under salinity stress

An intact water supply through the xylem pathway is a necessity for plant growth and survival to supplement water lost from stomata by transpiration (Sack and Scoffoni, 2013). The existing evidence shows that stomata performance is highly correlated with hydraulic systems, controlling the water supply capacity of plants (Zhang et al., 2013). Stomatal conductance, which is one of the major regulators of water flow in plants in the short term, could be impacted by enhanced water transfer efficiency (Liu et al., 2014; Pan et al., 2016). A lower leaf hydraulic capacity was found concomitantly with declining stomatal conductance in grasses and crops exposed to water stress (Corso et al., 2020). In this study, there was a significant decline in stomatal conductance at day 7 of stress but with increasing hydraulic capacity of leaves, the improved stomatal conductance of P. euphratica under mild and moderate salt stress was likely due to the water transfer efficiency in stems and sufficient water in leaves. Our study also showed a notable reduction in photosynthesis at day 7 under all salinity concentrations, with a rebound with longer periods of salinity. It has been previously reported that a decline in photosynthesis was an early response to salinity in P. euphratica seedlings, resulting from a decrease in osmotic potential and availability of water and nutrients due to the presence of salts in the soil (Li et al., 2013). Enhanced photosynthesis after a period of adaptation to salinity stress may be one of the adaptation strategies of P. euphratica. A rebound in photosynthesis reflected leaf economic traits that consisted of higher water transfer efficiency for leaf hydraulic traits. These results illustrated that the leaf economic traits in P. euphratica were consistent with the leaf hydraulic traits at the middle stages of salt stress.

There was an increase in stomatal conductance at day 21 of stress but with a decline in the hydraulic capacity of leaves. This suggested an inconsistent relationship between the hydraulic traits and economic traits of the leaf, which was consistent with earlier findings in subtropical and tropical forests in China (Li et al., 2015; Blackman et al., 2016). Li et al. (2015) observed that the hydraulic and economic traits of leaves were two functional subsystems involved in different mesophyll tissues located in different regions; leaf hydraulic and economic traits were related to spongy and palisade tissues, respectively, (Yin et al., 2018). Regulation of functional subsystems may not be synchronized, and the most likely causes of the differences were different conditions, in particular, water availability. The existing evidence showed that leaf stomatal regulation appeared more connected with water potential in stems and the xylem hydraulic system than in leaves (Quero et al., 2011; Zhang et al., 2013). These results showed consistency between leaf economic traits and leaf hydraulic traits in P. euphratica was a non-entity at late stages of salt stress.

4.4. Leaf intracellular traits under salinity stress

Salt stress exposed the chloroplasts to excessive excitation energy, which could result in an increase in the production of ROS and oxidative-induced stress (Ray et al., 2012). The generation of ROS is highly harmful to the integrity of a cell, and destruction by reactive oxygen species with increasing duration of salt stress (Ray et al., 2012; AbdElgawad et al., 2016). To dissipate these harmful molecules, peroxidase enzymes commence protecting trees against oxidative-induced stress, indicating increased production of ROS (Demidchik, 2015; Rajput et al., 2015). Foliar antioxidant enzyme activities were crucial in scavenging ROS and maintaining self-tolerance in coping with stress environments (Li et al., 2016a,b; Yu et al., 2020). In our study, the activity of SOD was stable at lower salinity treatment at a relatively shorter duration and then was highly enhanced. The activities of POD and CAT in P. euphratica leaves were enhanced with salinity stress, which illustrated that the enzymes POD and CAT played dominant roles in protection at lower salt stress. Higher activity of SOD, POD, and CAT observed in higher salinity-treated plants indicated that P. euphratica had a higher capacity for scavenging ROS, indicating that this may be a defensive mechanism to weaken oxidative damage induced by severe salt stress; this is consistent with previous studies (Rajput et al., 2015).

