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Article

Reducing Nitrogen Input Increases the Efficacy of Soil Nitrogen Utilization by Regulating Cotton–Arbuscular Mycorrhizal Fungi–Soil Nitrogen Interactions

by
Hushan Wang
1,†,
Yunzhu He
1,†,
Zihui Shen
1,2,
Mengjuan Liu
1,
Wangfeng Zhang
2 and
Xiaozhen Pu
1,*
1
Xinjiang Production and Construction Corps Key Laboratory of Oasis Town and Mountain-Basin System Ecology, College of Life Sciences, Shihezi University, Shihezi 832000, China
2
Key Laboratory of Oasis Eco-Agriculture of Xinjiang Corps, College of Agriculture, Shihezi University, Shihezi 832000, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Nitrogen 2025, 6(3), 55; https://doi.org/10.3390/nitrogen6030055
Submission received: 3 June 2025 / Revised: 27 June 2025 / Accepted: 30 June 2025 / Published: 3 July 2025
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Abstract

Crops and arbuscular mycorrhizal (AM) fungi can enhance nitrogen (N) transformation and utilization efficiency in the soil, and this effect is regulated by soil N application rates. However, it remains unclear whether the N utilization efficiency of cotton can be improved through the symbiosis of cotton with AM fungi under reduced N application rates. Therefore, we conducted 15N labeling experiments using a compartmentalized culture system with Gossypium hirsutum L. as the experimental plant. We established three N treatments (0.15 g·kg−1, 0.10 g·kg−1 and 0 g·kg−1) to investigate the effects of different fertilization rates on N utilization, soil N priming effects, and differences in N accumulation in various parts of cotton plants within the soil–AM fungi–cotton system. The results indicate that under reduced N application, symbiosis between cotton and AM fungi increased the N fertilizer utilization efficiency and the soil N priming effect. Specifically, reducing the fertilization dosage from 0.15 g·kg−1 to 0.10 g·kg−1 increased the N fertilizer utilization efficiency and soil N priming effect by 8.87% and 11.67%, respectively, and decreased the N loss rate by 7.02%. The symbiosis between cotton and AM fungi after N reduction significantly increased N accumulation in the roots and leaves. Moreover, the N fertilizer content accounted for 5.89% of the total N content in roots. Overall, when N application was reduced, symbiosis with AM fungi effectively promoted the rhizosphere N priming effect, which reconciled the conflict in N nutrient allocation within cotton and thus enabled the efficient utilization of soil N.

