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Article

The Growth and Physiological Responses of Gleditsia sinensis Lam. Seedlings with Different Phosphorus Efficiencies to Low Phosphorus Stress

by
Chunyun Lu
,
Rong Zou
,
Xiurong Wang
,
Yang Zhao
* and
Feng Xiao
Institute for Forest Resources and Environment of Guizhou, College of Forestry, Guizhou University, Guiyang 550025, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(8), 1343; https://doi.org/10.3390/f15081343
Submission received: 27 June 2024 / Revised: 24 July 2024 / Accepted: 30 July 2024 / Published: 2 August 2024
(This article belongs to the Section Forest Soil)
Browse Figures
Review Reports Versions Notes

Abstract

:
In order to elucidate the response mechanisms of Gleditsia sinensis Lam. with different phosphorus (P) efficiencies to low P stress, this study set up low P treatment (0.01 mmol·L−1, LP) and normal P treatment (1.00 mmol·L−1, NP). The experimental materials included low P-tolerant G. sinensis families F10 and F13, and low P-sensitive G. sinensis families F21 and F29. This study aimed to investigate the effects of low P stress on the agronomic traits, nutrient content, and physiological indices of G. sinensis seedlings with different P efficiencies. The results showed that the agronomic traits, such as plant height, stem diameter, and so on, of the low P-tolerant family, were significantly higher than those of the low P-sensitive family under low P stress. Low P stress significantly increased the total root length, total root surface area, total root projected area, total root volume, and main root diameter of the tolerant family. The tolerant family exhibited significantly higher net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, and transpiration rate compared to the sensitive family. Low P stress significantly increased the activities of protective enzymes, acid phosphatase activity, and malondialdehyde content in the low P-tolerant family. The tolerant family exhibited higher P absorption efficiency and P utilization efficiency compared to the sensitive family. Low P stress significantly increased the P utilization efficiency of the tolerant family. In summary, compared to the sensitive family, the low P-tolerant G. sinensis family has stronger reactive oxygen species scavenging ability and can accumulate more osmotic regulatory substances to maintain cell osmotic potential and better protect cells; this improves P utilization efficiency and nutrient content, thereby alleviating the harm caused by low P stress and maintaining normal growth and metabolism.

1. Introduction

Phosphorus is an essential nutrient element that plays a crucial regulatory role in the growth and development of plants [1]. Plants primarily obtain P from the soil, and P is the second most limiting nutrient in crop production, following nitrogen. However, P deficiency in soils is widespread in China, constituting a significant constraint on agricultural and forestry production. P in the soil often exists in an insoluble inorganic or organic form, making it challenging for plants to absorb directly. This condition leads to plants being susceptible to low P stress, thereby affecting plant growth, development, and yield [2]. The primary focus of plant breeding is to increase crop yield while reducing the dependence of plants on inorganic P fertilizers. Our understanding of how plants perceive and respond to P starvation is increasing, but there are still many aspects that remain undiscovered. A series of complex signal cascades control the P starvation response in plants. It is noteworthy that plants have developed various mechanisms to adapt to low P conditions. These mechanisms include inducing root development and promoting lateral root growth [3,4]; secreting more organic acids from the roots [5]; promoting the formation of mycorrhizae [6]; producing acid phosphatase to resist low P stress [7,8]; altering plant metabolic pathways [9,10]; and inducing or inhibiting the expression of P-related genes [11], among others. Studying the adaptive mechanisms of plants to low P, as well as breeding varieties with low P tolerance, forms the foundation for addressing P deficiency issues.
Gleditsia sinensis Lam. belongs to the Leguminosae family and the Gleditsia genus and is a common tall deciduous tree in China. It has been recognized for its pharmacological properties, including anti-tumor, anti-inflammatory, anti-allergic, and antimicrobial activities [12]. G. sinensis is widely utilized as both an economic and medicinal tree species. Furthermore, the plant contains abundant chemical components such as terpenoids, flavonoids, phenolic acids, steroids, and more, making it a natural resource for pharmaceuticals, food products, health supplements, cosmetics, and detergents [13,14]. With its high ecological, economic, and medicinal values, G. sinensis has gradually gained widespread attention. G. sinensis is mainly distributed in the southern regions of China, where the soil’s available P content is low. P deficiency in the soil hinders the growth and development of G. sinensis in these southern forested areas. The P efficiency of plants can be divided into absorption efficiency and utilization efficiency, referring, respectively, to the plant’s ability to absorb P from the growing environment and its capability to utilize the acquired P nutrition to produce biomass. P efficiency in plants can be improved by enhancing both P absorption and utilization efficiency [15]. Currently, a substantial amount of research has been conducted on the stress response mechanisms of plants to low P conditions. Numerous studies have reported significant differences in the morphological and physiological response mechanisms of plants to low P stress, both within and among species [16,17,18]. For instance, in Arabidopsis thaliana, when the primary root tip reaches a low-P area, stress proteins in the root tip alter the activity and distribution of hormones, thereby inhibiting the elongation of the main root and promoting lateral root growth [19,20]. However, research on the stress response mechanisms of G. sinensis to low P conditions has not been reported. The applicability of research findings on the low P adaptation mechanisms of different plant species to various families of G. sinensis remains uncertain. Therefore, building upon previous studies, this experiment utilized the low P-tolerant family (F10, F13) and low P-sensitive family (F21, F29) as experimental materials. This study aimed to determine the growth, photosynthetic physiology, root morphology, nutrient accumulation, and other indicators of four G. sinensis families. The goal was to analyze the differences in P acquisition strategies between low P-tolerant and low P-sensitive families of G. sinensis This analysis serves as a theoretical basis for cultivating the P-efficient G. sinensis family, holding significance for improving P utilization efficiency and breeding of G. sinensis.

2. Materials and Methods

2.1. Experimental Materials

The materials used in the experiment included the previously screened low P-tolerant family of G. sinensis (F10, F13) and the low P-sensitive family of G. sinensis (F21, F29) selected by our research group in the early stage.

2.2. Experimental Design

This study was conducted in the greenhouse of the College of Forestry at Guizhou University (26°27′ N latitude, 106°39′ E longitude, 1090 m elevation). The cultivation conditions for G. sinensis seedlings included a temperature of 25 °C ± 2 °C, a photoperiod of 12 h per day, and a relative humidity ranging from 50% to 75%. The substrate for this study is fine river sand. Using sand cultivation pots, the river sand was washed, dried, and sterilized at high temperature and pressure for 2 h before being placed into nutrient pots for later use. The experiment involved two P levels: normal P (1 mmol·L−1) and low P (0.01 mmol·L−1). After cultivating G. sinensis seedlings for two months, low P treatment was initiated. Each family was divided into two groups. One group was irrigated with Hoagland nutrient solution at a P concentration of 1 mmol·L−1, while the other group was irrigated with Hoagland nutrient solution at a P concentration of 0.01 mmol·L−1. The nutrient solution was applied every 7 days, with adequate water supplementation during the period. After subjecting the seedlings to stress treatment for three months, measurements were taken for various growth parameters, photosynthetic physiology, root morphology, and nutrient indicators of the four G. sinensis families under normal P and low P conditions. Thirty seedlings were evaluated for each treatment.
The formulation of the phosphorus-deficient Hoagland nutrient solution is as follows: K2SO4: 607 mg/L, MgSO4: 493 mg/L, (NH4)2SO4: 66.02 mg/L, C10H12 FeNaN2O8·3H2O: 20 mg/L, FeSO4: 15 mg/L, H3BO3: 2.86 mg/L, Na2B4O7·10H2O: 4.5 mg/L, MnSO4: 2.13 mg/L, CuSO4: 0.05 mg/L, and ZnSO4: 0.22 mg/L. The P source and its concentration are provided by KH2PO4. Potassium deficiency in low P concentration is supplemented with KCl. The prepared Hoagland nutrient solution is adjusted to a pH between 6 and 7 using 1 mol/L NaOH. Phosphorus-deficient Hoagland nutrient solution purchased from Qingdao Haibo Bio Co., Ltd. (Qingdao, China)

