Next Article in Journal
Land Use Preference for Ecosystem Services and Well-Being in Chittagong Hill Tracts of Bangladesh
Next Article in Special Issue
Grafting with Different Rootstocks Induced DNA Methylation Alterations in Pecan [Carya illinoinensis (Wangenh.) K. Koch]
Previous Article in Journal
Mechanical Properties of Three Bamboo Species: Effect of External Climatic Conditions and Fungal Infestation in Laboratory Conditions
Previous Article in Special Issue
In Situ Rainwater Collection and Infiltration System Alleviates the Negative Effects of Drought on Plant-Available Water, Fine Root Distribution and Plant Hydraulic Conductivity
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 13
Issue 12
10.3390/f13122085
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Root Development in Cunninghamia lanceolata and Schima superba Seedlings Expresses Contrasting Preferences to Nitrogen Forms

by
Haiyan Liang
,
Lidong Wang
,
Yanru Wang
,
Xiaoqiang Quan
,
Xiaoyu Li
,
Yaning Xiao
and
Xiaoli Yan
*
College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
Author to whom correspondence should be addressed.
Forests 2022, 13(12), 2085; https://doi.org/10.3390/f13122085
Submission received: 29 September 2022 / Revised: 30 November 2022 / Accepted: 5 December 2022 / Published: 7 December 2022
(This article belongs to the Special Issue Strategies for Tree Improvement under Stress Conditions)
Browse Figures
Versions Notes

Abstract

:
The inorganic nitrogen (N) that can be absorbed and utilized by plants is mainly ammonium N (NH4+-N) and nitrate N (NO3−-N), which may affect seedlings’ root morphology and growth through its heterogeneous distribution. Root morphology and seedling growth were investigated in a subtropical major conifer (Cunninghamia lanceolata) and a broadleaf tree species (Schima superba) under five different NH4+-N to NO3−-N ratios (10:0, 0:10, 7:3, 3:7, 5:5). Results: (1) While both species developed thinner roots under the treatment with a high NO3−-N concentration, the roots of C. lanceolata were longer than those of S. superba. In contrast, the roots of both species were thicker under the treatment with a high NH4+-N concentration, with those in S. superba being much longer than those in C. lanceolata. (2) The mixed NH4+-N and NO3−-N treatments were more conducive to the aboveground growth and biomass accumulation of both tree species and the underground growth of S. superba. N sources with high NO3−-N concentrations were more suitable for underground growth in C. lanceolata seedlings and aboveground growth in S. superba seedlings. Under the N sources with high NH4+-N concentrations, C. lanceolata tended to develop aboveground parts and S. superba tended to develop underground parts. (3) The roots of the two tree species adopted the expansion strategy of increasing the specific root length and reducing the root tissue density under the N sources with high NO3−-N concentrations but the opposite with high NH4+-N concentrations. The root-to-shoot ratio of C. lanceolata increased under high NO3−-N concentrations, while that of S. superba increased under high NO3−-N concentrations. These results indicate that the responses of root morphology to different N forms are species-specific. Furthermore, according to the soil’s N status, NH4+-N can be appropriately applied to C. lanceolata and NO3−-N to S. superba for cultivating seedlings.

1. Introduction

Nitrogen (N) is an essential mineral element for plant growth. The inorganic nitrogen that can be absorbed and utilized by plants is mainly ammonium nitrogen (NH4+-N) and nitrate nitrogen (NO3−-N). The two forms of N in soils are not uniformly distributed but instead occur in different proportions and change with time, so they are distributed heterogeneously in time and space [1,2]. Studies have shown that the ratio of NH4+-N and NO3−-N in the soil ranges from 8:2 to 2:8 [3]. Heterogeneous environments with different ammonium and nitrate contents will have different effects on plant growth. In one study, mixed nitrogen culture was more conducive to the growth of the aboveground parts of Citrus Sinensis × Poncirus trifoliata seedlings than nitrogen alone, and the best effect was observed at an ammonium to nitrate ratio of 5 to 5 [4]. The growth of the aboveground and underground parts of Pinus massoniana seedlings cultured from tissue both reached the maximum value under the ammonium nitrogen-only treatment [5]. When plants grow in an environment with a heterogeneous distribution of different forms of N, especially for a long time, they adopt different adaptation mechanisms for the underground and aboveground parts, and the roots’ regulatory pathway is particularly important.
As the main nutrient-absorbing organ in plants, the root system carries out nutrient exchange and metabolism for the underground and aboveground parts of the plant. Under natural soil nutrient adversity, tree roots can explore, acquire and utilize limited soil nutrient resources through regulating their morphology, physiology and mycorrhizal plasticity [5,6]. With the intensification of global N deposition, the plastic response of plants’ root morphology and structure [root length (RL), root surface area (RSA), root average diameter (RAD), root volume (RV), specific root length (SRL), etc.] to soil N is the most direct manifestation of plants’ ability to adapt to environmental changes and seek nutrients [6,7]. Under different N forms, the root morphology of plants will show different nitrogen-seeking strategies [8]. Studies have shown that mixed nitrogen can increase the surface area of the root system and increase RL and the number of root tips, thereby increasing the absorption capacity of the root system and promoting aboveground growth [9]. When the supply ratio of NO3−-N was higher than 50%, the root quality of Larix gmelinii seedlings decreased significantly [10]. The biomass of shoots and lateral roots of Cunninghamia lanceolata seedlings was largest under NH4+-N treatment [11]. However, compared with the NH4+-N treatment, hybrid poplar plants under a NO3−-N treatment exhibited a higher proportion of fine roots, thicker roots and bigger SRL [12]. C. lanceolata roots also tend to grow in NO3−-N patches, while Schima superba and P. massiniana tend to grow more and finer roots in NH4+-N patches [8]. In an environment of nitrogen deficiency, plants will adjust their nitrogen-seeking strategies by increasing the SRL and root-to-shoot ratio (RSR) [13,14]. Plants’ biomass allocation can reflect the nutrient utilization of plant organs [15]. According to the optimal balance theory, plants tend to allocate resources to organs that can obtain restricted resources in order to obtain more restricted resources [16,17]. The SRL, root tissue density (RTD) and RSR can reflect the carbon allocation strategy of plants from different perspectives, which also conforms to the theory of root economics [18,19]. Therefore, studying the morphological characteristics of plant roots can intuitively reveal the nutrient uptake status of plants and their growth status.
C. lanceolata is an important fast-growing afforestation tree species in southern China. In recent decades, C. lanceolata forests have mostly been cultivated as artificial forests. The continuous planting of forest stands and soil acidification have led to the exhaustion of forestland, declines in the yield of forest stands, and reductions in the forests’ ecological services [20,21]. Some studies have found that, in view of the problem of soil fertility declining after continuous planting of coniferous species, broadleaf tree species can effectively improve soil fertility and can thus be used as soil-improving tree species for mixed planting with conifers [22]. As an evergreen broadleaf tree species, S. superba produces a large amount of litter that decomposes quickly and contains high amounts of nutrients, which is conducive to water storage and fertilizer conservation. Therefore, S. superba is mostly used for mixing with coniferous species such as C. lanceolata to create a mixed coniferous and broadleaf forest. The resulting economic and ecological benefits have received widespread attention.
At present, research on the effects of different N forms on plant roots has mostly been conducted in crops, herbs and fruit trees, and research on the effects on roots of woody plants such as forest tree species is relatively limited and incomplete, especially regarding the coexistence mechanism of mixed C. lanceolata and S. superba forests. We hypothesized that the N uptake strategies of the roots of C. lanceolata and S. superba are different for different N forms. In view of this, in this experiment, the potted sand culture method was used to avoid the interference of soil N and to test the effects of different N forms on the morphological plasticity of C. lanceolata and S. superba roots’ responses to N uptake and their differences.

