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Article

Response of Leaf Non-Structural Carbohydrates to Elevation in Dioecious Plants, Populus cathayana and Hippophae rhamnoides

by
Jiamei Wu
1,2,3,4,
Shun Liu
1,2,
Qiuhong Feng
5,
Xiangwen Cao
1,2,
Hongshuang Xing
1,2 and
Zuomin Shi
1,2,6,*
1
Key Laboratory of Forest Ecology and Environment of National Forestry and Grassland Administration, Ecology and Nature Conservation Institute, Chinese Academy of Forestry, Beijing 100091, China
2
Sichuan Miyaluo Forest Ecosystem Observation and Research Station, Aba 623100, China
3
Chinese Academy of Natural Resource Economics, Beijing 101149, China
4
School of Economics and Management, Beijing Forestry University, Beijing 100083, China
5
Ecological Restoration and Conservation for Forest and Wetland Key Laboratory of Sichuan Province, Sichuan Academy of Forestry Sciences, Chengdu 610081, China
6
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, China
*
Author to whom correspondence should be addressed.
Forests 2025, 16(2), 246; https://doi.org/10.3390/f16020246
Submission received: 3 December 2024 / Revised: 29 December 2024 / Accepted: 14 January 2025 / Published: 27 January 2025
(This article belongs to the Section Forest Ecophysiology and Biology)
Browse Figures
Versions Notes

Abstract

:
Non-structural carbohydrates (NSCs) can reflect the balance of resource allocation and trade-offs, as well as the adaptability of plants to the environment. Alterations in environmental conditions across an elevation gradient may impact the carbon balance within leaves. Nonetheless, it remains highly uncertain whether the effect of elevation on NSCs differs among species and sexes. To reveal the response patterns of leaf NSCs in dioecious plants with elevation, Populus cathayana Rehd. and Hippophae rhamnoides L., distributed at four elevations in the subalpine region of western Sichuan, China, were selected, and female and male leaves were sampled and measured for their contents of NSCs, soluble sugar, and starch. Meanwhile, the relationships of NSCs, soluble sugar, and starch with leaf nitrogen and phosphorus were analyzed. The results showed that the elevational patterns of NSCs were mainly dependent on species and were slightly affected by sex. Leaf NSCs in both sexes of P. cathayana did not exhibit significant linear changes, whereas those in H. rhamnoides increased significantly and linearly with elevation. For P. cathayana, a significant increase in leaf starch with elevation was only found in female plants and may benefit from phosphorus deficiency, as it was significantly negatively correlated with phosphorus. However, leaf soluble sugar and starch between sexes of H. rhamnoides showed similar patterns of significant increases with elevation, and they were not correlated significantly with nitrogen and phosphorus. This might be due to H. rhamnoides, which is a nitrogen-fixing plant and thereby did not show deficiencies or limitations in nitrogen and phosphorus, as shown by the decreased or unchanged elevational patterns of nitrogen/phosphorus, starch/phosphorus, and soluble sugar/phosphorus. Overall, our results emphasize that species, rather than sex, is an important factor influencing the elevational pattern of NSCs, but for specific species, such as P. cathayana, in this study, there was a divergence in the elevational response of the allocation of starch and soluble sugar between sexes, reflecting the specific adaptive strategies of different plant species or sexes in response to changes in the growing environment.