2.3. Measurement Indicators and Methods

(1) Measurement of growth indicators: Select 10 G. sinensis seedlings, and use a ruler to measure the plant height, stem diameter, leaf number, leaf length, leaf width, etc., before and after low P treatment. After low P stress treatment, divide the G. sinensis seedlings into three parts: roots, stems, and leaves. Weigh their fresh weight using a precision balance, then dry in an oven at 105 °C for half an hour, followed by drying at 65 °C to a constant weight. Weigh the dry weight of each part and calculate the root–shoot ratio. The SPAD value is determined using a SPAD meter to measure the SPAD value of the third leaf from the top of the plant.
(2) Estimation of photosynthesis: Three G. sinensis seedlings were selected from each treatment for photosynthetic parameter measurement. An open infrared gas exchange analyzer system (Licor-6400XT, Li-Cor Inc., Lincoln, NE, USA) was used to provide the photosynthetic photon flux density (PPFD), and a red–blue light source (6400-02B, Li-Cor Inc., Lincoln, NE, USA) to measure the leaf gas exchange parameters. On clear days between 09:00 and 11:00, the third, fourth, and fifth leaves from the tops of healthy G. sinensis plants were placed to fill the leaf chamber. Measurements were conducted at a PPFD of 1500 μmol m−2 s−1, with the leaf chamber CO2 concentration set at 400 μmol mol−1 and a flow rate of 500 μmol s−1. The instantaneous leaf gas exchange parameters measured included net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), transpiration rate (Tr), leaf instantaneous water use efficiency (WUE = Pn/Tr), and stomatal limitation value (Ls = 1 − Ci/Ca, where Ca is the CO2 concentration in the air).
(3) Physiological index measurement: For each measurement, take 2–3 fresh leaflets from each plant with three replicates per treatment. Label the samples and place them in liquid nitrogen, then store them at −80 °C. Measure the content of malondialdehyde (MDA) and the activities of peroxidase (POD), superoxide dismutase (SOD), catalase (CAT), and acid phosphatase (ACP) using reagent kits from Suzhou Grace Biotech Co., Ltd. (Suzhou, China).
(4) Root morphological index measurement: After low-P stress treatment, select 10 G. sinensis seedlings. Rinse the roots with tap water, scan the roots using an Epson Scan root scanner (Expression 12000XL, Suwa, Japan), and then use the WinRHIZO Pro 2019 root analysis system to quantify total root length, total root surface area, total root volume, and average root diameter.
(5) Determination of mineral element content: The total contents of P, K, Ca, Mg, and Na in roots, stems, and leaves after low-P stress treatment were determined using inductively coupled plasma (ICPE-9820) atomic emission spectroscopy. N content was determined using the fully automated Kjeldahl nitrogen (HGK55).

2.4. Data Analysis

We utilized Microsoft Excel 2019 for data statistics and chart creation. Data analysis was conducted using SPSS 23.0, and multiple comparisons were performed using the LSD test. The significance of differences between the two datasets was assessed using the t-test:
P A E = P C × D W
In the formula, PAE represents P absorption efficiency (mg), PC represents P concentration (mg·g−1), and DW represents dry weight (g).
P U E = D W ÷ P A E
In the formula, PUE represents P utilization efficiency (g·mg−1).
L s = 1 − C i C a
In the formula, Ls represents the stomatal limitation value, Ci represents the intercellular carbon dioxide concentration, and Ca represents the atmospheric carbon dioxide concentration.
W U E = P n T r
In the formula, WUE represents water utilization efficiency, Pn represents the net photosynthetic rate, and Tr represents the transpiration rate.

3. Results

3.1. Effects of Low P Stress on Agronomic Traits of G. sinensis Seedlings with Different P Efficiencies

According to Table 1, it can be observed that under LP stress, the agronomic traits of seedlings from four G. sinensis families are all affected to varying degrees. Compared to the NP treatment, under LP stress, G. sinensis exhibited a decrease in plant height, stem diameter, leaf number, leaf length, leaf width, compound leaf number, compound leaf width, and SPAD values. For the low-P-tolerant families, F10 and F13 of G. sinensis, the stem diameter and leaf number showed significant differences between LP and NP conditions, while other indicators such as plant height, leaf length, and leaf width did not show significant differences. Among the low-P-sensitive family, F21 exhibited significant differences in plant height, stem diameter, leaf width, compound leaf length, and compound leaf width between LP and NP conditions, while F29 showed significant differences in plant height, stem diameter, leaf width, and SPAD values between LP and NP conditions. Under LP stress, there are significant differences in the magnitude of changes in various indicators among the G. sinensis family with different P efficiencies. The reduction percentages in plant height, leaf width, and SPAD values are as follows: F10 (4.08%, 4.31%, 0.17%) < F13 (7.28%, 11.02%, 0.92%) < F21 (21.35%, 13.60%, 6.99%) < F29 (25.12%, 20.67%, and 14.91%). The stem diameter reduction in the F29 family is the highest (40.82%), while the stem diameter increase in the F10 family is the highest (13.80%). The reduction in various indicators for the low-P-tolerant families F10 and F13 is smaller than that for the low-P-sensitive families F21 and F29. LP increased the stem diameter and leaf length in the F10 family, and it increased the leaf number and compound leaf length in the F13 family. The low-P-sensitive families F21 and F29 were significantly affected by LP stress, which greatly inhibited the growth of these two G. sinensis. The LP/NP values for F10 and F13 are both relatively large, and their ratios are generally greater than those for F21 and F29. This indicates that the low-P-tolerant G. sinensis family can maintain higher P- utilization efficiency under LP stress.

