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Article

Response of Non-Structural Carbohydrates and Carbon, Nitrogen, and Phosphorus Stoichiometry in Pinus yunnanensis Seedlings to Drought Re-Watering

by
Chengyao Liu
,
Junwen Wu
*,
Jianyao Gu
and
Huaijiao Duan
College of Forestry, Southwest Forestry University, Kunming 650224, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(11), 1864; https://doi.org/10.3390/f15111864
Submission received: 22 September 2024 / Revised: 20 October 2024 / Accepted: 23 October 2024 / Published: 24 October 2024
(This article belongs to the Special Issue Physiological Mechanisms of Plant Responses to Environmental Stress)
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Abstract

Pinus yunnanensis is an endemic tree species in southwest China that has high ecological and economic benefits. Nowadays, global climate change is remarkable, the frequency of drought is increasing day by day, the distribution of rainfall is unbalanced, and even the phenomenon of alternating drought and flood has appeared, which is unfavorable to the growth of P. yunnanensis. We set up four treatments, namely normal water (CK), light drought (LD), moderate drought (MD), and severe drought (SD), and water content was controlled by the weighing method. After continuous drought for 30 days, re-watering was performed for 7 days. The stoichiometric characteristics of non-structural carbohydrates (NSC), soluble sugars (SS), and starch (ST), as well as carbon (C), nitrogen (N), and phosphorus (P), in various organs of P. yunnanensis seedlings were measured. The results revealed significant effects of re-watering on NSC and its components in P. yunnanensis seedlings. The SS and NSC contents in the leaves of P. yunnanensis seedlings treated with SD were significantly higher than those of the control. The C content in the leaves and stems of P. yunnanensis seedlings recovered to the CK level after re-watering under different drought degrees. The contents of N in different organs and P in the fine roots of P. yunnanensis seedlings increased after re-watering with the LD, MD, and SD treatments, while the C/N ratio decreased. In summary, the recovery mechanism of P. yunnanensis seedlings to re-watering varied with the drought degree. The contents and ratios of NSC, C, N, and P in different organs of P. yunnanensis seedlings were significantly affected by re-watering. Combining the phenotypic plasticity index and PCA results, seedlings of P. yunnanensis adapted to drought re-watering by adjusting leaf NSC, leaf P, stem SS/ST, fine root ST, and fine root NSC.