2. Materials and Methods

2.1. Plant Materials

The test materials used in this study were selected from C. lanceolata and S. superba, the two main coniferous and broadleaf tree species occurring in mixed stands in the subtropical zone. One-year-old seedlings with uniform growth that were free from disease and insect pests and had a complete root system were selected as the test seedlings. Plastic pots (26 cm diameter × 28 cm height) were used for cultivating the seedlings. The potting substrate selected was clean sand, which was repeatedly washed with distilled water until the N content in the sand was close to zero [23,24].

2.2. Experimental Setup

In April 2021, the sand culture experiments were conducted in a rainproof greenhouse with good ventilation and light transmission at Fujian Agriculture and Forestry University, China. The average temperature was 20.1 °C and the average relative humidity was about 77%. Each pot was filled with equal amount of clean sand. A matrix environment with different proportions of two N forms was constructed using different concentrations of NH4+-N and NO3−-N in the nutrient solution.
According to the research results of Zhang et al. [25] on the influence of fertilization on the soil nutrient content of C. lanceolata and the previous research results of Meng et al. [26] and Liu et al. [27], the total N concentration was set to 2 mmol·L−1. In this study, we used five different ratios of NH4+-N and NO3−-N supplied as NH4+-N:NO3−-N = 10:0, 0:10, 7:3, 3:7 and 5:5 (Table 1). The 10:0 and 0:10 treatments had highly heterogeneous N, 7:3 and 3:7 had medium heterogeneous N, and 5:5 had homogeneous N. NH4+-N was supplied as (NH4)2SO4, while NO3−-N was supplied as NaNO3. In all treatments, while the concentration of the two forms of N were different, the content of the macronutrients (Hoagland formula) and micronutrients (Amon formula) remained the same. To prevent the conversion of ammonium to nitrate, the nitrification inhibitor dicyandiamide (7 μmol·L−1) was added to the nutrient solution. The pH of the nutrient solution was adjusted to 5.8 with 2 mol·L−1 NaOH or HCl. Each treatment had six replicates, and the total number of pots was 60. The nutrient solutions were added to the corresponding compartments at a rate of 50 mL every 5 days. Each pot was supplied with 150 mL of distilled water every 2–3 days. We did not water the pots for 24 h before and after pouring in the nutrient solution.

2.3. Plant Harvesting and Data Collection

All the seedlings were harvested after 160 days of cultivation. The initial and final plant height and ground diameter of all seedlings were measured and recorded. Plants were separated into three parts: roots, stems and leaves. The fresh stems and leaves were oven-dried at 105 °C for half an hour to deactivate the enzymes and then at 65 °C to a constant weight.
The roots in each treatment were harvested carefully, cleaned with distilled water and dried with filter paper. We imaged all the roots using an Epson Expression 12,000XL scanner (Seiko Epson Corporation, Suwa, Nagano, Japan) and analyzed the images with WinRHIZO software (Pro2017a, Regent Instruments Inc., Quebec, Canada) to obtain the roots’ morphological parameters, including the total root length (TRL, cm), total root surface area (TRSA, cm2), total root volume (TRV, cm3) and the roots’ average diameter (RAD, mm). After scanning, all the roots were oven-dried at 105 °C for half an hour to deactivate the enzymes and then at 65 °C to a constant weight. The total seedling biomass (TSB, g) of the seedlings was the sum of the root, stem and leaf biomass in each treatment.

2.4. Data Analysis

All the data were processed and analyzed in Excel 2016 (Microsoft Office, Washington, Redmond, WA, USA). The increments in seedling height (ΔH, cm) and ground diameter (ΔGD, mm) were calculated by subtracting the seedlings’ initial height and ground diameter from the final height and ground diameter, respectively. Specific root length (SRL, cm·g−1) was calculated as total root length/total root biomass (TRB, g). Root tissue density (RTD, g·cm−3) was calculated by dividing the root biomass by the total root volume. The root-to-shoot ratio (RSR) was calculated as the ratio of root biomass to aboveground biomass.
Statistical analyses were conducted using SPSS 25.0 for Windows (SPSS Inc., Chicago, IL, USA). One-way ANOVA was conducted to evaluate the effect of nitrogen forms on the seedlings’ ΔH, ΔGD, TRL, TRSA, TRV, RAD, TRB, TSB, SRL, RTD and RSR. Two-way ANOVA was performed on the effects of tree species and different N forms on the roots’ morphological parameters, and plots were created using Origin 2018 (OriginLab, Northampton, USA). In this study, the ammonium and nitrate N concentrations were used as environmental factor variables, and the root and growth parameters of plants were used as biological factor variables to reflect the relationships among the parameters. The redundancy analysis (RDA) was conducted in Canoco 5.0 (Microcomputer Power, Ithaca, NY, USA).

3. Results

3.1. Significance Test of the Effects of Tree Species and Different Ratios of N Forms on the Seedlings’ Growth and the Roots’ Morphological Parameters

Table 2 shows that tree species and different N forms (a × b) had significant interaction effects on ΔH and ΔGD, TRL, TRSA, TRV, TRB, RTD and RSR (p < 0.05), while the interaction effect on RAD, TSB and SRL did not reach a significant level (p > 0.05). Separately, the effects of tree species (a) and different N forms (b) on all indicators reached the very significant level (p < 0.01), except for TRV under different ammonium to nitrate ratios, which reached the significant level (p < 0.05).

3.2. Effects of Different N Forms on Root Morphology in the Two Tree Species

The roots’ parameters were significantly influenced by the different N forms in each treatment (p < 0.05) (Figure 1). Under the five different ratios of the N forms, the TRL and TRSA of C. lanceolata followed the order 10:0 < 7:3 < 3:7 < 5:5 < 0:10 (Figure 1a,c). Under the NO3−-N-only treatment, the TRL and TRSA were 16.54–70.42% and 18.58–42.68% higher, respectively, than those under the other four treatments. The TRV followed the order 10:0 < 5:5 < 7:3 < 3:7 < 0:10 (Figure 1e). It was largest under the NO3−-N-only treatment, which was 11.48–24.64% larger than that under the other four treatments. The RAD of C. lanceolata followed the order 5:5 < 0:10 < 7:3 < 3:7 < 10:0 (Figure 1g), and was significantly larger under the NH4+-N-only treatment than under the other four treatments. In general, the roots of C. lanceolata preferred to grow under the treatments with higher NO3−-N concentrations.
The TRL, TRSA and TRV of S. superba followed the order 3:7 < 10:0 < 0:10 < 7:3 < 5:5 (Figure 1b,d,f). The TRL, TRSA and TRV under the 5:5 ratio were 15.42–76.27%, 9.19–71.05% and 7.97–72.24% larger, respectively, than those of the other four treatments. The RAD of S. superba followed the order 5:5 < 0:10 < 3:7 < 7:3 < 10:0 (Figure 1h). It showed the maximum value under the NH4+-N-only treatment, which did not differ significantly from that under the 7:3 treatment but was significantly greater than that under the other three treatments, showing a minimum value at a ratio of 5:5. The morphological parameters of the root system of S. superba were superior in the treatments with higher NH4+-N concentrations.