3.2. Effects of Low P Stress on Biomass and Root-to-Shoot Ratio of G. sinensis Seedlings with Different P Efficiencies

The biomass changes in different parts of G. sinensis seedlings with different P efficiencies vary under LP stress. As shown in Figure 1, under both LP stress and NP treatment, there is no significant difference in the leaf dry weight between the low-P-tolerant G. sinensis families F10 and F13. Additionally, there are no significant differences in the root dry weight for F10 and stem dry weight for F13. However, LP stress significantly increased the root dry weight of the F13 family by 60.21%. The root, stem, and leaf dry weights of the low-P-sensitive G. sinensis families F21 and F29 are significantly lower under LP stress compared to NP treatment. Specifically, under LP stress, the reduction percentages in root, stem, and leaf dry weights for the F21 family reached 62.47%, 65.11%, and 48.00%, respectively. For the F29 family, the reduction percentages were 62.74%, 47.67%, and 34.83% in root, stem, and leaf dry weights, respectively. From the perspective of the same P level, under LP treatment, the root, stem, and leaf dry weights of the tolerant family are significantly higher than those of the sensitive family. This indicates that, compared to the low-P-sensitive family, the low-P-tolerant family exhibits a clear advantage in biomass growth under LP conditions. Under NP treatment, the root and stem dry weights of the low-P-sensitive family are significantly higher than those of the low-P-tolerant family, but the leaf dry weight is significantly lower. This suggests that under conditions of abundant nutrients, the growth of a low-P-sensitive family does not show a clear disadvantage. Thus, it can be observed that the low-P-tolerant and low-P-sensitive families of G. sinensis respond differently to LP stress, with the growth of the low-P-sensitive family being severely inhibited under LP treatment.
The results of the root–shoot ratio indicate that G. sinensis responds to low P stress by increasing the root–shoot ratio. As shown in the graph, low P stress significantly increases the root–shoot ratio of the low-P-tolerant family, with the F13 family having a significantly higher ratio than the other family. Under NP conditions, the root–shoot ratio of the sensitive family is significantly higher than that of the tolerant family. Compared to NP conditions, LP significantly increases the root–shoot ratio of the F10 family by 79.35% and the F13 family by 62.05%. These results indicate that an increased root–shoot ratio is one of the adaptive measures of low-P-tolerant G. sinensis to cope with LP conditions.

3.3. Effects of Low P Stress on Root Morphology of G. sinensis Seedlings with Different P Efficiencies

G. sinensis seedlings with different P efficiencies exhibit significant changes in root morphology indicators under LP stress. From Figure 2, it can be observed that, compared to NP treatment, LP stress significantly increases the total root length, total root surface area, total root projected area, total root volume, and main root thickness of the low-P-tolerant G. sinensis families F10 and F13. For F10, the increases in these indicators reach 18.90%, 4.00%, 32.41%, 43.34%, and 6.80%, respectively. For F13, the increases are 144.39%, 53.10%, 50.22%, 5.68%, and 17.26%, respectively. Notably, F13 shows the highest increase in total root length. The low-P-sensitive G. sinensis families F21 and F29 are significantly affected by LP, inhibiting the growth of their root systems. As shown in the figure below, in addition to significantly increasing the total root length of F21 and F29, LP stress significantly decreases root morphology indicators such as total root surface area, total root projected area, total root volume, root average diameter, and main root thickness. For F21, the reduction percentages in these indicators reach 34.30%, 18.46%, 53.30%, 30.49%, and 43.49%, respectively. For F29, the reduction percentages are 18.56%, 29.10%, 52.56%, 13.27%, and 25.73%, respectively. Overall, the reduction percentages for F21 are higher than those for F29, indicating that F21 is more severely affected by LP stress. From the perspective of the same P level, under LP treatment, the low-P-tolerant G. sinensis family generally shows significantly higher values in total root length, total root surface area, total root projected area, total root volume, and main root thickness compared to the low-P-sensitive family. Under NP treatment, the root growth of the low-P-sensitive G. sinensis family is generally not significantly inhibited. Thus, it can be observed that under conditions of abundant nutrients, the root growth of low-P-sensitive G. sinensis appears to be generally in good condition compared to the low-P-tolerant family. In summary, when subjected to LP stress, the root morphology of the low-P-tolerant G. sinensis family changes to adapt to LP conditions. In contrast, the root growth of the low-P-sensitive family is significantly inhibited. The analysis results suggest that changes in root morphology are a common response for low-P-tolerant G. sinensis to adapt to LP conditions.

3.4. Effects of Low P Stress on Gas Exchange Parameters in G. sinensis Leaves

In order to investigate the response of photosynthesis to LP stress in different G. sinensis families, gas exchange parameters of G. sinensis leaves were measured. Results, as shown in Figure 3, Compared to NP conditions, both low-P-tolerant and low-P-sensitive G. sinensis family experience a significant reduction in net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular carbon dioxide concentration (Ci), and transpiration rate (Tr) under LP stress, the low-P-tolerant families F10 and F13 show reductions of 27.01% and 27.54%, 52.39% and 52.49%, 9.61% and 4.78%, and 36.14% and 47.97% in Pn, Gs, Ci, and Tr, respectively. The low-P-sensitive families F21 and F29 show reductions of 21.34% and 33.69%, 64.97% and 20.25%, 15.57% and 5.29%, and 60.30% and 19.69% in Pn, Gs, Ci, and Tr, respectively. This indicates that LP stress inhibits stomatal conductance, hinders the entry of carbon dioxide into plant leaves, and reduces transpiration rates. Based on the above results, stomatal limitation (Ls) and water utilization efficiency (WUE) were calculated. LP stress significantly increased the stomatal limitation in G. sinensis, except for the low-P-sensitive family F29. Additionally, it significantly increased the water utilization efficiency in G. sinensis, except for the low-P-sensitive family F29. Under LP stress, the reductions in Pn, Gs, Ci, and Tr indicate that the stomatal limitation factor is the main cause of the decrease in photosynthesis in G. sinensis under LP stress. The results indicate that under LP stress, the photosynthetic capacities of the low-P-tolerant G. sinensis families F10 and F13 are stronger than those of the low-P-sensitive families F21 and F29.

3.5. Effects of Low P Stress on Physiological Enzyme Activities in G. sinensis Seedlings with Different P Efficiencies

3.5.1. Effects of Low P Stress on Acid Phosphatase Activity in G. sinensis Seedlings with Different P Efficiencies

As shown in Figure 4, the results of acid phosphatase activity in the roots and leaves under LP stress indicate that in G. sinensis, compared to NP conditions, the acid phosphatase activity in both roots and leaves significantly increases under LP stress. The increases in acid phosphatase activity in the roots and leaves of the low-P-tolerant families F10 and F13 are 117.01% and 158.93% as well as 37.11% and 52.46%, respectively. For the low-P-sensitive families F21 and F29, the increases in the roots and leaves are 7.63% and 60.09% as well as 28.61% and 21.77%, respectively. The results indicate that under LP stress, the low-P-tolerant family shows a larger increase in acid phosphatase activity, while the low-P-sensitive family exhibits a smaller increase. From the perspective of the same P level. Under NP conditions, the leaf acid phosphatase activity of the tolerant family is significantly higher than that of the sensitive family. However, in root acid phosphatase activity, the sensitive family F21 has the highest activity under LP stress, which is not significantly different from the tolerant family F10, and there is also no significant difference between the tolerant family F13 and the sensitive family F29. The acid phosphatase activity in the roots of all families is lower than that in the leaves.