1. Introduction

The marked changes in the global climate have increased drought frequency, rainfall distribution imbalances, and drought–flood alternations [1]. As a common abiotic stress to plants, drought severely restricts plant growth [2]. Increases in the duration, frequency, and intensity of droughts are likely to alter the composition and structure of forests, and drought-related tree mortality and forest decline are currently observed on several forest continents [3,4]. Water is an important limiting factor in the growth of trees. The most direct effect of drought on the survival and growth of trees is water loss [5]. Thus, research on the changes in the plant physiological mechanism during the drought re-watering process is critical for analyzing the differences in plant drought resistance, plant regeneration, and reconstruction and for improving the productivity of agroforestry plants [6]. Re-watering restoration refers to the ability of plants to recover normal growth after drought stress [7]. Scholars have shown that the damage to plants under mild and moderate drought stress can be counteracted or even compensated after re-watering [8]. In particular, a series of adaptive changes in plant morphology, physiology, and biochemistry occurs following re-watering, which can reflect the drought resistance and recovery abilities of plants [9]. Extensive research has been conducted on plant drought stress, while studies on drought re-watering are relatively limited.
Non-structural carbohydrates (NSC) include soluble sugars (SS) and starches (ST). The concentrations and variations of NSC reflect the levels of substances available for plant growth [10]. Under drought stress, starch in plants can be converted into soluble sugar to resist adversity [11]. A change in water conditions will alter NSC content in plants [12,13]. Current studies on the effect of water change on the NSC content of plants mainly focus on drought [14,15]. Scholars reported a decrease in NSC root content under drought stress, while the NSC content in leaves and stems remained unchanged [16]. Studies have also found that NSC content increased in the early stage of drought and decreased in the later stage [17]. However, the effects of drought on the NSC of trees vary with the drought degree and may affect the physiological recovery processes of trees after drought, such as stomatal reopening, photosynthesis, and phloem transport recovery [18,19]. Therefore, studying the effect of plant re-watering on NSC under different degrees of drought can help to understand the drought resistance and recovery mechanisms of plants.
Carbon (C), nitrogen (N), and phosphorus (P) are essential elements for plant growth and physiological activities. Plants adapt to environmental changes through coordination among the elements in their bodies, which can—to a certain extent—reflect the relationship between plants and the environment [20,21]. Under drought stress, the content and ratios of C, N, and P in plant bodies will exhibit different change rules [22,23]. Drought can affect the fixation of C and the absorption of N and P, resulting in the reduction of C, N, and P contents in plants [24,25]. In addition, the mechanisms underlying the effects of different drought degrees on C, N, and P contents in plants are different. This leads to the decoupling of elements in plants, thus causing the imbalance of nutrients and forming nutrient limitations [26,27]. However, the changes in C, N, and P contents occurring in plants with the increase in water after drought stress are not fully understood [28,29]. Therefore, research on the C, N, and P stoichiometric changes after re-watering can help to understand the trade-off strategies of plants following environmental changes.
Pinus yunnanensis, an important endemic tree species in southwest China, is distributed in western Sichuan, Yunnan, western Guizhou, and northwestern Guangxi. It is the main forest species in the Yunnan Province, accounting for 52% of the forest area in the Yunnan Province [30]. P. yunnanensis is rich in resin and is used as an industrial raw material. It is widely employed in numerous industries (e.g., architecture and construction, medicine, and food and spices) [31]. Much research has been conducted on the effects of drought stress on P. yunnanensis, including the effects of growth, morphological characteristics, physiological regulation, and osmotic regulation [32,33]. However, the response of P. yunnanensis to drought re-watering remains unclear. In this study, we analyzed the responses of NSC and the C, N, and P stoichiometric characteristics of P. yunnanensis seedlings to re-watering under different degrees of drought and explored the recovery mechanism following re-watering and the adaptation strategy of P. yunnanensis seedlings.

2. Materials and Methods

2.1. Study Site and Test Materials

The experimental site was located at the Southwest Forestry University arboretum (Kunming, China, E 102°46′, N 25°03′) in the monsoon region of the subtropical plateau, with an altitude of 1964 m and a mild climate. The frost-free period lasts approximately 240 days. The annual average precipitation is 1035 mm. The soil type in this area is red loam. The temperature range during the experiment was 18 to 37 °C, and the relative humidity ranged from 22 to 47%.
The selection of an improved variety of Pinus yunnanensis (variety number: Yun R-SS-PY-035-2020) was conducted on 1 August 2021 in Malonghe Forest Farm, Shuangbai County, China. In April 2022, 8-month-old seedlings of 150 P. yunnanensis were transported to the Southwest Forestry University arboretum after cultivation in Malonghe Forest Farm, Shuangbai County Province. The seedlings were transplanted into 11 L plastic flowerpots, respectively. Each container was filled with 3.5 kg of mixed soil containing red loam soil from the sunny slope of the Jianshui Mountain area at the Red River and the pine needle nutrient humus soil of Songming County in Kunming City (3:2 ratio). The soil bulk density was determined to be 1.001 g/cm3, the soil pH was 6.65, and soil total carbon, total nitrogen, and total phosphorus were 3.26, 5.98, and 0.62 g/kg, respectively. A tray was placed at the bottom of the flowerpot, and after transplanting, the soil moisture content of the seedlings was maintained as the field water holding capacity to ensure the survival of the seedlings.