3.3. Effects of Different N Forms on Biomass in the Two Tree Species

The TRB of one-year-old seedlings of C. lanceolata ranged from 2.26 to 2.74 g·tree−1 after 160 days of the experimental treatment (Figure 2a), and the TSB was 8.59–9.71 g·tree−1 (Figure 2c). The TRB followed the order 3:7 > 0:10 > 5:5 > 7:3 >10:0, and there were no significant differences among the 3:7, 0:10 and 5:5 ratios (p > 0.05). Conversely, the TSB was largest under the NH4+-N-only treatment and followed the order 10:0 > 5:5 > 7:3 > 3:7 > 0:10. TRB accumulation was higher under the treatment with a high NO3−-N concentration than that with a high NH4+-N concentration. However, the TSB in C. lanceolata tended to accumulate at high NH4+-N concentrations and homogeneous N supply.
The TRB of S. superba seedlings ranged from 0.34 to 0.56 g·tree−1 (Figure 2b) and the TSB was 3.12–4.10 g·tree−1 (Figure 2d). The TRB followed the order 7:3 > 5:5 > 10:0 > 0:10 > 3:7, while the TSB followed the order 5:5 > 3:7 > 7:3 > 0:10 > 10:0. The TRB accumulation in S. superba was higher under the treatment with a high NH4+-N concentration and homogeneous N supply than under the treatment with a high NO3−-N concentration, while the TSB tended to accumulate under the treatments with homogeneous and medium heterogeneous N supply. The environment with highly heterogeneous N supply was the most unfavorable for the accumulation of TSB in S. superba.

3.4. Effects of Different N Forms on Root Abundance in the Two Tree Species

The SRL of C. lanceolata followed the order 0:10 > 5:5 > 7:3 > 3:7 > 10:0 (Figure 3a) and was the highest under the NO3−-N-only treatment, which was not significantly different from that under the control treatment (5:5) (p > 0.05) but was significantly higher than that under the other three treatments (p < 0.05). The RTD of C. lanceolata followed the order 3:7 > 5:5 > 10:0 > 7:3 > 0:10 (Figure 3c). There were no significant differences between the 3:7 and 5:5 ratios, but both of these treatments resulted in a significantly higher RTD than the other three treatments. In contrast, the RSR followed the order 0:10 > 3:7 > 7:3 > 5:5 > 10:0 (Figure 3e), showing higher values under the treatment with a high NO3−-N concentration.
The SRL of S. superba followed the order 5:5 > 0:10 > 3:7 > 10:0 > 7:3 (Figure 3b), showing a higher value under the treatment with a homogeneous N supply and a high NO3−-N level. The difference between the 5:5 and 0:10 ratios was not significant, but both of them had a significantly higher SRL than the other three treatments. The RTD of S. superba followed the order of 10:0 > 7:3 > 3:7 > 0:10 > 5:5 (Figure 3d), showing that the heterogeneous N supply resulted in a higher RTD than the homogeneous N supply. Moreover, the treatments with a high NH4+-N level resulted in a higher RTD than the treatments with a high NO3−-N level. The RSR followed the order 7:3 > 10:0 > 0:10 > 5:5 > 3:7 (Figure 3f) and was highest under the treatments with high NH4+-N.

3.5. Effects of Different N Forms on Aboveground Growth in the Two Tree Species

After 160 days of cultivation, the ΔH of C. lanceolata and S. superba seedlings was 10.2–17.7 cm and 7.0–10.5 cm (Figure 4a), respectively, and the ΔGD was 3.08–4.35 mm and 2.18–3.62 mm (Figure 4b), respectively. It can be seen that the ΔH and ΔGD of C. lanceolata were larger than those of S. superba.
Under different N forms, the ΔH of C. lanceolata followed the order 5:5 > 7:3 > 3:7 > 10:0 > 0:10 and was largest under the control treatment (Figure 4a), which was 9.05–73.20% larger than that under the other treatments. The ΔH of C. lanceolata was greater under the homogeneous N supply than under the heterogeneous N supply, and it was smallest under the NH4+-N-only and NO3−-N-only treatments. The ΔH of S. superba followed the order 5:5 > 3:7 > 0:10 > 7:3 > 10:0 and was largest under the control treatment (Figure 4a), which was 12.93–49.05% larger than that under the other treatments. The ΔH of S. superba was greater under the homogeneous N supply than the heterogeneous N supply, and it was greater under the treatment with a high NO3−-N concentration than under the treatment with a high NH4+-N concentration. In the two tree species, seedling height initially increased and then decreased with the increase in NO3−-N in the nutrients.
The ΔGD of C. lanceolata followed the order 7:3 > 5:5 > 10:0 > 0:10 > 3:7 and was largest at the ammonium to nitrate ratio of 7:3 (Figure 4b), which was 15.09–41.26% larger than that under the other treatments. The ΔGD of S. superba followed the order 0:10 > 3:7 > 7:3 > 5:5 > 10:0 (Figure 4b). It was largest at an ammonium to nitrate ratio of 0:10, which was 8.92–66.51% larger than that under the other treatments. Overall, C. lanceolata tended to increase the ground diameter of the seedlings under the treatment with a high NH4+-N concentration and a homogeneous N supply, whereas S. superba preferred to increase the ground diameter under the treatment with a high NO3−-N concentration.

3.6. Redundancy Analysis of Ammonium and Nitrate N Concentrations with Root and Growth Parameters

We used N forms as the environmental factor variables, and a redundancy analysis was performed on the roots’ morphological and growth parameters of C. lanceolata (Figure 5a) and S. superba (Figure 5b). A smaller angle between them (close to 0°) indicated that the positive correlation was significant, and a larger angle (close to 180°) indicated that the negative correlation was significant.
Figure 5a shows that the RAD, ΔGD and TSB of C. lanceolata had a positive correlation with NH4+-N and a negative correlation with NO3−-N. However, the ΔH and RTD decreased along the Y-axis, and the correlation with NH4+-N was not significant. In contrast, the RSR, TRB, SRL, TRL, TRSA and TRV of C. lanceolata had a positive correlation with NO3−-N and a negative correlation with NH4+-N. Among these, the RSR had the strongest positive correlation with NO3−-N. The RAD and RTD had a negative correlation with SRL.
Figure 5b shows that the RSR, RAD, TRB and RTD of S. superba had a positive correlation with NH4+-N and a negative correlation with NO3−-N. Conversely, the ΔGD, ΔH and TSB of S. superba had a positive correlation with NO3−-N and a negative correlation with NH4+-N. However, the correlations of TRSA, TRL and TRV with NH4+-N and that of SRL with NO3−-N were not significant. Among these, the ΔGD had the strongest positive correlation with NO3−-N. The RAD and RTD had a negative correlation with SRL.

