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Article

Differences in the Functional Traits of Populus pruinosa Leaves in Different Developmental Stages

by
Juntuan Zhai
,
Xiao Zhang
,
Zhijun Li
*,
Xiaoli Han
and
Shanhe Zhang
Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin of Xinjiang Production & Construction Corps, College of Life Science and Technology, Tarim University, Alar 843300, China
*
Author to whom correspondence should be addressed.
Plants 2023, 12(12), 2262; https://doi.org/10.3390/plants12122262
Submission received: 25 April 2023 / Revised: 3 June 2023 / Accepted: 6 June 2023 / Published: 9 June 2023
(This article belongs to the Special Issue Phytomorphology, Anatomy and Ultrastructure)
Browse Figures
Versions Notes

Abstract

:
Populus pruinosa Schrenk has the biological characteristics of heteromorphic leaves and is a pioneer species for wind prevention and sand fixation. The functions of heteromorphic leaves at different developmental stages and canopy heights of P. pruinosa are unclear. To clarify how developmental stages and canopy height affect the functional characteristics of leaves, this study evaluated the morphological anatomical structures and the physiological indicators of leaves at 2, 4, 6, 8, 10, and 12 m. The relationships of functional traits to the developmental stages and canopy heights of leaves were also analyzed. The results showed that blade length (BL), blade width (BW), leaf area (LA), leaf dry weight (LDW), leaf thickness (LT), palisade tissue thickness (PT), net photosynthetic rate (Pn), stomatal conductance (Gs), proline (Pro), and malondialdehyde (MDA) content increased with progressing developmental stages. BL, BW, LA, leaf dry weight, LT, PT, Pn, Gs, Pro, and the contents of MDA, indoleacetic acid, and zeatin riboside had significant positive correlations with canopy heights of leaves and their developmental stages. The morphological structures and physiological characteristics of P. pruinosa leaves showed more evident xeric structural characteristics and higher photosynthetic capacity with increasing canopy height and progressive developmental stages. Resource utilization efficiency and the defense ability against environmental stresses were improved through mutual regulation of each functional trait.

1. Introduction

With the frequent occurrence of global climate change and extreme climate change events, it is particularly important to cultivate plants with wide adaptability to cope with the constantly changing environment using effective methods [1]. Functional traits are attributes of plants, including phenotype, anatomical structure, physiological function, and other traits, that have significant impacts on plant growth and reproduction [2,3,4]. If the change range of plant functional traits is greater, then the plant will be more able to adapt to the complex and changeable environment [5,6], providing more choices of functional traits to study.
Variations in the functional traits of the same species can increase the competitiveness of the species [7]; such variations show differences at different ages to maximize the effective use of limited resources and avoid intraspecific competition [8,9]. The leaf is the organ most easily affected by environmental changes and can best reflect the functions of plants and their adaptability to the environment [5,10,11,12]. As they are the main carbon source of plants, changes in functional traits of leaves play an irreplaceable role in adapting to environmental stress [13,14,15,16]. Regardless of gymnosperms or angiosperms [17,18,19,20], specific leaf weight increases with increasing tree age, which may be due to the vulnerability of the leaves of older trees to water stress [21,22,23]. Eucalyptus regnans F. Muell. leaves become more polymorphic with increasing tree age and height; Sabina vulgaris Ant. has two leaf forms, scaly leaf and needle leaf, which are different in morphology and physiological characteristics, and the scaly leaf has higher drought resistance than the needle leaf [24]. Significant differences in leaf morphology, structure, and physiological functions of Populus euphratica Olivier occur at different developmental stages, and tree height gradients vary at the same developmental stage; these differences are related to the individual developmental stage and the crown position [25]. For P. euphratica, on the same individual, broad-ovate leaves in the upper part of the canopy have larger leaf area and leaf thickness and more developed xerophytic structures than the lanceolate leaves of the lower part [25,26]. Kenzo et al. (2015) studied 104 species in 29 families of trees in the Borneo rainforest and found that a significant linear relationship exists between leaf morphology, biochemical characteristics, and tree height [27]. Leaf structure exhibits significant differences at different tree heights, and as the tree height increases, the leaf structure exhibits more pronounced xerophytic characteristics [28]. Various studies have shown that leaf function traits are closely related to tree age and canopy height [29,30,31]. At the same time, drought has a certain impact on leaf functional traits. For morphological responses, leaf size and leaf mass area decrease in drought conditions; on the other hand, as for physiological responses, drought stress decreases the maximum photosynthesis rate and the electron transfer rate of the leaf [32]. In addition, the morphological and anatomical characteristics of leaves are closely related to physiological traits [33]; leaves with thicker Palisade cells and spongy tissue will generally show stronger photosynthetic capacities [32,33].
Populus pruinosa Schrenk belongs to the genus Populus L. of Salicaceae. It is distributed on desert riversides in the arid and semi-arid regions of the world and is an excellent tree species for wind prevention, sand fixation, and water and soil conservation. The anatomical structures of P. pruinosa leaves become more obvious with progressive developmental stages and increasing canopy height [26,34]. However, the relationship between the functional traits (morphology, structure, photosynthetic water physiology, osmotic substances, and endogenous hormone content) of P. pruinosa leaves and tree age is still unclear. Therefore, we hypothesized that there are significant differences in the functional traits of P. pruinosa leaves at different developmental stages and the changing trend is different with the increase in canopy height. The present study aims to provide a multifaceted measurement to understand the changes in the leaf functional traits of P. pruinosa in each canopy with increasing tree age and clarify the relationships between leaf functional traits and growth and development. The results provide insights into the growth of P. pruinosa in the desert riverside.

2. Results

2.1. Changes in the Morphological Characteristics of Leaves

The BL, BW, LA, and LDW increased and LI decreased with increasing diameter class, and a substantial difference was observed between classes 20 and 8 (Figure 1). From diameter classes 8 to 20, the BL, BW, LA, and LDW increased by 12.77%, 42.72%, 64.59%, and 75.19%, respectively, whereas the LI decreased by 14.16%. Among the diameter classes, the BW, LA, and LDW of class 20 were the largest, and the LI was the smallest. Class 8 had the largest SLA, which was 86.24 cm2/g, and class 12 had the smallest SLA, which was 12.05% smaller than the former. The BL, BW, LA, and LDW gradually increased with increasing leaf height (Figure 1).