Proline and total soluble sugar accumulation may offer leaves an osmotic adjustment, which is a common response in some herbaceous and woody plant species to osmotic stress induced by high ion accumulation in soils (Shamsi et al., 2020; Afefe et al., 2021). Accumulating organic compounds, such as sugars and amino acids in the cytoplasm, eventually lead to the restoration of cellular homeostasis, detoxification, and therefore survival under stress (Parihar et al., 2015). The magnitude of change in proline content in different species under salt stress may differ; thus, proline rapidly accumulated in mangrove and Australian wild rice under salt stress (Afefe et al., 2021; Nguyen et al., 2021), but it decreased in both pearl millet and wheat (Yadav et al., 2020). In this study, proline content was stable at lower salinity levels for a relatively short period but significantly accumulated with a higher salinity treatment. Proline content was low in roots of P. euphratica grown under NaCl stress but high in leaves of in vitro shoots (Watanabe et al., 2000); this was probably because the integrity of the plant can be properly regulated by osmotic adjustment through a low level of proline accumulation. Soluble sugars may act as a form of storage and be supplied to achieve plant survival under salinity stress conditions (Choat et al., 2018; Yu et al., 2020), such as in osmoregulation and xylem restoration (Secchi and Zwieniecki, 2011; Martínez-Vilalta et al., 2016). Previous studies have demonstrated that soluble sugars contribute to maintaining the water potential gradient between soil and plant during osmotic stress by osmotic adjustment (Baerdemaeker et al., 2017). Soluble sugars in this study were basically stable with higher salinity treatment at a relatively short duration but significantly accumulated with lower salinity treatment. The accumulation of proline and total soluble sugar in leaves may be connected with osmotic mechanisms and saline stress tolerance, consistent with the conclusions of previous studies. In addition, the accumulation of sugars in P. euphratica may contribute to osmotic adjustment more than the accumulation of proline (Watanabe et al., 2000; Moukhtari et al., 2020).

Malondialdehyde content could reflect the final level of cell membrane disruption, the generation of MDA will be lower, indicating a lower level of cell membrane disruption (Shamsi et al., 2020; Bezerra-Neto et al., 2022). Lower values of MDA caused by a combination of enzymatic defense and osmotic adjustment in P. euphratica remained stable to avoid membrane damage in salt stress. This showed that low MDA levels may significantly affect plant adaption to saline environments, as proposed by several researchers for some species with salt-tolerant mechanisms (Sergio et al., 2012). Intracellular regulatory mechanisms including enzymatic defense and osmotic adjustment in leaves were contributing factors in salt tolerance when P. euphratica was exposed to salinity stress. This illustrated that there was a coordination mechanism for plants during increasing salt stress, leaf intracellular traits in P. euphratica can coordinate with leaf hydraulic and with leaf economic traits, reduce salt damage, and guarantee the survival and growth of P. euphratica under salinity conditions.

5. Conclusion

Adaptation and coordination of leaf functional properties in P. euphratica under salt stress were determined with hydraulic parameters, gas exchange parameters, and physiological and biochemical factors. The range of deleterious effects of salt stress on plant leaf functional traits depends on salinity levels. Functional properties of the leaf, which link the external environment and plants, have a significant effect on the improvement of plant performance in changing environments. Changes in leaf functional traits reflect the resistance and fitness of riparian plants under different salt stress conditions in arid areas. We found that the leaf economic traits in P. euphratica were consistent with the leaf hydraulic traits at a medium level of salt stress, with inconsistent relationships during the onset and late stages of salt stress. There was almost no biochemical limitation under severe salinity conditions and the CO₂ enrichment of P. euphratica had a greater effect on leaf economic traits. Toxic ion exclusion based on water availability and the intracellular mechanisms in leaves were contributing factors in salt tolerance when P. euphratica was exposed to salinity. Leaf intracellular traits can coordinate with leaf economic traits and leaf hydraulic traits, then form a defense mechanism to reduce salt damage and guarantee the growth of P. euphratica under saline conditions.

Plants can mitigate stress damage and sustain their existence through protective mechanisms. Plants could acclimatize to abiotic conditions with an adjustment in adaptive functional traits as further evidence of survival for P. euphratica in the extreme zone. In conclusion, riparian forests of P. euphratica exhibit a survival strategy to adapt to the saline environment by adjusting and coordinating leaf functional traits. Changes in the functional properties of the leaf in riparian plants under different salt stress environments also offer a scientific basis for riparian plant restoration and protection of riparian forests. Future studies should address the functional traits of P. euphratica grown in the wild combined with the local specific hydrological environment to improve the understanding of the internal acclimation mechanism under salt conditions.

Data availability statement

The original contributions presented in this study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.

Author contributions

DL and JS collected the experimental data, analyzed it, and wrote the manuscript. XR and JL participated equally in conceptualization, data analysis, and manuscript preparation and review. All authors contributed to the article and approved the submitted version.

Funding

This research was funded by the Science and Technology Innovation Project of Colleges and Universities in Shanxi Province (No. 2022L414), the Inner Mongolia Special Fund Project for the Transformation of Scientific and Technological Achievements (No. 2021CG0046), and the Open Fund Project of Xinjiang Production and Construction Corps Key Laboratory of Tarim Basin Biological Resources Protection and Utilization (No. BRZD2202).

Acknowledgments

We thank the support received from the forest farm of Ejina Banner in the Alashan League. We also record our sincere appreciation for the helpful and constructive comments made by the reviewers of the draft manuscript.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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