2.2. Test Design

The drought stress experiment was performed during 1–30 October 2022 (30-day duration). The drought gradients were divided according to previous research [34]. Normal water (CK), light drought (LD), moderate drought (MD), and severe drought (SD) were assigned drought gradients of 90% ± 5%, 75% ± 5%, 60% ± 5%, and 45% ± 5% of the field water holding capacity (i.e., the actual water content was maintained at 19.13%–21.38%, 15.75%–18%, 12.38%–14.63%, and 9%–11.25%), respectively. The actual soil moisture content was measured with a soil moisture meter (Decagon Inc., Washington, DC, USA) every 24 h, and soil moisture was controlled by weighing. According to the target weight, the water was controlled or watered to 90% ± 5%, 75% ± 5%, 60% ± 5%, and 45% ± 5% of the field water holding capacity, respectively, and re-watered after the end of the continuous drought (1 November 2022) to restore and maintain the normal soil water content (CK, 90% ± 5%). Re-watering was completed on 8 November 2022, and sampling was performed.

2.3. Indicator Measurements

Four seedlings of P. yunnanensis were taken from each treatment. The leaves, stems, thick roots (diameter > 2 mm), and fine roots (diameter < 2 mm) of the four organs were sorted, weighed, and placed into envelopes. The samples were dried in an oven (Teste Instrument Co., Ltd., Tianjin, China) at 120 °C for 30 min and then at 80 °C for 48 h until a constant weight was reached. Following this, the samples were ground and stored in a sealed bag for the determination of carbon, nitrogen, phosphorus, soluble sugar, and starch contents. Soluble sugar concentrations were determined using the anthrone colorimetric method. A total of 0.5 g per sample was placed in a centrifuge tube (BKMAMLAB, Changsha, China), and 15 mL of 80% ethanol (Goldbush biotech, Hong Kong, China) was added. Next, the mixture was incubated at 95 °C in a shaking water bath for 10 min and then centrifuged at 5000 rpm for 10 min. The supernatants were retained, combined, and stored for later use. The extraction process was performed three times to ensure complete extraction of all of the sugar. Next, 5 mL of anthrone reagent (Solarbio, Beijing, China) was added to the 0.2 mL soluble sugar extraction liquid and placed in a 90 °C water bath for 15 min. The absorbance at 620 nm was measured to calculate the soluble sugar concentration according to the standard curve. Extraction of starch: Add 10 mL of distilled water (BKMAMLAB, Changsha, China) to the above extracted residue, extract at 100 °C for 15 min, add 2 mL of 9.2 mol/L perchloric acid (Beijing Zhongke Erhuan Technology Co., Ltd., Beijing, China) while hot, shake well, and leave it to extract for 15 min, then centrifuge to obtain the supernatant and to fix the volume, which can be used for the determination of starch content. The sum of the two contents was the non-structural carbohydrate (NSC) content [35]. The total C content was determined by the potassium dichromate method plus dilution heating, the total N content was determined by the colorimetric method, and the total P content was determined by the molybdenum antimony anti-colorimetric method [36].

2.4. Data Processing and Analysis

The data were pre-processed in Excel 2016 edition (Microsoft Corp., Albuquerque, NM, USA) and plotted in Origin 2021 edition (Origin Lab, Northampton, MA, USA) and GraphPad Prism 9.5 edition (GraphPad Software, Inc., San Diego, CA, USA). Data were expressed as the mean ± standard deviation. SPSS 27.0 edition (IBM Corp., Chicago, IL, USA) was used to conduct one-way ANOVA to analyze whether there were significant differences in the same organ among different treatments, and two-way ANOVA was used to analyze the effects of different organs and drought degree on the seedlings of P. yunnanensis. Principal component analysis and phenotypic plasticity analysis of the data were performed. The plasticity index (P) was determined as:
P = (Xmax − Xmin)/Xmax
where Xmax and Xmin represent the maximum and minimum values of each index, respectively.