2.2. Changes in Anatomical Structure Characteristics of Leaves

After a comparison of the anatomical structure characteristics of each diameter class (Figure 2), we found that the LT and PT in classes 8 to 20 increased by 5.05% and 21.79%, respectively, and the difference was significant. The VBA, LT, PT, and MXA of the other diameter classes, except class 8, of leaves increased with increasing leaf height and at the highest leaf height (Figure 2). A significant difference existed between the layer and the 2 m leaf height. From the lowest leaf height to the highest leaf height, the largest increases in the MVBA and the MXA appeared in class 20, of 73.99% and 113.5%, respectively, while the largest increase in the LT, of 72.74%, appeared in class 16. The PT increased by 36.77%, 27.29%, 29.49%, and 36.12%, respectively, from class 8 to class 20. The MVBA and the LT appeared in class 16, with values of 70,175.42 and 323.33 µm, respectively; class 20 had the largest MXA, of 23,607.83 µm, which was significant and considerably larger than that of class 8.

2.3. Changes in Photosynthetic Physiological Parameters of Leaves

Through comparison of light and abilities of leaves from different diameter classes (Figure 3), we found that the Pn and the Gs increased by 37.54% and 41.5% from class 8 to 20, respectively, and the difference was significant. No significant difference in Tr was detected among the diameter classes, but the Ci of class 20 was significantly higher than those of classes 8, 12, and 16. The Pn, Tr, and Gs values of the leaves of each diameter class gradually increased with increasing leaf height; the difference between the highest leaf height of each diameter class and the 2 m leaf height was significant, whereas the Ci showed a decreasing trend (Figure 3). The difference between the highest leaf height of class 16 and the 2 m leaf height was significant. For example, in diameter class 20, the Pn, Tr, and Gs increased by 9.94%, 54.25%, and 18.97%, respectively, from 2 m to 12 m. The largest increase in Gs, of 48.18%, occurred in class 8. The Ci decreased the most in class 16, by 30%.

2.4. Changes in Water Use Efficiency of Leaves

By comparing the water use efficiencies of different diameter classes (Figure 3), we found no significant difference in the δ13C value among the diameter classes, whereas the WUEi increased with the diameter class, to 36.56% higher than that of the former. The δ13C of the leaves increased with the leaf height in class 20. From 2 m to 12 m, the δ13C increased by 2.01%; the difference between the highest leaf height and the 2 m leaf height was significant (Figure 4). The increase in the WUEi with the leaf height showed a decreasing trend from 2 m to 12 m, with a corresponding decrease of 26.6%. The difference between the highest leaf height and the 2 m leaf height was significant.

2.5. Changes in Physiological Characteristics of Leaves

The comparison of the proline and malondialdehyde contents in leaves of different diameter classes (Figure 5) shows that the contents of Pro and MDA increased by 31.71% and 22.93% from class 8 to class 20, respectively. The difference in class 8 was significant; the Pro values of classes 16 and 20 were significantly higher than those of classes 8 and 12. The MDA contents of classes 12, 16, and 20 was significantly higher than that of class 8. In each diameter class, the leaf Pro and MDA contents increased with increasing leaf height, and the difference between the highest leaf height and the 2 m leaf height in each diameter class was significant (Figure 5). From 2 m to the highest leaf height, the largest increase in Pro appeared in class 12, with a value of 83.88%, while the greatest increase in the MDA content appeared in class 16, with a value of 51.03%.

2.6. Changes in Endogenous Hormones Content of Leaves

After comparing the contents of endogenous hormones in leaves of different diameter classes (Figure 6), we found that the contents of IAA and ZR showed an increasing trend with increasing diameter class; meanwhile, the content of ABA showed a decreasing trend. From class 8 to class 20, the ABA content decreased by 27.45%, while the contents of IAA and ZR increased by 15.31% and 15.81%, respectively, and the maximum values of IAA and ZR appeared in class 16, with values of 51.95 and 12.95 ng/g·FW, respectively, and were considerably larger than the rest. In each diameter class, the contents of endogenous hormones GA3, IAA, and ZR in heteromorphic leaves increased with increasing leaf height; by contrast, the ABA content decreased with increasing leaf height, and the differences among layers were significant (Figure 6). With increasing leaf height, the maximum decrease in the ABA content appeared in class 12 (46.48%), whereas the maximum increases in the GA3 and ZR contents appeared in class 16 (79.28% and 72.87%, respectively). From class 8 to class 20, from the lowest leaf height to the highest leaf height, the IAA content increased by 53.01%, 24.27%, 36.4%, and 65.21%, respectively.

2.7. Relationship between the Functional Characteristics of Leaves

According to the linear fitting of leaf traits of different diameter classes with tree height, we found that the BL, BW, LA, LDW, MVA, LT, PT, Pro, GA3, IAA, and ZR values of the four diameter classes increased linearly with increasing tree height (p < 0.05, Figure 7a–c,e, Figure 8b–d, and Figure 9a,d–f). The ABA decreased linearly with tree height (p <0.05, Figure 9c). The difference is that the leaf traits of LI, MVBA, and MDA only had no significant relationship to tree height in the 8th diameter class (Figure 7d,e and Figure 8b). At the same time, we found that the change rate of most leaf traits in diameter classes 8 and 12 was faster with increasing tree height. The BW, LA, LDW, MVBA, MVA, and MDA changed fastest in diameter class 12 (p < 0.05, Figure 7b,c,e, Figure 8a,b, and Figure 9b), while the LT, the PT, and hormone characteristics GA3, IAA, and ZR changed the fastest in diameter class 8 (p < 0.05, Figure 8c,d and Figure 9d–f).
Based on correlation analysis according to different diameter classes (Figure S1), the BL, BW, LA, LDW, LT, GA3, IAA, and ZR in the four diameter orders were significantly positively correlated with tree height; the ABA was significantly negatively correlated with tree height. The difference is the lack of significant correlation between the MVBA, the MXA, and tree height in diameter class 8, while a significant positive correlation exists between the MVBA and MXA values with tree height in diameter classes 12, 16, and 20.
Overall, the BL, BW, LA, LDW, Pn, Gs, Ci, WUEi, and Pro correlated significantly with diameter class, and the contents of δ13C and ABA had significant negative correlations (Figure S2); the BL, BW, LA, LDW, MVBA, MXA, LT, PT, Pn, Tr, Gs, Pro, MDA, GA3, IAA, and ZR had significant correlations with leaf height, whereas the LI and ABA contents correlated significantly with leaf height. In addition, the contents of GA3, IAA, and ZR correlated significantly positively with the contents of Pro and MDA, whereas the content of ABA correlated significantly negatively with the latter and leaf height and diameter class had significant interactive effects on it. The results show that heteromorphic leaf functional traits are closely related to developmental stages, the canopy heights of leaves, and the relationship between the two. The first two axes of the PCA explain 50.1% of the total variance of the studied leaf traits in four P. pruinosa diameter classes (Figure 10). In these four diameter classes of leaves, the PC1 was strongly influenced by the BL, LA, LT, PT, ABA, and ZR, while the PC2 was strongly influenced by the δ13C, WUEi, LDW, Ci, and MDA. In addition, Figure 10 shows the high contents of ABA and LI in diameter classes 8 and 12, respectively, with high Pn, Gs, PT, LT, LA, IAA, and ZR values in diameter classes 16 and 20.