4. Discussion

4.1. Effects of Different N Forms on Root Morphology in Different Tree Species

When trees grow for a long period of time in a soil environment with a certain ratio of the N forms, they gradually form a growth pattern adapted to this soil environment, which is generally the coordinated effect of the aboveground and the underground parts. As the root is in direct contact with the soil for nutrient exchange, the change in root morphology is the intuitive embodiment of and basis for understanding the growth of forest trees. The results of this study showed that the TRL, TRSA and TRV of C. lanceolata were positively correlated with NO3−-N (Figure 5a) and that the RAD was positively correlated with NH4+-N. The TRL, TRSA, TRV and RAD of S. superba tended to be greater at high NH4+-N concentrations, but the correlation was not significant (Figure 5b). Under a homogeneous N supply, the TRL, TRSA and TRV of S. superba were largest, while the RAD was smallest. C. lanceolata tended to grow more slender roots under the treatment with a high NO3−-N concentration, while the roots of S. superba were extended under the treatment with a high NH4+-N concentration and an ammonium to nitrate ratio of 5:5. This is consistent with the results showing that C. lanceolata grows more slender roots in NO3−-N patches and S. superba grows more slender roots in NH4+-N patches [8]. When C. lanceolata and S. superba were mixed in an environment with heterogenous nutrients, S. superba took advantage of the compensatory strategy of a vertical growth direction in its fine roots, and alleviated the strong competition for nutrients because of the different level of soil colonization and the niche differentiation of fine roots of the two species [28,29], which was conducive to the coordination of the relationship between the two species [30]. We infer that this opposite root growth response resulted from complementary patterns in the absorption strategies of different N forms in C. lanceolata and S. superba seedlings.
The nitrogen-seeking strategy of tree roots will change with changes in the environment and in their adaptive mechanism. The environmental factors affecting the growth of forest roots mainly include the concentration of soil nutrients (such as N), the soil’s pH value, and the soil’s temperature and humidity. The strategies of forest trees for obtaining nitrogen also vary according to the forest’s age, which will directly or indirectly affect the nitrogen uptake of trees [31]. For example, in an environment of mild nitrogen deficiency, the TRL of plants increased, while moderate nitrogen deficiency and excessive nitrogen supply inhibited the growth of the root system [32]. In acidic environments, NH4+-N is the main N source for plants and is usually more readily available than NO3−-N, especially in coniferous forests, where many conifers tend to absorb NH4+-N [33]. Under drought stress, the uptake of NH4+-N in different organs of C. lanceolata seedlings was significantly higher than that of NO3−-N, showing a preference for NH4+ [34]. The growth and nutrient acquisition of plant roots are affected and restricted by many factors. When trees are under nutrient, water and other stress conditions, the root system will produce a series of adaptive changes in its morphological structure to obtain the limited resources and adapt to the ecological strategy of overcoming adversity through self-regulation [35]. Numerous studies have shown that in nutrient-limited environments, plants mainly use strategies such as increasing the roots’ length and decreasing the roots’ diameter, which expand the growth range of roots to obtain more nutrients for growth [36,37,38]. Nitrogen deposition causes the growth rate of the TRL and TRV of C. lanceolata to be faster than that of the RSA and RAD, in which the root system is elongated and dilated [39]. In another study, nitrogen deposition caused the root system of S. superba seedlings to show an increasing trend in the TRL, RAD, TRSA and TRV, and the root system was thick and dilated [40]. The results of this study showed that the roots of C. lanceolata seedlings were slender and dilated under the treatment with a high NO3−-N concentration, while the roots of S. superba seedlings were sturdy and dilated under the treatment with a high NH4+-N concentration.

4.2. Effects of Different N Forms on Biomass and Root Abundance in Different Tree Species

The root biomass of plants is one of the manifestations of the amount of nutrients and water they absorb, and the allocation of aboveground and underground biomass also reflects the nutrient uptake and distribution in plants. The results of this study showed that in C. lanceolata, the accumulation of root biomass was higher under the treatment with a high NO3−-N concentration and, the total accumulation of seedling biomass was higher under the treatment with a high NH4+-N concentration (Figure 5a). However, the accumulation of root biomass in S. superba was higher under the treatment with a high NH4+-N concentration. The total biomass was highest under the treatment with a homogeneous N supply, and accumulation was relatively high under the treatment with a high NO3−-N concentration (Figure 5b). In a limited-resource environment, when plants are limited by nutrients, they allocate biomass to the roots and reduce the allocation to aboveground biomass [41]. Under low nutrient conditions, C. lanceolata seedlings increased the amount of nutrient absorbed, mainly by altering the root structure rather than by allocating more nonstructural carbohydrates to the roots, while nutrient alleviation driven by nitrogen addition resulted in more carbohydrate being allocated to the aboveground organs, resulting in the accumulation of structural carbohydrates in the aboveground parts [42]. This means that the addition of nitrogen leads to a reduction in fine root biomass in C. lanceolata seedlings [43]. The same study found that there was a significant positive correlation between the biomass of fine roots and the content of NH4+-N in a S. superba plantation [44]. The roots of S. superba from a heterogeneous N environment showed greater dry biomass and N absorption efficiency than those from a homogeneous N environment [45]. This is contrary to the results of this study, which may be a result of the differences in the provenance of the S. superba specimens, as they may have differences in their N uptake.
As important indicators of roots’ morphological characteristics, the SRL and RTD reflect the ability and efficiency of plants to allocate biomass to roots to absorb nutrients and water. In general, the larger the SRL and the smaller the root diameter, the stronger the ability of the root system to absorb nutrients and water [46]. To a certain extent, RTD can be considered a reflection of root tissue’s stretching force. Generally, the greater the RTD, the greater the stretching force of the root tissue [47]. Numerous studies have shown that SRL has a negative correlation with RTD and RAD [18,48]. After N application, Castanopsis fabri adopted a rapid absorption strategy by increasing the SRL and the growth rate of roots, while Castanopsis carlesii adopted a relatively conservative resource absorption strategy by increasing the tissue density of fine roots [49]. The N deposition treatment significantly increased the fine root length of S. superba but had no significant effect on the tissue density [50]. In this study, we found that the SRL of C. lanceolata and S. superba were negatively correlated with RTD (Figure 5a,b). Therefore, we speculated that C. lanceolata and S. superba adopt an expansion strategy of increasing their SRL and reducing their RTD in an environment with a high NO3−-N concentration.
The RSR is one of the indicators used to measure biomass allocation in plants. Numerous studies have shown that in a normal growth environment, the aboveground and underground parts of plants have synergistic growth, and biomass accumulation is also carried out synergistically [51]. Under stresses such as drought, plants allocate more biomass to the roots and increase the RSR to enhance the absorption capacity of water and other underground resources [41,52]. A previous study found that drought reduced fine root biomass and increased the RSR [53]. This study showed that the RSR of C. lanceolata was positively correlated with NO3−-N but negatively correlated with NH4+-N, which was consistent with the pattern shown by root biomass, and the RSR was largest under the treatments with NO3−-N only and an ammonium to nitrate ratio of 3:7. The RSR of S. superba showed the opposite pattern and was consistent with the pattern shown by root biomass (Figure 5a,b), and the RSR was largest under the treatment with an ammonium to nitrate ratio of 7:3 and under the NH4+-N-only treatment. Therefore, the results of this study showed that the allocation of biomass to aboveground and underground parts in C. lanceolata and S. superba seedlings responds differently to different N forms, and the N uptake strategy was adjusted by increasing or decreasing the RSR. Under the treatments with high NO3−-N concentrations, C. lanceolata increased the RSR to obtain more N sources, while S. superba increased the aboveground biomass by reducing the RSR, but the opposite was true at high NH4+-N concentrations. In a study of fine roots in hybrid poplar plantations, it was found that soil nutrient deficiencies caused by continuous cropping may lead to an increase in plants’ carbon input to the roots [54]. Therefore, we inferred that a high NO3−-N concentration may be a limiting nutrient for C. lanceolata seedlings. Correspondingly, N sources with high NH4+-N concentrations are more suitable for the aboveground growth of C. lanceolata seedlings, and N sources with high NO3−-N concentrations are more suitable for the development of aboveground parts in S. superba.