3. Results

3.1. Effects of Re-Watering on NSC and Its Components in Pinus yunnanensis Seedlings

The effects of re-watering, the organs, and their interactions on NSC and its component contents in Pinus yunnanensis seedlings are shown in Table 1. The contents of SS, ST, NSC, and the SS/ST ratio of P. yunnanensis seedlings were extremely significantly affected by re-watering, organs, and their interactions (p < 0.01).
The maximum content of SS in the leaves of P. yunnanensis seedlings was 169.6 ± 2.4 g/kg after the SD treatment (45.33% higher than that of CK, p < 0.05, Figure 1A). The stem SS content was the highest in the CK treatment (240.8 ± 2.1 g/kg), while the thick root SS contents in the LD, MD, and SD treatments were significantly higher than that in the CK treatment (by 43.66%, 9.76% and 4.07%, respectively, p < 0.05). The content of SS in fine roots was the highest in the LD treatment (146.8 ± 4.1 g/kg), exceeding that of the CK treatment by 18.96%. The highest ST content of P. yunnanensis seedling leaves was 129.3 ± 3.4 g/kg in the MD treatment (55.78% higher than that in the CK treatment, p < 0.05, Figure 1B). The stem ST contents of LD and SD treatments were 218.4 ± 2.8 and 239.6 ± 3.8 g/kg, which were 14.35% and 25.45% higher than CK treatments. With the increase in drought stress, the ST content in the thick and fine roots of P. yunnanensis seedlings decreased after re-watering, compared with the CK, LD, MD, and SD treatments, with significant reductions in the thick roots by 26.62%, 44.44%, and 56.95%, respectively. The LD, MD, and SD treatments significantly decreased the ST content in fine roots by 40.75%, 69.17%, and 76.40%, respectively. The contents of NSC in leaves of MD and SD treatments were 248.5 ± 2.3 and 252.3 ± 2.6 g/kg, respectively, which were 24.44% and 26.34% higher than CK treatments (Figure 1C). The content of NSC in the stem of the SD treatment was the highest (432.8 ± 2.8 g/kg). The content of NSC in the thick root was 316.9 g/kg in the LD treatment (9.05% higher than the CK treatment), while the thick and fine root NSC contents were the lowest in the SD treatment (25.98% and 64.79% significantly lower than the CK treatment, respectively). The highest SS/ST ratios of leaves and thick roots of P. yunnanensis seedlings were 2.1 ± 0.07 and 2.5 ± 0.09 in the SD treatment, respectively (exceeding those of the CK by 50% and 150%, respectively, p < 0.05, Figure 1D). The highest SS/ST ratios of stem and fine roots were 1.7 ± 0.08 and 1.1 ± 0.16 in the MD treatment, respectively (30.77% and 175% higher than the CK treatment, respectively).