3.5.2. Effects of Low P Stress on Malondialdehyde Content in G. sinensis Seedlings with Different P Efficiencies

As shown in Figure 5, the MDA content in the roots and leaves of G. sinensis seedlings under LP stress was significantly increased compared to NP conditions. The MDA content in the roots exhibited an increase of 18.04%, 97.83%, 46.86%, and 15.98% for the low P-tolerant families F10, F13, and the low P-sensitive families F21, F29, respectively. Similarly, the MDA content in the leaves showed an increase of 7.64%, 85.86%, 58.05%, and 57.18% for the respective families. The maximum increase in MDA content in both roots and leaves was observed in the family F13, indicating a faster response in MDA accumulation under LP stress. These results suggest that LP stress promotes the accumulation of malondialdehyde in the roots and leaves of G. sinensis seedlings.

3.5.3. Effects of Low P Stress on the Activity of Cell Protective Enzymes in G. sinensis Seedlings with Different P Efficiencies

As shown in Figure 6. Compared to NP supply, LP stress significantly increased the activities of SOD, POD, and CAT in the roots and leaves of two sensitive families. The percentage increases in root SOD activities for the low-P-tolerant families F10 and F13, as well as the low-P-sensitive families F21 and F29, were 13.34%, 10.59%, 12.39%, and 12.46%, respectively. The increases in POD activities were 23.09%, 120.79%, 989.33%, and 25.90%, respectively, while CAT activities showed increases of 25.51%, 29.65%, 175.06%, and 11.57%, respectively. Notably, the increase in root SOD activity relative to POD and CAT was smaller. From this, it can be inferred that tolerant families exhibit low sensitivity to LP stress and possess strong tolerance to LP conditions.
From the perspective of the same P level, it is noteworthy that under LP stress, the sensitive family F21 exhibited a particularly high increase in root and leaf POD and CAT activities, reaching a maximum of 989.33%. This indicates that when subjected to LP stress, the sensitive family F21 rapidly and significantly increased both root and leaf POD and CAT activities to defend against the imposed stress. Under NP conditions, overall, there were no significant differences in root SOD, POD, and CAT activities, as well as leaf SOD and POD activities between tolerant and sensitive families. The results indicate that when nutrients are sufficient, whether it is a tolerant or sensitive family, the changes in the activities of protective enzymes are not significant, and there is even a possibility that protective enzyme activities in sensitive families may be higher than those in tolerant families.

3.6. Effects of Low P Stress on Mineral Elements of G. sinensis Seedlings with Different P Efficiencies

3.6.1. Effects of Low P Stress on the Elemental Composition of the Root System in G. sinensis Seedlings with Different P Efficiencies

According to Table 2, compared to NP conditions, the contents of N, P, K, Mg, and Na in the roots of tolerant G. sinensis families F10 and F13 significantly decreased under LP stress. For F10 and F13, the reductions in N, P, K, Mg, and Na content were 5.50% and 12.62%, 33.79% and 25.29%, 15.86% and 27.80%, 21.38% and 11.80%, 51.50% and 16.09%, respectively. LP stress significantly increased the Ca contents in the roots of the tolerant family, with increases of 8.44% and 32.33%. However, the trend in the changes of elemental composition in the root system of the sensitive family was generally opposite to that of the tolerant family. Under LP stress, it significantly increased the contents of N, P, K, and Na in the roots of sensitive families F21 and F29, with increases in N and P contents of 26.21% and 12.51%, and 18.72% and 16.65%, respectively. It also significantly decreases the Ca and Mg contents in the root system of G. sinensis. From the perspective of the same P level, under LP stress, the contents of N, P, and K in the sensitive family are significantly higher than those in the tolerant family. Conversely, under NP conditions, the contents of N, P, K, and Na in the tolerant family are significantly higher than those in the sensitive family. The reason for this result may be that LP stress inhibits the growth of the sensitive G. sinensis family, leading to a significant reduction in biomass. However, the N, P, and K contents of G. sinensis itself do not decrease under LP conditions. Therefore, the N, P, and K contents per unit mass will correspondingly increase.

3.6.2. Effects of Low P Stress on the Elemental Composition of Stem Segments in G. sinensis Seedlings with Different P Efficiencies

From Table 3, it can be observed that, compared to NP conditions, the N and P contents in the stem segments of tolerant G. sinensis families F10 and F13 decreased under LP stress. However, LP stress significantly reduced the P content in the stem, with reductions of 13.75% and 4.29% for families F10 and F13, respectively. Additionally, LP stress significantly increased the contents of K, Ca, Mg, and Na in the seedlings of the tolerant G. sinensis family. The corresponding increases were 24.89% and 65.25%, 36.95% and 29.81%, 46.32% and 34.02%, 94.05% and 66.74%, respectively. The F10 family had the highest increase in sodium content, with an increase of 94.05%. It is worth noting that LP stress significantly increased the contents of N, P, Ca, Mg, and Na in the stem segments of sensitive families F21 and F29, with corresponding increases of 33.50% and 15.95%, 42.17%, and 33.59%, 8.37% and 27.87%, 11.42% and 20.15%, and 19.86% and 82.26%, respectively. Similar to the tolerant family, the highest increase was observed in Na content. From the perspective of the same P level, the trends in the changes of various elemental contents varied among different families under different P levels. Under LP stress, the contents of N and P in the sensitive family were significantly higher than those in the tolerant family, while the contents of K, Mg, and Na were significantly lower than those in the tolerant family. From this, it can be inferred that under LP stress, perhaps the tolerant family’s growth environment cannot absorb and utilize P. In order to maintain their growth and development, tolerant families might utilize P stored within themselves. On the other hand, sensitive families are highly sensitive to LP environments. When P is deficient, the roots cannot absorb enough P, and the roots retain the very small amount of P they have absorbed without further transportation upward. This leads to the observed results.

3.6.3. Effects of Low P Stress on the Elemental Composition of Leaves in G. sinensis Seedlings with Different P Efficiencies

From Table 4, it can be observed that the contents of major elements in the leaves of G. sinensis seedlings were higher than those in the roots and stems. Compared to NP conditions, under LP stress, the contents of N, P, and Na in the leaves of the tolerant G. sinensis family F10 significantly decreased, with reductions of 8.14%, 19.58%, and 60.67%, respectively. Family F13 showed the most significant decrease in Na content, with a reduction of 75.57%. There were significant increases in the contents of K, Ca, and Mg in the leaves of both F10 and F13, with increases of 80.31% and 49.9%, 24.46% and 2.73%, and 50.09% and 8.98%, respectively. The two sensitive families, F21 and F29, significantly increased the contents of six major elements—N, P, K, Ca, Mg, and Na—in their leaves when subjected to LP stress; the corresponding increases were 15.75% and 7.32%, 21.58% and 12.94%, 37.72% and 34.68%, 5.72% and 28.39%, 16.31% and 28.29%, and 94.75% and 192.67%, respectively. From this, it can be observed that the sensitive family, when facing LP stress, increases the content of other elements to meet their own growth and development, demonstrating the interactions among different elements. From the perspective of the same P level, whether under LP stress or NP conditions, different families exhibit different trends in the changes of various elements. Under LP stress, the P and Na contents in the sensitive family are significantly higher than those in the tolerant family. From this, it can be observed that LP stress not only disrupts the absorption and utilization of other elements but also increases the content of certain elements.

