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Article

Correlation between Non-Structural Carbohydrates and C:N:P Stoichiometric Ratio of Haloxylon ammodendron under Different Water–Salt Gradients

by
Fang Yang
1,2,3,
Guanghui Lv
1,2,3,* and
Yadong Qie
4
1
School of Ecology and Environment, Xinjiang University, Urumqi 830017, China
2
Key Laboratory of Oasis Ecology, Ministry of Education, Urumqi 830017, China
3
Xinjiang Jinghe Observation and Research Station of Temperate Desert Ecosystem, Ministry of Education, Jinghe 833300, China
4
Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning 530004, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(6), 1185; https://doi.org/10.3390/f14061185
Submission received: 30 March 2023 / Revised: 14 May 2023 / Accepted: 6 June 2023 / Published: 8 June 2023
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

:
Growth is restricted by both water and phosphorus (P), and balancing the relationship between non−structural carbohydrates (NSCs) and carbon: nitrogen: phosphorus (C:N:P) is essential for Haloxylon ammodendron to adapt to arid habitats. The survival and growth strategies of the dominant species H. ammodendron in a desert ecosystem were examined in order to better serve the restoration of degraded ecosystems and desertification control. Three water and salt gradients (high water and high salinity, medium water and salinity, and low water and low salinity) in the Aibi Lake Reserve were selected. We analyzed the accumulation and distribution of NSCs in the assimilation branches and secondary branches of H. ammodendron and the changes in the measurement ratio characteristics of C:N:P, as well as the soil organic carbon (SOC), total nitrogen (TN), and total phosphorus (TP) content. The results showed that: (1) With the decrease of soil water and salt content, the basal diameter, plant height, crown area, and NSC content of H. ammodendron significantly decreased. This morphological adjustment in the aboveground part is similar to a “self thinning” behavior, aimed at reducing transpiration area and balancing carbon distribution in the body. The carbon accumulation in the body helps the H. ammodendron to resist the dual stresses of drought and salt. (2) With the decrease of water and salt content, the C content of assimilating branches increased significantly, while there was no significant change in secondary branches. However, the N and P content of both branches decreased significantly, and the N: P of both branches was greater than 16, indicating that it was mainly limited by P. (3) The NSC of the two branches was significantly negatively correlated with C, and significantly positively correlated with N and P, and there was a strong positive correlation between the assimilation branches NSC: C: P and NSC: C: P. The synthesis and accumulation of NSC of H. ammodendron were influenced by the content and relationship of C, N, and P, and the abundance of P content transported by the root system to the aboveground portion may have an important and decisive role in regulating nutrient balance and non-structural carbon dynamics.

1. Introduction

As global drought intensifies, plants in desert ecosystems are living on the edge of water limitation [1]. Carbohydrates (CHO) are the energy currency for plant growth and metabolism [2], and the storage and distribution of CHO during plant growth and survival has become a research focus [3]. In recent years, increasing evidence has suggested that carbohydrates are also signal molecules. They can communicate with hormones, nitrogen, and other signals, participate in regulating a series of metabolic activities of plants, and form a complex signal network to regulate plant stress response, growth, and development [4]. CHO is generally divided into structural carbohydrates (SC) and non−structural carbohydrates (NSCs). SC includes lignin and cellulose, the main substances for plant morphology, while NSC is an energy indicator that characterizes the carbon budget in plants. It is mainly composed of soluble sugar (SS) [5] that has the function of maintaining cell osmotic pressure and resisting adversity and starch (ST) composition via a storage effect [6]. Different degrees of drought or salt stress can affect the dynamics of NSCs [7,8]. It is speculated that severe drought stress may not cause NSC consumption as in mild or moderate drought stress, as trees may die from irreversible xylem cavitation [9]. Therefore, it is necessary to explore how drought or salt stress intensity affects NSC dynamics.
Nutrient absorption is another important survival mechanism by which desert plants adapt to water deficit and nutrient−restricted environments. Nitrogen (N) and phosphorus (P) are essential nutrients for plant metabolism, growth, and reproduction in terrestrial ecosystems [10]. For example, plant N is closely related to photosynthesis, primary productivity, and litter decomposition [11]. P is an important component of plant genetic material, cell structure, and energy storage [12,13]. Basically, carbon (C):N and C:P ratios can represent the ability of plants to assimilate C while absorbing N and P. The N:P ratio can reflect the dynamic balance between soil nutrients and plant nutrient requirements [14]. Plant C:N:P stoichiometry reflects the ability of plants to adapt to local growth conditions [13]. Studies have shown that drought stress can cause changes in the distribution of C, N, and P elements in plant organs [15]. As the soil salinity increases, the plant’s N concentration and N:P ratio increase, while the P concentration decreases [16,17]. However, few studies have been reported on the C:N:P chemometrics in assimilation and secondary branches, especially under the interaction of water and salt. Therefore, it is important to understand the changes in the plant C:N:P ratio under varied water–salt gradients in typical ecosystems.
Drought and soil salinity can create physiological constraints in plants, including osmotic and oxidative stress, photosynthesis disturbance, nutrient metabolism disorder, and nutrient imbalance, which in turn affect plant growth and nutrient content [18,19,20]. These restrictions will change the stoichiometry of plants [17,20]. Studies have shown that leaf N content is positively correlated with the fixation capacity of NSCs, and P is a key element that affects plant metabolism [21,22]. Under shaded conditions, there is a trade-off between leaf NSCs and leaf C, and the interaction between leaf NSCs and leaf N and P contents will affect the growth rate and survival strategy of a species [6]. Therefore, exploring the changes in the C:N:P ratio and NSCs of desert plants under different water–salt gradients and the correlation between the two will help us to understand the survival strategies of desert plants for coping with climate change.
At present, the problems of global climate change and the intensification of human activities are becoming increasingly serious. Factors such as rising temperatures, changes in precipitation, and increasing extreme weather events are changing the structure, function, and services of global terrestrial ecosystems [23]. Due to its ecological fragility and sensitivity, the desert plant community has a particularly dramatic and significant response to global environmental changes. Haloxylon ammodendron is a small xerophytic tree widely distributed in the deserts of Asia and Africa [24]. It is the main constructive species of desert vegetation. It can not only tolerate drought, barrenness, and extreme temperature, but also has strong salt tolerance. Among the biological components of the desert ecosystem, it is often the plant species with the largest number of individuals, greatest biomass, and highest primary production. The goal of this study is to deepen our understanding of the survival and growth strategies of the dominant species H. ammodendron in desert ecosystems by analyzing the characteristics of the C:N:P ratio and NSC accumulation and distribution under different water–salt gradients. The results will be relevant to the restoration of degraded ecosystems and desertification control.