4.3. Effects of Different N Forms on the Growth of Different Tree Species

As one of the limiting elements of plant growth, N occurs in different forms in natural soil, and the different forms of N occur in different ratios, which will have different effects on plant growth. It is believed that the sole application of NH4+-N is prone to inducing NH4+ toxicity, which restrains plant growth [55,56]. Moreover, many plants prefer mixed NH4+-N and NO3−-N over a single N source [57]. In contrast, some studies have also found that the growth of the underground and aboveground parts of plant seedlings is positively correlated with treatments with NH4+-N only [5]. The results of this study showed that the ΔH of C. lanceolata seedlings showed higher values under ammonium to nitrate ratios of 5:5 and 7:3, and ΔGD showed higher values under ammonium to nitrate ratios of 7:3 and 5:5. The ΔH of S. superba was larger under ammonium to nitrate ratios of 5:5 and 3:7, and the ΔGD was higher under ammonium to nitrate ratios of 0:10 and 3:7, which both had positive correlations with NO3−-N and TSB (Figure 5b). Overall, our study supports the idea that C. lanceolata and S. superba seedlings prefer to develop aboveground parts under mixed NH4+-N and NO3−-N. Between the two, C. lanceolata seedlings are more inclined to absorb NH4+-N for aboveground growth, which is more suitable for growth under ammonium to nitrate ratios of 5:5 and 7:3. Conversely, S. superba seedlings are more inclined to absorb NO3−-N, which is more suitable for aboveground growth under ammonium nitrate ratios of 5:5, 3:7 and 0:10. The ΔGD of S. superba seedlings was largest under the ratio of 0:10, which may be because the application of NO3−-N alone is beneficial for the growth in the woody diameter of S. superba.
Because they are timber species, it is also worth considering the aboveground growth of C. lanceolata and S. superba. Because of differences in their leaves, conifer and broadleaf species respond differently to different N forms [58]. Studies suggest that conifer species tend to absorb NH4+-N, and broadleaf species tend to absorb NO3−-N [58,59]. This study supports this hypothesis, which proposes that C. lanceolata seedlings prefer NH4+-N over NO3−-N for aboveground growth, while the opposite is true for S. superba. It is worth noting that TRL, TRSA, TRV, TSB, ΔH and SRL all showed maximum values in S. superba under an ammonium to nitrate ratio of 5:5. This means that both the aboveground and underground parts grow simultaneously under a homogeneous N supply. As a result, we speculate that the roots of S. superba seedlings may increase their length within the root system to obtain nutrients and use nutrients for seedlings’ growth in terms of height and leaves to obtain more nutrients through photosynthesis under a homogeneous N supply [60].

5. Conclusions

In conclusion, the roots of C. lanceolata tended to be slender and accumulate more biomass under the treatment with a high NO3−-N concentration, while the opposite was true for S. superba. Under the high NO3−-N concentration, the roots of the two tree species adopted the expansion strategy of increasing the SRL and reducing the RTD. Moreover, C. lanceolata allocated more biomass to the root system at the high NO3−-N concentration, but S. superba allocated more biomass to the root system at the high NH4+-N concentration. Compared with the treatments with a single N form, the mixed NH4+-N and NO3−-N treatments were more conducive to the growth and biomass accumulation of the two tree species. C. lanceolata tends to grow under high NH4+-N concentrations, while S. superba tends to grow under high NO3−-N concentrations. C. lanceolata grows better under NH4+-N:NO3−-N ratios of 5:5 and 7:3, while S. superba grows better under NH4+-N:NO3−-N ratios of 5:5 and 3:7 ratios. Therefore, according to the soil N, we can appropriately apply more NH4+-N to C. lanceolata and more NO3−-N to S. superba for cultivating seedlings.