3.2. Effects of Re-Watering on the C, N, and P Contents and Stoichiometry of P. yunnanensis Seedlings

The effects of re-watering, organs, and their interactions on the C, N, and P contents and their stoichiometric characteristics of P. yunnanensis are shown in Table 2. The organs had extremely significant effects on the N content, C/P, and N/P ratio (p < 0.01), significant effects on the P content and C/N ratio (p < 0.05), and no significant effects on the C content. Drought dewatering exerted an extremely significant effect on the C, N, and P contents and a significant effect on the C/P and N/P ratios. The interaction between re-watering and organs had extremely significant effects on the P content and C/P and N/P ratios, significant effects on the C and N contents, and no significant effects on the C/N ratio.
The C contents of the leaves and stems of P. yunnanensis seedlings recovered to the CK level after re-watering. The C contents of thick roots and fine roots reached minimums of 425.7 ± 16.5 and 387.8 ± 1.6 g/kg under the LD treatment (11.34% and 6.73% lower than the CK treatment, respectively, p < 0.05, Figure 2A). After re-watering, the contents of N in all organs of P. yunnanensis seedlings treated with LD, MD, and SD exhibited an increasing trend, reaching maximum values in the SD treatment, which were 17.2 ± 0.01, 12.8 ± 1.3, 7.5 ± 0.4, and 20.1 ± 1.6 g/kg, respectively (Figure 2B). The content of N in each organ of P. yunnanensis seedlings treated with SD was 27.41%, 25.49%, 29.31%, and 51.13% higher than that of the CK, respectively (p < 0.05). The contents of P in the leaves of P. yunnanensis seedlings treated with MD and SD were 1.2 ± 0.4 and 1.1 ± 0.1 g/kg, significantly higher than those treated with CK by 71.43% and 57.14% (p < 0.05) (Figure 2C). Compared with the CK, the MD treatment significantly decreased the stem P content by 46.67%, while the LD and SD treatments did not exhibit any significant differences with CK. The MD treatment significantly increased the thick root P content by 22.22%, compared with the CK treatment. As drought stress increased, the fine root P content increased after re-watering and reached a maximum of 3.7 ± 0.4 g/kg in the SD treatment, which was 32.14% higher than that in the CK treatment.
The C/N ratios of P. yunnanensis seedling leaves in the MD and SD treatments were 31.1 ± 3.2 and 29.3 ± 1.6, which were significantly lower than those in the CK treatments by 19.64% and 24.29%, respectively (p < 0.05) (Figure 2D). Compared with CK, the C/N ratio of the SD treatment was significantly lower (by 21.79%). The C/N ratios of thick roots of MD and SD treatments were 62.6 ± 4.6 and 58.7 ± 8.2, which were 24.58% and 29.31% lower than those of the CK treatments. The C/N ratios of fine roots of the LD, MD, and SD treatments were 26.3 ± 2, 26.5 ± 1.2, and 22.1 ± 1, which were 15.97%, 15.34%, and 29.39% lower than those of the CK treatments. Compared with the CK, the C/P ratios of LD, MD, and SD were 70.60%, 105.71%, and 44.04% higher, respectively (Figure 2E). The C/P ratios of fine roots of P. yunnanensis seedlings decreased with the increase in drought stress, and the lowest C/P ratio was 121.1 ± 7.7 under the SD treatment, which was 18.72% lower than that under the CK treatment. The N/P ratio of the LD treatment of P. yunnanensis leaves was significantly higher than that of CK (72.16%) (Figure 2F). Under the MD and SD treatments, the stem N/P ratios were 108.70% and 33.33% higher than that of CK, respectively. Moreover, the N/P ratios of thick roots and fine roots were 17.8 ± 0.5 and 5.5 ± 0.1 in the SD treatment, 102.94% and 14.58% higher than CK, respectively.

3.3. Phenotypic Plasticity Index of P. yunnanensis Seedlings After Drought Re-Watering

After watering, the plasticity index of the NSC content and C, N, and P stoichiometries of P. yunnanensis seedlings ranged from 0.13 to 0.78 (Figure 3). Leaf CP, fine root ST, leaf P, leaf N/P, stem SS/ST, fine root NSC, and fine root SS/ST exhibited relatively high index values, while those of fine root C, fine root N/P ratio, leaf C, and stem C were relatively low. The results showed that the seedlings of P. yunnanensis mainly responded to changes in re-watering by altering the ST and P contents in fine roots, the C/P ratio in leaves, the N/P ratio in leaves, and the SS/ST ratio in fine roots.

3.4. Principal Component Analysis of P. yunnanensis Seedling Indexes After Re-Watering

PCA was performed on the NSC characteristics, C, N, and P contents, and their ratios in different organs of P. yunnanensis seedlings after re-watering (Figure 4). The cumulative contribution rates of the first two principal components of the leaves, stems, thick roots, and fine roots were 81.9%, 77.7%, 77%, and 87%, respectively. This indicates that the first two principal components can effectively explain the response characteristics of P. yunnanensis seedlings to drought re-watering. Leaf NSC and P (SS/ST and C/P) exhibited the greatest weight coefficients in PC1 (PC2) (Figure 4A). Similarly, the largest weight coefficients in PC1 (PC2) were observed for stem C/P and SS/ST (N) (Figure 4B). For thick roots, NSC and ST (C) had the highest weight coefficients in PC1 (PC2), while for fine roots, NSC, ST, and C/N (C) had the highest weights in PC1 (PC2) (Figure 4D). In summary, leaf NSC, leaf P, stem C/P, stem SS/ST, thick root NSC, thick root ST, fine root NSC, and fine root ST were determined to reflect the adaptation characteristics of P. yunnanensis seedlings following post-drought re-watering.