2. Materials and Methods

2.1. Overview of the Study Area

The test site was located to the north of the East Bridge Management and Protection Station of the Aibihu Wetland National Nature Reserve in Jinghe County, Xinjiang, China (44°30′–45°09′ N, 82°36′–83°50′ E), covering an area of approximately 267,000 hm2. The area is far from the sea and is affected by the strong winds of Alashankou. The area has a temperate continental arid climate, with dry, strong winds, frequent salt and dust storms, and floating dust activity. The annual average temperature is 7.8 °C; the extreme minimum temperature is −36.4 °C; and the extreme maximum temperature is 41.3 °C. The average annual precipitation is 105.17 mm; the average annual evaporation is 1662 mm; and the maximum wind speed is 55.0 m·s−1. The complex topography and harsh climatic conditions have created a unique desert–wetland–Gobi compound landscape in the basin [25]. The typical zonal soil types in the area include gray desert soil, gray brown desert soil, and aeolian sandy soil. The hidden soil types are saline (salinized) soil, meadow soil, and swamp soil. The diverse habitat types in the study area support relatively rich desert plant community types, and the representative plant types include xerophytes, sand plants, halophytes, wet plants, aquatic plants, and ephemeral plants. The main plant species are Populus euphratica, Haloxylon ammodendron, and Calligonum ebi-nuricum [26].

2.2. Experimental Design

In 2017, a 30 m × 3630 m standard sample zone (the southernmost end of the sample zone was about 500 m away from the bank of the Aqikesu River) established in 2016 was investigated and selected for markers of H. ammodendron plants (Figure 1). In this sample zone, a 30 m × 30 m standard sample square was selected every 90 m for a total of 31 sample squares (Figure 1). Two mature and healthy individuals of H. ammodendron were selected in each sample square and marked as test plants. If the growth of H. ammodendron in the sample square was poor or nonexistent, we selected the closest H. ammodendron plant outside the sample square in the horizontal direction. There were 62 H. ammodendron plants in total.

2.3. Sample Collection and Laboratory Measurement

2.3.1. Determination of Soil Moisture Content (SWC), Soil Salt Content (SSC), Soil pH, Soil Organic Carbon (SOC), Soil Total Nitrogen (TN), and Soil Total Phosphorus (TP) under the Canopy

SWC, SSC, and pH of soil samples were measured by the drying method, the conductivity method, and the potentiometric method, respectively. The SOC, TN, and TP of soil samples were determined by the potassium dichromate dilution heat method, the Kjeldahl method, and HClO4-H2SO4 molybdenum antimony anti colorimetry, respectively.

2.3.2. Determination of Plant C, N, and P

Assimilation branch and secondary branch (the definition of branch rank were classified following Strahler’s system [27]. The terminal is the 0th-grade branch of the current year, and the downward branch is, in turn, the 1st−grade branch). Element content determination: C content was measured by potassium dichromate dilution calorimetry. N content was measured by the Kjeldahl method. P content was measured by the acid-soluble–molybdenum-antimony colorimetric method.

2.3.3. Determination of Plant NSC Content

The determination of plant SS used the anthrone colorimetric method, and the determination of ST used the perchloric acid method via the relation NSC = SS + ST. The samples brought back from the field with calculated water content of assimilation branches and secondary branches were ground into powder, passed through an 80-mesh sieve, and then numbered and packed into sealed bags for the determination of SS and ST contents.

2.4. Data Analysis

One-way analysis of variance (ANOVA) was used to compare the differences of plant and soil-related indicators between different water–salt gradients. Tukey’s multiple comparison method and independent t-tests were used to compare the NSC and C:N:P measurement ratios in the assimilation branches and the secondary branches in the same plant. The analyses for the water–salt gradient were performed using SPSS v.22.0 (SPSS, Inc., Chicago, IL, USA). The charts were drawn with Excel 2016 and Origin 9.0.

3. Results

3.1. Characteristics of Soil Environmental Factors

Based on the clustering of the measured values, the soil moisture and salt contents under the canopy of H. ammodendron were divided into three gradients according to K-means clustering results (Table 1). According to the climate conditions and soil environment of the Aibi Lake basin, the community structure and vegetation function of the studied transects, and the salinization and drought attributes of the Haloxylon plant habitat, the transects were divided into high water and high salinity, medium water salinity, and low-water and low-salt types of soil moisture and salinity. The first type was mainly distributed in high-moisture and high−salinity areas (high water and high salinity, I) occurring within 1.5 km of the river bank (the first H. ammodendron individuals were about 500 m away from the river bank), and the second type was in the middle of the transect. The soil environmental characteristics (medium−water salt, II) of the middle-water and middle-salt soils in the zone (the distance from the river bank was about 1.5–3 km), while the third type was distributed at the end of the transect (the distance from the river bank was about 3–4.1 km) and designated as low−moisture, low−salinity soil environmental characteristics (low−water and low−salt, III). The soil water and salt content decreased significantly with the decrease of water and salt gradient.
At the same time, the area provides strong support for verification and interpretation of the research results. In addition to the soil water content (SWC) and salinity (SSC) factors in the study area, other soil background values were investigated (Table 2). With the decrease of water and salt content, the changes of pH, organic carbon, total nitrogen and total phosphorus of H. ammodendron are consistent; that is, they all show a trend of significant decrease. (p ≤ 0.05).