1. Introduction

Nitrogen (N) is an essential nutrient for crop growth and is a crucial factor for achieving high yield and quality in agriculture [1,2,3,4,5]. However, N rates in farmland soils in China have reached saturation. Excessive N application not only leads to resource waste and severe environmental pollution but also restricts root system function and increases N loss. Research has shown that the excessive application of nitrogen fertilizer can lead to soil acidification, compaction, changes in microbial community structure, and nutrient imbalance, thereby resulting in a decline in soil function (e.g., phosphorus (P) limitation induced by high N application rates) [6,7,8,9,10,11], reduced root absorption capacity, and, ultimately, decreased plant productivity [12,13]. When the amount of N fertilizer applied to the soil exceeds the threshold of plant absorption and utilization [14,15], a substantial portion of the N is either released into the atmosphere in gaseous forms (NH3/N2/N2O) or lost through leaching and runoff, posing considerable threats to atmospheric and groundwater resources [16,17,18]. Moderately reducing the N input promotes increases in root biomass and the number of lateral roots, a decrease in root diameter, and elongation of the main root, thereby effectively expanding the area for nutrient capture by the root system. Additionally, reducing the N input enhances the plant’s adaptability to environmental N by adjusting the N allocation strategy between the aboveground and belowground parts of the plant [19,20,21]. This improves the efficiency of plants in absorbing and utilizing N [22,23,24].
As a vital part connecting plants and soil, roots not only absorb nutrients from the soil for plant use but also transfer carbon (C)-containing compounds produced during photosynthesis into the rhizosphere soil through root turnover and secretion. These processes provide essential C sources and energy for soil microorganisms, and in some cases, they recruit soil microorganisms (mycorrhizal fungi) to rhizosphere hotspots, promoting N transformation processes in the rhizosphere soil (soil N priming effect) [25,26,27]. Therefore, plant root-mediated activities play an important role in C and nutrient cycling in terrestrial ecosystems [28]. During long-term evolution, more than 80% of terrestrial plants have formed unique and efficient symbioses with fungi known as mycorrhizae [29]. Unlike bacterial colonization, the symbiosis between AM fungi and plants involves five stages (recognition, formation of entry points, invasion of the cortex, formation of arbuscules and vesicles, and spore proliferation). This process is more complex and prolonged, but its contribution to plant nutrient uptake is undeniable [30]. For example, AM fungi transfer approximately 5–21% of the photosynthetic products of the host to soil regions that are inaccessible to the roots through their extensive extraradical mycelial networks. They directly or indirectly regulate the cycling processes of C and other nutrients and their potential microbial and abiotic interaction mechanisms through a series of activities, such as mycelial secretion and turnover [31,32]. In soils with low nutrient availability, AM fungi provide host plants with large amounts of N and P, thereby enhancing the nutrient acquisition capacity and survival of mycorrhiza-dependent plants [33,34,35,36,37]. In agricultural ecosystems, when the addition of external N is reduced or the soil concentration is maintained at N-limited rates, plants tend to increase their reliance on AM fungi. In particular, plants depend on extraradical mycelium to expand their absorption area and utilize soil resources, and AM fungi can also activate and enhance nutrient availability through their own activities, such as by inducing the host to secrete organic acids and extracellular enzymes [25,26] or inducing the expression of nutrient transporters at the symbiotic interface, thereby improving nutrient transport and utilization efficiency [38]. This results in a reduction in nutrient losses caused by leaching or denitrification [39]. In summary, moderate N reduction can enhance the interactive effects between AM fungi and plants, thereby promoting soil N transformation processes, improving plant N utilization efficiency, and reducing soil N losses [40,41].
Cotton is an important economic crop, and current research on the interaction between cotton and AM fungi has primarily focused on disease resistance, physiological stress, and the addition of different exogenous N sources [42,43,44,45]. However, few studies have investigated the effects of fertilization on N flow within the soil–root–shoot system and soil N priming effects. Therefore, in the present study, we selected Xinlu 84 as the experimental material and utilized the 15N tracer method to investigate the impact of reduced N application on the interactions between cotton, AM fungi, and soil N. The aim is to improve the utilization rate of N fertilizer, and reduce N fertilizer loss and planting costs by reducing the application of N fertilizer, so as to provide a theoretical basis for N fertilizer management in cotton fields. We hypothesized that (1) reducing N application promotes the stability of the symbiotic relationship between cotton and AM fungi; (2) under reduced N application, symbiosis with AM fungi enhances the rhizosphere N priming effect in cotton, facilitating soil N transfer and transformation and improving fertilizer utilization efficiency; and (3) based on the trade-off principle between rapid nutrient absorption and conservation, cotton primarily increases N accumulation in roots and leaves under reduced N application and the influence of AM fungi, thereby enhancing its overall adaptability to the environment.

2. Materials and Methods

2.1. Study Area and Soil Properties

The test soil (without adding any substances such as vermiculite or sand) was obtained from the cotton field at Shihezi University in Xinjiang, China (topography: plain, map coordinates: 85°59′47″ E, 44°19′28″ N, altitude: 412 m, aspect and slope angle: 1° and 0.6%). Calcisol is a typical soil type in this region, with relatively weak water and fertilizer retention capabilities. Therefore, in this study, the original soil from cotton fields was used.
In addition, soil in this area has been continuously planted with cotton for the past three years, during which manual weeding was carried out. Each year, 375 kg·hm−2 of nitrogen fertilizer (urea) and 300 kg·hm−2 of phosphorus and potassium fertilizer (KH2PO4) are applied. The irrigation and fertilization are managed through the method of film-mulched drip irrigation. The initial soil fungi spore density was 17 spores·g−1, with Paraglomus as the dominant genera [46]. The soil organic matter, total N, inorganic N, and pH of the original cotton field are shown in Table S1.