4. Discussion

Variations in plant NSC content are affected by changes in the environment. When the plant is under adversity stress, the stored NSC begins to hydrolyze to adjust the balance state [37]. In this study, drought re-watering, organs, and their interactions had extremely significant effects on the NSC content and its components (Table 1). The recovery of plant morphological and physiological characteristics after re-watering is an important factor in plant adaptation to adversity and the evaluation of plant drought tolerance [38]. The results showed that the contents of NSC and its components in P. yunnanensis seedlings under different degrees of drought were significantly different after re-watering (Figure 1). This indicates a variation in the recovery degree of P. yunnanensis seedlings with different drought degrees after re-watering. The leaf is the main site for photosynthesis and transpiration. After re-watering, the leaves distribute the remaining NSC from transpiration to the root through the stem to provide energy for the root system. Therefore, the above-ground plant components experience strong recovery [39]. In this study, the contents of SS and NSC in leaves of SD treatment P. yunnanensis seedlings were significantly higher than those of CK, while the contents of fine roots were significantly lower than those of CK. This indicates that the root damage of P. yunnanensis seedlings was more serious because of drought. The study by Hartmann et al. also showed that severe drought significantly reduced NSC content in fine roots of Picea abies [39]. The SS in trees is converted from stored ST and is also obtained from the transportation of photosynthetic products [40]. In this study, the ST content of the thick and fine roots of P. yunnanensis seedlings decreased after re-watering. This may be because the root is the most affected component under drought stress. After rehydration, ST needs to be converted into SS to resume growth. We also found that the SS/ST ratio of P. yunnanensis seedlings in the leaves, thick roots, and fine roots exceeded that of CK (except for the MD treatment, where it was lower). This indicates that the required soluble sugar for leaves, thick roots, and fine roots increased after re-watering. Zhao Nan’s research on Schima superba also showed that thick roots and fine roots increased their demand for soluble sugars after re-watering [41].
The contents of C, N, and P in the plant body can reflect the adaptability of plants to the environment and are sensitive to environmental changes [42]. In this study, the effects of re-watering, organs, their interactions with C, N, and P contents, and their stoichiometric characteristics were observed to vary (Table 2). C, the basic material component of the plant body, is essential for energy provision, growth, and development [43]. In this study, the C contents in thick and fine roots of P. yunnanensis seedlings were significantly lower than that of the CK after re-watering under different drought degrees (except for the LD treatment). The C levels were then observed to recover to the CK level (Figure 2). This shows that C, as the main substance of the plant skeleton, provides energy for the growth and metabolism of plants and has high stability in plants. After re-watering, the N contents in all organs of P. yunnanensis seedlings treated with LD, MD, and SD exhibited an increasing trend. This may be due to the increase in soil water content and N availability in soil [44]. In this study, the P contents in fine roots of P. yunnanensis seedlings increased after re-watering. This may be attributed to the damage in the root system of P. yunnanensis seedlings during the early stage of drought, which requires a large amount of P for root repair and carbohydrate transport. However, re-watering after drought can promote the formation of plant adaptation mechanisms, yet this also enhances P contents. Chen’s research has also shown that plants increase their ability to adapt to adversity by increasing the amount of P contents in their roots [45]. The C/N and C/P ratios can reflect the growth rate of plants, with higher values indicating higher nutrient utilization efficiency [46]. In this study, the C/N ratios of all organs of P. yunnanensis seedlings declined after re-watering. Thus, re-watering after drought affected the N utilization efficiency, which consequently impacted the C assimilation ability and nutrient utilization efficiency. The leaf C/P ratio of the LD treatment, the stem C/P ratio of the MD treatment, and the thick root C/P ratio of the SD treatment were significantly higher than those of the CK group. This demonstrates that the re-watering of P. yunnanensis seedlings stimulated the utilization of P. Plant N/P can reflect the biological characteristics of plants and is a key indicator of the degree of element restrictions in plants [47]. In this study, the leaf N/P ratio under the LD treatment, the stem N/P ratio under the MD treatment, and the thick and fine root N/P ratios under the SD treatment were significantly higher than the CK. This indicates that re-watering after drought relieved the restriction of N on the seedlings of P. yunnanensis.
During the plant growth process, all plant components promote growth and development and constantly interact with the surrounding environment for selection and adaptation, eventually achieving physiological and morphological adaptation [48]. Plant phenotypic plasticity is an important mechanism for plants to adapt to the environment and cope with adversity. It reflects the growth and development of plants, as well as the adaptability of plants to the environment [49,50]. In this study, the phenotypic plasticity indexes of leaf C/P, fine root ST, leaf P, leaf N/P, stem SS/ST, fine root NSC, and fine root SS/ST of P. yunnanensis seedlings were high, while fine root C, fine root N/P, leaf C, and stem C were low (Figure 3). PCA revealed leaf NSC, leaf P, stem C/P, stem SS/ST, thick root NSC, thick root ST, fine root NSC, and fine root ST to have high weight coefficients in the principal components (Figure 4). The results showed that the P. yunnanensis seedlings adapted to re-watering after drought, mainly by adjusting leaf NSC, leaf P, stem SS/ST, fine root ST, and fine root NSC.