3.2. Morphological Characteristics of H. ammodendron under Different Water−Salt Gradients

The base diameter, tree height, and crown area of H. ammodendron decreased with the decrease of water and salt gradient, and the difference between gradients was significant (Table 3).

3.3. Changes in Water Potential of Assimilating Branches and Secondary Branches of H. ammodendron with Water–Salt Gradients

With the decrease of the water−salt gradient, the predawn (ψpd−a) and midday (ψm−a) water potential of the assimilating branches of H. ammodendron decreased first and then increased. ψpd−a had the lowest median value of −4.93 ± 0.76 Mpa in environment III, while ψm−a had the lowest median value of −5.92 ± 0.94 Mpa in environment I. The predawn (ψpd−s) and midday (ψm−s) water potential of the secondary branches of H. ammodendron had significant differences in environments I, II, and III, and both had the lowest values in environment I, being −4.94 ± 0.82 Mpa and −5.91 ± 1.09 Mpa, respectively (Table 4).

3.4. Variation Characteristics of NSC and the Composition of H. ammodendron under Different Water–Salt Gradients

With the decrease of water and salt gradient, the content of soluble sugar (A−SS) and non-structural carbohydrate (A−NSC) in the assimilation branch of H. ammodendron decreased significantly, while the content of starch (A−ST) was the opposite, and I was significantly higher than II and III (p ≤ 0.05) (Figure 2A).
The contents of soluble sugar (S−SS), starch (S−ST), and non-structural carbohydrate (S−NSC) in the secondary branches of H. ammodendron showed a downward trend with the change of gradient, and the contents of (S−ST) and (S−NSC) in I and II were significantly higher than those in III, while there was no significant difference between I and II (Figure 2B).
With the decrease of water–salt gradient, the ratio of A−SS to S−SS of H. ammodendron decreased first and then increased, and there was a significant difference between gradient II and III, but there was no significant difference between I and II and III. The ratio of A−ST: S-ST and A−NSC: S−NSC increased with the change of water−salt gradient, and the starch ratio showed significant difference between I and II and III, while the ratio of A−NSC: S−NSC had no significant difference (Figure 2C).

3.5. Variation Ecostoichiometric Characteristics of H. ammodendron under Different Water–Salt Gradients

With the decrease of the water–salt gradients, the carbon (C) content of the assimilating branches of H. ammodendron increased significantly, and gradient III was significantly higher than gradient I and gradient II (p ≤ 0.05) (Figure 3A). The nitrogen (N) content and phosphorus (P) content showed a significant downward trend (p ≤ 0.05) (Figure 3B,C). Assimilating branches carbon C:N, C:P increased significantly with the decrease of water salt gradient (p ≤ 0.05) (Figure 3D,E), while N:P did not (p > 0.05) (Figure 3F).
With the decrease of water–salt gradients, the N and P content of secondary branches significantly decreased (p ≤ 0.05) (Figure 3H,I), while the C content did not significantly change (p > 0.05) (Figure 3G). The C:N, C:P, and N:P of the secondary branches have the maximum values in the III environments, 65.94 ± 2.26, 2431.57 ± 355.05, and 35.7 ± 4.20, respectively (Figure 3J–L). Based on ecological stoichiometry, leaf N:P <14 or >16 can be used as the basis for judging that vegetation is restricted by nitrogen or phosphorus. The N:P of assimilating branches and secondary branches is greater than 16.

3.6. The Relationship between the NSC of the Assimilation Branches and Secondary Branches of H. ammodendron and the Element Ratio Characteristics

The correlation analysis showed that the NSC content in the assimilation branches of H. ammodendron was significantly negatively correlated with the C content (R2 = 0.40, p < 0.001), C:N (R2 = 0.50, p < 0.001) and C:P (R2 = 0.44, p < 0.001) (Figure 4A,D,E), while it was significantly positively correlated with the N (R2 = 0.47, p < 0.001) and P content (R2 = 0.41, p < 0.001) (Figure 4B,C).
The content of NSC in secondary branches was significantly negatively correlated with C (R2 = 0.11, p < 0.001) content (Figure 4G) and C:N (R2 = 0.13, p < 0.001) (Figure 4J), significantly positively correlated with N (R2 = 0.10, p < 0.001) and P (R2 = 0.05, p ≤ 0.05) (Figure 4H,I), but not significantly correlated with C:P and N:P (p > 0.05) (Figure 4K,L).

4. Discussion

The extremely significant positive correlation results of water and salt data for 2008, 2014, 2015, 2016, and 2017 in the Aibi Lake basin indicate that plants face salt stress under high–water–content environments, while plants face drought stress under low–water–content environments. The physical and chemical environment of the soil under the canopy of the tested H. ammodendron plants in the observed transect was influenced by the interaction of water content and salt content. The difference in soil physicochemical environment directly affects the growth and survival of plants, determining their evolutionary direction and adaptive ability. The results of plant changes are reflected in the internal physiological response of plants in the short term, and in the long term by the external morphological adjustment of plants.