3. Discussion

3.1. Differences in and Relationships of Leaves’ Functional Traits at Different Developmental Stages

Differences in the special adaptive structures and functions of leaves may be caused in the same species under different ecological conditions or related to the crown position and the growth stage [19,24,28,35]. Differences in the morphologies and physiological characteristics of the scale and needle leaves of Sabina vulgaris are related to the growth stage. At the seedling stage, they grow under the canopy and only have needle leaves, whereas mature individuals grow in an open environment with needle and scale leaves. Compared with needles, scale leaves have a larger LMA, a higher leaf area photosynthetic rate, higher water use efficiency, and stronger resistance to photoinhibition [24]. Another typical case related to differences in leaf morphologies and physiological characteristics related to the crown position and the growth stage is the study of the morphologies and physiological characteristics of the heteromorphic leaves of P. euphratica. Significant differences existed in the morphological structures and physiological functions and are related to the ontogeny stage and the coronal position [25]. This finding revealed the differences in the types and functions of the heteromorphic leaves of P. euphratica at different developmental stages. The morphological and anatomical structures of the heteromorphic leaves of P. euphratica, such as the LA, LT, LDW, and PT, increased with increasing diameter class, and all correlated significantly with the diameters, at breast height, at different developmental stages. With age, the factor of heterogeneity of microenvironments and the factor of competition were more strongly pronounced [14]. The results of this study were similar to those for P. euphratica. The differences in the morphologies, structures, and physiological functions of heteromorphic leaves of P. pruinosa are related to developmental stages. The LA, Pn, Gs, WUEi, and Pro correlated significantly with diameter class, and the contents of δ13C and ABA correlated significantly negatively (Figure S2). Leaf area expansion is closely related to some major plant physiological events [36], such as photosynthesis, transpiration, and carbon flow, which are considered important requirements to enlarge light harvesting [37]. In the leaves of low-diameter P. pruinosa, where LA is small, as a P. pruinosa individual grows, more energy is needed to sustain nutritional growth and also to allocate energy to reproductive organs, such as flowers and seeds, which require individual trees to increase their productivity. With the large-diameter class of P. pruinosa, the LA was relatively large, the photosynthetic ability was strong, and the changes in the contents of Pro, MDA, and endogenous hormones also provided infiltration conditions for the water supply.

3.2. Differences in Functional Traits of Leaves at Different Canopy Heights and the Relationship to Canopy Height

Leaves represent highly plastic structures that respond to environmental gradients existing in plant canopies [38,39]. Differences in special adaptive structures and functions of leaves in woody plants are not only related to the growth stage but also to the coronal part [19,28]. Leaf morphology and physiological and biochemical characteristics vary with tree height, owing to changes in light availability and evapotranspiration requirements during ontogeny [40]. Leaf morphological structure exhibits more apparent xerophytic characteristics with increasing canopy height [25,28]. For example, to cope with the water stress caused by tree height, the leaf area of Parashorea chinensis Wang Hsie decreases with increasing tree height, and the palisade structure increases with increasing tree height. Such increases exhibit stronger xerophyte structures [28]. The proportions of scales and needles of Sabina vulgaris in the canopy of mature individuals changed significantly with a change in canopy position, and the scales at the top of the canopy had a higher photosynthetic rate, a stronger photosystem I capacity, and higher carbon in the light-saturated state, as well as a higher isotope ratio (δ13 C) and a higher water use efficiency than the needles [24]. Studies on Eucalyptus amygdalina F. Muell. found that the area of transpiration and photosynthesis decreased with increasing tree age and height in response to water stress [19]. Narayan’s research on apple quality showed that the net photosynthetic rate of the low canopy was lower than that of the high canopy, but after treatment with summer pruning and installation of reflective film, the net photosynthetic rate of the low canopy was significantly increased due to the increased amount of light, thereby improving the fruit quality [41]. The morphology, anatomical structure, and physiological characteristics of the heteromorphic leaves of Populus euphratica Olivier are related to the ontogeny stage and the coronal position. With increasing canopy height, the leaf area, leaf thickness, specific leaf weight, palisade tissue thickness, net photosynthetic rate, transpiration rate, stomatal conductance, and proline and malondialdehyde contents of the sampled height increased and correlated significantly positively with that height [25]. The LA, LDW, MVBA, LT, PT, net Pn, Tr, Gs, ABA, and MDA and endogenous hormones GA3, IAA, and ZR increased with increasing leaf height and correlated significantly positively with it. Within forest canopies, environmental gradients exist and enhance water losses in the direction of the treetops [42]. A range of anatomical traits (xylem cross-sectional area, number and dimensions of xylem conduits, leaf thickness, etc.) modulate the efficiency of water transfer from the stem xylem through the petiole, the veins, and the extravascular paths to the guard and mesophyll cells [43,44,45,46]. Increases in leaf area, leaf thickness, and palisade cells increase the photosynthetic area and the thickness of the palisade cell as the leaf height increases, leading to the enhancement of the photosynthetic capacity [33]. δ13C is the proxy of WUE and plant water relations and a useful method to determine drought resistance to provide insights into the chemical, physical, and metabolic processes involved in carbon transformation in stressed plants, which determines the water utility and water conservation status for the forest seedlings [32]. Narayan’s study on Prunus sargentii Rehder and Larix kaempferi Carr. seedlings under drought stress discovered that δ13C showed a decreasing trend [32], but our study found that in the leaves of P. pruinosa, there was no significant difference in δ13C among different canopies and developmental stages, possibly because the environmental conditions were not enough to cause significant changes in δ13C. As the leaf height increased, the productivity and water transport efficiency of P. pruinosa increased, as well as the abilities to obtain and use nutrients and fix carbon; as such, more photosynthetic products were used to build defense tissues and accumulate dry matter. Changes in the anatomical structure and osmoregulatory substances enhanced water storage in the body, maintained water balance, and enhanced defense against environmental stresses by regulating the leaf area, growth rate, and nutrient storage; reducing water loss; and enhancing drought tolerance.
Tree growth results in longer vertical water-conducting paths from the roots to the canopy, requiring a greater pulling force and greater moisture gradients [47]. In higher plants, water stress induces accumulation of osmotic regulators such as proline (Pro) and malondialdehyde content (MDA) [48]. Hormones can also induce accumulation of soluble osmotic substances by regulating the intracellular metabolism and enhancing the survival of plants under stress [49,50]. Our results showed that with increasing leaf height of P. pruinosa of different developmental stages, the contents of the osmotic regulator proline and the growth hormones GA3, IAA, and ZR increased significantly, while the ABA content decreased significantly. With increased tree height, the leaves at the top of the canopy need a stronger osmotic regulation ability to enhance the power of water absorption. An increase in endogenous hormone content can induce accumulation of osmotic regulatory substances. This synergistic effect provides a strong osmoregulation ability. When plants are under stress, an increase in ABA content reduces leaf stomatal conductance, transpiration water loss, and CO2 absorption and fixation, which has a certain inhibitory effect on plant growth [51]. In contrast to our results, the ABA contents of P. pruinosa of different diameter classes decreased significantly with increasing tree height. This decrease may be caused by an increase in the transpiration rate, and the synergistic changes of endogenous hormones and osmoregulatory substances play an important role in maintaining water balance.