2.2. Experimental Design

The experiment employed a single-factor experimental design and used compartmentalized cultivation to distinguish the effects of roots and AM fungal mycelium. Each treatment was replicated 4 times. We aimed to investigate the impact of reduced N application on the interactions between cotton, AM fungi, and soil N.
This study referred to the experimental design of Wu et al. [47]: A compartmentalized culture apparatus with dimensions of 13 × 10 × 13 cm3 was fabricated using a 1.2 mm thick iron plate. The interior was divided using nylon mesh with two different pore sizes (48 μm and 1 mm) (note: the pore diameter of 48 μm is not easily blocked by mycelium or other impurities, and can be kept unblocked for a long time, ensuring that the mycelium can continuously pass through the nylon mesh during the test and maintain the stability and continuity of the experimental system) [48], with one side serving as the cotton mycorrhiza chamber and the other as the mycelial chamber. The 48 μm pore size allows only mycelium to pass through, while the 1 mm pore size permits both mycelium and fine roots to pass (Figure 1). These two compartments were separated with a 3 mm gap to prevent the exchange of nutrient flow. The experiment included three N treatments: 0.15 g·kg−1, 0.10 g·kg−1, and 0 g·kg−1 (corresponding to field N application rates of 375, 250, and 0 kg·hm−2, denoted as N1, N2, and N3, respectively). The N fertilizer was applied to the soil with water, and the experiment lasted for 60 days.
The cotton variety “Xinlu 84” (Hexin Technology Development Co., Ltd., Shihezi, Xinjiang, China) was used in this research. High-quality cotton seeds (disease-, pest-, and damage-free) were selected after soaking seeds in 5% H2O2 and rinsing them with distilled water. Each compartmentalized culture apparatus was filled with 1500 g of soil in both the growth and mycelial chambers, and four seeds were planted in the growth chamber. The apparatuses were placed in a GXZ-430D intelligent illuminated incubator (China Ningbo City Science and Technology Park Xinjiangnan Instrument Co., Ltd., Ningbo, China) for cultivation. For the first 10 days, the daily light intensity was set at 12,000 lx for 16 h at 28 °C, and after 10 days, it was adjusted to 24,000 lx for 16 h at 32 °C, with 8 h of darkness at 25 °C. After the cotton plants developed two true leaves, two evenly growing plants were retained in the growth chamber. Every 2 days, 2 mL of N at the corresponding rate was applied to the mycelial chambers with 1 mm and 48 μm nylon mesh in the N1 and N2 treatments, with a total of 15 applications. The N3 treatment received the same volume of deionized water instead of fertilizer. We added N in the form of urea (in the field used as the study area, farmers commonly use urea as a N fertilizer), and 2 mL of modified Hoagland’s N-free nutrient solution (China Qingdao High-tech Industrial Park Haibo Biotechnology Co., Ltd., Qingdao, China) was added to the growth chamber. Additionally, during N fertilizer application, 0.1 g of 10% CO(15NH2)2 (China Haiyan Zhiheng Testing Technology Co., Ltd., Jiaxing, China) was added to the mycelial chamber with a 48 μm nylon mesh for N labeling. 15N was used as base N fertilizer. After 60 days, the cotton plant height and basal stem diameter were measured using a tape measure (cm) and a Vernier caliper (mm), respectively. Plant samples (root, stem, leaf) were then dried at 105 °C for 0.5 h and then dried to a constant weight at 70 °C. Soil samples were sieved through a 2 mm mesh screen and collected in self-sealing bags for determination of total N in plants and soil, as well as δ15N in roots and soil. Furthermore, the mycelial density in this study was determined using the method of Totsche [49]. The AM fungi colonization rate was determined using the method of Dickson and Smith [50]. The AM fungi colonization rate and mycelial density of each treatment are shown in Tables S2 and S3.

2.3. Measurement of Plant- and Soil-Related Indicators

The total N content in cotton leaves and stems was determined using Nessler’s colorimetric method [51]. The δ15N and %N in roots and soil were measured using a stable isotope ratio mass spectrometer coupled with an elemental analyzer (IRMS-EA, Elementar, Manchester, UK).

2.4. Statistical Analysis

The main calculation methods for N utilization and other related indicators were as follows:
Plant N accumulation = part N content (mg·g−1) × dry weight (g)
Proportion of 15N in soil total N (%) = (atom percent excess of 15N in soil total N/atom percent excess of 15N fertilizer) × 100
15N content in soil total N (g·kg−1) = soil total N content × proportion of 15N in soil total N (%)
N fertilizer residual rate (%) = (15N content in soil total N/applied N amount) × 100
Proportion of 15N in plant total N (%) = (atom percent excess of 15N in plants/atom percent excess of 15N fertilizer) × 100
Proportion of soil N in plant total N (%) = 1 − proportion of 15N in plant total N
15N content in plant total N (mg·g−1) = plant total N content (mg·g−1) × proportion of 15N in plant total N
Soil N content in plant total N (mg·g−1) = proportion of soil N in plant total N × plant total N content
15N fertilizer loss (g) = applied N amount − 15N content in plant total N—N fertilizer residue
15N fertilizer loss rate (%) = [(Applied N amount − 15N content in plant total N—N fertilizer residue)/applied N amount] × 100
Soil N priming effect (%) = (N content from soil in N − fertilized plants/N content in unfertilized plants) × 100
Data processing was conducted using Excel 2019, and data analysis was performed using SPSS 27.0. Prior to analysis, the homogeneity of variance test was applied to the data. In cases where the data did not meet the assumption of homogeneity of variance, a logarithmic transformation was performed. For comparison of mean values, the paired samples T-test was used for within-group comparisons, with a significance rate set at α = 0.05. Additionally, R version 4.3.0 was utilized for graphical representation, and SPSSAU (https://spssau.com/indexs.html (accessed on 10 May 2025)) was employed for random forest weight analysis.