4.1. Effects of Different Water–Salt Gradients on NSC of H. ammodendron

Non-structural carbohydrates (NSCs) are the main intermediate substances between photosynthesis and respiration, mainly composed of soluble sugars and starch [5]. Their content can directly reflect the level of substances that can provide plant growth and survival, and can also reflect the balance between carbon absorption and carbon consumption [28]. The balance is affected by drought and salt stress, which can cause changes in plant growth and metabolism [29,30]. The present study found that the contents of NSC and SS in the assimilation branches and secondary branches of H. ammodendron decreased with the decreasing water–salt gradient; the content of ST in the assimilation branches gradually increased, and the content of ST in the secondary branches gradually decreased (Figure 3). Although the serious salinization of the soil near the river bank has hindered the water absorption of plant roots, the adjustment of water potential of assimilation branches and secondary branches of H. ammodendron has alleviated the “physiological drought” phenomenon of high salt stress, ensuring the water balance in the body, and non-structural carbohydrates can be effectively accumulated and used for the growth of their own tree morphology, which is conducive to occupying a certain niche space in the river bank zone with high diversity.
With the decrease of soil water and salt content in the transect, the effect of salt stress decreases, and the effect of drought stress increases. H. ammodendron adopts a strategy of improving water conductivity (See attached Figure S1) to achieve water balance in the body. In addition, under weak light conditions, it has a lower stomatal limit value and a higher concentration of intercellular carbon dioxide (See attached Figure S2), which can improve the carbon fixation capacity in the body. However, in order to ensure a high−water−conductivity structural system, H. ammodendron must mobilize its internal NSCs to respond to external environmental stresses in a timely manner. This will increase carbon consumption. Gleason et al. (2016) believed that this behavior of consuming NSCs to maintain water conductivity often leaded to hydraulic failure due to insufficient or delayed mobilization of NSCs, which can lead to reduced carbon assimilation and obstruction of phloem transportation [31]. As we continue to approach the desert, the soil water content is significantly insufficient. At this time, the drought stress effect is greater than the salt stress effect. The base diameter, plant height, and crown area of H. ammodendron are the lowest, and the water conductivity and carbon assimilation decrease. The stomatal conductance, net photosynthetic rate, and water use efficiency of gradient III are higher than those of gradient II, which again indicates that the inefficient water diversion system is highly safe, avoiding the risks of refilling and NSC mobilization and repair, and that there will be sufficient carbohydrates available for plant morphological adjustment [32]. In addition, the ratio of assimilation branch NSCs to secondary branch NSCs of H. ammodendron gradually decreased, indicating that the strategy of preferentially allocating NSC to the root system of H. ammodendron with gradient III is to maintain the safety of underground tissue structure, which is the survival mechanism of the entire plant [9].

4.2. Changes in the C:N:P Dosing Ratio Characteristics of H. ammodendron with Different Water–Salt Gradients

The nutrient content in the plant is an important indicator of the status of the plant, and it can also reflect the growth status of the plant [33]. This study found that with the decrease of water and salt contents, the contents of N and P in the assimilation branches and secondary branches of H. ammodendron decreased significantly (Figure 3B,C). He et al. (2014) analyzed the changes in N and P contents in plants in 155 drought-treated or persistently arid regions around the world and found that drought reduced the N and P contents in plants, with average decreases of 3.73% and 9.18%, respectively [34]. Because high temperature and low rainfall reduce the decomposition rate of organic matter, drought slows the C, N, and P biogeochemical cycles [35]. The soil background values show that from gradient I to III, the contents of organic matter, total N, and total P in the soil decreased significantly (Table 2). Therefore, the reduction of soil water content limits the availability of soil N and P, reduces the N and P available for H. ammodendron, and therefore reduces the N and P content in the plant. The C content in the assimilation branch was significantly higher in III than the other two samples. The content of C in assimilated branches was significantly higher than that in the other two sample points in gradient III; the difference in C content in secondary branches was not significant under the three gradients, but the change range of C content in assimilated branches and secondary branches of H. ammodendron was lower than those of N and P (Figure 3A–C,G–I). The structural substances (C) constituting plant tissues are less affected by the environment than functional and storage substances (N, P) [36].
The average contents of C, N, and P in secondary branches were 437.84 g·kg−1, 7.55 g·kg−1, and 0.27 g·kg−1, respectively. Its C content was higher than that of the assimilating branches, while N and P content was lower than that of the assimilating branches. This indicated that the main function of branches was to channel the inorganic salts and water absorbed by the plant roots and the energy substances synthesized by them to the reproductive organs, while transferring the nutrient substances assimilated by the leaves to the roots [37]. For woody plants, branches have a strong storage function, and their xylem and phloem require a large amount of C to build [38]. With the decrease of water and salt content, H. ammodendron was mainly affected by drought stress. Under drought stress, nutrients such as N and P absorbed by H. ammodendron were more easily allocated to assimilation branches to complete normal physiological activities [39], resulting in higher N and P content in the assimilating branches than in the secondary branches.
C:N and C:P can be used to characterize the utilization efficiency of nutrient elements N and P by plants [40]. In gradient III, the C:N and C:P of assimilated branches and secondary branches of H. ammodendron were significantly higher than in the other two gradients (Figure 3J,K), indicating that with the increase of drought stress effects, H. ammodendron distributes more N and P to the photosynthetic structure in arid habitats, which helps to achieve the maximum photosynthetic volume and increase the C content. This is consistent with the results of Larsen et al. (2011) [41]. N:P ratio can reveal P availability in ecosystems and reveal nutrient translocation between soil and plants [42,43]. It also implies that the P element has the greatest impact on the N:P ratio [44]. In addition, the N:P ratio can better reflect the strong internal relationship between soil and plant nutrients [45]. In this study, the N:P ratios of assimilation branches and secondary branches of H. ammodendron were greater than 16 under three gradients, indicating that the growth of H. ammodendron was mainly restricted by P under the influence of soil moisture, salinity, and nutrients. With the decrease of water and salt content, the N:P ratio in the two branches gradually increases, and the N:P ratio in secondary branches gradient III is significantly higher than that in gradients I and II. This may be due to water constraints that require a large amount of phosphorus to maintain the high primary productivity required for growth and development, thereby exacerbating P constraints [46,47].