4. Materials and Methods

4.1. Study Area

The study area, located in the northwestern margin of the Tarim Basin in Xinjiang Province of China (81°17′56.52″ E, 40°32′36.90″ N, 980 m a.s.l.), has a typical temperate desert climate. The average annual rainfall is approximately 50 mm, the potential evaporation reaches up to 1900 mm, the yearly average temperature is 10.8 °C, and the average annual sunshine duration is 2900 h. The P. euphratica and P. pruinosa mixed forest at the study site covers an area of 180.6 ha, with a groundwater level of 1.5 m.

4.2. Experimental Design and Sampling

The diameter at breast height is 4 cm, which is the class, and the four diameter classes of 8 (5.9–9.9 cm), 12 (10–13.9 cm), 16 (14–17.9 cm), and 20 (18–21.9 cm) represent different developmental stages (tree age). Five sample trees with uniform crowns were selected from each diameter class, with a total of 20 trees (Table 1). The diameter class represents the developmental stage, and the leaf height represents the height of the canopy where leaves are located. Leaf samples were collected from the Populus pruinosa forest of Tarim University and stored in the Key Laboratory of Tarim University (voucher numbers: 2019-Populus pruinosa- [8/12/16/20]) (Table S1).
Sampling points were selected from the trunk bases of the sampled trees along the tree height (H) at 2 m intervals. The points were distributed at 2, 4, 6, 8, 10, and 12 m from the sample trees, as well as the height of the heteromorphic leaves in the vertical space of the canopy. At each sampling point, 1-year-old branches were collected from four directions (east, south, west, and north). A total of 30 branches were collected at each point, and leaves were collected at the fourth nodes from the bases of the branches to analyze the morphology, anatomy, dry mass, δ13C, and concentrations of proline (Pro) and malondialdehyde (MDA). The leaves used for the analyses of Pro, MDA, and the endogenous hormones were stored in liquid nitrogen after collection.

4.3. Measurements of Leaf Morphological and Anatomical Parameters

There were 18 sampling sites in 4 developmental stages. A total of 30 branches were collected at each point, and leaves were collected at the fourth nodes from the bases of the branches to analyze morphology. We used the blade length-to-width ratio (leaf index) to assess changes in leaf shape. Blade length (BL), blade width (BW), and leaf area were measured using using a SCANNER (MRS-9600TFU2, Shanghai, China) and LA-S plant image analysis software. The leaf index was calculated using the blade length/blade width ratio.
A total of 4 branches were collected at each point, and leaves were collected at the fourth nodes from the bases of the branches to analyze anatomical parameters (n = 360). The blade was cut transversely at its widest point. The material that retained the primary vein and leaf margin was fixed in a formalin–acetic acid–alcohol (FAA) solution. Tissue sections were prepared as 8 µm-thick paraffin sections, double-stained with saranine–fast green, and mounted in a neutral resin. The main vein vascular bundle area, main vein xylem area, leaf thickness, and palisade tissue thickness were measured using a Leica microscope (Leica DM4 B, Wetzlar, Germany). Five fields of view were observed for each leaf, and 20 values were obtained for each field of view. The average values of the leaf structural parameters in the five fields of view were collected as anatomical parameters [25].

4.4. Measurement of Leaf Dry Mass

After leaf morphology treatment, the samples were placed in a preheated oven. The oven temperature was increased to 105 °C to deactivate the samples for 10 min. The oven temperature was then lowered to 65 °C, at which the samples were dried to a constant weight. Paper bags containing the material were removed and placed in a desiccator. After cooling to room temperature, the samples were weighed using an electronic balance (0.001 g). Leaf mass per area (LMA) was calculated based on leaf area and dry mass.

4.5. Measurement of Leaf Photosynthesis

A total of 4 branches were collected at each point, and leaves were collected at the fourth nodes from the bases of the branches to analyze photosynthesis parameters (n = 360). One-year-old branches were collected with pruning shears and immediately wrapped in plastic wrap to cover the incisions. Photosynthetic gas exchange characteristics were measured with a portable photosynthesis system, LI-COR 6400XT (LI-COR, Lincoln, NE, USA), for each fourth fully expanded leaf between 09:00 a.m. and 12:00 a.m. on 20 and 28 July 2019. The light-saturated net photosynthesis rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr) were measured under the following conditions: leaf temperature, 25 °C; relative air humidity, 60%; ambient CO2 concentration, 400 ± 5 μmol CO2 mol−1; and photosynthetic photon flux density, 1250 μmol m−2 s−1. The instantaneous water use efficiency (WUEi) of the leaves was calculated as WUEi = Pn/Tr. Ten leaves from each sampling point were measured in triplicate [25].