Author Contributions

Conceptualization, H.L.; methodology and formal analysis, H.L. and L.W.; investigation, Y.W., X.Q. and X.L.; data curation, H.L. and Y.X.; writing—original draft preparation, H.L.; writing—review and editing, Y.W. and X.Q.; validation and visualization, L.W. and X.L.; supervision, X.Y.; funding acquisition, X.Y. 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 (32171773) and the Distinguished Young Scientific Research Talent Program of Fujian Agriculture and Forestry University (KXJQ20012).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank the numerous students and lab staff from the College of Forestry, Fujian Agriculture and Forestry University, for their assistance in the laboratory.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Zhou, X.; Fu, Y.; Zhou, L.; Li, B.; Luo, Y. An imperative need for global change research in tropical forests. Tree Physol. 2013, 33, 903–912. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Ma, Y.; Li, Y.; Nurbiye, A. Temporal and spatial distribution characteristics of soil ammonium and nitrate Nitrogen in different plant communities in the Ebinur Lake Wetland. Henan Sci. Tech. 2019, 26, 150–156. [Google Scholar]
  3. Ou, J.; Liu, Y.; Zhang, J.; Cui, N.; Zhang, J.; Song, X.; Deng, C. Early responses of soil ammonium and nitrate nitrogen to forest gap harvesting of a Pinus massoniana plantation in the upper reaches of Yangtze River. Chin. J. Appl. Envir. Biol. 2015, 21, 147–154. [Google Scholar]
  4. Sun, M.; Lu, X.; Cao, X.; Li, J.; Xiong, J.; Xie, S. Effect of different Nitrogen forms on root growth and dynamic kinetics characteristics for Citrus sinensis × Poncirus trifoliata. Scit. Silvae Sin. 2015, 51, 113–120. [Google Scholar]
  5. Wang, Y.; Yao, R. Effects of different nitrogen forms and ratios on growth of tissue cultured seedlings in Pinus massoniana. J. Cent. South Univ. For. Technol. 2021, 41, 18–24+71. [Google Scholar]
  6. Jia, L.; Chen, G.; Zhang, L.; Chen, T.; Jiang, Q.; Chen, Y.; Fan, A.; Wang, X. Plastic responses of fine root morphology and architecture traits to nitrogen addition in ectomycorrhizal and arbuscular mycorrhizal tree species in an evergreen broadleaved forest. Chin. J. Appl. Ecol. 2021, 32, 529–537. [Google Scholar]
  7. Lin, S.; Shao, L.; Hui, C.; Sandhu, H.; Fan, T.; Zhang, L.; Li, F.; Ding, Y.; Shi, P. The effect of temperature on the developmental rates of seedling emergence and leaf-unfolding in two dwarf bamboo species. Trees 2018, 32, 757–763. [Google Scholar] [CrossRef]
  8. Yan, X.; Hu, W.; Ma, Y.; Huo, Y.; Wang, T.; Ma, X. Nitrogen Uptake Preference of Cunninghamia lanceolata, Pinus massoniana and Schima superba under Heterogeneous Nitrogen Supply Environment and their Root Foraging Strategies. Scit. Silvae Sin. 2020, 56, 1–11. [Google Scholar]
  9. Qiao, Y.; Miao, S.; Han, X. Effects of nitrogen form on soybean root morphological characters and H+ release. Soybean Sci. 2006, 25, 265–269. [Google Scholar]
  10. Liu, C.; Cui, X.; Guo, Y.; Zheng, H. Effects of different ratios of NH4+-N/NO3− -N on growth of Larix gmelinii seedlings. J. Northeast For. Univ. 2011, 39, 28–30. [Google Scholar]
  11. Ye, Y.; Luo, H.; Li, M.; Liu, X.; Cao, G.; Xu, S. Effects of nitrogen forms on lateral roots development and photosynthetic characteristics in leaves of Cunninghamia lanceoata seedlings. Acta Bot. Boreal. Occident. Sin. 2018, 38, 2036–2044. [Google Scholar]
  12. Domenicano, S.; Coll, L.; Messier, C.; Berninfer, F. Nitrogen forms affect root structure and water uptake in the hybrid poplar. New For. 2011, 42, 347–362. [Google Scholar] [CrossRef] [Green Version]
  13. Hilbert, D. Optimization of plant root: Shoot ratios and internal nitrogen concentration. Ann. Bot. 1990, 66, 91–99. [Google Scholar] [CrossRef]
  14. Gedroc, J.; McConnaughay, K.; Coleman, J. Plasticity in root/shoot partitioning: Optimal, ontogenetic, or both? Func. Ecol. 1996, 10, 44–50. [Google Scholar] [CrossRef]
  15. Hermans, C.; Hammond, J.; White, P.; Verbruggen, N. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci. 2006, 11, 610–617. [Google Scholar] [CrossRef]
  16. McCarthy, M.; Enquist, B. Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Func. Ecol. 2007, 21, 713–720. [Google Scholar] [CrossRef]
  17. Kobe, R.; Iyer, M.; Walters, M. Optimal partitioning theory revisited: Nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology 2010, 91, 166–179. [Google Scholar] [CrossRef]
  18. Wang, Z.; Cheng, L.; Wang, M.; Sun, J.; Zhong, Q.; Li, M.; Cheng, D. Fine root traits of woody plants in deciduous forest of the Wuyi Mountains. Acta Ecol. Sin. 2018, 38, 1–10. [Google Scholar]
  19. Zhang, X.; Xing, Y.; Yan, G.; Wang, Q. Response of fine roots to precipitation change: A meta-analysis. Chin. J. Plant Ecol. 2018, 42, 164–172. [Google Scholar]
  20. Tuan, D.; Shen, Y.; Kang, W.; Xiang, W.; Yan, W.; Deng, X. Characteristics of nutrient cycling in first and second rotations of Chinese fir plantations. Acta Ecol. Sin. 2011, 31, 5025–5032. [Google Scholar]
  21. Suo, P.; Du, D.; Wang, Y.; Hu, Y.; Liu, X. Effects of successive rotation Chinese fir plantations on soil nitrogen content and soil enzyme activities related to nitrogen transformation. J. For. Envir. 2019, 39, 113–119. [Google Scholar]
  22. Wan, X.; Huang, Z.; He, Z.; Hu, Z.; Yang, J.; Yu, Z.; Wang, M. Effects of broadleaf plantation and Chinese fir (Cunninghamia lanceolata) plantation on soil carbon and nitrogen pools. Chin. J. Appl. Ecol. 2013, 24, 345–350. [Google Scholar]
  23. Hao, F.; Liu, X.; Fan, J. Study on key enzyme activity in nitrogen metabolism and the content of molybdenum and iron in alfalfa under different NO3−-N/NH4+-N ratio. Agric. Res. Arid. Areas 2017, 35, 190–197. [Google Scholar]
  24. Wu, P.; Ma, X.; Tigabu, M.; Wang, C.; Liu, A.; Odén, P. Root morphological plasticity and biomass production of two Chinese fir clones with high phosphorus efficiency under low phosphorus stress. Can. J. For. Res. 2011, 41, 228–234. [Google Scholar] [CrossRef]
  25. Zhang, J.; Sheng, W.; Xiong, Y.; Wan, X. Effects of fertilization on soil nutrient content of potted Chinese Fir seedling. Sci. Silv. Sin. 2006, 42, 44–50. [Google Scholar]
  26. Meng, S. Nitrogen Dynamic Uptake and Genetic Expression of Translocator of Tree Species in Fine Roots. Ph.D. Thesis, Northwest Agricultural and Forestry University, Yangling, China, 2016. [Google Scholar]
  27. Liu, Z.; Lin, W.; Yang, Z.; Lin, T.; Liu, X.; Chen, Y.; Yang, Y. Effects of soil warming and nitrogen deposition on available nitrogen in a young Cunninghamia lanceolata stand in mid-subtropical China. Acta Ecol. Sin. 2017, 37, 44–53. [Google Scholar]