1. Introduction

Non-structural carbohydrates (NSCs) are the primary photosynthates and temporary storage materials accumulated in trees when they are overproduced [1,2]. They are involved in growth and metabolic processes and serve important physiological and ecological functions in adapting to environmental changes in plants [1,2]. NSCs mainly comprise soluble sugar and starch. The former performs important physiological functions in supporting growth, respiration, and defense, directly or as intermediary metabolites, osmolytes, and substrates for transport, while the latter is a purely long-term storage compound [3]. Studies have suggested that the allocation of NSCs to soluble sugars and starch is involved in the metabolic processes related to osmoregulation and transformations between the two components in resistance to cold, which is essential for predicting how plants will respond to environmental changes [4,5,6].
Elevation is an important factor influencing plant life forms and geographic distributions [7]. Differences in growth environments caused by elevational variability drive diversification in plant physiological and morphological adaptation [8]. To compensate for the asynchrony between source and sink activities under environmental stress, plants rather prefer to store photosynthates at the expense of other sinks, such as growth and related respiration [5,9]. Massive previous studies have shown that leaf NSCs in tree species increase with elevation [5,10], but different trends have also been found in other reports [11,12]. Most of the research on variations in leaf NSCs along an elevational gradient emphasized only the total amount (the sum of soluble sugars and starches (NSCs)), but paid less attention to its components [5]. In addition, nitrogen and phosphorus are key nutrient elements for photosynthesis that might directly influence the content of NSCs in leaves and other tissues [2,13]. A review based on 40 fertilization experiments indicated that plant growth was mainly limited by phosphorus when the nitrogen/phosphorus ratio was higher than 16, by nitrogen when the ratio was lower than 14, and by nitrogen and/or phosphorus when the ratio was between 14 and 16 [14]. Therefore, further insights into the variation in leaf NSCs with elevation, and whether it is affected by plant nutrients, are necessary.
Dioecious angiosperms account for about 6% of extant angiosperms and make important contributions to terrestrial ecosystem species pools [15]. They exclude the risk of self-pollination completely and optimize the resource allocation in functionality of both male and female plants [16]. Differences in reproductive costs and needs between sexes may predispose different responses and adaptation strategies to environmental conditions [17]. In some experiments with artificial environmental gradients, greater reproductive investment prompted female plants to perform worse than males under stress conditions [18,19]. Previous studies comparing the performance of males and females have focused largely on short-term physiological responses under artificial conditions [20,21], and little attention has been paid to their sex-specific long-term responses throughout their natural habitats, which is of great significance for explaining plant responses to the environment [22,23]. The study of dioecious plants based on the growth of the natural habitat may, therefore, further truly reflect their response and adaptation to environmental changes, on which studies still need to be strengthened.
Leaves are the source of carbohydrates for plants. The gradient changes in environmental factors with elevation influence the carbon balance in leaf organs. Nevertheless, plants´ physiological differences between species and between sexes may also imply uncertainty in resource allocation and trade-offs. Populus cathayana Rehd., a species in the Salicaceae family, is a native species of China which is distributed over a large area of North, Central, and Southwest China and plays an important role in maintaining regional ecological stability [24]. Hippophae rhamnoides L., a species in the Elaeagnaceae family, is a nitrogen-fixing tree species that is widely distributed in the eastern Qinghai–Tibetan Plateau of China, with a wide range of habitats and a large elevation span [25]. These species are ideal for studying the response and adaptation of dioecious plants to elevation gradients. To gain a better insight into the response of leaf NSCs to elevation in dioecious plants, we quantitatively analyzed leaf NSCs, starch, and soluble sugar parameters in male and female plants of P. cathayana and H. rhamnoides distributed along an elevation gradient on the eastern Qinghai–Tibetan Plateau in China and explored their correlations with leaf nitrogen and phosphorus concentrations. We hypothesized the following: (1) due to species-specific differences, the elevational patterns of leaf NSCs might vary between P. cathayana and H. rhamnoides plants; (2) due to the different nitrogen-fixing capacity between the two species, leaf nutrients might influence NSC content; and (3) there might be different leaf NSC performance in different sexes under the condition of environmental variation along the elevation and/or differences in leaf nutrients.

2. Materials and Methods

2.1. Study Site

This study was conducted at the Wolong Nature Reserve and Miyaluo Nature Reserve located in the Wenchuan and Lixian counties of Aba Tibetan and Qiang Autonomous Prefecture, Sichuan Province, China, respectively (102°40′–103°13′ E, 31°02′–31°52′ N). The sites are characterized by alpines and gorges, and they experience a typical Tibetan Plateau climate, with the climate patterns being controlled by the eastern Asian monsoon, the Indian monsoon, and the continental westerlies. It has high mountains and deep valleys, with cool summers and cold winters. The mean annual temperature is approximately 8.7 °C (0.6 °C in January to 16.4 °C in July), decreasing with elevation to about 0.46 °C per 100 m. The mean annual precipitation is about 800 mm (over 80% from May to October) and generally increases with elevation [26].

2.2. Field Sampling

Four sites along an elevation gradient were selected with an interval of 400–600 m for leaf sampling (i.e., 1800, 2200, 2600 and 3100 m for P. cathayana, and 1900, 2500, 3100 and 3700 for H. rhamnoides). At each site, 7–9 female plants, as well as male plants with similar heights and diameters and healthy, naturally growing, unshaded, and essentially uniform growth characteristics were randomly selected for leaf sampling. A mixed sample of 20 new fully extended, healthy, and disease- and insect-free mature leaves from the middle of the crown in the four directions was sampled from each plant. The main vegetation types of the selected sites are the broad-leaved forests, coniferous-broad-leaved mixed forests, and shrubs. The broad-leaved forests are mainly dominated by Betula spp.; the coniferous-broad-leaved mixed forests by Abies spp. and Betula spp.; and the shrubs by Hippophae spp. and Salix spp. Their detailed characteristics are shown in Table 1.

2.3. Experimental Measurements

The collected leaf samples were firstly dried at 105 °C for 30 min and then dried to a constant weight at 70 °C. After crushing, the oven-dried leaf samples were passed through a 0.25 mm sieve. Leaf NSCs content was defined as the sum of the starch and soluble sugar contents. To determine the soluble sugar content, a dry powder sample (about 0.5 g) was added to a conical flask containing 50 mL of distilled water. The sample solution was boiled in a steam oven for 2 h and then cooled and filtered. Subsequently, the filtrate was injected into a Water 2695 high-performance liquid chromatograph equipped with a Sugar-Pak I column (Waters-Millipore, Milford, MA, USA) using distilled water as the mobile phase at a flow rate of 0.6 mL min−1 under a column temperature of 70 °C. A parallax detector was used to determine the soluble sugar. For the determination of starch, a dry powder sample (about 0.1 g) was added to a stoppered test tube containing 10 mL of distilled water, followed by 1 mL of 2:1 hydrochloric acid, and incubated at 100 °C for 8 h. After cooling, the solution pH was adjusted to neutral with 40% NaOH and then the volume was adjusted to 15 mL with distilled water. The solution was filtered for starch determination with the same procedure used for the determination of soluble sugar [27]. Leaf nitrogen and phosphorus concentrations (g kg−1) were determined via a VELP fully automated Kjeldahl nitrogen tester (UDK-139, Milano, Italy) and a plasma emission spectrometer (IRIS Intrepid II XSP, Thermo Fisher Scientifc Co., Waltham, MA, USA), respectively.