5. Conclusions

In this study, the seedlings of P. yunnanensis were re-watered under different degrees of drought, and the changes in NSC, SS, and ST and C, N, and P stoichiometric characteristics were determined. The following key observations and conclusions were identified: The effects of drought re-watering on NSC and its components in P. yunnanensis seedlings were significant. After drought re-watering, the demand for the SS of P. yunnanensis seedlings increased. As the main substance of plant skeleton, element C had high stability in the P. yunnanensis seedlings. After drought re-watering, the availability of N in soil increased with the increase in water content. Drought re-watering can promote the formation of plant adaptation mechanism and promote the increase in P contents. Combining the phenotypic plasticity index and PCA results revealed that the P. yunnanensis seedlings adapted to re-watering by adjusting leaf NSC, leaf P, stem SS/ST, fine root ST, and fine root NSC. This study explored the recovery mechanism and adaptive strategies of P. yunnanensis to drought re-watering and provided a theoretical basis for future afforestation and management of P. yunnanensis.

Author Contributions

J.W. was the experimental designer of this study. C.L. collated the data and wrote the first draft of the paper. J.G. and H.D. participated in the experiments. 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 number 31960306.

Data Availability Statement

All data generated or analyzed during this study are included in the article.

Acknowledgments

The authors wish to thank the editor and the anonymous reviewers for their valuable insights.

Conflicts of Interest

The authors declare no conflicts of interest.