3. Results

3.1. Impacts of Root and Mycelial Pathways on Soil N Content Under Different N Application Rates

Under the interaction between roots and AM fungi, at the same N application rate, the soil total N, soil 15N fertilizer residual rate, 15N content in soil total N, and 15N proportion in soil total N were lower in the root pathway than in the mycelial pathway (Figure 2). Specifically, under N1 and N2, the soil total N in the root pathway was reduced by 18.31% and 6.81%, respectively, compared with that in the mycelial pathway. Moreover, with a decrease in N application, whether through the root or mycelial pathway, the total N content in the soil was reduced (Figure 2A). The soil 15N fertilizer residual rate increased with decreasing N application. Under N2, the mycelial pathway had the highest 15N fertilizer residual rate, whereas under N1, both the root and mycelial pathways had the lowest 15N fertilizer residual rates of 16.09% and 20.07%, respectively. Compared with those under N1, the 15N residual rates of the root and mycelial pathways increased by 7.84% and 7.20%, respectively, under N2 (Figure 2B). Regarding the 15N proportion in the soil total N, both the root and mycelial pathways showed higher values under N2 than under N1. Specifically, under N2, the 15N proportions in the soil total N for the root and mycelial pathways were 10.18% and 11.11%, respectively (Figure 2D).

3.2. Absorption of Soil N by Roots Under Different N Application Rates

Under the interaction between roots and AM fungi, compared with N1, N2 improved the utilization efficiency of N fertilizer while reducing the nutrient loss of soil N. Specifically, the roots notably increased the uptake of N fertilizer under N2, with a relative increase of 21.74% compared with that under N1 (Figure 3A). The absorption of fertilizer N and original soil N by the roots varied depending on the N application rate. As shown in Figure 3B, under N1 and N2, the amount of fertilizer N absorbed by roots accounted for 5.28% and 5.89% of the total N content in the roots, respectively, whereas the content of original soil N absorbed by the roots accounted for 94.72% and 94.11% of the total N content in the roots, respectively. Compared with that under N1, the fertilizer N content absorbed by the roots under N2 increased by 0.60%, whereas the original soil N content absorbed by the roots decreased by 0.60%. The results confirm the higher utilization efficiency at smaller fertilizer application rates (Figure 3C). Under N1 and N2, the utilization efficiency of N fertilizer by cotton was 10.89% and 19.67%, respectively. Compared with that under N1, the utilization efficiency of N fertilizer by cotton increased by 8.78% under N2.

3.3. Changes in Cotton Growth and Plant Part N Accumulation Under Different N Application Rates

With a decreasing N application rate, the basal stem diameter of cotton first increased and then decreased, whereas the plant height gradually decreased (Figure S1). Compared with that under N3, the basal stem diameter of cotton was significantly larger under N1 and N2, with the diameter under N2 being larger than that under N1. For cotton height, the maximum value was observed under N1, and the minimum value was observed under N3. Additionally, the root-to-shoot ratio of cotton was significantly higher under N3 than under N1 and N2, with the root-to-shoot ratio under N2 being 3.29% higher than that under N1 (Figure S2A).
In addition to the morphological changes in cotton, N application also had an impact on N accumulation in different parts of cotton (Figure S2). The N accumulation in the roots increased with decreasing N application rate (Figure S2B). Compared with that under N1, N accumulation in the roots increased by 15.07% and 32.59% under N2 and N3, respectively. Compared with that under N2, N accumulation in the roots increased by 15.23% under N3 (Figure S2B). The N accumulation in the leaves reached the highest rate under the N2 treatment, increasing by 58.57% and 49.22% compared with that under N1 and N3, respectively (Figure S2C). Compared with that under N1 and N3, N accumulation in the stems increased by 6.82% and 57.27% under N2, respectively (Figure S2D).