2.4. Statistical Analysis

All variables were tested for normal distribution (Shapiro–Wilk test) and heterogeneity (Levene’s test) before analysis. One-way ANOVA was used to test the effects of elevation on leaf traits of the same sex, and multiple comparisons between elevations were made using the Scheffé method. Meanwhile, independent sample t-tests were used to compare differences in leaf traits between sexes at the same elevation. Two-way ANOVA was used to test the effects of elevation, sex, and their interactions on leaf traits. A univariate linear regression model was used to analyze the trend of leaf traits of the same sex with elevation, and an analysis of covariance (ANCOVA) was used to compare the differences in the trend of leaf traits of different sexes with elevation, in which the dependent variable was leaf traits, the fixed factor was sex, and the covariate was elevation. The relationships between leaf traits were analyzed using Spearman’s correlation. All statistical analyses were conducted with SPSS 22.0, and the figures were plotted with Origin 2021.

3. Results

3.1. Elevational Patterns of Leaf NSCs, Starch, and Soluble Sugar Contents

For P. cathayana, no significant linear variations in the leaf NSCs and soluble sugar contents of female and male plants, and in the starch content and soluble sugar/starch ratio of male plants with increasing elevation, were observed. The leaf starch content and soluble sugar/starch ratio of female plants increased and decreased significantly and linearly with elevation, respectively (Table 2). The leaf soluble sugar and NSC contents differed significantly between the female and male plants (PS < 0.05), and there were significant interaction effects of elevation and sex on the starch and NSC contents and the soluble sugar/starch ratio (PE×S < 0.05). The leaf soluble sugar content of male plants (25.17 g·100g−1) was significantly higher (p < 0.05) than that of females (22.69 g·100g−1) at 2600 m. The leaf starch content of male plants (8.12 g·100g−1) was significantly higher than that of females (5.15 g·100g−1) at 2200 m, but at 3100 m, it (5.68 g·100g−1) was significantly lower than that of females (9.72 g·100g−1). The leaf NSC contents of the male plants (32.92 and 32.50 g·100g−1, respectively) were significantly higher than that of the females (27.76 and 28.33 g·100g−1, respectively) at 2200 and 2600 m, but were significantly lower than that of the females at 3100 m. Meanwhile, the leaf soluble sugar/starch ratio of the male plants was significantly lower and higher than that of the females at 2200 and 3100 m, respectively (Figure 1). For H. rhamnoides, the contents of NSCs, soluble sugar, and starch were significantly increased, and the soluble sugar/starch ratio was significantly decreased along the elevation in both female and male plants. In addition, the above four indexes were not significantly different between female and male plants (Figure 1).

3.2. Elevational Patterns of Leaf Nitrogen and Phosphorus Concentrations

For P. cathayana, the leaf phosphorus content in females and male plants decreased linearly along the elevation, and an analysis of covariance showed that the magnitude of variation in male plants was higher than that in females (Table 3). In contrast, the leaf nitrogen/phosphorus ratio increased linearly with elevation for both sexes, and the magnitude of variation in male plants was lower than that in females (Table 3). As shown in Figure 2, differences in leaf phosphorus concentration and nitrogen/phosphorus ratio were significant between male and female plants (PS < 0.05). Male leaf nitrogen concentration (23.59 g·kg−1) was significantly lower than that of females (27.75 g·kg−1) at 3100 m. Male leaf nitrogen/phosphorus ratio (11.65 and 17.47 g·kg−1, respectively) was significantly lower than that of females (16.64 and 27.32 g·kg−1, respectively) at 1800 and 3100 m, whereas the leaf phosphorus content of male plants was significantly higher than that of females at 1800 and 3100 m (p < 0.05). The nitrogen/phosphorus ratios were only less than 14 in male plants at 1800 m, and were greater than 16 in both sexes at the other elevations. For H. rhamnoides, the leaf nitrogen and phosphorus contents of both female and male plants increased linearly, whereas the nitrogen/phosphorus ratio decreased linearly with elevation (Table 3). In addition, male and female plants did not differ significantly along the elevation (PS < 0.05). The nitrogen/phosphorus ratios were only less than 14 in female plants at 3700 m, and were greater than 14 in both sexes at other elevations, including greater than 16 at 1900 and 2500 m (Figure 2).