4.6. Measurement of Stable δ13C

The leaves collected at each sampling point were kept separately in paper bags and placed in a preheated oven; the samples were immediately rinsed with distilled water and deactivated in an oven at 105 °C (n = 270). The samples were oven-dried at 60 °C for 48 h to a constant weight. The dried samples were pulverized using a pulverizer and passed through a 90-mesh sieve. The carbon isotope composition of the purified gas was analyzed using a stable gas isotope mass spectrometer (Thermo Fisher Scientific, Inc., Waltham, MA, USA). Additional details are described by Zhai et al. [25].

4.7. Measurement of MDA and Pro Concentrations

The leaves (without petioles) at the fourth nodes of the branches were collected, quickly frozen with liquid nitrogen and stored at −80 °C (n = 270). The acid ninhydrin method was used to determine the leaf proline content (µg/g). The MDA content (µmol/g) was determined with the thiobarbituric acid color method. Additional details are described by Zhai et al. [25].

4.8. Measurement of Hormone Content

An enzyme-linked immunoassay was used to determine the contents of abscisic acid (ABA), gibberellin (GA3), indoleacetic acid (IAA), and zeatin riboside (ZR) at China Agricultural University.

4.9. Statistical Analysis

Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS, Chicago, IL, USA) version 18.0. All data were checked for normality and homogeneity of variances and log-transformed to correct deviations from these assumptions when necessary. Tukey HSD tests were conducted to detect significant differences among the treatments. Two-factor analysis of variance (ANOVA) was performed to analyze the effects of canopy height, DBH, and their interactions. All differences were considered statistically significant at p < 0.05.

5. Conclusions

The morphological structures and physiological characteristics of the heteromorphic leaves of P. pruinosa had evident canopy height gradient differences in each diameter class, and the leaf morphological structures and physiological characteristics showed more apparent xerophytic structure characteristics with advancing developmental stages and increasing canopy height gradients. P. pruinosa heteromorphic leaves are used to maintain material and energy requirements by regulating each functional trait, improving resource utilization efficiency, and enhancing defense against environmental stresses. This study was designed at different developmental stages to comprehensively investigate the changes in the functional traits of P. pruinosa leaves, including leaf morphology, anatomical structure, and physiological characteristics, providing theoretical support for desertification control.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants12122262/s1, Table S1: Sample tree number related information; Figure S1: Correlation analysis according to different diameter classes; Figure S2: Correlation analysis of δ13C and ABA content.

Author Contributions

This collaborative work was carried out among all the authors. Z.L. and J.Z. proposed the original idea. J.Z., X.Z., X.H. and S.Z. experimented. J.Z. wrote the original draft. Z.L. reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the National Natural Sciences Foundation of China (NSFC) to Z.L. (Project No. 31860198) and the Innovative team Building Plan for key areas of Xinjiang Production and Construction Corps (Project No. 2018BC003) to Z.L.

Data Availability Statement

The datasets generated for this study are available on request to the corresponding author.

Acknowledgments

The authors are grateful to Tarim University for technical service and support in the research area and to the key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin of Xinjiang Production & Construction Corps for providing equipment. Meanwhile, we appreciate the constructive suggestions from the editor as well as the reviewers, which greatly improved the quality of our manuscript.