  28. Ma, X. Research on Adaptability and Foraging Behavior of Different Afforestation Species to Soil Nutrient Heterogeneity. Master’s Thesis, Chinese Academy of Forestry, Beijing, China, 2009. [Google Scholar]
  29. Yao, J.; Chu, X.; Zhou, Z.; Tong, J.; Wang, H.; Yu, J. Effects of neighbor competition on growth, fine root morphology and distribution of Schima superba and Cunninghamia lanceolata in different nutrient environments. Chin. J. Appl. Ecol. 2017, 28, 1441–1447. [Google Scholar]
  30. Zheng, C. Study on nutrient characteristics of soil in the forest and rhizosphere of Schima Schima and Chinese fir mixed forest. Wuyi Sci. J. 2006, 22, 123–126. [Google Scholar]
  31. Xu, X.; Li, Q.; Wang, J.; Zhang, L.; Tian, S.; Zhi, L.; Li, Q.; Sun, Y. Inorganic and organic nitrogen acquisition by a fern Dicranopteris dichotoma in a subtropical forest in South China. PLoS ONE 2014, 9, e90075. [Google Scholar] [CrossRef]
  32. Giehl, R.; Von Wirén, N. Root nutrient foraging. Plant Physiol. 2014, 166, 509–517. [Google Scholar] [CrossRef] [Green Version]
  33. Wang, Y.; Hsu, P.; Tsay, Y. Uptake, allocation and signaling of nitrate. Trends Plant Sci. 2012, 17, 458–467. [Google Scholar] [CrossRef]
  34. Li, S.; Zhou, L.; Wu, S.; Sun, M.; Ding, G.; Lin, S. Effects of different nitrogen forms on nutrient uptake and distribution of Cunninghamia lanceolata plantlets under drought stress. J. Plant Nut. Fert. 2020, 26, 152–162. [Google Scholar]
  35. Li, L.; Zheng, S.; Xu, J.; Wu, P. Research Advance in Influence Mechanism of Tree Root Biomass Allocation. World For. Res. 2022, 35, 15–20. [Google Scholar]
  36. Zhang, X.; Xing, Y.; Wang, Q.; Yan, G.; Wang, M.; Liu, G.; Wang, H.; Huang, B.; Zhang, J. Effects of long-term nitrogen addition and decreased precipitation on the fine root morphology and anatomy of the main tree species in a temperate forest. Forest Ecol. Mana. 2020, 455, 117664. [Google Scholar] [CrossRef]
  37. Yan, G.; Chen, F.; Zhang, X.; Wang, J.; Han, S.; Xing, Y.; Wang, Q. Spatial and temporal effects of nitrogen addition on root morphology and growth in a boreal forest. Geoderma 2017, 303, 178–187. [Google Scholar] [CrossRef]
  38. Gan, H. The Molecular and Physiological Basis Underlying Acquisition of Nitrogen and Phosphorus in Fine Roots of Poplars. Ph.D. Thesis, Northwest Agricultural and Forestry University, Yangling, China, 2016. [Google Scholar]
  39. Wang, J. Root Competition and Allelopathic Effects of Cunninghamia lanceolata and Phoebe chekiangensis under the Simulated Nitrogen Deposition. Master’s Thesis, Zhejiang Agriculture and Forestry University, Lin’an, China, 2021. [Google Scholar]
  40. Zhang, R.; Wang, Y.; Zhou, Z.; Feng, Z. Nitrogen addition affects root growth, phosphorus and nitrogen efficiency of three provenances of Schima superba in barren soil. Acta Ecol. Sin. 2013, 33, 3611–3621. [Google Scholar] [CrossRef] [Green Version]
  41. Li, B.; Zhu, Q.; Pan, Y.; Jin, A.; Gao, Y.; Pan, Y.; Wang, Z. Research progress on plant growth strategies based on biomass allocation patterns. J. Green Sci. Tech. 2022, 24, 29–32+41. [Google Scholar]
  42. Wang, J.; Guan, X.; Zhang, W.; Huang, K.; Zhu, M.; Yang, Q. Responses of biomass allocation patterns to nitrogen addition of Cunninghamia lanceolata seedlings. Chin. J. Plant Ecol. 2021, 45, 1231–1240. [Google Scholar] [CrossRef]
  43. Shi, Z.; Xiong, D.; Feng, J.; Xu, C.; Zhong, B.; Deng, F.; Chen, Y.; Chen, G.; Yang, Y. Ecophysiological effects of simulated nitrogen deposition on fine roots of Chinese fir (Cunninghamia lanceolata) seedlings. Acta Ecol. Sin. 2017, 37, 74–83. [Google Scholar]
  44. Wang, J.; Yu, S.; Hao, Q.; Cao, Y.; Ge, Z.; Mao, L. Distribution differences of fine root biomass and morphology in subtropical secondary forest at different forest ages. J. Northwest Agric. For. Univ. 2021, 49, 38–46. [Google Scholar]
  45. Yao, J.; Zhou, Z.; Chu, X.; Xu, H.; Tong, J. Effect of neighborhood competition on dry matter accumulation, nitrogen and phosphorus efficiency of three provenances of Schima superba in a heterogeneous nutrient environment. Acta Ecol. Sin. 2018, 38, 1780–1788. [Google Scholar]
  46. Dhiman, I.; Bilheux, H.; DeCarlo, K.; Painter, S.L.; Santodonato, L.; Warren, J.M. Quantifying root water extraction after drought recovery using sub-mm in situ empirical data. Plant Soil 2018, 424, 73–89. [Google Scholar] [CrossRef]
  47. Zheng, Y.; Wen, Z.; Song, G.; Ding, M. The influence of environment and phylogenic background on variation in leaf and fine root traits in the Yanhe River catchment, Shaanxi, China. Acta Ecol. Sin. 2014, 34, 2682–2692. [Google Scholar]
  48. Zhang, L. Plastic Responses of Fine Root Traits to N and Pin Ectomycorrhizal and Arbuscular Mycorrhizal Tree Species in an Evergreen Broadleaved Forest. Master’s Thesis, Fujian Normal University, Fuzhou, China, 2019. [Google Scholar]
  49. Jia, L.; Chen, G.; Zhang, L.; Chen, T.; Jiang, Q.; Chen, Y.; Fan, A.; Wang, X. Plastic responses of fine root morphological traits of Castanopsis fabri and Castanopsis carlesii to short-term nitrogen addition. Chin. J. Appl. Ecol. 2019, 30, 4003–4011. [Google Scholar]
  50. Xie, Y. Morphological and Chemometrics of Schima superb Seeding Fine Root in Response of Nitrogen Deposition. Master’s Thesis, Fujian Normal University, Fuzhou, China, 2016. [Google Scholar]
  51. Xue, Z.; Wang, S.; Ding, J.; Li, C.; Ma, B.; Rebieguri, Y. Effects of different nitrogen forms on root morphology and nitrogen uptake of walnut seedlings. J. Shandong Agri. Univ. 2021, 52, 759–763. [Google Scholar]
  52. Gao, G.; Li, Z.; Ge, X.; Huang, R.; Li, A. Effects of nitrogen addition on biomass and root morphology of Phyllostachys edulis seedlings under drought stress. Chin. J. Ecol. 2022, 41, 858–864. [Google Scholar]
  53. Zhai, D. Effects of Drought on Root Respiration and the Mechanisms. Ph.D. Thesis, East China Normal University, Shanghai, China, 2021. [Google Scholar]
  54. Wang, Y.; Xu, T.; Zhu, W.; Wang, Q.; Liu, M.; Wang, H.; Li, C.; Dong, Y. Seasonal dynamics of quantitative and morphological traits of poplar fine roots and their differences between successive rotation plantations. Chin. J. Appl. Ecol. 2016, 27, 395–402. [Google Scholar]
  55. Tao, S.; Hua, X.; Wang, Y.; Guo, N.; Yan, X.; Lin, J. Research advance in effects of different nitrogen forms on growth and physiology of plants. Guizhou Agri. Sci. 2017, 45, 64–68. [Google Scholar]
  56. Borgognone, D.; Colla, G.; Rouphael, Y.; Cardarelli, M.; Rea, E.; Schwarz, D. Effect of nitrogen form and nutrient solution pH on growth and mineral composition of self-grafted and grafted tomatoes. Sci. Hortic. 2013, 149, 61–69. [Google Scholar] [CrossRef]
  57. Sui, L.; Yi, J.; Wang, K.; Li, Y. Effects of different forms and ratios of nitrogen on physiological characteristics of Perilla frutescens (L.) Britt under salt stress. Chin. J. Ecol. 2018, 37, 3277–3283. [Google Scholar]