3.3. Elevational Patterns of the Ratios of Leaf Soluble Sugar, Starch, and NSCs to Nitrogen and Phosphorus

For P. cathayana, the leaf soluble sugar/phosphorus ratio and NSCs/phosphorus ratio in both sexes, as well as the leaf starch/nitrogen ratio and starch/phosphorus ratio in female plants, increased linearly along the elevation, and their variability was shown to be higher in females than in males (Table 4). There were significant differences in the soluble sugar/nitrogen ratio, and the ratios of NSCs, soluble sugar, and starch to phosphorus between female and male plants (PS < 0.05). Elevation and sex interactions were present for the ratios of NSC and its components to nitrogen and phosphorus (PE×S < 0.05), except for the soluble sugar/nitrogen ratio. The male leaf soluble sugar/nitrogen ratio at 2600 and 3100 m and NSCs/nitrogen ratio at 2200 and 2600 m were significantly higher than those of females, whereas the NSCs/phosphorus ratio at 1800 and 3100 m was significantly lower than that of females (p < 0.05). Leaf soluble/phosphorus, starch/nitrogen, and starch/phosphorus ratios in male plants were significantly higher and lower than those of females at 2200 m and 3100 m, respectively (p < 0.05). In contrast, the ratios of leaf soluble sugar, starch, and NSCs to nitrogen and phosphorus did not differ significantly between sexes for H. rhamnoides. Elevation linearly increased the ratios of leaf soluble sugar and NSCs to phosphorus in both sexes of H. rhamnoides plants, whereas the other ratios exhibited insignificant elevational patterns (Table 4, Figure 3).

3.4. Correlations Between Soluble Sugar, Starch, and NSCs with Nitrogen and Phosphorus

In male P. cathayana plants, leaf NSCs were significantly positively correlated with soluble sugar and nitrogen. The soluble sugar/starch ratio was significantly negatively correlated with starch. Soluble sugar was significantly positively correlated with nitrogen, whereas starch and nitrogen/phosphorus were significantly negatively correlated with phosphorus. In female P. cathayana plants, leaf NSCs were significantly positively correlated with soluble sugar and starch. Starch was significantly negatively correlated with soluble sugar/starch and phosphorus. The ratio of nitrogen to phosphorus was significantly positively and negatively correlated with nitrogen and phosphorus, respectively. In both male and female H. rhamnoides plants, leaf NSCs were significantly positively correlated with soluble sugar and starch. The soluble sugar/starch ratio was significantly negatively correlated with starch, and nitrogen/phosphorus ratio was significantly negatively correlated with both nitrogen and phosphorus. Additionally, leaf starch and phosphorus in male H. rhamnoides plants were significantly positively correlated (Figure 4).

4. Discussion

4.1. The Response of Leaf NSCs to Elevation Varied with Species

Leaf NSCs are not only the primary products of plant photosynthesis, but also serve as the foundation for the synthesis of various substances [9]. Their storage may indicate two potential scenarios, with a gradual transition between them: one involves short- and long-term reserves for growth, respiration, and osmotic demand, whereas the other results from an oversupply due to an imbalance between synthesis and demand, leading to “accumulation” [28]. As elevation increases, temperature decreases gradually, and plant growth exhibits greater sensitivity to low temperatures than photosynthesis [29,30]. This disproportionate decline in growth relative to photosynthesis results in a corresponding increase in leaf NSC storage [5,31,32]. In this study, H. rhamnoides exhibited a similar pattern of a gradual increase in leaf NSCs with elevation (Table 2), consistent with the findings of Zhou et al. (2023) in a global meta-analysis of 90 vertical transection plant species [5] and of Li et al. (2019) on H. rhamnoides [33].
Nitrogen and phosphorus are recognized as critical determinants influencing the distribution of plant communities and constraining primary productivity in high-elevation regions [31]. Nitrogen is an essential element for chlorophyll synthesis, which directly contributes to the production of photosynthates [34,35]. Phosphorus serves as a fundamental component for the synthesis of ATP and Rubisco [36]. These two elements contribute to leaf photosynthetic capacity and the content of NSCs [35,37]. In this study, the concentrations of leaf nitrogen and phosphorus in both male and female H. rhamnoides increased with elevation, while the ratios of NSCs/nitrogen and NSCs/phosphorus remained unchanged and decreased, respectively. This suggested that per-unit nitrogen or phosphorus contents along the elevation gradient were sufficiently available for NSC formation [38], potentially due to nitrogen-fixing capabilities. Conversely, no significant changes were observed in the leaf NSCs of male and female P. cathayana with elevation. The marked decrease in leaf phosphorus and the significant increase in the NSCs/phosphorus ratio suggested an enhanced utilization efficiency of phosphorus by NSCs, indicating that the reduced phosphorus content might increasingly limit NSC accumulation. At high-elevation regions, increased nutrient limitations may impede the conversion of carbohydrates into nitrogen- and/or phosphorus-based compounds (e.g., amino acids and proteins) and their subsequent translocation from leaves to other plant organs [31]. Nevertheless, this limitation might be indirect or negligible due to the weak correlation between NSCs and phosphorus (Figure 4). Poplar species maintain a balance between source and sink, which remains unaffected by temperature variations associated with changes in elevation. Consistent with previous studies on P. beijingensi, P. alba and Betula albo-sinensis, leaf NSCs exhibited a similar trend of negligible changes with elevation [11,12]. In addition, some studies have reported a decreasing trend in NSCs with elevation [12,39]. These findings suggested that the response of leaf NSCs to elevation might be influenced by a combination of factors, including tree species, habitat conditions, and competition [2,39].
Although the performance of leaf NSCs in both male and female plants of the two species remained consistent, notable differences in NSC contents were observed between male and female plants at the same elevation (Figure 1). Specifically, in P. cathayana, male plants exhibited higher leaf NSC values than female plants at lower elevations, whereas the opposite pattern was observed at higher elevations. Studies have indicated that under conditions of short photoperiods [40] or elevated CO2 concentrations/temperatures [41], male P. cathayana exhibited more NSCs than females. This suggested that male plants might possess greater adaptability and more efficient carbohydrate utilization. The environmental conditions simulated in these studies are analogous to those at the lower and middle elevations in our research, providing a partial explanation for the observed differences in leaf NSC performance between male and female P. cathayana across various elevations. Furthermore, this disparity may be attributed to differential reproductive investments between the sexes, as it is generally accepted that female plants allocate more resources for reproduction. This allocation might result in significantly lower NSC contents in females at lower elevations compared to males. Such reproductive investment may not be advantageous for the performance of female plants under natural conditions and could reduce their stress resistance when resources are scarce [18,19]. Research conducted by Zhang et al. (2014) on P. cathayana plants demonstrated that phosphorus deficiency adversely affected females more than males, leading to a stronger constraint on the growth and subsequent NSCs accumulation in females plants [42]. A similar result was observed in this study. Female P. cathayana exhibited significantly lower leaf phosphorus concentrations compared to male plants and a nitrogen/phosphorus ratio greater than 16 at high elevations (Figure 2 and Figure 3). This suggested a more pronounced phosphorus restriction, which might contribute to the observed differences in plant growth between the sexes, and thus resulted in a significant difference in leaf NSC content. Alternatively, the higher utilization rate of NSCs in males at high elevations might also account for these differences [42]. Nonetheless, it is important to note that such sexual differences may be influenced by various factors, including species, environmental conditions, and the intensity and duration of stress presence [22], which could be manifested in the fact that there was no significant difference in leaf NSCs between the sexes in certain species, such as H. rhamnoides plants. In some cases, female plants, despite being under disadvantaged conditions, showed greater tolerance than males. Females appear to possess stronger capabilities to mitigate the negative effects associated with reproductive investment through compensatory mechanisms [22,43].