Conflicts of Interest

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

References

  1. White, T.L.; Adams, W.T.; Neale, D.B. Forest Genetics; CAB International: Cambridge, UK, 2007. [Google Scholar]
  2. Reich, P.B.; Wright, I.J.; Cavender-Bares, J.; Craine, J.M.; Oleksyn, J.; Westoby, M.; Walters, M.B. The evolution of plant functional variation: Traits, spectra, and strategies. Int. J. Plant. Sci. 2003, 164, 143–164. [Google Scholar] [CrossRef]
  3. Meng, T.; Ni, J.; Wang, G. Plant functional traits and environmental and ecosystem functions. J. Plant Ecol. 2007, 31, 150–165. [Google Scholar]
  4. Liu, X.; Ma, K. Advances in plant functional traits. Life Sci. 2015, 45, 325–339. [Google Scholar]
  5. Guittar, J.; Goldberg, D.; Klanderud, K.; Telford, R.J.; Vandvik, V. Can trait patterns along gradients predict plant community responses to climate change? Ecology 2016, 97, 2791–2801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Melo, A.G.; Posada, J.; Beauchêne, J.; Lehnebach, R.; Levionnois, S.; Rivera, K.; Clair, B. Radial variations in wood functional traits in a rain forest from eastern Amazonia. Trees 2022, 36, 569–581. [Google Scholar] [CrossRef]
  7. Paine, C.E.T.; Baraloto, C.; Chave, J.; Hérault, B. Functional traits of individual trees reveal ecological constraints on community assembly in tropical rain forests. Oikos 2011, 120, 720–727. [Google Scholar] [CrossRef]
  8. Simon, J.; Bilela, S.; Rennenberg, H. Nitrogen uptake capacity of European beech (Fagus sylvatica L.) only partially depends on tree age. Trees 2021, 35, 1739–1745. [Google Scholar] [CrossRef]
  9. Violle, C.; Enquist, B.J.; McGill, B.J.; Jiang, L.; Albert, C.H.; Hulshof, C.; Jung, V.; Messier, J. The return of the variance: Ntraspecific variability in community ecology. Trends Ecol. Evol. 2002, 27, 244–252. [Google Scholar] [CrossRef]
  10. Zirbel, C.R.; Bassett, T.; Grman, E.; Brudvig, L.A. Plant functional traits and environmental conditions shape community assembly and ecosystem functioning during restoration. J. Appl. Ecol. 2017, 54, 1070–1079. [Google Scholar] [CrossRef] [Green Version]
  11. Rodriguez, R.E.; Debernardi, J.M.; Palatnik, J.F. Morphogenesis of simple leaves: Regulation of leaf size and shape. Wiley Interdiscip Rev. Dev. Biol. 2014, 3, 41–57. [Google Scholar] [CrossRef]
  12. Xu, F.; Guo, W.; Xu, W.; Wei, Y.; Wang, R. Leaf morphology correlates with water and light availability: What consequences for simple and compound leaves? Prog. Nat. Sci. 2009, 19, 1789–1798. [Google Scholar] [CrossRef]
  13. Lambers, H.; Chapin, F.S.I.I.I.; Pons, T.L. Plant Physiological Ecology; Springer: New York, NY, USA, 2008. [Google Scholar]
  14. Zaitsev, G.A.; Kulagin, A.Y.; Davydychev, A.N. The particularities of the growth of Siberian fir (Abies sibirica Ledeb.) in the first stages of ontogeny in conifer forests (Ufa plateau, Pre-Ural). Trees 2018, 32, 511–518. [Google Scholar] [CrossRef]
  15. Dörken, V.M.; Parsons, R.F. The foliar change in two species of Melaleuca (Myrtaceae): A morpho-anatomic and ontogenetic approach. Trees 2018, 32, 1013–1028. [Google Scholar] [CrossRef] [Green Version]
  16. Bréda, N.; Huc, R.; Granier, A.; Dreyer, E. Temperate Forest trees and stands under severe drought: A review of Eco physiological responses, adaptation processes and long-term consequences. Ann. For. Sci. 2006, 63, 625–644. [Google Scholar] [CrossRef] [Green Version]
  17. Kull, O.; Koppel, A. Net photosynthetic response to light intensity of shoots from different crown positions and age in Picea abies (L.) Karst. Scand. J. For. Res. 1987, 2, 157–166. [Google Scholar] [CrossRef]
  18. Greenwood, M.S.; Ward, M.H.; Day, M.E.; Adams, S.L.; Bond, B.J. Age-related trends in red spruce foliar plasticity in relation to declining productivity. Tree Physiol. 2008, 28, 225–232. [Google Scholar] [CrossRef]
  19. England, J.R.; Attiwill, P.M. Changes in leaf morphology and anatomy with tree age and height in the broadleaved evergreen species, Eucalyptus regnans F. Muell. Trees 2006, 20, 79–90. [Google Scholar] [CrossRef]
  20. Nabeshima, E.; Hiura, T. Size dependency of photosynthetic water-and nitrogen-use efficiency and hydraulic limitation in Acer mono. Tree Physiol. 2004, 24, 745–752. [Google Scholar] [CrossRef] [Green Version]
  21. Niinemets, Ü.; Kull, O. Effects of light availability and tree size on the architecture of assimilative surface in the canopy of Picea abies: Variation in needle morphology. Tree Physiol. 1995, 15, 307–315. [Google Scholar] [CrossRef] [Green Version]
  22. Woodruff, D.R.; Bond, B.J.; Meinzer, F.C. Does turgor limit growth in tall trees? Plant Cell Env. 2004, 27, 229–236. [Google Scholar] [CrossRef]
  23. Niinemets, Ü.; Díaz-Espejo, A.; Flexas, J.; Galmés, J.; Warren, C.R. Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. J. Exp. Bot. 2009, 60, 2249–2270. [Google Scholar] [CrossRef] [Green Version]
  24. Tanaka-Oda, A.; Kenzo, T.; Kashimura, S.; Ninomiya, I.; Wang, L.H.; Yoshikawa, K.; Fukuda, K. Physiological and morphological differences in the heterophylly of Sabina vulgaris Ant. in the semi-arid environment of Mu Us Desert, Inner Mongolia, China. J. Arid. Env. 2010, 74, 43–48. [Google Scholar] [CrossRef]
  25. Zhai, J.; Li, Y.; Han, Z.; Li, Z. Morphological, structural and physiological differences in heteromorphic leaves of Euphrates poplar during development stages and at crown scales. Plant Biol. 2020, 22, 366–375. [Google Scholar] [CrossRef] [Green Version]
  26. Li, Z.; Jiao, P.; Wu, Z.; Zhai, J.; Zhang, X.; Zhang, S.; Gai, Z.; Guo, X. Heterophylly and Growth Adaptation Strategies of Populus Euphratica and Populus Pruinose; Science Press: Beijing, China, 2021. [Google Scholar]
  27. Kenzo, T.; Inoue, Y.; Yoshimura, M.; Yamashita, M.; Tanaka-Oda, A.; Ichie, T. Height-related changes in leaf photosynthetic traits in diverse Bornean tropical rain forest trees. Oecologia 2015, 177, 191–202. [Google Scholar] [CrossRef] [PubMed]
  28. He, C.; Li, J.; Zhou, P.; Guo, M.; Zheng, Q. Changes of leaf morphological, anatomical structure and carbon isotope ratio with the height of the Wangtian tree (Parashorea chinensis) in Xishuangbanna, China. J. Integr. Plant Biol. 2008, 50, 168–173. [Google Scholar] [CrossRef] [PubMed]
  29. Piovesan, G.; Lüttge, U. Tree growth dynamics during early ontogenetic stages in closed forests. Trees 2018, 32, 671–673. [Google Scholar] [CrossRef]
  30. Wang, M.; Jiang, Y.; Dong, M.; Zhang, W.; Wang, B.; Zhang, Y.; Ding, X.; Kang, M.; Xu, H. The contributions of rate and duration of stem radial increment to annual increments of Picea meyeri in a sub-alpine habitat, North-Central China. Trees 2018, 32, 1029–1041. [Google Scholar] [CrossRef]