4.3. The Relationship between the Characteristics of H. ammodendron NSC and the C:N:P Ratio under Different Water–Salt Gradients

There was a correlation between the NSC content composition of the assimilation branches and secondary branches of H. ammodendron and the characteristics of the C:N:P measurement ratio. The results showed that the NSC content of the two branches was significantly negatively correlated with the C content, indicating that with the increase in soil water and salt content, the carbon input into tissue construction of H. ammodendron increases, while the input to NSC decreases or the mobilization of H. ammodendron consumes NSC to resist the harm of environmental stress and the growth recovery [9], reflecting the strong dynamic balance regulation mechanism between NSC and C under a stress environment.
Leaf photosynthetic capacity and NSC synthesis are not only affected by leaf N concentration but are also closely related to leaf P concentration [48]. The higher the concentration of leaf N, the higher the photosynthesis rate. Leaf P is a key element in plant metabolism, energy, and protein synthesis [21]. The contents of N and P in assimilation branches were positively correlated with the content of NSC in assimilation branches and secondary branches. This indicated that the content of NSC in plants was affected by N and P content, and the absorption of N and P elements by H. ammodendron can increase the concentration of NSC pool in its body. Under gradient I, salt stress was more harmful, but the content of N and P in the soil was higher, which can provide more N and P for H. ammodendron to increase the plant NSC pool, helping H. ammodendron to resist interference and stabilize its growth. With the decrease of water and salt content, the N and P content in the soil gradually decreases, and drought stress gradually increases. The N and P elements that can be absorbed and utilized by H. ammodendron decreased, resulting in a decrease in the NSC content in the body or accelerating the consumption of NSC, reflecting that under the influence of water and salt interaction, H. ammodendron can ensure the nutritional balance between various constituent elements in the body, and maintain the metabolic process and breeding development.

5. Conclusions

Under the interaction of drought and salt stress, there was a balance regulation mechanism between the nutrient elements in the body of H. ammodendron. Its quantitative relationship can reflect the dynamics of carbon distribution in the body, and the relationship between non-structural carbohydrates and carbon (C), nitrogen (N), and phosphorus (P) was the most significant among the assimilation branches. Moreover, through the correlation between NSC and C:N:P, it can be inferred that the content of P transported by the roots of H. ammodendron to the assimilating branches played an important role in the balance of nutrient absorption and the synthesis and storage of NSC.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f14061185/s1, Figure S1: Changes of water conductivity per unit cross-sectional area of the secondary branches of H. ammodendron under different water-salt gradients. Lowercase letters represent the difference in the secondary branches hydraulic conductivity of H. ammodendron among different water-salt gradients; Figure S2: Net photosynthetic rate (A), intercellular co, concentration (B), stomatal conductance (C), transpiration rate (D), water use efficiency (E), and stomatal limit value (F) of H. ammodendron under different water-salt gradients. Lowercase letters represent the differences in photosynthetic parameters of the assimilation branches among different water-salt gradients; Figure S3: Study on correlation analysis of water and salt in Aibi Lake basin in recent years.

Author Contributions

F.Y. performed experiments, data analysis, and wrote the original draft. G.L. and Y.Q. conceived the study, performed the experiments and led writing. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Xinjiang Uygur Autonomous Region Graduate Innovation Project (Physiological Metabolism and Molecular Mechanism of Dioecious Populus euphratica in Dry and Wet Environment) (XJ2021G040).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data available for research upon request.