  58. Uscola, M.; Oliet, J.; Villar-Salvador, P.; Dıáz-Pine´s, E.; Jacobs, D. Nitrogen form and concentration interact to affect the performance of two ecologically distinct Mediterranean forest trees. Eur. J. For. Res. 2014, 133, 235–246. [Google Scholar] [CrossRef]
  59. Wang, X. Effects of Different Nitrogen Forms and Ratios on Growth Characteristics of Phyllostachys edulis and Evergreen Broad-leaved Forest Species Seedlings. Master’s Thesis, Zhejiang A&F University, Hangzhou, China, 2018. [Google Scholar]
  60. Chang, Y.; Li, B.; Zhong, Q.; Wang, G.; Shen, Q.; Xu, C.; Zhang, S. Biomass allocation strategies of three functional forest seedlings and their relation with fine root and leaf nutrient. Chin. J. Ecol. 2022, 25, 1–10. [Google Scholar]
Forests 13 02085 g001 550
Figure 1. Effects of different NH4+-N and NO3−-N ratios on the TRL (a,b), TRSA (c,d), TRV (e,f) and RAD (g,h) of the two tree species. Different lowercase letters indicate that the roots’ morphological parameters were significantly different under different N forms (p < 0.05).
Figure 1. Effects of different NH4+-N and NO3−-N ratios on the TRL (a,b), TRSA (c,d), TRV (e,f) and RAD (g,h) of the two tree species. Different lowercase letters indicate that the roots’ morphological parameters were significantly different under different N forms (p < 0.05).
Forests 13 02085 g001
Forests 13 02085 g002 550
Figure 2. Effects of different NH4+-N and NO3−-N ratios on the TRB (a,b) and TSB (c,d) of the two tree species. Different lowercase letters indicate that TRB and TB were significantly different under different N forms (p < 0.05).
Figure 2. Effects of different NH4+-N and NO3−-N ratios on the TRB (a,b) and TSB (c,d) of the two tree species. Different lowercase letters indicate that TRB and TB were significantly different under different N forms (p < 0.05).
Forests 13 02085 g002
Forests 13 02085 g003 550
Figure 3. Effects of different NH4+-N and NO3−-N ratios on SRL (a,b), RTD (c,d) and RSR (e,f) between the two tree species. Different lowercase letters indicate that the SRL, RTD and RSR were significantly different under different N forms (p < 0.05).
Figure 3. Effects of different NH4+-N and NO3−-N ratios on SRL (a,b), RTD (c,d) and RSR (e,f) between the two tree species. Different lowercase letters indicate that the SRL, RTD and RSR were significantly different under different N forms (p < 0.05).
Forests 13 02085 g003
Forests 13 02085 g004 550
Figure 4. Effects of different NH4+-N and NO3−-N ratios on ΔH (a) and ΔGD (b). Data are expressed as the mean ± standard error (SE). Different lowercase letters on the columns indicate significant differences among the treatments.
Figure 4. Effects of different NH4+-N and NO3−-N ratios on ΔH (a) and ΔGD (b). Data are expressed as the mean ± standard error (SE). Different lowercase letters on the columns indicate significant differences among the treatments.
Forests 13 02085 g004
Forests 13 02085 g005 550
Figure 5. Redundancy analysis of the responses of roots’ morphological and growth parameters to different ratios of the N forms. The proportions explained by Axis 1 and Axis 2 in (a) are 27.91% and 24.14% and those in (b) are 12.21% and 44.30%, respectively. Solid blue lines indicate the parameters. Solid red lines indicate NH4+-N and NO3−-N. Abbreviations for the parameters are as follows: TRL, total root length; TRSA, total root surface area; TRV, total root volume; RAD, roots’ average diameter; TRB, total root biomass; TSB, total seedling biomass; SRL, specific root length; RTD, root tissue density; RSR, root-to-shoot ratio; ΔH, height increment; ΔGD, ground diameter increment.
Figure 5. Redundancy analysis of the responses of roots’ morphological and growth parameters to different ratios of the N forms. The proportions explained by Axis 1 and Axis 2 in (a) are 27.91% and 24.14% and those in (b) are 12.21% and 44.30%, respectively. Solid blue lines indicate the parameters. Solid red lines indicate NH4+-N and NO3−-N. Abbreviations for the parameters are as follows: TRL, total root length; TRSA, total root surface area; TRV, total root volume; RAD, roots’ average diameter; TRB, total root biomass; TSB, total seedling biomass; SRL, specific root length; RTD, root tissue density; RSR, root-to-shoot ratio; ΔH, height increment; ΔGD, ground diameter increment.
Forests 13 02085 g005
Table
Table 1. Treatments with different nitrogen forms.
Table 1. Treatments with different nitrogen forms.
Treatment (NH4+/NO3−)Total N (mmol·L−1)Different N Forms (mmol·L−1)
NH4+NO3−
10:022.00
0:10202.0
7:321.40.6
3:720.61.4
5:521.01.0
Table
Table 2. Two-way ANOVA of the effects of tree species and different ratios of N forms on the seedlings’ growth and the roots’ morphological parameters.
Table 2. Two-way ANOVA of the effects of tree species and different ratios of N forms on the seedlings’ growth and the roots’ morphological parameters.
Factorp-Value and Significance Level
Tree Species (a)NH4+/NO3− (b)a × b
df144
Seedling height increment (ΔH)<0.001<0.001<0.001
Ground diameter increment (ΔGD)<0.001<0.001<0.001
Total root length (TRL)<0.001<0.001<0.01
Total root surface area (TRSA)<0.001<0.001<0.01
Total root volume (TRV)<0.001<0.05<0.05
Roots’ average diameter (RAD)<0.001<0.0010.835
Total root biomass (TRB)<0.001<0.01<0.001
Total seedling biomass (TSB)<0.001<0.010.08
Specific root length (SRL)<0.001<0.010.113
Root tissue density (RTD)<0.001<0.01<0.05
Root-to-shoot ratio (RSR)<0.001<0.001<0.001
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Liang, H.; Wang, L.; Wang, Y.; Quan, X.; Li, X.; Xiao, Y.; Yan, X. Root Development in Cunninghamia lanceolata and Schima superba Seedlings Expresses Contrasting Preferences to Nitrogen Forms. Forests 2022, 13, 2085. https://doi.org/10.3390/f13122085

AMA Style

Liang H, Wang L, Wang Y, Quan X, Li X, Xiao Y, Yan X. Root Development in Cunninghamia lanceolata and Schima superba Seedlings Expresses Contrasting Preferences to Nitrogen Forms. Forests. 2022; 13(12):2085. https://doi.org/10.3390/f13122085

Chicago/Turabian Style

Liang, Haiyan, Lidong Wang, Yanru Wang, Xiaoqiang Quan, Xiaoyu Li, Yaning Xiao, and Xiaoli Yan. 2022. "Root Development in Cunninghamia lanceolata and Schima superba Seedlings Expresses Contrasting Preferences to Nitrogen Forms" Forests 13, no. 12: 2085. https://doi.org/10.3390/f13122085

APA Style

Liang, H., Wang, L., Wang, Y., Quan, X., Li, X., Xiao, Y., & Yan, X. (2022). Root Development in Cunninghamia lanceolata and Schima superba Seedlings Expresses Contrasting Preferences to Nitrogen Forms. Forests, 13(12), 2085. https://doi.org/10.3390/f13122085

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop