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Article

Nitrogen Application Promotes Drought Resistance of Toona sinensis Seedlings

by
Xiaochi Yu
1,2,
Runhua He
3,
Fei Yi
4,
Ying Liu
2,
Peng Zhang
1,
Junhui Wang
2 and
Wenjun Ma
2,*
1
Forestry College, Northeast Forestry University, Harbin 150040, China
2
State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China
3
Hunan Botanical Garden, Changsha 410116, China
4
College of Biological and Pharmaceutical Sciences, Three Gorges University, Yichang 443002, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(8), 1351; https://doi.org/10.3390/f15081351
Submission received: 15 May 2024 / Revised: 31 July 2024 / Accepted: 1 August 2024 / Published: 2 August 2024
(This article belongs to the Section Forest Ecophysiology and Biology)
Browse Figures
Versions Notes

Abstract

:
A factorial design consisting of four N treatments (no N fertilization, 0.70, 0.14, and 0.28 mol N·plant−1) combined with two water conditions, drought (D = 25 ± 5% soil moisture content) and well-watered (W = 65 ± 5% soil moisture content), was used. Overall, the gas exchange parameters, chlorophyll, and growth of T. sinensis seedlings were significantly inhibited under drought conditions, while all of them showed improvement with N fertilizer, particularly at 0.14~0.28 mol N·plant−1. Under drought conditions, the root length and root surface area of T. sinensis increased; N application positively influenced the above root morphological changes. The activities of antioxidant enzymes such as superoxide dismutase (SOD; EC1.15.1.1) and peroxidase (POD; EC1.11.1.7) and the contents of osmotic adjustment substances such as soluble sugar and proline increased upon drought stress, but decreased under N application conditions. Overall, T. sinensis responds to drought stress through the synergistic action of drought resistance and drought tolerance mechanisms. N application enhances photosynthesis and improves root morphology, compensating for the need for osmotic regulation and reactive oxygen species scavenging.

1. Introduction

With the increasingly serious shortage of water resources, drought is becoming the main abiotic stress restricting plant growth and development [1,2]. Frequent and persistent droughts have caused limited photosynthesis, carbon distribution changes, slowed growth, expedited phenological period, and resulting death of trees and retreat of forests [3,4,5,6].
Plants respond to drought by adjusting their plasticity, increasing root length and surface area, and producing more fine roots, while reducing leaf area and leaf number and closing stomata to minimize water loss through transpiration [7,8].
Drought can also induce oxidative stress in plants, enhancing the activities of antioxidant enzymes such as SOD and POD, which help maintain the balance of reactive oxygen species and improve plant drought tolerance. Malondialdehyde (MDA) reflects the degree of lipid peroxidation in a plant membrane and serves as an important indicator of oxidative stress intensity. Osmotic regulatory substances such as proline, starch, and sugar increase to maintain cell swelling, thereby enhancing cell water retention capacity [9,10] and reducing MDA content.
In China, arid and semi-arid areas are predominantly located in the north, where soil N concentration in North China (except in Northeast China) is less than 1.0 g·kg−1, lower than the national average level (2.9 g·kg−1). This combination of drought and N deficiency constitutes a major constraint on forest growth and productivity [11]. Nitrogen (N) plays a crucial role in plant drought resistance, and applying an appropriate amount of N fertilizer can alleviate plant drought stress through the following: promoting plant stomatal closure, reducing water transpiration, and decreasing the rate of water loss, thereby alleviating plant water stress [12]. Additionally, N enhances the activity of the antioxidant system, enhances the resistance to oxidative stress caused by drought, and reduces cell damage. N can also help in osmotic regulation, maintaining cellular water balance and thereby enhancing the plant’s drought tolerance [13]. However, excessive application of N fertilizer can inhibit the root zone’s elongation, suppress water absorption, increase the plant’s sensitivity to drought, and aggravate the damage of drought stress to plant growth [14,15]. Therefore, optimizing plant growth and drought adaptation through judicious N management is crucial for determining appropriate application rates [16].
Toona sinensis, a precious timber species unique in China, features a straight trunk, excellent material and a beautiful texture, belongs to the Toona Roem Meliaceae. T. sinensis can also be used as an edible vegetable and medicinal material, with high medicinal and economic value. The species is widely distributed from the northeastern Liaoning Province (123°02′ E, 40°56′ W) to the southwestern Yunnan Province (97°31′ E, 21°8′ W), and most of its areas are arid or semi-arid regions. T. sinensis is facing significant challenges of drought stress. Pei et al. [17] demonstrated that N application can promote growth and enhance photosynthetic capacity in T. sinensis seedlings. However, there remains a dearth of comprehensive studies on the mechanism underlying nitrogen-mediated adaptation to drought stress in T. sinensis. In order to solve the following questions, a controlled trial was conducted: (i) What is the optimal range of N application levels that can promote plant growth and alleviate the negative effects of drought stress on T. sinensis in arid environments? (ii) How does T. sinensis respond to drought stress in terms of growth and physiology, and how does N regulate drought adaptability?