4.2. The Responses of Soluble Sugar and Starch to Elevation and Their Sex Differentiation Was Species-Specific

Leaf soluble sugar serves as a direct energy source and plays a crucial role in various physiological and metabolic processes in plants, such as the regulation of cytosol osmotic pressure [32]. It helps maintain the osmotic potential balance within cells and mitigates water loss by modulating its content, thereby protecting cells and maintaining cell membrane stability [44]. We observed a consistent and increasing trend in leaf soluble sugar content in P. cathayana and H. rhamnoides, respectively, supporting the findings from previous studies [10,11]. Increased soluble sugar content at high elevations enhances cytosolic osmotic pressure, providing osmotic protection to plants against frostbite, freezing, and against low temperatures [29,32]. The observed increase in the leaf soluble sugar/phosphorus ratio in both sexes of P. cathayana suggested that the limiting effect of phosphorus content on soluble sugar was enhanced at high elevations. However, consistent with H. rhamnoides, leaf soluble sugar content was not significantly correlated with nitrogen and phosphorus across different elevations.
When the soluble sugar content within a plant is adequate to support growth and development, and metabolic processes, the excess portion can be transformed into starch, which serves as the carbon reservoir in leaves and provides long-term energy storage in plant tissues [3]. Conversely, starch can also be hydrolyzed back into soluble sugars under specific conditions, thereby supplying a stable carbon source that enables plants to cope with environmental stresses and to sustain normal physiological activities [11,45]. Leaf starch in both sexes of H. rhamnoides and in female plants of P. cathayana showed an increasing trend with elevation (Table 2), which has been proposed as a passive response to reduced growth rates and as a strategic reserve to help plants withstand the more challenging environmental conditions encountered at high elevations [46,47]. However, the elevational trend of starch in male leaves of P. cathayana was inconsistent with that observed in females, showing no significant variation with elevation (Table 2). This divergent response to elevation between female and male leaves of P. cathayana resulted in a significantly higher starch concentration in female plants at higher elevations. This might be related to the fact that we observed greater phosphorus deficiency in female leaves at high elevations, which led to a greater starch accumulation compared to males, since we found that leaf starch was significantly correlated with phosphorus content in female plants. A previous study revealed that phosphorus deficiency reduces the triose-phosphate translocator (TPT) and the exchange of plastidic triose phosphate with cytoplasmic solute inorganic orthophosphate (Pi), which in turn leads to an increase in Calvin cycle intermediates within the chloroplasts, thereby increasing starch accumulation [48]. Additionally, phosphorus deficiency induces the upregulation of starch synthase pyrophosphorylase (AGPase) activity, further contributing to starch accumulation [49].
The interconversion of soluble sugar and starch has been recognized as an effective mechanism for plant stress resistance [50]. In response to elevation, the allocation of leaf NSCs to soluble sugar and starch may vary among different plant species, influenced by species specificity [51]. Leaf soluble sugar/starch ratio in male plants of P. cathayana did not change with elevation, whereas that in female plants of P. cathayana and in both sexes of H. rhamnoides showed a decrease with elevation (Table 1). It was significantly correlated with starch content (Figure 4), suggesting an increased partitioning to starch with elevation. This is inconsistent with the majority of previous studies, such as the study of Zhou et al. [6] and Zhou, Shi, Zhang, and Dang [5], who reported a significant increase in leaf soluble sugar/starch ratio with elevation, primarily attributed to an increase in soluble sugar. This result might be related to the fact that enzymes for starch synthesis are much more sensitive to low temperatures than enzymes for sucrose and fructose metabolism [52]. However, previous studies have also pointed out that this trend does not appear to be well-supported in nitrogen-fixing legumes, which may partially explain the increasing trend of leaf soluble sugar/starch ratio observed in H. rhamnoides along the elevation [28]. In contrast, the significant positive correlation between starch and phosphorus in female P. cathayana suggested that phosphorus deficiency may stimulate starch accumulation along the elevation, thereby resulting in a higher proportion of starch in high elevation. This might contribute to the different result of female P. cathayana from most previous studies.
This study aimed to explore the changes in NSCs along an elevation gradient and their relationships with nitrogen and phosphorus concentrations at the leaf level. While we have partially characterized the response of leaves and the interrelationships between traits, further research is necessary to elucidate the distribution of NSCs among different plant organs, the origins of changes in leaf nitrogen and phosphorus, and the influence of soil physicochemical properties for a more comprehensive understanding of the plant carbon source–sink dynamic and its constraints on plant growth across different species and sexes.

5. Conclusions

Leaf NSC content in the two dioecious plants, P. cathayana and H. rhamnoides, did not change and increased significantly with elevation, respectively. The reduced growth requirements due to lower temperatures might be a possible contributor to the enhanced accumulation of NSCs in H. rhamnoides along with elevation. Nevertheless, the balance between NSC supply and demand might have led to the leaf NSCs of P. cathayana remaining unaffected by elevation. Leaf nitrogen and phosphorus concentrations did not significantly influence the leaf NSC content in either plant species. Although the elevational patterns of NSCs in P. cathayana did not exhibit differences between males and females, phosphorus deficiency contributed to the divergent trends in leaf starch between male and female P. cathayana plants with elevation, i.e., an increase at high elevations in females versus unchanged levels across elevations in males. Whether the inconsistent response pattern of leaf NSCs along the elevational gradient in different functional dioecious plants, and the differences in NSC values between males and females of the non-nitrogen-fixing P. cathayana plants along elevation, are attributed to differences in nitrogen-fixing capacity require further elucidation through more comprehensive and multi-scale studies.