3.7. Effects of Low P Stress on P Absorption Efficiency and Utilization Efficiency in G. sinensis Seedlings with Different P Efficiencies

The response of G. sinensis seedlings with different P efficiencies to P absorption efficiencies is illustrated in Figure 7. Under LP treatment, both low-P-tolerant and low-P-sensitive families show overall lower P absorption efficiencies in roots, stems, leaves, and whole plants compared to the NP treatment. From the perspective of the same P treatment in different families, it is evident that under LP stress, the P absorption efficiencies in roots, stems, leaves, and whole plants are significantly higher in the tolerant family than in the sensitive family. However, under NP treatment, the trend is different from LP stress. Under NP conditions, the P absorption efficiencies in roots and whole plants are significantly higher in the sensitive family than in the tolerant family. The above results indicate that LP stress reduces the P absorption efficiency in G. sinensis Additionally, under LP stress, the P absorption efficiencies in all parts of the tolerant family are significantly higher than those in the sensitive family.
The response of G. sinensis seedlings with different P efficiencies to P utilization efficiencies is shown in Figure 7. Under LP stress, the P utilization efficiencies in roots, stems, leaves, and whole plants significantly increase in the tolerant family, while the trend is the opposite in the sensitive family. Under LP stress, except for the P utilization efficiency in the roots of family F29, the P utilization efficiencies in the roots, stems, leaves, and whole plants significantly decrease in the sensitive family. From the perspective of the same P treatment in different families, it is evident that under LP stress, the P utilization efficiencies in roots, stems, leaves, and whole plants are significantly higher in the tolerant family than in the sensitive family. However, under NP treatment, the utilization efficiency of P in the sensitive family is not low. In fact, the P utilization efficiencies in the roots, stems, leaves, and whole plants of the sensitive family F21 are significantly higher than those in the tolerant family F10. The above results indicate that under LP stress, a low-P-tolerant family increases P utilization efficiency to counteract the effects of LP stress. In contrast, low-P-sensitive families experience severe growth inhibition under LP stress and cannot further increase P utilization efficiency to counteract the LP environment. The tolerant family, under LP stress, shows higher efficiency in P utilization, indicating a better response mechanism to LP conditions.

3.8. Effects of Low P Stress on Element Allocation in G. sinensis Seedlings with Different P Efficiencies

From Figure 8, it can be observed that, except for the Na element, the distribution proportions of N, P, K, Ca, and Mg in the leaves are higher than those in the roots and stems. LP stress relatively reduces the distribution proportions of N, P, K, Ca, Mg, and Na in the roots and stems, while it increases the distribution proportions of these elements in the leaves. This indicates that during the growth and development of G. sinensis seedlings, LP stress enhances the allocation of stored nutrients in the leaves, alleviating the damage caused by reduced photosynthesis. The plant maximizes the production of organic compounds in the leaves and transports nutrients to other tissues as sources to resist LP stress, thereby maintaining the growth and development of G. sinensis.

4. Discussion

4.1. Changes in Plant Growth and Root Morphology under Low P Stress

P is an essential macronutrient for plant growth and development. The application of P fertilizer helps improve soil P supply, biomass, grain yield, and aboveground P absorption characteristics [21,22,23]. Additionally, the relationship between soil P supply, crop biomass, and P absorption shows synchronous growth from the lowest levels to asymptotic values [24,25]. The P supply level directly influences plant growth and development. Research indicates that under low P stress, plants increase root length, stimulate the synthesis and secretion of lignin and organic acids, and upregulate inorganic phosphate transporters, acid phosphatases, and purple acid phosphatase genes to enhance P absorption and transport [26]. This helps maintain stable P levels within the plant and enables better adaptation to low P stress. There is also research confirming that under P-sufficient conditions, the difference in yield among different P-efficient families is not significant. However, under low P stress, P-efficient families consistently exhibit higher biomass production compared to P-inefficient families [27]; the results of this study are largely consistent with those of previous research. Crops are highly sensitive to P deficiency during the early stages of growth. In this study, the changes in biomass of the P-tolerant family under LP stress were not significantly different. In contrast, the biomass of the sensitive G. sinensis family was significantly inhibited under LP stress, showing significant differences. Some scholars have pointed out that the increase in root–shoot ratio under low P stress is an effective adaptive mechanism for plants to cope with low P stress [28]. In this study, under LP stress, the root–shoot ratio significantly increased in the P-tolerant family, while the changes in the sensitive family were opposite to this trend. From this, it can be observed that different P-efficient families of G. sinensis respond differently to LP stress. The degree of damage in the low-P-tolerant family is significantly lower than in the low-P-sensitive family.
The main function of roots is to absorb water and nutrients from the soil. Plant root systems, influenced by both genetic factors and external environmental conditions, often exhibit strong plasticity. The response characteristics of root systems can vary due to differences in plant families. Therefore, having well-developed root morphology and physiological characteristics is of significant importance for plants to efficiently utilize soil P. Compared to families less tolerant to LP, P-tolerant varieties have stronger photosynthetic capacity and more developed root growth [29]. Plants can also adapt to low P conditions by altering root morphology, including changes in root configuration such as total root surface area and total root length. These changes increase the contact area between roots and soil, enhancing the activation, transport, and distribution of insoluble P. This, in turn, improves the efficiency of P absorption by plants [30,31,32]. The results of this study indicate that under LP stress, there are significant changes in root morphology between tolerant and sensitive families. Additionally, the root morphological parameters of the tolerant family were significantly higher than those of the sensitive family under LP stress. Therefore, altering root morphology is one of the adaptive strategies employed by the low P-tolerant G. sinensis to cope with LP conditions.

4.2. Changes in Plant Photosynthetic Capacity under Low P Stress

Restricted P nutrient supply typically promotes the downward transport of photosynthetic products, stimulating root growth [33]. This leads to a significant reduction in aboveground biomass and a substantial increase in root–shoot ratio [33,34,35]. P plays a crucial role in plant photosynthesis, participating in various cellular processes, including energy conservation, metabolic regulation, and signal transduction [36]. Farquhar et al. proposed the concept of “stomatal limitation analysis”, which suggests that the main reason for the decrease in the photosynthetic rate of plant leaves is the reduction in stomatal conductance and the increase in stomatal limitation. Conversely, if the stomatal conductance of plant leaves increases and stomatal limitation decreases, it indicates that the main cause of the decrease in the photosynthetic rate of plants is non-stomatal factors [37,38]. This study indicates that under LP stress, both tolerant and sensitive families exhibit a significant decrease in net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, and transpiration rate. These findings align with previous research results [29,39,40,41,42]. Stomatal conductance reflects the extent to which stomata are open. Plants regulate the opening of stomata to control the exchange of external CO2 and water vapor, thereby affecting photosynthesis and transpiration. The results of this study show a decrease in stomatal conductance, impacting the entry of atmospheric CO2 into the intercellular spaces. The significant increase in intercellular CO2 and stomatal limitation values suggests that LP stress may inhibit photosynthesis in G. sinensis leaves through stomatal limitation. Studies have shown that under LP stress, plants reduce water loss by closing stomata. Consequently, stomatal conductance and transpiration rates are significantly reduced [43,44]. The reduction in stomatal conductance observed in this study may represent a strategy employed by G. sinensis to cope with LP stress. This reduction allows the plant to adapt to LP stress by minimizing transpiration. Under LP stress, the tolerant family exhibited significantly higher values for Pn, Gs, Ci, and Tr compared to the sensitive family. This indicates that the impact of LP stress on the tolerant family is less severe than on the sensitive family, and the photosynthetic efficiency of the tolerant family is stronger than that of the sensitive family.