4. Discussion

4.1. Regulation of the Symbiotic System of Cotton and AM Fungi by N Application

Multiple studies have demonstrated that symbiosis between host plants and AM fungi in farmland ecosystems alters soil N transformation processes, thereby reducing soil N losses [52,53,54,55]. For instance, Bender et al. [56] reported that symbiosis between AM fungi and tomatoes led to the formation of a vast mycelial network, expanding the nutrient absorption area and significantly increasing soil N interception. Furthermore, symbiotic AM fungi compete with nitrifying and denitrifying bacteria in the soil for inorganic N, inhibiting the transformation of inorganic N between these bacteria, thus reducing soil N losses [57,58]. However, the synergistic effect of AM fungi is influenced by various environmental factors, such as the plant growth status, soil microbial community structure, soil inorganic nutrient content, and the exchange of benefits between AM fungi and plants [26,59,60]. As AM fungi cannot survive independently of plants, the occurrence of reciprocal benefits between plants and AM fungi determines the establishment and stability of the symbiotic relationship and is considered a key factor influencing the nature of plant–AM fungi interactions. Additionally, plants are selective in their symbiosis with AM fungi, and if the metabolic processes of symbiotic fungi cannot guarantee the N demand of the plant, the plant may utilize the high sensitivity of AM fungi to carbohydrates to inhibit mycelial growth, resulting in a restricted symbiotic relationship [61]. Simultaneously, plants will allocate more carbohydrates to root cells to promote root system development [62,63,64], substantially reducing their dependency on AM fungi. In this study, under high N application rates, the soil microbial richness decreased [65,66], leading to a reduction in the coverage area and activity of the mycelial network and a decrease in the N transported by the mycelium to the host plant. In such cases, cotton reduces its dependence on nutrient contributions from the mycelium and inhibits its allocation of carbohydrates to the mycelium [67,68]. Instead, the carbohydrates originally intended for the mycelium are redirected to the absorptive roots of cotton, ultimately forming a nutrient acquisition method primarily driven by the stimulation of the absorptive roots and root exudates (i.e., the root pathway) [69]. This shift may represent an autonomous mechanism performed by cotton based on the potential advantages and disadvantages under high N conditions. Although high N application rates provide cotton with more autonomy in acquiring N nutrients, they also make soil N acquisition more uniform. In a rapidly changing soil environment, the multidimensional trait variation in roots under high N application enhances the adaptability of crops to complex environments [26,70,71].
Multiple studies have demonstrated that AM fungi dependency in mycorrhizal plants increases under N deficiency [72,73,74,75]. In the present study, the symbiosis between AM fungi and plants markedly improved soil N availability under reduced N application, offsetting the relative decrease in soil N caused by N reduction. This is beneficial for enhancing the dependence of cotton on AM fungi for N and the stability of their relationship. One reason for this may be that the symbiosis between cotton and AM fungi considerably expands the space for plant nutrient acquisition after N reduction [69,76], improves the efficiency of N transfer from AM fungi to plants, and shifts most of the transferred nutrients to N “sink” organs such as leaves and fruits [77,78]. The increase in N in leaves can stimulate the production of more carbohydrates in the C “source” parts and transport them underground (e.g., to the mycelium) [67,79,80], while the increase in N in fruits may serve as an additional “compensation” to the plant after the AM fungi acquire plant C. From the perspective of the host plant, reproduction (“propagation”) and nutrient acquisition (“survival”) are equally important. This is one of the reasons why symbiosis between AM fungi and crops can increase crop yields [81,82,83]. Therefore, mycelia and roots may compensate for the limited growth of the aboveground parts of cotton caused by low N application through frequent C–N reward exchange mechanisms (Figure 4C). Furthermore, AM fungi release a portion of the allocated carbohydrates into the soil microenvironment in the form of mycelial secretions, promoting rhizosphere priming effects and achieving efficient conversion of soil N [25,26]. In the present study, the priming effect of the original soil N played a decisive role in cotton growth and N accumulation (Figure S3 and Table 1). Regardless of the N application rate, the original soil N content in the cotton roots accounted for more than 90%, indicating that original soil N remains the largest N supply source for the symbiosis between cotton and AM fungi. Deng et al. [84] showed that approximately 90% of the N required for plant growth comes from the reabsorption of N before leaf fall and the microbial decomposition and mineralization of the original soil N. The original soil N is relatively stable and continuous, and its biological interaction is closely linked with soil microorganisms and plant roots. Meanwhile, fertilizer N is typically fast-acting, easy to absorb, and easily lost, making its effect extremely unstable. This may be the main reason why plants primarily absorb original soil N. Therefore, reducing N application can promote the C and N reward mechanisms of the cotton–AM fungi symbiotic system, enhance the stability of their relationship, and facilitate the utilization of original soil N [26,71].

4.2. Effects of N Application and AM Fungi Interaction on Soil N

Our results indicate that for cotton colonized with AM fungi, as the amount of N applied increases, the loss of fertilizer N increases significantly, and the priming effect of soil N decreases. Specifically, at high N rates, the N fertilizer loss rates of the root and mycelial pathways reached 89.04% and 86.65%, respectively (Figure 4), which is consistent with previous reports [85]. This suggests that although the interaction between AM fungi and plants can increase soil N retention, the N retention effect of mycelia and roots is limited in N-rich agricultural soils. Nevertheless, at the same rate of N fertilizer application, the symbiosis between AM fungi and plants leads to a 15.0–17.8% reduction in plant N acquisition compared with that by plants without AM fungi. Assuming a N fertilizer application rate of 375 kg·ha−2, AM fungi can potentially save up to approximately 66.75 kg·ha−2 of N [86]. Therefore, AM fungi may play an important role in improving N fertilizer absorption efficiency and reducing fertilizer application, and the N-promoting effect of AM fungi is considerably influenced by soil N. In this study, the correlation between soil N and fertilizer N in roots indicates that reducing N application under conditions of abundant soil N can prompt the cotton–AM fungi symbiotic system to play a positive role in the absorption of fertilizer N (Figure S3 and Figure 5C). Similarly, Dong et al. [87] suggested that under conditions of abundant soil N, reducing N input could achieve the efficient utilization of fertilizer N by crops and maintain high crop yields. Additionally, after reducing the N input, the fertilizer N content in the N acquired from the root and mycelial pathways increased significantly, and there was a significant positive correlation between the soil total N and the N fertilizer residual rate, utilization rate, and loss (Figure 5A–C). This suggests that after reducing N input, the cotton–AM fungi symbiotic system promotes the dynamic balance of soil N rates while utilizing and enriching soil N. Maintaining the dynamic balance of soil N rates is conducive to promoting the interaction between beneficial microbial communities and plant roots, thereby regulating N cycle processes, such as N absorption, transport, and assimilation; improving the soil’s continuous N supply capacity; and ensuring the stability of plant N acquisition [88,89]. Recent studies have also shown that the dynamic balance of soil N is closely related to the synergistic effects of AM fungi and N-fixing bacteria [90,91,92,93,94]. Therefore, reducing N application not only enhances the interaction between cotton and AM fungi but also strengthens the synergistic effect of AM fungi and beneficial microorganisms such as N-fixing bacteria, thereby reducing the loss of soil N (original N and fertilizer N) (Figure S4A and Figure 6), promoting the dynamic balance of soil N rates, and ensuring the sustainable utilization of soil N resources [57,58,90,91,92,93].

4.3. Effects of N Application and AM Fungi Interaction on N Distribution in Various Plant Parts of Cotton

The N distribution is a crucial plastic trait that allows plants to adapt to different environments and competitive conditions. This adaptation often involves the challenge of allocating limited resources to different parts, which may lead to a N imbalance between the vegetative and reproductive parts [95]. According to the optimal allocation theory, plants limited by soil environmental factors (e.g., soil N) tend to prioritize the allocation of more assimilates and nutrients to underground parts for efficient nutrient absorption [96,97,98]. However, studies have also shown that under N deficiency in the soil, symbiosis between roots and AM fungi can distribute more nutrients to the stems and leaves, thereby enhancing photosynthesis and stress resistance in plants. This is a rapid growth strategy to occupy resources but comes at the cost of sacrificing the development of other parts such as roots [99,100,101,102]. In our study, N distribution to various organs of cotton changed with different N application rates after the symbiosis of cotton and AM fungi. At high N application rates, the N absorbed by cotton was mainly allocated to the stems rather than to the leaves or fruits. This may lead to an insufficient supply of nutrients being allocated to the cotton bolls after flowering, potentially causing premature cracking of the bolls without adequate development. Such an imbalance in N distribution among cotton parts can result in a “false N deficiency phenomenon” in reproductive growth, which may be an important reason for reduced cotton yield following high N application [103,104,105,106]. The cause of this phenomenon may be that long-term high N application rates restrict the function of a large number of beneficial symbiotic fungi and other soil microorganisms, making it difficult for cotton to manage complex N allocation patterns through its own regulation. Conversely, under reduced N conditions, symbiosis between cotton and mycorrhizal fungi demonstrated a stronger ability to acquire soil nutrients and synthesize photosynthetic products (Figure 5E,F and Figure S4B). This indicates that when N is limited, cotton increases N accumulation in the nutrient “source” parts, promoting the development of the nutrient “sink” parts. If the N demand of the nutrient “sink” parts increases, the nutrient “source” parts can be further stimulated to provide more N and assimilates. Additionally, symbiosis between plants and AM fungi after N reduction can regulate root morphology and function. According to root economics spectrum analysis, AM fungi not only aids in soil nutrient acquisition but also promotes plant root nutrient uptake and increases root lifespan [59,107]. In the long term, this not only maximizes benefits for plant nutrient acquisition but also ensures the persistence and stability of the symbiotic relationship. This allows plants to obtain maximum nutrient benefits at a lower cost, and the conserved C and N resources provide positive feedback to the aboveground parts of plants (e.g., stems, leaves, and fruits), reconciling the contradiction between aboveground and belowground N allocation in plants [108,109,110,111]. Notably, cultivated crops (e.g., wheat, rice, corn, and cotton) differ from plants in natural ecosystems (e.g., trees, shrubs, and herbaceous plants). In N-rich farmland ecosystems, the excessive application of N fertilizer can lead to yield reduction, owing to unreasonable nutrient allocation to the aboveground parts of crops. A large amount of N can also remain in the soil due to low root absorption and utilization efficiency, increasing N loss through leaching or gas emissions [104,112,113]. This threatens the sustainable development of agricultural ecosystems [105,106,114,115]. Therefore, for N-rich farmland soils, reducing the N application rate and optimizing the nutrient allocation of AM fungi and cotton symbiosis can support cotton in obtaining greater N benefits with relatively low mycorrhizal and root nutrient inputs. This helps reconcile the contradiction between belowground and aboveground N allocation in cotton.

5. Conclusions

The results of our experimental study indicate that reducing N application is beneficial for promoting C and N reward mechanisms within cotton and AM fungi symbiotic systems, enhancing the stability of their relationship. Symbiosis with AM fungi can facilitate the transformation and absorption of soil N, reduce N loss and residues, and reconcile conflicts in N allocation between the belowground and aboveground parts of cotton. This is conducive to efficient N utilization and increased cotton yield. Although our research cannot fully reveal the mechanisms of fertilization effects on soil N utilization in AM fungi–cotton symbiotic systems, it provides insights for the efficient cultivation and sustainable development of cotton. Furthermore, our future research will focus on investigating the effects of fertilization on soil fungal and bacterial communities, as well as the effects on related N metabolic pathways, using chemical methods, metabolomics, and genomics. This will enable us to better understand the interactions between exogenous N, cotton, microorganisms, and soil, thereby contributing to the sustainable development of agriculture.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/nitrogen6030055/s1: Figure S1: Effects of different N application rates on cotton height (A) and basal stem (B). Note: The error bar represents standard error; N1: 0.15 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different lowercase letters indicate significant (p < 0.05) differences of each index among different N treatments; Figure S2: Changes in N accumulation in root–shoot ratio (A), roots (B), leaves (C), and stems (D) under different N rates. Note: The error bar represents standard error; N1: 0.15 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different lowercase letters indicate that the differences of each index were significant among the different N treatments (p < 0.05); Figure S3: Effects of N application rate and soil N priming on N accumulation in cotton and soil N. Note: “*”< 0.05, “**”< 0.01, “***”< 0.001, “****”< 0.0001; Figure S4: Relative weight sizes of affecting total soil N (A) and linear analysis of total N and root-to-shoot ratio (B); Table S1: Base physical and chemical properties of soil in the test area; Table S2: Colonization rate of cotton roots by AMF; Table S3: Mycelial density between treatments (mean ± standard error).

Author Contributions

H.W. and Y.H.: methodology, software, data curation, formal analysis, writing—original draft. Z.S. and M.L.: software, investigation, formal analysis, data curation. W.Z.: conceptualization, methodology, writing—review and editing. X.P.: conceptualization, methodology, data curation, project administration, resources, writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

We would like to acknowledge the support from National Natural Science Foundation of China (32460538), Xinjiang Production and Construction Corps Science and Technology Program (2024DB015), and Xinjiang Production and Construction Corps Guiding Science and Technology Program (2023ZD049) for this research.

Data Availability Statement

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

Acknowledgments

We appreciate the professional English editor for improving the language of the article.

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

Abbreviations

AMArbuscular mycorrhizal
NNitrogen
CCarbon
MPMycelium pathway
RPRoot pathway

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Figure 1. Nutrient uptake pattern of cotton root pathway (A) and mycelial pathway (B).
Figure 1. Nutrient uptake pattern of cotton root pathway (A) and mycelial pathway (B).
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Figure 2. Under the interaction between roots and AM fungi, effects of different N application rates on soil total N (A), 15N fertilizer residual rate (B), N content of 15N in soil total N (C), and N ratio of 15N in soil total N (D). Note:The error bar represents standard error; MP: mycelium pathway, RP: root pathway; N1: 0.15 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different uppercase letters denote significant (p < 0.05) differences between MP and RP under the same N treatment for each indicator, and different lower case letters denote significant differences (p < 0.05) between different N treatments at MP and MP, RP and RP.
Figure 2. Under the interaction between roots and AM fungi, effects of different N application rates on soil total N (A), 15N fertilizer residual rate (B), N content of 15N in soil total N (C), and N ratio of 15N in soil total N (D). Note:The error bar represents standard error; MP: mycelium pathway, RP: root pathway; N1: 0.15 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different uppercase letters denote significant (p < 0.05) differences between MP and RP under the same N treatment for each indicator, and different lower case letters denote significant differences (p < 0.05) between different N treatments at MP and MP, RP and RP.
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Figure 3. Under the interaction between roots and AM fungi, effects of different rates of N application on N fertilizer content in the root system (A); N fertilizer percentage in the roots (B); and N fertilizer utilization rate (C). Note: The error bar represents standard error; N1: 015 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different lowercase letters indicate significant differences (p < 0.05) between the N treatments for each indicator.
Figure 3. Under the interaction between roots and AM fungi, effects of different rates of N application on N fertilizer content in the root system (A); N fertilizer percentage in the roots (B); and N fertilizer utilization rate (C). Note: The error bar represents standard error; N1: 015 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different lowercase letters indicate significant differences (p < 0.05) between the N treatments for each indicator.
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Figure 4. Under the interaction between roots and AM fungi, effects of different N treatments on N fertilizer loss content (A), soil N priming effect (B) and a model diagram of the carbon and N reward mechanisms of the roots and mycelium (C). Note: The error bar represents standard error; MP: mycelium pathway, RP: root pathway; N1: 0.15 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different uppercase letters denote significant (p < 0.05) differences between MP and RP under the same N treatment for each indicator, and different lowercase letters denote significant differences (p < 0.05) between different N treatments at MP and MP, RP, and RP.
Figure 4. Under the interaction between roots and AM fungi, effects of different N treatments on N fertilizer loss content (A), soil N priming effect (B) and a model diagram of the carbon and N reward mechanisms of the roots and mycelium (C). Note: The error bar represents standard error; MP: mycelium pathway, RP: root pathway; N1: 0.15 g·kg−1, N2: 0.10 g·kg−1, N3: 0 g·kg−1; different uppercase letters denote significant (p < 0.05) differences between MP and RP under the same N treatment for each indicator, and different lowercase letters denote significant differences (p < 0.05) between different N treatments at MP and MP, RP, and RP.
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Figure 5. Linear correlation between soil total N and N fertilizer residual rate (A), utilization rate (B), root N fertilizer content (C), N fertilizer loss amount (D), root N accumulation (E), and stem N accumulation (F).
Figure 5. Linear correlation between soil total N and N fertilizer residual rate (A), utilization rate (B), root N fertilizer content (C), N fertilizer loss amount (D), root N accumulation (E), and stem N accumulation (F).
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Figure 6. Conceptual diagram of the impact of cotton and mycelium on N fertilizer absorption and N loss under different N application rates.
Figure 6. Conceptual diagram of the impact of cotton and mycelium on N fertilizer absorption and N loss under different N application rates.
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Table 1. Partial correlation analysis of influencing factors on priming effect.
Table 1. Partial correlation analysis of influencing factors on priming effect.
Assessment ItemAssociation and SignificanceAssociation Ranking
Stem N accumulation0.96 **1
Root fertilizer N0.94 **2
Root-to-shoot ratio−0.90 **3
N application rates0.89 **4
N loss amount0.86 **5
N residual rate0.84 **6
N utilization rate0.82 **7
Root N accumulation−0.80 **8
Note: ** indicates highly significant difference (p < 0.01).
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MDPI and ACS Style

Wang, H.; He, Y.; Shen, Z.; Liu, M.; Zhang, W.; Pu, X. Reducing Nitrogen Input Increases the Efficacy of Soil Nitrogen Utilization by Regulating Cotton–Arbuscular Mycorrhizal Fungi–Soil Nitrogen Interactions. Nitrogen 2025, 6, 55. https://doi.org/10.3390/nitrogen6030055

AMA Style

Wang H, He Y, Shen Z, Liu M, Zhang W, Pu X. Reducing Nitrogen Input Increases the Efficacy of Soil Nitrogen Utilization by Regulating Cotton–Arbuscular Mycorrhizal Fungi–Soil Nitrogen Interactions. Nitrogen. 2025; 6(3):55. https://doi.org/10.3390/nitrogen6030055

Chicago/Turabian Style

Wang, Hushan, Yunzhu He, Zihui Shen, Mengjuan Liu, Wangfeng Zhang, and Xiaozhen Pu. 2025. "Reducing Nitrogen Input Increases the Efficacy of Soil Nitrogen Utilization by Regulating Cotton–Arbuscular Mycorrhizal Fungi–Soil Nitrogen Interactions" Nitrogen 6, no. 3: 55. https://doi.org/10.3390/nitrogen6030055

APA Style

Wang, H., He, Y., Shen, Z., Liu, M., Zhang, W., & Pu, X. (2025). Reducing Nitrogen Input Increases the Efficacy of Soil Nitrogen Utilization by Regulating Cotton–Arbuscular Mycorrhizal Fungi–Soil Nitrogen Interactions. Nitrogen, 6(3), 55. https://doi.org/10.3390/nitrogen6030055

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