Author Contributions

Conceptualization, methodology, investigation, writing—original draft, J.W.; Methodology, investigation, writing—original draft, S.L.; Methodology, investigation, Q.F.; Investigation, X.C. and H.X.; Conceptualization, writing—review and editing, Z.S.; Funding acquisition, Z.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (Grant No. 31570240 and 32171506).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We sincerely thank Zhenlin Fan of the Chinese Academy of Natural Resource Economics for his help in revising the paper.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. The contents of leaf NSCs (A), starch (B), soluble sugar (C), and soluble sugar/starch ratio (D) for male and female plants of P. cathayana and H. rhamnoides at different elevations. PE, elevation effect; PS, sex effect; PE×S, interaction effect of elevation and sex. Different lowercase and uppercase letters above the bars indicate significant differences (p < 0.05) among elevations for male and female leaves, respectively. Asterisks designate significant differences (p < 0.05) between male and female leaves at the same elevation. *, **, and *** indicate significant differences at the p < 0.05, p < 0.01, and p < 0.001 levels, respectively, and “ns” denotes no significant difference.
Figure 1. The contents of leaf NSCs (A), starch (B), soluble sugar (C), and soluble sugar/starch ratio (D) for male and female plants of P. cathayana and H. rhamnoides at different elevations. PE, elevation effect; PS, sex effect; PE×S, interaction effect of elevation and sex. Different lowercase and uppercase letters above the bars indicate significant differences (p < 0.05) among elevations for male and female leaves, respectively. Asterisks designate significant differences (p < 0.05) between male and female leaves at the same elevation. *, **, and *** indicate significant differences at the p < 0.05, p < 0.01, and p < 0.001 levels, respectively, and “ns” denotes no significant difference.
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Figure 2. The concentrations of nitrogen (A) and phosphorus (B), and the nitrogen/phosphorus ratio (C) for male and female P. cathayana and H. rhamnoides plants at different elevations. PE, elevation effect; PS, sex effect; PE×S, interaction effect of elevation and sex. The bars are the standard errors of the means. Different lowercase or uppercase letters above the bars indicate significant differences (p < 0.05) among elevations for male and female leaves, respectively. * designate significant differences (p < 0.05) between male and female leaves at the same elevation. *** indicate significant differences at the p < 0.001 levels, and “ns” denotes no significant difference.
Figure 2. The concentrations of nitrogen (A) and phosphorus (B), and the nitrogen/phosphorus ratio (C) for male and female P. cathayana and H. rhamnoides plants at different elevations. PE, elevation effect; PS, sex effect; PE×S, interaction effect of elevation and sex. The bars are the standard errors of the means. Different lowercase or uppercase letters above the bars indicate significant differences (p < 0.05) among elevations for male and female leaves, respectively. * designate significant differences (p < 0.05) between male and female leaves at the same elevation. *** indicate significant differences at the p < 0.001 levels, and “ns” denotes no significant difference.
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Figure 3. The ratios of soluble sugar/nitrogen (A), soluble sugar/phosphorus (B), starch/nitrogen (C), starch/phosphorus (D), NSCs/nitrogen (E), and NSC/phosphorus (F) of male and female P. cathayana and H. rhamnoides plants at different elevations. The bars are the standard errors of the means. PE, elevation effect; PS, sex effect; PE×S, interaction effect of elevation and sex. The bars are the standard errors of the means. Different lowercase or uppercase letters above the bars indicate significant differences (p < 0.05) among elevations for male and female leaves, respectively. Asterisks designate significant differences (p < 0.05) between male and female leaves at the same elevation. *, **, and *** indicate significant differences at the p < 0.05, p < 0.01, and p < 0.001 levels, respectively, and “ns” denotes no significant difference.
Figure 3. The ratios of soluble sugar/nitrogen (A), soluble sugar/phosphorus (B), starch/nitrogen (C), starch/phosphorus (D), NSCs/nitrogen (E), and NSC/phosphorus (F) of male and female P. cathayana and H. rhamnoides plants at different elevations. The bars are the standard errors of the means. PE, elevation effect; PS, sex effect; PE×S, interaction effect of elevation and sex. The bars are the standard errors of the means. Different lowercase or uppercase letters above the bars indicate significant differences (p < 0.05) among elevations for male and female leaves, respectively. Asterisks designate significant differences (p < 0.05) between male and female leaves at the same elevation. *, **, and *** indicate significant differences at the p < 0.05, p < 0.01, and p < 0.001 levels, respectively, and “ns” denotes no significant difference.
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Figure 4. Correlations between the contents of leaf soluble sugar, starch, nitrogen, and phosphorus and soluble sugar/starch and nitrogen/phosphorus in male and female P. cathayana and H. rhamnoides plants. Asterisks denote the following: *, 0.01 < p < 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.