  31. Nezu, I.; Ishiguri, F.; Aiso, H.; Hiraoka, Y.; Wasli, M.E.; Ohkubo, T.; Ohshima, J.; Yokota, S. Secondary xylem maturation evaluated by modeling radial variations in anatomical characteristics and wood properties of Shorea macrophylla (De Vr.) Ashton planted in Sarawak, Malaysia. Trees 2022, 36, 659–668. [Google Scholar] [CrossRef]
  32. Bhusal, N.; Lee, M.; Han, A.R.; Han, A.; Kim, H.S. Responses to drought stress in Prunus sargentii and Larix kaempferi seedlings using morphological and physiological parameters. Forest Ecol. Manag. 2020, 465, 118099. [Google Scholar] [CrossRef]
  33. Bhusal, N.; Bhusal, S.J.; Yoon, T.M. Comparisons of physiological and anatomical characteristics between two cultivars in bi-leader apple trees (Malus × domestica Borkh.). Sci. Hortic. Amst. 2018, 231, 73–81. [Google Scholar] [CrossRef]
  34. Zhai, J.; Han, X.; Li, Z. Evaluation of drought resistance of P. pruinosa at different developmental stages based on leaf anatomy. J. Tarim Univ. 2019, 31, 12–21. [Google Scholar]
  35. Xia, H.; Yang, L.; Tu, Z.; Zhang, C.; Hao, Z.; Zhong, W.; Li, H. Growth performance and G × E interactions of Liriodendron tulipifera half-sib families across ages in eastern China. Eur. J. Forest Res. 2022, 141, 1089–1103. [Google Scholar] [CrossRef]
  36. Shi, P.; Liu, M.; Ratkowsky, D.; Gielis, J.; Su, J.; Yu, X.; Wang, P.; Zhang, L.; Lin, Z.; Schrader, J. Leaf area-length allometry and i ts implications in leaf shape evolution. Trees 2019, 33, 1073–1085. [Google Scholar] [CrossRef]
  37. Cleugh, H.A.; Leuning, R.; Mu, Q.; Running, S.W. Regional evaporation estimates from flux tower and MODIS satellite data. Remote Sens. Env. 2007, 106, 285–304. [Google Scholar] [CrossRef]
  38. Niinemets, Ü.; Keenan, T.F.; Hallik, L. A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytol. 2015, 205, 973–993. [Google Scholar] [CrossRef] [Green Version]
  39. Messier, J.; McGill, B.J.; Enquist, B.J.; Lechowicz, M.J. Trait variation and integration across scales: Is the leaf economic spectrum present at local scales? Ecography 2017, 40, 685–697. [Google Scholar] [CrossRef]
  40. Russo, S.E.; Kitajima, K. The ecophysiology of leaf lifespan in tropical forests: Adaptive and plastic responses to environmental heterogeneity. Trop. Tree Physiol. 2016, 6, 357–383. [Google Scholar]
  41. Bhusal, N.; Han, S.G.; Yoon, T.M. Summer pruning and reflective film enhance fruit quality in excessively tall spindle apple trees. Hortic. Environ. Biotechnol. 2017, 58, 560–567. [Google Scholar]
  42. Sellin, A.; Alber, M.; Jasińska, A.K.; Rosenvald, K. Adjustment of leaf anatomical and hydraulic traits across vertical canopy profiles of young broadleaved forest stands. Trees 2021, 36, 67–80. [Google Scholar] [CrossRef]
  43. Aasamaa, K.; Niinemets, Ü.; Sõber, A. Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny. Tree Physiol. 2005, 25, 1409–1418. [Google Scholar] [CrossRef] [Green Version]
  44. Sack, L.; Frole, K. Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 2006, 87, 483–491. [Google Scholar] [CrossRef]
  45. Brodribb, T.J.; Field, T.S.; Jordan, G.J. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol. 2007, 144, 1890–1898. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Xiong, D.; Flexas, J.; Yu, T.; Peng, S.; Huang, J. Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza. New Phytol. 2017, 213, 572–583. [Google Scholar] [CrossRef]
  47. Zhang, Y.; Meinzer, F.C.; Hao, G.; Scholz, F.G.; Bucci, S.J.; Takahashi, F.S.; Villalobos-Vega, R.; Giraldo, J.P.; Cao, K.; Hoffmann, W.A.; et al. Size-dependent mortality in a Neotropical savanna tree: The role of height-related adjustments in hydraulic architecture and carbon allocation. Plant Cell Env. 2009, 32, 1456–1466. [Google Scholar] [CrossRef]
  48. Kishor, P.; Sangam, S.; Amrutha, R. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr. Sci. 2005, 88, 424–438. [Google Scholar]
  49. Han, X.; Zhai, J.; Gai, Z.; Li, Z. The relationship between the morphological and structural changes of Populus euphratica Oliv. and endogenous hormone contents. Appl. Ecol. Env. Res. 2021, 19, 2259–2280. [Google Scholar] [CrossRef]
  50. Yao, M. Several kinds of phytohormone in plants responses to salt-stress. Biol. Bull. 2011, 11, 1–5. [Google Scholar]
  51. Jia, H.; Lu, C. Effects of abscisic acid on photoinhibition in maize plants. Plant Sci. 2003, 165, 1403–1410. [Google Scholar] [CrossRef]
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Figure 1. Changes in leaves’ morphological characteristics in different diameter classes of P. pruinosa. Note: (a) blade length; (b) blade width; (c) leaf area; (d) leaf index; (e) leaf dry weight; (f) specific leaf area. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***; 0.001 < p < 0.01: **).
Figure 1. Changes in leaves’ morphological characteristics in different diameter classes of P. pruinosa. Note: (a) blade length; (b) blade width; (c) leaf area; (d) leaf index; (e) leaf dry weight; (f) specific leaf area. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***; 0.001 < p < 0.01: **).
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Figure 2. Changes in leaves’ anatomical structure characteristics in different diameter classes of P. pruinosa. Note: (a) main vein vascular bundle area; (b) main vein xylem area; (c) leaf thickness; (d) palisade tissue thickness. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***).
Figure 2. Changes in leaves’ anatomical structure characteristics in different diameter classes of P. pruinosa. Note: (a) main vein vascular bundle area; (b) main vein xylem area; (c) leaf thickness; (d) palisade tissue thickness. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***).
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Figure 3. Changes in leaves’ photosynthetic physiological parameters in different diameter classes of P. pruinosa. Note: (a) photosynthetic rate; (b) transpiration rate; (c) stomatal conductance; (d) intercellular CO2 concentration. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***; 0.001 < p < 0.01: **).
Figure 3. Changes in leaves’ photosynthetic physiological parameters in different diameter classes of P. pruinosa. Note: (a) photosynthetic rate; (b) transpiration rate; (c) stomatal conductance; (d) intercellular CO2 concentration. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***; 0.001 < p < 0.01: **).
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Figure 4. Changes in leaves’ water use efficiency in different diameter classes of P. pruinosa. Note: (a) stable carbon isotope value; (b) instantaneous water use efficiency. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.01: **; p > 0.05: ns).