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Forests 15 01864 g001
Figure 1. Effect of drought re-watering on NSC and its components of P. yunnanensis seedlings. Different lowercase letters on the column superscripts indicate that the same organ exhibits significant differences among different treatments (p < 0.05). The same holds below. (A) schematic diagram of soluble sugar content. (B) schematic diagram of starch content. (C) schematic diagram of NSC content. (D) schematic diagram of soluble sugar/starch.
Figure 1. Effect of drought re-watering on NSC and its components of P. yunnanensis seedlings. Different lowercase letters on the column superscripts indicate that the same organ exhibits significant differences among different treatments (p < 0.05). The same holds below. (A) schematic diagram of soluble sugar content. (B) schematic diagram of starch content. (C) schematic diagram of NSC content. (D) schematic diagram of soluble sugar/starch.
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Figure 2. Effects of drought re-watering on the C, N, and P contents and the stoichiometry of P. yunnanensis seedlings. Different lowercase letters on the column superscripts indicate that the same organ exhibits significant differences among different treatments (p < 0.05). (A) schematic diagram of C content. (B) schematic diagram of N content. (C) schematic diagram of P content. (D) C/N schematic diagram. (E) C/P schematic diagram. (F) N/P schematic diagram.
Figure 2. Effects of drought re-watering on the C, N, and P contents and the stoichiometry of P. yunnanensis seedlings. Different lowercase letters on the column superscripts indicate that the same organ exhibits significant differences among different treatments (p < 0.05). (A) schematic diagram of C content. (B) schematic diagram of N content. (C) schematic diagram of P content. (D) C/N schematic diagram. (E) C/P schematic diagram. (F) N/P schematic diagram.
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Figure 3. Phenotypic plasticity index analysis of different organs of P. yunnanensis seedlings after drought re-watering.
Figure 3. Phenotypic plasticity index analysis of different organs of P. yunnanensis seedlings after drought re-watering.
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Figure 4. Principal component analysis of the NSC characteristics, C, N, and P contents, and their ratios in different organs of P. yunnanensis seedlings after re-watering. Dot colors represent different drought stress intensities; ellipses denote the confidence interval of each parameter under different drought stress intensities; and arrows represent the relationship between each index and the principal components. (A) principal component analysis of leaves. (B) principal component analysis of stem. (C) principal component analysis of thick roots. (D) principal component analysis of fine roots.
Figure 4. Principal component analysis of the NSC characteristics, C, N, and P contents, and their ratios in different organs of P. yunnanensis seedlings after re-watering. Dot colors represent different drought stress intensities; ellipses denote the confidence interval of each parameter under different drought stress intensities; and arrows represent the relationship between each index and the principal components. (A) principal component analysis of leaves. (B) principal component analysis of stem. (C) principal component analysis of thick roots. (D) principal component analysis of fine roots.
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Table 1. Two-factor analysis of variance of the effects of drought re-watering and organs on NSC content and its components of P. yunnanensis.
Table 1. Two-factor analysis of variance of the effects of drought re-watering and organs on NSC content and its components of P. yunnanensis.
FactorSoluble SugarStarchNSCSoluble Sugar/Starch
Organs1700.383 **1815.087 **2089.130 **590.947 **
Drought re-watering36.640 **870.676 **755.185 **163.356 **
Organs × drought re-watering464.096 **707.498 **707.979 **145.729 **
** p < 0.01. The same holds below.
Table 2. Two-way ANOVA of the effects of drought re-watering and organs on the C, N, and P contents and their stoichiometry in P. yunnanensis seedlings.
Table 2. Two-way ANOVA of the effects of drought re-watering and organs on the C, N, and P contents and their stoichiometry in P. yunnanensis seedlings.
FactorCNPC/NC/PN/P
Organs1.82213.559 **6.845 *2.921 *9.741 **7.811 **
Drought re-watering48.516 **60.177 **546.906 **6.040 *155.460 **152.568 **
Organs × drought re-watering7.765 *2.326 *17.817 **0.95740.125 **25.892 **
* p < 0.05; ** p < 0.01.
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Liu, C.; Wu, J.; Gu, J.; Duan, H. Response of Non-Structural Carbohydrates and Carbon, Nitrogen, and Phosphorus Stoichiometry in Pinus yunnanensis Seedlings to Drought Re-Watering. Forests 2024, 15, 1864. https://doi.org/10.3390/f15111864

AMA Style

Liu C, Wu J, Gu J, Duan H. Response of Non-Structural Carbohydrates and Carbon, Nitrogen, and Phosphorus Stoichiometry in Pinus yunnanensis Seedlings to Drought Re-Watering. Forests. 2024; 15(11):1864. https://doi.org/10.3390/f15111864

Chicago/Turabian Style

Liu, Chengyao, Junwen Wu, Jianyao Gu, and Huaijiao Duan. 2024. "Response of Non-Structural Carbohydrates and Carbon, Nitrogen, and Phosphorus Stoichiometry in Pinus yunnanensis Seedlings to Drought Re-Watering" Forests 15, no. 11: 1864. https://doi.org/10.3390/f15111864

APA Style

Liu, C., Wu, J., Gu, J., & Duan, H. (2024). Response of Non-Structural Carbohydrates and Carbon, Nitrogen, and Phosphorus Stoichiometry in Pinus yunnanensis Seedlings to Drought Re-Watering. Forests, 15(11), 1864. https://doi.org/10.3390/f15111864

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