Figure 4. Correlations between the contents of leaf soluble sugar, starch, nitrogen, and phosphorus and soluble sugar/starch and nitrogen/phosphorus in male and female P. cathayana and H. rhamnoides plants. Asterisks denote the following: *, 0.01 < p < 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.
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Table 1. Growth conditions and characteristics of the sampling trees.
Table 1. Growth conditions and characteristics of the sampling trees.
Elevation
(m a.s.l)		Slope
(°)		Slope
Exposure		Mean Air
Temperature (°C) *		Precipitation
(mm) *		Height (m)Diameter (cm)Vegetation
Type
MaleFemaleMaleFemale
Populus cathayana
180015.2SE16.9715.914 ± 215 ± 233.1 ± 4.935.8 ± 3.5BLF
220012.6S14.2636.018 ± 219 ± 236.1 ± 2.936.6 ± 3.3BLF
260016.3SE12.4645.019 ± 120 ± 238.9 ± 6.635.2 ± 3.3CBF
310013.7S9.4667.718 ± 120 ± 335.7 ± 2.834.7 ± 4.4CBF
Hippophae rhamnoides
19004.0S14.7770.07 ± 17 ± 112.6 ± 3.515.7 ± 4.3BLF
25008.5S11.7651.76 ± 28 ± 312.9 ± 1.914.7 ± 3.0CBF
31009.4SE8.6675.77 ± 17 ± 213.6 ± 5.012.5 ± 2.8CBF
37006.8S6.5696.06 ± 25 ± 314.9 ± 4.813.8 ± 5.5SL
* The data were collected during the growing season. The data for height and diameter were means ± standard deviations. BLF, broad-leaved forest; CBF, coniferous and broad-leaved mixed forest; SL, shrubland.
Table 2. Linear regression relationships of leaf NSCs, starch, soluble sugar, and soluble sugar/starch with elevation in male and female P. cathayana and H. rhamnoides plants.
Table 2. Linear regression relationships of leaf NSCs, starch, soluble sugar, and soluble sugar/starch with elevation in male and female P. cathayana and H. rhamnoides plants.
Populus cathayanaHippophae rhamnoides
pR2Regression EquationspR2Regression Equations
Soluble sugarMale---0.0010.384y = 15.985 + 0.002x
Female---0.0030.381y = 15.490 + 0.002x
ANCOVA-
StarchMale---0.0030.330y = 1.849 + 0.001x
Female<0.0010.516y = −0.619 + 0.003x0.0060.335y = 1.432 + 0.0016x
ANCOVA-
NSCsMale---0.0010.402y = 17.835 + 0.003x
Female---0.0010.421y = 16.922 + 0.003x
ANCOVA-
Soluble sugar/starchMale---0.0070.287y = 7.131 − 0.001x
Female0.0020.423y = 7.417 − 0.001x0.0370.209y = 7.770 − 0.001x
ANCOVA-
Table 3. Linear regression relationship of leaf nitrogen, phosphorus, and nitrogen/phosphorus ratio with elevation in male and female P. cathayana and H. rhamnoides plants.
Table 3. Linear regression relationship of leaf nitrogen, phosphorus, and nitrogen/phosphorus ratio with elevation in male and female P. cathayana and H. rhamnoides plants.
Populus cathayanaHippophae rhamnoides
pR2Regression EquationspR2Regression Equations
NitrogenMale0.0400.253y = 32.909 − 0.003x<0.0010.446y = 23.641 + 0.003x
Female---0.0040.361y = 19.761 + 0.004x
ANCOVA-
PhosphorusMale<0.0010.594y = 3.281 − 0.001x<0.0010.619y = 0.562 + 0.001x
Female<0.0010.841y = 2.486 − 0.0005x<0.0010.577y = −0.311 + 0.001x
ANCOVA<0.001
Nitrogen/phosphorusMale0.0120.351y = 7.398 + 0.003x<0.0010.580y = 24.365 − 0.003x
Female<0.0010.631y = 1.803 + 0.008x<0.0010.732y = 27.447 − 0.004x
ANCOVA-
Table 4. Linear regression analysis of leaf soluble sugar/nitrogen, starch/nitrogen, NSCs/nitrogen, soluble sugar/phosphorus, starch/phosphorus, and NSCs/phosphorus ratios with elevation in male and female P. cathayana and H. rhamnoides plants.
Table 4. Linear regression analysis of leaf soluble sugar/nitrogen, starch/nitrogen, NSCs/nitrogen, soluble sugar/phosphorus, starch/phosphorus, and NSCs/phosphorus ratios with elevation in male and female P. cathayana and H. rhamnoides plants.
Populus cathayanaHippophae rhamnoides
pR2Regression EquationspR2Regression Equations
Soluble sugar/nitrogenMale------
Female------
ANCOVA-
Starch/nitrogenMale------
Female<0.0010.600y = −0.052 + 0.0001x---
ANCOVA-
NSCs/nitrogenMale------
Female------
ANCOVA-
Soluble sugar/phosphorusMale<0.0010.537y = 4.467 + 0.005x0.0060.294y = 158.539 − 0.017x
Female<0.0010.692y = 3.511 + 0.006x0.0100.303y = 192.596 − 0.027x
ANCOVA0.008
Starch/phosphorusMale------
Female<0.0010.711y = −6.520 + 0.005x---
ANCOVA-
NSCs/phosphorusMale0.0080.380y = 6.711 + 0.006x0.0210.221y = 181.875 − 0.018x
Female<0.0010.720y = −3.009 + 0.011x0.0280.229y = 221.154 − 0.029x
ANCOVA-
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Wu, J.; Liu, S.; Feng, Q.; Cao, X.; Xing, H.; Shi, Z. Response of Leaf Non-Structural Carbohydrates to Elevation in Dioecious Plants, Populus cathayana and Hippophae rhamnoides. Forests 2025, 16, 246. https://doi.org/10.3390/f16020246

AMA Style

Wu J, Liu S, Feng Q, Cao X, Xing H, Shi Z. Response of Leaf Non-Structural Carbohydrates to Elevation in Dioecious Plants, Populus cathayana and Hippophae rhamnoides. Forests. 2025; 16(2):246. https://doi.org/10.3390/f16020246

Chicago/Turabian Style

Wu, Jiamei, Shun Liu, Qiuhong Feng, Xiangwen Cao, Hongshuang Xing, and Zuomin Shi. 2025. "Response of Leaf Non-Structural Carbohydrates to Elevation in Dioecious Plants, Populus cathayana and Hippophae rhamnoides" Forests 16, no. 2: 246. https://doi.org/10.3390/f16020246

APA Style

Wu, J., Liu, S., Feng, Q., Cao, X., Xing, H., & Shi, Z. (2025). Response of Leaf Non-Structural Carbohydrates to Elevation in Dioecious Plants, Populus cathayana and Hippophae rhamnoides. Forests, 16(2), 246. https://doi.org/10.3390/f16020246

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