4.3. Changes in Physiological Enzyme Activities of Plants under Low P Stress

Low P not only induces adaptive changes in the root morphology of plants and reduces their photosynthetic capacity but also triggers a series of physiological changes in the root system and even the entire plant. The secretion of acid phosphatase is also considered an important mechanism by which plants adapt to LP stress. Studies have shown that Triticum aestivum under low P stress significantly increases the activity of acid phosphatase in the roots [45]. Low P stress can induce the secretion of acid phosphatase in Capsicum annuum [46]. This study found that LP stress significantly increased the acid phosphatase activities in the roots and leaves of G. sinensis, and the tolerant family exhibited a greater increase than the sensitive family. This indicates that LP promotes the expression of acid phosphatase, and the tolerant family can secrete more acid phosphatase to adapt to LP stress, maintaining the normal growth of G. sinensis. When the P supply is sufficient, the P nutrition around the roots is more abundant, and the direct contact and absorption of P by the roots are sufficient to meet the growth needs of the plants. As a result, the activity of root acid phosphatase decreases, consistent with previous research findings [47]. MDA is one of the main products of intracellular lipid peroxidation, and its content can reflect the degree of lipid peroxidation in organisms. Studies have shown that MDA content tends to increase under P deficiency stress [48]. Previous studies have indicated that P deficiency may lead to an increase in MDA content in Polygala tatarinowii [49]. Our research results indicate that under low P stress, MDA content in the roots and leaves of G. sinensis seedlings significantly increased. This suggests that LP exacerbates lipid peroxidation in plant membranes, consistent with previous research findings. Some studies suggest that the MDA content in low-P-tolerant families is lower than that in low-P-sensitive families, and P-efficient families exhibit higher resistance to LP stress than P-inefficient families [41]. However, the results of this study did not show a similar pattern, which may be due to differences between species. In this study, LP stress significantly increased the activity of protective enzymes in the roots of tolerant and sensitive families, as well as in the leaves. These results are consistent with previous research findings [42]. Therefore, it can be seen that the tolerant family has a low sensitivity to LP stress and a strong tolerance to LP. The increase in the activity of protective enzymes under LP stress is considered a self-protection mechanism in G. sinensis.

4.4. Changes in Plant Nutrients under Low P Stress

There are interactive effects in the absorption of nutritional elements by plants, involving both synergistic and antagonistic interactions. After 30 days of P deficiency treatment, there is a significant decrease in root P content. Additionally, the ratios of P, K, Mg, and Cu contents between the roots and aboveground parts increase, while the contents of Ca, Fe, and Mn decrease [50]. There is also research indicating that P deficiency generally restricts the absorption of mineral elements by plants [51]. In this study, under LP stress, the mineral element contents in various organs of the sensitive G. sinensis seedlings increased compared to the NP condition. The P content also increased, indicating a relatively low degree of P recycling and reuse within the plant. Apart from Na content in the leaves, the tolerant family showed increases in N, K, Ca, Mg, and Na in various organs. However, LP stress reduced the P content in the tolerant family, suggesting that LP stress enhances the internal P recycling and reuse efficiency. The results of this study differ slightly from those of the aforementioned researchers, and this disparity may be attributed to interspecies differences.

4.5. Changes in Plant P Utilization Efficiency under Low P Stress

Plants primarily require inorganic P from the soil for their growth. The content of inorganic P that can be directly absorbed and converted by plants in the soil is minimal compared to the total P content in the soil. Therefore, improving plant P absorption efficiency and enhancing P nutrition genetic traits are important approaches to address soil P deficiency. P- utilization efficiency can serve as an indicator for selecting plants with the ability to efficiently utilize P in low P stress environments. In recent years, many scholars have conducted research on the mechanisms of P-efficient utilization in different crops. Research has confirmed that there is not much difference in yield between different P-efficient families under P-sufficient conditions. Under low P stress, P-efficient families consistently exhibit higher biomass production compared to P-inefficient families [52]. P-efficient wheat families exhibit higher P- utilization efficiency, root biomass, and root–shoot ratio compared to P-inefficient Triticum aestivum families [53]. Plants can alter the P content in different organs to resist low P stress and can allocate more P to the aboveground parts to enhance P utilization efficiency [54]. Under low P treatment, Zygophyllum xanthoxylum exhibits strong rhizospheric P activation capability and higher P absorption efficiency [55]. Some P-efficient plants possess higher P- utilization efficiency, which is one of their strategies to cope with low P stress [56]. The results of this study indicate that under LP stress, the P- utilization efficiencies in the roots, stems, leaves, and whole plants of tolerant families are significantly higher than those of sensitive families. Whether it is a low P-tolerant or P-sensitive family, the P absorption efficiencies in roots, stems, leaves, and whole plants are lower than those in the NP treatment. This is consistent with previously reported research results. From this, under LP stress, tolerant families exhibit significantly higher P- utilization efficiency compared to sensitive families. Low P-tolerant families demonstrate a higher efficiency in P utilization, indicating a better response mechanism to LP conditions.

5. Conclusions

Gleditsia sinensis seedlings with different P efficiencies exhibit significant differences in growth and physiology under LP and NP conditions. LP stress significantly affects the growth and development of both low P-tolerant and low P-sensitive Gleditsia sinensis seedlings. Compared to the low P-sensitive Gleditsia sinensis families, the low P-tolerant Gleditsia sinensis families enhance their P- utilization efficiency by increasing root–shoot ratio, total root length, total root surface area, total root projected area, total root volume, and main root diameter. They also improve acid phosphatase activity and cell protective enzyme activity, significantly increase the contents of other macronutrients in stems and leaves, and adjust the nutrient distribution ratio to store more macronutrients in the leaves. This mitigates the harm caused by LP stress and maintains high P efficiency. Therefore, there are clear differences in the ability to tolerate low P among different Gleditsia sinensis families. The low P-tolerant Gleditsia sinensis families perform well overall, providing a reference for selecting germplasm resources of Gleditsia sinensis varieties that tolerate low P.

Author Contributions

C.L. and Y.Z. conceived and designed the study. C.L., R.Z. and X.W. collected the data. C.L., R.Z. and F.X. analyzed and interpreted the data. C.L. wrote and translated the paper. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the China National Key R&D Program (grant no. 2022YFD1601712); the characteristic forestry industry research project of Guizhou province (GZMC-ZD20202102).

Data Availability Statement

All data are presented in the article and can be requested from the corresponding author if required.

Conflicts of Interest

The authors declare no competing interests.

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Forests 15 01343 g001
Figure 1. Differential comparison of dry biomass of G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences (p < 0.05) among different families. Different uppercase letters indicate significant differences (p < 0.05) within the same family under different P level treatments.
Figure 1. Differential comparison of dry biomass of G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences (p < 0.05) among different families. Different uppercase letters indicate significant differences (p < 0.05) within the same family under different P level treatments.
Forests 15 01343 g001
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Figure 2. Differential comparison of root morphology of G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences (p < 0.05) among different families. Different uppercase letters indicate significant differences (p < 0.05) within the same family under different P level treatments.
Figure 2. Differential comparison of root morphology of G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences (p < 0.05) among different families. Different uppercase letters indicate significant differences (p < 0.05) within the same family under different P level treatments.
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Figure 3. Comparison of photosynthetic parameters in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same-colored column indicate significant differences (p < 0.05) among different families. Different uppercase letters indicate significant differences (p < 0.05) within the same family under different P level treatments.
Figure 3. Comparison of photosynthetic parameters in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same-colored column indicate significant differences (p < 0.05) among different families. Different uppercase letters indicate significant differences (p < 0.05) within the same family under different P level treatments.
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Figure 4. Differential comparison of acid phosphatase activity in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences among different families (p < 0.05), while different uppercase letters indicate significant differences within the same family under different P supply levels (p < 0.05).
Figure 4. Differential comparison of acid phosphatase activity in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences among different families (p < 0.05), while different uppercase letters indicate significant differences within the same family under different P supply levels (p < 0.05).
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Figure 5. Differential comparison of MDA content in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color column indicate significant differences among different families (p < 0.05), and different uppercase letters indicate significant differences among different P supply levels within the same family (p < 0.05).
Figure 5. Differential comparison of MDA content in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color column indicate significant differences among different families (p < 0.05), and different uppercase letters indicate significant differences among different P supply levels within the same family (p < 0.05).
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Figure 6. Differential comparison of protective enzyme activity in G. sinensis seedlings with different P efficiencies under low P Stress. Note: Different lowercase letters on the same color series column indicate significant differences between different families (p < 0.05), while different uppercase letters indicate significant differences between different P supply levels within the same family (p < 0.05).
Figure 6. Differential comparison of protective enzyme activity in G. sinensis seedlings with different P efficiencies under low P Stress. Note: Different lowercase letters on the same color series column indicate significant differences between different families (p < 0.05), while different uppercase letters indicate significant differences between different P supply levels within the same family (p < 0.05).
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Figure 7. Comparison of the differences in phosphorus absorption efficiency and utilization efficiency in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences (p < 0.05) among different families under the same P supply level. Different uppercase letters indicate significant differences (p < 0.05) among different P supply levels within the same family.
Figure 7. Comparison of the differences in phosphorus absorption efficiency and utilization efficiency in G. sinensis seedlings with different P efficiencies under low P stress. Note: Different lowercase letters on the same color-coded column indicate significant differences (p < 0.05) among different families under the same P supply level. Different uppercase letters indicate significant differences (p < 0.05) among different P supply levels within the same family.
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Figure 8. Comparative analysis of the differences in element allocation proportions in G. sinensis seedlings with different P efficiencies under low P stress.
Figure 8. Comparative analysis of the differences in element allocation proportions in G. sinensis seedlings with different P efficiencies under low P stress.
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Table 1. Agronomic traits of G. sinensis seedlings from different P efficiency families under low P stress.
Table 1. Agronomic traits of G. sinensis seedlings from different P efficiency families under low P stress.
IndicatorsDifferent P Efficiency Families
F10F13F21F29
Plant height/cmLP21.87 aA15.67 bA15.47 bB13.53 cB
NP22.80 aA16.90 cA19.67 bA18.07 cA
LP/NP0.96 a0.93 a0.69 b0.86 a
Stem diameter/mmLP4.04 aA4.34 aB2.60 bB2.74 bB
NP3.55 bB4.70 aA3.72 bA4.63 aA
LP/NP1.14 a0.92 b0.70 c0.59 d
Number of leaves/leafLP22.67 aB23.33 aA18.67 bA16.00 cA
NP32.67 aA20.67 bB18.67 bA19.33 bA
LP/NP0.70 d1.13 a1.00 b0.83 c
Leaf length/mmLP12.00 aA11.96 aA8.65 bA10.84 aA
NP11.98 aA12.76 aA10.46 bA12.76 aA
LP/NP1.00 a0.94 a0.83 a0.85 a
Leaf width/mmLP6.21 aA5.73 abB5.59 bB5.22 bB
NP6.49 aA6.44 aA6.47 aA6.58 aA
LP/NP0.96 a0.89 ab0.87 ab0.79 b
Compound leaf number/leafLP11.00 aB6.33 bA6.33 bA7.00 bA
NP16.67 aA6.67 bA9.00 bA7.67 bA
LP/NP0.66 a0.95 a0.73 a0.92 a
Compound leaf length/cmLP8.83 aA7.10 bA5.50 cB6.00 bcA
NP9.67 aA6.40 bcA7.47 bA5.47 cA
LP/NP0.92 ab1.12 a0.74 b1.10 a
Compound leaf width/cmLP2.37 aA2.33 aA2.03 aB2.10 aA
NP2.47 aA2.40 aA2.37 aA2.17 aA
LP/NP0.96 a0.97 a0.86 b0.97 a
SPAD valueLP57.27 bA60.37 aA53.60 cA60.73 aB
NP57.37 bA60.93 bA57.63 bA71.37 aA
LP/NP1.00 a0.99 a0.93 b0.85 c
Note: Different lowercase letters in the same row indicate significant differences (p < 0.05) among different families under the same P level, and different uppercase letters in the same column indicate significant differences (p < 0.05) within the same family under different P level treatments.
Table 2. Comparative analysis of the differences in the elemental composition of the root system in G. sinensis seedlings with different P efficiencies under low P stress.
Table 2. Comparative analysis of the differences in the elemental composition of the root system in G. sinensis seedlings with different P efficiencies under low P stress.
IndicatorsDifferent P Efficiency Families
F10F13F21F29
N (g·kg−1)LP16.61 ± 0.12 cB14.72 ± 0.23 dB21.88 ± 0.13 aA20.38 ± 0.55 bA
NP17.58 ± 0.29 abA16.85 ± 0.36 cA17.34 ± 0.45 bcB18.12 ± 0.23 aB
P (g·kg−1)LP0.67 ± 0.04 cB0.65 ± 0.03 cB0.99 ± 0.01 aA0.95 ± 0.01 aA
NP1.01 ± 0.04 aA0.87 ± 0.02 cA0.83 ± 0.04 cB0.82 ± 0.03 cB
K (g·kg−1)LP8.79 ± 0.05 bB8.89 ± 0.72 bB14.41 ± 0.5 aA9.08 ± 0.94 bA
NP10.45 ± 0.59 bA12.31 ± 0.57 aA8.88 ± 0.54 cB9.66 ± 0.73 bcA
Ca (g·kg−1)LP8.58 ± 0.20 aA5.82 ± 0.08 bA5.91 ± 0.58 bA5.39 ± 0.06 bB
NP7.91 ± 0.27 aB4.40 ± 0.11 cB4.81 ± 0.44 cA5.87 ± 0.04 bA
Mg (g·kg−1)LP2.57 ± 0.03 bB2.49 ± 0.09 bcB2.84 ± 0.04 aB2.46 ± 0.02 cB
NP3.27 ± 0.13 bcA2.82 ± 0.08 cA3.57 ± 0.29 abA3.98 ± 0.38 aA
Na (g·kg−1)LP1.00 ± 0.11 cB1.60 ± 0.08 aB1.55 ± 0.03 abA1.45 ± 0.04 bA
NP2.07 ± 0.12 aA1.91 ± 0.17 aA1.36 ± 0.06 bB1.50 ± 0.07 bA
Note: Different lowercase letters within the same row indicate significant differences (p < 0.05) among different families under the same P supply level. Different uppercase letters within the same column indicate significant differences (p < 0.05) among different P supply levels within the same family.
Table 3. Comparative analysis of the differences in the elemental composition of stem segments in G. sinensis seedlings with different P efficiencies under low P stress.
Table 3. Comparative analysis of the differences in the elemental composition of stem segments in G. sinensis seedlings with different P efficiencies under low P stress.
IndicatorsDifferent P Efficiency Families
F10F13F21F29
N (g·kg−1)LP16.42 ± 1.37 bA17.69 ± 0.45 bA25.92 ± 0.12 aA25.88 ± 0.11 aA
NP17.92 ± 0.2 dA18.52 ± 0.14 cA19.41 ± 0.1 bB22.32 ± 0.19 aB
P (g·kg−1)LP0.73 ± 0.01 dB0.87 ± 0.01 cB1.14 ± 0.01 bA1.39 ± 0.02 aA
NP0.84 ± 0.01 cA0.91 ± 0.01 bA0.81 ± 0.01 dB1.04 ± 0.01 aB
K (g·kg−1)LP13.66 ± 0.19 aA12.8 ± 0.42 bA9.12 ± 0.18 cA9.52 ± 0.26 cA
NP10.94 ± 0.01 aB7.74 ± 0.41 cB8.63 ± 0.26 bA9.23 ± 0.45 bA
Ca (g·kg−1)LP7.32 ± 0.89 bA8.41 ± 0.45 aA7.21 ± 0.1 bA8.36 ± 0.23 aA
NP5.34 ± 0.07 bB6.48 ± 0.07 aB6.65 ± 0.21 aB6.54 ± 0.15 aB
Mg (g·kg−1)LP3.71 ± 0.24 aA3.59 ± 0.19 aA3.13 ± 0.02 bA3.17 ± 0.09 bA
NP2.53 ± 0.2 aB2.68 ± 0.03 aB2.81 ± 0.05 aB2.64 ± 0.03 aB
Na (g·kg−1)LP1.13 ± 0.02 aA0.92 ± 0.06 bA0.63 ± 0.01 cA0.50 ± 0.01 dA
NP0.58 ± 0.02 aB0.55 ± 0.06 aB0.52 ± 0.02 abB0.28 ± 0.03 cB
Note: Different lowercase letters within the same row indicate significant differences (p < 0.05) among different families under the same P supply level. Different uppercase letters within the same column indicate significant differences (p < 0.05) among different P supply levels within the same family.
Table 4. Comparative analysis of the differences in the elemental composition of leaves in G. sinensis seedlings with different P efficiencies under low P stress.
Table 4. Comparative analysis of the differences in the elemental composition of leaves in G. sinensis seedlings with different P efficiencies under low P stress.
IndicatorsDifferent P Efficiency Families
F10F13F21F29
N (g·kg−1)LP32.67 ± 0.72 cB35.98 ± 0.31 bA35.6 ± 0.44 bA38.46 ± 0.58 aA
NP35.56 ± 0.61 aA34.13 ± 0.07 bB30.76 ± 0.08 cB35.83 ± 0.31 aB
P (g·kg−1)LP0.97 ± 0.01 cB1.05 ± 0.06 bA1.35 ± 0.01 aA1.33 ± 0.02 aA
NP1.20 ± 0.02 aA1.11 ± 0.01 bA1.11 ± 0.02 bB1.17 ± 0.02 aB
K (g·kg−1)LP28.94 ± 1.05 bA22.98 ± 1.14 dA40.04 ± 0.73 aA27.12 ± 0.43 cA
NP16.05 ± 0.52 cB15.33 ± 0.3 cB29.07 ± 0.49 aB20.14 ± 0.15 bB
Ca (g·kg−1)LP27.91 ± 0.62 bA26.06 ± 1.45 cA27.01 ± 0.4 bcA34.69 ± 0.35 aA
NP22.42 ± 0.3 cB25.37 ± 0.16 bA25.55 ± 0.44 bB27.02 ± 0.51 aB
Mg (g·kg−1)LP7.04 ± 0.17 bA5.95 ± 0.25 dA7.83 ± 0.05 aA6.43 ± 0.06 cA
NP4.69 ± 0.08 dB5.46 ± 0.03 bB6.73 ± 0.12 aB5.01 ± 0.10 cB
Na (g·kg−1)LP0.65 ± 0.04 cB0.43 ± 0.02 dB2.05 ± 0.01 aA1.29 ± 0.00 bA
NP1.66 ± 0.03 aA1.75 ± 0.03 aA1.05 ± 0.09 bB0.44 ± 0.01 cB
Note: Different lowercase letters within the same row indicate significant differences (p < 0.05) among different families under the same P supply level. Different uppercase letters within the same column indicate significant differences (p < 0.05) among different P supply levels within the same family.
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Lu, C.; Zou, R.; Wang, X.; Zhao, Y.; Xiao, F. The Growth and Physiological Responses of Gleditsia sinensis Lam. Seedlings with Different Phosphorus Efficiencies to Low Phosphorus Stress. Forests 2024, 15, 1343. https://doi.org/10.3390/f15081343

AMA Style

Lu C, Zou R, Wang X, Zhao Y, Xiao F. The Growth and Physiological Responses of Gleditsia sinensis Lam. Seedlings with Different Phosphorus Efficiencies to Low Phosphorus Stress. Forests. 2024; 15(8):1343. https://doi.org/10.3390/f15081343

Chicago/Turabian Style

Lu, Chunyun, Rong Zou, Xiurong Wang, Yang Zhao, and Feng Xiao. 2024. "The Growth and Physiological Responses of Gleditsia sinensis Lam. Seedlings with Different Phosphorus Efficiencies to Low Phosphorus Stress" Forests 15, no. 8: 1343. https://doi.org/10.3390/f15081343

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