2. Materials and Methods

2.1. Plant Cultivation and Treatments

The experiment was conducted in the greenhouse of the Chinese Academy of Forestry (China, Beijing, 40°0′27″ N, 116°15′22″ E), a glass-enclosed greenhouse. The cuttings (length of ca. 15 cm, diameter of ca. 3–5 mm) of T. sinensis were rooted and planted in pots (one plant in each pot) with a mixture of vermiculite and perlite (Vvermiculite:Vperlite, 1:1). The plants were irrigated with tap water regularly and cultivated in the greenhouse (light: natural light; temperature during the day: 24 ± 2 °C; temperature at night: 18 ± 2 °C; relative humidity: 60 ± 5%) for a duration of four weeks.
Plants (120 plants in total) with similar growth performance were selected for further experiments. The plants were divided into two groups (60 plants in each group), which were provided with two water treatments [drought (D = 25 ± 5% soil moisture content) and water (W = 65 ± 5% soil moisture content)]. Each pot was weighed daily and water was added equivalent to the transpiration and evaporation rates of the plants. After watering, soil moisture content was measured using a soil moisture meter (VM-210S, VICOMETR, Taizhou, China) to maintain soil moisture levels at D = 25 ± 5% and W = 65 ± 5%.
The plants in each group were further divided into four subgroups (15 plants per subgroup) (Table 1). The plants in each subgroup were supplied with one of the following: no N fertilization, 0.07, 0.14, or 0.28 mol N (urea). In this instance, 0 mol N/subgroup indicates no N fertilization, serving as the control treatment. The urea was dissolved in the 100 mL nutrient solution and applied three times, once a month. The dosage for each application was 0.00 mol, 0.10 mol, 0.20 mol, and 0.40 mol, respectively. The drought and N treatments lasted four months. During the treatments, each plant was supplied with the basic nutrient solution without N (0.5 mM KCl, 0.9 mM CaCl2, 0.3 mM MgSO4, 0.6 mM KH2PO4, 42 μM K2HPO4, 10 μM Fe-EDTA, 2 μM MnSO4, 10 μM H3BO3, 7 μM Na2MoO4, 0.05 μM CoSO4, 0.2 μM ZnSO4, and 0.2 μM CuSO4; 100 mL every 5 days).

2.2. Harvesting

Gas exchange and leaf chlorophyll content were analyzed before harvesting. Nine leaves were selected from three seedlings with comparable growth; 3 leaves from the 3rd to 5th healthy functional leaves from top to bottom for each seedling were selected to measure photosynthetic rates (Pn), stomatal conductance (Cond), intercellular CO2 concentration (Ci), and transpiration rate (Tr) using a portable photosynthesis system (Li-6400, LI-COR Biosciences, Lincoln, NE, USA) and an LI-6400XT red and blue light source. The measurements were carried out from 09:00 to 11:00. During the measurement of gas exchange, the photosynthetic photon flux density (PPFD) was set at 1200 µmol·m−2·s−1, CO2 levels at 400 ppm, block temperature at 30 °C, and relative humidity (RH) at 44.7%. And the single leaf area of these nine leaves was scanned with a portable laser leaf area meter CI-203 (CID Bio Science, Inc., Camas, NE, USA). The images were analyzed and calculated with Image J software (version 6.0) after scanning (accurate to 0.01 cm2). Leaves (0.5 g) were collected to determine the chlorophyll content, and the measurement method was performed according to Wen [18].
After gas exchange, leaf area, and leaf chlorophyll content measurements, the same group of leaves was harvested and frozen in liquid nitrogen immediately and stored at −80 °C for further physiological analysis of MDA content, enzyme activities, soluble sugars, and proline. Root, stem, and leaf samples were dried separately at 70 °C for 72 h to determine biomass (0.01 g).

2.3. Root Characteristics

The root system of each plant was carefully washed and cleaned with paper to remove soil and water from the root surface. Subsequently, the total root length, root average diameter, root surface area, and root volume of each plant were scanned and analyzed using the WinRHIZO root analyzer system (WinRHIZO version 2012b, Regent Instruments, Montreal, QC, Canada).

2.4. Analysis of Nitrogen Concentration

After crushing roots, stems, and leaves with a tissue lyser II, the total N concentration of the crushed sample was determined using the Kjeldahl method, following the procedure described by Li et al. (2013) [7].

2.5. Analysis of Malondialdehyde (MDA)

Each frozen tissue sample was ground into a fine powder in liquid N2. The MDA content in leaves was quantified using the thiobarbituric acid method [7].

2.6. Determination of Enzymatic Activities, Soluble Sugars, and Proline

SOD activity and POD activity were measured via the nitroblue tetrazolium method (NBT) and the guaiacol method, respectively [16]. The soluble sugar content and free proline (Pro) in leaves were measured via anthrone colorimetry and spectrophotometry [19].

2.7. Statistical Analysis

The data were checked for normality and homogeneity before statistical analysis. Drought and nitrogen were set as both experimental factors. All data were tested using the two-way ANOVA procedure in SPSS (version 22.0). Multiple mean comparisons (Duncan test) were applied. Differences were considered to be significant if the p value was less than 0.05. The figures were prepared in GraphPad Prism (version 7).

3. Results

3.1. Gas Exchange and Chlorophyll Content

Gas exchange parameters (Pn, Cond, Ci, Tr) and chlorophyll content (Chl a and Chl b) of T. sinensis were inhibited significantly by drought (p < 0.01) (Figure 1 and Figure 2). N applications increased these characters under drought and water. Specifically, Pn, Cond, Ci, and Tr showed the highest values when 0.14 mol N·plant−1 was applied (Figure 1), and significantly higher values than the treatment without N fertilization. Chl a and Chl b reached their maximum values upon 0.28 mol N·plant−1 application (Figure 2), and these values were also significantly higher compared to the no N fertilization treatment.

3.2. Growth and Biomass

After 3 months of exposure to no N fertilization, 0.70 mol N·plant−1, 0.14 mol N·plant−1, or 0.28 mol N·plant−1 under drought and water, changes were observed in the growth of T. sinensis (Figure 3 and Figure 4). In particular, the root, stem, leaf, and total biomass and leaf area of T. sinensis were significantly suppressed by drought. Under both drought and water conditions, N remarkably stimulated the biomass and leaf area. Under drought, root, stem, leaf, and total biomass and leaf area with 0.14 mol N·plant−1 were the highest among all N treatments. However, leaf and root biomass and leaf area decreased when 0.28 mol N was applied. Under well-watered conditions, root and total biomass reached their maximum values when 0.14 mol N·plant−1 was applied, whereas the stem, leaf biomass, and leaf area were the highest when 0.28 mol N·plant−1 was applied.

3.3. Root Morphology

When N was not applied, the root length increased, while the average root diameter decreased under drought, with no significant impacts observed on root volume and root surface area (Figure 5). The root length, average root diameter, root volume, and root surface area were significantly affected by N. Under drought, root length, root surface area, and root volume initially increased and then decreased with increasing N application, and reached a maximum when 0.14 mol N·plant−1 was applied. Under well-watered conditions, the root length and root surface area were the largest upon 0.14 mol N·plant−1, whereas the average root diameter and root volume reached the maximum with 0.28 mol N·plant−1.

3.4. Nitrogen Concentrations

Drought inhibited the N concentrations of leaves of T. sinensis, but the effects of drought were alleviated gradually with increasing N application (Figure 6). Roots and leaves showed similar trends. Without N fertilization, the N concentrations of leaves, stems and roots were reduced by 38.1%, 41.8%, and 44.5% by drought, respectively. However, the minimal decrease occurred with 0.28 mol N·plant−1. The N concentration of each organ was stimulated with the application of N. Under well-watered conditions, N concentrations peaked within the range of 0.14 mol N·plant−1 to 0.28 mol N·plant−1, whereas in drought conditions, the maximum N concentrations in each organ were observed at the application of 0.28 mol N·plant−1.

3.5. MDA

Drought increased the MDA content of T. sinensis seedlings (Figure 7), while the application of N reduced the MDA content. When 0.14 mol N·plant−1 was applied, the MDA content (7.31 µmol/g) was significantly lower compared to the application of no N fertilization. N application effectively reduced the MDA content when water was sufficient. Similarly, when 0.14 mol N·plant−1 was applied, the MDA content was 4.69 µmol/g, significantly lower than when no N fertilization was applied. This showed that the 0.14 ± 0.07 mol N·plant−1 application is suitable for the growth of T. sinensis seedlings.

3.6. Antioxidant Physiological Changes

SOD and POD activity, as well as the contents of Pro and soluble sugar, all increased under drought, and the impact of drought gradually increased with the application of N (Figure 8). Compared to the water treatments, when no N fertilization was applied, SOD activity, POD activity, the soluble sugar content, and the Pro content increased by 91.18%, 37.87%, 65.15%, and 109.21%, respectively. With the application of 0.70 mol N·plant−1, POD activity, the soluble sugar content, and the Pro content increased by 44.70%, 39.07%, and 128.78%, respectively, compared with the water treatments. However, when 0.14 mol N·plant−1, and 0.28 mol N·plant−1 were applied, the increases in SOD activity, POD activity, and the soluble sugar content under drought conditions were not significant. Under the two water treatments, the activities of SOD and POD, as well as the contents of soluble sugar and Pro, all showed the same trend of first decreasing and then increasing with increasing N application, and all reached a minimum at 0.14 mol N·plant−1.

4. Discussion

4.1. Optimum Nitrogen Application Range

N is an essential nutrient element for plants, directly affecting their growth and development. Insufficient N inhibits plant protein synthesis, destroys chloroplast structure, affects photosynthesis, and reduces photosynthetic yield [20]. Conversely, excessive N reduces the fine root biomass and inhibits root development [21]. Excessive N application can also lead to soil leaching, acidification, and environmental pollution [22]. Therefore, it is crucial to determine the optimal N application range for plant growth. In this study, under the two water treatments, the root morphology of T. sinensis was better when 0.14 to 0.28 mol N/plant was applied (Figure 5). Additionally, the total biomass was higher (Figure 3), the photosynthetic performance was stronger (Figure 1), and malondialdehyde (MDA) content was lower (Figure 7). This can be attributed to the fact that appropriate N levels promote root development, which enhances water and fertilizer absorption and improves photosynthesis. The increased photosynthetic rates lead to greater dry matter accumulation and provide additional energy for cell division and elongation, thus accelerating the growth of T. sinensis, which is consistent with studies in sugarcane (Saccharum officinarum L.) [23]. In addition, appropriate N levels reduce the production and accumulation of reactive oxygen species (ROS), resulting in lower MDA content in T. sinensis, which is consistent with the findings in rice (Oryza sativa L.) [24]. In contrast, when the N application was lower than 0.14 mol N·plant−1, the biomass of T. sinensis decreased (Figure 3), the MDA content (Figure 7) increased significantly, and photosynthesis (Figure 1) was notably inhibited. This is due to the fact that low N inhibits photosynthesis, which leads to the excess of light energy, the increase in ROS and membrane lipid peroxides, the destruction of the ROS balance, and finally the inhibition of plant growth [25]. Therefore, under the experimental conditions, applying 0.14–0.28 mol N per plant was found to be suitable for annual cultivation growth.

4.2. Effects of Nitrogen on Drought Avoidance of T. sinensis

Plants can exhibit “drought avoidance” by reducing water loss and increasing water uptake, specifically by lowering Tr, increasing Cond, and undergoing adaptive changes in root morphology [26,27]. Additionally, plants can exhibit “drought tolerance” by maintaining tissue turgor through osmotic adjustment and maintaining the homeostasis of reactive oxygen species (ROS) via antioxidants [28,29]. Both mechanisms contribute to improved adaptation and yield of plants under drought stress.
As a drought avoidance mechanism, stomatal regulation plays a fundamental role in preventing water loss through transpiration. In this study, T. sinensis seedlings reduced water loss by decreasing leaf area, closing stomata, and lowering the Tr. However, stomata are channels for CO2 exchange between plant leaves and the environment, and their closure affects CO2 exchange, significantly inhibiting Pn (Figure 1). This ultimately impacts the synthesis of photosynthetic products, resulting in a significantly lower biomass of T. sinensis seedlings under drought conditions compared to well-watered conditions (Figure 3). Leaf N concentration and chlorophyll content largely determine the photosynthetic capacity [30,31]. After N application, the leaf N concentration (Figure 6) and chlorophyll content (Figure 2) of T. sinensis seedlings increased, enhancing photosynthetic capacity. Nevertheless, under drought conditions, the photosynthetic performance of T. sinensis remained lower than under well-watered conditions even with N application, indicating that N application alone could not restore the photosynthetic levels of T. sinensis seedlings under drought conditions to normal levels, which was consistent with the findings of Wang [32].
Root structure plasticity plays a key role in plant stress adaptation [13]. In this study, under varying N levels, although the root biomass, root diameter, and root volume of T. sinensis did not show significant changes, the roots primarily enhanced their water absorption capacity and alleviated the negative effects of drought by increasing root length and total surface area (Figure 3). This indicates that under drought conditions, plants can expand their root–soil contact area to enhance water and nutrient absorption [1]. Additionally, the increase in root length and surface area of T. sinensis, without significant changes in root biomass and volume, is due to the fact that fine roots require less carbon during formation while having strong water and nutrient absorption capabilities. Therefore, under drought conditions, T. sinensis maintain growth by increasing the smallest diameter of fine roots, which is consistent with the conclusion of Eissenstat [33]. When 0.14 mol N·plant−1 was applied under drought conditions, root length and surface area reached a maximum, significantly higher than the value when 0.28 mol N·plant−1 was applied (Figure 5). This suggests that appropriate N supply can enhance root plasticity [34] and promote root structure optimization [35]. However, under well-watered conditions, these traits were not significantly different when 0.14 mol N·plant−1 and 0.28 mol N·plant−1 were applied. This is because, under well-water conditions, there is no need for excessive adjustment of root morphology for water absorption, so the effect of N is relatively small. These findings highlight the capacity of drought to prompt T. sinensis seedlings to modify their root morphology, increase the contact area with soil, and enhance water and nutrients absorption. An appropriate amount of N fertilizer application can enhance the morphological adjustment ability, and further alleviate the negative effect of drought.

4.3. T. sinensis Copes with Drought through the Synergistic Coordination of Drought-Tolerance and Drought-Avoidance Mechanisms after Nitrogen Application

Plants accumulate osmosis substances, such as sugars and amino acids, to maintain cell turgor pressure and resist drought [11]. They can also enhance the activity of antioxidant enzymes and eliminate O2− and H2O2 produced by drought stress, thereby alleviating damage [36]. For example, under drought stress, cotton (Gossypium hirsutum L.) mitigates oxidative stress caused by excessive MDA by increasing the content of free amino acids and soluble proteins (Pro) [37]. Wheat (Triticum aestivum L.) enhances drought resistance by increasing the activity of antioxidant enzymes (SOD, POD, catalase) and increasing the content of osmoregulatory substances such as soluble sugars (SS), soluble proteins (SP), and Pro [38]. In this study, T. sinensis improved osmotic regulation by increasing the content of soluble sugar and Pro, and protected membrane protein integrity. It also elevated the activity of SOD and POD to scavenge reactive oxygen species like O2− and H2O2 (Figure 8). MDA is an important indicator of oxidative damage under stress [39]. In this study, the increased content of soluble sugar and Pro, along with enhanced SOD and POD activity, led to a reduction in MDA levels, thereby improving drought tolerance in T. sinensis.
However, as N application increased, the response ability of these characteristics to drought decreased. Under both water treatments, N application reduced the content of osmoregulatory substances and slowed the activity of antioxidant enzymes in T. sinensis (Figure 8). This is inconsistent with the previous conclusion that an appropriate amount of N can enhance the osmotic adjustment and antioxidant capacity, promote drought adaptation, and maintain growth [34]. This discrepancy is likely due to the need to reduce water loss during drought, which led to a decrease in the number and area of leaves (Figure 4). Consequently, the energy demand for leaf growth decreased, leading to increased soluble sugar content. After applying an appropriate amount of N, leaf number and area increased, enhancing N assimilation, which required the consumption of more organic carbon and energy, resulting in a decrease in soluble sugar content. Additionally, with the increase in the N application amount, the root system transported more nitrate into the leaves for participation in osmotic regulation, reducing the demand for Pro and other substances [40,41]. On the other hand, T. sinensis gradually increased its drought resistance by adjusting the root morphology to absorb more water. At this time, the demand for alleviating the negative effects of drought through osmotic regulation and reactive oxygen species removal declined. Therefore, with increasing N application, the content of osmotic adjustment substances decreased, and the activity of antioxidant enzymes in T. sinensis also decreased. Based on these findings, it can be inferred that in the drought response of T. sinensis, the mechanisms such as adjusting root morphology, reducing transpiration water loss, and improving antioxidant capacity may have a certain compensatory effect. Adjusting root morphology and improving photosynthetic capacity likely play a major role. These findings enrich our comprehension of the drought resistance of plants.
T. sinensis reduces leaf area, closes stomata, and decreases Tr to minimize water loss (Figure 9). It increases root length and root surface area to expand the root–soil interface, thereby enhancing water and nutrient absorption capacity. This ultimately reduces water loss and increases water uptake to improve drought resistance. Simultaneously, T. sinensis employs enzymatic and non-enzymatic antioxidant systems to scavenge reactive oxygen species and protect membrane proteins, thereby enhancing drought tolerance. Application of appropriate N enhances leaf N concentration, promoting photosynthesis and increasing assimilate production. Photosynthetic products allocated to the root system prioritize synthesis of fine roots with low carbon requirements but strong water and nutrient absorption capabilities. Therefore, N application ultimately enhances T. sinensis’s drought resistance by increasing their contact area with the soil. However, N application also reduces the need for osmotic regulation and the scavenging of reactive oxygen species to mitigate drought stress. Consequently, N application reduces the content of osmotic regulatory substances and decreases antioxidant enzyme activity in T. sinensis. Therefore, after the application of an appropriate amount of N, the content of osmotic regulatory substances in T. sinensis decreased, and the antioxidant enzyme activity in T. sinensis was reduced. This indicates that the drought resistance and drought tolerance mechanisms of T. sinensis work synergistically to cope with drought stress. N application enhanced photosynthesis and improved root morphology, compensating for the need for osmotic regulation and reactive oxygen species scavenging. These findings enrich our understanding of plant drought resistance.

5. Conclusions

In conclusion, the application of 0.14~0.28 mol N·plant−1 is most effective in enhancing the drought resistance of annual T. sinensis seedlings. Under drought stress, T. sinensis responds to drought stress through the synergistic action of drought resistance and drought tolerance mechanisms. N application enhances photosynthesis and improves root morphology, compensating for the need for osmotic regulation and reactive oxygen species scavenging (Figure 9).

Author Contributions

R.H., F.Y. and Y.L. conducted the experiments, collected the data, and analyzed them; J.W. and W.M. supervised the research work; writing and editing of the manuscript was carried out by X.Y., F.Y., P.Z. and W.M. All authors reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research work was funded by the National Key R&D Program of China (2021YFD2200305). Therefore, the authors gratefully acknowledge the Chinese Academy of Forestry Sciences.

Data Availability Statement

The original contributions presented in the study are included in the article; further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. The effect of different nitrogen concentrations on gas exchange in T. sinensis under water and drought conditions. Pn, photosynthetic rate (a); Cond, stomatal conductance (b); Ci, intercellular CO2 concentration (c); and Tr, transpiration rate (d) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), nitrogen treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; ns, not significant.
Figure 1. The effect of different nitrogen concentrations on gas exchange in T. sinensis under water and drought conditions. Pn, photosynthetic rate (a); Cond, stomatal conductance (b); Ci, intercellular CO2 concentration (c); and Tr, transpiration rate (d) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), nitrogen treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; ns, not significant.
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Figure 2. The effect of different N concentrations on chlorophyll content in T. sinensis under water and drought conditions. Chl a, chlorophyll a contents (a) and Chl b, chlorophyll b contents (b) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments by the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; ns, not significant.
Figure 2. The effect of different N concentrations on chlorophyll content in T. sinensis under water and drought conditions. Chl a, chlorophyll a contents (a) and Chl b, chlorophyll b contents (b) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments by the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; ns, not significant.
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Figure 3. The effect of different N concentrations on biomass in T. sinensis under water and drought conditions. Total biomass, root biomass, stem biomass, and leaf biomass under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. * p < 0.05, the same applies below. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
Figure 3. The effect of different N concentrations on biomass in T. sinensis under water and drought conditions. Total biomass, root biomass, stem biomass, and leaf biomass under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. * p < 0.05, the same applies below. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
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Figure 4. The effect of different N concentrations on biomass in T. sinensis under water and drought conditions. Leaf area under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5.
Figure 4. The effect of different N concentrations on biomass in T. sinensis under water and drought conditions. Leaf area under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5.
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Figure 5. The effect of different N concentrations on root morphology in T. sinensis under water and drought conditions. Length, total root length (a); AvgDiam, root average diameter (b); SurfArea, root surface area (c); and Volume, root volume (d) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; ns, not significant.
Figure 5. The effect of different N concentrations on root morphology in T. sinensis under water and drought conditions. Length, total root length (a); AvgDiam, root average diameter (b); SurfArea, root surface area (c); and Volume, root volume (d) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; ns, not significant.
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Figure 6. The effect of different N concentrations on N concentrations in T. sinensis under water and drought conditions. Root N concentration (a), stem N concentration (b), and leaf N concentration (c) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
Figure 6. The effect of different N concentrations on N concentrations in T. sinensis under water and drought conditions. Root N concentration (a), stem N concentration (b), and leaf N concentration (c) under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
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Figure 7. The effect of different N concentrations on MDA in T. sinensis under water and drought conditions. MDA, malondialdehyde content under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
Figure 7. The effect of different N concentrations on MDA in T. sinensis under water and drought conditions. MDA, malondialdehyde content under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