Figure 4. Changes in leaves’ water use efficiency in different diameter classes of P. pruinosa. Note: (a) stable carbon isotope value; (b) instantaneous water use efficiency. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.01: **; p > 0.05: ns).
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Figure 5. Changes in leaves’ physiological characteristics in different diameter classes of P. pruinosa. Note: (a) proline content; (b) malondialdehyde content. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***; p > 0.05: ns).
Figure 5. Changes in leaves’ physiological characteristics in different diameter classes of P. pruinosa. Note: (a) proline content; (b) malondialdehyde content. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***; p > 0.05: ns).
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Figure 6. Changes in leaves’ endogenous hormone content in different diameter classes of P. pruinosa. Note: (a) abscisic acid content; (b) gibberellin content; (c) indoleacetic acid content; (d) zeatin riboside content. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***).
Figure 6. Changes in leaves’ endogenous hormone content in different diameter classes of P. pruinosa. Note: (a) abscisic acid content; (b) gibberellin content; (c) indoleacetic acid content; (d) zeatin riboside content. The lowercase letters and the uppercase letters represent the significance of the differences between different leaf heights and different diameter classes of P. pruinosa (p < 0.05). Two-factor analyses of variance (ANOVA) were applied to evaluate the effects of different factors and interactions. FH, leaf height effect; FDC, diameter class effect; FH×DC, leaf height × diameter class effect (p < 0.001: ***).
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Figure 7. Linear fitting of leaf morphology characteristics of different diameter classes (8/12/16/20) with leaf height of P. pruinosa. (p < 0.01: **; p > 0.05: NS). Note: (a) BL, blade length; (b) BW, blade width; (c) LA, leaf area; (d) LI, leaf index; (e) LDW, leaf dry weight; (f) SLA, specific leaf area.
Figure 7. Linear fitting of leaf morphology characteristics of different diameter classes (8/12/16/20) with leaf height of P. pruinosa. (p < 0.01: **; p > 0.05: NS). Note: (a) BL, blade length; (b) BW, blade width; (c) LA, leaf area; (d) LI, leaf index; (e) LDW, leaf dry weight; (f) SLA, specific leaf area.
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Figure 8. Linear fitting of leaf anatomical structure characteristics of different diameter classes (8/12/16/20) with leaf height of P. pruinosa. (p < 0.01: **; p > 0.05: NS) Note: (a) MVBA, main vein vascular bundle area; (b) MXA, main vein xylem area; (c) LT, leaf thickness; (d) PT, palisade tissue thickness.
Figure 8. Linear fitting of leaf anatomical structure characteristics of different diameter classes (8/12/16/20) with leaf height of P. pruinosa. (p < 0.01: **; p > 0.05: NS) Note: (a) MVBA, main vein vascular bundle area; (b) MXA, main vein xylem area; (c) LT, leaf thickness; (d) PT, palisade tissue thickness.
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Figure 9. Linear fitting of leaf physiological and biochemical characteristics of different diameter classes (8/12/16/20) with leaf height of P. pruinosa. (p < 0.01: **; 0.01 < p < 0.05: *; p > 0.05: NS) Note: (a) Pro, proline; (b) MDA, malondialdehyde; (c) ABA, abscisic acid; (d) GA3, gibberellin; (e) IAA, indoleacetic acid; (f) ZR, zeatin riboside.
Figure 9. Linear fitting of leaf physiological and biochemical characteristics of different diameter classes (8/12/16/20) with leaf height of P. pruinosa. (p < 0.01: **; 0.01 < p < 0.05: *; p > 0.05: NS) Note: (a) Pro, proline; (b) MDA, malondialdehyde; (c) ABA, abscisic acid; (d) GA3, gibberellin; (e) IAA, indoleacetic acid; (f) ZR, zeatin riboside.
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Figure 10. Principal component analysis (PCA) based on leaf traits in P. pruinosa at different heights across four diameter classes. The diamond, upper triangle, right triangle, and left triangle represent the tree heights of 2, 4, 6, 8, 10, and 12 m, respectively; the light blue, dark blue, green, and red represent diameter classes 8, 12, 16, and 20, respectively. BL, blade length; BW, blade width; LA, leaf area; LI, leaf index; LDW, leaf dry weight; SLA, specific leaf area; MVBA, main vein vascular bundle area; MXA, main vein xylem area; LT, leaf thickness; PT, palisade tissue thickness; Pn, photosynthetic rate; Tr, transpiration rate; Gs, stomatal conductance; Ci, intercellular CO2 concentration; δ13C, stable carbon isotope value; WUEi, instantaneous water use efficiency; Pro, proline; MDA, malondialdehyde; ABA, abscisic acid; GA3, gibberellin; IAA, indoleacetic acid; ZR, zeatin riboside.
Figure 10. Principal component analysis (PCA) based on leaf traits in P. pruinosa at different heights across four diameter classes. The diamond, upper triangle, right triangle, and left triangle represent the tree heights of 2, 4, 6, 8, 10, and 12 m, respectively; the light blue, dark blue, green, and red represent diameter classes 8, 12, 16, and 20, respectively. BL, blade length; BW, blade width; LA, leaf area; LI, leaf index; LDW, leaf dry weight; SLA, specific leaf area; MVBA, main vein vascular bundle area; MXA, main vein xylem area; LT, leaf thickness; PT, palisade tissue thickness; Pn, photosynthetic rate; Tr, transpiration rate; Gs, stomatal conductance; Ci, intercellular CO2 concentration; δ13C, stable carbon isotope value; WUEi, instantaneous water use efficiency; Pro, proline; MDA, malondialdehyde; ABA, abscisic acid; GA3, gibberellin; IAA, indoleacetic acid; ZR, zeatin riboside.
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Table
Table 1. Sample-tree-related information.
Table 1. Sample-tree-related information.
InformationDiameter
Class		Average Diameter at Breast Height (cm)Average Height of First Branch (cm)Average Tree Height (m)
Sample Tree
Number
8–387.51152.517.42
12–51212.13155.739.15
16–41616.07177.1310.83
20–72019.6188.5712.90
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Zhai, J.; Zhang, X.; Li, Z.; Han, X.; Zhang, S. Differences in the Functional Traits of Populus pruinosa Leaves in Different Developmental Stages. Plants 2023, 12, 2262. https://doi.org/10.3390/plants12122262

AMA Style

Zhai J, Zhang X, Li Z, Han X, Zhang S. Differences in the Functional Traits of Populus pruinosa Leaves in Different Developmental Stages. Plants. 2023; 12(12):2262. https://doi.org/10.3390/plants12122262

Chicago/Turabian Style

Zhai, Juntuan, Xiao Zhang, Zhijun Li, Xiaoli Han, and Shanhe Zhang. 2023. "Differences in the Functional Traits of Populus pruinosa Leaves in Different Developmental Stages" Plants 12, no. 12: 2262. https://doi.org/10.3390/plants12122262

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