Acknowledgments

We thank Zhoukang Li, Dong Hu, Dexiong Teng, and Zhiqiang Li for their assistance in field work. We thank the anonymous reviewers for their constructive comments on the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Choat, B.; Jansen, S.; Brodribb, T.J.; Cochard, H.; Delzon, S.; Bhaskar, R.; Bucci, S.J.; Feild, T.S.; Gleason, S.M.; Hacke, U.G.; et al. Global convergence in the vulnerability of forests to drought. Nature 2012, 491, 752–755. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Mooney, H.A. The Carbon Balance of Plants. Annu. Rev. Ecol. Syst. 1972, 3, 315–346. [Google Scholar] [CrossRef]
  3. Dietze, M.C.; Sala, A.; Carbone, M.S.; Czimczik, C.I.; Mantooth, J.A.; Richardson, A.D.; Vargas, R. Nonstructural Carbon in Woody Plants. Annu. Rev. Plant Biol. 2014, 65, 667–687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Foyer, C.L.; Noctor, G. Photosynthetic nitrogen assimilation: Inter-pathway control and signaling. In Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism; Foyer, C.H., Noctor, G., Eds.; Springer: Dordrecht, The Netherlands, 2002. [Google Scholar]
  5. Ramírez-Briones, E.; Rodríguez-Macías, R.; Salcedo-Pérez, E.; Martínez-Gallardo, N.; Tiessen, A.; Molina-Torres, J.; Délano-Frier, J.P.; Zañudo-Hernández, J. Seasonal variation in non-structural carbohydrates, sucrolytic activity and secondary metabolites in deciduous and perennial Diospyros species sampled in Western Mexico. PLoS ONE 2017, 12, e0187235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Xie, H.T.; Yu, M.K.; Cheng, X.Y. Leaf non-structural carbohydrate allocation and C:N:P stoichiometry in response to light acclimation in seedlings of two subtropical shade-tolerant tree species. Plant Physiol. Biochem. 2018, 124, 146–154. [Google Scholar] [CrossRef] [PubMed]
  7. Ditmarová, L.; Kurjak, D.; Palmroth, S.; Kmeť, J.; StřElcovÁ, K. Physiological responses of Norway spruce (Picea abies) seedlings to drought stress. Tree Physiol. 2009, 30, 205–213. [Google Scholar] [CrossRef] [Green Version]
  8. Gao, Y.; Sun, Y.; Ou, Y.; Zheng, X.; Feng, Q.; Zhang, H.; Fei, Y.; Luo, J.; de Dios, V.R.; Yao, Y. Pretreating poplar cuttings with low nitrogen ameliorates salt stress responses by increasing stored carbohydrates and priming stress signaling pathways. Ecotox Environ. Safe 2021, 225, 112801. [Google Scholar] [CrossRef]
  9. McDowell, N.; Pockman, W.T.; Allen, C.D.; Breshears, D.D.; Cobb, N.; Kolb, T.; Plaut, J.; Sperry, J.; West, A.; Williams, D.G.; et al. Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytol. 2008, 178, 719–739. [Google Scholar] [CrossRef]
  10. Elser, J.J.; Sterner, R.W.; Gorokhova, E.A.; Fagan, W.F.; Markow, T.A.; Cotner, J.B.; Harrison, J.F.; Hobbie, S.E.; Odell, G.M.; Weider, L.W. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 2000, 3, 540–550. [Google Scholar] [CrossRef] [Green Version]
  11. Lebauer, D.S.; Treseder, K.K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 2008, 89, 371–379. [Google Scholar] [CrossRef] [Green Version]
  12. Elser, J.J.; Bracken, M.E.S.; Cleland, E.E.; Gruner, D.S.; Harpole, W.S.; Hillebrand, H.; Ngai, J.T.; Seabloom, E.W.; Shurin, J.B.; Smith, J.E. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 2007, 10, 1135–1142. [Google Scholar] [CrossRef] [Green Version]
  13. Elser, J.J.; Fagan, W.F.; Kerkhoff, A.J.; Swenson, N.G.; Enquist, B.J. Biological stoichiometry of plant production: Metabolism, scaling and ecological response to global change. New Phytol. 2010, 186, 593–608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Güsewell, S. N: P ratios in terrestrial plants: Variation and functional significance. New Phytol. 2004, 164, 243–266. [Google Scholar] [CrossRef] [PubMed]
  15. Wang, K.; Shen, C.; Sun, B.; Wang, X.N.; Wei, D.; Lyu, L.Y. Effects of drought stress on C, N and P stoichiometry of Ulmus pumila seedlings in Horqin sandy land. J. Appl. Ecol. 2018, 29, 2286–2294. [Google Scholar]
  16. Patel, A.D.; Jadeja, H.; Pandey, A.N. Effect of salinization of soil on growth, water status and nutrient accumulation in seedlings of Acacia auriculiformis (Fabaceae). J. Plant Nutr. 2010, 33, 914–932. [Google Scholar] [CrossRef]
  17. Rong, Q.; Liu, J.; Cai, Y.; Lu, Z.; Zhao, Z.; Yue, W.; Xia, J. Leaf carbon, nitrogen and phosphorus stoichiometry of Tamarix chinensis Lour. in the Laizhou Bay coastal wetland, China. Ecol. Eng. 2015, 76, 57–65. [Google Scholar] [CrossRef]
  18. Sardans, J.; Peñuelas, J.; Ogaya, R. Drought-induced changes in C and N stoichiometry in a Quercus ilex Mediterranean forest. Forest Sci. 2008, 54, 513–522. [Google Scholar]
  19. Van Dijk, G.; Smolders, A.J.P.; Loeb, R.; Bout, A.; Roelofs, J.G.M.; Lamers, L.P.M. Salinization of coastal freshwater wetlands; effects of constant versus fluctuating salinity on sediment biogeochemistry. Biogeochemistry 2015, 126, 71–84. [Google Scholar] [CrossRef]
  20. Sun, X.; Gao, Y.; Wang, D.; Chen, J.; Zhang, F.; Zhou, J.; Yan, X.; Li, Y. Stoichiometric variation of halophytes in response to changes in soil salinity. Plant Biol. 2017, 19, 360–367. [Google Scholar] [CrossRef]
  21. Reich, P.B.; Oleksyn, J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc. Nat. Acad. Sci. USA 2004, 101, 11001–11006. [Google Scholar] [CrossRef] [Green Version]
  22. McGroddy, M.E.; Daufresne, T.; Hedin, L.O. Scaling of C:N:P stoichiometry in forests worldwide: Implications of terrestrial Redfield-type ratios. Ecology 2004, 85, 2390–2401. [Google Scholar] [CrossRef]
  23. IPCC. Climate Change 2014: Impacts, Adaptation, and Vulnerability-Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge, UK, 2014; p. 1132. [Google Scholar]
  24. Yan, S.; Weihong, Z.; Kequan, P.; Keping, M.A. Genetic variation within and among populations of a dominant desert tree Haloxylon ammodendron (Amaranthaceae) in China. Ann. Bot. 2005, 96, 245–252. [Google Scholar]
  25. Gong, X.W.; Lyu, G.H.; Ran, Q.Y.; Yang, X.D. Response of vegetative growth and biomass allocation of Lappula semiglabra seedlings to dew gradient. J. Appl. Ecol. 2016, 27, 2257–2263. [Google Scholar]
  26. Yang, X.D.; Lü, G.H.; Tian, Y.H.; Yang, J.; Zhang, X.M. Ecological groups of plants in Ebinur Lake Wetland Nature Reserve of Xinjiang. Chin. J. Ecol. 2009, 28, 2489–2494. [Google Scholar]
  27. Mcmahon, T.A.; Kronauer, R.E. Tree structures: Deducing the principle of mechanical design. J. Theor. Biol. 1976, 59, 443. [Google Scholar] [CrossRef]
  28. von Arx, G.; Arzac, A.; Fonti, P.; Frank, D.; Zweifel, R.; Rigling, A.; Galiano, L.; Gessler, A.; Olano, J.M. Responses of sapwood ray parenchyma and non-structural carbohydrates of Pinus sylvestris to drought and long-term irrigation. Funct. Ecol. 2017, 31, 1371–1382. [Google Scholar] [CrossRef] [Green Version]
  29. McDowell, N.G.; Beerling, D.J.; Breshears, D.D.; Fisher, R.A.; Raffa, K.F.; Stitt, M. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 2011, 26, 523–532. [Google Scholar] [CrossRef]
  30. Todea, I.M.; González-Orenga, S.; Boscaiu, M.; Plazas, M.; Sestras, A.F.; Prohens, J.; Vicente, O.; Sestras, R.E. Responses to water deficit and salt stress in Silver Fir (Abies alba Mill.) seedlings. Forests 2020, 11, 395. [Google Scholar] [CrossRef] [Green Version]
  31. Gleason, S.M.; Westoby, M.; Jansen, S.; Choat, B.; Hacke, U.G.; Pratt, R.B.; Bhaskar, R.; Brodribb, T.J.; Bucci, S.J.; Cao, K.F.; et al. Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol. 2016, 209, 123–136. [Google Scholar] [CrossRef] [Green Version]
  32. Brodribb, T.J.; Cochard, H. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 2009, 149, 575–584. [Google Scholar] [CrossRef] [Green Version]
  33. Niu, D.; Zhang, C.; Ma, P.; Fu, H.; Elser, J.J. Responses of leaf C: N: P stoichiometry to water supply in the desert shrub Zygophyllum xanthoxylum. Plant Biol. 2019, 21, 82–88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. He, M.Z.; Dijkstra, F.A. Drought effect on plant nitrogen and phosphorus: A meta-analysis. New Phytol. 2014, 204, 924–931. [Google Scholar] [CrossRef] [PubMed]
  35. Hartley, A.N.; Bargerj, B.; Okin, G. Dryland Ecosystems Nutrient Cycling in Terrestrial Ecosystems; Marschner, P., Rengel, Z., Eds.; Springer: Berlin/Heidelberg, Germany, 2007; pp. 271–308. [Google Scholar]
  36. Sterner, R.W.; Elser, J.J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere; Princeton University Press: Princeton, NJ, USA, 2002; p. 357. [Google Scholar]
  37. Wang, J.Y.; Wang, J.N.; Wu, T.G. Stoichiometric homeostasis, physiology, and growth responses of three tree species to nitrogen and phosphorus addition. Trees 2018, 32, 1377–1386. [Google Scholar] [CrossRef]
  38. Yin, H.; Zheng, H.; Zhang, B.; Tariq, A.; Lv, G.; Zeng, F.; Graciano, C. Stoichiometry of C:N:P in the Roots of Alhagi sparsifolia Is More Sensitive to Soil Nutrients Than Aboveground Organs. Front. Plant Sci. 2021, 12, 698961. [Google Scholar] [CrossRef]
  39. Ding, D.; Arif, M.; Liu, M.; Li, J.; Hu, X.; Geng, Q.; Yin, F.; Li, C. Plant-soil interactions and C:N:P stoichiometric homeostasis of plant organs in riparian plantation. Front. Plant Sci. 2022, 13, 979023. [Google Scholar] [CrossRef]
  40. Vitousek, P. Nutrient cycling and nutrient use efficiency. Am. Nat. 1982, 119, 553–572. [Google Scholar] [CrossRef]
  41. Larsen, K.S.; Andresen, L.C.; Beier, C.; Jonasson, S.; Albert, K.; Ambus, P.; Arndal, M.F.; Carter, M.S.; Christensen, S.; Holmstrup, M.; et al. Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: Synthesizing results of the CLIMAITE project after two years of treatments. Global Change Biol. 2011, 17, 1884–1899. [Google Scholar] [CrossRef]
  42. Fan, H.B.; Wu, J.P.; Cai, Q.K. Linkages of plant and soil C:N:P stoichiometry and their relationships to forest growth in subtropical plantations. Plant Soil 2015, 392, 127–138. [Google Scholar] [CrossRef]
  43. Cao, Y.; Chen, Y.M. Coupling of plant and soil C:N:P stoichiometry in black locust (Robinia pseudoacacia) plantations on the Loess Plateau, China. Trees 2017, 31, 1559–1570. [Google Scholar] [CrossRef]
  44. Luo, Y.; Peng, Q.; Li, K.; Gong, Y.; Liu, Y.; Han, W. Patterns of nitrogen and phosphorus stoichiometry among leaf, stem and root of desert plants and responses to climate and soil factors in Xinjiang, China. Catena 2020, 199, 105100. [Google Scholar] [CrossRef]
  45. Zhang, W.; Liu, W.; Xu, M.; Deng, J.; Han, X.; Yang, G.; Feng, Y.; Ren, G. Response of forest growth to C:N:P stoichiometry in plants and soils during Robinia pseudoacacia afforestation on the Loess Plateau, China. Geoderma 2018, 337, 280–2899. [Google Scholar] [CrossRef]
  46. Warren, C.R.; Adams, M.A.; Chen, Z.L. Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Funct. Plant Biol. 2000, 27, 407–416. [Google Scholar] [CrossRef]
  47. Qi, D.D.; Feng, F.J.; Fu, Y.M. C:N:P stoichiometry of different soil components after the transition of temperate primary coniferous and broad-leaved mixed forests to secondary forests. Soil Till Res. 2022, 216, 105260. [Google Scholar] [CrossRef]
  48. Barbaroux, C.; Breda, N. Contrasting distribution and seasonal dynamics of carbohydrate reserves in stem wood of adult ring-porous sessile oak and diffuse-porous beech trees. Tree Physiol. 2002, 22, 1201–1210. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Distribution of sample points.
Figure 1. Distribution of sample points.
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Figure 2. Change characteristics of NSCs and their components of H. ammodendron under different water–salt gradients. (A) Change characteristics of NSCs and their components in assimilating branches; (B) change characteristics of NSCs and their components in secondary branches; (C) soluble sugar, starch, and non-structural carbon compound d ratio of secondary branches and assimilating branches of H. ammodendron under different water–salt gradients. Lowercase letters indicate the difference in NSC content of assimilation branches or secondary branches under different water–salt gradients (p ≤ 0.05); mean ± standard error (n = 3).