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Figure 8. The effect of different N concentrations on antioxidant physiological characteristics in T. sinensis under water and drought conditions. SOD activity, superoxide dismutase enzyme activity (a); POD activity, peroxidase enzyme activity (b); soluble sugar, soluble sugar content (c); Pro, protein content (d). under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
Figure 8. The effect of different N concentrations on antioxidant physiological characteristics in T. sinensis under water and drought conditions. SOD activity, superoxide dismutase enzyme activity (a); POD activity, peroxidase enzyme activity (b); soluble sugar, soluble sugar content (c); Pro, protein content (d). under drought and water treatments with no N fertilization, 0.70 mol N, 0.14 mol N, or 0.28 mol N·plant−1. Different letters on the bars indicate significant differences in each index among eight treatments via the Duncan test (p < 0.05). p values obtained from the two-way ANOVAs for water treatments (W), N treatments (N), and their interactions (N × W) are indicated. ** p < 0.01; * 0.01 < p < 0.5, ns, not significant.
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Figure 9. Schematic model of N application to alleviate drought stress in T. sinensis. Under drought, T. sinensis seedlings can obtain more water and fertilizer by adjusting the root configuration and increasing the contact area between roots and soil. Applying an appropriate amount of N could enhance this morphological plasticity and further relieve the negative effect of drought. The application of N also increased the leaf N concentration and chlorophyll content of T. sinensis, promoted the photosynthetic rate, and compensated for the photosynthetic loss caused by drought. Thus, the growth of seedlings was promoted. Additionally, T. sinensis seedlings also adapted to drought by increasing osmotic adjustment substances and improving antioxidant capacity. Moreover, N application alleviated the negative effects of drought on T. sinensis seedlings by adjusting root morphology and improving photosynthetic capacity, and these adaptations offset some of the need for antioxidants.
Figure 9. Schematic model of N application to alleviate drought stress in T. sinensis. Under drought, T. sinensis seedlings can obtain more water and fertilizer by adjusting the root configuration and increasing the contact area between roots and soil. Applying an appropriate amount of N could enhance this morphological plasticity and further relieve the negative effect of drought. The application of N also increased the leaf N concentration and chlorophyll content of T. sinensis, promoted the photosynthetic rate, and compensated for the photosynthetic loss caused by drought. Thus, the growth of seedlings was promoted. Additionally, T. sinensis seedlings also adapted to drought by increasing osmotic adjustment substances and improving antioxidant capacity. Moreover, N application alleviated the negative effects of drought on T. sinensis seedlings by adjusting root morphology and improving photosynthetic capacity, and these adaptations offset some of the need for antioxidants.
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Table 1. Water and nitrogen treatments of T. sinensis seedlings.
Table 1. Water and nitrogen treatments of T. sinensis seedlings.
Nitrogen Application Amount/mol N·plant−10.000.070.140.28
D (drought treatment,
D = 25 ± 5% soil moisture content)		D0D1D2D4
W (well-watered treatment,
W = 65 ± 5% soil moisture content)		W0W1W2W4
Note: This study was divided into two water treatments, drought (D = 25 ± 5% soil moisture content) and well-watered treatment (W = 65 ± 5% soil moisture content), each further subdivided into four N treatments: application of 0.00, 0.07, 0.14, and 0.28 mol N, totaling eight treatments. D0, D1, D2, D4 denote the application of 0.00, 0.07, 0.14, and 0.28 mol N under drought conditions, respectively. W0, W1, W2, W4 denote the application of 0.00, 0.07, 0.14, and 0.28 mol N under well-watered conditions, respectively.
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Yu, X.; He, R.; Yi, F.; Liu, Y.; Zhang, P.; Wang, J.; Ma, W. Nitrogen Application Promotes Drought Resistance of Toona sinensis Seedlings. Forests 2024, 15, 1351. https://doi.org/10.3390/f15081351

AMA Style

Yu X, He R, Yi F, Liu Y, Zhang P, Wang J, Ma W. Nitrogen Application Promotes Drought Resistance of Toona sinensis Seedlings. Forests. 2024; 15(8):1351. https://doi.org/10.3390/f15081351

Chicago/Turabian Style

Yu, Xiaochi, Runhua He, Fei Yi, Ying Liu, Peng Zhang, Junhui Wang, and Wenjun Ma. 2024. "Nitrogen Application Promotes Drought Resistance of Toona sinensis Seedlings" Forests 15, no. 8: 1351. https://doi.org/10.3390/f15081351

APA Style

Yu, X., He, R., Yi, F., Liu, Y., Zhang, P., Wang, J., & Ma, W. (2024). Nitrogen Application Promotes Drought Resistance of Toona sinensis Seedlings. Forests, 15(8), 1351. https://doi.org/10.3390/f15081351

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