Figure 2. Change characteristics of NSCs and their components of H. ammodendron under different water–salt gradients. (A) Change characteristics of NSCs and their components in assimilating branches; (B) change characteristics of NSCs and their components in secondary branches; (C) soluble sugar, starch, and non-structural carbon compound d ratio of secondary branches and assimilating branches of H. ammodendron under different water–salt gradients. Lowercase letters indicate the difference in NSC content of assimilation branches or secondary branches under different water–salt gradients (p ≤ 0.05); mean ± standard error (n = 3).
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Figure 3. Ecological stoichiometric characteristics of H. ammodendron under different water–salt gradients. (A–F) are the C content, N content, P content, C:N, C:P, and N:P of the assimilating branches, respectively; (G–L) are the C content, N content, P content, C:N, C:P, and N:P of the secondary branches, respectively. Lowercase letters indicate the difference in the ecological stoichiometry of the assimilation branches or secondary branches of H. ammodendron under different water–salt gradients (p ≤ 0.05); mean ± standard error (n = 3).
Figure 3. Ecological stoichiometric characteristics of H. ammodendron under different water–salt gradients. (A–F) are the C content, N content, P content, C:N, C:P, and N:P of the assimilating branches, respectively; (G–L) are the C content, N content, P content, C:N, C:P, and N:P of the secondary branches, respectively. Lowercase letters indicate the difference in the ecological stoichiometry of the assimilation branches or secondary branches of H. ammodendron under different water–salt gradients (p ≤ 0.05); mean ± standard error (n = 3).
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Figure 4. The stoichiometric relationship between non−structural carbohydrates (NSCs) and carbon (C), nitrogen (N), and phosphorus (P) in assimilating branches and secondary branches of H. ammodendron under the influence of water and salt. (A–F) are the correlations between NSCs and C, N, P, C:N, C:P, and N:P in the assimilation branches, respectively; (G–L) are the correlations between NSCs and C, N, P, C:N, C:P, and N:P in the secondary branches, respectively.
Figure 4. The stoichiometric relationship between non−structural carbohydrates (NSCs) and carbon (C), nitrogen (N), and phosphorus (P) in assimilating branches and secondary branches of H. ammodendron under the influence of water and salt. (A–F) are the correlations between NSCs and C, N, P, C:N, C:P, and N:P in the assimilation branches, respectively; (G–L) are the correlations between NSCs and C, N, P, C:N, C:P, and N:P in the secondary branches, respectively.
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Table
Table 1. K-means clustering results of soil water and salt under the canopy of Haloxylon ammodendron.
Table 1. K-means clustering results of soil water and salt under the canopy of Haloxylon ammodendron.
Clustering ResultsSample NumberSWC (%)SSC (g·kg−1)
I1–8, 10, 2218.39 ± 0.63 a9.02 ± 0.53 a
II9, 11–21, 23–34, 37, 399.84 ± 0.40 b5.22 ± 0.19 b
III35–36, 38, 40–623.46 ± 0.25 c2.48 ± 0.12 c
Note: Different lowercase letters indicate significant differences between different water–salt gradients (p ≤ 0.05). The values in the table are mean ± standard error (n = 3).
Table
Table 2. Soil background values under different water–salt gradients.
Table 2. Soil background values under different water–salt gradients.
Water–Salt GradientpHSOC (g·kg−1)TN (g·kg−1)TP (g·kg−1)
I8.55 ± 0.08 a7.66 ± 1.02 a1.26 ± 0.12 a0.62 ± 0.01 a
II8.20 ± 0.06 b1.90 ± 0.12 b0.41 ± 0.02 b0.48 ± 0.01 b
III7.71 ± 0.04 c1.06 ± 0.07 b0.20 ± 0.01 c0.37 ± 0.01 c
Note: Different lowercase letters indicate significant differences between different water–salt gradients (p ≤ 0.05). The values in the table are mean ± standard error (n = 3).
Table
Table 3. Changes of H. ammodendron characters under different water–salt gradients.
Table 3. Changes of H. ammodendron characters under different water–salt gradients.
Water–Salt GradientBase Diameter (cm2)Tree Height (m)Crown Area (m2)
I22.73 ± 2.71 a4.10 ± 0.28 a33.86 ± 4.95 a
II15.69 ± 1.49 b3.04 ± 0.13 b 15.72 ± 2.83 b
III10.21 ± 0.47 c2.53 ± 0.09 c8.73 ± 0.75 c
Note: Different lowercase letters indicate significant differences between different water–salt gradients (P ≤ 0.05). The values in the table are mean ± standard error (n = 3).
Table
Table 4. Changes in water potential of assimilating branches and secondary branches under different water–salt gradients.
Table 4. Changes in water potential of assimilating branches and secondary branches under different water–salt gradients.
Water–Salt GradientAssimilating BranchesSecondary Branches
PredawnMiddayPredawnMidday
I−4.62 ± 0.29 ab−5.92 ± 0.94 b−4.94 ± 0.82 c−5.91 ± 1.09 c
II−4.24 ± 0.79 a−4.77 ± 0.95 a−3.55 ± 0.75 a−3.78 ± 1.02 a
III−4.93 ± 0.76 b−5.29 ± 0.85 ab−4.23 ± 0.85 b−4.53 ± 1.12 b
Note: Different lowercase letters indicate significant differences between different water–salt gradients (p ≤ 0.05). The values in the table are mean ± standard error (n = 3).
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Yang, F.; Lv, G.; Qie, Y. Correlation between Non-Structural Carbohydrates and C:N:P Stoichiometric Ratio of Haloxylon ammodendron under Different Water–Salt Gradients. Forests 2023, 14, 1185. https://doi.org/10.3390/f14061185

AMA Style

Yang F, Lv G, Qie Y. Correlation between Non-Structural Carbohydrates and C:N:P Stoichiometric Ratio of Haloxylon ammodendron under Different Water–Salt Gradients. Forests. 2023; 14(6):1185. https://doi.org/10.3390/f14061185

Chicago/Turabian Style

Yang, Fang, Guanghui Lv, and Yadong Qie. 2023. "Correlation between Non-Structural Carbohydrates and C:N:P Stoichiometric Ratio of Haloxylon ammodendron under Different Water–Salt Gradients" Forests 14, no. 6: 1185. https://doi.org/10.3390/f14061185

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